available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 81: 149–189.

Phylogenetic classification of yeasts and related taxa within Pucciniomycotina

Q.-M. Wang1, A.M. Yurkov2, M. Göker2, H.T. Lumbsch3, S.D. Leavitt3, M. Groenewald4, B. Theelen4, X.-Z. Liu1, T. Boekhout1,4,5*, and F.-Y. Bai1,4*

1State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; 2Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany; 3Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA; 4CBS Fungal Biodiversity Centre (CBS–KNAW), Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 5Shanghai Key Laboratory of Molecular Medical Mycology, Changzheng Hospital, Second Military Medical University, Shanghai, China

*Correspondence: T. Boekhout, [email protected]; F.-Y. Bai, [email protected]

Abstract: Most small genera containing yeast species in the Pucciniomycotina (Basidiomycota, Fungi) are monophyletic, whereas larger genera including Bensingtonia, Rhodosporidium, Rhodotorula, Sporidiobolus and Sporobolomyces are polyphyletic. With the implementation of the “One Fungus = One Name” nomenclatural principle these polyphyletic genera were revised. Nine genera, namely Bannoa, Cystobasidiopsis, Colacogloea, Kondoa, Erythrobasidium, Rhodotorula, Sporobolomyces, Sakaguchia and Sterigmatomyces, were emended to include anamorphic and teleomorphic species based on the results obtained by a multi-gene phylogenetic analysis, phylogenetic network analyses, branch length-based methods, as well as morphological, physiological and biochemical comparisons. A new class Spiculogloeomycetes is proposed to accommodate the order Spiculogloeales. The new families Buckleyzymaceae with Buckleyzyma gen. nov., Chrysozymaceae with Chrysozyma gen. nov., Microsporomycetaceae with Microsporomyces gen. nov., Ruineniaceae with Ruinenia gen. nov., Symmetrosporaceae with Symmetrospora gen. nov., Colacogloeaceae and Sakaguchiaceae are proposed. The new genera Bannozyma, Buckleyzyma, Fellozyma, Hamamotoa, Hasegawazyma, Jianyunia, Rhodosporidiobolus, Oberwin- klerozyma, Phenoliferia, Pseudobensingtonia, Pseudohyphozyma, Sampaiozyma, Slooffia, Spencerozyma, Trigonosporomyces, Udeniozyma, Vonarxula, Yamadamyces and Yunzhangia are proposed to accommodate species segregated from the genera Bensingtonia, Rhodosporidium, Rhodotorula, Sporidiobolus and Sporobolomyces. Ballistosporomyces is emended and reintroduced to include three Sporobolomyces species of the sasicola clade. A total of 111 new combinations are proposed in this study.

Key words: Fungi, GMYC approach, Molecular phylogeny, Phylogenetic rank boundary optimisation, Pucciniomycotina, Taxonomy, Yeasts.

Taxonomic novelties: New class: Spiculogloeomycetes Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; New families: Buckleyzymaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Chrysozymaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Colacogloeaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Microsporomycetaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Ruineniaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sakaguchiaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Symmetrosporaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; New genera: Bannozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Buckleyzyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Chrysozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Fellozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Hamamotoa Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Hasegawazyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Jianyunia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Microsporomyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Oberwinklerozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Phyllozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Phenoliferia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Pseudobensingtonia F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, Pseudohyphozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Rhodosporidiobolus Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Ruinenia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sampaiozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Slooffia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Spencerozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Symmetrospora Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Trigonosporomyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Udeniozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Vonarxula Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Yamadamyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Yunzhangia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout; New combinations: Ballistosporomyces sasicola (Nakase & M. Suzuki) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, B. taupoensis (Hamam. & Nakase) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, Bannoa bischofiae (Hamam., Thanh & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. syzygii (Hamam., Thanh & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. ogasawarensis (Hamam., Thanh & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Bannozyma arctica (Vishniac & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. yamatoana (Nakase, M. Suzuki & M. Itoh) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Buckleyzyma armeniaca (R.G. Shivas & Rodr. Mir.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. aurantiaca (Saito) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. kluyveri-nielii (van der Walt) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. phyllomatis (van der Walt & Y. Yamada) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, B. salicina (B.N. Johri & Bandoni) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Chrysozyma fushanensis (Nakase, F.L. Lee & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. griseoflava (Nakase & M. Suzuki) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Colacogloea cycloclastica (Thanh, M.S. Smit, Moleleki & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. diffluens (Ruinen) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. eucalyptica (C.H. Pohl, M.S. Smit & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. falcata (Nakase, M. Itoh & M. Suzuki) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. foliorum (Ruinen) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. philyla (van der Walt, Klift & D.B. Scott) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. retinophila (Thanh, M.S. Smit, Moleleki & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. terpenoidalis (Thanh, M.S. Smit, Moleleki & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Cystobasidiopsis lactophilus (Nakase, M. Itoh, M. Suzuki & Bandoni) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, C. lophatheri (Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Cystobasidium portillonense (F. Laich, I. Vaca & R. Chavez) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Erythrobasidium elongatum (R.G. Shivas & Rodr. Mir.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, E. yunnanense (F.Y. Bai, M. Takash., Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Fellozyma inositophila (Nakase & M. Suzuki) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Hamamotoa lignophila (Dill, C. Ramírez & Gonzalez) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, H. singularis (Phaff & do Carmo-Sousa) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Hasegawazyma lactosa (Hasegawa) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Jianyunia sakaguchii (Sugita, M. Takash., Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Kondoa changbaiensis (F.Y. Bai & Q.M. Wang) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, K. miscanthi (Nakase & M. Suzuki) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, K. phyllada (van der Walt & Y. Yamada) Q.M.

