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Enigmatic Sebacinales Franz Oberwinkler, Kai Riess, Robert Bauer, Marc-André Selosse, Michael Weiß, Sigisfredo Garnica & A

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Enigmatic Sebacinales Franz Oberwinkler, Kai Riess, Robert Bauer, Marc-André Selosse, Michael Weiß, Sigisfredo Garnica & A Enigmatic Sebacinales Franz Oberwinkler, Kai Riess, Robert Bauer, Marc-André Selosse, Michael Weiß, Sigisfredo Garnica & Alga Zuccaro Mycological Progress ISSN 1617-416X Mycol Progress DOI 10.1007/s11557-012-0880-4 1 23 Your article is protected by copyright and all rights are held exclusively by German Mycological Society and Springer-Verlag Berlin Heidelberg. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Mycol Progress DOI 10.1007/s11557-012-0880-4 REVIEW ARTICLE Enigmatic Sebacinales Franz Oberwinkler & Kai Riess & Robert Bauer & Marc-André Selosse & Michael Weiß & Sigisfredo Garnica & Alga Zuccaro Received: 12 November 2012 /Revised: 6 December 2012 /Accepted: 11 December 2012 # German Mycological Society and Springer-Verlag Berlin Heidelberg 2013 Abstract A historical retrospect and a taxonomic update will suggesting future possibilities for agricultural applications. The deal with Sebacina s.l. and s.str., Craterocolla, Efibulobasidium, genomes of this species and of Sebacina vermifera have been Serendipita, Tremellodendron, Tremelloscypha, sequenced recently, thus opening new fields in studying and Tremellostereum, and Piriformospora, the Sebacinaceae, and understanding functional and evolutionary aspects. the Sebacinales. Phylogenetic hypotheses for the order and subordinal taxa are discussed, including environmental se- quence taxa. The cryptic biodiversity in Sebacinales is extensive History and taxonomy but mostly unresolved with respect to the species involved. Trophic stages are manifold in Sebacinales but restricted to plant In 1871, the french mycologists Louis René and Charles dependencies. Most of the species grow endophytically or form Tulasne erected the genus Sebacina with the type species S. various mycorrhizae, but Craterocolla and Efibulobasidium incrustans (Figs. 1a and 2c). They recognized that Corticium species appear to be saprobic. The sebacinalean mycorrhizal incrustans, described by Persoon in 1796,isphragmobasidi- diversity is unparalleled: ectomycorrhizae, ericoid and orchid ate in contrast to the holobasidiate Corticium species. The mycorrhizae are frequent, both in autotrophs and heterotrophs, species prefers to grow on soil, encrusting litter and plant as well as mycothalli with Jungermanniales. Mycorrhizal com- material on the ground. Also, fruiting on soil is typical for munity structures are difficult to evaluate in Sebacinales because another common species in forests, S. epigaea (Fig. 1b), of the high percentage of environmental sequence taxa lacking transferred by Bourdot and Galzin (1927)toSebacina. further characteristics. Nutritional requirements and exchanges Already in 1848, Berkley and Broome found the longitudi- have been studied extensively in Piriformospora indica, nally septate, tremelloid basidia, and consequently described the thus far unknown species as Tremella epigaea. A species with a dimitic hyphal system was recognized by Oberwinkler : : : (1963) and described as S. dimitica (Fig. 1c). F. Oberwinkler K. Riess R. Bauer S. Garnica (*) When studying inconspicuous corticioid Basidiomycetes, Institut für Evolution und Ökologie, Evolutionäre Ökologie Oberwinkler (1964)foundaSebacina with scattered hyphae, der Pflanzen, Universität Tübingen, Auf der Morgenstelle 1, 72076 Tübingen, Germany which forms neither a basidiocarp nor a hymenial layer, and is e-mail: [email protected] therefore not visible to the naked eye. Because of its nematode-like basidiospores, the species was named S. vermi- M.-A. Selosse fera (Figs. 1j and 2l). Warcup and Talbot (1967)succeededto Centre d’Écologie Fonctionnelle et Évolutive (CNRS, UMR 5175), 1919 Route de Mende, isolate and cultivate a basidiomycetous fungus from orchid 34 293 Montpellier cedex 5, France roots in South Australia. They found tremelloid basidia and vermiform basidiospores in culture, and consequently identi- M. Weiß fied the isolate as S. vermifera.Roberts(1993) typified his Fachbereich Biologie, Universität Tübingen, Auf der Morgenstelle 5, newly introduced genus Serendipita with S. vermifera ss. 72076 Tübingen, Germany Oberwinkler. Another inconspicuous species with efibulate hyphae, Sebacina allantoidea, has been described by A. Zuccaro Kirschner and Oberwinkler (2002). Additional taxa cannot Max-Planck-Institut für, terrestrische Mikrobiologie, Karl-von-Frisch-Straße 10, be discussed here, because micromorphology is not docu- 35043 Marburg, Germany