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ORIGINAL PAPER
Arbuscular, ecto-related, orchid mycorrhizas—three
independent structural lineages towards
mycoheterotrophy: implications for classification?
Stephan Imhof
Received: 4 November 2008 /Accepted: 17 March 2009 /Published online: 27 March 2009
#Springer-Verlag 2009
Abstract The classification of mycorrhizas in seven equally
ranked types glosses over differences and similarities and, in
particular, does not acknowledge the structural diversity of
arbuscular mycorrhizas. This article emphasizes the parallel
continua of ecto-related mycorrhizas and arbuscular mycor-
rhizas, exemplified within Ericaceae and Gentianales,
respectively, as well as the proprietary development of
orchid mycorrhizas, all three of which have independently
developed mycoheterotrophic plants. A hierarchical classi-
fication according to structural similarities is suggested.
Keywords Arbuscular mycorrhiza .Ectomycorrhiza .
Orchid mycorrhiza .Mycorrhizal structures .
Mycorrhizal classification .Mycoheterotrophy
Introduction
Classification of mycorrhizas started with Frank (1887) who
distinguished between ectotrophic and endotrophic mycor-
rhizas (including ericoid and orchid mycorrhizas), which
were amended by Melin (1923, p. 95) adding “ectendo-
trophic.”In a rarely cited paper, Dominik (1956) accepted
the two main types of Frank (1887) and the subdivision of
endotrophic mycorrhizas by Burgeff (1943) but suggested a
refined classification of ectotrophic mycorrhizas in 12
subtypes (A through L). After some debate on the suffix
instead of -trophic, suggesting -cellular (Wilde and Lafond
1967) and -mycorrhiza (Peyronel et al. 1969), Lewis (1973)
proposed a new classification using “sheathing,”“vesicular-
arbuscular”(formerly treated as an endomycorrhiza),
“ericaceous,”and “orchidaceous,”which is close to the
top level types suggested much later by Brundrett (2004).
Interestingly, Trappe (1987), not explicitly categorizing
mycorrhizas, summarized “zygomycotous”and “asco-
and basidiomycotous”(including ericoid mycorrhiza) in
his taxonomic accounts of mycorrhizas, coming close to the
view expressed in the present article.
Currently, mycorrhizas are classified into seven types of
equal rank: arbuscular (AM), ecto- (ECM), ectendo-,
arbutoid, ericoid, monotropoid, and orchid mycorrhiza
(Smith and Read 2008). However, AM have turned out to
be much more diverse in structural features than previously
thought (e.g., Widden 1996; Imhof 1997,1999a,2003,
2007; Dickson 2004; Dominguez and Sérsic 2004),
whereas the distinctions between ecto-, ectendo-, and
arbutoid mycorrhizas are slight (e.g., Brundrett 2004; Smith
and Read 2008). Thus, ranking all these types at the same
level runs the risk of overemphasizing the distinctions
between ecto-related types and glosses over the consider-
able structural diversity of AM.
The present article argues for the recognition of three
structural lineages of mycorrhizas, ecto-related, arbuscular,
and orchid, as mycorrhizal groups in a hierarchical system
keeping the established names for the well-known mycor-
rhizal syndromes as mycorrhizal types. This approach is
from the plant perspective and based on the notion that the
phenotype of mycorrhizas, like any other functional feature
of plants and fungi, is subject to evolution. Hence, it is not
surprising that ecto-related associations can be linked by
gradual morphological-anatomical changes (Fig. 1) and
thus represent an analogous mycorrhizal continuum as
stated for AM by Dickson (2004). These changes become
even more convincing if they are paralleled by other
Mycorrhiza (2009) 19:357–363
DOI 10.1007/s00572-009-0240-7
S. Imhof (*)
Spezielle Botanik und Mykologie, Fachbereich Biologie,
Philipps-Universität,
35032 Marburg, Germany
e-mail: imhof@staff.uni-marburg.de
structural trends pointing in the same direction. In fact, the
two monophyla Ericaceae and Gentianales (APG 2003)
exemplify the evolutionary trend from trees to mycohetero-
trophic herbs paralleled by changes of ecto-related mycor-
rhizal types and AM, respectively.