Studies in Mycology Peer review under responsibility of CBS-KNAW Fungal Biodiversity Centre. Copyright © 2016, CBS-KNAW Fungal Biodiversity Centre. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).

149 WANG ET AL.

Wang, M. Groenew., F.Y. Bai & Boekhout, K. sorbi (F.Y. Bai & Q.M. Wang) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, K. subrosea (Nakase & M. Suzuki) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, K. thailandica (Fungsin, Hamam. & Nakase ) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, K. yuccicola (Nakase & M. Suzuki) Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout, Microsporomyces bloemfonteinensis (Pohl, M.S. Smit & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, M. magnisporus (Nakase, Tsuzuki, F.L. Lee, Sugita, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, M. pini (Pohl, M.S. Smit & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, M. orientis (Pohl, M.S. Smit & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Oberwinklerozyma silvestris (Golubev & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, O. straminea (Golubev & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, O. yarrowii (A. Fonseca & van Uden) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Phenoliferia psychrophenolica (Margesin & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. psychrophila (Margesin & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. glacialis (Margesin & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. himalayensis (Shivaji, Bhadra & Rao) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Phyllozyma coprosmicola (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. corallina (N. Furuya & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. dimennae (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. linderae (Nakase, M. Takash. & Hamam.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. novozealandica (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. producta (N. Furuya & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. subbrunnea (Nakase & M. Suzuki) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Pseudobensingtonia ingoldii (Nakase & Itoh.) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, P. musae (M. Takash., S.O. Suh & Nakase) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, Pseudohyphozyma bogoriensis (Deinema) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. buffonii (C. Ramírez) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, P. pustula (Buhagiar) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Rhodotorula alborubescens (Derx) Q.M. Wang, F.Y. Bai, Groenew. & Boekhout, R. babjevae (Golubev) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. diobovata (S.Y. Newell & I.L. Hunter) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. kratochvilovae (Hamam., Sugiy. & Komag.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. paludigena (Fell & Tallman) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. sphaerocarpa (S.Y. Newell & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. toruloides (I. Banno) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Rhodosporidiobolus fluvialis (Fell, Kurtzman, Tallman & J.D. Buck) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. azoricus (J.P. Samp. & Gadanho) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. microsporus (Higham ex Fell, Blatt & Statzell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. nylandii (M. Takash. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. ruineniae (Holzschu, Tredick & Phaff) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. lusitaniae (A. Fonseca & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. colostri (T. Castelli) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. odoratus (J.P. Samp., A. Fonseca & Valerio) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. poonsookiae (M. Takash. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Ruinenia clavata (F.Y. Bai & Q.M. Wang) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. diospyroris (Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. dracophylli (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. pyrrosiae (Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, R. rubra (Nakase, Oakada & Sugiy.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sakaguchia cladiensis (Fell, Statzell & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. lamellibrachiae (Nagah., Hamam., Nakase & Horikoshi) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. meli (Libkind, van Broock & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. oryzae (F.Y. Bai & Y.M. Cai) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sampaiozyma ingeniosa (Di Menna) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. vanillica (J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Slooffia cresolica (Middelhoven & Spaaij) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. pilati (F.H. Jacob, Faure-Raynaud & Berton) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. tsugae (Phaff & do Carmo-Sousa) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Spencerozyma crocea (Shifrine & Phaff) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sporobolomyces longiusculus (Libkind, van Broock & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. johnsonii (Nyland) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sterigmatomyces hyphaenes (Har. & Pat.) F.Y. Bai, Q.M. Wang, Groenewald & Boekhout, S. pulcherrima (J.E. Wright) F.Y. Bai, Q.M. Wang, Groenewald & Boekhout, S. novozelandica (W.B. Kendr. & X.D. Gong) F.Y. Bai, Q.M. Wang, Groenewald & Boekhout, Symmetrospora coprosmae (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. foliicola (R.G. Shivas & Rodr. Mir.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. gracilis (Derx) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. vermiculata (M. Takash. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. marina (Phaff, Mrak & Williams) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, S. symmetrica (F.Y. Bai & Q.M. Wang) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Trigonosporomyces hylophilus (van der Walt, van der Klift & D.B. Scott) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Ustilentyloma graminis (Rodr. Mir. & Diem) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Udeniozyma ferulica (J.P. Samp. & van Uden) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Vonarxula javanica (Ruinen) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Yamadamyces rosulatus (Golubev & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Yunzhangia auriculariae (Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Y. sonckii (Hopsu-Havu, Tunnela & Yarrow) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout.

