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Submitted 12 July 2016, Accepted 5 September 2016, Published online 26 September 2016 582
Corresponding Author: To-anun C – e-mail – agppi006@chiangmai.ac.th
Mycosphere Essays 13 – Do xylariaceous macromycetes make up most
of the Xylariomycetidae?
Daranagama DA1,2, Jones EBG3, Liu XZ1, To-anun C3*, Stadler M1,4 and Hyde
KD2
1 State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, No 31 st West Beichen
Road, Chaoyang District, Beijing, 100101, People’s Republic of China.
2 Centre of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand.
3 Division of Plant Pathology, Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai
University, Chiang Mai 50200, Thailand.
4 Helmholtz-Zentrum für Infektionsforschung GmbH, Dept. Microbial Drugs, Inhoffenstrasse 7, 38124, Braunschweig,
Germany.
Daranagama DA, Jones EBG, Liu XZ, To-anun C, Stadler M, Hyde KD. 2016 – Mycosphere
Essays 13 – Do xylariaceous macromycetes make up most of the Xylariomycetidae? Mycosphere
7(5), 582–601, Doi 10.5943/mycosphere/7/5/5
Abstract
In this essay, we focus on the micro-xylariaceous genera (with inconspicuous ascomata and
asexual morphs) in the Xylariomycetidae, with special emphasis on Xylariaceae. Are micro-
xylariaceous less diverse than macro-xylariaceous genera (with conspicuous stromata) genera? This
paper also reviews their taxonomic significance and current systematic relationship and evaluates
different characters used in their taxonomic placement. So far, only a few micro-xylariaceous taxa
have been studied in detail in comparison with the stromatic macroscopic xylariaceous taxa and the
reasons for this are discussed. It is hoped that further sampling and study of different substrata and
habitats, with greater emphasis on sequence data, may lead to the discovery of many more micro-
xylariaceous genera.
Key words – Ascomycetes – micro-Xylariaceae – taxonomy – phylogeny – Xylariales
Introduction
The family Xylariaceae (Sordariomycetes, Xylariomycetidae, Xylariales) comprises 87
genera and more than 1300 species (Maharachchikumbura et al. 2015, 2016). The Xylariaceae is
one of the largest and well known families of Ascomycota, and has a worldwide distribution
(Maharachchikumbura et al. 2015, 2016). The Xylariaceae are important wood degraders, but some
are endophytes and others plant pathogens (Petrini et al. 1995, Edwards et al. 2003). Most
xylariaceous species inhabit wood, while others are encountered on dung or associated with insect
nests, such as termites and ants, with several species being economically important as plant
pathogens (Edwards et al. 2003, Visser et al. 2009, Hsieh et al. 2010). Xylariaceae species exhibit a
great diversity in tropical regions, from where many new taxa are described (Whalley et al. 1996,
Rogers 2000, Stadler et al. 2013, Kuhnert et al. 2014, Daranagama et al. 2014, 2015 a, c, Liu et al.
2015, Ariyawansa et al. 2015, Li et al. 2016). Species delimitation in Xylariaceae is complicated as
they exhibit a diverse range of morphological characters, ranging from massive, stalked or sessile
Mycosphere 7 (5): 582–601 (2016) www.mycosphere.org ISSN 2077 7019
Article
Doi 10.5943/mycosphere/7/5/5
Copyright © Guizhou Academy of Agricultural Sciences
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stromata, to minute rudimentary stromata with ascomata immersed in the substrata. Typically
xylariaceous species are characterized by pigmented, aseptate ascospores, frequently with a germ
slit. The asci, which have a conspicuous apical apparatus, are usually found in perithecia embedded
in stromata of Xylariaceae species (Stadler 2011, Maharachchikumbura et al. 2016).
Intrageneric and intergeneric relationships of Xylariaceae with other related families in
Xylariomycetidae are not well-studied (Stadler 2011). The lack of available data for this large
group is a major drawback in establishing the boundaries among genera, as well as families.
However, recent comprehensive phylogenetic studies have contributed much knowledge towards
the interpretation of generic and familial relationships of the Xylariomycetidae (Stadler et al. 2013,
Daranagama et al. 2015a, b, Maharachchikumbura et al. 2015, 2016, Senanayake et al. 2015).
