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Agaricales) Reveals Polyphyly of Agaricoid Members

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Agaricales) Reveals Polyphyly of Agaricoid Members Mycologia, 108(5), 2016, pp. 860–868. DOI: 10.3852/15-370 # 2016 by The Mycological Society of America, Lawrence, KS 66044-8897 Multilocus phylogenetic reconstruction of the Clavariaceae (Agaricales) reveals polyphyly of agaricoid members Joshua M. Birkebak is a single club-shaped (clavarioid) or branched (coral- Slavomír Adamcˇík1,2 loid) basidiome represented by the genera Clavaria L.: Brian P. Looney Fr. (abbreviated Cl.), Clavulinopsis Overeem, Ramariop- P. Brandon Matheny sis (Donk) Corner and Mucronella Fr. Mucronella occu- Department of Ecology and Evolutionary Biology, University pies a well-supported position sister to the remaining of Tennessee, 332 Hesler, Biology Building, Knoxville, groups in the family (Birkebak et al. 2013). Clavulinop- Tennessee 37996-1610 sis and Ramariopsis form a well-supported monophylet- ic group. All agaricoid members of the family (with a differentiated pileus, stipe, and lamellate hymeno- Abstract: The genus Camarophyllopsis contains species phore) are currently classified in the single genus with lamellate (agaricoid) basidiomes in the family Cla- Camarophyllopsis Doty. The genus Hyphodontiella Å. variaceae (Agaricales), a group otherwise dominated Strid produces resupinate morphotypes and, accord- by club-like (clavarioid) or branched (coralloid) ing to Birkebak et al. (2013), is poorly supported as forms. Previous studies have suggested that species the sister group to a clade of Clavicorona-Clavaria- classified in Camarophyllopsis occur in two independent Camarophyllopsis. The genus Clavicorona produces basi- lineages. We reconstructed a multilocus phylogeny of diomes that are inflated upward and have a sterile the Clavaria-Camarophyllopsis-Clavicorona clade in the upper surface but lack lamellar modification of the Clavariaceae using RNA polymerase II second largest hymenophore. Although traditionally classified in the subunit (rpb2), nuclear ribosomal 28S, and nuclear Hygrophoraceae Lotsy, the agaricoid genus Camaro- ribosomal ITS1-5.8S-ITS2 regions data and detected phyllopsis has a phylogenetic affinity with the Clavaria- three independent groups of agaricoid fungi, includ- ceae (Matheny et al. 2006) and was later shown as ing the genera Camarophyllopsis, Hodophilus, and Lamel- nested within the genus Clavaria (Birkebak et al. loclavaria gen. nov, which distinctly differ in their 2013). In the latter work, Camarophyllopsis was recov- pileipellis structure. In all, nine major lineages within ered in two separate clades, but resolution and support the Clavaria-Camarophyllopsis-Clavicorona clade were were insufficient in this single gene study to reject the recovered: Clavaria sensu stricto, Camarophyllopsis monophyly of Camarophyllopsis. The two clades recov- sensu stricto, Hodophilus, the Clavaria pullei clade, the ered corresponded to Camarophyllopsis subgenus Clavaria fumosa clade, Lamelloclavaria gen. nov., the Camarophyllopsis and Camarophyllopsis subgenus Hodo- Clavaria atrofusca clade, Holocoryne (5 Clavaria sect. philus (Singer) Arnolds, which can be separated by Holocoryne), and Clavicorona. Clavaria is paraphyletic the structure of the pileipellis. and represented by five clades. Additional gene sam- The aims of this study are to investigate the systemat- pling is necessary to determine and confirm related- ics of the genus Camarophyllopsis further with the fol- ness of these lineages before splitting Clavaria into lowing objectives: (i) to produce a supermatrix to test additional genera. the monophyly of the genus Camarophyllopsis; (ii) to Key words: Agaricomycetes, Basidiomycota, evolu- assess the taxonomic relationships between agaricoid tion, systematics Clavariaceae members and other genera of the family; and (iii) to propose a modified taxonomic arrange- INTRODUCTION ment based on these new evolutionary relationships. The family Clavariaceae Chevall. sensu stricto, com- prising seven genera and at least ca. 125 species (Birke- MATERIALS AND METHODS bak et al. 2013), contains a diverse assemblage of Morphological examinations.