A molecular phylogenetic reappraisal of the Hysteriaceae, Mytilinidiaceae and Gloniaceae (Pleosporomycetidae, Dothideomycetes) with keys to world species

Abstract

A reappraisal of the phylogenetic integrity of bitunicate ascomycete fungi belonging to or previously affiliated with the Hysteriaceae, Mytilinidiaceae, Gloniaceae and Patellariaceae is presented, based on an analysis of 121 isolates and four nuclear genes, the ribosomal large and small subunits, transcription elongation factor 1 and the second largest RNA polymerase II subunit. A geographically diverse and high density taxon sampling strategy was employed, including multiple isolates/species from the following genera: Anteaglonium (6/4), Encephalographa (1/1), Farlowiella (3/1), Gloniopsis (8/4), Glonium (4/2), Hysterium (12/5), Hysterobrevium (14/3), Hysterographium (2/1), Hysteropatella (2/2), Lophium (4/2), Mytilinidion (13/10), Oedohysterium (5/3), Ostreichnion (2/2), Patellaria (1/1), Psiloglonium (11/3), Quasiconcha (1/1), Rhytidhysteron (8/3), and 24 outgroup taxa. Sequence data indicate that although the Hysteriales are closely related to the Pleosporales, sufficient branch support exists for their separation into separate orders within the Pleosporomycetidae. The Mytilinidiales are more distantly related within the subclass and show a close association with the Gloniaceae. Although there are examples of concordance between morphological and molecular data, these are few. Molecular data instead support the premise of a large number of convergent evolutionary lineages, which do not correspond to previously held assumptions of synapomorphy relating to spore morphology. Thus, within the Hysteriaceae, the genera Gloniopsis, Glonium, Hysterium and Hysterographium are highly polyphyletic. This necessitated the transfer of two species of Hysterium to Oedohysteriumgen. nov. (Od. insidenscomb. nov. and Od. sinense comb. nov.), the description of a new species, Hysterium barrianumsp. nov., and the transfer of two species of Gloniopsis to Hysterobreviumgen. nov. (Hb. smilaciscomb. nov. and Hb. constrictumcomb. nov.). While Hysterographium, with the type Hg. fraxini, is removed from the Hysteriaceae, some of its species remain within the family, transferred here to Oedohysterium (Od. pulchrumcomb. nov.), Hysterobrevium (Hb. moricomb. nov.) and Gloniopsis (Gp. subrugosacomb. nov.); the latter genus, in addition to the type, Gp. praelonga, with two new species, Gp. arciformissp. nov. and Gp. kenyensis sp. nov. The genus Glonium is now divided into Anteaglonium (Pleosporales), Glonium (Gloniaceae), and Psiloglonium (Hysteriaceae). The hysterothecium has evolved convergently no less than five times within the Pleosporomycetidae (e.g., Anteaglonium, Farlowiella, Glonium, Hysterographium and the Hysteriaceae). Similarly, thin-walled mytilinidioid (e.g., Ostreichnion) and patellarioid (e.g., Rhytidhysteron) genera, previously in the Mytilinidiaceae and Patellariaceae, respectively, transferred here to the Hysteriaceae, have also evolved at least twice within the subclass. As such, character states traditionally considered to represent synapomorphies among these fungi, whether they relate to spore septation or the ascomata, in fact, represent symplesiomorphies, and most likely have arisen multiple times through convergent evolutionary processes in response to common selective pressures.

Keywords: Evolution; Hysteriales; Mytilinidiales; Patellariales; fungi; phylogeny; speciation; taxonomy.

Fig. 1.

Combined ribosomal (nuSSU & nuLSU) and protein coding gene (TEF1 & RPB2) DNA phylogeny for bitunicate ascomycetes belonging to or previously affiliated with the Hysteriaceae, Mytilinidiaceae, Gloniaceae and Patellariaceae. Also included are representatives from allied groups such as the Pleosporales, Jahnulales, Patellariales, and Botryosphaeriales, as well as representatives from the Dothideales, Myriangiales and Capnodiales in the Dothideomycetidae. The Arthoniomycetes, chosen as outgroup, are not presented here due to space limitations, but are available in the full tree on TreeBASE. The tree is the highest scoring tree obtained by maximum likelihood in RAxML. Nodal values, given as percentages, are as follows: Bayesian posterior probability / maximum likelihood bootstrap. Only values above 50 % are shown.

Fig. 2.