Most stromatic Xylariaceae are well-studied and characterized based on morphology and
phylogeny. Genera such as Annulohypoxylon, Daldinia, Entonaema, Hypoxylon, Rhopalostroma
and Xylaria have been studied extensively for their morphology and phylogeny, as well as chemical
profiles and chemotaxonomic relationships (Ju & Rogers 1996, Hsieh et al 2005, 2010, Stadler et
al. 2010a, b, 2014a, b, Daranagama et al. 2014, 2015c, Kuhnert et al. 2014, 2015). Unfortunately,
most of the non stromatic, microscopic genera in Xylariaceae are less well-studied, and their
affinities to other genera and families are poorly established. Appendixia, Calceomyces, Emarcea,
Halorosellinia, Helicogermslita, Induratia and Xylotumulus are a few examples. Most of these
genera are only known from their type collections and some are restricted to specific localities or
habitats (Figures 1, 2), while some are recently collected and monotypic. Therefore, they have not
been phylogenetically analyzed for their taxonomic placements. In this paper we address the
reasons why the non stromatic xylariaceous fungi have been neglected and are less well-studied.
Micro-Xylariaceae and Macro-Xylariaceae
The concept of defining the xylariaceous fungi as micro-Xylariaceae and macro-
Xylariaceae is rather subjective. There is no established protocol or a set of guidelines for this
distinction. It is also noteworthy that some species in genera that mainly contain taxa usually
characterized by conspicuous stromata can have species with relatively minute ones. For example,
in the genus Xylaria, species such as X. albocincta (Rehm) Y.M. Ju et al., X. carabayensis (Mont.)
Y.M. Ju et al. and X. discolor (Berk. & Broome) Y.M. Ju et al. have small, discoid to pulvinate,
soft stromata (Ju et al. 2012). On the other hand, several asexual states are classified in the genera
known as ―larger‖ Xylariaceae. Likewise the precise circumscriptions of the genera may not be
possible at this stage with the available data. Thus our attempt at defining micro-Xylariaceae and
macro-Xylariaceae genera may be suspended until more data are available and more taxa are
discovered especially with the recollected type species.
The cardinal feature of Xylariaceae is perithecial ascoma embedded in more or less well-
developed stromata (Rogers 2000) although some micro-Xylariaceae taxa even lack stromata (eg.
Anthostomella, Brunneiperidium, Lunatiannulus, Occultitheca). Except for a few micro-
xylariaceous, asexual genera discovered in earlier decades, most of the common xylariaceous
species discovered by early mycologists possessed massive stromata, for example, Daldinia,
Entonaema, Engleromyces, Hypoxylon, Sarcoxylon, Squamotubera and Xylaria. These large-sized
Xylariaceae are often referred to as ―macrofungi‖ in the popular mycological literature. However,
several xylariaceous species lack stromata or have reduced stromata, and are usually referred to as
―microfungi‖. These microfungal taxa are immersed in the host tissue, visible only as blackened
dots or areas even under a stereoscope. Some examples are Anthostomella, Appendixia,
Brunneiperidium, Cannonia, Fasciatispora, Lunatiannulus, Nipicola, Occultitheca, Pandanicola,
Pyriformiascoma, Sabalicola and Spirodecospora.
