ChapterPDF Available

Fungal Root Endophytes

April 2013

April 2013

DOI:10.1201/b14550-45

In book: The Hidden Half (pp.38.31-38.49)
Edition: 4th edn.
Chapter: 38
Publisher: CRC Press, Taylor & Francis Group, Boca Raton, FL, USA
Editors: A Eshel, T Beeckman

Authors:

Thomas N Sieber

ETH Zurich

Christoph R Grunig

Microsynth AG

The peripheral root tissues form a morphologically, physically, and chemically complex microcosm that provides a broad selection of different habitats for a myriad of microorganisms: bacteria, actinomycetes, protozoa, nematodes, microalgae, and fungi. The boundary between roots and soil changes all the time because roots constantly modify the nearby soil structure by their mechanical and metabolic activity (Foster et al. 1983). The rhizoplane, the epidermis, and the outer cortex are colonized by microorganisms in a nonrandom manner. Heavy microbial growth can occur on some individual cells, while neighboring cells are almost devoid of microorganisms (Bowen and Rovira 1976). Patchiness of microbial root colonization probably reflects the uneven distribution of organic debris in the soil, which serves as food base for the microorganisms. Many soil bacteria and fungi are able to colonize inter- and or intracellularly the epidermal and the outer cortical cells (OCO) of healthy roots. Only a comparatively small number of organisms, for example, mycorrhizal fungi, endophytes, and pathogens, possess, however, the ability to cross the inner boundary of the rhizosphere and to colonize the inner of root tissues (Bazin et al. 1990).

Content uploaded by Thomas N Sieber

Content may be subject to copyright.

Content uploaded by Thomas N Sieber

Content may be subject to copyright.

38-1

I. Introduction

e peripheral root tissues form a morphologically, physically,

and chemically complex microcosm that provides a broad selec-

tion of dierent habitats for a myriad of microorganisms: bac-

teria, actinomycetes, protozoa, nematodes, microalgae, and

fungi. e boundary between roots and soil changes all the time

because roots constantly modify the nearby soil structure by

their mechanical and metabolic activity (Foster etal. 1983). e

rhizoplane, the epidermis, and the outer cortex are colonized

by microorganisms in a nonrandom manner. Heavy microbial

growth can occur on some individual cells, while neighboring

cells are almost devoid of microorganisms (Bowen and Rovira

1976). Patchiness of microbial root colonization probably re ects

the uneven distribution of organic debris in the soil, which

serves as food base for the microorganisms. Many soil bacteria

and fungi are able to colonize inter- and or intracellularly the

epidermal and the outer cortical cells (OCO) of healthy roots.

Only a comparatively small number of organisms, for example,

mycorrhizal fungi, endophytes, and pathogens, possess, how-

ever, the ability to cross the inner boundary of the rhizosphere

and to colonize the inner of root tissues (Bazin etal. 1990).

An endophyte is literally dened as one plant living within

another organism. Applying the generally accepted ve-

kingdom system of Whittaker (1969), the term “endomycete”

would, thus, seem more appropriate for a fungus living inter-

nally in a plant. is term is, however, ambiguous because it

may lead to confusion with members of the Endomycetes, a

class introduced by von Arx (1967) to accommodate ascomyce-

tous yeasts and fungi with an yeast like growth phase. De Bary

(1866) coined the term “endophyte” to distinguish organisms

that invade and reside within host tissues or cells from “epi-

phytes,” those fungi living on the outer surfaces of plants.

Various plant/fungus symbioses constitute a continuum from

antagonism to mutualism, and the type of symbiosis may

change over time and space. Diseases caused by highly viru-

lent pathogens or well-developed ectomycorrhizae are imme-

diately obvious also to the nonspecialist, whereas the result

of a plant/fungus association in between these two extremes

may escape observation even by a specialist. e impossibil-

ity to unequivocally dene the behavior of an endophyte as

antagonistic or mutualistic becomes obvious by the ndings

of Freeman and Rodriguez (1993) who observed a fungal plant

pathogen to convert to a nonpathogenic, endophytic mutual-

ist by mutation at a single locus. us, a pragmatic denition

of endophytism should be applied, which includes all organ-

isms located within apparently healthy, functional root tissues

at the moment of sample collection. e currently available

methods to detect endophytes are destructive and, thus, the

addendum “at the moment of sample collection” was necessary

to account for the dynamic nature of plant–fungus interac-

tions. Only fungi will be considered in this chapter although

bacteria can live endophytically too (Chanway 1996; Schulz

et al. 2006). Endophytic bacteria have been shown to be of

vital importance in some symbioses, for example, actinorhi-

zal symbiosis between tree roots (Alnus spp.) and Frankia spp.,

symbiosis between sugarcane (Saccharum ocinarum L.) and

Acetobacter diazotrophicus, a nitrogen-xing bacterial endo-

phyte (Dong etal. 1994), or plant growth–promoting rhizo-

bacteria (Wei etal. 1994). e fungal partners in mycorrhizal

associations are clearly also endophytes because part or all

of their thallus is localized within the roots. Comprehensive

articles, reviews, and books have been provided for many of

Fungal Root Endophytes

I. Introduction ...........................................................................................................................38-1

II. Species and Hosts of Root Endophytes ..............................................................................38-2

Dark Septate Endophytes

III. Methods of Detection........................................................................................................... 38-4

IV. Root Endophytes of Herbaceous Plants .............................................................................38-5

Grass Endophytes • Orchid Endophytes • Other Herbaceous Plant Hosts

V. Root Endophytes of Woody Plant Species .......................................................................38-22

Root Endophytes of Woody Ericales • Root Endophytes of Pinales • Root Endophytes

in Other Woody Plant Species

VI. Conclusions and Outlook ...................................................................................................38-38

References .........................................................................................................................................38-38

Thomas N. Sieber

ETH (Swiss FederalInstitute

of Technology)

Christoph R. Grünig

Microsynth AG

38-2 Root–Rhizosphere Interactions

the groups of classical mycorrhizal associations, namely,

ecto-(ECM), ectendo-(EEM), or arbuscular mycorrhizae (AM)

and the ericoid, arbutoid, orchid, or monotropoid mycorrhi-

zae (Harvais and Hadley 1967; Read 1983; Mikola 1988; Allen

etal. 1991; Egger etal. 1991; Allen and Allen 1992; Currah and

Zelmer 1992; Read 1992, 1996; Brundrett 2004; Smith and

Read 2008; Brundrett 2009). Emphasis in this chapter will

be laid on root–fungus associations that are not regarded as

mycorrhizae in the classical sense although literally they also

form “fungus–root” entities of tightly interwoven fungus-

plant tissues. Fungal root endophytes are ubiquitous and prob-

ably more abundant than classical mycorrhizae because they

are not conned to the root tips and can occur everywhere

in the root system. ey are regularly isolated during studies

about classical mycorrhizae but are then rather regarded as

nuisance than interesting research objects. Since fungal root

endophytes have been largely neglected, information about

their functions is rare. Aer all, the number of publications

about fungal root endophytes started to increase exponentially

since about a decade ago, and there is hope that this group of

organisms will eventually obtain the attention it deserves. In

addition to mycorrhizae, root-colonizing obligate biotrophs

with a prolonged latent phase such as certain smuts (Garcia-

Guzman etal. 1996) or rust fungi, that is, Tranzschelia fusca

(G. Winter) Dietel in the rhizomes of Anemone nemorosa L.,

will not be discussed in this chapter.

is chapter is based in part upon information in several

previous reviews (which it does not supersede): (Melin 1923;

Pearson and Read 1973; Garrett 1981; Foster etal. 1983; Read

1983; Wilcox 1983; Duddrige 1985; Foster 1986; Deacon 1987;

Bazin et al. 1990; Petrini 1991; Newell 1992; Cannon and

Hawksworth 1995; Bills 1996; Wilcox 1996; Jumpponen

andTrappe 1998a; Sieber 2002; Addy etal. 2005; Mandyamand

Jumpponen 2005; Sieber and Grünig 2006; Grünig etal. 2008b;

Peterson etal. 2008; Newsham etal. 2009). Our referencing

is not comprehensive, but we tried to include key references

that can provide access to more literature on fungal root endo-

phytes. In this chapter, we will concentrate on the taxonomy,

diversity, physiology, and ecology of root endophytes and con-

clude with some ideas about interesting avenues for future

research. Nomenclature of fungal names follows the system

applied in the Index Fungorum (http://www.indexfungorum.

org/Names/Names.asp). If both the teleomorph (sexual repro-

ductive stage) and the anamorph (asexual reproductive stage)

are produced, the name of the teleomorph will be used. Names

of the anamorph(s) can be retrieved from the list of synonyms

provided for teleomorphs with known anamorph(s) in the

Index Fungorum.

Morphology of the endophyte–root symbioses is very variable

and changes over time. It depends on both host and endophyte

species; developmental stage of the tree, type, and age of the

roots; edaphic and climatic conditions; and the microbial com-

munity in the rhizosphere. Sections IV.A1, IV.B1, IV.C1, V.A1,

V.B1, and V.C1 about the histology of the endophyte–root inter-

face will be included into this chapter of each host taxon.

II. Species and Hosts

ofRoot Endophytes

Endophytic fungi were detected in the roots of all examined

plant species. Grasses, orchids, and species of the Ericaceae and

Pinaceae are the best-studied plants (Figure 38.1). Diversity, fre-

quency, and population density of endophyte species depend

on the edaphic and climatic conditions, on the heterogeneity of

habitats and niches present within the host tissues, and on the

competing organisms. Dark septate endophytes (DSE) probably

occur in the roots of any plant species. ey are the most fre-

quent and most widespread root endophytes (Stoyke etal. 1992;

Ahlich and Sieber 1996; Jumpponen and Trappe 1998a; Grünig

etal. 2008b; Figure 38.1). Species of Cylindrocarpon, Fusarium,

Gibberella, Ilyonectria, and Neonectria and the Sebacinales are

frequent non-DSE. Fungi of the Sebacinales form mycorrhizae

with ECM plants and orchids (OM) and associations of uncertain

status with many other plant species (Warcup 1988; Weiss and

Oberwinkler 2001; Weiss etal. 2011). e genera Microdochium

and Cryptosporiopsis comprise both DSE and non-DSE species.

Microdochium nivale (Fr.) Samuels & I.C. Hallett (anamorph of

Monographella nivalis (Schanit) E. Müll.) and Microdochium

bolleyi (R. Sprague) de Hoog & Herm.-Nijh. are both endophytes

in grasses, but colonies of M. nivale are white changing to orange

where sporodochia form, whereas those of M. bolleyi are black.

A. Dark Septate Endophytes

DSE is a form taxon and serves primarily to dierentiate these

fungi from endophytes with septate, hyaline hyphae and from

fungi with sparsely septate, hyaline hyphae, which are character-

istic for AM fungi. However, the distinction based on the degree

of pigmentation is oen arbitrary because melanization varies

greatly in some species (Addy etal. 2005; Hambleton and Sigler

2005) especially that of mycelia in colonized roots (Yu etal. 2001;

Barrow 2003). We propose to dene DSE as those endophytic

fungi, which form either at least partly dark brown, dark gray, or

black colonies on 2% (w/v) malt extract agar (MEA) when incu-

bated at 20°C and/or distinctly melanized structures in roots.

Most DSE are ascomycetes, and consequently dematiaceous

ascomycetes that are able to colonize the interior of plant tissues

without inducing disease are potential DSE. However, the most

frequent root-colonizing DSE belong to the genera Microdochium

(anamorphic Monographella (Xylariales)), Periconia (anamor-

phic Pleosporales), Harpophora (anamorphic Gaeumannomyces),

Cadophora (anamorphic Helotiales), Cryptosporiopsis (anamor-

phic Pezicula (Helotiales)), Phialocephala, and Acephala (both

anamorphic Helotiales) (Figure 38.1). Some of the best-studied

DSE are Microdochium bolleyi, Periconia macrospinosa Lefebvre

& Aar.G. Johnson, Gaeumannomyces and Harpophora species,

Acephala applanata Grünig & T.N. Sieber, and Phialocephala

fortinii s.l. C.J.K. Wang& H.E. Wilcox. P. fortinii s.l. consists of

several morphologically indistinguishable but reproductively iso-

lated cryptic species (CSP) (Grünig 2004; Grünig etal. 2007) that

together with A. applanata form the P. fortinii s.l.–A. applanata

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-3Fungal Root Endophytes

species complex (PAC) (Grünig etal. 2008b). PAC are among the

best-characterized DSE. ey are very widespread and abundant

in roots of woody plants, especially conifers and ericaceous plants,

all over the Northern Hemisphere (Tables 38.4 through 38.6).

Section II.A1 is therefore dedicated to them (see below).

Host specicity of DSE is the exception, but some species pre-

fer certain host taxa. Microdochium, Periconia, and Harpophora

species prefer grasses, whereas Cadophora, Cryptosporiopsis,

and PAC species preferentially occur on orchids and woody

plant species (Grünig etal. 2008b; Figure 38.1). PAC seem to be

conned to forest ecosystems because reports about their pres-

ence in arable soils or in roots of plants growing in these soils are

very rare (Ahlich-Schlegel 1997; Brenn etal. 2008).

1. Phialocephala fortinii s.l.–Acephalaapplanata

Species Complex

A. applanata is the only morphologically distinct PAC species,

because its colonies on MEA dier from those of Phialocephala

fortinii s.l. by the absence of aerial mycelium (Grünig and Sieber

2005). e structures of conidiophores are similar among spe-

cies and highly variable within species and, consequently, do not

allow to discriminate species (Grünig etal. 2008a). Dierentiation

of PAC species is only possible using molecular methods. Seven

of the Phialocephala fortinii s.l. species were formally described

based on population dierentiation and dierences at ve

sequence loci (Grünig etal. 2007, 2008a): Phialocephala fortinii

s.s., Phialocephala subalpina, Phialocephala letzii Grünig &

T. N. Sieber, Phialocephala uotilensis Grünig & T. N. Sieber,

Phialocephala turicensis Grünig & T. N. Sieber, Phialocephala

europaea Grünig & T.N. Sieber, and Phialocephala helvetica

Grünig & T.N. Sieber. Identication of members of PAC is pos-

sible using ITS sequencing (Grünig etal. 2008b). However, species

identication within PAC to the species level requires sequencing

of at least three of the sequence loci (Grünig etal. 2008a). Usually,

sequencing of the pPF-076, pPF-018, and beta-tubulin locus using

the primers listed in Grünig etal. (2007) is enough to identify

the species. Alternatively, identication can occur by multiplex-

polymerase-chain-reaction (PCR)-amplied microsatellite (MS)

loci using the primers developed by Queloz etal. (2008, 2010).

e geographical distribution of PAC species ranges from arc-

tic to subtropical regions throughout the Northern Hemisphere

(Piercey etal. 2004; Zhang etal. 2009; Queloz etal. 2011). e

wide geographic distribution of PAC contrasts with the results

obtained from baiting experiments, which provided no evidence

for aerial dispersal of PAC (Bachmann 2010). Nevertheless,

strains with identical inter-simple sequence repeats (ISSR) nger-

print and single-copy restriction fragment length polymorphism

(RFLP) haplotype were repeatedly found in forest stands situated

a few km apart, and migration rates measured between conti-

nents were low but still sucient to prevent speciation (Grünig

etal. 2004, 2011; Grünig and Sieber 2005; Queloz 2010). is is at

least surprising, since PAC do not or only rarely sporulate aer

prolonged incubation at low temperature, and germination of

conidia was never observed. Probably, anthropogenic gene and

genotype ow occurs by the movement of nursery plants colo-

nized by PAC locally and around the globe (Brenn etal. 2008).

Herbaceous plants

Others

Woody plants

Ericaceae

Poaceae

Others

DSE

PAC

Cadophora spp.

Pezicula spp.

Cryptosporiopsis spp.

Ilyonectria spp.

Neonectria spp.

Cylindrocarpon spp.

Microdochium spp.

Periconia

macrospinosa

Gibberella spp.

Fusarium spp.

Gaeumannomyces spp.

Harpophora spp.

Sebacinales

Pinaceae

non-DSE

Orchidaceae

FIGURE 38.1 Simplied schematic display of the main taxa of root endophytes and the major groups of their plant hosts. e black upper box

indicates occurrence of DSE, the blank lower box occurrence of non-DSE; species of taxa positioned in the black box are DSE, those in the blank

box non-DSE; the genera Microdochium and Pezicula (Cryptosporiopsis) comprise both DSE and non-DSE species.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-4 Root–Rhizosphere Interactions

Abundance distribution curves of PAC species in local com-

munities are hyperbolic with a few abundant species and many

“rare” species (Grünig et al. 2006), consistent with the com-

munity structures observed in many other biological systems

(McGill et al. 2007). In a recent study, 44 communities from

the Northern Hemisphere comprising more than 5000 PAC

strains were analyzed (Queloz et al. 2011). Species diversity

and community structure were neither correlated with the tree

community, geographical location, soil properties, manage-

ment practices, precipitation, nor temperature, supporting the

hypothesis of “everything is everywhere” (Baas-Becking 1934).

Indeed, it is known that host specicity of PAC species is low or

lacking because most species can be isolated from a broad range

of woody plant species (Grünig etal. 2008b). For example, the

most abundant PAC species, Phialocephala subalpina Grünig

& T.N. Sieber, was isolated from 16 plant species compared

to many fungal pathogens that oen have narrow host ranges

(Tables 38.4 through 38.6).

PAC species were shown to be a genetically highly variable on

a regional level (Harney etal. 1997; Grünig etal. 2001). Within

forest plots of 200 m

, PAC can form communities of up to 13

sympatrically occurring species (Grünig et al. 2004; Queloz

etal. 2010). More than 25 genets were present in an area of only

9 m

of forest soil, and this community remained stable for sev-

eral years (Queloz etal. 2005). More homogenous population

structures would be expected for these supposedly mitotic PAC

fungi. ere are at least two possibilities to explain this phe-

nomenon. Either the assumption of asexuality is wrong, and

PAC enjoy some hidden sex such as parasexuality, or it is a poly-

phyletic species complex, and what we see today is the result of

a convergent evolutionary process. From a molecular genetics

point of view, PAC meet the requirements for sex, because they

possess mating-type genes (Zaarano etal. 2010), and probably,

they are also functional because no gametic disequilibrium

can be found in PAC species based on single-copy RFLP data

(Grünig etal. 2007). Whereas mating-type genes of Acephala

applanata are organized in a homothallic fashion (MAT1-1 and

MAT1-2 in the same individual interrupted by a transposable

element), other PAC species are heterothallic possessing only

either the MAT1-1 or MAT1-2 idiomorph in their genomes

(Zaarano et al. 2010, 2011). Zaarano et al. (2010) showed

that in more than 80% of the populations of PAC species a 1:1

mating-type ratio and gametic equilibrium can be observed.

In addition, MAT genes were shown to evolve under strong

purifying selection. All three observations support the assump-

tion that cryptic sexual reproduction occurs in PAC species.

Moreover, the presence of sexual reproduction is also supported

by the nding of the teleomorphic state in Phaeomollisia piceae

T.N. Sieber & Grünig, a phylogenetically closely related species

(Grünig etal. 2009).

Another secret is whether PAC fungi are able to grow

through soil. PAC can readily be baited from forest soil using

Norway-spruce seedlings as bait (Ahlich et al. 1998; Trüssel

2011). However, it is not known if PAC actively grow through

soil toward host roots or are passively waiting as dormant

propagules, for example, microsclerotia in or on root debris,

until a susceptible root “grows past.” Trüssel (2011) tested myce-

lial growth through soil substrate in nonsterilized and gamma-

sterilized forest soil and peat–vermiculite. Norway-spruce

seedlings were used as bait separated from the PAC inoculated

substrate by a mesh screen that did not allow passage of roots.

Growth of mycelium occurred only in the sterilized substrates

and was slow with maximal distances of 2 cm covered in 3

months at 20°C, although the pH of 3.8 was optimal (Trüssel

2011). No growth occurred in nonsterilized forest soil probably

due to inhibition by other soil microorganisms. us, it remains

dubious if PAC can actively grow through soil or are transmitted

only by root contacts.

III. Methods of Detection

Isolation from plant tissues (1), histological examination (2),

assays of fungal-specic molecules, for example, ergosterol,

a sterol characteristic of fungal membranes (3), and culture-

independent DNA extraction and sequencing of specic loci

(4) are the four major groups of methods used to detect and

describe communities of endophytic fungi (Parsons 1981;

Savage and Sall 1981; El-Nashaar et al. 1986; Newell et al.

1988; Hampton etal. 1990; Newell 1992; Reissinger etal. 2001;

Sieber 2002; Schulz and Boyle 2005; Jumpponen and Jones

2009). Each of these methods has its advantages and disad-

vantages. Methods (1) and (4) but not (2) and (3) allow iden-

tication of the fungi. Only culturable fungi can be detected

with method (1), and the number and kind of species retrieved

depend on the strength of surface sterilization, the medium

used for incubation, and the sample size. With method (4),

it remains obscure whether the DNAs originated from liv-

ing or dead fungi, and consequently, the surface-sterilization

method used in combination with method (4) must not only

kill organisms on the plant surface but also remove their DNA.

Furthermore, method (4) strongly depends on the quality of

the databases used for sequence identication. Consequently,

only the application of several of these methods combined

allows obtaining a complete picture of the endophytic myco-

biota in a plant tissue.

Methods were developed to specically detect certain spe-

cies. Quantitative PCR was developed to detect and quantify

PAC in root tissues (Tellenbach etal. 2010). Quantication by

qPCR is, however, problematic because the amount of DNA is

measured and used to estimate biomass. Even if it is assumed

that each cell contains one nucleus, type and size of fungal cells

can vary considerably within and among isolates making esti-

mates inaccurate. For example, the method worked ne for PAC

strains that formed uniform, regular mycelia in the host but not

for those that produced lots of microsclerotia (Tellenbach etal.

2010). Although based on DNA, microsatellites provide an even

more sensitive detection and quantication method because

genets of the same species can be dierentiated and quantied

provided that genets possess dierent alleles at at least one locus

(Reininger etal. 2011b).

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-5Fungal Root Endophytes

IV. Root Endophytes of

Herbaceous Plants

Agricultural plants are among the best-studied herbaceous

plants in regard to root endophytes. Nonagricultural herbaceous

plants have only rarely been examined, and the detection of non-

mycorrhizal root endophytes was mostly a by-product during

studies of OM or AM fungi.

A. Grass Endophytes

Members of the Clavicipitaceae are the best-known grass

endophytes. They have received a lot of attention in the past

due to their beneficial effects upon their hosts (Clay 1988;

Schardl 2010). Some function as biocontrol agents against

insects and other herbivores, others produce growth-pro-

moting metabolites. Most effects are based on various kinds

of alkaloids produced by these endophytes. Clavicipitaceous

grass endophytes are considered to colonize their hosts sys-

temically. However, roots are usually not colonized. Azevedo

and Welty (1995) inoculated axenically grown tall fescue

(Festuca arundinacea Schreb.) seedlings with Neotyphodium

coenophialum (Morgan-Jones & W. Gams) Glenn, C.W.

Bacon & Hanlin but could not observe direct penetration

of the fungus into intact root cortex cells. Consequently,

improved growth and biomass accumulation of roots as well

as altered root morphology of infected plants grown at low

nutrient availability (e.g., phosphorus) are mediated by the

endophyte activity in the aerial plant parts (Malinowski

etal. 1998; Malinowski and Belesky 1999). However, roots of

grasses are habitats for many non-clavicipitalean endophytes

(Table 38.1).

e most frequent genera of grass-root endophytes are

Fusarium, Gaeumannomyces, Gibberella, Harpophora,

Microdochium, Monographella, and Periconia (Figure 38.1).

For example, Riesen and Sieber (1985) and Sieber etal. (1988)

isolated more than 100 species from roots of winter wheat.

Fusarium culmorum (W.G. Sm.) Sacc., Fusarium oxysporum

Schltdl., Gibberella zeae (Schwein.) Petch, Microdochium bol-

leyi, Monographella nivalis, Periconia macrospinosa Lefebvre

& Aar.G. Johnson, and Phaeosphaeria nodorum (E. Müll.)

Hedjar., the causal agent of glume blotch, were the dominant

fungal species. M. bolleyi was also regularly recovered from the

roots of healthy eld-grown barley (Hordeum vulgare L.), oats

(Avena sativa L.), and pasture grass (Murray and Gadd 1981).

Stoyke and Currah (1991) isolated DSE from an unidenti-

fied grass species in an alpine habitat of the Rocky Mountains

in Alberta, Canada. Similarly, dark septate endophytic

hyphae were observed in grasses collected on various islands

of the Southern Atlantic Ocean and the Antarctic Peninsula

(Christie and Nicolson 1983), and Upson et al. (2009) iso-

lated 243 DSE strains from the roots of Deschampsia ant-

arctica E. Desv. and Colobanthus quitensis (Kunth) Bartl.

(Caryophyllaceae) collected from 17 sites across a 1470 km

transect through maritime and sub-Antarctica. Most DSE

belonged to the Helotiales. Leptodontidium orchidicola Sigler

& Currah, Pezoloma ericae (D.J. Read) Baral, and species

of Tapesia and Mollisia could be identified by ITS sequence

comparison. Li etal. (2005) detected considerable coloniza-

tion of roots of several grass species collected in Kunming,

China, by DSE.

Grass and cereal roots are often colonized by dark sep-

tate Gaeumannomyces species and relatives. Take-all, caused

by Gaeumannomyces graminis var. tritici J. Walker and

Gaeumannomyces graminis var. avenae (E.M. Turner) Dennis,

is the most important root disease of wheat and oat world-

wide (Freeman and Ward 2004), but many Gaeumannomyces

species are nonpathogenic (Deacon 1981; Sieber 1985; Deacon

1987; Skipp and Christensen 1989; Blaschke 1991; Crous etal.

1995; Gutteridge etal. 2007). Gaeumannomyces species pos-

sess Phialophora-like anamorphs, which have been accom-

modated in the genus Harpophora by Gams (2000). Whereas

it is accepted that Harpophora graminicola (Deacon) W. Gams

is the anamorph of Gaeumannomyces cylindrosporus Hornby,

Slope, Gutter. & Sivan. (Ward and Bateman 1999; Freeman and

Ward 2004), there is some debate about other Harpophora–

Gaeumannomyces connections, especially when it comes to

the anamorphs of the various varieties of G. graminis (Sacc.)

Arx & D.L. Olivier. A Harpophora species isolated by McKeen

(1952) from corn roots was described as Harpophora radicic-

ola (Cain) W. Gams by Cain (1952). Some workers interpreted

H. radicicola as the anamorphic state of G. graminis var.trit-

ici (Lemaire and Ponchet 1963; Simonsen 1971). However, this

was considered not tenable by Walker (1981). In fact, identity

of H. radicicola with Gaeumannomyces graminis var. maydis

J.M. Yao, Yong C. Wang & Y.G. Zhu, the maize take-all fungus

from China (Yao etal. 1992), was demonstrated using molec-

ular genetics methods (Ward and Bateman 1999). In addition,

the same authors found H. radicicola to be almost identical to

Harpophora zeicola (Deacon & D.B. Scott) W. Gams, which

was described as a weak parasite of drought or otherwise

stressed maize plants in South Africa and France (Deacon

and Scott 1983). G. graminis var. maydis was also observed

in the roots of three alpine grasses (Deschampsia caespitosa

(L.) P. Beauv., Festuca pumila Chaix, and Poa alpina L.) grow-

ing at timberline (1900 m asl.) in Bavaria (Blaschke 1991).

Colonization of roots of Deschampsia flxuosa (L.) Trin. by

an unidentified DSE increased with increasing temperature

under a global warming scenario but was not affected by ele-

vated CO

levels (Olsrud etal. 2010; Table 38.1).

1. Anatomy

Epidermal and cortical root cells of cereal and grass roots lled

with heavily melanized microsclerotia are characteristic for

colonization by M. bolleyi (Murray and Gadd 1981). In con-

trast, inter- and intracellular hyphae of this fungus are hyaline.