The ECM group
In order to sketch a putative morphological progression within
ecto-related mycorrhizas (Fig. 1), we may start with ECM as
listed by Smith and Read (2008), who did not distinguish
between cortical and epidermal types. Cortical ECM in
gymnosperms (Brundrett 2004) already shows the tendency
towards intracellular colonization in the ectendomycorrhiza
(e.g., Yang and Wilcox 1984; Scales and Peterson 1991;Yu
et al. 2001). The epidermal ECM (Brundrett 2004) not only
of the Fagales but also in Ericaceae (Largent et al. 1980;
Smith et al. 1995; Richard et al. 2005)onlydifferinbeing
restricted to the root epidermis. The switch to arbutoid
mycorrhiza of some Ericaceae (Scannerini and Bonfante-
Fasolo 1983; Massicotte et al. 1993) is an identical structural
change as from cortical ECM to ectendomycorrhiza. It still
keeps hyphal mantle and hartig net of the epidermal ECM
but shows intracellular colonization of the epidermis.
Recently, a morphotype of arbutoid mycorrhiza, coined
cavendishioid, was reported from the hemiepiphytic Caven-
dishia nobilis (Ericaceae), where the hartig net is less promi-
nent and the intracellular hyphal phase comprises swollen
hyphae (Setaro et al. 2006). In the herbaceous Pyrola
(Furman and Trappe 1971), either considered to be arbutoid
mycorrhizal (e.g., Peterson and Farquhar 1994) or ectendo-
mycorrhizal (Wang and Qiu 2006), it is not the hartig net
but the hyphal mantle that can be reduced, whereas the
hyphae still build dense intracellular coils in the epidermis
(Robertson and Robertson 1985). These “pyroloid”(as such
referred to by Cullings 1996) and cavendishioid morpho-
types underline the plasticity of ecto-related mycorrhizas
and corroborate the notion of gradual evolutionary changes
within the lineage. There might be even more findings in the
future, showing other combinations of lack or differentiation
of the three components mantle, hartig net, and intracellular
colonization. In fact, one conceivable combination, namely
the reduction of both the hyphal mantle and the hartig net
keeping the hyphal coils in the rhizodermis, have already
been found: the ericoid mycorrhiza. The similarities of
ectomycorrhizas, ectendomycorrhiza, arbutoid, and mono-
tropoid mycorrhizas have been already acknowledged by
Brundrett (2004). However, the ericoid mycorrhizas also
(see Read 1996) have much closer morpho-anatomical
affinities to ectomycorrhiza than to orchid or arbuscular
mycorrhiza (e.g., Cullings 1996, Wang and Qiu 2006). Not
only are the fungi involved in ectomycorrhizas and ericoid
mycorrhizas closely related so that one fungus species may
develop ecto-, ectendo-, as well as ericoid mycorrhizas in
different hosts (e.g., Björkman 1960; Monreal et al. 1999;
Bergero et al. 2000; Vrålstad et al. 2000;Yuetal.2001;
Perotto et al. 2002; Villarreal-Ruiz et al. 2004). There are
also reports of intermediate structural features in ericoid
mycorrhizas such as hyphal mantles (Xiao and Berch 1996;
Rains et al. 2003) and residues of a hartig net (Bergero et al.
2000; Rains et al. 2003) and likewise reports of arbutoid
mycorrhizas with hardly a hyphal mantle (Fusconi and
Bonfante-Fasolo 1984). Moreover, arbutoid and ericoid
mycorrhiza have obvious structural similarities with the
only difference of some intercellular hyphae in the former
(compare e.g., Figures 188/189 and 171 in Peterson et al.
2004) and already Harley (1969) assumed the arbutoid
mycorrhiza to link ectomycorrhiza and ericoid mycorrhiza.
Eventually, in the monotropoid mycorrhizas of the achloro-
phyllous Sarcodes sanguinea and Pterospora andromedea
(Robertson and Robertson 1982)andMonotropa hypopitys
(Duddridge and Read 1982), the intracellular phase of the
mycorrhiza is reduced to a fungal peg (Duddridge and Read
1982). Taking the advanced character of these achlorophyl-
lous species and their necessity for an efficient mycorrhiza
into account, the fungal pegs are best interpreted as coil
rudiments, as such omitting the presumably retarding coil
development, and directly “burst”(Duddrigde and Read
1982) their content into the cells. Within the monotropoid
mycorrhizas, we may even distinguish two morphotypes: in
Monotropa the pegs go through the outer periclinal wall of
the epidermis (Lutz and Sjolund 1973; Duddridge and Read
1982), whereas in Sarcodes and Pterospora they penetrate
the radial walls (Robertson and Robertson 1982).