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Table 1 Comparison of Micro-Xylariaceae and Macro-Xylariaceae and their major studies
Genus
Molecular
data
Key references
Micro-Xylariaceae
Amphirosellinia$
Yes
Ju et al. (2004)
Anthocanalis$
Yes
Daranagama et al. (2015a)
Anthostomella
Yes
Francis (1975)
Francis et al. (1980)
Hyde (1996)
Lu & Hyde (2000a)
Lu & Hyde (2000b)
Daranagama et al. (2015a)
Jones et al. (2015)
Appendixia
No
Lu et al. (2000c)
Areolospora
No
Jong et al. (1974)
Hawksworth (1980)
Ascotricha$
= Dicyma
= Puciola
Yes
Hawksworth (1971)
Berkeley (1838)
Cheng et al. (2015)
Astrocystis$
Yes
Berkeley & Broome (1873)
Læssøe et al. (1994)
Dulymamode et al. (1998)
Jones et al. (2015)
Barrmaelia
Yes
Rappaz (1995)
Brunneiperidium$
Yes
Daranagama et al. (2015a)
Calceomyces$
Yes
Udagawa & Ueda (1988)
Cannonia
No
Taylor & Hyde (1999)
Chaenocarpus
No
Rebentisch (1804)
Collodiscula$
= Acanthodochium
Yes
Hino et al. (1955)
Réblová et al. (2016)
Coniolariella$
= Coniolaria
Yes
García et al. (2006)
Cyanopulvis
No
Fröhlich & Hyde (2000)
Emarcea$
Yes
Duong et al. (2004)
Fasciatispora$
Yes
Hyde (1991)
Alias et al. (1994)
Halorosellinia$
Yes
Whalley et al. (2000)
Schlingham et al. (1998)
Xia et al. (2007)
Helicogermslita
No
Hawksworth & Lodha (1983)
Hypocopra
Yes
Kirk (1867)
Spegazzini (1880)
Saccardo & Saccardo (1905)
Krug & Cain (1974)
Hypocreodendron
= Discoxylaria*$
No
Lindqvist & Wright (1964)
Rogers et al. (1995)
Réblová et al. (2016)
Leptomassaria
No
Petrak (1914)
Ahmad & Lodhi (1953)
Munk (1957)
Lunatiannulus$
Yes
Daranagama et al. (2015a)
Myconeesia
No
Kirschstein (1936)
Nipicola
No
Hyde (1992)
Hyde & Taylor (1996)
Fröhlich & Hyde (2000)
Jones et al. (2015)
Nodulisporium**
= Pleurographium
Yes
Cox et al. (1994)
Stadler et al. (2013)
585
Genus
Molecular
data
Key references
Occultitheca
No
Rogers & Ju (2003)
Ophiorosellinia
No
Rogers et al. (2004)
Pandanicola
No
Hyde (1994)
Paramphisphaeria
No
Fernández et al. (2004)
Paucithecium
No
Lloyd (1923)
Pyriformiascoma$
Yes
Daranagama et al. (2015a)
Rosellinia$
= Dematophora
= Vrikshopama
Yes
De Notaris (1844)
Saccardo (1913)
Ellis & Everhart (1890)
Smith & Ramsbottom (1915)
Rappaz (1995)
Spegazzini (1898)
Petrini (2003)
Petrini (2013)
Réblová et al. (2016)
Sabalicola
No
Hyde (1995)
Spirodecospora
No
Lu et al. (1998)
Striatodecospora
No
Zhou et al. (2000)
Virgaria$ = Ascovirgaria
Yes
Rogers & Ju (2002)
Réblová et al. (2016)
Macro-Xylariaceae
Annulohypoxylon$
Yes
Ju & Rogers (1996)
Hsieh et al. (2005)
Biscogniauxia$
Yes
Kuntze (1891)
Ju et al. (1998)
Camillea
= Basidiobotrys
= Masoniomyces
= Xylocladium
Yes
Fries (1849)
Læssøe et al. (1989)
Whalley et al.(1998)
San Martín et al. (1993)
Chlorostroma
No
Miller et al. (2007)
Daldinia$
= Annellosporium
= Versiomyces
Yes
Cesati & De Notaris (1863)
Stadler et al. (2014a)
Réblová et al. (2016)
Durotheca
No
Læssøe et al. (2013)
Engleromyces
No
Hennings (1900)
Whalley et al. (2010)
Entoleuca
Yes
Sydow & Petrak (1922)
Ju et al. (2004)
Entonaema
Yes
Möller (1901)
Martin (1938)
Rogers (1981)
Sihanonth et al. (1998)
Euepixylon$
Yes
Füisting (1867)
Læssøe & Spooner (1994)
Gigantospora
No
Lu & Hyde (2003)
Guestia
No
Smith & Hyde (2001)
Hypoxylon$
= Pyrenopolyporus
= Triplicaria
= Nodulisporium
Yes
Bulliard (1791)
Saccardo (1882)
Berkeley & Broome (1883)