Colonization of the stelar tissues of healthy roots does usually not

occur. ese patterns of colonization correspond well with those

observed by Rasmann etal. (2009) for M. bolleyi in tomato roots

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-6 Root–Rhizosphere Interactions

TABLE 38.1 Endophytes in Grasses (Family: Poaceae), Sedges (Family: Cyperaceae) and Bromeliads (Family: Bromeliaceae)

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acremonium sp. Hypocreales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Acremonium strictum Hypocreales Not DSE Ammophila arenaria Poales Grass In vitro exp a Hol etal. (2007)

Alternaria sp. Pleosporales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Alternaria sp. Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Aspergillus sp. Eurotiales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Bipolaris sp. Pleosporales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Campanella sp. Agaricales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Chaetomium funicola Sordariales Not DSE Hordeum vulgare Poales Grass In vitro exp b Vilich etal. (1998)

Chaetomium globosum Sordariales Not DSE Hordeum vulgare Poales Grass In vitro exp b Vilich etal. (1998)

Cladorrhinum foecundissimum Sordariales N.A. Elytrigia repens Poales Grass Isol & in

vitro exp

c Gasoni and Stegamn de

Gurnkel (2009)

Cladosporium cladosporiodes Capnodiales DSE Bothriochloa macra Poales Grass Isol White and Backhouse (2007)

Cladosporium cladosporiodes Capnodiales DSE Hyparrhenia hirta Poales Grass Isol White and Backhouse (2007)

Coniothyrium sp. Pleosporales Not DSE Triticum aestivum Poales Grass Isol Crous etal. (1995)

Cryptosporiopsis rhizophila Helotiales DSE Deschampsia exuosa Poales Grass In vitro exp d Zijlstra etal. (2005)

Curvularia inaequalis Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Cylindrocarpon didymum Hypocreales Not DSE Triticum aestivum Poales Grass Isol Sieber (1985)

Dictyochaeta fertilis Chaetosphaeriales Not DSE Lolium perenne Poales Grass Isol Skipp and Christensen (1989)

Drechslera sp. Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Embellisia chlamydospora Pleosporales DSE Carex stenophylla Poales Sedge Isol Graf, pers. comm. (2008)

Epicoccum sp. Pleosporales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Fusarium culmorum Hypocreales Not DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Fusarium oxysporum Hypocreales Not DSE Bothriochloa macra Poales Grass Isol White and Backhouse (2007)

Fusarium oxysporum Hypocreales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Fusarium oxysporum Hypocreales Not DSE Hyparrhenia hirta Poales Grass Isol White and Backhouse (2007)

Fusarium oxysporum Hypocreales Not DSE Lolium perenne Poales Grass Isol Skipp and Christensen (1989)

Fusarium oxysporum Hypocreales Not DSE Oryza sativa Poales Grass Isol Fisher and Petrini (1992)

Fusarium oxysporum Hypocreales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Fusarium redolens Hypocreales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Fusarium sp. Hypocreales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010), Khidir

etal. (2010)

Fusarium sp. Hypocreales DSE Sporobolus cryptandrus Poales Grass Isol Khidir etal. (2010)

Fusarium spp. Hypocreales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Gaeumannomyces cylindrosporus

Magnaporthaceae DSE Poa pratensis Poales Grass Isol Saleh and Leslie (2004)

Gaeumannomyces cylindrosporus

Magnaporthaceae DSE Various grass species Poales Grass Isol e Deacon (1981)

Gaeumannomyces cylindrosporus

Magnaporthaceae DSE Vulpia ciliata Poales Grass In vitro exp f Newsham (1999)

Gaeumannomyces graminis var.

graminis

Magnaporthaceae DSE Oryza sativa Poales Grass Isol Saleh and Leslie (2004)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-7Fungal Root Endophytes

Gaeumannomyces graminis var.

maydis

Magnapothaceae DSE Lolium perenne Poales Grass Isol Skipp and Christensen (1989)

Gaeumannomyces graminis var.

maydis

Magnaporthaceae DSE Zea mays Poales Grass Isol Cain (1952)

Gaeumannomyces graminis var.

maydis

Magnaporthaceae DSE Zea mays Poales Grass Isol Ward and Bateman (1999)

Gaeumannomyces sp. Magnaportaceae DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Gibberella avenacea Hypocreales Not DSE Triticum aestivum Poales Grass Isol Crous etal. (1995)

Gibberella zeae Hypocreales Not DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Harpophora oryzae Magnaporthaceae DSE Oryza sativa Poales Grass Isol Yuan etal. (2010)

Idriella lunata Helotiales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Ilyonectria radicicola Hypocreales Not DSE Triticum aestivum Poales Grass Isol Sieber (1985)

Leptodontidium sp. Helotiales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Meliniomyces variabilis

LtVB3

Leotiomycetes DSE Hordeum vulgare Poales Grass Isol Narisawa etal. (2004)

Microdochium bolleyi Xylariales DSE Elymus farctus Poales Grass Isol Sánchez Márquez etal. (2008)

Microdochium bolleyi Xylariales DSE Poa alpigena Poales Grass Isol Väre etal. (1992)

Microdochium bolleyi Xylariales DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Microdochium bolleyi Xylariales DSE Triticum aestivum Poales Grass In vitro &

eld exp

g Reinecke (1978)

Microdochium bolleyi Xylariales DSE Triticum aestivum Poales Grass Isol Riesen and Sieber (1985)

Microdochium bolleyi Xylariales DSE Triticum aestivum Poales Grass In vitro exp h Kirk and Deacon (1987)

Microdochium sp. Xylariales DSE Andropogon gerardii Poales Grass In vitro exp i Mandyam etal. (2010)

Microdochium sp. Xylariales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Microdochium sp. Xylariales DSE Grasses Poales Grass Isol Mandyam etal. (2010)

Microdochium spp. Xylariales DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Mollisia sp. Helotiales DSE Deschampsia antarctica Poales Grass Isol Upson etal. (2009)

Moniliophthora sp. Agaricales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010), Khidir

etal. (2010)

Moniliophthora sp. Agaricales DSE Sporobolus cryptandrus Poales Grass Isol Khidir etal. (2010)

Monodictys sp. Dothideomycetes DSE Carex stenophylla Poales Sedge Isol Graf, pers. comm. (2008)

Monographella nivalis Xylariales Not DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Monosporascus sp. Xylariales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Neurospora sp. Sordariales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Paraphaeosphaeria sp. Pleosporales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010), Khidir

etal. (2010)

Paraphaeosphaeria sp. Pleosporales DSE Sporobolus cryptandrus Poales Grass Isol Khidir etal. (2010)

Paraphoma meti Pleosporales DSE Vulpia ciliata Poales Grass In vitro exp f Newsham (1994)

Penicillium sp. Eurotiales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Penicillium sp. Eurotiales Stipa grandis Poales Grass Isol Su etal. (2010)

Periconia macrospinosa Pleosporales DSE Andropogon gerardii Poales Grass In vitro exp j Mandyam etal. (2010)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-8 Root–Rhizosphere Interactions

TABLE 38.1 (continued) Endophytes in Grasses (Family: Poaceae), Sedges (Family: Cyperaceae) and Bromeliads (Family: Bromeliaceae)

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Periconia macrospinosa Pleosporales DSE Bothriochloa macra Poales Grass Isol White and Backhouse (2007)

Periconia macrospinosa Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Periconia macrospinosa Pleosporales DSE Hyparrhenia hirta Poales Grass Isol White and Backhouse (2007)

Periconia macrospinosa Pleosporales DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Periconia macrospinosa Pleosporales DSE Andropogon gerardii Poales Grass In vitro exp k Mandyam etal. (2010)

Periconia macrospinosa Pleosporales DSE Grasses Poales Grass Isol Mandyam etal. (2010)

Periconia macrospinosa Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Periconia sp. Pleosporales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Phaeocytostroma plurivorum Pezizomyc incert N.A. Stipa grandis Poales Grass Isol Su etal. (2010)

Phaeosphaeria nodorum Pleosporales Not DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Phialocephala fortinii s.l. Helotiales DSE Deschampsia exuosa Poales Grass Isol Tejesvi and Ruotsalainen (2010)

Phialocephala fortinii s.l. Helotiales DSE Deschampsia exuosa Poales Grass In vitro exp l Zijlstra etal. (2005)

Phialocephala fortinii s.l. Helotiales DSE Poa alpigena Poales Grass Isol Väre etal. (1992)

Phialocephala sp. 8 Helotiales DSE Carex aquatilis Poales Sedge Isol Grünig etal. (2009)

Phialophora sp. N.A. DSE Carex curvula Poales Sedge Isol Haselwandter and Read (1982)

Phialophora sp. N.A. DSE Carex rma Poales Sedge Isol f Haselwandter and Read (1982)

Phialophora sp. Helotiales N.A. Deschampsia exuosa Poales Grass Isol Tejesvi and Ruotsalainen (2010)

Phialophora sp. Helotiales N.A. Stipa grandis Poales Grass Isol Su etal. (2010)

Phialophora sp. 1 Helotiales DSE Triticum aestivum Poales Grass Isol Rooden, unpublished

Phoma sp. Pleosporales DSE Bouteloua gracilis Poales Grass Isol Herrera etal. (2010)

Phoma glomerata Pleosporales DSE Triticum aestivum Poales Grass Isol Crous etal. (1995)

Podospora sp. Sordariales Not DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Polymyxa sp. Plasmodiophoraceae Not DSE Sorghum bicolor Poales Grass In vitro exp Galamay etal. (1992)

Pyrenochaeta sp. 1 Pleosporales DSE Holcus lanatus Poales Grass Isol Sánchez Márquez etal. (2010)

Rhizoctonia sp. Cantharellales DSE Carex curvula Poales Sedge Isol Haselwandter and Read (1982)

Rhizoctonia sp. Cantharellales DSE Carex rma Poales Sedge Isol f Haselwandter and Read (1982)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-9Fungal Root Endophytes

Rhizoctonia sp. Cantharellales DSE Carex lasiocarpa, C.

aquatilis

Poales Sedge Isol ormann etal. (1999)

Rhizoctonia spp. Cantharellales Not DSE Triticum aestivum Poales Grass Isol Sieber etal. (1988)

Tapesia sp. Helotiales DSE Deschampsia antarctica Poales Grass Isol Upson etal. (2009)

ielavia appendiculata Sordariales Not DSE Stipa grandis Poales Grass Isol Su etal. (2010)

Trematosphaeria clarkii Pleosporales DSE Oryza sativa Poales Grass Isol Fisher and Petrini (1992)

Unidentied DSE DSE Arrhenatherum elatius Poales Grass Micros Deram etal. (2008)

Unidentied DSE DSE Bouteloua eriopoda Poales Grass In vitro exp Barrow etal. (2004)

Unidentied DSE DSE Bouteloua gracilis Poales Grass ITS Green etal. (2008)

Unidentied DSE DSE Bouteloua gracilis Poales Grass Micros Medina-Roldan etal. (2008)

Unidentied DSE DSE Cynodon dactylon Poales Grass Micros Li etal. (2005)

Unidentied DSE DSE Cyperus rotundus Poales Grass Micros Li etal. (2005)

Unidentied DSE DSE Deschampsia exuosa Poales Grass Open-top

chambers

in forest

m Olsrud etal. (2010)

Unidentied DSE DSE Deuterocohnia

longipetala

Poales Bromelia Micros Lugo etal. (2009)

Unidentied DSE DSE Digitaria cruciata Poales Grass Micros Li etal. (2005)

Unidentied DSE DSE Dyckia spp. Poales Bromelia Micros Lugo etal. (2009)

Unidentied DSE DSE Paspalum distichum Poales Grass Micros Li etal. (2005)

Unidentied DSE DSE Phragmites australis Poales Grass Micros Dolinar and Gaberscik (2010)

Unidentied DSE DSE Poa annua Poales Grass Micros Li etal. (2005)

Unidentied DSE DSE Tillandsia spp. Poales Bromelia Micros Lugo etal. (2009)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

the anamorph (asexual reproductive stage) are produced, the name of the teleomorph is given. Names of anamorph(s) can be retrieved from the list of the teleomorph’s synonyms provided in the index. e

next lower taxon is given if the fungus Order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots; in vitro exp, fungus used in in-vitro experiment(s); ITS, detection by DNA extraction, sequencing of the ITS regions and sequence comparison with sequence

databases; Micros, detection by microscopy.

Special eect details: (a) Plant growth stimulation; improved sand stabilizing role of host in coastal dunes; control of nematodes. (b) Growth stimulation of roots; control of Blumeria graminis. (c) Biocontrol

of damping-o, root and stem rot, caused by anatephorus cucumeris, in cotton. (d) Enhanced nitrogen uptake. (e) Control of Gaeumannomyces graminis. (f) Plant growth stimulation. (g) Control of

Phaeosphaeria nodorum, Fusarium and Gibberella species. (h) Control of Gaeumannomyces graminis var. tritici and Gaeumannomyces cylindrosporus. (i) Plant growth stimulation by one isolate. (j) Plant growth

stimulation by two of three isolates. (k) Plant growth stimulation by one of two isolates. (l) Increase of nitrogen uptake. (m) Increased colonization at higher temperatures, but not at elevated CO

Anamorph: Harpophora graminicola.

Anamorph: Harpophora radicicola.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-10 Root–Rhizosphere Interactions

(Figure38.2A). Microsclerotia like those formed by M. bolleyi

were also observed in roots of Poa alpina (cited as Poa alpi-

gena) in Spitsbergen (Väre etal. 1992).

Colonization by Harpophora spp. (anamorphic

Gaeumannomyces spp.) is usually recognized by dark septate

runner hyphae growing on the root surface. e surface myce-

lium of some species also possesses hyphopodia that can be

lobed or unlobed (Deacon 1981), a feature that is considered suit-

able to discriminate the varieties tritici, avenae, and maydis of

G. graminis, which possess simple hyphopodia from the variety

graminis that has lobed hyphopodia (Freeman and Ward 2004;

Figure38.2B). Depth of penetration into the root cortex and the

stele and, thus, virulence depend on the fungus and host species,

the environmental conditions, and the age and type of roots.

G. graminis var. maydis forms a net of stout brown runner

hyphae with lateral hyphopodia on the root surface (McKeen

1952). Infection of the cortical cells of primary, seminal, and

adventitious roots occurred by slender colorless microhy-

phae, but the roots appeared usually healthy. Sometimes indi-

vidual cells were completely lled with enlarged fungus cells

that later assumed thick, brown walls typical for microscle-

rotia (McKeen 1952). Skipp and Christensen (1989) observed

microsclerotia similar to those observed by McKeen (1952)

in cortical cells of roots of Lolium perenne L. from various

sites in New Zealand. Isolations from surface-sterilized root

segments conrmed presence of G. graminis var. maydis. G.

cylindrosporus is a nonpathogenic endophyte (Deacon 1987).

Mycelia of G. cylindrosporus and G. graminis develop similarly

on roots, but G. cylindrosporus does not penetrate the vascular

system. Whereas in young regions of the roots, the dark, lysis-

resistant runner hyphae of G. cylindrosporus are conned to

the root surface and the fungus penetrates only little into the

cortex, on older regions, the runner hyphae grow intercellu-

larly deep within the cortex (Deacon 1987).

Intracellular pycnidia of Phoma meti Brunaud were observed

in the root cortex of the annual grass Vulpia ciliata Dumort

(Newsham 1994). Intracellular sporulation may be ecologically

advantageous because conidia can spread rapidly right aer rup-

ture of the cell wall in sloughed-o cortical cells.

Galamay et al. (1992) observed blackberry-like sclero-

tia of an endophyte in the epidermal and hypodermal cells

of nodal and rst-order lateral roots of Sorghum bicolor (L.)

Moench. e fungus was tentatively identied as Polymyxa

sp. (Plasmodiophoromycetes). Since tissues internal to the

(A) (B)

60 μm,

(C)

(E)

(F)

(D)

FIGURE 38.2 (A) Multicellular microsclerotia of Microdochium bolleyi lling single cortex cells in a tomato root. (From Rasmann, C. etal.,

Appl. Soil Ecol., 43, 22, 2009.) (B) Hyphopodia of Gaeumannomyces graminis var. graminis wild-type strain JH2033 formed on Mylar lms.

(From Money, N.P. etal., Fungal Genet. Biol., 24, 240, 1998.) Scale bar = 20 μm. (C) Intracellular spherical to pear-shaped chlamydospores of

Piriformospora indica in cortical cells of a barley root. (From Waller, F. etal., Proc. Natl. Acad. Sci. U S A, 102, 13386, 2005.) (D) Morphology and

fungal colonization (most probably Inocybe sp.) of coralloid rhizomes of the orchid Epipogium aphyllum. Magnication detail of infected cells with

view of elongated fungal pelotons cut transversally in P1 and longitudinally in P2 (n, orchid cell nucleus, is, in orescence shoots). (From Roy, M.

etal., Ann. Bot., 104, 595, 2009.) Scale bar = 50 μm. (E) Squash mount of mycorrhizal root of Calypso bulbosa stained with chlorazol black showing

sclerotium-like structures of a DSE in cortical cells. (From Currah, R.S. etal., Am. J. Bot., 75, 739, 1988.) Scale bar = 13 μm. (F) Epidermal micro-

sclerotium (*) of Phialocephala fortinii s.l. (CSP 12, strain UAMH 9525) in a root of Asparagus ocinalis. (From Yu, T. etal., Can. J. Microbiol., 47,

741, 2001.) Scale bar = 15 μm.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-11Fungal Root Endophytes

hypodermis were never colonized, it was assumed that the hypo-

dermis functions as a barrier to protect the inner tissues from

colonization by the fungus.

In substrate inoculated with Piriformospora indica Sav.

Verma, Aj. Varma, Rexer, G. Kost & P. Franken, the fungus

entered barley (H. vulgare L.) roots primarily via root hairs

and proceeded intracellularly into rhizodermal cells and later

on into the root cortex (Waller etal. 2005). It forms spherical

to pear-shaped chlamydospores in both root hairs and cortical

cells (Figure 38.2C). Hyphae were detected neither in the central

part of the roots beyond the endodermis nor in stems or leaves.

2. Endophyte–Pathogen Interactions,

Biological Control

Antagonism between Phaeosphaeria nodorum and M. bolleyi

was observed by Reinecke (1978) and Reinecke and Fokkema

(1981). M. bolleyi behaved also as an antagonist against Fusarium

species (Reinecke 1978; Sieber 1985) and was reported to

reduce damage to or colonization of cereal roots by G. graminis

var. tritici (Kirk and Deacon 1987). Similarly, G. cylindrosporus

controlled pathogens in Vulpia ciliata (Newsham 1999) and

gave signicant control of take-all by competition for senescing

root tissues (Deacon 1981). G. cylindrosporus is found in rela-

tively low amounts on cereal roots unless the cereal crop fol-

lows 1 or 2 years of grass (or cereal crop) (Deacon 1987). Crop

rotation, a very eective form of disease management with a

long tradition, seems to be disadvantageous for G. cylindrospo-

rus and, thus, for control of take-all. Several other endophytic

fungi possess antagonistic activity against G. graminis var.

tritici (Macia-Vicente etal. 2008): Acremonium blochii (Matr.)

W. Gams, Acremonium furcatum (Moreau & V. Moreau) ex

W. Gams, Aspergillus fumigatus Fresen., Cyclindrocarpon sp.,

Dactylaria sp., Gibberella intricans Wollenw. (teleomorph

of Fusarium equiseti (Corda) Sacc.), Ilyonectria radicicola

(Gerlach & L. Nilsson) Chaverri& C. Salgado (teleomorph of

Cylindrocarpon destructans (Zinsm.) Scholten), Phoma her-

barum Westend., P. leveillei Boerema & G.J. Bollen. A. blochii,

Aspergillus fumigatus, Dactylaria sp., G. intricans, and Phoma

herbarum reduced colonization of barley roots by this fungus.

Cladorrhinum foecundissimum Sacc. & Marchal, isolated from

the grass Elytrigia repens (L.) Desv. ex Nevski, controlled root

and stem rot caused by Rhizoctonia solani J.G. Kühn in cotton

(Gossypium hirsutum L.) (Gasoni and Stegman de Gurnkel

2009). Disease severity of powdery mildew (Blumeria graminis

(DC.) Speer f. sp. hordei Jacz.) on primary leaves of H. vulgare

was reduced when seeds had been treated with spore suspen-

sions of Chaetomium globosum Kunze ex Fr. and Chaetomium

funicola Cooke (Vilich etal. 1998). Endophytic Acremonium

strictum W. Gams in roots of the grass Ammophila arenaria

(L.) Link was nematicidal and reduced the adverse eects of

nematodes (Hol etal. 2007).

3. Endophyte–Plant Interactions

Root inoculations with a Microdochium species (DSE)

and Periconia macrospinosa Lefebvre & Aar.G. Johnson

(DSE) from grass roots collected in a mesic tallgrass prai-

rie increased the biomass of the grass Andropogon gerardii

Vitman (Mandyam etal. 2010). Nitrogen uptake of D. flex-

uosa was enhanced by the DSE Cryptosporiopsis rhizophila

Verkley & Zijlstra and Phialocephala fortinii s.l. (Zijlstra etal.

2005). Presence of the DSE Phoma fimeti in the roots of the

annual grass V. ciliata increased root and shoot biomass, root

lengths, and tiller numbers (Newsham 1994). Similarly, G. cyl-

indrosporus increased tiller number and biomass production

of V. ciliata (Newsham 1999). Metacordyceps chlamydosporia

(H.C. Evans) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,

a clavicipitalean nematode parasite colonized barely roots

endophytically and promoted plant growth (Macia-Vicente

etal. 2008). Acremonium strictum was shown to increase root

biomass and the number of tillers in Ammophila arenaria

(Hol etal. 2007). Increased root fresh weight was observed

after seeds of barley (H. vulgare) were treated with spore sus-

pensions of C. globosum or C. funicola (Vilich etal. 1998).

Similarly, inoculations with Piriformospora indica enhanced

yield in barley (Waller etal. 2005).

B. Orchid Endophytes

Classical OM fungi of the Rhizoctonia-type are polyphyletic

and belong to several different orders of the Basidiomycotina

(Sebacinales, Ceratobasidiales, Tulasnellales) (Currah

and Zelmer 1992; Smith and Read 2008; Weiss etal. 2011).

Orchids, especially achlorophyllous, mycoheterotrophic ones,

often associate also with basidiomycetes that form ECM with

woody plants, for example, Inocybe, Hebeloma, Xerocomus,

Lactarius, or Thelephora species and, thus, probably indi-

rectly exploit the neighboring trees as carbon sources (Roy

etal. 2009; Table 38.2). In addition, many orchids host mem-

bers of the ascomycotina. Leptodontidium orchidicola Sigler

& Currah, Phialocephala fortinii s.l., Trichocladium opacum

(Corda) S. Hughes, and Trichosporiella multisporum Sigler

& Currah were frequently isolated from terrestrial orchids

(Currah etal. 1987, 1988, 1990; Currah and Sherburne 1992).

Tao etal. (2008) examined the endophytes of the terrestrial

orchid Bletilla ochracea Schltr. using denaturing gradi-

ent gel electrophoresis (DGGE) and random cloning analy-

sis and detected 10 operational taxonomic units (OTUs) of

endophytic fungi. Two Mycosphaerella species, an unknown

ascomycete species, and an Alternaria species dominated.

Oidiodendron spp. may be significant symbionts in orchids

because they are also known to form endomycorrhizae with

ericaceous plants (Currah and Zelmer 1992). Vujanovic

et al. (2000) described Phialocephala victorinii Vujan. &

St-Arn., an orchid endophyte with dark septate hyphae.

Epiphytic and lithophytic orchids in the tropics often yield

large numbers of isolates of fungi belonging to the Xylariales

(Bayman etal. 1997; Table 38.2). Members of the Xylariaceae

are also the most frequently isolated endophytes of leaves

of tropical palms (Rodrigues 1996). Epiphytic orchids may,

thus, harbor the same endophytes as the trees they grow on.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-12 Root–Rhizosphere Interactions

TABLE 38.2 Endophytes in Orchids (Family Orchidaceae)

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acremonium sp. Hypocreales Not DSE Dendrobium loddigesii Asparagales Orchid Isol Chen etal (2010b)

Alternaria sp. Pleosporales DSE Oncidium warmingii Asparagales Orchid Isol and in vitro

exp with crude

extracts

a Vaz etal. (2009)

Alternaria sp. Pleosporales DSE Bletilla ochracea Asparagales Orchid Mol Tao etal. (2008)

Armillaria mellea Agaricales Not DSE Gastrodia elata Asparagales Orchid Isol Xu and Guo (2000)

Aspergillus spp. Eurotiales Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Cadophora malorum Helotiales DSE Bletilla striata Asparagales Orchid Isol Chen etal. (2010a)

Cadophora sp. Helotiales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Cenococcum geophilum Dothideomycetes Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Colletotrichum sp. Sordariomycetes Not DSE Dendrobium nobile Asparagales Orchid Isol Yuan etal. (2009)

Colletotrichum sp. Sordariomycetes Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Cryptococcus carnescens Tremellales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Cryptosporiopsis ericae Helotiales DSE Spiranthes sinensis Asparagales Orchid Isol Chen etal. (2010a)

Cylindrocarpon sp. Hypocreales Not DSE Cremastra appendiculata Asparagales Orchid Isol Zhang etal. (2006)

Cylindrocarpon sp. Hypocreales Not DSE Sophronitis fournieri Asparagales Orchid Isol Vaz etal. (2009)

Epicoccum nigrum Pleosporales DSE Maxillaria rigida Asparagales Orchid Isol and in vitro

exp with crude

extracts

b Vaz etal. (2009)

Exophiala sp. Chaetothyriales DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Fusarium chlamydosporum Hypocreales Not DSE Dendrobium crumenatum Asparagales Orchid Isol Siddiquee etal. (2010)

Fusarium oxysporum Hypocreales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Fusarium sp. Hypocreales Not DSE Anacamptis pyramidalis Asparagales Orchid Isol Gezgin and Eltem (2009)

Fusarium sp. Hypocreales Not DSE Bulbophyllum involutum Asparagales Orchid Isol and in vitro

exp with crude

extracts

b Vaz etal. (2009)

Fusarium sp. Hypocreales Not DSE Dendrobium loddigesii Asparagales Orchid Isol Chen etal. (2010b)

Fusarium sp. Hypocreales Not DSE Isochilus linearis Asparagales Orchid Isol Vaz etal. (2009)

Fusarium sp. Hypocreales Not DSE Ophrys fusca Asparagales Orchid Isol Gezgin and Eltem (2009)

Fusarium sp. Hypocreales Not DSE Orchis sancta Asparagales Orchid Isol Gezgin and Eltem (2009)

Fusarium sp. Hypocreales Not DSE Serapias vomeracea

subsp. orientalis

Asparagales Orchid Isol Gezgin and Eltem (2009)

Geopyxis sp. Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Gibberella fujikuroi var.

fujikuroi

Hypocreales Not DSE Epidendrum secundum Asparagales Orchid Isol Vaz etal. (2009)

Guignardia mangifera Botryosphaeriales Not DSE Dendrobium nobile Asparagales Orchid Isol Yuan etal. (2009)

Gymnopus sp. Agaricales Not DSE Wullschlaegelia aphylla Asparagales Orchid Isol c Martos etal. (2009)

Hebeloma sp. Agaricales Not DSE Epipogium aphyllum Asparagales Orchid Isol Roy etal. (2009)

Hypocrea sp. Hypocreales not DSE Sophronitis longipes Asparagales Orchid Isol Vaz etal. (2009)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-13Fungal Root Endophytes

Hypoxylon sp Xylariales not DSE Dendrobium nobile Asparagales Orchid Isol Yuan etal. (2009)

Ilyonectria radicicola Hypocreales not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Inocybe sp. Agaricales not DSE Epipogium aphyllum Asparagales Orchid Isol Roy etal. (2009)

Lactarius pubescens Agaricales not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Lactarius sp. Agaricales not DSE Epipogium aphyllum Asparagales Orchid Isol Roy etal. (2009)

Lecanora sp. Lecanorales not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Leptodontidium orchidicola Helotiales DSE Orchids Asparagales Orchid Isol Currah etal. (1987, 1988, 1990)

Leptodontidium orchidicola Helotiales not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Leptodontidium sp. Helotiales DSE Cephalanthera longifolia Asparagales Orchid Isol Abadie etal. (2006)

Leptodontidium sp. Helotiales DSE Dendrobium nobile Asparagales Orchid Isol and in vitro exp d Hou and Guo (2009)

Morchella sp. Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Mycena alphitophora Agaricales Not DSE Gastrodia elata Asparagales Orchid Isol Xu and Guo (2000)

Mycena sp. Agaricales Not DSE Wullschlaegelia aphylla Asparagales Orchid Isol c Martos etal. (2009)

Mycosphaerella sp. N.A. Bletilla ochracea Asparagales Orchid Mol Tao etal. (2008)

Penicillium griseofulvum Ascomycota

incert

Not DSE Dendrobium nobile Asparagales Orchid Isol Yuan etal. (2009)

Penicillium spp. Eurotiales Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Pestalotia spp. Xylariales Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Peziza sp. Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Phialocephala fortinii s.l. Helotiales DSE Orchids Asparagales Orchid Isol Currah etal. (1987, 1988, 1990)

Phialocephala victorinii Helotiales DSE Orchids Asparagales Orchid Isol Vujanovic etal. (2000)

Phialocephala europaea Helotiales DSE Calypso bulbosa Asparagales Orchid Isol Currah etal. (1988)

Phialophora sp. Chaetothyriales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Phialophora sp. Helotiales Not DSE Cypripedium spp. Asparagales Orchid Isol Sheerson etal. (2005)

Resinicium sp. Aphyllophorales Not DSE Gastrodia similis Asparagales Orchid Isol c Martos etal. (2009)

Rhizoctonia spp. Cantharellales Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Rhodotorula mucilaginosa Sporidiobolales Not DSE Acianthera hamosa Asparagales Orchid Isol Vaz etal. (2009)

Russula brevipes Agaricales Not DSE Limodorum abortivum Asparagales Orchid Isol Girlanda etal. (2006)

Russula chloroides Agaricales Not DSE Limodorum abortivum Asparagales Orchid Isol Girlanda etal. (2006)

Russula delica Agaricales Not DSE Limodorum abortivum Asparagales Orchid Isol Girlanda etal. (2006)

Russula exalbicans Agaricales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Russula lepidicolor Agaricales Not DSE Dipodium hamiltonianum Asparagales Orchid Isol Dearnaley and Le Brocque

(2006)

Russula lilacea Agaricales Not DSE Dipodium hamiltonianum Asparagales Orchid Isol Dearnaley and Le Brocque

(2006)

Russula sp. Agaricales Not DSE Cypripedium parviorum Asparagales Orchid Isol Sheerson etal. (2005)

Serendipita vermifera Auriculariales Not DSE Orchids Asparagales Orchid Isol & in vitro exp d Weiss etal. (2011)

Terfezia sp. Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Tetracladium sp. Helotiales DSE Cephalanthera longifolia Asparagales Orchid Isol Abadie etal. (2006)

Tetracladium sp. Helotiales DSE Orchis militaris Asparagales Orchid Isol Vendramin etal. (2010)

elephora sp. elephorales Not DSE Epipogium aphyllum Asparagales Orchid Isol Roy etal. (2009)

Titaea maxilliforme Helotiales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-14 Root–Rhizosphere Interactions

TABLE 38.2 (continued) Endophytes in Orchids (Family Orchidaceae)

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Trichocladium opacum Sordariales DSE Orchids Asparagales Orchid Isol Currah etal. (1987, 1988, 1990)

Trichoderma asperellum Hypocreales Not DSE Epidendrum secundum Asparagales Orchid Isol Vaz etal. (2009)

Trichosporiella multisporum Helotiales Not DSE Orchids Asparagales Orchid Isol Currah etal. (1987, 1988, 1990)

Verpa conica Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Wilcoxina rehmii Pezizales Not DSE Gymnadenia conopsea Asparagales Orchid Isol Stark etal. (2009)

Wilcoxina sp. Pezizales DSE Cephalanthera longifolia Asparagales Orchid Isol Abadie etal. (2006)

Xerocomus sp. Agaricales Not DSE Epipogium aphyllum Asparagales Orchid Isol Roy etal. (2009)

Xylaria spp. Xylariales Not DSE Dendrobium nobile Asparagales Orchid Isol Yuan etal. (2009)

Xylaria spp. Xylariales Not DSE Lepanthes spp. Asparagales Orchid Isol Bayman etal. (1997)

Unidentied DSE DSE Maianthemum bifolium Asparagales Herb Isol Postma etal. (2007)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

next lower taxon is given if the Fungus order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots; in vitro exp, fungus used in in-vitro experiment(s); Mol, culture-free, molecular detection method.

Special eect details: (a) Antibacterial against Escherichia coli and Staphylococcus aureus. (b) Antimycotic against pathogenic yeasts Candida krusei and C. albicans. (c) Food chain link between dead leaves

and orchid. (d) Plant growth stimulation.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-15Fungal Root Endophytes

Confirmation of this assumption would evoke the question

of whether the infection occurs by hyphae growing directly

from one host to the other or by inoculi (spores, conidia) on

each host independently.

1. Anatomy

In contrast to the complex globular masses (hyphal coils) or

pelotons of branched and anastomosed hyphae formed by

classical orchid mycorrhizae within cortical cells (Roy et al.

2009; Figure 38.2D), L. orchidicola and Phialocephala forti-

nii were observed to form small sclerotia (Currah etal. 1988;

Figure38.2E).

2. Endophyte–Pathogen and Endophyte–Plant

Interactions

Crude extracts from Alternaria sp. (DSE) from the roots of

Oncidium warmingii Rchb. f. showed signicant antibac-

terial activity against Escherichia coli and Staphylococcus

aureus (Vaz et al. 2009). Similarly, Epicoccum nigrum Link

(DSE) from Maxillaria rigida Barb. Rodr. and an unidenti-

ed Fusarium species from Bulbophyllum involutum Borba,

Semir & F. Barros controlled the human pathogenic yeasts

Candida krusei (Castell.) Berkhout and Candida albicans (C.P.

Robin) Berkhout (Vaz etal. 2009). A Leptodontidium species

associated with a subtropical Dendrobium species stimu-

lated growth of Dendrobium nobile Lindl. seedlings in vitro

(Hou and Guo 2009).

C. Other Herbaceous Plant Hosts

A plethora of fungi were detected in asymptomatic, healthy

roots of many non-graminiculous, non-orchid herbaceous

plant species growing in arctic, alpine (Christie and Nicolson

1983; Stoyke and Currah 1991; Väre etal. 1992; Ruotsalainen

etal. 2004; Schmidt etal. 2008; Lv etal. 2010), aquatic (Kai

and Zhao 2006), arid (Lugo etal. 2009), or neotropical habi-

tats (Lehnert etal. 2009; Table 38.3). Terrestrial Bromeliaceae

were colonized by both AM fungi and DSE except Bromelia

urbaniana (Mez) L.B. Sm., which was not colonized by either

one of them. In contrast, epiphytic Bromeliaceae were colo-

nized only by DSE (Lugo etal. 2009). AM structures were

observed in seven and DSE in four of 32 hydrophyte species

from lakes and streams in Southwestern China (Kai and Zhao

2006). The frequency of hydrophytes hosting AM fungi and/

or DSE was higher in water bodies of the Upper Parana in

South America where AM was detected in nine species and

DSE in 16 of 24 species (De Marins etal. 2009). Fourteen spe-

cies of endophytes were isolated from the roots of Saussurea

involucrata Kar. & Kir. collected at >2600 m asl in the

Tianshan Mountains in China. Species of Cylindrocarpon,

Phoma, and Fusarium dominated the endophytic fungal

community (Lv etal. 2010). Fernandez etal. (2008) detected

DSE in the roots of Lycopodium paniculatum Desv. ex Poir.

and Equisetum bogotense Kunth in a Valdivian temperate

forest of Patagonia, Argentina. DSE were also detected in

Gentianaceae Gentianella magellanica Gaudich., Gentianella

parviflora (Griseb.) T.N. Ho, Gentianella multicaulis (Gillies

ex Griseb.) Fabris, and Gentiana prostrata Haenke indig-

enous in Argentina (Salvarredi et al. 2010). Trichoderma

asperellum Samuels, Lieckf. & Nirenberg, Gliocladium virens

J.H. Mill., Giddens & A.A. Foster, and Hypocrea lixii Pat.

were endophytic in and epiphytic on banana roots (Xia etal.

2011), whereas Trichoderma brevicompactum G.F. Kraus,

C.P. Kubicek & W. Gams was isolated only from inside of the

roots. Genetic diversity of endophytic T. asperellum and G.

virens was lower than that of epiphytic ones, suggesting that

only selected genotypes are able to infect the roots. Väre etal.

(1992) studied the fungi associated with roots of 76 (72 herba-

ceous) plant species in Spitsbergen. Ectomycorrhizae and AM

fungi were absent from all herbaceous plant species, except

Pedicularis dasyantha Hadač that showed slight ectomycor-

rhizal colonization. In contrast, root endophytes were com-

monly isolated. As already mentioned earlier, Upson et al.

(2009) isolated 243 mostly helotialean DSE strains from the

roots of Deschampsia antarctica (grass) and Colobanthus

quitensis (Kunth) Bartl. (Caryophyllaceae) along a transect

across sub-Antarctica.

