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Multi-Gene Phylogeny and Taxonomy of <I>Amauroderma</I> S. Lat. (<I

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Multi-Gene Phylogeny and Taxonomy of <I>Amauroderma</I> S. Lat. (<I Persoonia 44, 2020: 206–239 ISSN (Online) 1878-9080 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE https://doi.org/10.3767/persoonia.2020.44.08 Multi-gene phylogeny and taxonomy of Amauroderma s.lat. (Ganodermataceae) Y.-F. Sun1,2, D.H. Costa-Rezende3, J.-H. Xing1, J.-L. Zhou1, B. Zhang4, T.B. Gibertoni5, G. Gates6, M. Glen6, Y.-C. Dai1,2, B.-K. Cui1,2,* Key words Abstract Amauroderma s.lat. has been defined mainly by the morphological features of non-truncate and double- walled basidiospores with a distinctly ornamented endospore wall. In this work, taxonomic and phylogenetic stu- Ganodermataceae dies on species of Amauroderma s.lat. are carried out by morphological examination together with ultrastructural morphology observations, and molecular phylogenetic analyses of multiple loci including the internal transcribed spacer regions phylogeny (ITS), the large subunit of nuclear ribosomal RNA gene (nLSU), the largest subunit of RNA polymerase II (RPB1) Polyporales and the second largest subunit of RNA polymerase II (RPB2), the translation elongation factor 1-α gene (TEF) and ultrastructure the β-tubulin gene (TUB). The results demonstrate that species of Ganodermataceae formed ten clades. Species previously placed in Amauroderma s.lat. are divided into four clades: Amauroderma s.str., Foraminispora, Furtadoa and a new genus Sanguinoderma. The classification of Amauroderma s.lat. is thus revised, six new species are described and illustrated, and eight new combinations are proposed. SEM micrographs of basidiospores of Foramini­ spora and Sanguinoderma are provided, and the importance of SEM in delimitation of taxa in this study is briefly discussed. Keys to species of Amauroderma s.str., Foraminispora, Furtadoa, and Sanguinoderma are also provided. Article info Received: 19 January 2019; Accepted: 4 November 2019; Published: 4 May 2020. INTRODUCTION Coetzee et al. 2015, Hapuarachchi et al. 2015, Xing et al. 2016, 2018, Thawthong et al. 2017) and only a few studies dealt with Amauroderma was established by Murrill (1905) and is usually Amauroderma (Gomes-Silva et al. 2015, Costa-Rezende et classified in Ganodermataceae. The type species, A. schom­ al. 2016, 2017, Song et al. 2016). Regarding this phylogenetic burgkii was described from Guyana. The species of the genus context, Amauroderma has been pointed as polyphyletic and often emerged from the roots of living or dead trees on the regarded as Amauroderma s.lat., in which Amauroderma s.str. ground (Ryvarden 2004), and as traditional circumscription has been defined as a Neotropical clade (Gomes-Silva et al. the genus is distributed mainly in Neotropics and tropical or 2015, Costa-Rezende et al. 2016); as for the relevance of subtropical areas of Africa, Asia and Oceania. The taxonomy hyphal system composition and basidiospore ultrastructure for of the genus was mostly based on traditional morphological generic delimitation in the group was observed, as well as two characteristics. Macroscopically, it is usually characterized by new genera called Foraminispora and Furtadoa were proposed annual and stipitate to sessile basidiomata, dull to laccate pilei, (Costa-Rezende et al. 2017). Furthermore, the generic status fresh pore surface colour changing or not when bruised or dry. of Amauroderma s.lat. species from Asia and Oceania still was Microscopically, the genus presents dimitic to trimitic hyphal questioned (Song et al. 2016), such as ‘Amauroderma rude system, globose to ellipsoid basidiospores, without truncate clade’ composed by A. rude, A. rugosum and A. perplexum; apex, which are double-walled with thick and ornamented and ‘Amauroderma yunnanense clade’ composed by A. yun­ endospore wall (rarely smooth) (Furtado 1981, Corner 1983, nanense (Costa-Rezende et al. 2017), as well as a variety of Aime et al. 2003, Ryvarden 2004). Asian and African species which were not phylogenetically Taxonomic and phylogenetic studies of Ganodermataceae have tested. In this study, taxonomic and phylogenetic analyses of been carried out in recent years, but most studies focused on Amauroderma s.lat. were carried out based on more samples Ganoderma (Smith & Sivasithamparam 2000, Hong & Jung from areas outside the neotropics, such as Africa, Asia and 2004, Pilotti et al. 2004, Wang et al. 2009, Cao et al. 2012, Oceania. Based on the abundant specimens, morphological Cao & Yuan 2013, Li et al. 2014b, Lima Júnior et al. 2014, descriptions inclu ding ultrastructural features combined with six gene markers provided convincing evidence to clarify the 1 Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, taxonomic status of the species in Amauroderma s.lat. Beijing Forestry University, Beijing 100083, China. 