—Macromorphological descrip- basidiome morphologies (FIG. 1) (Dentinger and tions were prepared from fresh collections. Color nomencla- McLaughlin 2006, Matheny et al. 2006, Larsson 2007, ture standards followed Kornerup and Wanscher (1967). All Birkebak et al. 2013). The most frequent morphotype micro-morphological characters were observed under an Olympus CX-41 light microscope with an oil-immersion lens at a magnification of 10006. All drawings of microscopic Submitted 23 Dec 2015; accepted for publication 20 Apr 2016. structures, with the exception of basidiospores, were made 1 Corresponding author. E-mail: [email protected] 2 with a camera lucida using an Olympus U-DA drawing attach- Current address: Department of Cryptogams, Institute of Botany, 6 Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 23 Bratislava, ment at a projection scale of 2000 . Basidiospores were Slovakia. scanned with an Artray Artcam 300MI camera and measured 860 BIRKEBAK ET AL.: PHYLOGENY OF AGARICOID CLAVARIACEAE 861 FIG. 1. Diversity of basidiome morphology in the Clavaria-Camarophyllopsis-Clavicorona clade of the Clavariaceae. A. Clavicorona taxophila (cantharelloid, photograph by Sava Kristic). B. Camarophyllopsis schulzeri (agaricoid, photograph by Soňa Jancˇovicˇová). C. Lamelloclavaria petersenii (agaricoid, photograph by Stefan Jacobsson). D. Clavaria fragilis group (clavarioid, photograph by Mike Wood). E. Hodophilus foetens group (agaricoid, photograph by Zuzana Egertová). Scale bar 5 1 cm. by QuickPHOTO MICRO 2.1. Enlarged scanned pictures of et al. (2013). The supermatix consisted of a total of 299 basidiospores were used for measuring with an accuracy of DNA sequences, of which 193 were newly produced by this 0.1 mm and for making line drawings. Microscopic structures study (41 rpb2, 77 28S, 75 ITS). The majority of the remain- were examined on desiccated herbarium specimens in ing sequences were included from previous works by Birke- Congo red solution with ammonia after a short treatment bak et al. (2013) and Kautmanová et al. (2012). Twenty-one in warm aqueous 10% KOH. Q-value is the length/width percent of individuals are represented by three loci, 31% by ratio of the basidiospores. Measurements exclude ornamen- two loci, and 48% by 28S only. Specimens were identified tation. Statistics for measurements of microscopic characters morphologically based on most recent key to identification are based on 30 measurements and given as a mean value (Petersen 1988, Knudsen and Vesterholt 2012). Morpho- plus/minus standard deviation; values in parentheses pro- types showing discrepancies with the phylogenetic analysis vide measured minimum or maximum values. Amyloidity (showing polyphyly or with uncertain delimitation) are and dextrinoidity of basidiospores were tested in Melzer’s labelled as species groups or complexes. reagent (Moser 1978). Phylogenetic analysis.—Alignments for individual regions were DNA extraction, PCR, and sequencing.—Protocols of Birkebak assembled using ClustalX (Larkin et al. 2007) and manually et al. (2013) were followed for DNA extraction, PCR, and adjusted by eye in MacClade 4.08 (Maddison and Maddison sequencing. The primer pairs ITS1F-ITS4 (White et al. 2005). Individual alignments were concatenated in SeaView 1990, Gardes and Bruns 1993) were used to amplify the ITS 4 (Gouy et al. 2010). gBlocks 0.91 (Castresana 2000, Talavera region. Combinations of LR0R-LR7, LR0R-LR5, or LR0R- and Castresana 2007) was used to exclude ambiguously LR16 (http://sites.biology.duke.edu/fungi/mycolab/primers. aligned sites. PartitionFinder (Lanfear et al. 2014) was used htm) were used to amplify and sequence the 28S region. to identify the best partition scheme and molecular models The primer pair b6F and b7.1R (Matheny 2005) were used under the AIC criterion. The sequence alignment files have to amplify and sequence the most variable region of the been deposited in TreeBASE (19107). Maximum likelihood rpb2 gene. (ML) phylogenetic reconstruction was performed with RAxML 7.4.2 (Stamatakis 2006) implemented in RAxML Taxon sampling.—171 total taxa were analyzed as a superma- GUI (Silvestro and Michalak 2012) with 1000 bootstrap repli- trix, 167 of which are in the Clavaria-Camarophyllopsis-Clavicor- cates. Bayesian inference (BI) was performed in MrBayes ona clade as recovered by Birkebak et al. (2013) 3.2.2 (Ronquist et al. 2011) running 10 000 000 generations (SUPPLEMENTARY TABLE I). Two species of Clavulinopsis and and sampling parameter states and trees every 10 000 genera- Ramariopsis each were used as outgroups based on Birkebak tions. To ensure that convergence had been reached, the 862 MYCOLOGIA average standard deviation of split frequencies was moni- The resulting clavarioid clades are not all well sup- tored to ensure that it fell below 0.01, and trace files of all ported in their placement in both phylogenetic recon- parameters were examined to ensure proper mixing. A structions. However, Clavaria sensu stricto (typified by 25% burn-in was used. The approximately unbiased test Cl. fragilis Holmsk.: Fr.) is well supported as the sister (AU test, Shimodaira 2002) was performed in CONSEL (Shi- group to Camarophyllopsis sensu stricto. The Cl. pullei modaira and Hasegawa 2001) to evaluate whether agaricoid clade (containing species identified as Cl. pullei Donk taxa could constitute a monophyletic group and whether spe- cies assigned to the genus Clavaria could also form a mono- and Cl. atroumbrina Corner) is sister to Hodophilus
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