1. Anatomy

Rodríguez-Gálvez and Mendgen (1995) studied the ultrastructure

of the infection process by Fusarium oxysporum f. sp. vasinfectum,

causal agent of tracheomycosis of species of the Malvaceae, for

example, cotton. High-pressure freezing of infected cortical cells

revealed that F. oxysporum penetrates and grows within the host

cells without inducing damages such as plasmolysis, cell degenera-

tion, or host necrosis. It was suggested, therefore, that F. oxyspo-

rum f. sp. vasinfectum has an endophytic, biotrophic phase during

colonization of the root tips.

e most frequently observed fungal structures in the roots of

30 of 72 examined herbaceous plant species in Spitsbergen were

inter- and intracellularly growing melanized, septate mycelia

(DSE) (Väre etal. 1992). In addition, cortical cells of Polemonium

boreale Adams, a herbaceous Ericaceae, were lled with dark

microsclerotia that resembled those formed by M. bolleyi and

Phialocephala fortinii s.l. Similarly, Treu et al. (1996) detected

dark microsclerotia in root cells of various alpine plants collected

in Denali National Park, Alaska. A strain of P. fortinii s.l. CSP

12 (UAMH 9525) isolated from Vaccinium vitis-idaea L. formed

microsclerotia having a “puzzle-like” appearance in the roots

of Asparagus ocinalis L. similar to those observed in conifer

roots (Yu etal. 2001; Figure 38.2F). In the cortex of young roots

of Chinese cabbage, dark septate hyphae of Cladophialophora

(Heteroconium) chaetospira (Grove) Crous & Arzanlou were

abundant (Figure 38.3A), whereas the cortex of older roots was

lled with microsclerotia (Yonezawa et al. 2004). Similarly,

hyphae and chlamydospores of DSE were observed in primary

roots of Xenophyllum rosenii (R.E. Fr.) V.A. Funk (Asteraceae) col-

lected at 5389 m asl (Schmidt etal. 2008; Figure38.3B). Sclerotia

and hyphae growing very close to vascular bundles were also

observed in Equisetum pratense Ehrh. roots (Hodson etal. 2009).

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-16 Root–Rhizosphere Interactions

TABLE 38.3 Endophytes in Other Herbaceous Plants

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acremonium alternatum Hypocreales Not DSE Brassica oleracea var.

gemmifera

Brassicales Herb In vitro exp a Raps and Vidal (1998),

Dugassa-Gobena etal.

(1998)

Acremonium strictum Hypocreales Not DSE Solanum lycopersicum Solanales Herb In vitro exp b Raps and Vidal (1996), Vidal

(1996)

Aureobasidium pullulans Dothideales Not DSE Pteridium aquilinum Pteridophyta Perennial fern Isol Petrini etal. (1992)

Cladophialophora chaetospira Chaetothyriales DSE Brassica campestris Brassicales Herb In vitro exp c Narisawa etal. (1998)

Cladosporium sp. Capnodiales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Cylindrocarpon sp. Hypocreales Not DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Discocistella grevillei Helotiales Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Fusarium oxysporum Hypocreales Not DSE Brassica oleracea var.

capitata

Brassicales Herb In vitro exp Davis (1967), Matta (1989)

Fusarium oxysporum Hypocreales Not DSE Citrullus vulgaris Cucurbitales Herb In vitro exp d Davis (1967), Matta (1989)

Fusarium oxysporum Hypocreales Not DSE Dianthus caryophyllus Caryophyllales Herb In vitro exp d Davis (1967), Matta (1989)

Fusarium oxysporum Hypocreales Not DSE Linum usitatissimum Malpighiales Herb In vitro exp d Davis (1967), Matta (1989)

Fusarium oxysporum Hypocreales Not DSE Lycopersicon esculentum Solanales Herb In vitro exp d Davis (1967), Matta (1989)

Hypocrea lixii Hypocreales Not DSE Musa acuminata Zingiberales Herb Isol Xia etal. (2011)

Ilyonectria radicicola Hypocreales Not DSE Pteridium aquilinum Pteridophyta Perennial fern Isol Petrini etal. (1992)

Leptodontidium orchidicola Helotiales DSE Colobanthus quitensis Caryophyllales Herb Isol Upson etal. (2009)

Leptodontidium orchidicola Helotiales DSE Pedicularis bracteosa Lamiales Herb Isol Currah etal. (1987)

Leptodontidium orchidicola Helotiales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Leptosphaeria sp. Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Meliniomyces variabilis LtVB3 Leotiomycetes DSE Brassica rapa Brassicales Herb In vitro exp e Ohtaka and Narisawa (2008)

Meliniomyces variabilis LtVB3 Leotiomycetes DSE Solanum lycopersicum Solanales Herb In vitro exp f Ohtaka and Narisawa (2008)

Microdochium bolleyi Xylariales DSE Lycopersicon esculentum Solanales Herb Isol and Micros g Rasmann etal. (2009)

Mortierella sp. Zygomycota Not DSE Pteridium aquilinum Pteridophyta Perennial fern Isol Petrini etal. (1992)

Mycocentrospora acerina Pleosporales DSE Saussurea involucrata Asterales Herb In vitro exp h Wu etal. (2010)

Mycocentrospora acerina Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Phaeosphaeria avenaria Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Phialophora cyclaminis Chaetothyriales DSE Cyclamen persicum Ericales Herb Isol Schol-Schwarz (1970)

Phoma chrysanthemicola Pleosporales DSE Chrysanthemum

morifolium

Asterales Herb Isol Aveskamp etal. (2009)

Phoma chrysanthemicola Pleosporales DSE Heteropappus

semiprostratus

Asterales Herb Isol de Graaf (unpublished)

Phoma chrysanthemicola Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Phoma glomerata Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Phoma sclerotioides Pleosporales DSE Saussurea involucrata Asterales Herb Isol Lv etal. (2010)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-17Fungal Root Endophytes

Piriformospora indica Sebacinales Not DSE Various spp. N.A. Various In vitro exp i Varma etal. (2001)

Tapesia sp. Helotiales DSE Colobanthus quitensis Caryophyllales Herb Isol Upson etal. (2009)

Trichoderma asperellum Hypocreales Not DSE Musa acuminata Zingiberales Herb Isol Xia etal. (2011)

Trichoderma virens Hypocreales Not DSE Musa acuminata Zingiberales Herb Isol Xia etal. (2011)

Trichoderma brevicompactum Hypocreales Not DSE Musa acuminata Zingiberales Herb Isol Xia etal. (2011)

Triscelophorus monosporus Pezizomycotina Not DSE Angiopteris evecta Pteridophyta Perennial fern Isol Raviraja etal. (1996)

Triscelophorus monosporus Pezizomycotina Not DSE Christela dentata Pteridophyta Small fern Isol Raviraja etal. (1996)

Unidentied DSE DSE Astragalus cf. arequipensis Fabales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Bartsia pumila Lamiales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Ceradenia spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Cochlidium serrulatum Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Elaphoglossum spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Equisetum bogotense Equisetales Herb Micros Fernandez etal. (2008)

Unidentied DSE DSE Galium odoratum Gentianales Herb Isol Postma etal. (2007)

Unidentied DSE DSE Gramitis paramicola Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Hydrilla verticillata Alismatales Herb Micros Kai and Zhao (2006)

Unidentied DSE DSE Hygrophila cf. costata Lamiales Herb Micros De Marins etal. (2009)

Unidentied DSE DSE Hymenophyllum spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Lellingeria spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Limnobium laevigatum Apiales Herb Micros De Marins etal. (2009)

Unidentied DSE DSE Lycopodium sp. Lycopodiales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Lycopodium paniculatum Lycopodiales Herb Micros Fernandez etal. (2008)

Unidentied DSE DSE Melpomene spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Mercurialis perennis Malpighiales Herb Isol Postma etal. (2006)

Unidentied DSE DSE Micropolypodium sp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Mnioides sp. Asterales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Myriophyllum brasiliense Saxifragales Herb Micros De Marins etal. (2009)

Unidentied DSE DSE Oenanthe decumbens Apiales Herb Micros Kai and Zhao (2006)

Unidentied DSE DSE Pedicularis spp. Lamiales Herb Isol Li and Guan (2007)

Unidentied DSE DSE Perezia coerulescens Asterales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Plantago asiatica Lamiales Herb Micros Li etal. (2005)

Unidentied DSE DSE Polygonum spp. Caryophyllales Herb Micros De Marins etal. (2009)

Unidentied DSE DSE Potamogeton tepperi Alismatales Herb Micros Kai and Zhao (2006)

Unidentied DSE DSE Rotala rotundifolia Myrtales Herb Micros Kai and Zhao (2006)

Unidentied DSE DSE Saxifraga aizoides Saxifragales Herb Isol j Ruotsalainen etal. (2004)

Unidentied DSE DSE Senecio sp. Asterales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Sibbaldia procumbens Rosales Herb Isol j Ruotsalainen etal. (2004)

Unidentied DSE DSE Solidago virgaurea Asterales Herb Isol j Ruotsalainen etal. (2004)

Unidentied DSE DSE Stellaria nemorum Caryophyllales Herb Isol Postma etal. (2006)

Unidentied DSE DSE Stylidium productum Asterales Herb Isol Chambers etal. (2008)

Unidentied DSE DSE Terpsichore spp. Polypodiales Herb Micros Lehnert etal. (2009)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-18 Root–Rhizosphere Interactions

TABLE 38.3 (continued) Endophytes in Other Herbaceous Plants

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Unidentied DSE DSE Trichomanes spp. Polypodiales Herb Micros Lehnert etal. (2009)

Unidentied DSE DSE Trientalis europaea Ericales Herb Isol j Ruotsalainen etal. (2004)

Unidentied DSE DSE Trifolium repens Fabales Herb Micros Li etal. (2005)

Unidentied DSE DSE Viola biora Malpighiales Herb Isol j Ruotsalainen etal. (2004)

Unidentied DSE DSE Werneria orbignyana Asterales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Werneria sp. Asterales Herb Isol Schmidt etal. (2008)

Unidentied DSE DSE Xenophyllum rosenii Asterales Herb Isol Schmidt etal. (2008)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

the anamorph (asexual reproductive stage) are produced, the name of the teleomorph is given. Names of anamorph(s) can be retrieved from the list of the teleomorph’s synonyms provided in the index.

e next lower taxon is given if the Fungus order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots; in vitro exp, fungus used in in-vitro experiment(s); Micros, detection by microscopy.

Special eect details: (a) Control of diamondback moth and cabbage aphid Brevicoryne brassicae. (b) Control of nematodes and greenhouse white y larvae. (c) Control of clubroot (Plasmodiophora

brassicae). (d) Induction of resistance. (e) Control of Verticillium longisporum. (f) Control of Fusarium wilt. (g) Increased colonization by Microdochium bolleyi like fungi in organically grown tomatoes. (h)

Stimulation of plant root development. (i) Plant growth stimulation. (j) No correlation with altitude.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-19Fungal Root Endophytes

2. Endophyte–Pathogen, Endophyte–Nematode,

and Endophyte–Insect Interactions

More than 70 formae speciales of Fusarium oxysporum are

pathogenic on dierent hosts (Armstrong and Armstrong

1981). In general, each form causes symptoms only on one or

a few related plant species, whereas they occur as nonpatho-

genic endophytes in other plant species. Absence of adverse

eects of F. oxysporum isolates in infection experiments is in

line with this observation (Davis 1967; Gessler and Kuc 1982;

Rodríguez-Gálvez and Mendgen 1995). Nonpathogenic iso-

lates of F. oxysporum were shown to be able to penetrate and

colonize the tissues of carnation and tomato plants without

symptom expression (Postma and Rattink 1991; Hallmann and

Sikora 1994). Fusarium wilt disease is inhibited in plants inoc-

ulated with formae speciales of F. oxysporum to which they are

not susceptible prior to inoculation with forms to which they

are susceptible. is phenomenon is called “cross-protection”

or “induced resistance” (Davis 1967; Matta 1989). Inoculation

of individual tomato, ax, carnation, cabbage, and watermelon

seedlings with any one of nine formae speciales of F. oxyspo-

rum markedly reduced susceptibility to forms that they are

susceptible to (Davis 1967). Similarly, resistance of cucumber

(Cucumis sativus L.) against F. oxysporum f. sp. cucumeri-

num J.H. Owen was induced by inoculation of formae spe-

ciales that are not pathogenic on cucumber (Gessler and Kuc

1982). Cross-protection can be based on an indirect mecha-

nism mediated by the plant or on direct interactions between

inducer and challenger (Matta 1989). Chitin synthase–de-

cient mutants of the tomato root pathogen F. oxysporum f. sp.

lycopersici (Sacc.) W.C. Snyder & H.N. Hansen elicited plant

defense response and protected the plants against wild-type

infections (Pareja-Jaime et al. 2010). Fusarium solani colo-

nized tomato roots endophytically and protected them against

(C)

(D)

(A)

50 μm

(B)

ICO

OCO

FIGURE 38.3 (A) Scanning electron micrographs of cross section of a Chinese cabbage root infected by Cladophialophora chaetospira. Abundant

fungal hyphae developing in EPs and within OCO (arrowheads, appressorium-like swollen structures; ICO, inner cortical cells; VC, vascular cyl-

inder). (From Yonezawa, M. etal., Mycoscience, 45, 367, 2004.) Scale bar = 5 μm. (B) Dark septate endophytic fungi in roots of Xenophyllum rosenii

at 5389 m. (From Schmidt, S.K. etal., Arct. Antarct. Alp. Res., 40, 576, 2008.) (C) Gaultheria poeppiggi EP of hair root lled with sclerotia of the

Phialocephala type. (From Urcelay, C., Mycorrhiza, 12, 89, 2002.) Scale bar = 10 μm. (D) Roots of Pinus strobus colonized by Phialocephala fortinii

s.l. (strain UAMH 10266). Longitudinal section of colonized root showing surface hyphae (arrowhead) and Hartig net (arrows) and intercellular

hyphae. (From Peterson, R.L. etal., Botany, 86, 445, 2008.) Scale bar = 50 μm.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-20 Root–Rhizosphere Interactions

the root pathogen F. oxysporum f. sp. radicis-lycopersici

Jarvis& Shoemaker (Kavroulakis etal. 2007). Vascular dis-

colorations were reduced compared to the controls when

wounded roots of tomato seedlings were treated with an

unidentied Acremonium species prior to inoculation with the

pathogen, F.oxysporum f.sp. lycopersici (Phillips etal. 1967).

Inoculations with nonpathogenic Fusarium forms can provide

protection not only against other forms of Fusarium but also

against other diseases. Metabolites of F. oxysporum can also

signicantly reduce growth of soilborne pathogens such as

Phytophthora cactorum (Lebert & Cohn) J. Schröt., Pythium

ultimum Trow, and anatephorus cucumeris (A.B. Frank)

Donk in vitro (Hallmann and Sikora 1996), and F. oxysporum

strain EF 119 was ecient against tomato late blight caused by

Phytophthora infestans (Mont.) de Bary and inhibited growth

of Pythium ultimum and Phytophthora capsici Leonian (Kim

et al. 2007). Inoculations of tomato plants with nonpatho-

genic F. oxysporum strains signicantly reduced coloniza-

tion by the plant parasitic root-knot nematode Meloidogyne

incognita Kofoid & White without adversely aecting plant

health (Hallmann and Sikora 1994; Dababat and Sikora 2007;

Dababat etal. 2008). Similarly, endophytic F. oxysporum can

control the burrowing nematode Radopholus similis Cobb,

which is one of the key pests of banana (Athman etal. 2006;

Mendoza and Sikora 2009; Paparu etal. 2009).

Biological control of diseases, nematode, or insect pests was

also reported for root endophytes other than Fusarium spp.

Root inoculations of tomato plants with the soilborne endo-

phyte Acremonium strictum signicantly reduced the fre-

quency of root-knots induced by the nematode Meloidogyne

hapla Chitwood (Raps and Vidal 1996). Altered plant growth

of endophyte-colonized roots and direct parasitism of A. stric-

tum on the nematode eggs were assumed to be responsible for

nematode control. Culture ltrates of endophytic fungi isolated

from roots of tomato and banana plants in Kenya and Uganda

caused a signicant reduction of the activity of several nema-

tode species (Schuster et al. 1995). Mortality of greenhouse

white ies (Trialeurodes vaporariorum Westwood [Homoptera])

on tomato plants inoculated with the endophyte A. strictum

was only increased if the plants suered from drought stress.

Interestingly, the insects were preferentially feeding on plants

with inoculated roots (Vidal 1996). Similarly, the insect also

preferred French beans (Phaseolus vulgaris L.) inoculated with

A. strictum to uninoculated ones (Moll and Vidal 1995). In

0.5 mm

(E)

(F)

(G)

FIGURE 38.3 (continued) (E) Ectomycorrhiza formed by Acephala macrosclerotiorum on Pinus sylvestris. e mantle appears verrucous due to

characteristic, melanized wartlike sclerotia (arrowheads). (From Münzenberger, B. etal., Mycorrhiza, 19, 481, 2009.) (F) Cells of the phlobaphene

cork of a Norway-spruce (Picea abies) ne root lled with multicellular sclerotia composed of bubble-shaped, thick-walled, melanized cells of

Phialocephala fortinii s.l. Scale bar = 10 μm. (Courtesy of O. Holdenrieder). (G) Section of root of axenically grown Salix glauca inoculated with

P. fortinii s.l. (CSP13, strain UAMH 8148). Transverse section of a lateral root with a patchy fungal mantle (arrows) associated with the epidermal

layer and Hartig net initials (arrowheads). (From Fernando, A.A. and Currah, R.S., Can. J. Bot., 74, 1071, 1996.) Scale bar = 10 μm.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-21Fungal Root Endophytes

addition, females laid more eggs on inoculated than on unin-

oculated plants, and performance of the larvae on endophyte-

infected plants was slightly better. e observed changes of

the sugar and amino acid composition of the phloem sap were

assumed responsible for the behavior of the insects.

Root inoculations of Brussels sprouts (Brassica oleracea var.

gemmifera DC.) with the soilborne endophyte Acremonium

alternatum Link had a signicant eect on the performance of

diamondback moth (Plutella xylostella L.) (Dugassa-Gobena

et al. 1998; Raps and Vidal 1998). Larvae fed with leaves of

endophyte-inoculated plants experienced a higher mortality or

showed delayed growth, development, and pupation compared

to controls. e observed changes of the phytosterol composi-

tion of the host plants infected by endophytes were suspected to

confer control of the insect, because these changes altered the

suitability of certain phytosterols to be enzymatically dealkyl-

ated to cholesterol in insects. is subsequently interfered with

the molting processes of the larvae (Dugassa-Gobena etal. 1998;

Raps and Vidal 1998).

Sixteen endophytic fungal isolates from roots of Chinese

cabbage (Brassica campestris L.) almost completely suppressed

clubroot, caused by the soilborne fungus Plasmodiophora bras-

sicae Woronin, in sterile soil (Narisawa etal. 1998). Two of these

isolates were also eective in nonsterile soil and could be identi-

ed as Cladophialophora chaetospira (DSE), a species commonly

found on rotting wood in Europe (Ellis 1976) and isolated from

roots of Picea abies (L.) Karst. (Crous etal. 2007). Similarly, DSE

isolate LtVB3 from barley roots was shown to colonize roots

of Chinese cabbage and tomato endophytically and suppress

Verticillium yellows of Chinese cabbage and Fusarium wilt of

tomato (Narisawa etal. 2004). LtVB3 could meanwhile be iden-

tied as Meliniomyces variabilis Hambl. & Sigler (Ohtaka and

Narisawa 2008). Several endophytes (Phaeosphaeria avenaria

(G.F. Weber) O.E. Erikss., Leptosphaeria sp., Phoma chrysanthe-

micola Hollós, Cladosporium sp., and Cylindrocarpon sp.) iso-

lated from the roots of the alpine plant Saussurea involucrata

(Kar. & Kir.) Sch. Bip. in the Tianshan Mountains in China pos-

sessed antimicrobial activity against human pathogenic fungi

and bacteria (Lv etal. 2010).

Piriformospora indica Sav. Verma, Aj. Varma, Rexer, G. Kost &

P. Franken (Sebacinales, Basidiomycota), a fungus isolated from

an AM spore collected from desert soil in India, is able to colo-

nize the roots of various plant species as an endophyte (Verma

et al. 1998; Figure 38.2C). Inoculation with the fungus and

application of fungal culture induced resistance of their hosts

against biotic and abiotic stress (Varma etal. 2001; Deshmukh

and Kogel 2007; Ser ing etal. 2007; Achatz etal. 2010). Due to

its ease of culture, this fungus serves as a model organism for

the study of benecial plant–microbe interactions and a new

tool for improving plant production systems. Colonization was

inter- and intracellular with coils and branches or round chla-

mydospore-like structures and no arbuscules. Neither shoot nor

stelar tissues were colonized. Recently, sebacinalean endophytes

were found to be universally present as symptomless endophytes

in many liverworts, bryophytes, pteridophytes, and herbaceous

angiosperms, for example, wheat, maize, and the model plant

Arabidopsis thaliana (Weiss etal. 2011).

3. Endophyte–Plant Interactions

Chinese cabbage seedlings from seed treated with the two

C. chaetospira strains isolated by Narisawa etal. (1998) appeared

healthy, and inoculation with one of the isolates promoted

plant growth. Similarly, Mycocentrospora acerina (R. Hartig)

Deighton, another DSE, promoted root development of

S. involucrata (Wu etal. 2010). Inoculation with Piriformospora

indica and application of fungal culture ltrate promoted plant

growth and seed yield (Varma etal. 2001; Deshmukh and Kogel

2007; Ser ing etal. 2007; Achatz etal. 2010).

Growth promotion and improved uptake of phosphorus were

observed also in cotton when the roots were colonized endo-

phytically by C. foecundissimum Sacc. & Marchal (Gasoni and

Stegman De Gurnkel 1997). Intercellular hyphae formed dense

layers on the distal (outer) side of the endodermis. e fungus

grew also intracellularly in root hairs.

4. Endophyte–Environment Interactions

Inoculation of DSE (Cadophora and Rhizoctonia species)

onto aseptically grown seedlings of the alpine sedges Carex

curvula All. and Carex firma Host. resulted in a significant

increase of dry matter production in C. firma but not in C.

curvula compared to uninoculated controls (Haselwandter

and Read 1982). The authors concluded that the function of

the relationship between Carex roots and their DSE may be

comparable to that found between plants and AM fungi. Like

AM, DSE provided improved phosphorus supply to the plant.

DSE may replace AM in stressed environments. This hypoth-

esis is supported by the findings of Currah and Van Dyk

(1986) who observed roots growing in alpine soils with little

organic matter to have DSE and those growing in habitats

with visibly more organic matter to have AM. Three alpine

species of the Fabaceae (Astragalus alpinus L., A. vexilliflexus

E. Sheld., Oxytropis jordalii A.E. Porsild), a family that is usu-

ally endomycorrhizal in other habitats, lacked AM but were

colonized by DSE (Currah and Van Dyk 1986), an observa-

tion similar to that made by Christie and Nicolson (1983)

for two grass species in the Antarctic region. Conversely,

O’Dell and Trappe (1992) detected AM in Astragalus cottonii

M.E. Jones, Lupinus latifolius Lindl. ex J. Agardh, L. lepidus

Douglas ex Lindl., and Oxytropis campestris (L.) DC. from

alpine habitats. The two Lupinus species and O. campestris

were also colonized by septate endophytes, whereas A. cot-

tonii was not. One of the DSE observed in the roots of L. lati-

folius was later on identified as Phialocephala fortinii (O’Dell

etal. 1993).

AM fungi were absent in Xenophyllum rosenii (R.E. Fr.)

V.A. Funk and Perezia coerulescens Wedd. (both Asteraceae),

but roots of both plant species were heavily colonized by DSE

fungi at 5391 m asl in the Peruvian Andes (Schmidt etal. 2008;

Figure 38.3B). At slightly lower elevations (5240–5250 m),

AM fungi were present while DSE fungi were rare except in

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-22 Root–Rhizosphere Interactions

Bartsia pumila Benth. (Scrophulariaceae) and plants outside

of the Asteraceae. In Colorado at 4300 m asl, AM fungi were

rare, but all examined plants were colonized by DSE fungi

(Schmidt etal. 2008). Absence of AM fungi and presence of

dark septate hyphae were also observed for roots of various

herbaceous plant species collected in Arctic Canada (Bledsoe

etal. 1990). DSE occurred also in several alpine plants in the

Canadian Rocky Mountains (Stoyke and Currah 1991). In

contrast, Kohn and Stasovski (1990) found no DSE in roots

collected in arctic Canada, but AM was observed in one plant

species. Ruotsalainen etal. (2004) could not nd any consis-

tent correlation between the colonization of various Arctic–

alpine plants by AM or DSE and altitude in Northern Norway.

DSE might not only replace AM at high altitudes and latitudes

but also in acidic soils as suggested by Postma etal. (2007)

who found that colonization of herbaceous plants (Galium

odoratum (L.) Scop., Mercurialis perennis L., Stellaria nemo-

rum L.) by DSE increased with decreasing pH whereas colo-

nization by AM decreased. e same authors also detected a

positive correlation between leaf magnesium concentrations

and the presence of DSE in G. odoratum. DSE are probably the

most widespread root–fungus association in polar regions,

but their roles in plant nutrition and survival are still poorly

understood (Newsham etal. 2009). Li etal. (2005) detected

considerable colonization of roots of Trifolium repens L. and

Plantago asiatica L. by DSE. Colonization by DSE correlated

with relative humidity and sunlight hours but not with AM

colonization, temperature, rainfall, nitrogen, phosphorus

potassium, or organic matter content in the soil.

V. Root Endophytes of Woody

Plant Species

Many shrub and trees species belonging to various plant families

were examined for the presence of root endophytes (Tables 38.4

through 38.6). Members of the Cupressaceae (Lihnell 1939; Hennon

et al. 1990), Ericaceae (including Epacridaceae) (Oberholzer-

Tschütscher 1982; Widler and Müller 1984; Hutton etal. 1994;

Ahlich and Sieber 1996; Steinke etal. 1996; Hambleton and Currah

1997; Vodnik etal. 1997; Verkley etal. 2003; Ruotsalainen etal.

2004;Hambleton and Sigler 2005; Sigler etal. 2005; Grünig etal.

2009; Newsham etal. 2009; Bagyalakshmi etal. 2010; Kjoller etal.

2010; Tian etal. 2011), and Pinaceae (Bloomberg 1966; Parkinson

and Crouch 1969; Galaaen and Venn 1979; Kowalski 1982a,b;

Courtois and Ruschen 1987; Summerbell 1989; Courtois 1990b;

Danielson and Visser 1990; Kattner and Schönhar 1990; Fisher

etal. 1991a; Manka and Mroczkiewicz 1991; Heslin etal. 1992;

Holdenrieder and Sieber 1992; Kattner 1992a; Ahlich and Sieber

1996; Horton etal. 1998; Grönberg etal. 2006; Kaparakis and Sen

2006; Menkis etal. 2006; Brenn etal. 2008; Grünig etal. 2008b,

2009; Bachmann 2010; Kandalepas et al. 2010; Rivera-Orduna

etal. 2011; Wagg etal. 2011) are among the most intensively stud-

ied plant species. Some broadleaf tree and shrub species have been

examined as well (Currah and Van Dyk 1986; Domanski and

Kowalski 1987; Summerbell 1989; Sridhar and Bärlocher 1992;

Cother and Gilbert 1994; Fisher etal. 1995a, 1995b; Iqbal etal.

1995; Ahlich and Sieber 1996; Raviraja etal. 1996; Werner etal.

1997; Barrow etal. 2004; Beauchamp etal. 2005; Newsham etal.

2009; Bagyalakshmi etal. 2010; Kandalepas etal. 2010).

Since presence and function of fungal root endophytes have

most intensively been studied for members of the Ericales and

Pinales, Sections V.A and V.B will be dedicated to these two

groups of hosts.

A. Root Endophytes of Woody Ericales

Non-mycorrhizal endophytes are oen isolated from

ericaceous hosts in addition to the classical mycorrhi-

zal fungi Pezoloma (Hymenoscyphus) ericae (D.J. Read)

Baral (anamorph: Scytalidium vaccinii Dalpé, Litten

& Sigler) and Oidiodendron spp. Species of the genera

Acephala, Cryptosporiopsis, Cylindrocarpon, Meliniomyces,

Phialocephala, and Trichocladium are most oen observed

(Oberholzer-Tschütscher 1982; Widler and Müller 1984;

Väre etal. 1992; Hambleton and Currah 1997; Vodnik etal.

1997; Verkley etal. 2003; Hambleton and Sigler 2005; Sigler

et al. 2005; Grünig et al. 2006; Grünig et al. 2008b, 2009,

2011; Queloz et al. 2010; Table 38.4). Phialocephala forti-

nii s.l. were present in 17 of 19 ericaceous hosts from boreal

and alpine sites in Alberta, Canada (Hambleton and Currah

1997), in Gaultheria shallon Pursh from coastal British

Columbia, Canada, and in Calluna vulgaris (L.) Hull as well

as Vaccinium myrtillus L. from a subalpine site in Switzerland

(Ahlich and Sieber 1996; Grünig etal. 2006). A fungus iso-

lated by Vodnik etal. (1997) from the roots of Erica carnea

L. from Slovenia and deposited as Phialocephala fortinii at

UAMH as strain number 8433 could meanwhile be identi-

ed as Phialocephala subalpina Grünig & T.N. Sieber (Grünig

et al. 2008b). A hitherto unknown species of Phialocephala

was isolated from Vaccinium vitis-idaea, V. myrtillus and

V. uliginosum growing on permafrost soil in the Jura moun-

tains of Switzerland and described as Phialocephala glacialis

Grünig & T.N. Sieber (Grünig etal. 2009). Interestingly, the

same species was also detected in healthy needles of Norway-

spruce trees nearby. Allseven described species of P. fortinii

s.l. and A. applanata could be detected in roots of V. myrtillus

and other Vacciniumspecies in many countries in Europe and

some of them also in North America (Queloz 2010; Table 38.4).

Unidentied DSE were also isolated from Symplocos cochinchi-

nensis (Lour.) S. Moore and several other plant species from

shola vegetation in the Western Ghats region, southern India

(Bagyalakshmi etal. 2010).