Martin (1967)
Martin (1976)
Jones et al. (2015)
Rogers & Samuels (1985)
Ju & Rogers (1996)
Ju et al. (2005)
Réblová et al. (2016)
Induratia
No
Samuels et al. (1987)
Kretzschmaria$
= Holttumia
Yes
Fries (1849)
Saccardo (1883)
586
Genus
Molecular
data
Key references
Martin (1976)
Rogers & Ju (1998)
Pereira et al. (2009)
Hladki & Romero (2001)
Kretzschmariella
No
Viégas (1944)
Ju & Rogers (1994)
Leprieuria
No
Læssøe et al. (1989)
Nemania$
= Geniculisynnema
= Geniculosporium
Yes
Gray (1821)
Pouzar (1985)
Ju & Rogers (2002)
Ju et al. (2005)
Rogers et al. (2006)
Jones et al. (2015)
Réblová et al. (2016)
Obolarina$
Yes
Pouzar (1986)
Mirabolfathy et al. (2013)
Phylacia
Yes
Léveillé (1845)
Dennis (1957)
Speer (1980)
Rodrigues & Samuels (1989)
Medel et al. (2006)
Podosordaria$
Yes
Holway (1897)
Krug & Cain (1974)
Martin (1976)
Rogers & Læssøe (1992)
Hyde et al. (1996)
Rogers et al. (1998)
Poroleprieuria
No
González et al. (2004)
Poronia
= Lindquistia
Yes
Willdenow (1787)
Möller (1901)
Patouillard (1906)
Sydow et al. (1911)
Rogers et al. (1998)
Hembrom et al. (2013)
Pyrenomyxa
= Pulveria
Yes
Morgan (1895)
Stadler et al. (2005)
Rhopalostroma
Yes
Hawksworth (1977) Hawksworth et al.
(1979)
Hawksworth & Whalley (1985)
Whalley et al. (1998)
Kaur & Ojha (2000)
Stadler et al. (2010a)
Daranagama et al. (2014)
Rostrohypoxylon$
Yes
Fournier et al. (2010)
Ruwenzoria$
Yes
Stadler et al. (2010c)
Sarcoxylon$
Yes
Cooke (1883)
Petch (1924)
Patouillard (1927)
Rogers (1981)
Squamotubera
No
Hennings (1903)
Rogers (1981)
Stromatoneurospora$
Yes
Jong & Davis (1973)
Stilbohypoxylon
Yes
Hennings (1902)
Rogers & Ju (1997)
Hladki & Romero (2003)
Petrini (2004)
Pereira et al. (2009)
Thamnomyces
Yes
Nees von Esenbeck (1820)
Montagne (1834)
Cooke (1884)
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Genus
Molecular
data
Key references
Lloyd (1920)
Stadler et al. (2010b)
Theissenia$
Yes
Maublanc (1914)
Ju et al. (2003)
Ju et al. (2007)
Thuemenella
Yes
Penzig & Saccardo (1897)
Boedijn (1964)
Rifai & Webster (1965)
Dennis (1970)
Vivantia
No
Rogers et al. (1996)
Wawelia
No
Namyslowski (1908)
Minter & Webster (1983)
Lundqvist (1992)
Webster et al. (1999)
Xylaria$
= Moelleroclavus
= Padixonia
= Pseudoxylaria
= Xylocoremium
Yes
Schrank (1789)
Gray (1821)
Rogers et al. (1988)
San Martín et al. (1989)
San Martín et al. (2001)
Ju & Hsieh (2007)
Hladki & Romero (2010)
Hsieh et al. (2010)
Réblová et al. (2016)
Xylocrea
No
Möller (1901)
Smith (1901)
Rick (1906)
Xylotumulus$
Yes
Rogers et al. (2006)
$ – Reliable sequences of the respective type species are available
*– Sexual morph and stromatic Xylariaceae
**– Asexual state of several stromatic Xylariaceae
Microfungal genera in Xylariaceae
According to the outline provided by Maharachchikumbura et al. (2015) the family
Xylariaceae comprises 87 genera and more than 1300 species. Among these, over 30 genera may be
considered as microfungal with reduced reproductive structures or lacking stromata. Unlike the
well-known stromatic genera in Xylariaceae, the above mentioned microfungal genera have been
less well-studied and neglected by mycologists over a long time. Microfungal genera account for
almost 1/3 of the currently accepted genera of Xylariaceae, but databases such as Index Fungorum
and MycoBank, provide little data on these fungi.