Published online 11 January 2016; http://dx.doi.org/10.1016/j.simyco.2015.12.002. Hard copy: June 2015.

INTRODUCTION (Fell et al. 2000, Scorzetti et al. 2002, Boekhout et al. 2011, Sampaio 2011). With the implementation of the “One The subphylum Pucciniomycotina (Phylum Basidiomycota, Fungus = One Name” nomenclatural principle (Hawksworth Kingdom Fungi) presently includes eight classes, and four of 2011, Taylor 2011, McNeill et al. 2012) these five polyphyletic these, namely the Agaricostilbomycetes, Cystobasidiomycetes, genera need to be revised. Microbotryomycetes and Mixiomycetes, contain taxa with a Several studies using molecular analyses of ribosomal DNA dominant yeast stage (Aime et al. 2006, 2014, Bauer et al. 2006, sequences have provided a detailed grouping of species in Hibbett et al. 2007, Boekhout et al. 2011, Wang et al. 2015a). So clades among the four classes that contain yeast and yeast-like far 28 genera with yeast states have been proposed within species (Hamamoto & Nakase 2000, Nakase 2000, Fell et al. Pucciniomycotina (Boekhout et al. 2011, Turchetti et al. 2011, 2000, Scorzetti et al. 2002, Boekhout et al. 2011), but many Toome et al. 2013). Most of these genera are monophyletic, species remained unassigned (Boekhout et al. 2011). Thus the whereas five genera, namely Bensingtonia, Rhodosporidium, boundaries of the clades and genera have to be reassessed by Rhodotorula, Sporidiobolus and Sporobolomyces are poly- analysing a robust molecular dataset. In another study we phyletic (Fell et al. 2000, Scorzetti et al. 2002, Boekhout et al. analysed seven gene fragments, namely SSU (18S) rRNA, LSU 2011, Wang et al. 2015a, b). Bensingtonia, Rhodotorula and (26S/28S) rRNA D1/D2 domains, the ITS region (including the Sporobolomyces species are placed in various classes of Puc- 5.8S rRNA), RPB1 (the largest subunit of DNA polymerase II), ciniomycotina (Fell et al. 2000, Scorzetti et al. 2002, Boekhout RPB2 (the second largest subunit of DNA polymerase II), TEF1 et al. 2011, Hamamoto et al. 2011, Sampaio 2011, Yurkov (translation elongation factor 1-α) and CYTB (cytochrome b) that et al. 2015). Species of the teleomorphic genera Rhodospori- placed most pucciniomycetous yeast species into 51 well- dium and Sporidiobolus together with some asexual Rhodotorula supported clades (Wang et al. 2015a). These data are used and Sporobolomyces species are nested within Sporidiobolales here to address the taxonomic affiliations of those fungi. We propose 26 of the 51 recognised clades as new taxa at the