Cryptosporiopsis species (anamorphic Pezicula species) are

regularly isolated from rhizomes and ne roots of ericaceous

plants. Cryptosporiopsis ericae Sigler from roots of Vaccinium

membranaceum Douglas ex Torr., V. ovalifolium Sm. and G.

shallon Pursh, and C. brunnea Sigler from G. shallon from

northwestern North America were described as new species

(Sigler etal. 2005), and a Cryptosporiopsis species was isolated

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-23Fungal Root Endophytes

TABLE 38.4 Endophytes in Ericoid Plants (Family Ericaceae)

Endophyte Host

Type of

Experiment

Special Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acephala applanata Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Acephala sp. 1 Helotiales DSE Cassiope

mertensiana

Ericales Woody shrub Isol Grünig etal. (2009)

Acephala sp. 3 Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Grünig etal. (2009)

Acephala sp. 7 Helotiales DSE Calluna vulgaris Ericales Woody shrub Isol Pietrowski (unpublished)

Cryptocline dubia Helotiales Not DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Cryptosporiopsis sp. Helotiales DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Cryptosporiopsis sp. Helotiales DSE Erica carnea Ericales Woody shrub Isol Oberholzer-Tschütscher (1982)

Cryptosporiopsis brunnea Helotiales DSE Gaultheria shallon Ericales Woody shrub Isol Sigler etal. (2005)

Cryptosporiopsis ericae Helotiales Variable Vaccinium

membranaceum

Ericales Woody shrub Isol Sigler etal. (2005)

Cryptosporiopsis rhizophila Helotiales DSE Erica tetralix Ericales Woody shrub Isol Verkley etal. (2003)

Cylindrocarpon didymum Hypocreales Not DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Cylindrocarpon didymum Hypocreales Not DSE Erica carnea Ericales Woody shrub Isol Oberholzer-Tschütscher (1982)

Cystodendron dryophilum Helotiales Not DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Gliocladium solani f. nigrovirens Hypocreales Variable Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Herpotrichia sp. Pleosporales DSE Vaccinium sp. Ericales Woody shrub Isol Müller (unpublished)

Ilyonectria radicicola Hypocreales Not DSE Erica carnea Ericales Woody shrub Isol Vodnik etal. (1997)

Marasmius scorodonius Agaricales Not DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Meliniomyces sp. 3 Leotiomycetes Variable Gaultheria shallon Ericales Woody shrub Isol Hambleton and Sigler (2005)

Meliniomyces sp. 3 Leotiomycetes Variable Vaccinium

myrtillus

Ericales Woody shrub Isol Hambleton and Sigler (2005)

Meliniomyces variabilis Leotiomycetes DSE Andromeda

polifolia

Ericales Woody shrub Isol Kjoller etal. (2010)

Meliniomyces variabilis Leotiomycetes DSE Empetrum

hermaphroditum

Ericales Woody shrub Isol Kjoller etal. (2010)

Meliniomyces variabilis Leotiomycetes DSE Rhododendron

albiorum

Ericales Woody shrub Isol Hambleton and Sigler (2005)

Meliniomyces variabilis Leotiomycetes DSE Vaccinium

uliginosum

Ericales Woody shrub Isol Kjoller etal. (2010)

Meliniomyces variabilis Leotiomycetes DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Kjoller etal. (2010)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-24 Root–Rhizosphere Interactions

TABLE 38.4 (continued) Endophytes in Ericoid Plants (Family Ericaceae)

Endophyte Host

Type of

Experiment

Special Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Microdochium bolleyi Xylariales DSE Polemonium

boreale

Ericales Herb Isol Väre etal. (1992)

Monodictys putredinis Dothideomycetes Not DSE Erica carnea Ericales Woody shrub Isol Oberholzer-Tschütscher (1982)

Oidiodendron griseum Dothideomycetes DSE Loiseleuria

procumbens

Ericales Woody shrub Isol Stoyke and Currah (1991),

Hambleton and Currah

(1997)

Oidiodendron griseum Dothideomycetes DSE Phyllodoce

glanduliora

Ericales Woody shrub Isol Stoyke and Currah (1991),

Hambleton and Currah

(1997)

Oidiodendron griseum Dothideomycetes DSE Vaccinium

myrtilloides

Ericales Woody shrub Isol Stoyke and Currah (1991),

Hambleton and Currah

(1997)

Oidiodendron griseum Dothideomycetes DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Stoyke and Currah (1991),

Hambleton and Currah

(1997)

Oidiodendron maius Dothideomycetes DSE Various spp. Ericales Woody shrub Isol Hambleton and Currah (1997)

Pezoloma ericae Leotiomycetes DSE Calluna vulgaris Ericales Woody shrub Isol Read (1974)

Pezoloma ericae Leotiomycetes DSE Ledum

groenladicum

Ericales Woody shrub Isol Hambleton etal. (1999)

Phialocephala fortinii s.l. Helotiales DSE Polemonium

boreale

Ericales Herb Isol Väre etal. (1992)

Phialocephala fortinii s.l. Helotiales DSE Various spp. Ericales N.A. Isol Hambleton and Currah (1997)

Phialocephala europaea Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Vaccinium

uliginosum

Ericales Woody shrub Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Cassiope

mertensiana

Ericales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Kalmia

microphylla

Ericales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Luteka pectinata Ericales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Grünig etal. (2008a)

Phialocephala fortinii s.s. Helotiales DSE Vaccinium

uliginosum

Ericales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Queloz (2010)

Phialocephala glacialis Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Grünig etal. (2009)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-25Fungal Root Endophytes

Phialocephala helvetica Helotiales DSE Erica carnea Ericales Woody shrub Isol Queloz (2010)

Phialocephala helvetica Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Empetrum

hermaphroditum

Ericales Woody shrub Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Erica carnea Ericales Woody shrub Isol Vodnik etal. (1997)

Phialocephala subalpina Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Grünig etal. (2008a)

Phialocephala subalpina Helotiales DSE Vaccinium

uliginosum

Ericales Woody shrub Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Vaccinium

vitis-idaea

Ericales Woody shrub Isol Queloz (2010)

Phialocephala turicensis Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Phialocephala uotilensis Helotiales DSE Vaccinium

myrtillus

Ericales Woody shrub Isol Queloz (2010)

Phialophora bubakii Chaetothyriales Not DSE Erica carnea Ericales Woody shrub Isol Oberholzer-Tschütscher (1982)

Rhizoctonia sp. Cantharellales DSE Erica carnea Ericales Woody shrub Isol Vodnik etal. (1997)

Trichocladium opacum Sordariales DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Trichocladium opacum Sordariales Not DSE Erica carnea Ericales Woody shrub Isol Oberholzer-Tschütscher (1982)

Varicosporium sp. Helotiales DSE Arctostaphylos

uva-ursi

Ericales Woody shrub Isol Widler and Müller (1984)

Unidentied DSE DSE Empetrum

hermaphroditum

Ericales Woody shrub Isol a Ruotsalainen etal. (2010)

Unidentied DSE DSE Symplocos

cochinchinensis

Ericales Tree Isol Bagyalakshmi etal. (2010)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

the anamorph (asexual reproductive stage) are produced, the name of the teleomorph is given. Names of anamorph(s) can be retrieved from the list of the teleomorph’s synonyms provided in the index.

e next lower taxon is given if the Fungus order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots.

Special eect details: (a) Colonization frequency positively correlated with light intensity.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-26 Root–Rhizosphere Interactions

from C. vulgaris, Erica tetralix L., V. vitis-idaea, and V. myrtil-

lus in the Netherlands and described as C. rhizophila Verkley &

Zijlstra (Verkley etal. 2003).

Meliniomyces species seem to be widespread endophytes in

roots of Andromeda polifolia L., Empetrum hermaphroditum

Hagerup, Phyllodoce empetriformis (Sm.) D. Don, Rhododendron

albiorum Hook., V. membranaceum, V. uliginosum L., and

V. vitis-idaea in alpine heathlands and subarctic mires (Hambleton

and Sigler 2005; Kjoller etal. 2010).

Dark-colored, sterile, and slow-growing mycelia were also

isolated in Australia from Epacridaceae, a family close to the

Ericaceae but distributed in the Southern Hemisphere (Hutton

et al. 1994). Pectic zymogram analysis revealed that none of

the Australian isolates matched fungi known to be infective

with Ericaceae in the Northern Boreal and Alpine Zone, for

example, Pezoloma ericae and Oidiodendron spp., even though

all isolates appeared morphologically similar and had simi-

lar growth rates. Two-thirds of the endophytes isolated from

Leucopogon parviorus (H. Andrews) Lindl., another represen-

tative of Epacridaceae, were sterile and had slow growth rates.

Some of them were dark and similar to P. ericae. Inspection of

roots under the light microscope revealed that there were at least

two dierent fungi that consistently formed ericoid mycorrhizal

structures at these sites, possibly P. ericae and Oidiodendron sp.

(Steinke etal. 1996).

1. Anatomy

Dark septate inter- and intracellular hyphae and microsclerotia

were observed in epidermal cells (EPs) of ericaceous “hair roots”

of Gaultheria poeppiggi DC. collected in the Cordoba mountains

of central Argentina (Urcelay 2002; Figure 38.3C). Similarly, DSE

were present in hair roots of Woollsia pungens (Cav.) F. Muell.

in New South Wales (Chambers etal. 2008). Phialocephala for-

tinii s.s. occurred as extensive wes of dark, septate hyphae on

the root surface and as intracortical sclerotia of compact, darkly

pigmented and irregularly lobed, thick-walled hyphae in axenic

seedlings of Menziesia ferruginea Sm. (Ericaceae) (Stoyke and

Currah 1991, 1993). Intracellular coils and colonization of the

vascular tissues were not observed. is association diers from

the ericoid mycorrhizal type, in which elaborate intracellular

hyphal branches are ensheathed by invaginations of the host

plasma membrane but represents a fungus–root association

that seems to be common in alpine plants. Similarly, the pattern

of root colonization of Rhododendron brachycarpum D.Don by

Phialocephala fortinii s.l. diered from that observed in ericoid

mycorrhizae (Currah etal. 1993). Phialocephala fortinii s.l. colo-

nized the EPs, in which it sometimes formed black sclerotia, but

was not able to colonize the thick-walled, phenol-rich exoder-

mal layer of hair roots. Intercellular colonization between epi-

dermis and exodermis layers was, however, common.

2. Endophyte–Plant Interactions

Presence of Phialocephala fortinii s.s. in axenic cultures of

M. ferruginea (Ericaceae) caused a 10-fold increase of seed-

ling mortality compared to mortality of control plants (Stoyke

and Currah 1993). Established plants and growth rates were,

however, not aected. Phialocephala fortinii-like DSE strains

were shown to dier in virulence against R. brachycarpum.

In resynthesis experiment, one strain had a signicant nega-

tive eect on dry weight accumulation of seedlings, but

plants looked healthy, whereas a second one had no eect

(Currah etal. 1993).

3. Endophyte–Environment Interactions

Phialocephala fortinii s.l. was only rarely detected in erica-

ceous roots from an acidic wetland but occurred quite fre-

quently in roots from an alpine site in Alberta (Hambleton

and Currah 1997). Phialocephala subalpina and a Rhizoctonia

sp. were shown to be sensitive to heavy metals and mainly

occurred in roots of E. carnea growing in non-polluted soil,

whereas Cladosporium herbarum (Pers.) Link and Ilyonectria

radicicola were the fungi most frequently isolated from

plant roots originating from lead contaminated soil (Vodnik

etal. 1997). Stress levels along three abiotic gradients (pol-

lution, elevation, distance from seashore) on Kola Peninsula

in Russia had no effect on root colonization of crowberry

(E. hermaphroditum) by DSE, but distance to mountain birch

(Betula pubescens ssp. czerepanovii (Orlova) Hämet-Ahti)

had an effect; colonization was higher outside the canopy

area (Ruotsalainen etal. 2010). Substitution of AM fungi at

higher altitude could not be observed for Trientalis europaea

L. and several other alpine plants collected along a gradient

from 0 to 1400 m at Mt. Paras, North Norway (Ruotsalainen

etal. 2004).

B. Root Endophytes of Pinales

Endophyte species diversity strongly depends on the degree of

surface sterilization and the sample size; the weaker the ster-

ilization and the more samples, the more species are detected.

For example, Holdenrieder and Sieber (1992) could detect 120

taxa in >500 serially washed Norway-spruce root segments.

However, if surface sterilization is applied, diversity of fun-

gal communities steeply decreases. Moreover, the diversity of

endophyte communities in roots is also much lower than that

of endophyte communities in aboveground plant parts (Sieber

1988, 1989, 2007; Sridhar and Bärlocher 1992; Kowalski 1993;

Sieber-Canavesi and Sieber 1993; Ahlich and Sieber 1996;

Menkis 2004; Rivera-Orduna etal. 2011). Only ve species of

endophytes (Alternaria sp., Cochliobolus sp., Penicillium sp.,

Phoma medicaginis, and a species of the Xylariaceae) could

be isolated from roots of Taxus globosa Schltdl. in Mexico,

whereas bark contained at least 17 dierent species (Rivera-

Orduna etal. 2011). More than 90% of the isolates collected

from root tips of Picea abies and Pinus sylvestris L. belonged

to the genus Phialocephala (Menkis 2004; Table 38.5). Non-

mycorrhizal ne roots of healthy Abies alba Mill., Picea abies,

and Pinus sylvestris in Europe are heavily colonized by endo-

phytic fungi. Depending on the site, between 88% and 100%

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-27Fungal Root Endophytes

TABLE 38.5 Endophytes in Conifers

Endophyte Host

Type of

Experiment

Special Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acephala applanata Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Acephala applanata Helotiales DSE Picea abies Pinales Tree Isol Grünig and Sieber (2005)

Acephala applanata Helotiales DSE Pinus mugo Pinales Tree Isol Queloz (2010)

Acephala applanata Helotiales DSE Pinus sylvestris Pinales Tree Isol Queloz (2010)

Acephala macrosclerotiorum Helotiales DSE Picea abies Pinales Tree Isol Menkis etal. (2004)

Acephala macrosclerotiorum Helotiales DSE Pinus sylvestris Pinales Tree Isol Münzenberger etal. (2009)

Acephala sp. 2 Helotiales DSE Pinus sylvestris Pinales Tree Isol Grünig etal. (2009)

Acephala sp. 4 Helotiales DSE Pinus banksiana Pinales Tree Isol Grünig etal. (2009)

Alternaria sp. Pleosporales DSE Taxus globosa Pinales Tree Isol Rivera-Orduna etal. (2011)

Anguillospora liformis Pleosporales Not DSE Picea glauca Pinales Tree Isol Sridhar and Bärlocher (1992)

Aspergillus versicolor Eurotiales Not DSE Picea abies Pinales Tree Isol Courtois (1990a,b)

Cadophora nlandica Helotiales DSE Picea abies Pinales Tree Isol Menkis (unpublished)

Cadophora nlandica Helotiales DSE Pinus resinosa Pinales Tree in vitro exp a Alberton etal. (2010)

Cadophora nlandica Helotiales DSE Pinus sylvestris Pinales Tree Isol Wang and Wilcox (1985)

Cadophora malorum Helotiales DSE Picea abies Pinales Tree Isol Sieber (unpublished)

Cadophora sp. 1 Helotiales DSE Picea abies Pinales Tree Isol Queloz (2010)

Cadophora sp. 2 Helotiales DSE Abies alba Pinales Tree Isol Ahlich and Sieber (1996)

Cadophora sp. 2 Helotiales DSE Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Chloridium paucisporum Chaetosphaeriales DSE Pinus resinosa Pinales Tree In vitro exp a Alberton etal. (2010)

Cladophialophora chaetospira Chaetothyriales DSE Picea abies Pinales Tree Isol Crous etal. (2007)

Cochliobolus sp. Pleosporales DSE Taxus globosa Pinales Tree Isol Rivera-Orduna etal. (2011)

Coniothyrium sp. Pleosporales Not DSE Pinus sylvestris Pinales Tree Isol Görke (1998)

Cryptosporiopsis abietina Helotiales Not DSE Picea abies Pinales Tree Isol Kattner and Schönhar (1990)

Cryptosporiopsis radicicola Helotiales DSE Abies alba Pinales Tree Isol Ahlich and Sieber (1996)

Cryptosporiopsis radicicola Helotiales DSE Pinus sylvestris Pinales Tree Isol Ahlich and Sieber (1996)

Cryptosporiopsis sp. Helotiales DSE Chamaecyparis

nootkatensis

Pinales Tree Isol Hennon etal. (1990)

Cryptosporiopsis cf melanigena Helotiales DSE Picea abies Pinales Tree Isol Queloz (2010)

Cryptosporiopsis ericae Helotiales Variable Picea abies Pinales Tree Isol Sigler etal. (2005)

Cylindrocarpon aquaticum Hypocreales Not DSE Picea glauca Pinales Tree Isol Sridhar and Bärlocher (1992)

Cylindrocarpon didymum Hypocreales Not DSE Chamaecyparis

nootkatensis

Pinales Tree Isol Hennon etal. (1990)

Cylindrocarpon didymum Hypocreales Not DSE Pinus sylvestris Pinales Tree Isol Ahlich and Sieber (1996)

Cylindrocarpon obtusisporum Hypocreales Variable Picea abies Pinales Tree Isol Queloz (2010)

Didymella bryoniae Pleosporales DSE Picea abies Pinales Tree Isol Queloz (2010)

Didymosphaeria sp. Pleosporales DSE Picea abies Pinales Tree Isol Brenn etal. (2008)

Gelatinosporium sp. Helotiales Not DSE Chamaecyparis

nootkatensis

Pinales Tree Isol Hennon etal. (1990)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-28 Root–Rhizosphere Interactions

TABLE 38.5 (continued) Endophytes in Conifers

Endophyte Host

Type of

Experiment

Special Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Herpotrichia sp. Pleosporales DSE Picea abies Pinales Tree Isol Grünig (unpublished)

Humicolopsis cephalosporioides Pezizomycotina DSE Picea abies Pinales Tree Isol Courtois (1990a,b)

Ilyonectria radicicola Hypocreales Not DSE Picea abies Pinales Tree Isol Görke (1998)

Ilyonectria radicicola Hypocreales Variable Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Leptosphaeria sp. 1 Pleosporales DSE Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Macrophomina phaseolina Botryosphaeriales DSE Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Meliniomyces sp. 2 Leotiomycetes Variable Pinus sylvestris Pinales Tree Isol Hambleton and Sigler (2005)

Meliniomyces sp. 4 Leotiomycetes Variable Pinus sylvestris Pinales Tree Isol Hambleton and Sigler (2005)

Meliniomyces variabilis Leotiomycetes DSE Pinus resinosa Pinales Tree In vitro exp a Alberton etal. (2010)

Meliniomyces variabilis Leotiomycetes DSE Tsuga heterophylla Pinales Tree Isol Hambleton and Sigler (2005)

Meliniomyces vraolstadiae Leotiomycetes DSE Pinus resinosa Pinales Tree In vitro exp a Alberton etal. (2010)

Paecilomyces sp. Eurotiales Not DSE Pinus radiata Pinales Tree Isol Sieber and Langenegger

(unpublished)

Penicillium nigricans Eurotiales DSE Picea abies Pinales Tree Isol Courtois (1990a,b)

Phialocephala europaea Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Larix kaempferi Pinales Tree Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Phialocephala europaea Helotiales DSE Picea glauca Pinales Tree Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Pinus sylvestris Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.l. Helotiales DSE Abies alba Pinales Tree Isol Ahlich and Sieber (1996)

Phialocephala fortinii s.l. Helotiales DSE Picea abies Pinales Tree Isol Ahlich and Sieber (1996)

Phialocephala fortinii s.l. Helotiales DSE Pinus resinosa Pinales Tree In vitro exp a Alberton etal. (2010)

Phialocephala fortinii s.l. Helotiales DSE Larix decidua Pinales Tree Isol Grünig etal. (2008a)

Phialocephala fortinii s.s. Helotiales DSE Pinus sylvestris Pinales Tree Isol Ahlich and Sieber (1996)

Phialocephala fortinii s.s. Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Larix decidua Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Phialocephala fortinii s.s. Helotiales DSE Picea glauca Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Picea mariana Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Pinus cembra Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Pinus mugo Pinales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Pinus sylvestris Pinales Tree Isol Grünig etal. (2008a)

Phialocephala helvetica Helotiales DSE Juniperus sp. Pinales Tree Isol Queloz (2010)

Phialocephala helvetica Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Phialocephala helvetica Helotiales DSE Pinus leucodermis Pinales Tree Isol Queloz (2010)

Phialocephala helvetica Helotiales DSE Pinus sylvestris Pinales Tree Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-29Fungal Root Endophytes

Phialocephala sphaeroides Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2009)

Phialocephala subalpina Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Abies spectabilis Pinales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Phialocephala subalpina Helotiales DSE Picea glauca Pinales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Pinus mugo Pinales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Pinus strobus Pinales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Pinus sylvestris Pinales Tree Isol Grünig etal. (2008a)

Phialocephala subalpina Helotiales DSE Tsuga dumosa Pinales Tree Isol Queloz (2010)

Phialocephala turicensis Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala turicensis Helotiales DSE Picea abies Pinales Tree Isol Queloz (2010)

Phialocephala turicensis Helotiales DSE Taxus baccata Pinales Tree Isol Queloz (2010)

Phialocephala uotilensis Helotiales DSE Abies alba Pinales Tree Isol Queloz (2010)

Phialocephala uotilensis Helotiales DSE Picea abies Pinales Tree Isol Grünig etal. (2008a)

Phialophora melinii Helotiales Not DSE Chamaecyparis

nootkatensis

Pinales Tree Isol Hennon etal. (1990)

Phoma sp. 1 Pleosporales DSE Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Phoma exigua Pleosporales DSE Picea abies Pinales Tree Isol Queloz (2010)

Phoma medicaginis Pleosporales DSE Taxus globosa Pinales Tree Isol Rivera-Orduna etal. (2011)

Phoma radicina Pleosporales DSE Pinus sylvestris Pinales Tree Isol Bachmann (2010)

Phomopsis sp. Diaporthales Not DSE Pinus radiata Pinales Tree Isol Sieber and Langenegger

(unpublished)

Rhizoctonia sp. Cantharellales Not DSE Pinus sylvestris Pinales Tree in vitro exp b Grönberg etal. (2006)

Sphaeropsis sapinea Pezizomycotina DSE Pinus radiata Pinales Tree Isol Sieber and Langenegger

(unpublished)

Sporidesmium sp. Pleosporales Not DSE Chamaecyparis

nootkatensis

Pinales Tree Isol Hennon etal. (1990)

Sydowia polyspora Dothideales DSE Pinus sylvestris Pinales Tree Isol Görke (1998)

Trichoderma hamatum Hypocreales Not DSE Picea abies Pinales Tree Isol Kattner and Schönhar (1990)

Trichoderma polysporum Hypocreales Not DSE Picea abies Pinales Tree Isol Kattner and Schönhar (1990)

Trichoderma viride Hypocreales Not DSE Picea abies Pinales Tree Isol Kattner and Schönhar (1990)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

the anamorph (asexual reproductive stage) are produced, the name of the teleomorph is given. Names of anamorph(s) can be retrieved from the list of the teleomorph’s synonyms provided in the index.

e next lower taxon is given if the Fungus order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots; in vitro exp, fungus used in in-vitro experiment(s).

Special eect details: (a) Plant growth stimulation at elevated CO

. (b) Stimulation of early root development.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-30 Root–Rhizosphere Interactions

of the trees examined in Finland, Germany, and Switzerland

had roots colonized by endophytes, and DSE were most abun-

dant (Ahlich and Sieber 1996; Görke 1998). ey were present

in between 53% and 90% of the trees, and the majority of the

isolates belonged to PAC. Up to 70% of the ne roots of a single

root system of Norway spruce (Picea abies) can be colonized by

DSE (Holdenrieder and Sieber 1992). Taxodium distichum (L.)

Rich. seems to be an exception regarding dominance of DSE,

because DSE were very rare in roots of this tree species and

occurred in only 0.33% of the root samples (Kandalepas etal.

2010). Whereas DSE, especially PAC, dominate the endophyte

communities, species of Cryptosporiopsis and Cylindrocarpon

occur sometimes also quite frequently in conifer roots

(Courtois 1990a; Kattner and Schönhar 1990; Holdenrieder

and Sieber 1992; Ahlich and Sieber 1996; Table38.5). A special

community was observed in submersed roots of Picea glauca

(Moench) Voss (Sridhar and Bärlocher 1992). e commu-

nity was dominated by aquatic hyphomycetes, for example,

Anguillospora liformis Greath. and Heliscus lugdunensis Sacc.

& erry (Table 38.5).

Non-mycorrhizal endophytes are oen associated with ecto-

mycorrhizae of conifers. DSE, Umbelopsis isabellina (Oudem.)

W. Gams, Penicillium spinulosum om, and Penicillium mon-

tanense M. Chr. & Backus were most frequently associated with

ectomycorrhizae of Picea mariana (Mill.) Britton, Sterns &

Poggenb. (Summerbell 1989). Oidiodendron sp. considered non-

mycorrhizal on conifers, and DSE were most frequently isolated

from ectomycorrhizae of Sitka spruce (Picea sitchensis (Bong.)

Carrière) in Irish forest mixed stands (Schild etal. 1988; Heslin

etal. 1992). Oidiodendron sp. and DSE appeared to be antag-

onistic. DSE were only abundant when Oidiodendron sp. was

rare and vice versa. Douglas-r seedlings preinoculated with

the ectomycorrhizal fungus Rhizopogon vinicolor A.H. Sm. and

outplanted on eastern Vancouver Island were to some extend

colonized by DSE aer one growing season (Berch and Roth

1993). DSE were shown to survive forest res as resident inocu-

lum and to colonize Pinus muricata D. Don seedlings right aer

germination (Horton etal. 1998). Eighteen percent of the seed-

lings sampled until 5 months aer germination were colonized

by AM fungi, ectomycorrhizal fungi, and DSE simultaneously.

Except for members of the Epacridaceae, root endophytes of

woody plant species have not been examined intensively in the

Southern Hemisphere. is is especially true for conifers. Root

samples of Pinus radiata D. Don collected at four sites in Western

Australia revealed Sphaeropsis sapinea (Fr.) Dyko & B. Sutton,

a fungus usually conned to pine needles in the Northern

Hemisphere, to be the main colonizer at two of the four sites

(Sieber and Langenegger, unpublished). A Paecilomyces sp. and

a Phomopsis sp. dominated at each one of the other two sites.

DSE are prevalent in roots of conifer seedlings in nurser-

ies and naturally regenerating seedlings in the forest. Primary

roots of 1-year-old nursery-grown Douglas-r (Pseudotsuga

menziesii (Mirb.) Franco) seedlings were most frequently

colonized by DSE, Fusarium spp., and Cylindrocarpon spp.

(Bloomberg 1966). Similarly, DSE were among the earliest and

most abundant root colonizers of nursery-grown seedlings of

Pinus banksiana Lamb., Pinus contorta Douglas ex Loudon, and

Picea glauca (Moench) Voss (Danielson and Visser 1990). e

frequency of root segments of nursery seedlings of Picea abies

and Pinus sylvestris L. colonized by endophytic fungi in general

varied between 0.5% and 10% and that by PAC between 0% and

4%, that is, colonization density was signicantly lower than

expected from densities observed in spruce forests (Brenn etal.

2008). Interestingly, PAC could only be detected in plants from

nurseries situated directly in forests or very close to forests but

not in plants from nurseries on agricultural plots, because PAC

are very rare in arable soils (Ahlich-Schlegel 1997). Endophytic

fungi were isolated from 1- to 5-year-old seedlings of Pinus

nigra var. laricio Maire sampled in an area of natural tree regen-

eration (Parkinson and Crouch 1969). DSE were most frequently

isolated from roots of 5-year-old seedlings and Penicillium spp.

dominated in roots of younger plants. e frequency of coloni-

zation by DSE varied between 30% and 100% among plant indi-

viduals. DSE did not show any preference for specic parts in

the root system. Penicillium spp. were, however, most frequently

isolated from the upper tap and upper lateral roots, whereas

Ilyonectria radicicola showed a preference for the lower vertical

roots.

1. Anatomy

Structural features of the endophyte–root symbioses of conifers

are best studied for symbioses with PAC fungi. In contrast to

mycorrhizal fungi, PAC are not conned to the root tips but can

occur everywhere in the root system from root tips to the bark

of coarse roots at the stem base. First- and second-order laterals

of primary roots of Pinus contorta colonized by Phialocephala

fortinii s.l. were characterized by surface patches of sclerotia and

loose wes of hyphae growing along the root surface and hyphae

as well as sclerotia growing inter- and intracellularly in the

outer cortex (O’Dell etal. 1993). Occasionally, patches of inter-

cellular labyrinthine fungal tissue, similar to Hartig net tissue,

were formed on the surface of primary pine roots, and proxi-

mal portions of lateral roots frequently had a sporadic mantle.

Similarly, roots of Pinus strobus L. showed varying amounts of

surface hyphae, Hartig net structures, and intracellular hyphae

(Peterson etal. 2008; Figure 38.3D). Acephala macrosclerotio-

rum Münzenberger & Bubner, a recently described close relative

of PAC, formed thin mantles and a distinct Hartig net on Pinus

sylvestris and Picea abies (Münzenberger etal. 2009). A. mac-

rosclerotiorum forms characteristic, melanized wartlike scle-

rotia giving the mantle a verrucous appearance (Figure 38.3E).

DSE formed good mantles and Hartig nets on some of the best

nursery stocks of pines and white spruce (Danielson and Visser

1990). It persisted on the stock for as long as the seedlings were

in the nursery, but once outplanted, it was replaced by mycor-

rhizal fungi, especially elephora terrestris Ehrh. and E-strain

fungi. Hartig net structures could not be observed in resynthe-

sis experiments between Picea abies and various PAC strains,

and microsclerotia production was strongly strain dependent

(Tellenbach etal. 2010).

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-31Fungal Root Endophytes

Colonization of ne roots (diameter <5 mm) of Norway

spruce and Scots pine by DSE was examined in eld samples

from Finland and Switzerland (Sieber, unpublished). Density

of surface mycelia and intracortical fungal structures are much

lower in eld samples than in roots from in vitro synthesis

experiments, and thus, the endophytes are more dicult to

locate. DSE were observed to colonize primary roots down to

the innermost cortical cells. Colonization of the endodermis

or the expanded pericycle did not occur. DSE most frequently

occurred as intra- and intercellular hyphae and small intracellu-

lar microsclerotia composed of cells with thin, melanized walls.

e rhytidome of older conifer roots is frequently colonized by

dark, septate hyphae down to the youngest layer of phellem cells.

Intensely colonized roots can be recognized already in the eld

by the black appearance of the rhytidome; sometimes, it is nec-

essary to remove the loose bark scales to see the more proxi-

mal phellem tissues (Grünig etal. 2008b). e black appearance

of the rhytidome is due to cells of the phlobaphene cork lled

with multicellular sclerotia composed of bubble-shaped, thick-

walled, melanized cells (Holdenrieder, personal communica-

tion, 1997; Figure 38.3F). ese sclerotia might serve as inoculi

and food bases from where mycelia can grow to colonize new

substrates. Holdenrieder (1989) presented excellent SEM pic-

tures of hyphal aggregations of DSE lling entire phellem cells of

Norway-spruce roots. Endophytic colonization of cells proximal

to the phellem has, so far, not conclusively been demonstrated

but is certainly possible considering the frequent colonization of

the xylem in forest trees by DSE (including PAC) (Görke 1998).

Intracellular colonization of Norway-spruce seedlings inocu-

lated with DSE and Cryptosporiopsis cf. abietina Petr., possibly

conspecic with C. radiciola Kowalski & Kehr, was observed in

root cortex cells (Haug etal. 1988). Whereas the infection by

DSE was conned to the cortex, C. cf. abietina colonized also

the vascular tissue and caused decline of the seedlings. e older

seedlings (5-month-old compared to 3-week-old) resisted for a

longer period of time. Interestingly, addition of malt caused DSE

to become pathogenic and to colonize the vascular tissues.

2. Endophyte–Pathogen Interactions,

Biological Control

Some endophytes were demonstrated to confer biological

control against other microorganisms. Duda and Sierota (1987)

successfully used Trichoderma viride Pers., which was found

highly pathogenic on Norway-spruce seedlings (Forbrig 1989)

to control damping-o of Pinus sylvestris seedlings caused by

Fusarium oxysporum or Rhizoctonia solani. DSE were shown to

protect roots of Picea abies, Pinus sylvestris, and Quercus robur L.

against other organisms, for example, F. oxysporum and R. solani

(Manka 1960; Manka and Przezbòrski 1978, 1987). DSE had only

an adverse eect onto the trees when these had been planted on

an unsuitable site or aer an Armillaria attack. Some isolates of

Phialocephala subalpina increased survival of Norway-spruce

seedlings inoculated with either one of the two root pathogens

Phytophthora plurivora T. Jung & T.I. Burgess (syn. P. citri-

cola Sawada) or Elongisporangium undulatum (H.E. Petersen)

Uzuhasi, Tojo & Kakish. (syn. Pythium undulatum H.E. Petersen)

(Tellenbach and Sieber 2012). Phialocephala subalpina seems to

confer an indirect benet to its host and might therefore be tol-

erated in natural spruce populations, despite negative eects on

plant performance.

Biological control seems to be eective not only among fungal

species but also among genotypes (strains) of the same species.

Pathogenicity is oen strain dependent (Tellenbach etal. 2011)

(see text in the following paragraph). Nonpathogenic PAC strains

signicantly reduced density of colonization of Norway-spruce

(Picea abies) roots by pathogenic PAC strains, attenuating adverse

eects on plant growth (Reininger etal. 2011a, 2012). is high-

lights the importance of high genotypic diversity of PAC fungi

colonizing the same root system.

3. Endophyte–Plant Interactions

DSE had very marked pathogenic properties toward Pinus syl-

vestris under pure culture conditions. However, DSE could

achieve dominance on root surfaces of healthy elongating roots

of pines growing under natural conditions, when its pathogenic

eects appear to be reduced (Robertson 1954). De la Bastide and

Kendrick (1990) treated white-pine seedlings (Pinus strobus)

with benomyl to reduce the pathogenic eect of DSE. Adverse

eects caused by DSE occurred also in experiments of Richard

etal. (1971) with Picea mariana, Wilhelm etal. (1969) with Pinus

pinea L. seedlings, Wilcox and Wang (1987) with Pinus resinosa

Aiton, Picea rubens Sarg., and Betula alleghaniensis Britton, and

Melin (1923) with Pinus sylvestris and Picea abies.