mented sufficiently and molecular data are lacking. Author's personal copy Mycol Progress Fig. 1 Basidiocarps of representative species of sebacinalean genera: basal layer, bar 2 cm. i Tremellodendron candidum,bar2cm.j a Sebacina incrustans, bar 1 cm. b S. epigaea, bar 5 mm. c S. dimitica, Sebacina (Serendipita) vermifera,bar20μm, basidial clusters are bar 5 mm. d Efibulobasidium albescens, bar 5 mm. e Craterocolla scattered on loose generative hyphae, a basidiocarp is lacking. SEM cerasi, bar 1 cm. f Tremellostereum dichroum, bar 2 cm. g Tremello- photo P. Blanz. All other photos F. Oberwinkler scypha gelatinosa, bar 4 cm. h Tremellodendron sp. with sebacinoid The family Sebacinaceae has been proposed by Piriformospora indica (Verma et al. 1998), isolated Oberwinkler and Wells (in Wells and Oberwinkler 1982) from soil of the Indian Thar Desert as an anamorphic to cover species of the genera Sebacina, Tremelloscypha fungus, has dolipores with continuous parenthesomes of (Figs. 1g and 2d–g), and Tremellodendron (Figs. 1h, i the sebacinalean type. The phylogenetic relationship and 2j, k). Efibulobasidium (Figs. 1d and 2h, i)was with Sebacinales has been documented by various mo- assigned tentatively to the new family. Ryvarden (1986) lecular hypotheses, e.g. Weiß et al. (2004, 2011). A erected Tremellostereum with a single species, previously second species, P. williamsii, with multinucleate cells, called Stereum dichroum Lloyd (Fig. 1f), which shares has been recently described by Zuccaro and Weiß in sebacinoid characters. Based on molecular phylogenetic Basiewicz et al. (2012).Basedonmolecularphyloge- analyses, Weiß et al. (2004)confirmedEfibulobasidium as a netic analyses, enzymatic profiling, genome size estima- member of the family, including in it also Craterocolla tions and karyotype analyses of five S. vermifera (Figs. 1e and 2a,b), and raising the group to ordinal rank. strains,P. indica,andP. williamsii, the authors could Molecular phylogenetic evidence for the ectomycorrhizal sta- identify specific differences in the physiological and tus of Tremellodendron was found by Walker and Parrent molecular parameters inferred from these morphological- (2004). ly very similar strains. Author's personal copy Mycol Progress Fig. 2 Teleomorphic and anamorphic stages of Sebacinales. a Cra- Oberwinkler 1982). h Efibulobasidium sp., part of the hymenium with terocolla cerasi, section of hymenium and subhymenium with basidio- basidia of different developmental stages, bar 20 μm. i Conidia of spores on the hymenial surface, bar 20 μm. b conidial stage of C. Chaetospermum gossypinum derived from cultivated Efibulobasidium cerasi with conidiogenous cells and conidia, bar 20 μm. c Sebacina albescens, bar 20 μm (from Kirschner and Oberwinkler 2009). j, k incrustans, section of hymenium and subhymenium with basidiospores Tremellodendron candidum (from Wells and Oberwinkler 1982); j on the hymenial surface, bar 20 μm (from Wells and Oberwinkler basidiocarp, bar 2 cm, k section of hymenium and subhymenium with 1982). d–g Tremelloscypha gelatinosa; d section of basidiocarp, bar basidiospores, bar 20 μm. l Sebacina (Serendipita) vermifera, hyphae, 2 cm, e hyphae of pileus surface, f hyphae of stipe, g part of the basidia in different developmental stages, and basidiospores, bar hymenium with basidia of different developmental stages, dikaryoph- 20 μm (from type, Oberwinkler 1964) yses and basidiospores, bar 20 μm for e, f, g, (g from Wells and Ultrastructure of septal pores (Fig. 3) selected species of the Rhizoctonia s.l. complex, Andersen (1996), and Müller et al. (1998) were able to document Dolipores with continuous parenthesomes are a common dolipores with continuous parenthesomes. Epulorhiza ultrastructural marker for Sebacinales, first documented for (Sebacina) strains, isolated from Australian orchids and studied Sebacina and Tremellodendron by Khan and Kimbrough by Gleason and McGee (2001), showed the same ultrastructural (1980) and confirmed for Sebacina by Oberwinkler characteristics. Dolipores of sebacinoid, tulasnelloid, ceratoba- (1985). A basidiomycete with sebacinoid dolipores occurred sidioid and homobasidiomycetous mycobionts of Ecuadorian in living cells of mycorrhizal hair roots of Calluna vulgaris ORMs were illustrated by Kottke and Suárez Chacón (2009, (Bonfante-Fasolo 1980). Ultrastructural studies by Filipello Fig. 3d). Sebacina in ectomycorrhizae (ECM) of Carpinus Marchisio et al. (1985) of endophytes of native Italian betulus, Corylus avellana were illustrated by Selosse et al. Dactylorhiza maculata, D. sambucina, and Platanthera (2002a), in ECM of Tilia sp. by Urban et al. (2003), and Salix bifolia revealed dolipores with continuous parenthesomes,
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