150 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA genus, family and class levels based on a phylogenetic and before for tremellomycetous fungi (Liu et al. 2015). Firstly, the taxonomic analysis of the combined seven genes-based and the overall GMYC analysis was carried out for the simulation at class enlarged LSU rRNA gene datasets. The assessment of taxo- level, and secondly nested analyses were run for the higher ESUs nomic ranks followed the branch length-based methods as identification at family level for each clade. Outgroup samples described in Liu et al. (2015). were excluded from the dataset using the drop.tip command in ape (Paradis 2006). A chronogram was calculated from the ML-based tree using the penalised likelihood method (Sanderson 2002)as MATERIALS AND METHODS implemented in the chronopl command in ape (Paradis 2006). The chronogram was then analysed using a modified GMYC package in SPLITS in R (version 2.10, www.cran.r-project.org) using the Strains and molecular phylogenetic analyses single threshold method. In the case of clades with a small number of samples the modified GMYC approach would not result in Multi-gene data of the yeast strains used were taken from a significant differences simply because of sampling size: these previous study (Wang et al. 2015a). As described previously were marked as ‘NA’ (not analysed). (Wang et al. 2015a) multi-gene phylogenetic trees constructed Phylogenetic rank boundary optimisation (PRBO), a phylo- from Maximum likelihood (ML), Maximum parsimony (MP) and genetic variant of clustering optimisation (Göker et al. 2009, 2010, Bayesian inference (BI) analyses of a dataset comprising Stielow et al. 2011), was conducted based on taxonomy-based nucleotide sequences of the ITS region (including the 5.8S reference information as described in Liu et al. (2015).A rRNA), the D1/D2 domains of the LSU rRNA, the SSU rRNA, and reduced classification including twelve putatively reliable genera the RPB1, RPB2, TEF1 and CYTB genes is used here to of pucciniomycetous yeasts was chosen as reference taxonomy. address the taxonomy of the pucciniomycetous yeasts. Fifty-one The resulting optimal upper boundaries for the divergence of each clades that may be equal to the generic rank, including 16 single- taxonomic rank were then applied back to the entire dataset. species lineages, were recognised among the pucciniomycetous These boundaries for each taxonomic rank were compared with yeasts used in the previous study with strong statistical support boundaries estimated from the entire classification (Table 1). For values in all trees drawn using different phylogenetic algorithms each newly proposed or already established taxon, maximum (Wang et al. 2015a). In order to detect the reliability of those 51 subtree height (MaSH) of its corresponding clade, absolute clades, a phylogenetic network approach was employed to infer deviation and significant deviation (Sigdev) from the threshold the relationships between those pucciniomycetous yeasts. The optimal for the reliable taxa were calculated. One hundred seven genes-based phylogenetic network was constructed in bootstrap replicates were applied to obtain the 95% confidence SplitsTree4 (Huson & Bryant 2006) using the ConsensusNetwork intervals for the boundaries to detect the significances of the algorithm with default parameter settings. The seven single-gene divergences from the optimal range for each taxonomic rank. ML trees used in the phylogenetic network analysis were con- The seven genes-based ML tree used in Wang et al. (2015a) structed using RAxML-HPC 7.2.8 (Stamatakis 2006) using the was employed as the basis for the PRBO and iterative modified parameter settings described previously (Wang et al. 2015a). GMYC analyses. The taxa within Ustilaginomycotina were used The supplementary LSU rRNA gene (D1/D2 domains) as outgroup and taxa within Pucciniomycetes were used as sequence dataset containing data from newly published pucci- ingroup in the above two analyses. Note that none of the two fi niomycetous yeast species and a few additional lamentous methods was followed strictly in the current study. Where possible, teleomorphic taxa was constructed and subjected to constrained wider circumscriptions of taxa were chosen to lower the number of maximum likelihood (ML) and maximum parsimony (MP) ana- taxonomic changes suggested; moreover, where possible, clades lyses based on the topology of a seven genes-based dataset with distinct phenotypic or ecological features were proposed as taken from Wang et al. (2015a). The LSU sequences were new taxa (Liu et al. 2015). Additionally, already established taxa aligned with MAFFT version 7 and the G-INS-i option (Standley were kept unless they appeared evidently non-monophyletic. K 2013). Constrained phylogenetic analyses were only inforced for species previously analysed using seven DNA loci. Only bi- partitions that received at least 85% bootstrap support during fast bootstrapping of the seven genes-based dataset (Wang et al. RESULTS AND DISCUSSION 2015a) conducted with Pthreads-parallelised RAxML version 8.1.24 (Stamatakis 2014) were used as a backbone constraint Taxonomic units addressed by the iterative for LSU phylogenetic inference. Fast bootstrapping in conjunc- modified GMYC and PRBO analyses tion with the autoMRE bootstopping criterion (Pattengale et al. 2009) and subsequent search for the best tree (Stamatakis The pucciniomycetous yeast species belong to four recognised et al. 2008) were conducted using the GTRCAT model approx- classes, namely Agaricostilbomycetes, Cystobasidiomycetes, imation. MP bootstrapping with 1 000 replicates was conducted Microbotryomycetes and Mixiomycetes (Bauer et al. 2006, with TNT version 1.1/June 2015 (Goloboff et al. 2008). The Hibbett et al. 2007, Boekhout et al. 2011). The overall modified alignments and trees were deposited in TreeBASE (No. 18537). GMYC analysis supported the Agaricostilbomycetes without Spiculogloeales as a class in agreement with the indication that Quantitative assessment of taxonomic ranks Spiculogloeales may represent a new class within Pucciniomy- cotina based on the seven genes-based phylogenetic analyses The modified Generalized Mixed Yule Coalescent (GMYC) (Wang et al. 2015a). Thus Spiculogloeomycetes is proposed as method (Humphreys & Barraclough 2014) was applied iteratively a new class to accommodate the order Spiculogloeales. to identify higher evolutionary significant units (higher ESUs) The nested analyses of the GMYC approach identified five above the species levels in the pucciniomycetous yeasts as done families in the class Agaricostilbomycetes (Table 2), including the