General health status as expressed by needle color, pres-

ence or absence of needle-tip chlorosis, mortality rate, and dry

weight of Norway-spruce seedlings used to bait DSE from for-

est soils was not correlated with the colonization of the roots

by DSE (mainly PAC) (Ahlich etal. 1998). Hennon etal. (1990)

frequently isolated DSE, Cryptosporiopsis sp., Gelatinosporium

sp., Sporidesmium sp., Cylindrocarpon didymum (Harting)

Wollenw., and Cadophora melinii Nannf. from healthy

and declining cedar roots during their studies on declin-

ing Chamaecyparis nootkatensis (D. Don) Spach in Southeast

Alaska. DSE were most frequently isolated. Healthy and

declining trees were equally frequently colonized. Except for

C. didymum, none of the fungi proved to be pathogenic in infec-

tion experiments with cedar seedlings. None of the seedlings

died. Similarly, DSE were isolated from diseased and healthy

seedlings of Norway spruce equally frequently and were not

pathogenic in infection experiments (Galaaen and Venn 1979).

is contrasts with Pythium sylvaticum W.A. Campb. & F.F.

Hendrix that was isolated almost only from diseased seedlings

and was highly virulent when inoculated onto axenically grown

seedlings. e endophytic mycobiota in roots of European silver

r (A. alba) seedlings was examined at a site with natural regen-

eration and another site where r did not regenerate (Kowalski

1982a). Ilyonectria radicicola (teleomorph of C. destructans)

was the most frequently isolated pathogenic fungus, especially

in young, 1-year-old seedlings. In natural regenerations, DSE

were very common and I. radicicola occurred only sporadically.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-32 Root–Rhizosphere Interactions

Likewise, I. radicicola was demonstrated to be pathogenic on

r and pine seedlings in vitro (Dahm etal. 1987). Virulence

was aected by pH, temperature, light intensity, and also by

associated bacteria and actinomycetes. In contrast, Bloomberg

(1966) isolated DSE and Cylindrocarpon spp. more frequently

from healthy Douglas-r seedlings. e frequency of Fusarium

spp. did, however, not depend on the health status of the plants.

DSE, Trichoderma viride, and I. radicicola were pathogenic

when inoculated onto 2 to 3-week-old axenically grown seed-

lings of Picea abies (Forbrig 1987, 1989). T. viride and I. radici-

cola killed the seedlings rapidly. DSE were suspected to infect

only weakened trees. e interactions with Norway spruce of

more than 30 isolates of four dierent PAC species and from

three geographical regions were strongly isolate dependent

and ranged from neutral to highly virulent, but no strain had

a stimulating eect on plant growth (Tellenbach etal. 2011).

Variation in virulence was much higher within than among

PAC species, but only isolates of Phialocephala subalpina, one

of the most frequent PAC species, were highly virulent. Disease

caused by Phialocephala subalpina genotypes from the native

range of Norway spruce was more severe than that induced by

genotypes from outside the range. Virulence was not correlated

with the phylogenetic relatedness of the isolates but was posi-

tively correlated with the extent of fungal colonization as mea-

sured by quantitative real-time PCR. e results obtained by

Tellenbach etal. (2011) contrast with those reported by Peterson

et al. (2008) who observed the production of lateral roots of

Pinus strobus seedlings inoculated with Phialocephala fortinii

s.l. being greater than that of uninoculated controls.

Chloridium paucisporum C.J.K. Wang & H.E. Wilcox from

3-year-old nursery seedlings of Pinus resinosa was found to stim-

ulate Pinus resinosa seedlings growth (Wilcox and Ganmore-

Neumann 1974). e plant–fungus association was found to

be EEM but dierent from that of E-strain fungi. Jumpponen

and Trappe (1998b) showed that the culture system under which

an association is studied may also aect the host–fungus inter-

action. e eects of various glucose concentrations on Pinus

contorta seedlings inoculated with Phialocephala fortinii s.l.

were studied in an axenic and an open pot system. Inoculation

resulted in substantial increase of biomass in the axenic system,

and host biomass increased with increasing glucose concentra-

tion. Glucose alone did not signicantly aect host biomass. In

the open pot cultures, inoculation did not aect biomass. e

observed growth stimulation in the closed culture system was

probably due to CO

fertilization as a consequence of fungal

respiration (Jumpponen and Trappe 1998b). Growth stimula-

tion and inhibition were observed also in cell-free extracts of

endophytes. Culture ltrates of T. viride reduced and ltrates of

DSE stimulated elongation of excised roots of Pinus sylvestris,

whereas I. radicicola reduced formation of lateral roots (Turner

1962). Binucleate Rhizoctonia endophytes promoted formation

of adventitious roots of Scots pine (Pinus sylvestris L.) hypo-

cotyl cuttings (Kaparakis and Sen 2006). Similarly, Rhizoctonia

stimulated early seedling growth in a nitrogen-limited soil

(Grönberg etal. 2006).

4. Endophyte–Environment Interactions

Knowledge about the in uence of environmental factors on

frequency and colonization of root endophytes is sparse.

Although some factors were identied in the past, more eorts

are needed to get a more complete picture of the key factors

and how they interact with each other and with the endo-

phyte–plant system. e proton [H

] concentration (pH) in

the soil and the type of biogeoclimatic zone were identied as

factors aecting root endophyte communities. Statistically

signicant correlations existed between soil pH and the fre-

quency of colonization by Cryptosporiopsis radicicola Kowalski

& C. Bartnik, Cylindrocarpon didymum, and DSE (Ahlich and

Sieber 1996). e correlations with C. radicicola and C. didy-

mum were positive, and the correlation with DSE was negative.

Some Cylindrocarpon species are well known to prefer alkaline

conditions (Matturi and Stenton 1964; Domsch et al. 1980;

Schönhar 1987). DSE were, however, considered not to be in u-

enced by soil pH according to Melin (1924). Although DSE were

absent in the soil samples of only 2 of 72 sites, DSE occurred

less frequently in soils with a high pH value (Ahlich etal. 1998).

Maximum isolation was from soils with pH values ranging from

3.5 to 4.5. Similarly, Manka (1960) gives pH 4 as the optimum

for growth of DSE. Danielson and Visser (1989) considered a pH

value of 3.1 the minimum for growth of DSE contrasting with

the results of Ahlich etal. (1998) who detected DSE in almost

90% of the root segments of the Norway-spruce seedlings used

to bait endophytes from a forest soil with pH 3.0. A relationship

between altitude and pH value was reported by Holdenrieder

and Sieber (1992) who found the most prominent dierence in

fungal associations in Norway-spruce roots to exist between

roots colonized mainly by I. radicicola from alkaline soils at low

altitude and roots dominated by DSE from acidic soil (peat bog),

as well as from alkaline soil at high altitude.

In Switzerland, Phialocephala fortinii s.l. proofed to occur

preferentially on high altitudes (Ahlich and Sieber 1996).

Trichoderma viride occurred preferentially in roots from

extremely acidic soils, T. hamatum (Bonord.) Bainier from

moderately acidic, and T. polysporum (Link) Rifai from weakly

acidic soils (Kattner and Schönhar 1990). Cryptosporiopsis abi-

etina (perhaps conspecic with C. radicicola) and I. radicicola

preferred a neutral environment. Liming reduced T. viride and

a Penicillium sp., whereas the frequency of DSE, Penicillium

spinulosum om, T. polysporum, and some Mortierella spp.

increased (Kattner 1992b). Inoculations with root endophytes

may enhance survival rates of seedlings planted at polluted sites.

LoBuglio and Wilcox (1988) inoculated Pinus resinosa seedlings

with Cadophora nlandica (C.J.K. Wang & H.E. Wilcox) T.C.

Harr. & McNew and planted them onto iron tailings in an old

iron mine. C. nlandica inoculated seedlings had a higher sur-

vival rate than uninoculated controls. In addition, mortality of

seedlings treated with C. nlandica was lower than that of seed-

lings treated with ectomycorrhizal fungi.

Data about the in uence of phosphorus (P) and nitro-

gen (N) availability on colonization by endophytes and plant

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-33Fungal Root Endophytes

performance are sparse. Pinus contorta seedlings inoculated

with Phialocephala fortinii s.l. showed enhanced P uptake and

increased growth (Jumpponen etal. 1998). In addition, N uptake

was increased when Phialocephala fortinii s.l. inoculation was

combined with addition of N. N fertilization of a 20-year-old

stand of western hemlock (Tsuga heterophylla (Raf.) Sarg.)

with urea did not change the total number of ne roots and

the number of basidiomycetous mycorrhizae (Kernaghan etal.

1995). However, Cenococcum geophilum mycorrhizae decreased

slightly, whereas those lacking mantels such as EEM and DSE

increased.

Pinus sylvestris seedlings inoculated with DSE (Phialocephala

fortinii s.l., Cadophora nlandica, Chloridium paucisporum,

Pezoloma ericae, Meliniomyces variabilis, and M. vraolstadiae

Hambl. & Sigler) accumulated on average 17% more biomass

than control seedlings under elevated CO

combined with N

limitation, indicating that DSE fungi increase plant nutrient

use eciency and are, thus, more benecial to the plant under

elevated CO

(Alberton etal. 2010).

5. Extracellular Enzymes and Fungicide Resistance

e production of biocidal metabolites, plant growth hormones,

exoenzymes, and siderophores or the resistance against noxious

substances can be advantageous when competing with other

soil microorganisms for space, nutrients, and/or infection sites

(Currah and Tsuneda 1993; Ahlich-Schlegel 1997; Caldwell etal.

2000; Bartholdy et al. 2001; Schulz etal. 2002; Grünig et al.

2008b). C. nlandica and several PAC isolates utilized cellulose,

laminarin, starch, and xylan as sole carbon source and pro-

teins and nucleic acids as sole nitrogen and phosphorus sources

(Caldwell et al. 2000). However, lignolytic activity was not

observed. T. viride, Mortierella nana Linnem., and DSE exhib-

ited higher pectolytic than cellulolytic activity, and the activity

was strain dependent (Dahm 1987). Trichoderma isolates were

the most active, DSE the least. Presence of cellulolytic activ-

ity of DSE was demonstrated by Gams (1963), Levisohn (1954),

and Melin (1923). e opposite observation by Schelling (1952)

may be due to the fact that she used neither trace elements nor

growth factors in her experiments. Ahlich-Schlegel (1997) tested

more than 200 DSE isolates for fungicide resistance and the

presence of extracellular enzymes and was able to demonstrate

that enzyme activity is strain dependent. One-third of all strains

produced proteases. Some Acephala applanata strains were able

to produce amylases, but other PAC species were not. Laccase

activity, an oxidase used to degrade lignin, was observed in all

A. applanata strains but was present only in half of the other

PAC strains. Most strains produced phenoloxidases, but activity

was much higher in A. applanata isolates. Similar observations

were made by Grünig etal. (2008b) who found A. applanata to

be a good producer of amylases, laccases, and proteases in con-

trast to other PAC species. Benomyl at a concentration of ≥10

mg L

−1

inhibited all strains, whereas thiabendazole did so only

at a concentration of ≥100 mg L

−1

(Ahlich-Schlegel 1997). At

10 mg L

−1

thiabendazole, all A. applanata isolates were inhib-

ited; the reaction of the other DSE was variable. Cycloheximide

at ≥100 mg L

−1

inhibited A. applanata, Phialocephala letzii,

Phialocephala helvetica, and Phialocephala subalpina the most

and Phialocephala uotilensis and Phialocephala turicensis the

least (Ahlich-Schlegel 1997; Grünig etal. 2008a,b). Toxins were

responsible for pathogenicity of I. radicicola but the high pec-

tinase and cellulase production of this fungus were assumed to

enhance virulence (Lyr and Kluge 1968).

Bartholdy etal. (2001) studied the siderophore proles of ve

PAC strains. Siderophores controlling the uptake of iron ions by

fungi play a crucial role in the infection process in some plant–

fungus systems (Johnson 2008). e siderophore proles of two

Phialocephala fortinii s.s. strains were highly similar. ey pro-

duced almost exclusively ferricrocin. In contrast, a strain each of

Phialocephala subalpina and Phialocephala europaea possessed

unique siderophore proles and produced ferrirubin in addition

to ferricrocin, but the amount of ferricrocin produced was signi-

cantly lower in Phialocephala subalpina and signicantly higher in

Phialocephala europaea than in Phialocephala fortinii s.s. A strain

of CSP9 isolated from Larix decidua Mill. in Germany produced

the plant growth hormone IAA (Schulz etal. 2002). e vacuolar

system in hyphae of PAC strain UAMH_9608 (Phialocephala

fortinii s.s.) was investigated, and the presence of polyphosphate

in the vacuoles was conrmed (Saito etal. 2006). An endophytic

strain of Phialocephala scopiformis T. Kowalski & Kehr, a species

with high anities to the PAC, was recently reported to produce

rugulosin—a toxic metabolite against some herbivores of Picea

glauca needles (Miller etal. 2008; Sumarah etal. 2008). Whether

PAC members also produce secondary metabolites toxic to some

herbivores feeding on roots remains to be tested.

6. Stress Tolerance and Oligotrophic Growth of DSE

DSE are resistant against repeated thawing–freezing and against

permanent drought and are able to grow under oligotrophic

conditions. MEA discs and cellophane pieces colonized by PAC

isolates were frozen at −20°C and thawn and refrozen daily

(Ahlich-Schlegel 1997). Most isolates survived for at least 10 days.

Phialocephala fortinii s.l. survived on average longer than A. appla-

nata. One Phialocephala fortinii s.l. isolate survived for more than

50 days. Drought resistance was tested by putting cellophane sheets

colonized by PAC isolates in a desiccator. All isolates survived for

at least 8 months. PAC isolates were grown on nitrogen-free water

agar and subcultured four times every 21 days. Mycelium was very

sparse in all isolates, but growth was not reduced even aer the

fourth subculture. Colony diameters ranged from 29 to 43 mm

for Acephala applanata and 43–63 for Phialocephala fortinii s.l.

Growth under oligotrophic conditions was studied in plastic Petri

dishes that may have released some nitrogen into the medium.

us, the experiment should be repeated using glass Petri dishes.

C. Root Endophytes in Other

Woody Plant Species

Members of the Betulaceae, Fagaceae, and Salicaceae are the

best studied for the presence of root endophytes (Table 38.6).

Species of Cryptosporiopsis, Cylindrocarpon, Meliniomyces, and

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-34 Root–Rhizosphere Interactions

TABLE 38.6 Endophytes in Other Woody Plants

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Acephala applanata Helotiales DSE Betula pubescens Fagales Tree Isol Queloz (2010)

Acephala sp. 2 Helotiales DSE Sorbus aucuparia Rosales Tree Isol Grünig etal. (2009)

Alternaria alternata Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Alternaria chlamydospora Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Anguillospora liformis Pleosporales Not DSE Acer spicatum Sapindales Tree Isol Sridhar and Bärlocher (1992)

Anguillospora liformis Pleosporales Not DSE Betula papyrifera Fagales Tree Isol Sridhar and Bärlocher (1992)

Anguillospora longissima Pleosporales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Articulospora proliferata Helotiales Not DSE Mangifera indica Sapindales Tree Isol Iqbal etal. (1995)

Articulospora proliferata Helotiales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Ascochyta sp. Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Cadophora fastigiata Helotiales DSE Quercus robur Fagales Tree Isol Halmschlager and Kowalski (2004)

Cadophora sp. Helotiales DSE Quercus petraea Fagales Tree Isol Halmschlager and Kowalski (2004)

Cadophora sp. 3 Helotiales DSE Myricaria prostrata Caryophyllales Woody shrub Isol Graf, pers. comm. (2008)

Chaetomium cochliodes Sordariales Not DSE Aphelandra tetragona Lamiales Woody shrub Isol Werner etal. (1997)

Cladosporium tenuissimum Capnodiales DSE Alnus glutinosa Fagales Tree Isol Fisher etal. (1991b)

Clavariopsis aquatica Pleosporales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Coniothyrium sp. Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Cryptosporiopsis radicicola Helotiales DSE Fagus sylvatica Fagales Tree Isol Ahlich and Sieber (1996)

Cryptosporiopsis radicicola Helotiales DSE Quercus petraea Fagales Tree Isol Halmschlager and Kowalski (2004)

Cryptosporiopsis melanigena Helotiales DSE Quercus petraea Fagales Tree Isol Kowalski etal. (1998)

Cryptosporiopsis radicicola Helotiales DSE Quercus robur Fagales Tree Isol Kowalski and Bartnik (1995)

Cylindrocarpon didymum Hypocreales Not DSE Fagus sylvatica Fagales Tree Isol Ahlich and Sieber (1996)

Cylindrocarpon magnusianum Hypocreales Not DSE Fagus sylvatica Fagales Tree Isol Görke (1998)

Cystodendron sp. Helotiales Variable Quercus petraea Fagales Tree Isol Halmschlager and Kowalski (2004)

Embellisia chlamydospora Pleosporales DSE Myricaria prostrata Caryophyllales Woody shrub Isol Graf, pers. comm. (2008)

Flagellospora curvula Hypocreales Not DSE Mangifera indica Sapindales Tree Isol Iqbal etal. (1995)

Flagellospora curvula Hypocreales Not DSE Populus hybrida Malpighiales Tree Isol Iqbal etal. (1995)

Flagellospora curvula Hypocreales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Flagellospora fusaroides Hypocreales Not DSE Mangifera indica Sapindales Tree Isol Iqbal etal. (1995)

Flagellospora fusaroides Hypocreales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Gibberella intricans Hypocreales Not DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Werner etal. (1997)

Fusarium oxysporum Hypocreales Not DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Fusarium sp. Hypocreales Not DSE Mangifera indica Sapindales Tree Isol Iqbal etal. (1995)

Fusarium sp. Hypocreales Not DSE Populus hybrida Malpighiales Tree Isol Iqbal etal. (1995)

Fusarium sp. Hypocreales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Gibberella baccata Hypocreales Not DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Gibberella nygamai Hypocreales Not DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Haematonectria haematococca Hypocreales Not DSE Aphelandra tetragona Lamiales Woody shrub Isol Werner etal. (1997)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-35Fungal Root Endophytes

Ilyonectria radicicola Hypocreales Not DSE Alnus glutinosa Fagales Tree Isol Fisher etal. (1991b)

Ilyonectria radicicola Hypocreales Not DSE Aphelandra tetragona Lamiales Woody shrub Isol Werner etal. (1997)

Ilyonectria radicicola Hypocreales Not DSE Betula pendula Fagales Tree Isol Görke (1998)

Ilyonectria radicicola Hypocreales Not DSE Fagus sylvatica Fagales Tree Isol Görke (1998)

Ilyonectria radicicola Hypocreales Not DSE Gynoxys oleifolia Asterales Tree Isol Fisher etal. (1995b)

Ilyonectria radicicola Hypocreales Variable Quercus robur Fagales Tree Isol Halmschlager and Kowalski (2004)

Ilyonectria radicicola Hypocreales Variable Tilia petiolaris Malvales Tree Isol Schroers etal. (2008)

Nectria lugdunensis Hypocreales Not DSE Acer spicatum Sapindales Tree Isol Sridhar and Bärlocher (1992)

Nectria lugdunensis Hypocreales DSE Alnus glutinosa Fagales Tree Isol Fisher etal. (1991b)

Leptodontidium sp. Helotiales DSE Eucalyptus regnans Myrtales Tree Isol Tedersoo etal. (2009)

Leptodontidium sp. Helotiales DSE Nothofagus

cunninghamii

Fagales Tree Isol Tedersoo etal. (2009)

Leptodontidium sp. Helotiales DSE Pomaderris apetala Rosales Tree Isol Tedersoo etal. (2009)

Libertella spp. Xylariales Not DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Lunulospora curvula Pezizomycotina Not DSE Populus hybrida Malpighiales Tree Isol Iqbal etal. (1995)

Lunulospora curvula Pezizomycotina Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Meliniomyces bicolor Leotiomycetes DSE Nothofagus procera Fagales Tree Isol Hambleton and Sigler (2005)

Meliniomyces bicolor Leotiomycetes DSE Quercus robur Fagales Tree Isol Hambleton and Sigler (2005)

Meliniomyces sp. 1 Leotiomycetes Variable Betula pubescens Fagales Tree Isol Hambleton and Sigler (2005)

Meliniomyces vraolstadiae Leotiomycetes Variable Betula pubescens Fagales Tree Isol Hambleton and Sigler (2005)

Monodictys arctica Dothideomycetes DSE Saxifraga oppositifolia Saxifragales Woody shrub Isol Day etal. (2006)

Oidiodendron sp. Dothideomycetes DSE Eucalyptus regnans Myrtales Tree Isol Tedersoo etal. (2009)

Oidiodendron sp. Dothideomycetes DSE Nothofagus

cunninghamii

Fagales Tree Isol Tedersoo etal. (2009)

Oidiodendron sp. Dothideomycetes DSE Pomaderris apetala Rosales Tree Isol Tedersoo etal. (2009)

Penicillium pinetorum Eurotiales Not DSE Aphelandra tetragona Lamiales Woody shrub Isol Werner etal. (1997)

Penicillium restrictum Eurotiales Not DSE Betula pendula Fagales Tree Isol Görke (1998)

Penicillium restrictum Eurotiales Not DSE Fagus sylvatica Fagales Tree Isol Görke (1998)

Phialocephala europaea Helotiales DSE Fagus sylvatica Fagales Tree Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Salix sp. Malpighiales Tree Isol Queloz (2010)

Phialocephala europaea Helotiales DSE Sorbus aucuparia Rosales Woody shrub Isol Queloz (2010)

Phialocephala fortinii s.l. Helotiales DSE Betula pendula Fagales Tree Isol Görke (1998)

Phialocephala fortinii s.l. Helotiales DSE Fagus sylvatica Fagales Tree Isol Ahlich and Sieber (1996)

Phialocephala fortinii s.s. Helotiales DSE Betula pendula Fagales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Betula pubescens Fagales Tree Isol Queloz (2010)

Phialocephala fortinii s.s. Helotiales DSE Sorbus aucuparia Rosales Woody shrub Isol Queloz (2010)

Phialocephala helvetica Helotiales DSE Fagus sylvatica Fagales Tree Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Fagus sylvatica Fagales Tree Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Helianthemum sp. Malvales Woody shrub Isol Queloz (2010)

Phialocephala letzii Helotiales DSE Sorbus aucuparia Rosales Woody shrub Isol Queloz (2010)

(continued)

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-36 Root–Rhizosphere Interactions

TABLE 38.6 (continued) Endophytes in Other Woody Plants

Endophyte Host

Type of

Experiment

Special

Eect

ReferencesGenus

Species

Fungus Order

DSE/Not DSE Species Plant Order

Woody/

Herbaceous

Phialocephala sp. 9 Helotiales DSE Myricaria prostrata Caryophyllales Woody shrub Isol Graf, pers. comm. (2008)

Phialocephala sphaeroides Helotiales DSE Aralia nudicaulis Apiales Woody shrub Isol Wilson etal. (2004)

Phialocephala subalpina Helotiales DSE Betula pendula Fagales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Betula tortuosa Fagales Tree Isol Queloz (2010)

Phialocephala subalpina Helotiales DSE Sorbus aucuparia Rosales Woody shrub Isol Queloz (2010)

Phialocephala turicensis Helotiales DSE Fagus sylvatica Fagales Tree Isol Queloz (2010)

Phoma prunicola Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Phoma variospora Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Phomopsis alnea Diaporthales Not DSE Alnus glutinosa Fagales Tree Isol Fisher etal. (1991b)

Phomopsis spp. Diaporthales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Pleospora herbarum Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Pleospora obrusa Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Pleospora phaeocomoides Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Pyrenochaeta sp. 1 Pleosporales DSE Caragana versicolor Fabales Woody shrub Isol Graf, pers. comm. (2008)

Serendipita vermifera Auriculariales Not DSE Tilia sp. Malvales Tree In vitro exp a Oberwinkler (1964)

Sesquicillium candelabrum Hypocreales Not DSE Betula pendula Fagales Tree Isol Görke (1998)

Sesquicillium candelabrum Hypocreales Not DSE Fagus sylvatica Fagales Tree Isol Görke (1998)

Sporormiella intermedia Pleosporales DSE Atriplex vesicaria Caryophyllales Woody shrub Isol Cother and Gilbert (1994)

Tetracladium marchalianum Helotiales Not DSE Mangifera indica Sapindales Tree Isol Iqbal etal. (1995)

Tetracladium marchalianum Helotiales Not DSE Populus hybrida Malpighiales Tree Isol Iqbal etal. (1995)

Tetracladium marchalianum Helotiales Not DSE Salix babylonica Malpighiales Tree Isol Iqbal etal. (1995)

Trichoderma viride Hypocreales Not DSE Aphelandra tetragona Lamiales Woody shrub Isol Werner etal. (1997)

Triscelophorus konajensis Pezizomycotina Not DSE Coea arabica Gentianales Woody shrub Isol Raviraja etal. (1996)

Triscelophorus monosporus Pezizomycotina Not DSE Coea arabica Gentianales woody shrub Isol Raviraja etal. (1996)

Unidentied DSE DSE Atriplex canescens Caryophyllales Woody shrub In vitro exp Barrow etal. (2004)

Unidentied DSE DSE Daphniphyllum

neilgherrense

Saxifragales Tree Isol Bagyalakshmi etal. (2010)

Unidentied DSE DSE Elaeocarpus munronii Oxalidales Tree Isol Bagyalakshmi etal. (2010)

Unidentied DSE DSE Euodia roxburghiana Sapindales Tree Isol Bagyalakshmi etal. (2010)

Unidentied DSE DSE Syzygium arnottianum Myrtales Tree Isol Bagyalakshmi etal. (2010)

Unidentied DSE DSE Syzygium montanum Myrtales Tree Isol Bagyalakshmi etal. (2010)

Unidentied DSE DSE Tamarix ramosissima Caryophyllales Woody shrub Isol Beauchamp etal. (2005)

Genus, species and order (family) names according to index fungorum (http://www.indexfungorum.org/Names/Names.asp, December 20, 2011). If both the teleomorph (sexual reproductive stage) and

next lower taxon is given if the Fungus order is not known with certainty (“incertae sedis”).

Isol, isolation from surface-sterilized roots; in vitro exp, fungus used in in-vitro experiment(s).

Special eect details: (a) Plant growth stimulation.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-37Fungal Root Endophytes

Phialocephala were most frequently isolated. Cryptosporiopsis

radicicola, a species oen isolated from roots of Quercus robur

(Kowalski and Bartnik 1995; Halmschlager and Kowalski

2004), was the dominant endophyte in roots of European beech

(Fagus sylvatica) in Switzerland (Ahlich and Sieber 1996), and

Cryptosporiopsis melanigena T. Kowalski & Halmschl. was

oen isolated from roots of Q. robur and Q. petraea (Kowalski

etal. 1998). According to Kowalski (1983), the wood and bark

endophyte Pezicula cinnamomea (DC.) Sacc., with its ana-

morph Cryptosporiopsis grisea (Pers.) Petr., can also spread

into the roots of dying trees. e main colonizer of Dryas

octopetala L. roots sampled at Spitsbergen was a Cryptosporiopsis

species (Fisher etal. 1995a). DSE (including Phialocephala forti-

nii s.l.) were demonstrated to be the most frequent endophytes

in apparently healthy xylem of roots of Betula pendula and F.

sylvatica in Germany (Görke 1998; Table 38.6). Similarly, DSE

were observed in 42% and 40% of the root samples from Iva

frutescens L. and Triadica sebifera (L.) Small, respectively, col-

lected in the southeastern marshes of Louisiana (Kandalepas

etal. 2010). DSE also dominated the endophyte community in

woody shrubs collected in Kailash-Manasarovar Region on the

Tibetan plateau at 4700 m (F. Graf, personal communication,

July 2008; Table 38.6). Desertication by wind and water erosion

is a serious threat in this region, and the mycelium of mycor-

rhizal and other endophytic fungi could have a stabilizing eect

(Burri etal. 2009).

However, DSE do not always dominate the non-mycorrhizal

endophyte community in roots of woody plants. DSE were absent

or rare in roots of Gynoxis oleifolia Muchler (Compositae) col-

lected in Ecuador at 3300 m asl. I. radicicola, Epicoccum nigrum

Link, Trichoderma harzianum Rifai, and Truncatella angustata

(Pers.) S. Hughes were the endophytic fungi most frequently

observed (Fisher etal. 1995b).

Very special endophyte communities are found on roots con-

stantly submersed in water (Sengupta etal. 1988; Fisher etal.

1991b; Sridhar and Bärlocher 1992; Iqbal etal. 1995; Raviraja

et al. 1996). Submersed roots are oen colonized by aquatic

hyphomycetes in addition to “terrestrial” fungi (Table 38.6). e

eects of aquatic hyphomycetes on their host are probably small.

Submersed roots may, however, constitute refuge and perma-

nent sources of inoculum for the aquatic hyphomycetes to per-

sist in streams (Raviraja etal. 1996). Two septate, dematiaceous

endophytes, a coelomycete and a Rhizoctonia-like fungus, were

frequently isolated from roots of some mangroves and saline-

resistant plants growing in the seabound delta region of West

Bengal (Sengupta etal. 1988). ey grew inter- and intracellu-

larly either alone or simultaneously with AM and formed sclero-

tia in culture. Absence of AM in some halophytes indicates that

endophytes may replace AM in extreme habitats, similar to what

has been observed for arctic and alpine herbaceous plants.

Some woody plant species were examined also on the Southern

Hemisphere. Roots of Nothofagus cunninghamii (Hook.) Oerst.,

Eucalyptus regnans F. Muell., and Pomaderris apetala Labill.

from Tasmania were colonized by species of Leptodontidium

and Oidiodendron (Tedersoo etal. 2009). ese helotialean fungi

are phylogenetically closely related to root endophytes and eri-

coid mycorrhizal fungi of the Northern Hemisphere, suggest-

ing strong ecological and evolutionary links. Seventy-one fungal

endophytes could be isolated from bladder saltbush (Atriplex

vesicaria Heward ex Benth.) in Southern Australia (Cother and

Gilbert 1994). Fusarium spp., Alternaria chlamydospora Mouch.,

Libertella spp., Phoma variospora Shreem., and Sporormiella

intermedia (Auersw.) S.I. Ahmed & Cain ex Kobayasi were iso-

lated as root endophytes for the rst time in Australia. Species of

known pathogenic genera (Ascochyta, Coniothyrium, Phomopsis,

Pleospora) occurred also quite frequently.

1. Anatomy

Phialocephala fortinii CSP 13 (CSP 13 according to Grünig etal.

(2008b)) formed a Hartig net and a thin, patchy mantle in axenic

culture with Salix glauca L. seedlings (Fernando and Currah

1996; Figure 38.3G). An interesting fungus–root association was

described by Sequerra etal. (1995). Penicillium nodositatum Valla

was observed to penetrate and colonize cortical cells of roots of

Alnus incana (L.) Moench and to induce myconodules similar to

those formed by actinorhizal bacteria (Frankia spp.). Host defense

was minimal, and the host plasma membrane, invaginated around

the endophyte, kept its integrity as it does in symbiotic associations.

Penicillium nodositatum was, thus, considered as a neutral micro-

symbiont similar to a compatible but ineective Frankia strain.

2. Endophyte–Pathogen Interactions

Trichoderma spp. and Gliocladium spp. were shown to control

Phytophthora cactorum root and crown rot of apple (Smith etal.

1990). Some isolates signicantly reduced root rot and increased

plant weight. DSE were shown to protect roots of Picea abies,

Pinus sylvestris, and Q. robur against other organisms, for

example, F. oxysporum and R. solani (Manka 1960; Manka and

Przezbòrski 1978, 1987).

3. Endophyte–Plant Interactions

Leptodontidium orchidicola caused a marked increase in host root

length but also invaded the stele, causing extensive cellular lysis in

axenic culture with Salix glauca seedlings (Fernando and Currah

1996). In pot monocultures with various subalpine plant spe-

cies, the eects of L. orchidicola strains on host dry weight were

strain and host specic (Fernando and Currah 1996). e eects

of Phialocephala fortinii CSP 13 were also host specic. In pot

combination cultures (Dryas octopetala, Picea abies, Potentilla

fruticosa L., and S. glauca in the same pot), the Phialocephala

fortinii s.l.–Potentilla fruticosa symbiosis resulted in a signicant

increase in shoot weight in contrast to the results of the same sym-

biosis in monoculture resynthesis. DSE isolated from mangroves

stimulated growth of Cajanus cajan (L.) Millsp. in the absence of

easily available phosphorus (Sengupta etal. 1988).

4. Endophyte–Environment Interactions

Caldwell etal. (2000) studied the utilization of major forms of

carbon, nitrogen, and phosphorus commonly present in plant

litter and detritus for two dark septate, root endophyte isolates

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-38 Root–Rhizosphere Interactions

from alpine Salix species. Both isolates utilized cellulose, lam-

inarin, starch, and xylan as sole carbon source and proteins

and ribonucleic acids as sole nitrogen and phosphorus sources.

However, lignolytic activity could not be detected.