“The Problem” with micro-xylariaceous genera
Stromatic Xylariaceae with their massive (up to 10 cm tall and sometimes even more),
conspicuous, highly developed stromata are well-represented in the tropics, while the less
conspicuous microfungal genera in Xylariaceae and other families of Xylariomycetidae, including
Amphisphaeriaceae, Apiosporaceae, Cainiaceae, Clypeosphaeriaceae, Coniocessiaceae,
Hyponectriaceae, Diatrypaceae, Melogrammataceae, Myelospermataceae and Vialaeaceae are less
collected and therefore poorly studied (Carroll 1988, Hyde and Wong 2000, Carmarán et al. 2006,
Daranagama et al. 2015a). Most stromatic Xylariaceae are readily visible to the unaided eye and are
often collected and well-characterized macroscopically. This is especially true in Xylariaceae in
which the gross morphology of the stromata has been described in detail, while microscopic
characters, such as ascomatal shape, peridium and ascal characters, have been less well-
documented (Miller 1961, Rogers 1981, Læssøe 1994, Rogers et al. 1997). However, with the
recent development of molecular phylogeny and chemical profiling, these stromatic Xylariaceae
genera are well-characterized and easily identified (Triebel et al. 2005, Stadler et al 2008, 2010a,
2014a, Daranagama et al. 2014).
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Fig. 1 – Appendixia closterium (Holotype) a. Herbarium details. b, c. Stromata in wood. d. Cross
section of stromata showing perithecia encased in stromatal tissue. e. Peridium. f, g. Mature asci. h.
Asci with apical apparatus slightly bluing in Melzer’s reagent. i, j. Ascospores with polar
appendages. Scale bars: d= 100 µm, e = 20 µm, f= 50 µm, g-h = 25 µm.
Comparatively very few micro-Xylariaceae have been carefully examined and even fewer
have been thoroughly studied using both morphology and phylogeny. The major reason for this
omission is the microscopic nature of the ascomata with apparent lack of any visible stromata.
Therefore, fewer micro-Xylariaceae have been collected over the past 100 years. Unlike the
stromatic Xylariaceae, the differences of micro-Xylariaceae mostly lie in their microscopic
characters such as, shape, size of ascomata, peridium characters, morphology of apical apparatus,
length and configuration of germ slits and also morphology of ascospores (Lu and Hyde 2000a, b
Réblová and Seifert 2004, Petrini 2013, Réblová 2013, Daranagama et al. 2015a, Senanayake et al.
2015). Therefore, earlier mycologists focused mainly on external morphological characters of these
microfungi. Several of the micro-Xylariaceae have been observed only once (e.g. Appendixia
closterium (Berk. & M. A. Curtis) B.S. Lu & K.D. Hyde (Figure 1), Areolospora S.C. Jong & E.E.
Davis, Calceomyces lacunosus Udagawa & S. Ueda and Emarcea Duong et al.), and then
superficially (e.g. Stereosphaeria americana (M.E. Barr & Samuels) K.D. Hyde et al.). This can be
seen in the number of micro-Xylariaceae recorded over the years, and fewer than half of those have
any sequence data available (Table 1). It is only recently that they have been intensively studied
with emphasis on ultrastructural characters and molecular phylogeny.
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Fig. 2 – Engleromyces goetzei (Holotype a. Herbarium details, b. Stromata with faded white flesh
c. Stromatal surface with ostioles, d and e. Roughened stromatal surface, f and g. Cross section of
stromata showing perithecia encased in stromatal tissue h and j. Ascospores, i. Ascospores with
appendage present at one end (arrow head). Scale bars: b–e = 2 mm, f, g = 1mm, h–j = 20 µm.
Limitations in the studies of microfungi
The major limitation in understanding the micro-Xylariaceae is the lack of fresh collections,
especially from tropical locations from where majority of the known species have been described.
