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Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) Introducing the Ant-Associated Genus Myrmecopterula Gen

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Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) Introducing the Ant-Associated Genus Myrmecopterula Gen bioRxiv preprint doi: https://doi.org/10.1101/718809; this version posted September 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Reclassification of Pterulaceae Corner (Basidiomycota: Agaricales) introducing the ant-associated genus Myrmecopterula gen. nov., Phaeopterula Henn. and the corticioid Radulomycetaceae fam. nov. Caio A. Leal-Dutra1,5, Gareth W. Griffith1, Maria Alice Neves2, David J. McLaughlin3, Esther G. McLaughlin3, Lina A. Clasen1 & Bryn T. M. Dentinger4 1 Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DD WALES 2 Micolab, Departamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil 3 Department of Plant and Microbial Biology, University of Minnesota, 1445 Gortner Avenue, St. Paul, Minnesota 55108, USA 4 Natural History Museum of Utah & Biology Department, University of Utah, 301 Wakara Way, Salt Lake City, Utah 84108, USA 5 CAPES Foundation, Ministry of Education of Brazil, P.O. Box 250, Brasília – DF 70040-020, Brazil ABSTRACT Pterulaceae was formally proposed to group six coralloid and dimitic genera [Actiniceps (=Dimorphocystis), Allantula, Deflexula, Parapterulicium, Pterula and Pterulicium]. Recent molecular studies have shown that some of the characters currently used in Pterulaceae Corner do not distin- guish the genera. Actiniceps and Parapterulicium have been removed and a few other resupinate genera were added to the family. However, none of these studies intended to investigate the relation- ship between Pterulaceae genera. In this study, we generated 278 sequences from both newly col- lected and fungarium samples. Phylogenetic analyses support by morphological data allowed a re- classification of Pterulaceae where we propose the introduction of Myrmecopterula gen. nov. and Radulomycetaceae fam. nov., the reintroduction of Phaeopterula, the synonymisation of Deflexula in Pterulicium and 51 new combinations. Pterula is rendered polyphyletic requiring a reclassification; thus, it is split into Pterula, Myrmecopterula gen. nov., Pterulicium and Phaeopterula. Deflexula is re- covered as paraphyletic alongside several Pterula species and Pterulicium, and is sunk into the latter genus. Phaeopterula is reintroduced to accommodate species with darker basidiomes. The neotropi- cal Myrmecopterula gen. nov. forms a distinct clade adjacent to Pterula, and most members of this clade are associated with active or inactive attine ant nests. The resupinate genera Coronicium and Merulicium are recovered in a strongly supported clade close to Pterulicium. The other resupinate genera previously included in Pterulaceae, and which form basidiomes lacking cystidia and with monomitic hyphal structure (Radulomyces, Radulotubus and Aphanobasidium), are reclassified into Radulomycetaceae fam. nov. Allantula is still an enigmatic piece in this puzzle known only from the type specimen that requires molecular investigation. A key for the genera of Pterulaceae and Radu- lomycetaceae fam. nov. is provided here. KEYWORDS: Molecular phylogeny; fungal taxonomy; Pleurotineae; corticioid fungi; coralloid fungi; clavarioid fungi; coral mushroom; Aphyllophorales; fungal diversity; neotropical fungi; attine ants; fun- gus-farming ants; Attini; Attina 1 bioRxiv preprint doi: https://doi.org/10.1101/718809; this version posted September 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. INTRODUCTION was proposed in the family (Zhao et al. 2016) (Fig. 2). The history of Pterulaceae Corner begins with the hesitant proposal of the genus Pterula The ecological roles of Pterulaceae are not Fr. (hereinafter abbreviated as Pt.) in the well understood, most being classified from 1820s and 1830s by Elias Magnus Fries (Fries superficial observations as saprotrophs, grow- 1821, 1825, 1830). The typification of this ge- ing on wood or leaf litter, with wood decay po- nus was addressed by Lloyd (1919) and this tentially being the ancestral state. Whilst many was followed by discussion between M.S. species are found inhabiting soil or litter, two Doty, M.A. Donk and D.P. Rogers (Doty 1948; species are reported to associate with living Donk 1949; Rogers 1949, 1950). Ultimately plants, namely Pterula cf. tenuissima, endo- Corner (1952c) provided a thorough discus- phytic in asymptomatic leaves of Magnolia sion of the timeline of Fries’ decisions, which grandiflora, and Pterulicium xylogenum, causal was later confirmed with further clarification by agent of culm rot disease of bamboo (Munkac- M.A. Donk (Donk 1954; Donk 1963). si et al. 2004; Villesen et al. 2004; Harsh et al. 2005) and possibly also a pathogen of sugar- The number of species in Pterula grew dur- cane [see Corner (1952b)]. ing the late 19th and early 20th centuries, with J.H. Léveille, N.T Patouillard, P. C. Hennings, Pterulaceae has attracted more attention P. A. Saccardo, C. G. Lloyd, C. L. Spegazzini recently following the discovery of two distinct and M. J. Berkeley being the most active in the symbionts of fungus-farming ants in the genus naming of taxonomic novelties of Pterula in Apterostigma Mayr being included in several this period (Corner 1950, 1970). Lloyd (1919) phylogenetic and ecological studies (Matheny devoted an entire chapter to discuss the tax- et al. 2006; Hibbett 2007; Dentinger et al. onomy of the genus. However, the major con- 2009; Binder et al. 2010; Leal-Dutra 2015). tribution to the genus was made by E. J. H. Despite the absence (hitherto) of any teleo- Corner who added at least 45 new taxa (Cor- morph, phylogenetic analyses placed both ner 1950, 1952b, 1970, 1966, 1967). Corner species [Pterula nudihortorum Dentinger and (1950) created the Pteruloid series in Clavari- Pterula velohortorum Dentinger, previously aceae Chevall. to group, besides Pterula, oth- known as G2 and G4 (Dentinger 2014)] in a er genera with coralloid basidiome and dimitic strongly supported clade within Pterulaceae hyphal system. The Pteruloid series was (Munkacsi et al. 2004; Villesen et al. 2004). raised by Donk (1964) to Pteruloideae, a sub- family of Clavariaceae. Pterulaceae was for- Whilst these earlier phylogenetic studies mally proposed by Corner (1970) including the did not focus on resolving evolutionary rela- genera from the original Pteruloideae: Allantu- tionships of the genera, they did demonstrate la Corner, Deflexula Corner, Dimorphocystis that the coralloid genera of Pterulaceae are Corner (=Actiniceps Berk. & Broome), clearly polyphyletic. Amongst the morphologi- Parapterulicium Corner, Pterula and Pterulic- cal characters previously used to separate the ium Corner (hereinafter abbreviated as Pm.) genera, but now known to be phylogenetically (Corner 1950, 1952a, b, 1970) (Fig. 1). unreliable, is the orientation of basidiome growth that differentiates Pterula from Deflex- Following Corner’s reclassifications, the ula and the presence of a corticioid patch at major changes in Pterulaceae have resulted the base of the basidiome in Pterulicium (Cor- from molecular phylogenetic analyses. Actini- ner 1950, 1952a, 1970). Therefore, the reclas- ceps Berk. & Broome was shown within Agari- sification of Pterulaceae is required to restore cales to be distantly related to Pterulaceae and the monophyly of the genera. Parapterulicium was removed to Russulales (Dentinger and McLaughlin 2006; Leal-Dutra We aimed to clarify the phylogenetic rela- et al. 2018). Four resupinate genera were tionships of the various genera within Pteru- transferred to Pterulaceae: Aphanobasidium laceae through collection of new samples dur- Jülich, Coronicium J. Erikss. & Ryvarden, ing fieldwork campaigns in Brazil and addition- Merulicium J. Erikss. & Ryvarden, and Radu- ally sampling of fungarium specimens. This lomyces M.P. Christ. (Larsson 2007; Larsson has yielded sequence data from many speci- et al. 2004) and, finally, the new poroid genus mens not included in previously phylogenetic Radulotubus Y.C. Dai, S.H. He & C.L. Zhao analyses, permitting a comprehensive reap- praisal of the phylogeny of Pterulaceae. Here 2 bioRxiv preprint doi: https://doi.org/10.1101/718809; this version posted September 27, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Fig. 1 Diversity of coralloid genera of Pterulaceae. A-F: Myrmecopterula (A: Apterostigma sp. nest with M. velohorto- rum with Myrmecopterula sp. SAPV1 growing atop of the garden veil; B, C, F: Myrmecopterula sp. D: Apterostigma sp. nest with M. nudihortorum; E: M. moniliformis). G-H: Pterula (G: P. cf. loretensis; H: P. cf. verticillata). I-L: Pterulicium (I: P. secundirameum; J: P. aff fluminensis; K: P. lilaceobrunneum. L: P. sprucei). M-O: Phaeopterula (M: Phaeopterula sp.; N: P. stipata; O: P. juruensis). Close observation on photos B and C reveal the basidiomes growing from granular sub- strate resembling substrate of ants’ fungus garden. Photos D, E and G kindly provided by Ted Schultz, Susanne Sourell and Michael Wherley
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