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Pleosporomycetidae, Dothideomycetes, Ascomycota ) Using Four Nuclear Genes

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Pleosporomycetidae, Dothideomycetes, Ascomycota ) Using Four Nuclear Genes On the evolution of the Hysteriaceae and Mytilinidiaceae (Pleosporomycetidae, Dothideomycetes, Ascomycota ) using four nuclear genes Eric W.A. BOEHM 1, Conrad L. SCHOCH 2, Joseph W. SPATAFORA 2 1 Department of Biological Sciences, Kean University, 1000 Morris Ave., Union, New Jersey 2 Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon Hysterium Lophium Tree of Life web project: Hysteriaceae & Mytilinidiaceae Subphylum Pezizomycotina Ascomycota Class Dothideomycetes pseudoparaphyses absent pseudoparaphyses present Classification history Zogg (1962) Luttrell (1973) Barr (1987) Kirk et al. (2001) Eriksson (2006) Lumbsch & Huhndorf (2007) Loculoascomycetes Dothideomycetes Dothideomycetes Dothideomycetes Dothideomycetes Dothideales Hysteriales Pleosporales Hysteriales Hysteriales Dothideomycetes orders incertae sedis Hysteriaceae Hysteriaceae Hysteriaceae Hysteriaceae Hysteriaceae Hysteriales Hysterioideae Hysteriaceae Melanommatales Dothideomycetes Pleosporomycetidae fam. incertae sedis Pleosporales Lophiaceae Lophioideae Mytilinidiaceae Mytilinidiaceae Mytilinidiaceae Mytilinidiaceae The Hysteriaceae Chevall.: The ascoma • Fungi classified in the Hysteriaceae are defined by a specialized ascocarp, termed the hysterothecium. • Hysterothecia are dense, persistent carbonaceous structures, distinctly navicular in outline, and bear a pronounced longitudinal slit running the length of the long axis of the fruitbody. Bar = 1 mm The Hysteriaceae Chevall.: Early images... • Early authors provided remarkably accurate figures of hysteriaceous fungi (e.g., Bolton 1789). • Greville (1825) was the first to provide illustrations of asci and ascospores. left: Bolton J, 1789. An history of fungusses growing about Halifax, Vol III. right: Greville RK, 1825. Scottish Cryptogamic Flora, III. Edinburgh, Scotland. The Hysteriaceae Chevall.: Peridium & hamathecium • In vertical section, hysterothecia are globose to obovoid, typically with a thick three-layered peridium. • Hamathecium composed of persistent cellular pseudoparaphyses, often borne in a gel matrix, tips darkened or branched at maturity to form an epithecium. Zogg, 1962 The Hysteriaceae Chevall.: Spore septation defines genera pedicillate amerospores: Farlowiella Sacc. pigmented phragmospores: Hysterium Pers. : Fr. hyaline phragmospores: Gloniella Sacc. pigmented dictyospores: Hysterographium Corda hyaline dictyospores: Gloniopsis De Not. hyaline didymospores: Glonium Muhl. : Fr. pigmented didymospores: Actidiographium Vasilyeva White bar = 1 mm; Black bar = 10 um The Mytilinidiaceae Kirschst.: The ascoma • Obovoid to strongly laterally compressed, erect oyster- or bivalve shell-shaped (conchate) or hatchet-shaped (dolabrate) pseudothecia, standing on edge, with a prominent longitudinal keel or cristate apex. • Peridium: Unlike Hysteriaceae, mytilinidiaceous fungi possess a thin-walled, fragile prosenchymatous peridium. • Hamathecium: Unlike Hysteriaceae, narrow non-cellular, trabeculate pseudoparaphyses, sparse to lacking at maturity. Ostreichnion Mytilinidion Lophium The Mytilinidiaceae Kirschst.: Spore septation defines genera pigmented phragmospores: Mytilinidion Duby subgenus Eu-Mytilinidion Lohman pigmented dictyospores: Ostreichnion Duby, Ostreola Darker pigmented didymospores: Actidium Fr. pigmented scolecospores: Mytilinidion Duby subgenus Lophiopsis Lohman hyaline scolecospores: Lophium Fr. Ostreola Mytilinidion Mytilinidion subgenus subgenus Ostreichnion Lophiopsis Eu-Mytilinidion Actidium Lophium credits: Barr, 1990; Ellis & Ellis 1985; Lohman, 1934; Zogg, 1962 Morphological character states versus molecules Barr (1987) established a number of morphological character states used to differentiate the Hysteriaceae from the Mytilinidiaceae. Question: Will morphological character states prove to be phylogenetically informative in the context of sequence-based phylogenies ? Character states Hysteriaceae Mytilinidiaceae Pseudothecium elongate navicular globoid, conchate, dolabrate Hysterium Dehiscence invaginated sulcus connivent with cristate apex (keel) Peridium thick-walled, thin-walled, multilayered prosenchymatous Centrum elongate, cylindrical elongate, laterally compressed Hamathecium persistent cellular evanescent narrow pseudoparaphyses trabeculate type Ascospore asymmetric symmetric symmetry Lophium Taxon sampling strategy: single ascospore cultures Hysteriaceae : 35 isolates, representing five of the eight currently accepted genera. Mytilinidiaceae : 11 isolates, representing three of the currently accepted seven genera. Hysteriaceae Chevall. Mytilinidiaceae Kirschst. * Hysterium Pers. : Fr. (6) * Mytilinidion Duby (7) Gloniella Sacc. * Ostreichnion