An overview of the genus Glyphium and its phylogenetic placement in Patellarialesby E. W. A. Boehm, G. Marson, G. H. Mathiassen, A. Gardiennet, C. L. Schoch

Mycologia

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An overview of the genus Glyphium and its phylogenetic placement in Patellariales

Eric W.A. Boehm 42 Longacre Drive, Livingston, New Jersey 07039

Guy Marson

Division of Mycology, Museum of Natural History, 25 rue Mu¨nster, L-2160 Luxembourg

Geir H. Mathiassen

Department of Natural Sciences, Tromsø University

Museum, the Arctic University of Norway, NO–9037

Tromsø, Norway

Alain Gardiennet 14 rue Roulette, 21260 Veronnes, France

Conrad L. Schoch1

National Center for Biotechnology (NCBI), National

Library of Medicine, National Institutes of Health,

Bethesda, Maryland 20892

Abstract: Glyphium encompasses species with erect, carbonaceous ligulate to dolabrate ascomata that are strongly laterally compressed and dehisce along a longitudinal slit. The five currently recognized members of the genus are separated primarily by whether the ascospores disassociate into part-spores within the ascus. Glyphium has traditionally been placed in Mytilinidiaceae (Mytilinidiales, Pleosporomycetidae, Dothideomycetes). The present study, based on freshly collected material of G. elatum and

G. grisonense, was initiated to determine the phylogenetic placement of Glyphium. Phylogenies inferred from the analysis of sequences of six gene regions (nuLSU, nuSSU, mtSSU, TEF1, RPB1, RPB2) derived from six accessions indicate that Glyphium belongs to

Patellariales (Pleosporomycetidae, Dothideomycetes). Our phylogenies also support the phylogenetic relationship of Patellaria and Hysteropatella within this order. The nomenclatural history of Glyphium is summarized and a key to species is provided.

Key words: Bayesian, maximum likelihood, multigene phylogeny, Patellariaceae

INTRODUCTION

Species of Glyphium Nitschke ex F. Lehm. possess distinctive hatchet-shaped carbonaceous ascomata that dehisce along a longitudinal slit (FIGS. 1–5).

Although the ascomata are superficial, their bases are occasionally embedded in the substrate and might be associated with black interwoven hyphal strands that anchor the ascomata to a dense subicular matrix (FIG. 4). The hamathecium consists of trabeculate pseudoparaphyses borne in a gel-matrix that are thin to lacking at maturity (Zogg 1962, Barr 1990). The ascospores are filiform, multiseptate, occupy the greater length of the ascus in which they are often spirally arranged and become light brown at maturity (FIGS. 6, 7). In some species the ascospores disarticulate into part-spores before maturity while still within the ascus (FIG. 6), while in others the ascospores remain intact even after release (FIG. 7). Glyphium are lignicolous or corticolous and have been recovered from a wide range of hosts, including Alnus, Fagus,

Fraxinus, Malus, Populus, Pyrus, Rhamnus, Rhus,

Ulmus and Salix; one species is described from

Tillandsia (Zogg 1962).

Glyphium currently encompasses five species separated primarily by whether the ascospores disassociate into part-spores (FIG. 6, 7). Species with ascospores that remain entire include G. elatum (Grev.: Fr.) H.

Zogg (FIG. 1), the type of the genus and G. tillandsiae (E.K. Cash) H. Zogg (FIG. 5) (Cash 1943). Three species with ascospores that disassociate into partspores include G. corrugatum (Ellis) Goree (FIG. 3), a species found in the western United States and

Canada (Sutton 1970, Goree 1974), and two morphologically similar European species, G. grisonense Math. (FIG. 2) and G. schizosporum (Maire) H. Zogg (FIG. 4) (Zogg 1962, Sutton 1970). Anamorphs belonging to the form genus Peyronelia have been described for these latter three species (Lohman 1933a, Sutton 1970, Goree 1974) but are unknown for Glyphium possessing intact ascospores.

The first sequence data for Glyphium was provided by Lindemuth et al. (2001) and Lumbsch et al. (2005). They sequenced CBS 268.34, the only available culture of G. elatum derived from the rhizoidal strands and subiculum subtending the ascoma of this species. These workers employed sequences from the nuclear small (nuSSU) and large (nuLSU) ribosomal subunits, as well as the mitochondrial small (mtSSU) and large (mtLSU) ribosomal subunits. This demonstrated that Glyphium was not a member of the

Mytilinidiaceae but closely associated with Chaetothyriales, in the Eurotiomycetes. The unexpected placement of Glyphium in Chaetothyriales was reSubmitted 24 Jul 2014; accepted for publication 15 Jan 2015. 1 Corresponding author. E-mail: schoch2@ncbi.nlm.nih.gov

Mycologia, 107(3), 2015, pp. 607–618. DOI: 10.3852/14-191 # 2015 by The Mycological Society of America, Lawrence, KS 66044-8897 607

FIGS. 1–8. Ascomatal variation within the genus Glyphium. 1. Glyphium elatum (EB 0329/BPI 892669), Salix caprea,

Luxembourg. 2. Glyphium schizosporum (BPI 652567), Salix appendiculata, Switzerland. 3. Glyphium corrugatum (BPI 1107474), decorticated deciduous wood, Oregon, USA. 4. Glyphium grisonense (TROM 4395), Salix caprea ssp. sphacelata, Norway. (photo credit: Jostein Kjærandsen, UiT). 5. Glyphium tillandsiae (labeled as Lophium tillandsiae, BPI 1108420), Tillandsia fasciculata,

Florida, USA. 6. Intact ascus containing eight disarticulating ascospores of G. schizosporum (BPI 652567). 7. Intact ascus containing eight filiform ascospores of G. elatum (EB 0342/BPI 892670). 8. Filiform ascospore sending out multiple germ tubes on water agar, recovered from fresh material of G. elatum (EB 0342/BPI 892670). Bars: 1–5 5 0.5 mm, 6–8 5 50 mm. 608 MYCOLOGIA stated in a number of studies based on CBS 268.34.

However, subsequent work by Gueidan et al. (2008),

Tsuneda et al. (2011) and Re´blova´ et al. (2013) positioned this CBS culture within Knufia in Chaetothyriales, resulting in the relabeling of the sequence accessions at GenBank corresponding to CBS 268.34 as ‘‘Knufia sp. CBS 268.34’’.

Based on morphological work, scientists (e.g. Barr 1990) placed Glyphium in what is now Mytilinidiales in Dothideomycetes. The aim of the current study was to determine the phylogenetic placement of this genus based on sequences obtained from fresh, recently collected material of G. elatum and G. grisonense from Luxembourg, France and Norway.