The genus Hysterium (Clade C). A–B. Hysterium pulicare [CBS 123377 (BPI 878723), U.S.A.]; C–F. Hysterium angustatum [ANM 120 (ILLS), U.S.A.; not incl.]; G–K. Hysterium vermiforme [GKM 1234 (BPI 879785), Kenya]; L–Q. Hysterium barrianum sp. nov. [ANM 1495 (ILLS 59908 = holotype), U.S.A.]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 20 μm.

Fig. 3.

The genus Oedohysterium (Clade D). A–D. Oedohysterium insidens [ANM 1443 (BPI 879799), U.S.A.]; E–H. Oedohysterium sinense [ANM 119 (ILLS), U.S.A.; not incl.]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 20 μm.

Fig. 4.

The genus Hysterographium. A–B. Hysterographium flexuosum (EB 0098, U.S.A.; not incl.); C–D. Hysterographium fraxini (EB 0100, U.S.A.; not incl.). Scale bar (habitat) = 1 mm; Scale bar (spores) = 20 μm.

Fig. 5.

The genus Hysterobrevium (Clade A). A–E. Hysterobrevium constrictum [SMH 5211.1 (F), New Zealand]; F–I. Hysterobrevium smilacis [GKM 426N (EA), Kenya]; L–N. Hysterobrevium mori [SMH 5273 (BPI 879787), U.S.A.]; O–R. Hysterobrevium mori [ANM 43 (ILLS), U.S.A.; not incl]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 10 μm.

Fig. 6.

The genus Gloniopsis (Clade D). A–B. Gloniopsis praelonga [CBS 123337 (BPI 878725), U.S.A.]; C–F. Gloniopsis subrugosa [GKM 1214 (BPI 879776), Kenya]; G. Gloniopsis subrugosa (CBS 123346, BPI 878735; South Africa). Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 20 μm.

Fig. 7.

The genus Gloniopsis (Clade D). A–H. Gloniopsis arciformis sp. nov. [GKM L166A (BPI 879774 = holotype), Kenya]; I–M. Gloniopsis kenyensis sp. nov. [GKM 1010 (BPI 879775 = holotype), Kenya]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 10 μm.

Fig. 8.

The genus Psiloglonium (Clade B). A–D. Psiloglonium simulans [ANM 1557 (BPI 879803), U.S.A.]; E–H. Psiloglonium clavisporum [GKM 344A (BPI 879801), Kenya]; I–M. Psiloglonium lineare [ANM 117 (ILLS), U.S.A.; not incl.]; N–Q. Psiloglonium araucanum [ANM 42 (ILLS), U.S.A.; not incl.]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 10 μm.

Fig. 9.

The genus Anteaglonium (Pleosporales). A–E. Anteaglonium abbreviatum [ANM 37 (ILLS), U.S.A.; not incl.]; F–I. Anteaglonium globosum [ANM 925.2 (ILLS), U.S.A.]; J–M. Anteaglonium parvulum [GKM 219N (EA), Kenya; not incl.]; N–R. Anteaglonium latirostrum [GKM L100N.2 (EA), Kenya]. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 5 μm.

Fig. 10.

The genus Rhytidhysteron (Clade E). A–D. Rhytidhysteron opuntiae [GKM 1190 (BPI 879805), Kenya]; E–J. Rhytidhysteron rufulum [GKM 361A (BPI 879806), Kenya]; K. Rhytidhysteron rufulum [EB 0382 (BPI 879808), Ghana]; L. Rhytidhysteron rufulum [EB 0381 (BPI 879807), Ghana]; M. Rhytidhysteron hysterinum [EB 0351 (BPI 879804) France, photo by Alain Gardiennet]. Scale bar (habitat) = 1 mm; Scale bar (spores and asci) = 10 μm.

Fig. 11.

The Mytilinidiaceae. A–B. Mytilinidion tortile [EB 0377 (BPI 879798), France]; C–D. Mytilinidion mytilinellum [EB 0386 (BPI 879796), France]; E–I. Mytilinidion australe [ANM 1524 (ILLS), U.S.A.; not incl.]; J–K. Lophium mytilinum [CBS 123344 (BPI 878736), U.S.A.]. Photo credits Alain Gardiennet, Figs. A–D. Scale bar (habitat) = 500 μm; Scale bar (spores and asci) = 10 μm.

Fig. 12.

The Gloniaceae. A–E. Glonium stellatum [ANM 41 (ILLS), U.S.A.; not incl.], arrows in 12B, subiculum. F–H. Glonium circumserpens [CBS 123343 (BPI 878739), Tasmania]. Scale bar (habitat) = 1 mm; Scale bar (spores and asci) = 10 μm.