Interestingly, this lineage of ecto-related mycorrhizas is
roughly parallel to the morphological reduction from trees to
mycoheterotrophic plants in Ericaceae. Henderson (1919),
based on extensive morphological-anatomical investigations,
drew a line of reduction from the woody Ericaceae (trees,
Fig. 1 Hierarchy of structural
changes linking the types and
morphotypes of ECM group,
“Pyroloid”based on Robertson
and Robertson (1985) and
“Pisonioid”based on Ashford
and Allaway (1982)
358 Mycorrhiza (2009) 19:357–363
shrubs, and sub-shrubs) over the herbaceous Pyrolaceae to
the achlorophyllous Monotropaceae and already challenged
the family delimitations. In fact, the latter two taxa are
nowadays considered as Monotropoideae in Ericaceae (Kron
et al. 2002). With respect to the Pyrolaceae/Monotropaceae
complex, Furman and Trappe (1971) further refined this
progression line. They stressed the parallel trends of the
reduction of leaves associated with evolution of achloro-
phylly and the abbreviation of the root systems from fibrous
roots over coralloid root systems, reaching the stage of
tight root balls in Monotropa or Pterospora (see Table 2 in
Furman and Trappe 1971).
The AM group
The structural diversity of AM apart from the types
described by Gallaud (1905) has been discovered rather
recently (e.g., Widden 1996; Imhof 1998,1999b,c,2001,
2006; Dominguez and Sérsic 2004; Dickson 2004; Beck
et al. 2005). Despite the substantial differences between the
morphotypes, most authors refrained from naming them, in
contrast to the ecto-related mycorrhizas. Nevertheless, the
AM morphotypes can likewise be linked according to
morphological differences (Fig. 2). The Gentianales are a
good example where the predominantly intercellular Arum
type is linked by intermediate types to the exclusively
intracellular Paris type (Gallaud 1905; Smith and Smith
1997; Dickson 2004; Appelhans et al. 2008), all types of
which are found in Apocynaceae (Tiemann et al. 1994a,
1994b; Untch and Weber 1995; Weber et al. 1995). Further-
more, the Paris type shows numerous morphological
deviations in achlorophyllous species not only in the
Gentianaceae (e.g., Imhof 1998,1999c,2001,2007; Imhof
and Weber 2000). The fossil record suggests the Arum type
to be the oldest mycorrhiza (Kidston and Lang 1921; Remy
et al. 1994; Taylor et al. 1995), but it is difficult to detect an
evolutionary trend of AM types, since they are scattered all
around the plant kingdom (Smith and Smith 1997; Dickson
et al. 2007).
At the family level, however, evolutionary changes of
AM pattern can be found. Within Gentianaceae, exclusively
having Paris type AM, there are chlorophyllous (shrubs,
sub-shrubs, and herbs), semichlorophyllous (Obolaria and
Bartonia, Holm 1897,1906), and achlorophyllous genera
(Voyria,Voyriella, and Sebaea oligantha) showing pro-
nounced morphological reductions. These are very similar
to those described in Ericaceae, also paralleled by changes
of mycorrhizal structures. Voyria truncata shows runner-
like, plagiotropic roots (Imhof et al. 1994); intermediate
roots are present in e.g., Voyria aphylla (Imhof 1999c)
and Voyria rosea (Maas and Ruyters 1986); and small
Fig. 2 Hierarchy of structural
changes linking the types and
morphotypes of AM group
(T. type, div. diverse). “Paired
arbuscule”after Dickson et al.
(2003)
Table 1 Classification of mycorrhizas
AM group (Fig.1) ECM group (Fig.2) OM group Ill-defined group
Arum type
a
Cortical ECM
d
Tolypophagous type?
h
e.g., Mycorrhiza in Thysanotus (McGee 1988),
Dark Septate Endophyte (Jumpponen 2001;
Mandyam and Jumpponen 2005)
Intermediate types
b
Ectendomycorrhiza Ptyophagous type?
h
Paris type
c
Epidermal ECM
d,e
Arbutoid mycorrhiza
f
Ericoid mycorrhiza
Monotropoid mycorrhiza
g
a
Includes one morphotype with “paired arbuscules”(Dickson et al. 2003)
b
Morphotypes see Dickson (2004)
c
Includes many morphotypes especially in mycoheterotrophic plants
d
Extensive morphotyping done by Dominik (1956) and Agerer (1995)
e
Includes morphotype in Pisonia grandis (Ashford and Allaway 1982)
f
May include morphotypes in Cavendishia nobilis (Setaro et al. 2006) and Pyrola (Robertson and Robertson 1985)
g
May include morphotypes in Monotropa (Duddridge and Read 1982) as well as Sarcodes and Pterospora (Robertson and Robertson 1982)
h
More structural investigations required
Mycorrhiza (2009) 19:357–363 359
star-like root systems exist in Voyria tenella (Imhof 1997),
Voyria obconica (Imhof and Weber 2000), or Voyria
flavescens (Franke 2002). This is strikingly similar to the
root systems in Monotropoideae (see Furman and Trappe
1971). Farther like Pyrola,Sarcodes,Pterospora,and
Monotropa that show specialized mycorrhizal forms of the
ECM group, Voyria spp. develop little (V. truncata, Imhof
and Weber, 1997) but also strongly deviant colonization
pattern of Paris type AM (e.g., V. tenella, Imhof 1997),
which are linked by a structurally mediating pattern in V.
aphylla (Imhof 1999c). Ecto-related mycorrhizas and AM
thus appear as parallel structural lineages of mycorrhizas,
both culminating in the evolution of mycoheterotrophic
plants.