VI. Conclusions and Outlook

e presence of non-mycorrhizal fungal endophytes in plant

roots is a worldwide phenomenon. ere is probably no plant

species without root endophytes. Species diversity of endophyte

communities in roots is low compared to the one in aerial tis-

sues. However, the within-species genotypic diversity of root

endophytes can be high. Fungi with melanized, septate hyphae

are prevalent in many of the communities. ese fungi usually

do not sporulate readily in culture and are, therefore, assigned to

the form taxon DSE. DSE are a very diverse group of fungi. ey

can be separated into two subgroups. e rst includes DSE,

which occur mainly on herbaceous plants such as species of

the Harpophora–Gaeumannomyces complex, Microdochium or

Periconia. e second subgroup is formed by PAC, which occur

preferentially in woody plant roots. PAC are rare or absent in

plant roots from arable soils or pastures. Antagonism with spe-

cies of the Harpophora–Gaeumannomyces complex and/or other

microorganisms could be the reason. Harpophora species were

shown to confer induced resistance (cross-protection) against

closely related species or varieties in agricultural plants, espe-

cially cereals. Similarly, PAC were shown to protect forest trees

in a similar way, for example, against oomycetous root patho-

gens. e system of induced resistance is expected to be even

more balanced in undisturbed forest ecosystems than in agri-

cultural systems because the microbial community in the rhi-

zosphere and in the roots was allowed to equilibrate for decades

if not centuries. e study of these systems is hampered by the

high genotypic variability of the organisms involved.

With the availability of many dierent molecular genetics

markers, it is now possible to identify and characterize species

and genets of PAC allowing experimentation with clearly dened

strains. Several strains are available from international culture

collections. e high variability of DSE and PAC also explains,

at least in part, the contradictory results obtained in endophyte–

plant interaction experiments. Whereas there are several exam-

ples of non-PAC DSE with benecial eects on plant growth, the

majority of PAC revealed no eect or only slightly positive eects.

More recent in vitro multi-strain experiments with dened PAC

strains indicate that PAC function along a continuum from neu-

tral to pathogenic. Plant growth promotion has not been observed.

However, though PAC are costly, they seem to provide control

of more serious pathogens and perhaps also herbivores. Future

experiments should be shied more toward natural conditions.

e genome of strain UAMH11012 of Phialocephala subalpina

was sequenced, and gene models are currently manually validated

and annotated. First estimates based on 10 Mbp manually vali-

dated gene models show that the Phialocephala subalpina genome

will include roughly 20,000 gene models. Special emphasis is given

to annotation of gene clusters related to secondary metabolites.

e availability of the annotated genome of Phialocephala subal-

pina will allow performing transcriptomic analysis of host–PAC

interactions and comparative genomic studies with ectomycor-

rhizal and pathogenic fungi in the near future. In addition, the

completely sequenced and annotated mitochondrial genome of

Phialocephala subalpina is already available (Duò et al. 2012).

Several mitochondrial loci proved to be suitable for species diag-

nosis in PAC and can be used for community studies.

We do not know the functions root endophytes had in the

past nor which functions they will have in the future. We only

know that nature is a dynamic system. What we see today is one

picture in the evening-lling lm entitled “Evolution,” but it is

fascinating to speculate about the next step.

References

Abadie J-C, Puttsepp U, Gebauer G, Faccio A, Bonfante P,

Selosse M-A. 2006. Cephalanthera longifolia (Neottieae,

Orchidaceae) is mixotrophic: A comparative study between

green and nonphotosynthetic individuals. Can J Bot

84:1462–1477.

Achatz B, von Rueden S, Andrade D etal. 2010. Root coloniza-

tion by Piriformospora indica enhances grain yield in barley

under diverse nutrient regimes by accelerating plant devel-

opment. Plant Soil 333:59–70.

Addy HD, Piercey MM, Currah RS. 2005. Microfungal endo-

phytes in roots. Can J Bot 83:1–13.

Ahlich K, Rigling D, Holdenrieder O, Sieber TN. 1998. Dark sep-

tate hyphomycetes in Swiss conifer forest soils surveyed

using Norway-spruce seedlings as bait. Soil Biol Biochem

30:1069–1075.

Ahlich K, Sieber TN. 1996. e profusion of dark septate endo-

phytic fungi in non-ectomycorrhizal ne roots of forest

trees and shrubs. New Phytol 132:259–270.

Ahlich-Schlegel K. 1997. Vorkommen und Charakterisierung

von dunklen, septierten Hyphomyceten (DSH) in

Gehölzwurzeln. PhD thesis, Zürich, Switzerland: ETH

Zürich.

Alberton O, Kuyper TW, Summerbell RC. 2010. Dark septate

root endophytic fungi increase growth of Scots pine seed-

lings under elevated CO

through enhanced nitrogen use

eciency. Plant Soil 328:459–470.

Allen MF, Allen EB. 1992. Mycorrhizae and plant community

development: Mechanisms and patterns. In e Fungal

Community, eds. GC Carroll, DT Wicklow, pp. 455–479.

New York: Marcel Dekker, Inc.

Allen EA, Hoch HC, Steadman JR, Stavely RJ. 1991. In uence of leaf

surface features on spore deposition and the epiphytic growth

of phytopathogenic fungi. In Microbial Ecology of Leaves, eds.

JH Andrews, SS Hirano, pp. 87–110. New York: Springer.

Armstrong GM, Armstrong JK. 1981. Formae speciales and races

of Fusarium oxysporum causing wilt diseases. In Fusarium:

Diseases, Biology, and Taxonomy, eds. PE Nelson, TA

Tousson, RJ Cook, pp. 391–399. University Park, PA: e

Pennsylvania State University Press.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-39Fungal Root Endophytes

von Arx JA. 1967. Pilzkunde—Ein kurzer Abriss der Mykologie

unter besonderer Berücksichtigung der Pilze in Reinkultur.

Vaduz, Fürstentum Liechtenstein: J. Cramer.

Athman SY, Dubois T, Viljoen A etal. 2006. In vitro antago-

nism of endophytic Fusarium oxysporum isolates against

the burrowing nematode Radopholus similis. Nematology

8:627–636.

Aveskamp MM, Verkley GJM, de Gruyter J etal. 2009. DNA phy-

logeny reveals polyphyly of Phoma section Peyronellaea

and multiple taxonomic novelties. Mycologia 101:363–382.

Azevedo MD, Welty RE. 1995. A study of the fungal endophyte

Acremonium coenophialum in the roots of tall fescue seed-

lings. Mycologia 87:289–297.

Baas-Becking LGM. 1934. Geobiologie of inleiding tot de milieu-

kunde. Den Haag, the Netherlands: W.P. van Stockum and

Zoon.

Bachmann S. 2010. Zur Ausbreitungsbiologie von endo-

phytischen Wurzelpilzen des Phialocephala fortinii s.l.—

Acephala applanata Artenkomplexes (PAC). BSc esis,

Zürich, Switzerland: ETH Zürich.

Bagyalakshmi G, Muthukumar T, Sathiyadash K, Muniappan V.

2010. Mycorrhizal and dark septate fungal associations in

shola species of Western Ghats, southern India. Mycoscience

51:44–52.

Barrow JR. 2003. Atypical morphology of dark septate fungal root

endophytes of Bouteloua in arid southwestern USA range-

lands. Mycorrhiza 13:239–247.

Barrow JR, Osuna-Avila P, Reyes-Vera I. 2004. Fungal endo-

phytes intrinsically associated with micropropagated plants

regenerated from native Bouteloua eriopoda torr. and

Atriplex canescens (Pursh) Nutt. In Vitro Cell Dev Biol Plant

40:608–612.

Bartholdy BA, Berreck M, Haselwandter K. 2001. Hydroxamate

siderophore synthesis by Phialocephala fortinii, a typical

dark septate fungal root endophyte. BioMetals 14:33–42.

Bayman P, Lebron LL, Tremblay RL, Lodge DJ. 1997. Variation

in endophytic fungi from roots and leaves of Lepanthes

(Orchidaceae). New Phytol 135:143–149.

Bazin MJ, Markham P, Scott EM, Lynch JM. 1990. Population

dynamics and rhizosphere interactions. In e Rhizosphere,

ed. JM Lynch, pp. 99–127. Chichester, UK: John Wiley &

Sons.

Beauchamp VB, Stromberg JC, Stutz JC. 2005. Interactions

between Tamarix ramosissima (saltcedar), Populus fre-

montii (cottonwood), and mycorrhizal fungi: Eects on

seedling growth and plant species coexistence. Plant Soil

275:221–231.

Berch SM, Roth AL. 1993. Ectomycorrhizae and growth of

Douglas r seedlings preinoculated with Rhizopogon vini-

color and outplanted on eastern Vancouver Island. Can J For

Res 23:1711–1715.

Bills GF. 1996. Isolation and analysis of endophytic fungal com-

munities from woody plants. In Endophytic Fungi in Grasses

and Woody Plants, eds. SC Redlin, LM Carris, pp. 31–65.

St. Paul, MN: APS Press.

Blaschke H. 1991. Distribution, mycorrhizal infection, and struc-

ture of roots of calcicole oral elements at treeline, Bavarian

Alps, Germany. Arct Alp Res 23:444–450.

Bledsoe C, Klein P, Bliss LC. 1990. A survey of mycorrhizal plants

on Truelove Lowland, Devon Island, N. W. T., Canada. Can

J Bot 68:1848–1856.

Bloomberg WJ. 1966. e occurrence of endophytic fungi in

Douglas-r seedlings and seed. Can J Bot 44:413–420.

Bowen GD, Rovira AD. 1976. Microbial colonization of plant

roots. Annu Rev Phytopathol 14:121–144.

Brenn N, Menkis A, Grünig CR, Sieber TN, Holdenrieder O.

2008. Community structure of Phialocephala fortinii s. lat.

in European tree nurseries, and assessment of the poten-

tial of the seedlings as dissemination vehicles. Mycol Res

112:650–662.

Brundrett M. 2004. Diversity and classication of mycorrhizal

associations. Biol Rev 79:473–495.

Brundrett MC. 2009. Mycorrhizal associations and other means

of nutrition of vascular plants: Understanding the global

diversity of host plants by resolving con icting informa-

tion and developing reliable means of diagnosis. Plant Soil

320:37–77.

Burri K, Graf F, Böll A. 2009. Revegetation measures improve

soil aggregate stability: A case study of a landslide area in

Central Switzerland. For Snow Landsc Res 82:45–60.

Cain RF. 1952. Studies of fungi imperfecti. I. Phialophora. Can J

Bot 30:338–343.

Caldwell BA, Jumpponen A, Trappe JM. 2000. Utilization of

major detrital substrates by dark-septate, root endophytes.

Mycologia 92:230–232.

Cannon PF, Hawksworth DL. 1995. e diversity of fungi asso-

ciated with vascular plants: e known, the unknown and

the need to bridge the knowledge gap. Adv Plant Pathol

11:277–302.

Chambers SM, Curlevski NJA, Cairney JWG. 2008. Ericoid

mycorrhizal fungi are common root inhabitants of non-

Ericaceae plants in a south-eastern Australian sclerophyll

forest. FEMS Microbiol Ecol 65:263–270.

Chanway CP. 1996. Endophytes: ey’re not just fungi! Can J Bot

74:321–322.

Chen XM, Dong HL, Hu KX, Sun ZR, Chen JA, Guo SX. 2010a.

Diversity and antimicrobial and plant-growth-promoting

activities of endophytic fungi in Dendrobium loddigesii

Rolfe. J Plant Growth Regul 29:328–337.

Chen JA, Dong HL, Meng ZX, Guo SX. 2010b. Cadophora malo-

rum and Cryptosporiopsis ericae isolated from medicinal

plants of the Orchidaceae in China. Mycotaxon 112:457–461.

Christie P, Nicolson TH. 1983. Are mycorrhizas absent from the

antarctic? Trans Br Mycol Soc 80:557–560.

Clay K. 1988. Fungal endophytes of grasses: A defensive mutual-

ism between plants and fungi. Ecology 69:10–16.

Cother EJ, Gilbert RL. 1994. e endophytic myco ora of blad-

der saltbush (Atriplex vesicaria Hew. ex Benth.) and its pos-

sible role in the plant’s periodic decline. Proc Linn Soc NSW

114:149–169.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-40 Root–Rhizosphere Interactions

Courtois H. 1990a. Die Pilz ora im Kronenbereich und in der

Rhizosphäre von Fichten (P. abies Karst.) und ihre Bedeutung

zur Interpretation von “Waldsterbe”-Symptomen. Angew

Bot 64:381–392.

Courtois H. 1990b. Endophytische Mikropilze in

Fichtenfeinwurzeln. Zur Grundbelastung des Baumsterbens.

Allg Forst- J-Ztg 161:189–198.

Courtois H, Ruschen G. 1987. Haben wurzelinzierende

Mikropilze Ein uss auf das “Waldsterben”? Allg Forst- J-Ztg

158:189–194.

Crous PW, Petrini O, Marais GF, Pretorius ZA, Rehder F. 1995.

Occurrence of fungal endophytes in cultivars of Triticum

aestivum in South Africa. Mycoscience 36:105–111.

Crous PW, Schubert K, Braun U et al. 2007. Opportunistic,

human-pathogenic species in the Herpotrichiellaceae are

phenotypically similar to saprobic or phytopathogenic spe-

cies in the Venturiaceae. Studies Mycol 53:185–234.

Currah RS, Hambleton S, Smreciu A. 1988. Mycorrhizae

and mycorrhizal fungi of Calypso bulbosa. Am J Bot

75:739–752.

Currah RS, Sherburne R. 1992. Septal ultrastructure of some fun-

gal endophytes from boreal orchid mycorrhizas. Mycol Res

96:583–587.

Currah RS, Sigler L, Hambleton S. 1987. New records and new

taxa of fungi from the mycorrhizae of terrestrial orchids of

Alberta. Can J Bot 65:2473–2482.

Currah RS, Smreciu AE, Hambleton S. 1990. Mycorrhizae and

mycorrhizal fungi of boreal species of Platanthera and

Coeloglossum (Orchidaceae). Can J Bot 68:1171–1181.

Currah RS, Tsuneda A. 1993. Vegetative and reproductive

morphology of Phialocephala fortinii (Hyphomycetes,

Mycelium radicis atrovirens) in culture. Trans Mycol Soc Jpn

34:345–356.

Currah RS, Tsuneda A, Murakami S. 1993. Morphology and

ecology of Phialocephala fortinii in roots of Rhododendron

brachycarpum. Can J Bot 71:1639–1644.

Currah RS, Van Dyk M. 1986. A survey of some perennial vascu-

lar plant species native to Alberta for occurrence of mycor-

rhizal fungi. Can Field-Nat 100:330–342.

Currah RS, Zelmer C. 1992. A key and notes for the genera of

fungi mycorrhizal with orchids and a new species in the

genus Epulorhiza. Rep Tottori Mycol Inst 30:43–59.

Dababat AE-FA, Selim ME, Saleh AA, Sikora RA. 2008. In uence

of Fusarium wilt resistant tomato cultivars on root coloni-

zation of the mutualistic endophyte Fusarium oxysporum

strain 162 and its biological control ecacy toward the

root-knot nematode Meloidogyne incognita. J Plant Dis Prot

115:273–278.

Dababat AE-FA, Sikora RA. 2007. Induced resistance by the

mutualistic endophyte, Fusarium oxysporum strain 162,

toward Meloidogyne incognita on tomato. Biocontrol Sci

Technol 17:969–975.

Dahm H. 1987. Cellulolytic and pectolytic activity of nonmy-

corrhizal fungi associated with roots of forest trees. Acta

Microbiol Pol 36:317–324.

Dahm H, Strzelczyk E, Michniewicz M. 1987. Eect of pH, tem-

perature and light on the pathogenicity of Cylindrocarpon

destructans to pine seedlings in associative cultures with

bacteria and actinomycetes. Eur J For Pathol 17:141–148.

Danielson RM, Visser S. 1989. Eects of forest soil acidication

on ectomycorrhizal and vesicular-arbuscular mycorrhizal

development. New Phytol 112:41–47.

Danielson RM, Visser S. 1990. e mycorrhizal and nodulation

status of container-grown trees and shrubs reared in com-

mercial nurseries. Can J For Res 20:609–614.

Davis D. 1967. Cross-protection in Fusarium wilt diseases.

Phytopathology 57:311–314.

Day MJ, Gibas CFC, Fujimura KE, Egger KN, Currah RS. 2006.

Monodictys arctica, a new hyphomycete from the roots

of Saxifraga oppositifolia collected in the Canadian High

Arctic. Mycotaxon 98:261–272.

De Bary A. 1866. Morphologie und Physiologie der Pilze, Flechten

und Myxomyceten. Leipzig, Germany: Engelmann.

De la Bastide PY, Kendrick B. 1990. e in vitro eects of beno-

myl on disease tolerance, ectomycorrhiza formation, and

growth of white pine (Pinus strobus) seedlings. Can J Bot

68:444–448.

De Marins JF, Carrenho R, omaz SM. 2009. Occurrence and

coexistence of arbuscular mycorrhizal fungi and dark sep-

tate fungi in aquatic macrophytes in a tropical river- ood-

plain system. Aquat Bot 91:13–19.

Deacon JW. 1981. Ecological relationships with other fungi:

Competitors and hyperparasites. In Biology and Control of

Take-All, eds. MJC Asher, PJ Shipton, pp. 75–101. London,

U.K.: Academic Press.

Deacon JW. 1987. Programmed cortical senescence: A basis for

understanding root infection. In Fungal Infection of Plants,

eds. GF Pegg, PG Ayres, pp. 285–297. Cambridge, U.K.:

Cambridge University Press.

Deacon JW, Scott DB. 1983. Phialophora zeicola sp. nov., and its

role in the root-rot stalk-rot complex of maize. Trans Br

Mycol Soc 81:247–262.

Dearnaley JDW, Le Brocque AF. 2006. Molecular identication of

the primary root fungal endophytes of Dipodium hamilto-

nianum (Orchidaceae). Aust J Bot 54:487–491.

Deram A, Languereau-Leman F, Howsam M, Petit D, Van

Haluwyn C. 2008. Seasonal patterns of cadmium accu-

mulation in Arrhenatherum elatius (Poaceae): In uence of

mycorrhizal and endophytic fungal colonisation. Soil Biol

Biochem 40:845–848.

Deshmukh SD, Kogel KH. 2007. Piriformospora indica protects

barley from root rot caused by Fusarium graminearum.

J Plant Dis Prot 114:263–268.

Dolinar N, Gaberscik A. 2010. Mycorrhizal colonization and

growth of Phragmites australis in an intermittent wetland.

Aquat Bot 93:93–98.

Domanski S, Kowalski T. 1987. Fungi occurring on forests injured

by air pollutants in the Upper Silesia and Cracow industrial

regions. X. Myco ora of dying young trees of Alnus incana.

Eur J For Pathol 17:337–348.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-41Fungal Root Endophytes

Domsch KH, Gams W, Anderson TH. 1980. Compendium of Soil

Fungi. London, U.K.: Academic Press.

Dong Z, Canny MJ, McCully ME et al. 1994. A nitrogen-

xing endophyte of sugarcane stems. Plant Physiol

105:1139–1147.

Duda B, Sierota ZH. 1987. Survival of Scots pine seedlings aer

biological and chemical control of damping-o in plastic

greenhouses. Eur J For Pathol 17:110–117.

Duddrige JA. 1985. A comparative ultrastructural analysis of the

host-fungus interface in mycorrhizal and parasitic asso-

ciations. In Developmental Biology of Higher Fungi, eds. D

Moore, LA Casselton, DA Wood, JC Frankland, pp. 141–173.

Cambridge, U.K.: Cambridge University Press.

Dugassa-Gobena D, Raps A, Vidal S. 1998. In uence of fungal

endophytes on allelochemicals of their host plants and

the behaviour of insects. Med Fac Landbouww Univ Gent

63:333–337.

Duò A, Bruggmann R, Zoller S, Grünig CR. 2012. Mitochondrion

genome evolution in species belonging to the Phialocephala

fortinii s.l.—Acephala applanata species complex. BMC

Genomics 13:166.

Egger KN, Danielson RM, Fortin JA. 1991. Taxonomy and popu-

lation structure of E-strain mycorrhizal fungi inferred from

ribosomal and mitochondrial DNA polymorphisms. Mycol

Res 95:866–872.

El-Nashaar HM, Moore LW, George RA. 1986. Enzyme-linked

immunosorbent assay quantification of initial infec-

tion of wheat by Gaeumannomyces graminis var. tritici

as moderated by biocontrol agents. Phytopathology

76:1319–1322.

Ellis MB. 1976. More Dematiaceous Hyphomycetes. Kew, Surrey,

U.K.: CAB International Mycological Institute (IMI).

Fernandez N, Messuti MI, Fontenla S. 2008. Arbuscular mycor-

rhizas and dark septate fungi in Lycopodium paniculatum

(Lycopodiaceae) and Equisetum bogotense (Equisetaceae)

in a valdivian temperate forest of Patagonia, Argentina. Am

Fern J 98:117–127.

Fernando AA, Currah RS. 1996. A comparative study of the

eects of the root endophytes Leptodontidium orchidi-

cola and Phialocephala fortinii (fungi imperfecti) on the

growth of some subalpine plants in culture. Can J Bot

74:1071–1078.

Fisher PJ, Graf F, Petrini LE, Sutton BC, Wookey PA. 1995a.

Fungal endophytes of Dryas octopetala from a high arc-

tic polar semidesert and from the Swiss Alps. Mycologia

87:319–323.

Fisher PJ, Petrini O. 1992. Fungal saprobes and pathogens as endo-

phytes of rice (Oryza sativa L.). New Phytol 120:137–143.

Fisher PJ, Petrini O, Petrini LE. 1991a. Endophytic Ascomycetes

and Deuteromycetes in roots of Pinus sylvestris. Nova

Hedwigia 52:11–15.

Fisher PJ, Petrini LE, Sutton BC, Petrini O. 1995b. A study of fun-

gal endophytes in leaves, stems and roots of Gynoxis oleifo-

lia Muchler (Compositae) from Ecuador. Nova Hedwigia

60:589–594.

Fisher PJ, Petrini O, Webster J. 1991b. Aquatic hyphomycetes and

other fungi in living aquatic and terrestrial roots of Alnus

glutinosa. Mycol Res 95:543–547.

Forbrig R. 1987. Anatomische und histologische Untersuchungen

an pilzinzierten Fichtenkeimlingen (Picea abies Karst.).

Allg Forst- J-ztg 158:222–229.

Forbrig R. 1989. Anatomische und biologische Untersuchungen

an pilzinzierten Fichtenkeimlingen (Picea abies Karst.). II.

Allg Forst- J-ztg 160:137–144.

Foster RC. 1986. e ultrastructure of the rhizoplane and rhizo-

sphere. Annu Rev Phytopathol 24:211–234.

Foster RC, Rovira AD, Cock TW. 1983. Ultrastructure of the Root-

Soil Interface. St. Paul, MN: APS Press.

Freeman S, Rodriguez RJ. 1993. Genetic conversion of a fungal

plant pathogen to a nonpathogenic, endophytic mutualist.

Science 260:75–78.

Freeman J, Ward E. 2004. Gaeumannomyces graminis, the take-all

fungus and its relatives. Mol Plant Pathol 5:235–252.

Galaaen R, Venn K. 1979. Pythium sylvaticum Campbell &

Hendrix and other fungi associated with root dieback of 2/0

seedlings of Picea abies (L.) Karst. in Norway. Rep Norw For

Res Inst 34:265–280.

Galamay TO, Yamauchi A, Kono Y, Hioki M. 1992. Specic colo-

nization of the hypodermis of sorghum roots by an endo-

phyte, Polymyxa sp. Soil Sci Plant Nutr 38:573–578.

Gams W. 1963. Mycelium radicis atrovirens in forest soils,

isolation from soil microhabitats and identication.

In Soil Organisms, eds. J Dockson, J van der Dri,

pp. 176–182. Amsterdam, the Netherlands: North

Holland Publications.

Gams W. 2000. Phialophora and some similar morphologically

little-dierentiated anamorphs of divergent ascomycetes.

Stud Mycol 45:187–199.

Garcia-Guzman G, Burdon JJ, Nicholls AO. 1996. Eects of the

systemic ower infecting-smut Ustilago bullata on the

growth and competitive ability of the grass Bromus catharti-

cus. J Ecol 84:657–665.

Garrett SD. 1981. Soil Fungi and Soil Fertility, 2nd edn. Oxford,

U.K.: Pergamon Press.

Gasoni L, Stegman De Gurnkel B. 1997. e endophyte

Cladorrhinum foecundissimum in cotton roots: Phosphorus

uptake and host growth. Mycol Res 101:867–870.

Gasoni L, Stegman de Gurnkel B. 2009. Biocontrol of Rhizoctonia

solani by the endophytic fungus Cladorrhinum foecundissi-

mum in cotton plants. Aust Plant Pathol 38:389–391.

Gessler C, Kuc J. 1982. Induction of resistance to Fusarium wilt

in cucumber by root and foliar pathogens. Phytopathology

72:1439–1441.

Gezgin Y, Eltem R. 2009. Diversity of endophytic fungi from vari-

ous Aegean and Mediterranean orchids (saleps). Turk J Bot

33:439–445.

Girlanda M, Selosse MA, Cafasso D etal. 2006. Inecient photo-

synthesis in the Mediterranean orchid Limodorum aborti-

vum is mirrored by specic association to ectomycorrhizal

Russulaceae. Mol Ecol 15:491–504.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-42 Root–Rhizosphere Interactions

Görke C. 1998. Mykozönosen von Wurzeln und Stamm von

Jungbäumen unterschiedlicher Bestandsbegründungen.

Biblio Mycol 173:1–462.

Green LE, Porras-Alfaro A, Sinsabaugh RL. 2008. Translocation

of nitrogen and carbon integrates biotic crust and grass

production in desert grassland. J Ecol 96:1076–1085.

Grönberg H, Kaparakis G, Sen R. 2006. Binucleate Rhizoctonia

(Ceratorhiza spp.) as non-mycorrhizal endophytes alter

Pinus sylvestris L. seedling root architecture and aect

growth of rooted cuttings. Scan J For Res 21:450–457.

Grünig CR. 2004. Population biology of the tree-root endophyte

Phialocephala fortinii. PhD thesis no. 15313, Zürich,

Switzerland: ETH Zürich, http://e-collection.ethbib.ethz.

ch/cgi-bin/show.pl?type = diss&nr = 15313

Grünig CR, Brunner PC, Duò A, Sieber TN. 2007. Suitability

of methods for species recognition in the Phialocephala

fortinii–Acephala applanata species complex using DNA

analysis. Fung Genet Biol 44:773–788.

Grünig CR, Duò A, Sieber TN. 2006. Population genetic analysis

of Phialocephala fortinii s.l. and Acephala applanata in two

undisturbed forests in Switzerland and evidence for new

cryptic species. Fung Genet Biol 43:410–421.

Grünig CR, Duò A, Sieber TN, Holdenrieder O. 2008a.

Assignment of species rank to six reproductively isolated

cryptic species of the Phialocephala fortinii s. l.-Acephala

applanata species complex. Mycologia 100:47–67.

Grünig CR, McDonald BA, Sieber TN, Rogers SO, HoldenriederO.

2004. Evidence for subdivision of the root-endophyte

Phialocephala fortinii into cryptic species and recombina-

tion within species. Fung Genet Biol 41:676–687.

Grünig CR, Sieber TN. 2005. Molecular and phenotypic descrip-

tion of the widespread root symbiont Acephala applanata

gen. et sp. nov., formerly known as “Dark Septate Endophyte

Type 1.” Mycologia 97:628–640.

Grünig CR, Sieber TN, Holdenrieder O. 2001. Characterisation

of dark septate endophytic fungi (DSE) using inter-sim-

ple-sequence-repeat-anchored polymerase chain reaction

(ISSR-PCR) amplication. Mycol Res 105:24–32.

Grünig CR, Queloz V, Duo A, Sieber TN. 2009. Phylogeny of

Phaeomollisia piceae gen. sp. nov.: A dark, septate, conifer-

needle endophyte and its relationships to Phialocephala and

Acephala. Mycol Res 113:207–221.

Grünig CR, Queloz V, Sieber TN. 2011. Structure of diversity

in dark septate endophytes: From species to genes. In

Endophytes of Forest Trees: Biology and Applications, eds.

AM Pirttilä, AC Frank, pp. 3–30. Forestry Sciences 80,

Berlin, Germany: Springer Science & Business Media.

Grünig CR, Queloz V, Sieber TN, Holdenrieder O. 2008b. Dark septate

endophytes (DSE) of the Phialocephala fortinii s.l.—Acephala

applanata species complex in tree roots: Classication, popula-

tion biology, and ecology. Botany 86:1355–1369.

Gutteridge RJ, Jenkyn JF, Bateman GL. 2007. e potential of

non-pathogenic Gaeumannomyces spp., occurring natu-

rally or introduced into wheat crops or preceding crops, for

controlling take-all in wheat. Ann Appl Biol 150:53–64.

Hallmann J, Sikora RA. 1994. Occurrence of plant parasitic nema-

todes and non-pathogenic species of Fusarium in tomato

plants in Kenya and their role as mutualistic synergists for

biological control of root-knot nematodes. Int J Pest Manage

40:321–325.

Hallmann J, Sikora RA. 1996. Toxicity of fungal endophyte

secondary metabolites to plant parasitic nematodes and

soil-borne plant pathogenic fungi. Eur J Plant Pathol

102:155–162.

Halmschlager E, Kowalski T. 2004. e mycobiota in nonmy-

corrhizal roots of healthy and declining oaks. Can J Bot

82:1446–1458.

Hambleton S, Currah RS. 1997. Fungal endophytes from the roots

of alpine and boreal Ericaceae. Can J Bot 75:1570–1581.

Hambleton S, Sigler L. 2005. Meliniomyces, a new anamorph

genus for root-associated fungi with phylogenetic ani-

ties to Rhizoscyphus ericae (Hymenoscyphus ericae),

Leotiomycetes. Stud Mycol 53:1–27.

Hambleton S, Huhtinen S, Currah RS. 1999. Hymenoscyphus

ericae: A new record from western Canada. Mycological

Research 103:1391–1397.

Hampton R, Ball E, De Boer S. 1990. Serological Methods. St. Paul,

MN: APS Press.

Harney SK, Rogers SO, Wang CJK. 1997. Molecular charac-

terization of dematiaceous root endophytes. Mycol Res

101:1397–1404.

Harvais G, Hadley G. 1967. e relation between host and endo-

phyte in orchid mycorrhiza. New Phytol 66:205–215.

Haselwandter K, Read DJ. 1982. e signicance of a root-fungus

association in two Carex species of high-alpine plant com-

munities. Oecologia 53:352–354.

Haug I, Weber G, Oberwinkler F. 1988. Intracellular infection

by fungi in mycorrhizae of damaged spruce trees. Eur J For

Pathol 18:112–120.

Hennon PE, Shaw III CG, Hansen EM. 1990. Symptoms and fun-

gal associations of declining Chamaecyparis nootkatensis in

Southeast Alaska. Plant Dis 74:267–273.

Herrera J, Khidir HH, Eudy DM, Porras-Alfaro A, Natvig DO,

Sinsabaugh RL. 2010. Shiing fungal endophyte commu-

nities colonize Bouteloua gracilis: Eect of host tissue and

geographical distribution. Mycologia 102:1012–1026.

Heslin MC, Blasius D, McElhinney C, Mitchell DT. 1992.

Mycorrhizal and associated fungi of Sitka spruce in Irish

forest mixed stands. Eur J For Pathol 22:46–57.

Hodson E, Shahid F, Basinger J, Kaminskyj S. 2009. Fungal endo-

rhizal associates of Equisetum species from Western and

arctic Canada. Mycol Prog 8:19–27.

Hol WHG, de la Pena E, Moens M, Cook R. 2007. Interaction

between a fungal endophyte and root herbivores of

Ammophila arenaria. Basic Appl Ecol 8:500–509.

Holdenrieder O. 1989. Endophytes and rhizoplane fungi of

Norway spruce. In Proceedings of the Seventh International

Conference on Root and Butt Rots, ed. DJ Morrison,

pp. 531–545. August 9–16, 1988. Victoria, British Columbia,

Canada: Forestry Canada, Pacic Forestry Centre.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-43Fungal Root Endophytes

Holdenrieder O, Sieber TN. 1992. Fungal associations of serially

washed healthy non-mycorrhizal roots of Picea abies. Mycol

Res 96:151–156.

Horton TR, Cazares E, Bruns TD. 1998. Ectomycorrhizal, vesic-

ular-arbuscular and dark septate fungal colonization of

bishop pine (Pinus muricata) seedlings in the rst 5 months

of growth aer wildre. Mycorrhiza 8:11–18.