www.studiesinmycology.org 151 WANG ET AL.

Table 1. PRBO results showing the divergences, if any, of the Consequently, B. sakaguchii is placed into a new genus (see ‘ ’ proposed genera from the optimal range of divergences for Taxonomy), which is presently treated as incertae sedis in the their rank as inferred from selected reference data. Agaricostilbales. Nine clades were indentified at the family level within Cys- Taxa Rank MaSH Deviation Sigdev tobasidiomycetes by the nested analyses of GMYC (Table 2). Agaricostilbomycetes Class 0.71223 0.07318 0 The presently accepted families Cystobasidiaceae, Eryth- Agaricostilbum clade Genus 0.22827 0 0 robasidiaceae and Naohideaceae belong to Cystobasidiales, Erythrobasidiales and Naohideales, respectively. The genus ingoldii clade Genus 0.14859 0 0 Occultifur is separated from Cystobasidiaceae as a family in the Chionosphaera* Genus 0.29924 0 0 GMYC analyses, but we presently prefer to keep this genus in Kurtzmanomyces* Genus 0.33350 0.02844 0 the Cystobasidiaceae due to the low number of taxa in this lactophilus clade Genus 0.25804 0 0 genus. The Cyrenella and Rhodotorula lactosa lineages were sasicola clade Genus 0.15364 0 0 suggested as two new families in the Erythrobasidiales by the Kondoa clade* Genus 0.28874 0 0 GMYC nested analyses, however, these two lineages represent single species each, and, therefore, we temporarily placed them Bensingtonia* Genus 0.24787 0 0 as ‘incertae sedis’ in the Erythrobasidiales. The aurantiaca and ruber clade Genus 0.29828 0 0 marina clades were grouped into one family in the GMYC nested subbrunneus clade Genus 0.39731 0.09225 0 analyses, which is not supported by the phylogenetic analysis of Cystobasidiomycetes Class 0.51968 0 0 seven genes that showed the two clades as a paraphyletic group Erythrobasidium clade* Genus 0.16907 0 0 (Wang et al. 2015a). The magnisporus and Sakaguchia clades fi Bannoa clade* Genus 0.15301 0 0 were identi ed as families in agreement with the phylogenetic analysis of seven genes (Wang et al. 2015a). aurantiaca clade Genus 0.16265 0 0 Within Microbotryomycetes two families, namely Leucospor- marina clade Genus 0.23897 0 0 idiaceae and Microbotryaceae, were supported by the nested Sakaguchia clade* Genus 0.29017 0 0 analyses of GMYC approach (Table 2). The family Spor- magnisporus clade Genus 0.33920 0.03414 0 idiobolaceae in the Sporidiobolales was divided into three fam- Cystobasidium (minuta) clade* Genus 0.18036 0 0 ilies represented by the Sporidiobolus clade, the Microbotryomycetes Class 0.72324 0.08419 0 Rhodosporidium clade and the mixed Rhodosporidium/ Sporidiobolus clade, respectively. We preserve the current Sporidiobolus clade Genus 0.34525 0.04020 0 taxonomic status of Sporidiobolaceae because the phenotype of Rhodosporidium clade Genus 0.40759 0.10253 0 these three clades is similar and it forms a strongly supported mixed Rhodosporidium/ Genus 0.16275 0 0 lineage in the phylogenetic analysis of seven genes (Wang et al. Sporidiobolus clade 2015a). The Kriegeriaceae and Camptobasidiaceae in the Kriegeria* Genus 0.21892 0 0 Kriegeriales were grouped into a single family in the nested glacialis clade Genus 0.16560 0 