Duby (2) * Hysterographium Corda (4) Ostreola Darker Hysterocarina Zogg Actidium Fr. * Gloniopsis De Not. (2) Quasiconcha Barr & Blackw. * Glonium Muhl. : Fr. (5) * Lophium Fr. (1) Actidiographium Vasil. Zoggium Vassil. * Farlowiella Sacc. (1) Four gene phylogeny: nuSSU, nuLSU, RPB2 & TEF1α Contiguous data set consisted of four genes (3400+ nucleotides per taxon ). RPB2 RPB2-5F 123 4 5 6 7891011 fRPB2-7cR Vilgalys 526F 983FEFcf EFdf 1577F Elongation Factor 1 α EFjrEFir 1567R EFgr 1953R2218R Vilgalys Hysteriaceae & Mytilinidiaceae Hysteriaceae Multigene phylogenies provide strong support for: • Monophyly for the Hysteriaceae. • Monophyly for the Mytilinidiaceae. Pezizomycotina • Both in the Pleosporomycetidae. Mytilinidiaceae • Both families not closely related within the subclass . The Hysteriales Lindau 1897 We propose that the Hysteriaceae be retained under the original ordinal designation, Hysteriales Lindau 1897 : • High support (90/100) as monophyletic entity. Pezizomycotina • Strong support for its separation from the Pleosporales. Mytilinidiaceae • Elongated hysteriaceous locule, capable of relatively indeterminate linear growth , as distinct from the strict Pleospora-type centrum, defined as it is by constrained concentric growth . • We believe these two centrum types are distinct enough to warrant ordinal status. • Supported by large taxon sampling strategy & a large contiguous data set of four genes (3400+ nucleotides per taxon). A new ascomycete order: Mytilinidiales Boehm, Schoch & Spatafora 2008, ord. nov. MycoBank No.: MB 511989 Typus: Mytilinidion Duby, Mémoires de la Société de Physique et Histoire Naturelle de Pezizomycotina Genève 16: 15-70 (1862). • Very high support (100/100) as a monophyletic entity. • High indices of support indicate a clear separation between the Mytilinidiales and the Hysteriales & Pleosporales . • Supported by large taxon sampling strategy & a large contiguous data set of four genes (3400+ nucleotides per taxon). The evolution of the didymospore The genus Glonium is polyphyletic! Glonium Muhl. : Fr. & Psiloglonium Hohn. Psiloglonium Höhn., Annales Mycologici 16: 145 (1918). Typus: Psiloglonium lineare (Fr.) Petr. Hysteriales • The genus is reinstated within the Hysteriaceae , with P. lineare , as type, to accommodate non-subiculate Pleosporomycetidae species, with apically obtuse didymospores, as distinct from the genus Glonium . Pleosporales Gloniaceae (Corda) Boehm, Schoch & Spatafora fam. nov. MycoBank No.: MB 511999; Basionym: Gloniaceae Corda, Mytilinidiales Icones Fungorum, Hucusque Cognitorum. 5: 34 (1842): Typus: Glonium stellatum Muhl. : Fr. • subiculate, dichotomously-branched, laterally anastomosed hysterothecia, bearing acuminate didymospores. 83 / 100 Zogg, 1962 The evolution of the phragmospore The genus Hysterium Pers. : Fr. Hysteriales H. pulicare Pleosporomycetidae H. angustatum Pleosporales Zogg, 1962 H. insidens Mytilinidiales Rhytidhysteron H. sinense Patellariaceae! The evolution of the dictyospore Hysterographium Corda & Gloniopsis De Not. Hysteriales Gs. smilacis Pleosporomycetidae Hg. mori Pleosporales Zogg, 1962 Gs. praelonga Hg. subrugosum Mytilinidiales Hg. fraxini (Typus for Hysterographium!) Farlowiella! The hysterothecium is not synapomorphic! Conclusions – • Multigene phylogenies indicate that the Hysteriaceae and the Mytilinidiaceae represent two unrelated monophyletic families, situated within the Pleosporomycetidae . • We retain the Hysteriales for the Hysteriaceae and establish the Mytilinidiales ord. nov. for the Mytilinidiaceae . • We reserve the genus Glonium for forms closely allied to the type G. stellatum , as circumscribed by von Höhnel (1918) and Petrak (1923), and place them within the Gloniaceae fam. nov. , Pleosporomycetidae incertae sedis . • We reinstate the genus Psiloglonium Höhn. in the Hysteriaceae , with the type species P. lineare (Fr.) Petrak (Petrak 1923), to accommodate non-subiculate species previously classified in the genus Glonium , a position supported by Barr (1987). Conclusions – • Remarkably, the hysterothecium, the classic hallmark of the family Hysteriaceae, long considered a synapomorphic character state, has in fact arisen multiple times among unrelated groups within the Pleosporomycetidae. • The ability to perennate may be the driving force behind the evolution of the hysterothecium among unrelated groups, since most of these fungi occur on decorticated woody substrates prone to prolonged periods of desiccation. http://www.eboehm.com/ The Mytilinidiaceae Kirschst.: The question of Glyphium • The genus Glyphium Nitschke ex Lehmann, with erect dolabrate ascomata, was originally included by Zogg (1962), Barr (1987, 1990) and others in the Mytilinidiaceae . • However, recent molecular evidence, based on the nuLSU, nuSSU, mtLSU & mtSSU, has removed the genus Glyphium to the Chaetothyriales
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