The OM group
I propose orchid mycorrhiza (OM) as the third distinct
structural lineage of mycorrhizas in addition to ecto-related
and arbuscular mycorrhiza. Although the fungi in some,
mostly achlorophyllous orchids have been proved to develop
ECM in other plants (e.g., Warcup 1985; Taylor and Bruns
1997; McKendrick et al. 2000; Selosse et al. 2002,2004;
Julou et al. 2005; Girlanda et al. 2006; Dearnaley 2007;
Ogura-Tsujita and Yukawa 2008; Zimmer et al. 2008), the
morpho-anatomical gap between ECM and OM and, most
notably, the lack of intermediate forms are good reasons to
retain it as a separate mycorrhizal group. Moreover, most
root fungi in orchids have no mycorrhizal but saprophytic or
parasitic life forms (see list in Rasmussen 2002), signifying
a group of fungi newly adopted by orchids for their needs. A
morphological progression within OM, as suggested above
for the ECM and AM groups, is not yet apparent. Possibly,
the two forms of OM already described by Burgeff (1932)
as “tolypophagy”(digestion of coils) and “ptyophagy”
(releasing fungal content into the cell), which gained a
revival after the description of Wang et al. (1997)on
Gastrodia elata (see also Rasmussen 2002), may be signs of
progressive changes.
Interestingly, ptyophagy in OM is restricted to myco-
heterotrophic orchids, just as the monotropoid mycorrhiza
is restricted to the achlorophyllous Monotropoideae. At all,
the ptyophagy in the mycoheterotrophic G. elata shows
remarkable similarities to the fungal pegs of monotropoid
mycorrhiza, both showing vermiform protrusions from the
penetrating fungal peg (compare Fig. 2e or 3c in Duddridge
and Read 1982 with Figs. 7 and 8 in Wang et al. 1997).
Burgeff (1943) even explicitly called the mycorrhiza in M.
hypopitys ptyophagy, too. So far, the mycorrhizas of six
Gastrodia species (Kusano 1911; Burgeff 1932; McLennan
1959; Campbell 1962,1963,1964; Wang et al. 1997) and
Lecanorchis javanica (Janse 1896) have been shown to be
ptyophagous. Further structural research on more of the
over 200 achlorophyllous orchids (Leake 1994) is urgently
needed.
Conclusions
The degree of structural diversity within the arbuscular
mycorrhizas (rarely named) is as remarkable as the differences
among the ecto-related mycorrhizas (ecto-, “pisonioid,”
ectendo-, arbutoid, cavendishoid, “pyroloid,”ericoid, and
monotropoid mycorrhizas; expressions which have not been
explicitly coined in double quotes). Within the monophyla
Gentianales (AM) and Ericaceae (ecto-related), both struc-
tural lineages of mycorrhiza can even be considered as
phylogenetically cohesive, indicated by the gradual changes
of mycorrhizal structures in a line from woody autotrophic to
herbaceous mycoheterotrophic plants. Hence, ranking all
established mycorrhizal types at the same level camouflages
known differences and similarities. The three-level hierar-
chical classification suggested here (Table 1) may still not be
able to exactly mirror the structural evolution of mycor-
rhizas. However, it is useful for both expression of
distinction as well as affinities and also is better adaptable
to integrate new findings. It distinguishes three mycorrhizal
groups representing the most distinctive structural lineages,
all of which independently developed mycoheterotrophy:
ECM, AM, and OM. Each group comprises mycorrhizal
types, where we find the well known and named structural
syndromes such as e.g., Paris type, ectendomycorrhiza, or,
monotropoid mycorrhiza. The mycorrhizal types may be
subdivided into morphotypes, which are often less known
(e.g. cavendishioid) and even unnamed (e.g., mycorrhiza in
Afrothismia spp. or Pisonia grandis). Little known associ-
ations are summarized as “Ill-defined”until more informa-
tion allows proper integration.
Acknowledgments Many thanks to Andrew Smith (Adelaide) and
three anonymous referees for their valuable comments on the
manuscript.
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