Hou X-Q, Guo S-X. 2009. Interaction between a dark septate

endophytic isolate from Dendrobium sp. and roots of D.

nobile seedlings. J Integr Plant Biol 51:374–381.

Hutton BJ, Dixon KW, Sivasithamparam K. 1994. Ericoid endo-

phytes of Western Australian heaths (Epacridaceae). New

Phytol 127:557–566.

Iqbal SH, Firdaus EB, Yousaf N. 1995. Freshwater hyphomycete

communities in a canal: 1. Endophytic hyphomycetes of

submerged roots of trees sheltering a canal bank. Can J Bot

73:538–543.

Johnson L. 2008. Iron and siderophores in fungal-host interac-

tions. Mycol Res 112:170–183.

Jumpponen A, Jones KL. 2009. Massively parallel 454 sequenc-

ing indicates hyperdiverse fungal communities in tem-

perate Quercus macrocarpa phyllosphere. New Phytol

184:438–448.

Jumpponen A, Mattson KG, Trappe JM. 1998. Mycorrhizal func-

tioning of Phialocephala fortinii with Pinus contorta on

glacier forefront soil: Interactions with soil nitrogen and

organic matter. Mycorrhiza 7:261–265.

Jumpponen A, Trappe JM. 1998a. Dark septate endophytes: A

review of facultative biotrophic root-colonizing fungi. New

Phytol 140:295–310.

Jumpponen A, Trappe JM. 1998b. Performance of Pinus contorta

inoculated with two strains of root endophytic fungus,

Phialocephala fortinii: Eects of synthesis system and glu-

cose concentration. Can J Bot 76:1205–1213.

Kai W, Zhao ZW. 2006. Occurrence of arbuscular mycorrhizas

and dark septate endophytes in hydrophytes from lakes and

streams in southwest China. Int Rev Hydrobiol 91:29–37.

Kandalepas D, Stevens KJ, Shaer GP, Platt WJ. 2010. How abun-

dant are root-colonizing fungi in Southeastern Louisiana’s

degraded marshes? Wetlands 30:189–199.

Kaparakis G, Sen R. 2006. Binucleate Rhizoctonia (Ceratorhiza

spp.) induce adventitious root formation in hypocotyl cut-

tings of Pinus sylvestris L. Scan J For Res 21:444–449.

Kattner D. 1992a. Der Ein uss von Trockenstress auf die

Besiedlung von Fichtenfeinwurzeln (Picea abies Karst.) durch

Trichoderma viride und andere endophytische Mikropilze.

Forstwissenschaliches Centralblatt 111:383–389.

Kattner D. 1992b. Langzeitwirkung einer Calciumdüngung auf

die Besiedlung von Fichtenwurzeln durch Mikropilze. Allg

Forst- J-ztg 163:138–142.

Kattner D, Schönhar S. 1990. Untersuchungen über das

Vorkommen mikroskopischer Pilze in Feinwurzeln

optisch gesunder Fichten (Picea abies Karst.) auf verschie-

denen Standorten. Mitteilungen des Vereins Forstlicher

Standortskunde und Forstpanzenzüchtung 35:39–43.

Kavroulakis N, Ntougias S, Zervakis GI, Ehaliotis C, HaralampidisK,

Papadopoulou KK. 2007. Role of ethylene in the protection

of tomato plants against soil-borne fungal pathogens con-

ferred by an endophytic Fusarium solani strain. J Exp Bot

58:3853–3864.

Kernaghan G, Berch S, Carter R. 1995. Eect of urea fertilization

on ectomycorrhizae of 20-year-old Tsuga heterophylla. Can

J For Res 25:891–901.

Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO,

Sinsabaugh RL. 2010. A general suite of fungal endophytes

dominate the roots of two dominant grasses in a semiarid

grassland. J Arid Environ 74:35–42.

Kim HY, Choi GJ, Lee HB etal. 2007. Some fungal endophytes

from vegetable crops and their anti-oomycete activities

against tomato late blight. Lett Appl Microbiol 44:332–337.

Kirk JJ, Deacon JW. 1987. Control of the take-all fungus by

Microdochium bolleyi, and interactions involving M. bolleyi,

Phialophora graminicola and Periconia macrospinosa on

cereal roots. Plant Soil 98:231–237.

Kjoller R, Olsrud M, Michelsen A. 2010. Co-existing ericaceous

plant species in a subarctic mire community share fungal

root endophytes. Fungal Ecol 3:205–214.

Kohn LM, Stasovski E. 1990. e mycorrhizal status of plants at

Alexandra Fiord, Ellesmere Island, Canada, a high arctic

site. Mycologia 82:23–35.

Kowalski S. 1982a. Role of mycorrhiza and soil fungi in natural

regeneration of r (Abies alba Mill.) in Polish Carpathians

and Sudetes. Eur J For Pathol 12:107–112.

Kowalski T. 1982b. Vorkommen von Pilzen in durch

Luverunreinigung geschädigten Wäldern im

Oberschlesischen und Krakauer Industriegebiet. VIII.

Myko ora von Larix decidua an einem Standort mit mit-

tlerer Immissionsbelastung. Eur J For Pathol 12:262–272.

Kowalski T. 1983. Fungi occurring in forest injured by air-pollutants

in the upper Silesi and Cracow industrial regions. 9. Myco ora

on Quercus robur L and Quercus rubra L. located in a zone

with medium-high air-pollution damage. Eur J For Pathol

13:46–59.

Kowalski T. 1993. Fungi in living symptomless needles of Pinus

sylvestris with respect to some observed disease processes.

JPhytopathol 139:129–145.

Kowalski T, Bartnik C. 1995. Cryptosporiopsis radicicola sp. nov.

from roots of Quercus robur. Mycol Res 99:663–666.

Kowalski T, Halmschlager E, Schrader K. 1998. Cryptosporiopsis

melanigena sp. nov., a root-inhabiting fungus of Quercus

robur and Q. petraea. Mycol Res 102:347–354.

Lehnert M, Kottke I, Setaro S, Pazmino LF, Pablo Suarez J,

Kessler M. 2009. Mycorrhizal associations in ferns from

Southern Ecuador. Am Fern J 99:292–306.

Lemaire JM, Ponchet J. 1963. Phialophora radicicola Cain, forme

conidienne du Linocarpon cariceti B. et Br. Comptes Rendus

Hebdomadaires des Séances de l’Académie d’Agriculture de

France 49:1067–1069.

Levisohn I. 1954. Test for the pseudomycorrhizal group of soil

fungi. Nature 174:408–409.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-44 Root–Rhizosphere Interactions

Li A-R, Guan K-Y. 2007. Mycorrhizal and dark septate endophytic

fungi of Pedicularis species from northwest of Yunnan

Province, China. Mycorrhiza 17:103–109.

Li LF, Yang A, Zhao ZW. 2005. Seasonality of arbuscular mycor-

rhizal symbiosis and dark septate endophytes in a grassland

site in southwest China. FEMS Microbiol Ecol 54:367–373.

Lihnell D. 1939. Untersuchungen über die Mykorrhizen und

die Wurzelpilze von Juniperus communis. Symb Bot Upsal

3:1–141.

LoBuglio KF, Wilcox HE. 1988. Growth and survival of ectomy-

corrhizal and ectendomycorrhizal seedlings of Pinus resi-

nosa on iron tailings. Can J Bot 66:55–60.

Lugo MA, Molina MG, Crespo EM. 2009. Arbuscular mycorrhi-

zas and dark septate endophytes in bromeliads from South

American arid environment. Symbiosis 47:17–21.

Lv Y-L, Zhang F-S, Chen J etal. 2010. Diversity and antimicrobial

activity of endophytic fungi associated with the alpine plant

Saussurea involucrata. Biol Pharm Bull 33:1300–1306.

Lyr H, Kluge E. 1968. Zusammenhänge zwischen Pathogenität,

Enzym- und Toxinproduktion bei Cylindrocarpon radici-

cola. Phytopathol Z 62:220–231.

Macia-Vicente JG, Jansson H-B, Mendgen K, Lopez-Llorca LV.

2008. Colonization of barley roots by endophytic fungi

and their reduction of take-all caused by Gaeumannomyces

graminis var. tritici. Can J Microbiol 54:600–609.

Malinowski DP, Alloush GA, Belesky DP. 1998. Evidence for chem-

ical changes on the root surface of tall fescue in response to

infection with the fungal endophyte Neotyphodium coeno-

phialum. Plant Soil 205:1–12.

Malinowski DP, Belesky DP. 1999. Neotyphodium coenophi-

alum-endophyte infection aects the ability of tall fes-

cue to use sparingly available phosphorus. J Plant Nutr

22:835–853.

Mandyam K, Jumpponen A. 2005. Seeking the elusive function

of the root-colonising dark septate endophytic fungi. Stud

Mycol 53:173–189.

Mandyam K, Loughin T, Jumpponen A. 2010. Isolation and

morphological and metabolic characterization of common

endophytes in annually burned tallgrass prairie. Mycologia

102:813–821.

Manka K. 1960. O grzybie korzenowym Mycelium radicis atrovi-

rens Melin. Monogr Bot 10:147–158.

Manka K, Mroczkiewicz M. 1991. A contribution to Mycelium

radicis atrovirens Melin occurrence in scots pine (Pinus sil-

vestris L.) roots. Phytopathol Polonica 2:102–105.

Manka K, Przezbòrski A. 1978. Biologiczne zwalczanie zgorzeli

siewek sosny zwyczajnej za pomoca grzyba Mycelium radi-

cis atrovirens Melin. Zeszyty Problemowe Postepow Nauk

Rolniczych 213:173–180.

Manka K, Przezbòrski A. 1987. W kierunku biologicznej ochrony

siewek drzew lesnych przed pasozytnicza zgorzela. Sylwan

131:53–59.

Martos F, Dulormne M, Pailler T etal. 2009. Independent recruit-

ment of saprotrophic fungi as mycorrhizal partners by trop-

ical achlorophyllous orchids. New Phytol 184:668–681.

Matta A. 1989. Induced resistance to Fusarium wilt diseases.

In Vascular Wilt Diseases of Plants—Basic Studies and

Control, eds. EC Tjamos, CH Beckman, pp. 175–96. Berlin,

Geramny: Springer.

Matturi ST, Stenton H. 1964. Distribution and status in the soil

of Cylindrocarpon species. Trans Br Mycol Soc 47:577–587.

McGill BJ, Etienne RS, Gray JS etal. 2007. Species abundance

distributions: Moving beyond single prediction theories

to integration within an ecological framework. Ecol Lett

10:995–1015.

McKeen WE. 1952. Phialophora radicicola Cain, a corn rootrot

pathogen. Can J Bot 30:344–347.

Medina-Roldan E, Arredondo JT, Huber-Sannwald E, Chapa-

Vargas L, Olalde-Portugal V. 2008. Grazing eects on fungal

root symbionts and carbon and nitrogen storage in a short-

grass steppe in Central Mexico. J Arid Environ 72:546–556.

Melin E. 1923. Experimentelle Untersuchungen über die

Konstitution und Ökologie der Mykorrhizen von Pinus

sylvestris L. und Picea abies (L.) Karst. In Mykologische

Untersuchungen und Berichte 2, ed. R Flack, pp. 334–373.

Kassel, Germany: Druck und Verlag G. Gottheilt.

Melin E. 1924. Über den Ein uss der Wasserstoonenkonzentration

auf die Virulenz der Wurzelpilze von Kiefer und Fichte.

Botaniska Notiser1924:38–48.

Mendoza AR, Sikora RA. 2009. Biological control of Radopholus

similis in banana by combined application of the mutualistic

endophyte Fusarium oxysporum strain 162, the egg patho-

gen Paecilomyces lilacinus strain 251 and the antagonistic

bacteria Bacillus rmus. Biocontrol 54:263–272.

Menkis A. 2004. Ecology and molecular characterization of

dark septate fungi from roots, living stems, coarse and ne

woody debris. Mycol Res 108:965–973.

Menkis A, Vasiliauskas R, Taylor AFS, Stenstrom E, Stenlid J,

Finlay R. 2006. Fungi in decayed roots of conifer seedlings

in forest nurseries, aorested clear-cuts and abandoned

farmland. Plant Pathol 55:117–129.

Mikola P. 1988. Ectendomycorrhiza of conifers. Silva Fennica

22:19–27.

Miller JD, Sumarah MW, Adams GW. 2008. Eect of a rugulo-

sin-producing endophyte in Picea glauca on Choristoneura

fumiferana. J Chem Ecol 34:362–368.

Moll M, Vidal S. 1995. Ein uss des wurzelbürtigen Endophyten

Acremonium strictum Gams auf das Wirtswahlverhalten

und die Entwicklung von Trialeurodes vaporariorum

(Westwood) (Homoptera, Aleyrodidae) an Buschbohnen.

Mitteilungen der Deutschen Gesellscha für allgemeine und

angewandte Entomologie 10:445–448.

Money NP, Caesar-Tonat T-C, Frederick B, Henson JM. 1998.

Melanin synthesis is associated with changes in hyphopodial

turgor, permeability, and wall rigidity in Gaeumannomyces

graminis var. graminis. Fungal Genet Biol 24:240–251.

Münzenberger B, Bubner B, Wöllecke J etal. 2009. e ectomycor-

rhizal morphotype Pinirhiza sclerotia is formed by Acephala

macrosclerotiorum sp nov., a close relative of Phialocephala

fortinii. Mycorrhiza 19:481–492.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-45Fungal Root Endophytes

Murray DIL, Gadd GM. 1981. Preliminary studies on

Microdochium bolleyi with special reference to colonization

of barley. Trans Br Mycol Soc 76:397–403.

Narisawa K, Tokumasu S, Hashiba T. 1998. Suppression of club-

root formation in Chinese cabbage by the root endophytic

fungus, Heteroconium chaetospira. Plant Pathol 47:206–210.

Narisawa K, Usuki F, Hashiba T. 2004. Control of verticillium

yellows in Chinese cabbage by the dark septate endophytic

fungus LtVB3. Phytopathology 94:412–418.

Newell SY. 1992. Estimating fungal biomass and productiv-

ity in decomposing litter. In e Fungal Community, eds.

GC Carroll, DT Wicklow, pp. 521–561. New York: Marcel

Dekker, Inc.

Newell SY, Arsu TL, Fallon RD. 1988. Fundamental proce-

dures for determining ergosterol content of decaying plant

material by liquid chromatography. Appl Environ Microbiol

54:1876–1879.

Newsham KK. 1994. First record of intracellular sporulation by a

coelomycete fungus. Mycol Res 98:1390–1392.

Newsham KK. 1999. Phialophora graminicola, a dark septate fun-

gus, is a benecial associate of the grass Vulpia ciliata ssp.

ambigua. New Phytol 144:517–524.

Newsham KK, Upson R, Read DJ. 2009. Mycorrhizas and dark sep-

tate root endophytes in polar regions. Fungal Ecol 2:10–20.

O’Dell TE, Massicotte HB, Trappe JM. 1993. Root colonization

of Lupinus latifolius Agardh. and Pinus contorta Dougl. by

Phialocephala fortinii Wang & Wilcox. New Phytol 124:93–100.

O’Dell TE, Trappe JM. 1992. Root endophytes of lupin and

some other legumes in northwestern USA. New Phytol

122:479–485.

Oberholzer-Tschütscher B. 1982. Untersuchungen über endo-

phytische Pilze von Erica carnea L., Zürich, Switzerland:

Institute of Microbiology, Swiss Federal Institute of

Technology.

Oberwinkler F. 1964. Intrahymenial Heterobasidiomycetes.

Sebacina strains without fruiting bodies and their system-

atic placement. Nova Hedwigia 7:489–499.

Ohtaka N, Narisawa K. 2008. Molecular characterization and endo-

phytic nature of the root-associated fungus Meliniomyces

variabilis (LtVB3). J Gen Plant Pathol 74:24–31.

Olsrud M, Carlsson BA, Svensson BM, Michelsen A, Melillo JM.

2010. Responses of fungal root colonization, plant cover

and leaf nutrients to long-term exposure to elevated atmo-

spheric CO

and warming in a subarctic birch forest under-

story. Global Change Biol 16:1820–1829.

Paparu P, Dubois T, Coyne D, Viljoen A. 2009. Dual inoculation

of Fusarium oxysporum endophytes in banana: Eect on

plant colonization, growth and control of the root burrow-

ing nematode and the banana weevil. Biocontrol Sci Technol

19:639–655.

Pareja-Jaime Y, Martin-Urdiroz M, Gonzalez Roncero MI,

Antonio Gonzalez-Reyes J, Ruiz Roldan MDC. 2010. Chitin

synthase-decient mutant of Fusarium oxysporum elicits

tomato plant defence response and protects against wild-

type infection. Mol Plant Pathol 11:479–493.

Parkinson D, Crouch R. 1969. Studies on fungi in a pinewood

soil. V. Root myco oras of seedlings of Pinus nigra var. lari-

cio. Revue d’ Écologie et de Biologie du Sol 6:263–275.

Parsons JW. 1981. Chemistry and distribution of amino sugars in

soils and soil organisms. In Soil Biochemistry. Vol. 5, eds. EA

Paul, JN Ladd, pp. 197–227. New York: Marcel Dekker, Inc.

Pearson V, Read DJ. 1973. e biology of mycorrhiza in the

Ericaceae. New Phytol 72:371–379.

Peterson RL, Wagg C, Pautler M. 2008. Associations between

microfungal endophytes and roots: Do structural features

indicate function? Botany 86:445–456.

Petrini O. 1991. Fungal endophytes of tree leaves. In Microbial

Ecology of Leaves, eds. JH Andrews, SS Hirano, pp. 179–197.

New York: Springer.

Petrini O, Fisher PJ, Petrini LE. 1992. Fungal endophytes of

bracken (Pteridium aquilinum), with some re ections on

their use in biological control. Sydowia 44:282–293.

Phillips DV, Leben C, Allison CC. 1967. A mechanism for the

reduction of Fusarium wilt by a Cephalosporium species.

Phytopathology 57:916–919.

Piercey MM, Graham SW, Currah RS. 2004. Patterns of genetic

variation in Phialocephala fortinii across a broad latitudinal

transect in Canada. Mycol Res 108:955–964.

Postma J, Rattink H. 1991. Biological control of Fusarium wilt of

carnation with a nonpathogenic isolate of Fusarium oxyspo-

rum. Can J Bot 70:1199–1205.

Postma JWM, Olsson PA, Falkengren-Grerup U. 2007. Root col-

onisation by arbuscular mycorrhizal, ne endophytic and

dark septate fungi across a pH gradient in acid beech for-

ests. Soil Biol Biochem 39:400–408.

Queloz V. 2010. Biogeography and evolution of the Phialocephala

fortinii s.l.—Acephala applanata species complex (PAC).

PhD thesis, Zürich, Switzerland: ETH Zürich.

Queloz V, Duo A, Grünig CR. 2008. Isolation and characteriza-

tion of microsatellite markers for the tree-root endophytes

Phialocephala subalpina and Phialocephala fortinii s.s. Mol

Ecol Resour 8:1322–1325.

Queloz V, Duo A, Sieber TN, Grünig CR. 2010. Microsatellite size

homoplasies and null alleles do not aect species diagnosis

and population genetic analysis in a fungal species complex.

Mol Ecol Resour 10:348–367.

Queloz V, Grünig CR, Sieber TN, Holdenrieder O. 2005.

Monitoring the spatial and temporal dynamics of a com-

munity of the tree-root endophyte Phialocephala fortinii sl.

New Phytol 168:651–660.

Queloz V, Sieber TN, Holdenrieder O, McDonald BA, Grünig

CR. 2011. No biogeographical pattern for a root-associated

fungal species complex. Global Ecol Biogeogr 20:160–169.

Raps A, Vidal S. 1996. e in uence of a root-colonizing endo-

phyte on the development of root-knot nematodes on

tomato. Mitteilungen aus der Biologischen Bundesanstalt für

Land- und Forstwirtscha (Berlin-Dahlem) 321:453.

Raps A, Vidal S. 1998. Indirect eects of an unspecialized

endophytic fungus on specialized plant-herbivorous insect

interactions. Oecologia 114:541–547.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-46 Root–Rhizosphere Interactions

Rasmann C, Graham JH, Chellemi DO, Datno LE, Larsen J. 2009.

Resilient populations of root fungi occur within ve tomato

production systems in southeast Florida. Appl Soil Ecol

43:22–31.

Raviraja NS, Sridhar KR, Bärlocher F. 1996. Endophytic aquatic

hyphomycetes of roots of plantation crops and ferns from

India. Sydowia 48:152–160.

Read DJ. 1974. Pezizella ericae sp nov, perfect state of a typical

mycorrhizal endophytes of ericaceae. Trans Br Mycol Soc

63:381.

Read DJ. 1983. e biology of micorrhiza in the Ericales. Can J

Bot 61:985–1004.

Read DJ. 1992. e mycorrhizal fungal community with spe-

cial reference to nutrient mobilization. In e Fungal

Community, eds. GC Carroll, DT Wicklow, pp. 631–652.

New York: Marcel Dekker, Inc.

Read DJ. 1996. e structure and function of the ericoid mycor-

rhizal root. Ann Bot 77:365–374.

Reinecke P. 1978. Microdochium bolleyi at the stem base of cereals.

Z Panzenkrank Panzensch 85:679–685.

Reinecke P, Fokkema NJ. 1981. An evaluation of methods of

screening fungi from the haulm base of cereals for antago-

nism to Pseudocercosporella herpotrichoides in wheat. Trans

Br Mycol Soc 77:343–350.

Reininger V, Grünig CR, Sieber TN. 2011a. Are plant commu-

nities shaped by fungal root endophytes? Phytopathology

101:S151–S152.

Reininger V, Grünig CR, Sieber TN. 2011b. Microsatellite-based

quantication method to estimate biomass of endophytic

Phialocephala species in strain mixtures. Microb Ecol

61:676–683.

Reininger V, Grünig CR, Sieber TN. 2012. Host species and strain

combination determine growth reduction of spruce and

birch seedlings colonized by root-associated dark septate

endophytes. Environ Microbiol 14:1064–1076.

Reissinger A, Vilich V, Sikora RA. 2001. Detection of fungi in

planta: Eectiveness of surface sterilization methods. Mycol

Res 105:563–566.

Richard C, Fortin J-A, Fortin A. 1971. Protective eect of an ecto-

mycorrhizal fungus against the root pathogen Mycelium

radicis atrovirens. Can J For Res 1:246–251.

Riesen T, Sieber TN. 1985. Endophytic Fungi in Winter Wheat

(Triticum aestivum L.). Zürich, Switzerland: Institute of

Microbiology, Swiss Federal Institute of Technology.

Rivera-Orduna FN, Suarez-Sanchez RA, Flores-Bustamante ZR,

Gracida-Rodriguez JN, Flores-Cotera LB. 2011. Diversity of

endophytic fungi of Taxus globosa (Mexican yew). Fungal

Divers 47:65–74.

Robertson NF. 1954. Studies on the mycorrhiza of Pinus sil-

vestris. I. Pattern of development of mycorrhizal root

and its signicance for experimental studies. New Phytol

53:253–283.

Rodrigues KF. 1996. Fungal endophytes of palms. In Endophytic

Fungi in Grasses and Woody Plants, eds. SC Redlin, LM

Carris, pp. 121–132. St. Paul, MN: APS Press.

Rodríguez-Gálvez E, Mendgen K. 1995. e infection process

of Fusarium oxysporum in cotton root tips. Protoplasma

189:61–72.

Roy M, Yagame T, Yamato M etal. 2009. Ectomycorrhizal Inocybe

species associate with the mycoheterotrophic orchid

Epipogium aphyllum but not its asexual propagules. Ann

Bot 104:595–610.

Ruotsalainen AL, Markkola AM, Kozlov MV. 2010. Birch eects on

root fungal colonisation of crowberry are uniform along dif-

ferent environmental gradients. Basic Appl Ecol 11:459–467.

Ruotsalainen AL, Vare H, Oksanen J, Tuomi J. 2004. Root fungus

colonization along an altitudinal gradient in North Norway.

Arct Antarct Alp Res 36:239–243.

Saito K, Kuga-Uetake Y, Saito M, Peterson RL. 2006. Vacuolar

localization of phosphorus in hyphae of Phialocephala for-

tinii, a dark septate fungal root endophyte. Can J Microbiol

52:643–650.

Saleh AA, Leslie JE. 2004. Cephalosporium maydis is a distinct

species in the Gaeumannomyces-Harpophora species com-

plex. Mycologia 96:1294–1305.

Salvarredi LA, Crespo EM, Menoyo E, Filippa EM, Barboza GE,

Lugo MA. 2010. Arbuscular mycorrhizas and dark septates

endophytes in native Gentianaceae from Argentina. Boletin

De La Sociedad Argentina De Botanica 45:223–229.

Sánchez Márquez S, Bills GF, Domínguez Acuña D, ZabalgogeazcoaI.

2010. Endophytic mycobiota of leaves and roots of the grass

Holcus lanatus. Fungal Divers 41:115–123.

Sánchez Márquez S, Bills GF, Zabalgogeazcoa I. 2008. Diversity

and structure of the fungal endophytic assemblages from

two sympatric coastal grasses. Fungal Divers 33:87–100.

Savage SD, Sall MA. 1981. Radioimmunosorbent assay for Botrytis

cinerea. Phytopathology 71:411–415.

Schardl CL. 2010. e Epichloë, symbionts of the grass subfamily

Pooideae. Ann Missouri Bot Gard 97:646–665.

Schelling CL. 1952. Zur Kenntnis von Mycelium radicis atrovirens

Melin mit besonderer Berücksichtigung der Verwertbarkeit

verschiedener Kohlenstoquellen. ed. Zürich, Switzerland:

Swiss Federal Institute of Technology.

Schild DE, Kennedy A, Stuart MR. 1988. Isolation of symbiont

and associated fungi from ectomycorrhizas of Sitka spruce.

Eur J For Pathol 18:51–61.

Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP,

Schadt CW. 2008. Mycorrhizal and dark-septate fungi in

plant roots above 4270 meters elevation in the Andes and

Rocky Mountains. Arct Antarct Alp Res 40:576–583.

Schol-Schwarz MB. 1970. Revision of the genus Phialophora

(Moniliales). Persoonia 6:59–94.

Schönhar S. 1987. Untersuchungen über das Vorkommen pil-

zlicher Parasiten an Feinwurzeln 70–90jähriger Fichten

(Picea abies Karst.). Mitteilungen des Vereins Forstlicher

Standortskunde und Forstpanzenzüchtung 33:77–80.

Schroers HJ, Zerjav M, Munda A, Halleen F, Crous PW. 2008.

Cylindrocarpon pauciseptatum sp nov., with notes on

Cylindrocarpon species with wide, predominantly 3-septate

macroconidia. Mycol Res 112:82–92.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-47Fungal Root Endophytes

Schulz B, Boyle C. 2005. e endophytic continuum. Mycol Res

109:661–686.

Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K. 2002.

Endophytic fungi: A source of novel biologically active sec-

ondary metabolites. Mycol Res 106:996–1004.

Schulz B, Boyle C, Sieber TN. 2006. Microbial Root Endophytes.

Berlin, Germany: Springer.

Schuster RP, Sikora RA, Amin N. 1995. Potential of endo-

phytic fungi for the biological control of plant parasitic

nematodes. Mededelingen Faculteit Landbouwkundige en

Toegepaste Biologische Wetenschappen Universiteit Gent

60:1047–1052.

Sengupta A, Chakraborty DC, Chaudhuri S. 1988. Do septate

endophytes also have a mycorrhizal function for plants

under stress? In Mycorrhizae for Green Asia: First Asian

Conference on Mycorrhizae, eds. A Mahadevan, N Raman, K

Natarajan, pp. 169–174. Madras, India: Centre of Advanced

Studies in Botany, University of Madras, Guindy Campus.

Sequerra J, Capellano A, Gianinazzi-Pearson V, Moiroud A. 1995.

Ultrastructure of cortical root cells of Alnus incana infected

by Penicillium nodositatum. New Phytol 130:545–555.

Ser ing A, Wirsel SGR, Lind V, Deising HB. 2007. Performance of

the biocontrol fungus Piriformospora indica on wheat under

greenhouse and eld conditions. Phytopathology 97:523–531.

Sheerson RP, Weiss M, Kull T, Taylors DL. 2005. High speci-

city generally characterizes mycorrhizal association in

rare lady’s slipper orchids, genus Cypripedium. Mol Ecol

14:613–626.

Siddiquee S, Yusuf UK, Zainudin NAIM. 2010. Morphological

and molecular detection of Fusarium chlamydosporum

from root endophytes of Dendrobium crumenatum. Afr

JBiotechnol 9:4081–4090.

Sieber TN. 1985. Endophytische Pilze von Winterweizen

(Triticum aestivum L.). Zürich, Switzerland: Institute of

Microbiology, Swiss Federal Institute of Technology.

Sieber T. 1988. Endophytic fungi in needles of healthy-looking

and diseased Norway spruce (Picea abies L. Karsten). Eur

JFor Pathol 18:321–342.

Sieber TN. 1989. Endophytic fungi in twigs of healthy and dis-

eased Norway spruce and white r. Mycol Res 92:322–326.

Sieber TN. 2002. Fungal root endophytes. In Plant Roots: e

Hidden Half, eds. Y Waisel, A Eshel, U Kaa, 3rd edn.,

pp. 887–917. New York: Marcel Dekker, Inc.

Sieber TN. 2007. Endophytic fungi in forest trees: Are they mutu-

alists? Fungal Biol Rev 21:75–89.

Sieber TN, Grünig CR. 2006. Biodiversity of fungal root-endo-

phyte communities and populations in particular of the dark

septate endophyte Phialocephala fortinii. In Microbial Root

Endophytes, eds. B Schulz, C Boyle, TN Sieber, pp.107–132.

Berlin, Germany: Springer.

Sieber TN, Riesen TK, Müller E, Fried PM. 1988. Endophytic fungi

in four winter wheat cultivars (Triticum aestivum L.) dier-

ing in resistance against Stagonospora nodorum (Berk.) Cast.

& Germ. = Septoria nodorum (Berk.) Berk. JPhytopathol

122:289–306.

Sieber-Canavesi F, Sieber TN. 1993. Successional patterns of fun-

gal communities in needles of European silver r (Abies

alba Mill.). New Phytol 125:149–161.

Sigler L, Allan T, Lim SR, Berch S, Berbee M. 2005. Two new

Cryptosporiopsis species from roots of ericaceous hosts in

western North America. Stud Mycol 53:53–62.

Simonsen J. 1971. Phialophora radicicola Cain, the conidial

state of Gaeumannomyces graminis in Denmark. Friesia

9:361–368.

Skipp RA, Christensen MJ. 1989. Fungi invading roots of peren-

nial ryegrass (Lolium perenne L.) in pasture. NZ J Agric Res

32:423–431.

Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis, 3rd edn. San

Diego, CA: Academic Press.

Smith VL, Wilcox WF, Harman GE. 1990. Potential biologi-

cal control of Phytophthora root and crown rots of apple

by Trichoderma and Gliocladium spp. Phytopathology

80:880–885.

Sridhar KR, Bärlocher F. 1992. Endophytic aquatic hypho-

mycetes of roots of spruce, birch and maple. Mycol Res

96:305–308.

Stark C, Babik W, Durka W. 2009. Fungi from the roots of the

common terrestrial orchid Gymnadenia conopsea. Mycol

Res 113:952–959.

Steinke E, Williams PG, Ashford AE. 1996. e structure and

fungal associates of mycorrhizas in Leucopogon parviorus

(Andr.) Lindl. Ann Bot 77:413–419.

Stoyke G, Currah RS. 1991. Endophytic fungi from the mycorrhi-

zae of alpine ericoid plants. Can J Bot 69:347–352.

Stoyke G, Currah RS. 1993. Resynthesis in pure culture of a com-

mon subalpine fungus-root association using Phialocephala

fortinii and Menziesia ferruginea (Ericaceae). Arct Alp Res

25:189–193.

Stoyke G, Egger KN, Currah RS. 1992. Characterization of sterile

endophytic fungi from the mycorrhizae of subalpine plants.

Can J Bot 70:2009–2016.

Su Y-Y, Guo L-D, Hyde KD. 2010. Response of endophytic fungi of

Stipa grandis to experimental plant function group removal

in Inner Mongolia steppe, China. Fungal Divers 43:93–101.

Sumarah MW, Puniani E, Blackwell BA, Miller JD. 2008.

Characterization of polyketide metabolites from foliar

endophytes of Picea glauca. J Nat Prod 71:1393–1398.