Therefore, progress in our understanding of the micro-Xylariaceae should come with more
intensive collecting, particularly of habitats and substrates other than wood, and greater emphasis
on obtaining sequence data. The lack of stromata means greater emphasis must be placed on
ascomatal anatomy, peridium structure, asci and ascospore morphology and ultrastructure. The lack
of dichotomous keys, with reliance on single characters, is another problem in their taxonomic
discourse. Thus, the importance of molecular approaches has been highlighted in order to determine
the phylogenetic relationships (Stadler et al. 2013, Daranagama et al. 2015a, Maharachchikumbura
et al. 2015).
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The second problem in the study of micro-Xylariaceae is that many species were described
long ago and have never been recollected (Engleromyces, Sarcoxylon, and Squamotubera). Stadler
et al. (2013) highlighted that many type species of xylariaceous genera are only known from their
original collections or else from the drawings made many years ago, for example, the holotype
material of Engleromyces goetzei Henn., collected from Zambia in 1899 and deposited in B
herbarium is now hard and degraded and not suitable for morphological observation (Figure 2).
Also, Podosordaria mexicana Ellis & Holw., collected in 1896 on cow dung, is highly deteriorated.
Similarly, the genus Squamotubera is only known from its short Latin prologue by Hennings
(1903) with no illustrations. The types of the genera Appendixia, Cannonia, Fasciatispora,
Occultitheca and Sabalicola have been encountered in earlier decades, but attempts to recollect
them have so far failed as they were often isolated from specific hosts or from remote localities. For
example, the monotypic genera Appendixia and Sabalicola were encountered from USA around
1893 and 1882, respectively. However, so far they have not been reported again.
The third problem with micro-Xylariaceae genera is that their spores are often difficult to
germinate and thus many were not isolated into axenic culture. Unlike macrofungi, multi spore
isolation or sterile tissue culture is not possible with microfungi, which leaves single spore isolation
as the only option. For example, Lu and Hyde (2000b) and Daranagama et al. (2015a) addressed the
difficulty of obtaining cultures from Anthostomella species. Many other Xylariaceae, such as
Kretzschmaria and Camillea spp., are difficult to culture from ascospores. Anthostomella can be
considered as the most frequently collected and well-studied micro-Xylariaceae genus (Eriksson
1966, Francis 1975, Francis et al. 1980, Hyde and Goh 1999, Lee and Crous 2000, Lu and Hyde
2000a, b, c, Daranagama et al. 2015a). However, most of these studies were only based on
morphology (Eriksson 1966, Francis 1975, Francis et al. 1980, Hyde and Goh 1999, Lu and Hyde
2000a, b, c,). Lu and Hyde (2000b) examined more than 2600 anthostomella–like specimens from
35 herbaria in their monograph. They accepted 86 species, while 95 species were synonymized, 105
taxa were relocated to other genera and 65 species were regarded as doubtful. The genus clearly
shows considerable morphological diversity and is thought to be a heterogenous group.
Daranagama et al. (2015a) used a multi gene approach to show that the genus is polyphyletic. This
highlights the need to study other micro-Xylariaceae at the molecular level. These fungi should be
recollected and cultured to generate sequence data. Only then can their familial affinities and
species numbers can be accurately established.
The fourth problem, closely tied to the previously described one, is the lack of reliable
sequence data of representative micro-xylariaceous fungi. Very few morphologically validated
strains are deposited in public databases such as, GenBank. Most of the sequences belonging to
Xylariomycetidae species deposited in public databases are not derived from type specimens or
cultures. Most of the sources of these sequences are always missing, and the specimens or cultures
never deposited in public collections. It is pertinent to point out that many sequences of Xylariaceae
are misidentifications, a common feature of sequences in GenBank (Bridge et al. 2005). Stadler et
al. (2013) highlighted the mislabeled strain ATCC 42768 which has continuously been referred to
as Xylaria hypoxylon in many studies, but it actually corresponds to X. longiana Rehm. It was only
very recently that the generic type of Xylariaceae (Xylaria hypoxylon (L.) Grev.) was formally
epitypified and an ex-epitype strain deposited with authentic sequences (Stadler et al. 2014b).