0 GMYC analyses. However, the Camptobasidiaceae, including buffonii clade Genus 0.10602 0 0 Glaciozyma antarctica, clustered together with the Kriegeriaceae yarrowii clade Genus 0.09543 0 0 lacking support value in the ML analysis and they did not occur in the same cluster in the MP and BI analyses (Wang et al. 2015a, tsugae clade Genus 0.23831 0 0 Fig. 1 of this study). Consequently the two families are main- singularis clade Genus 0.05035 0 0 tained in this study. yamatoana clade Genus 0.06763 0 0 Ten clades and seven single-species lineages in Micro- griseoflavus clade Genus 0.16370 0 0 botryomycetes could not be assigned to presently recognised Curvibasidium clade* Genus 0.04099 0 0 families and orders (Wang et al. 2015a). These clades are Colacogloea clade* Genus 0.23771 0 0 strongly divergent from each other and seem to have a sister relationship to the known families and orders within Micro- sonckii clade Genus 0.06955 0 0 botryomycetes (Fig. 1). The species Rhodotorula hylophila, vanillica clade Genus 0.07445 0 0 R. javanica, R. crocea and Reniforma strues were not included in Leucosporidium clade* Genus 0.15399 0 0 the nested GMYC analyses because they occurred outside the Microbotryum clade Genus 0.14270 0 0 Microbotryomycetes in the overall GMYC analysis. In the nested fl Note: MaSH: Maximum Subtree Height; Deviation: deviation from the point GMYC analyses, the griseo avus, yamatoana, singularis estimate for the upper (positive value) or lower (negative value) threshold of the clades and Sporobolomyces inositophilus were identified as one rank of the taxon; Sigdev: significant deviation, i.e. a deviation even outside the family that was supported by the phylogenetic analysis of seven upper or lower 95 % confidence band of the upper or lower threshold, respec- genes with strong support values (Wang et al. 2015a); the tively. Zero indicates taxa with the appropriate divergence, negative values buffonii, tsugae and yarrowii clades were assigned to one indicate taxa that are too small, positive values taxa that are too large. An asterisk (*) indicates the well-established taxa that were used as a reference classification family, but this was weakly supported by the seven genes ML for PRBO. analysis (57 % BP), lacking support in the BI analysis and were not supported by the MP analysis (Fig. 1), and consequently, recognised families Agaricostilbaceae, Chionosphaeraceae and they are not treated as a single family in this study; the other Kondoaceae, a new Agaricostilbales family 1 (ruber clade) and a clades and the single-species lineages were identified as new Agaricostilbales family 2 (Bensingtonia sakaguchii line- separate families in the nested GMYC analyses (Table 2). age). Because only B. sakaguchii occurs in the new Agar- Among 51 pucciniomycetous yeast clades suggested as icostilbales family 2, this family is not proposed in this study. genera in the previous multi-gene phylogenetic study (Wang

152 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Table 2. Analyses with the modified GMYC approach showing the supported classification of the pucciniomycetous yeast at family and class levels. Class/Order family Genus GMYC