Summerbell RC. 1989. Microfungi associated with the mycor-

rhizal mantle and adjacent microhabitats within the rhizo-

sphere of black spruce. Can J Bot 67:1085–1095.

Tao G, Liu ZY, Hyde KD, Liu XZ, Yu ZN. 2008. Whole rDNA

analysis reveals novel and endophytic fungi in Bletilla

ochracea (Orchidaceae). Fungal Divers 33:101–122.

Tedersoo L, Paertel K, Jairus T, Gates G, Poldmaa K, TammH.

2009. Ascomycetes associated with ectomycorrhizas:

Molecular diversity and ecology with particular reference

to the Helotiales. Environ Microbiol 11:3166–3178.

Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttila AM. 2010.

Root endophytes along a primary succession gradient in

northern Finland. Fungal Divers 41:125–134.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-48 Root–Rhizosphere Interactions

Tellenbach C, Sieber TN. 2012. Do colonization by dark septate

endophytes and elevated temperature aect pathogenicity

of oomycetes? FEMS Microbiology Ecology 82:157–168.

Tellenbach C, Grünig CR, Sieber TN. 2010. Suitability of quanti-

tative real-time PCR to estimate the biomass of fungal root

endophytes. Appl Environ Microbiol 76:5764–5772.

Tellenbach C, Grünig CR, Sieber TN. 2011. Negative eects on

survival and performance of Norway spruce seedlings colo-

nized by dark septate root endophytes are primarily isolate-

dependent. Environ Microbiol 13:2508–2517.

ormann MN, Currah RS, Bayley SE. 1999. e mycorrhizal sta-

tus of the dominant vegetation along a peatland gradient

in southern boreal Alberta, Canada. Wetlands 19:438–450.

Tian W, Zhang CQ, Qiao P, Milne R. 2011. Diversity of cultur-

able ericoid mycorrhizal fungi of Rhododendron decorum in

Yunnan, China. Mycologia 103:703–709.

Treu R, Laursen GA, Stephenson SL, Landolt JC, Densmore R.

1996. Mycorrhizae from Denali National Park and Preserve,

Alaska. Mycorrhiza 6:21–29.

Trüssel D. 2011. Zur Verbreitungsbiologie von Phialocephala sub-

alpina, P. fortinii s.s. und Acephala applanata—Vegetative

Ausbreitung im Boden. MSc thesis, Zürich, Switzerland:

ETH Zürich.

Turner PD. 1962. Morphological in uence of exudates of mycor-

rhizal and non-mycorrhizal fungi on excised root cultures

of Pinus sylvestris L. Nature 194:551–552.

Upson R, Newsham KK, Bridge PD, Pearce DA, Read DJ. 2009.

Taxonomic anities of dark septate root endophytes of

Colobanthus quitensis and Deschampsia antarctica, the

two native antarctic vascular plant species. Fungal Ecol

2:184–196.

Urcelay C. 2002. Co-occurrence of three fungal root symbionts in

Gaultheria poeppiggi DC in Central Argentina. Mycorrhiza

12:89–92.

Väre H, Vestberg M, Eurola S. 1992. Mycorrhiza and root associ-

ated fungi in Spitsbergen. Mycorrhiza 1:93–104.

Varma A, Singh A, Sudha etal. 2001. Piriformospora indica: An

axenically culturable mycorrhiza-like endosymbiotic fun-

gus. In e Mycota IX. Fungal Associations, ed. B Hock,

pp. 125–150. Berlin, Germany: Springer.

Vaz ABM, Mota RC, Bomm MRQ etal. 2009. Antimicrobial

activity of endophytic fungi associated with Orchidaceae in

Brazil. Can J Microbiol 55:1381–1391.

Vendramin E, Gastaldo A, Tondello A, Baldan B, Villani M,

Squartini A. 2010. Identication of two fungal endophytes

associated with the endangered orchid Orchis militaris L.

J Microbiol Biotechnol 20:630–636.

Verkley GJM, Zijlstra JD, Summerbell RC, Berendse F. 2003.

Phylogeny and taxonomy of root-inhabiting Cryptosporiopsis

species, and C. rhizophila sp nov., a fungus inhabiting roots

of several Ericaceae. Mycol Res 107:689–698.

Verma S, Varma A, Rexer KH etal. 1998. Piriformospora indica,

gen. et sp. nov., a new root-colonizing fungus. Mycologia

90:896–903.

Vidal S. 1996. Changes in suitability of tomato for white ies

mediated by a non-pathogenic endophytic fungus. Entomol

Exp Appl 80:272–274.

Vilich V, Dolfen M, Sikora RA. 1998. Chaetomium spp. coloni-

zation of barley following seed treatment and its eect on

plant growth and Erysiphe graminis f. sp. hordei disease

severity. Z Panzenkrank Panzensch 105:130–139.

Vodnik D, Mihelcic M, Gogala N. 1997. Isolation of root associ-

ated fungi from Erica herbacea and their tolerance to lead.

Acta Biol Slovenica 41:35–42.

Vujanovic V, St-Arnaud M, Barabé D, ibeault G. 2000.

Phialocephala victorinii sp. nov., endophyte of Cypripedium

parviorum. Mycologia 92:571–576.

Wagg C, Husband BC, Green DS, Massicotte HB, Peterson RL.

2011. Soil microbial communities from an elevational cline

dier in their eect on conifer seedling growth. Plant Soil

340:491–504.

Walker J. 1981. Taxonomy of take-all fungi and related genera and

species. In Biology and Control of Take-All, eds. MJC Asher,

PJ Shipton, pp. 15–74. London, U.K.: Academic Press.

Waller F, Achatz B, Baltruschat H etal. 2005. e endophytic fun-

gus Piriformospora indica reprograms barley to salt-stress

tolerance, disease resistance, and higher yield. Proc Natl

Acad Sci U S A 102:13386–13391.

Wang CJK, Wilcox HE. 1985. New species of ectendomycorrhi-

zal and pseudomycorrhizal fungi: Phialophora nlandia,

Chloridium paucisporum, and Phialocephala fortinii.

Mycologia 77:951–958.

Warcup JH. 1988. Mycorrhizal associations of isolates of Sebacina

vermifera. New Phytol 110:2272–2231.

Ward E, Bateman GL. 1999. Comparison of Gaeumannomyces-

and Phialophora-like fungal pathogens from maize and

other plants using DNA methods. New Phytol 141:323–331.

Wei G, Kloepper JW, Tuzun S. 1994. Induced systemic resistance

to cucumber diseases and increased plant growth by plant

growth-promoting rhizobacteria under eld conditions.

In Improving Plant Productivity with Rhizosphere Bacteria,

eds. MH Ryder, PM Stephens, GD Bowen, pp. 70–71. Glen

Osmond, Australia: CSIRO Division of Soils.

Weiss M, Oberwinkler F. 2001. Phylogenetic relationships in

Auriculariales and related groups—Hypotheses derived

from nuclear ribosomal DNA sequences. Mycol Res

105:403–415.

Weiss M, Sykorova Z, Garnica S etal. 2011. Sebacinales every-

where: Previously overlooked ubiquitous fungal endo-

phytes. PLOS One 6:e16793.

Werner C, Petrini O, Hesse M. 1997. Degradation of the poly-

amine alkaloid aphelandrine by endophytic fungi iso-

lated from Aphelandra tetragona. FEMS Microbiol Lett

155:147–153.

White IR, Backhouse D. 2007. Comparison of fungal endophyte

communities in the invasive panicoid grass Hyparrhenia

hirta and the native grass Bothriochloa macra. Aust J Bot

55:178–185.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

38-49Fungal Root Endophytes

Whittaker RH. 1969. New concepts of kingdoms of organisms.

Science 163:150–160.

Widler B, Müller E. 1984. Untersuchungen über endophytische

Pilze von Arctostaphylos uva-ursi (L.) Sprengel (Ericaceae).

Botanica Helvetica 94:307–337.

Wilcox HE. 1983. Fungal parasitism of woody plant roots

from mycorrhizal relationships to Plant Dis. Annu Rev

Phytopathol 21:221–242.

Wilcox HE. 1996. Mycorrhizae. In e Hidden Half, eds. Y Waisel, A

Eshel, U Kaa, pp. 689–721. New York: Marcel Dekker, Inc.

Wilcox HE, Ganmore-Neumann R. 1974. Ectendomycorrhizae in

Pinus resinosa seedlings. I. Characteristics of mycorrhizae pro-

duced by a black imperfect fungus. Can J Bot 52:2145–2155.

Wilcox HE, Wang CJK. 1987. Mycorrhizal and pathological asso-

ciations of dematiaceous fungi in roots of 7-month-old tree

seedlings. Can J For Res 17:884–899.

Wilhelm S, Nelson PE, Ford DH. 1969. A gray sterile fungus patho-

genic on strawberry roots. Phytopathology 59:1525–1529.

Wilson BJ, Addy HD, Tsuneda A, Hambleton S, Currah RS. 2004.

Phialocephala sphaeroides sp nov., a new species among the

dark septate endophytes from a boreal wetland in Canada.

Can J Bot 82:607–617.

Wu LQ, Lv YL, Meng ZX, Chen J, Guo SX. 2010. e promoting

role of an isolate of dark-septate fungus on its host plant

Saussurea involucrata Kar. et Kir. Mycorrhiza 20:127–135.

Xia X, Lie TK, Qian X, Zheng Z, Huang Y, Shen Y. 2011. Species

diversity, distribution, and genetic structure of endophytic

and epiphytic Trichoderma associated with banana roots.

Microb Ecol 61:619–625.

Xu JT, Guo SX. 2000. Retrospect on the research of the cultivation

of Gastrodia elate Bl, a rare traditional Chinese medicine.

Chin Med J 113:686–692.

Yao JM, Wang YC, Zhu YG. 1992. A new variety of the pathogen

of maize take-all. Acta Mycol Sin 11:99–104.

Yonezawa M, Usuki F, Narisawa K, Takahashi J, Hashiba T. 2004.

Anatomical study on the interaction between the root

endophytic fungus Heteroconium chaetospira and Chinese

cabbage. Mycoscience 45:367–371.

Yu T, Nassuth A, Peterson RL. 2001. Characterization of the

interaction between the dark septate fungus Phialocephala

fortinii and Asparagus ocinalis roots. Can J Microbiol

47:741–753.

Yuan Z-L, Chen Y-C, Yang Y. 2009. Diverse non-mycorrhizal fun-

gal endophytes inhabiting an epiphytic, medicinal orchid

(Dendrobium nobile): Estimation and characterization.

World J Microbiol Biotechnol 25:295–303.

Yuan ZL, Lin FC, Zhang CL, Kubicek CP. 2010. A new species

of Harpophora (Magnaporthaceae) recovered from healthy

wild rice (Oryza granulata) roots, representing a novel

member of a benecial dark septate endophyte. FEMS

Microbiol Lett 307:94–101.

Zaarano PL, Duò A, Grünig CR. 2010. Characterization of the

mating type (MAT) locus in the Phialocephala fortinii s.l.—

Acephala applanata species complex. Fungal Genet Biol

47:761–772.

Zaarano PL, Queloz V, Duò A, Grünig CR. 2011. Sex in the PAC:

A hidden aair in dark septate endophytes? BMC Evol Biol

11:282.

Zhang C, Yin L, Dai S. 2009. Diversity of root-associated fungal

endophytes in Rhododendron fortunei in subtropical forests

of China. Mycorrhiza 19:417–423.

Zhang MS, Wu SJ, Jie XJ etal. 2006. Eect of endophyte extract

on micropropagation of Cremastra appendiculata (D.

Don.) Makino (Orchidaceae). Propag Ornament Plants

6:83–89.

Zijlstra JD, Van’t Hof P, Baar J etal. 2005. Diversity of symbiotic

root endophytes of the Helotiales in ericaceous plants and

the grass, Deschampsia exuosa. Stud Mycol 53:147–162.

Downloaded by [ETH BIBLIOTHEK (Zurich)] at 03:43 27 March 2015

Two new root endophyte and nematode cyst parasite species of the widely distributed genus Laburnicola

Article

Full-text available

Nov 2022

Fungal root endophytes, including the common form group of dark septate endophytes (DSEs), represent different taxonomic groups with potentially diverse life strategies. During surveys of DSE communities and of nematode cysts colonizing fungi, isolates representing Laburnicola ( Didymosphaeriaceae , Pleosporales ) lineages were discovered. Here we carried out a comprehensive study of the phylogenetic relationships and taxonomy of fungi collected from plant roots in Hungary, Mongolia, and Kazakhstan and from eggs of the cereal cyst nematode Heterodera filipjevi in Turkey. In addition to the study of the morphology and culture characteristics of the strains, four loci (internal transcribed spacer, partial large and small subunit regions of nuclear ribosomal DNA and partial translation elongation factor 1-alpha) were used to infer the molecular phylogenetic relationships of the strains within Laburnicola . The isolates were found to represent two distinct lineages, which are described here as novel species, Laburnicola nematophila and L. radiciphila . The interaction of the strains with plants and nematodes was examined using in vitro bioassays, which revealed endophytic interactions with the plant roots and parasitic interactions with the nematode eggs. Analyses of similar ITS sequences found in public databases revealed that members of the genus Laburnicola are widely distributed characteristic members of the plant microbiome, and they are reported as parasites of plant parasitic cyst nematodes here for the first time.

Cultivable Fungal Endophytes in Roots, Rhizomes and Leaves of Posidonia oceanica (L.) Delile along the Coast of Sicily, Italy

Article

Full-text available

Apr 2022

The presence of endophytic fungi in the roots, rhizomes, and leaves of Posidonia oceanica was evaluated in different localities of the Sicilian coast. Samples of roots, rhizomes, and leaves were submitted to isolation techniques, and the obtained fungal colonies were identified by morphological and molecular (rRNA sequencing) analysis. Fungal endophytes occurred mainly in roots and occasionally in rhizomes and leaves. Lulwoana sp. was the most frequent of the isolated taxa, suggesting a strong interaction with the host. In addition, eight other fungal taxa were isolated. In particular , fungi of the genus Ochroconis and family Xylariaceae were identified as endophytes in healthy plants at all sampling stations, whereas Penicillium glabrum was isolated at only one sampling station. Thus, several organs, especially roots of Posidonia oceanica, harbor endophytic fungi, potentially involved in supporting the living host as ascertained for terrestrial plants.

Dark septate endophytes: mutualism from by-products?

Article

Oct 2021
TRENDS PLANT SCI

Plant roots are abundantly colonized by dark septate endophytic (DSE) fungi in virtually all ecosystems. DSE fungi are functionally heterogeneous and their relationships with plants range from antagonistic to mutualistic. Here, we consider the role of by-product benefits in DSE and other root–fungal symbioses. We compared host investments against symbiont-derived benefits for the host plant and categorized these benefits as by-products or benefits requiring reciprocal investment from the host. By-product benefits may provide the variability required for the evolution of invested mutualisms between the host and symbiont. We suggest that DSE could be considered as ‘a by-product mutualist transitional phase’ in the evolution of cooperative mycorrhizal symbionts from saprotrophic fungi.

Physiological response mechanism of heavy metal‐resistant endophytic fungi isolated from the roots of Polygonatum kingianum

Article

Full-text available

Aug 2023

This study aims to evaluate the tolerance of endophytic fungi isolated from the fibrous roots of Polygonatum kingianum to arsenic (As) and cadmium (Cd) and their physiological response mechanisms. Five isolated strains were obtained with EC50 values for As(V) ranging from 421 to 1281 mg/L, while the other three strains tolerated Cd(II) with an EC50 range of 407–1112 mg/L. Morphological and molecular identification indicated that these eight strains were Cladosporium spp. belonging to dark septate endophytes (DSEs). The contents of metal ions in mycelium sharply increased, reaching 38.87 mg/kg for strain MZ‐11 under As(V) stress and 0.33 mg/kg for fungus PR‐2 under Cd(II). The physiological response revealed that the biomass decreased with increasing concentrations of As(V) or Cd(II), and the activity of superoxide dismutase significantly improved under the corresponding EC50‐concentration As/Cd of the strains, as well as the contents of antioxidant substances, including metallothionein, glutathione, malondialdehyde, melanin, and proline. Taken together, the filamentous fungi of Cladosporium spp. accounted for a high proportion of fungi isolated from the fibrous roots of P. kingianum and had a strong capacity to tolerate As(V) or Cd(II) stress by improving antioxidase activities and the content of antioxidant substances, and immobilization of metal ions in hyphae.

Multilocus molecular phylogenetic-led discovery and formal recognition of four novel root- colonizing Fusarium species from northern Kazakhstan and the phylogenetically divergent Fusarium steppicola lineage

Article

Nov 2022
MYCOLOGIA

In this study, DNA sequence data were used to characterize 290 Fusarium strains isolated during a survey of root-colonizing endophytic fungi of agricultural and nonagricultural plants in northern Kazakhstan. The Fusarium collection was screened for species identity using partial translation elongation factor 1-α (TEF1) gene sequences. Altogether, 16 different Fusarium species were identified, including eight known and four novel species, as well as the discovery of the phylogen-etically divergent F. steppicola lineage. Isolates of the four putatively novel fusaria were further analyzed phylogenetically with a multilocus data set comprising partial sequences of TEF1, RNA polymerase II largest (RPB1) and second-largest (RPB2) subunits, and calmodulin (CaM) to assess their genealogical exclusivity. Based on the molecular phylogenetic and comprehensive morphological analyses, four new species are formally described herein: F. campestre, F. kazakhstanicum, F. rhizicola, and F. steppicola.

Host and Tissue Affiliations of Culturable Endophytic Fungi Associated with Xerophytic Plants in the Desert Region of Northwest China

Article

Full-text available

Mar 2022

Endophytic fungi isolated from plants under drought stress have been evidenced to confer hosts adaptive benefits to withstand drought. In this study, endophytic fungi associated with five typical desert shrubs in different tissue from extremely arid desert in Northwest China were investigated based on ITS sequence analysis. A total of 158 endophytic fungal stains were isolated from 1088 tissue segments of 12 samples, and 28 taxa represented by 25 species and 15 genera were identified as Ascomycetes. Alternaria sp. was the dominant genus with generic abundance ranging from 20% to 65%. The colonization rate of root was significantly lower, but the root-endophytic fungi (19 species) conversely presented a higher diversity than stem and leaf (11 and 7 species, respectively). Endophytic fungi had pronounced relative host and tissue preferences, while tissue explained more endophytic fungal variation than plant species. Additionally, soil pH, organic carbon, and phosphatase elicited significant responses from fungal species, which significantly affected the species richness of Fusarium redolens, Alternaria chlamydospore, Didymella glomerata, and Xylariales sp. This research provides a basis for the further understanding of the ecological distribution of endophytic fungi associated with xerophytic plants and their potential application for vegetative restoration and agricultural cultivation in drylands.

Balance and trade: charting the course of fungal symbiosis in sugarcane root systems

Thesis

Mar 2018

Anders Claassens

The root systems of sugarcane (Saccharum L. spp. hybrids) host a variety of symbiotic fungal organisms including arbuscular mycorrhizal (AM) fungi and dark septate endophytes (DSE). AM/DSE symbioses are widely reported to influence the productive capacity of a range of agricultural crops via enhanced nutrient assimilation and plant stress tolerance. Presently, the biological and functional characteristics AM/DSE in sugarcane have only been examined superficially and remain poorly understood. Before the potential benefits of AM/DSE symbioses can be exploited through management strategies, characterisation of the temporal changes in AM/DSE colonisation over the sugarcane crop cycle is required. This study investigated the colonisation dynamics of AM/DSE in sugarcane roots during 1st and 2nd ratoon crop phases. A field study was undertaken at two proximal sites with different cropping histories to assess AM/DSE colonisation of sett and shoot roots over 28 weeks of crop growth. At each observation, the functional structures produced by AM (arbuscules, hyphae, spores and vesicles) were delineated and quantified. Significant differences in the rate of AM/DSE colonisation over time and between root types were observed. There were no significant differences in AM sett root colonisation between sites. For both fungal types, differences in shoot root colonisation between sites were not significant. DSE sett root colonisation was significantly lower in the 2nd ratoon compared to the 1st ratoon crop. For both fungal types, sett root colonisation was significantly higher than for shoot roots at both sites. Maximum AM/DSE sett root colonisation occurred between 5–7 weeks, prior to the establishment of shoot roots and rapid developmental period of ratoon crops. While AM sett root colonisation was consistent across ratoon phases, there is a need to account for the differences in DSE sett root colonisation levels between 1st and 2nd ratoon crops. The composition of total AM colonisation at both sites was dominated by arbuscules and hyphae with comparatively lower levels of spores and vesicles. A diversity of AM fungal morphologies previously undocumented in sugarcane was observed co-occupying individual root systems. These data provide a basis for the development of appropriate sampling regimes in future studies investigating management impacts on AM/DSE symbioses in sugarcane cropping systems.

Poaceascoma zborayi sp. nov. and Agrorhizomyces patris gen. et spec. nov. – Two novel dark septate endophytes colonizing wheat (Triticum aestivum) roots from a cropland in Hungary

Article

Full-text available

Jun 2024

In this study, we investigated two distinct new phylogenetic lineages of root-colonizing dark septate endophytic fungi colonizing wheat ( Triticum aestivum ) roots from a long-term agricultural experimental site in Hungary. According to four-locus (internal transcribed spacer, partial large and small subunit regions of nuclear ribosomal DNA, and partial translation elongation factor 1-alpha) phylogenetic analyses, the isolates belong to the Lentitheciaceae and Didymosphaeriaceae of the Pleosporales ( Dothideomycetes ). We studied the morphology and culture characteristics of the strains. We carried out in vitro resynthesis pot experiments with their original hosts and found no overall negative effect of the inoculation with different isolates of the new taxa. One of the lineages belonged to the genus Poaceascoma ( Lentitheciaceae ) and represented a novel species described here as Poaceascoma zborayi . We could describe conidia-like structures from this species. Isolates of the other lineage represented a monotypic novel genus in the Didymosphaeriaceae . Accordingly, the new genus, Agrorhizomyces , represented by the species A. patris , is introduced. Sterile, globose structures resembling immature sporocarps were detected. Sequence similarity searches indicated that P. zborayi might be widely distributed, while no sequence similar to A. patris was found outside the sampling area.

ENDOPHYTES AS AGENTS OF PHYTOREMEDIATION

Chapter

Mar 2024

Endophytes are endosymbiotic microorganisms colonizing the internal tissues of healthy host plants [1] and possess the ability to improve the quality and growth rate of theirrespective hosts [2]. Their colonization does not produce any disease symptoms or morphological changes like gall formation of plant tissues [3]. Most of the plants on earth arehost to one or more types of endophytes [4]. These endophytes can be either bacteria or fungi [5,6]. Their population density in a host plant can vary from hundreds to more than 9 x 109 bacteria per gram of plant tissue [7,8, 9]. They can be either obligate or a facultative and the obligate types cannot be cultured due to their specificity of growth conditions. On the other hand, facultative endophytes can be cultured outside the plant tissue using artificial nutrient media [10, 11]. Endophytes form an important part of the micro-ecosystem inside plant tissues [12]. The most explored endophytes are non-pathogenic fungi that provide a number of useful characteristics to their host plant. However, bacterial endophytes remain an unexplored group [13]. Any bacteria which could be isolated from a surface-sterilized plant or extracted from its tissues can be called an endophyte if it does not affect the plant negatively. Bacteria can positively promote plant growth whereas studies show that plants are able to select these beneficial bacterial members in their microbiome including those inside the plant tissues [14, 15, 16]. There is no shred of evidence suggesting that these bacteria take advantage in this relationship [17], but certainly, they get protection from pathogens in adverse times. They could also communicate much better than the rhizospheric bacteria at times of stress [18,19]

Harnessing the Pedosphere Microbial Diversity in Sustainable Agriculture Production

Chapter

Jun 2022

There is a need to increase food productivity due to the ever-increasing human population worldwide. Modern agriculture practices including extensive application of synthetic chemicals for crop production and protection have led to decreased soil fertility and other hazards to the environment. However, the exploration of a wide range of microorganisms inhabiting the soil can improve crop growth and productivity. The plant–microbe interaction forms an important network in agriculture. The beneficial soil microorganisms including arbuscular mycorrhizal (AM) fungi, plant growth-promoting rhizobacteria (PGPR), nutrient-solubilizing bacteria, cyanobacteria, some groups of protozoa, and nematodes have a crucial role in plant’s growth promotion, nutrient acquisition, imparting tolerance against different environmental stresses, and improving soil structure. Some of the important mechanisms involved in soil microbe-mediated processes are improved plant growth including phytohormone production, nutrient solubilization, and suppression of phytopathogens. The development of bioinoculants using efficient microbial consortiums can reduce the dependence on chemical fertilizers and could enhance crop productivity even under stressful conditions in an eco-friendly and cost-effective manner. In addition, soil health is strongly related to sustainable agriculture as the diversity and activity of soil microorganisms form a vital part of soil health. Therefore, in this chapter, we highlight the diversity of beneficial microbes in the pedosphere and their role in sustainable agriculture production.

Piriformospora indica , gen. et sp. nov., a new root-colonizing fungus

Article

Full-text available

Sep 1998

A new fungus isolate was discovered in an arbuscular mycorrhizal fungal spore from a desert soil in India. It could easily be cultivated on various synthetic media, and formed pear-shaped chlamydospores. Inoculation of maize showed that the fungus colonized the root cortex. Since it did not resemble any known fungus based on morphology and ultrastructure, a new genus was described. For its characteristic spore structure the isolate was named Piriformospora indica. Electron microscopy revealed the presence of typical dolipores with continuous parenthesomes, which indicated that P. indica belongs to the Hymenomycetes (Basidiomycota). DNA was extracted and the 5′ end of the 18S rRNA was amplified and sequenced. Comparison with sequences from the Genbank data base indicated that P. indica is related to the Rhizoctonia group.

O grzybie korzeniowym Mycelium radicis atrovirens Melin [Der Wurzerlpilz Mycelium radicis atrovirens Melin]

Article

Full-text available

Jul 2018

Karol Mańka

Utilization of major detrital substrates by dark-septate, root endophytes

Article

Mar 2000

Utilization of major forms of carbon, nitrogen and phosphorus commonly present in plant litter and detritus was determined for cultures of Phialophora finlandia, Phialocephala fortinii and five dark-septate, root endophyte isolates from alpine plant communities. All cultures utilized cellulose, laminarin, starch and xylan as sole carbon source. Protein and ribonucleic acids were hydrolyzed by all cultures as sole nitrogen and phosphorus sources, respectively. The fatty acid ester, Tween 40, was hydrolyzed by all cultures. None of the cultures decolorized two polymeric dyes used as presumptive tests for lignolytic activity. These hydrolytic capabilities suggest that these dark-septate root endophytes, either as biotrophs or saprotrophs, are able to access major organic detrital nutrient pools.

Phialocephala victorinii sp. nov., endophyte of Cypripedium parviflorum

Article

May 2000

A new hyphomycete Phialocephala victorinii sp. nov. is an endophyte isolated from living roots of the terrestrial orchid Cypripedium parviflorum. Phialocephala victorinii is typical of the genus in morphology and ecology, but clearly different from other known species of Phialocephala in having characters not previously described: slow growing colony, dark brown to golden brown on malt agar, and sporulating readily on corn meal agar, bearing regular conidiophores, sterile lateral protuberances present on hyphae in fertile region and not on the conidiophores, stipe base and apex subhyaline, collarettes extremely expanded, and conidia of two kinds: dark brown, obovoid or lunate, and light brown, allantoid conidia. Its sensitivity to cycloheximide suggests an affinity inside Phialocephala and no teleomorph connection with Ophiostoma. The taxonomic placement of the new species and a key to the members of Phialocephala are given.

The Mycorrhizal Status of Plants at Alexandra Fiord, Ellesmere Island, Canada, a High Arctic Site

Article

Jan 1990

On the eastern coast of central Ellesmere Island, adjacent to Alexandra Fiord (78°53′N, 75°55′W) is a lowland arctic oasis with relatively lush and diverse vegetation compared to the polar desert and ice fields that cover most of the surrounding area. Twenty-four species of plants were sampled at this site and their roots examined for fungal colonization. Although 19 species showed some irregular, interor intracellular colonization by rhizosphere fungi or endophytes, only 11 species could, by the morphology and extent of the fungal colonization, be classified as mycorrhizal. Dark-walled, septate endophytes and Cenococcum-type mycorrhizal infections were not observed in our samples. Colonization classified as ectomycorrhizal was observed in Salix arctica, Dryas integrifolia, Pedicularis capitata, Saxifraga oppositifolia, Cassiope tetragona, and Kobresia myosuroides. Colonization classified as ericoid mycorrhizal was observed in Vaccinium uliginosum, Cassiope tetragona, and possibly in Carex nardina and Silene acaulis. Arbutoid mycorrhizae were observed in Pyrola grandiflora. Endomycorrhizae, with non-septate hyphae and arbuscles, but no vesicles, were observed in only one species, Dryopteris fragrans. The paucity of VA-mycorrhizal colonization in herbaceous species was notable at this site, especially when compared to reports for the same species from other arctic and alpine sites.

Fungal endophytes of Dryas octopetala from a high arctic polar semidesert and from the Swiss Alps

Article

May 1995

Endophytes were isolated from leaves, stems and roots of Dryas octopetala sampled in Switzerland and Spitsbergen. Endophyte assemblages from different sites and at different sampling times were diverse. Seventy-three species were isolated in the four sites examined and 38 had frequencies of more than 10% in at least one sample. Samples from the subalpine region were generally richer in species than those collected in the alpine or Arctic regions. Leaves tended to host more endophyte taxa than twigs or roots.

Microbial Root Endophytes

Book

Jan 2006

Plant roots may not only be colonized by mycorrhizal fungi, but also by a myriad of bacterial and fungal root endophytes that are usually not considered by the investigators of classic symbioses. This is the first book dedicated to the interactions of non-mycorrhizal microbial endophytes with plant roots. The phenotypes of these interactions can be extremely plastic, depending on environmental factors, nutritional status, genetic disposition and developmental stages of the two partners. The book deals with diversity, life history strategies, interactions, applications in agriculture and forestry, methods for isolation, cultivation, and both conventional and molecular methods for identification and detection of these endophytes. The comprehensive reviews demonstrate the high diversity of interactions and will provoke further studies to better understand the mechanisms which determine whether a plant-microbial interaction remains asymptomatic, leads to disease or to a mutualistic interaction.

Ectomycorrhizae and growth of Douglas-fir seedlings preinoculated with Rhizopogon vinicolor and outplanted on eastern Vancouver Island

Article

Jan 1993

Ectomycorrhizal colonization of container-growth Pseudotsuga menziesii inoculated with Rhizopogon vinicolor was determined after cold storage and after one growing season. Inoculated Douglas-fir seedlings were taller than noninoculated controls when outplanted but, perhaps because of browse damage, no growth differences were found after one field season. Rhizopogon colonized almost half of the control and 10% of the inoculated seedlings before outplanting. After one field season, inoculated and control seedlings were colonized by 15 ectomycorrhizal fungi each, only eight of which were found on both. -from Authors

Cephalosporium maydis is a distinct species in the Gaeumannomyces-Harpophora species complex

Article

Nov 2004

Cephalosporium maydis is an important plant pathogen whose phylogenetic position relative to other fungi has not been established clearly. We compared strains of C. maydis, strains from several other plant-pathogenic Cephalosporium spp. and several possible relatives within the Gaeumannomyces-Harpophora species complex, to which C. maydis has been suggested to belong based on previous preliminary DNA sequence analyses. DNA sequences of the nuclear genes encoding the rDNA ITS region, β-tubulin, histone H3, and MAT-2 support the hypothesis that C. maydis is a distinct taxon within the Gaeumannomyces-Harpophora species complex. Based on amplified fragment length polymorphism (AFLP) profiles, C. maydis also is distinct from the other tested species of Cephalosporium, Phialophora sensu lato and members of Gaeumannomyces-Harpophora species complex, which supports its classification as Harpophora maydis. Oligonucleotide primers for H. maydis were developed that can be used in a PCR diagnostic protocol to rapidly and reliably detect and identify this pathogen. These diagnostic PCR primers will aid the detection of H. maydis in diseased maize because this fungus can be difficult to detect and isolate, and the movement of authentic cultures may be limited by quarantine restrictions.

Soil Fungi and Soil Fertility.

Article

Jul 1964

Fungal Root Endophytes

Abstract

Recommended publications

The use of an aquatic microcosm for pollution effects assessment

Etude expérimentale des voies d'élimination de l'azote en présence de trois microalgues - Synechocys...

Temporal Responses of the Macrophyte, Potamogeton perfoliatus L., and Its Associated Autotrophic Com...

The influence of macrofauna on estuarine benthic community metabolism: a microcosm study