However, not only this species, but many other generic types in Xylariaceae, are in need of proper
epitypification with living cultures and authentic sequence data.
When we blast the GenBank database for Xylariaceae there are more than 5000 hits of
which more than 2000 correspond to Xylaria. The actual problem occurs when these data are used
in molecular studies. Only about 15–20% of data can be considered as authentic, thus their use in
other studies is highly questionable, devaluing the accuracy of the analysis. Many sequences from
different genes representing the stromatic Xylariaceae genera, such as Annulohypoxylon, Daldinia,
Hypoxylon and Xylaria are now available in GenBank because of the extensive studies carried out
recently on these genera (Hsieh et al. 2005, 2010, Visser et al. 2009, Kuhnert et al. 2014, Stadler et
al. 2014a). However, the opposite applies to the micro-Xylariaceae. For example, Barrmaelia
591
comprises seven species, but sequences for only two species are available in GenBank. Data for
over half of the genera listed in Table 1 have no sequence data e.g. Appendixia, Cannonia,
Occultitheca, Sabalicola, Spirodecospora, Nipicola and Pandanicola. Stadler (2011) reported that
about 80% of the cultures belonging to Annulohypoxylon, Daldinia and Hypoxylon, have
morphological, chemotaxonomic and molecular data available for their species. In the case of
micro-Xylariaceae the opposite is the case because of the practical difficulties in DNA extraction
from fruiting bodies. In the case of stromatic genera, their massive stromata can also be used in
DNA extraction and thus direct sequencing.
A fifth problem is that a significant number of xylariaceous fungi occur as asexual morphs
(for example: Arthroxylaria, Dicyma, Discoxylaria, Lindquistia, Muscodor, Padixonia, Virgaria
and Xylocoremium) and some have not been connected to their sexual morphs, e.g. Muscodor.
These taxa have been isolated from soil or other substrata and attempts to obtain the sexual morphs
have been unsuccessful. The asexual morphs of other sexual genera may yet still be discovered.
A further issue is that many xylariaceous taxa have been isolated as endophytes with some
remaining sterile, while others have been identified as the asexual morphs: e.g. Surculiseries and
Muscodor (Okane et al. 2001). Cultures of Muscodor are sterile and its position in Xylariaceae is
not yet confirmed, therefore Maharachchikumbura et al. (2016) placed Muscodor in the Xylariales
incertae sedis. Surculiseries rugispora Okane, Nakagiri & Tad. Ito, is an endophytic asexual taxon
isolated from the leaves of the mangrove tree Bruguiera gymnorrhiza (L.) Lam.
The stromatic Xylariaceae genera are of great interest as sources for novel compounds, thus
they have been extensively investigated for their secondary metabolites. The well-developed,
massive, conspicuous stromata are a rich source of secondary metabolites and lend themselves to
study (Stadler 2011). However, the same is not the case for micro-Xylariaceae genera with the
exception of Halorosellinia oceanica (S. Schatz) Whalley et al. from which a wide range of new
chemical structures have been reported (Schilingham et al. 1998, Chinworrungsee et al. 2005, Xia
et al. 2007, Jones 2008, 2013). Since they lack stromata, where most novel chemicals have been
derived, the micro-Xylariaceae has generally been neglected in the search for new chemical
metabolites.
Current status of the micro-Xylariaceae
In many phylogenetic analyses of Xylariaceae only the macro-Xylariaceae genera have been
investigated (Smith et al. 2003, Pelaéz et al. 2008, Tang et al. 2009), and many have been
monographed and revised (Rodrigues and Samuels 1989, Ju and Rogers 1996, Hsieh et al. 2005,
Stadler et al. 2010b, 2014a, Petrini 2013, Jacklitsch et al. 2014) using morphology, molecular and
even chemical data. Many microfungal genera in the Xylariales (ex Xylariaceae) have been
extensively studied including Anthostomella, Amphisphaeria, Arecophila, Kiliophora,
Pestalotiopsis and Seimatosporium (Hyde 1996, Lu and Hyde 2000b, Wang et al. 2004, Barber et
al. 2011, Maharachchikumbura et al. 2014, Daranagama et al. 2015a, Norphanphoun et al. 2015).