2 Institute of Microbiology, School of Ecology and Nature Conservation, Nine genera are accepted in Ganodermataceae, of which Beijing Forestry University, Beijing 100083, China. Amauroderma s.str., Foraminispora, Furtadoa, Haddowia and 3 Universidade Estadual de Feira de Santana, Departamento de Biologia, Magoderna have non-truncate basidiospores, while Gano­ Campus Universitário, CEP 44031-460, Feira de Santana, BA, Brasil. derma, Tomophagus, Humphreya and Trachyderma have ba- 4 Engineering Research Centre of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun 130118, China. sidiospores with obvious truncate apex (Karsten 1881, Imazeki 5 Universidade Federal de Pernambuco, Centro de Biociências, Departa- 1939, 1952, Steyaert 1972, Corner 1983, Moncalvo & Ryvarden mento de Micologia, Av. Avenida da Engenharia, s/n, CEP 50740-600, 1997, Costa-Rezende et al. 2017). Amauroderma s.str. is Recife, Pernambuco, Brasil. distinguished by di-trimitic hyphal system and endospore wall 6 Tasmanian Institute of Agriculture, Private bag 98, Hobart, Tasmania 7001, Australia. with solid columnar to semi-reticulated ornamentation (Costa- * Corresponding author e-mail: [email protected]. Rezende et al. 2017). Foraminispora has the unique ultrastruc- © 2020 Naturalis Biodiversity Center & Westerdijk Fungal Biodiversity Institute You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. Y.-F. Sun et al.: Phylogeny and taxonomy of Amauroderma 207 ture features of basidiospores with hollow columnar endospore DNA extraction, amplification and sequencing ornamentation, which persist to the exospore wall forming holes A CTAB rapid plant genome extraction kit-DN14 (Aidlab Bio- sometimes under SEM (Costa-Rezende et al. 2017). Furtadoa technologies Co., Ltd, Beijing, China) and an FH plant DNA is distinguished by a monomitic hyphal system in context, with kit II (Demeter Biotech Co., Ltd., Beijing, China) were used clamped and simple-septate generative hyphae which are differ- to extract total genomic DNA from dried specimens and to ent from other genera (Costa-Rezende et al. 2017). Haddowia perform the polymerase chain reaction (PCR) according to the has distinctive basidiospores, of which the exo spore wall with manufacturer’s instructions with some modifications (Cui et al. longitudinal ridges partly connected with short transverse walls 2019, Shen et al. 2019). (Steyaert 1972, Corner 1983). Magoderna can be distinguished The internal transcribed spacer regions (ITS) was amplified with by woody hard basidiomata with slightly shiny pileus and fibrotic primer pairs ITS5 and ITS4 (White et al. 1990); for the large context, and its hyphae in pileal cover anticlinal (Steyaert 1972). subunit of nuclear ribosomal RNA gene (nLSU) we used LR0R Tomophagus has light basidiomata, with a pale and soft context and LR5 (Vilgalys & Hester 1990). The primer pairs RPB1-Af (Le et al. 2012). Humphreya can be characterized by basidi- and RPB1-Cr (Matheny et al. 2002) were used to amplify the ospores with reticular or erratic irregular ridged double walls largest subunit of RNA polymerase II (RPB1), and primer (Steyaert 1972). Trachyderma is mainly characterized by a pairs fRPB2-5F and fRPB2-7CR (Liu et al. 1999) were used fleshy succulent context when growing (Imazeki 1939, 1952). to amplify the second subunit of RNA polymerase II (RPB2). In this study, in order to clarify the taxonomy and phylogeny of The translation elongation factor 1-α gene (TEF) was amplified taxa in Amauroderma s.lat., specimens from different regions with primer pairs EF1-983F and EF1-1567R (Rehner & Buckley of the world were studied using macro-morphology, microscopic 2005). Primer pairs Bt-1a and Bt-1b (Glass & Donaldson 1995) examinations together with ultrastructural observations and mo- were used to amplify the β-tubulin gene (TUB). The primer LR7 lecular phylogenetic analyses of six genes (including ITS, nLSU, (Vilgalys & Hester 1990) was used sometimes as an alternative RPB1, RPB2, TEF and TUB). According to the integrative re- to LR5; i2.2F and aCr (Binder et al. 2010) were used as alterna- search,
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