The examples given above should certainly be sufficient to indicate that the microfungal genera
have so far been neglected.
Phylogenetic relationships between families in Xylariomycetidae
The phylogenetic affinities of families in the Xylariomycetidae have not been clearly
established (Rogers 2000, Senanayake et al. 2015). Likewise, the assignment of genera to families
sometimes cannot be done with certainty only using morphology, in which similar taxa are grouped
together. However, in many cases the phylogenetic relationship of genera is not clear either. For
example, xylariaceous genera such as Biscogniauxia and Camellia have bipartite stromata and this
is also found in some species of Diatrypaceae; e.g. Diatrype stigma (Hoffm.) Fr. The
interrelationship between Xylariaceae and Diatrypaceae has long been the topic of study (Munk
1957, Acero et al. 2004, Stadler et al. 2013). For example, the genera Creosphaeria and
Lopadostoma with libertella-like asexual morphs were included in Xylariaceae, but others opined
592
affinities with Diatrypaceae (Acero et al. 2004, Daranagama et al. 2015a). More recently these two
genera were referred to the family Lopadostomataceae based on phylogeny and morphology by
Senanayake et al. (2015) and Maharachchikumbura et al. (2016) Jumillera and Whalleya were
introduced to encompass taxa based on morphological differences of their asexual morphs (Rogers
et al. 1997). However, both genera produce scolecosporous conidia, which is a characteristic
feature of Lopadostomaceae. Some Jumillera species produce libertella-like asexual morphs and
species such as J. cinerea (Ellis & Everh.) J.D. Rogers et al. produce geniculosporium-like
synanamorphs in culture (Rogers et al. 1997). Whalleya microplaca (Berk. & M.A. Curtis) J.D.
Rogers et al. produced a similar asexual morph to Lopadostoma pouzarii Granmo & L.E. Petrini
(Granmo and Petrini 1996). Therefore, Jumillera and Whalleya have affinities with both
Xylariaceae and Lopadostomaceae. Therefore their phylogenetic placement remains to be
established as fresh material and molecular data becomes available.
Pyriformiascoma is a new xylariaceaous genus with unknown affinities, which appeared to
be in a basal clade to other xylariaceous genera (Darangama et al. 2015a). However, this genus may
be better referred to other families in the Xylariales or to others when there are enough strains
collected in the future. For example, Krug (1977) introduced the family Cainiaceae to
accommodate Cainia a genus often placed in Amphisphaeriaceae. Cainia obviously has affinities
with both the Amphisphaeriaceae and Xylariaceae as reported by Rogers (1994), and Kang et al.
(1998, 1999a, 1999b). Therefore it is evident that there are several evolutionary interfaces that have
been observed in this group and many of these microfungal genera represent unrecognized
evolutionary lineages. On the other hand formalization of these evolutionary patterns based on the
few data available may not be wise. Therefore additional studies are clearly needed to clarify this
issue.
Conclusion
Although research studies have mostly focused on the larger Xylariaceae it is unlikely they
are the most diverse forms in Xylariomycetidae. This essay indicates that future studies should
focus on the micro-fungi in Xylariales. Many of these micro-fungi have not been studied due to
lack of material, especially sequence data. Many new lineages in the Xylariomycetidae remain to
be introduced and wider collecting, modern descriptions and illustrations are required, along with
sequence data. In particular, early described genera need recollecting and epitypifying so as to
obtain a better knowledge of lineages within Xylariomycetidae. A culture-based study of
endophytes associated with rubber trees in Peru yielded a new genus and species: Xylona heveae
Gazis & P. Chave., resulting in the introduction of a new class of Pezizomycotina: Xylonomycetes
(Gazis et al. 2012). This shows that many more xylariaceous and other endophytic taxa remain to
be collected and characterized.
Acknowledgments
The authors appreciate the financial support and postgraduate scholarship provided by State
Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing
and the Mushroom Research Foundation, Chiang Mai, Thailand. The authors gratefully thank Dr.
Eric McKenzie from Landcare Research University of Auckland, New Zealand and Prof. D. J.
Bhat, India for their valuable comments and advice on this manuscript.
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