Agaricostilbomycetes supported Agaricostilbales Kondoaceae supported Kondoa Bensingtonia Agaricostilbaceae supported Sterigmatomyces (Agaricostilbum clade) Pseudobensingtonia (ingoldii clade) Chionosphaeraceae supported Chionosphaera Kurtzmanomyces Mycogloea nipponica Ballistosporomyces (sasicola clade) Cystobasidiopsis (lactophilus clade) Ruineniaceae new family Ruinenia (ruber clade) incertae sedis in Jianyunia (Bensingtonia sakaguchii) new family the Agaricostilbales Spiculogloeomycetes not supported Spiculogloeales Spiculogloeaceae supported Phyllozyma (subbrunneus clade) Cystobasidiomycetes not supported Cystobasidiales Cystobasidiaceae not supported Occultifur Cystobasidium (minuta clade) Erythrobasidiales Erythrobasidiaceae supported Erythrobasidium Bannoa incertae sedis in Hasegawazyma (Rhodotorula lactosa) new family the Erythrobasidiales Cyrenella new family Naohideales Naohideaceae supported Naohidea incertae sedis in the Cystobasidiomycetes Buckleyzymaceae not supported Buckleyzyma (aurantiaca clade) Symmetrosporaceae not supported Symmetrospora (marina clade) Sakaguchiaceae new family Sakaguchia Microsporomycetaceae new family Microsporomyces (magnisporus clade) Microbotryomycetes not supported Sporidiobolales (continued on next page)

www.studiesinmycology.org 153 WANG ET AL.

Table 2. (Continued). Class/Order family Genus GMYC

Sporidiobolaceae not supported Rhodotorula (Rhodosporidium clade) new family Rhodosporidiobolus new family (mixed Rhodosporidium/Sporidiobolus clade) Sporobolomyces (Sporidiobolus clade) new family Kriegeriales Kriegeriaceae not supported Kriegeria Meredithblackwellia Phenoliferia (glacialis clade) Yamadamyces (Rhodotorula rosulata) Camptobasidiaceae not supported Glaciozyma Leucosporidiales Leucosporidiaceae supported Leucosporidium Microbotryales Microbotryaceae supported Microbotryum Ustilentylomataceae supported Ustilentyloma Heterogastridiales Heterogastridiaceae supported Heterogastridium incertae sedis in the Microbotryomycetes Chrysozymaceae new family Chrysozyma (griseoflavus clade) Bannozyma (yamatoana clade) Hamamotoa (singularis clade) Fellozyma (Sporobolomyces inositophilus) Colacogloeaceae new family Colacogloea Genera incertae sedis in the Microbotryomycetes Pseudohyphozyma (buffonii clade) new family Slooffia (tsugae clade) Oberwinklerozyma (yarrowii clade) Sampaiozyma (vanillica clade) new family Yunzhangia (sonckii clade) new family Curvibasidium new family Pseudoleucosporidium (Leucosporidium fasciculatum) Udeniozyma (Rhodotorula ferulica) new family Reniforma new family Trigonosporomyces (Rhodotorula hylophila) new family Vonarxula (Rhodotorula javanica) new family Spencerozyma (Rhodotorula crocea) Mixiomycetes not supported Mixiales Mixiaceae NA Mixia Note: NA means “not analysed”. In the overall GMYC analysis, Naohideales is a separate class from Cystobasidiomycetes; Spiculoglomycetes and Mixiomycetes were identified as one class; Heterogastridium, Rhodotorula hylophila, and Reniforma form a separate class from Microbotryomycetes; Rhodotorula javanica and Rhodotorula crocea form another separate class from Microbotryomycetes.

154 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Fig. 1. Phylogenetic tree inferred using the combined sequences of SSU rRNA, LSU rRNA D1/D2 domains, ITS regions (including 5.8S rRNA), RPB1, RPB 2, TEF1 and CYTB, depicting the phylogenetic positions of existing yeast taxa and new genera (in bold) within Pucciniomycotina. The tree backbone was constructed using maximum likelihood analysis. Bootstrap percentages of maximum likelihood and maximum parsimony analyses over 50 % from 1 000 bootstrap replicates and posterior probabilities of Bayesian inference above 0.95 are shown respectively from left to right on the deep and major branches. Bar = 0.2 substitutions per nucleotide position. Note: ns, not supported (BP < 50 % or PP < 0.9); nm, not monophyletic. The new taxa are in bold.

www.studiesinmycology.org 155 WANG ET AL. et al. 2015a), only few were found to deviate from the optimal species were added to the dataset, namely Cystobasidium range of divergences as determined in the PRBO analysis, and fimetarium, Camptobasidium hydrophilum, Meredithblackwellia were found to significantly deviate (Table 1), which supports the eburnea and Microbotryozyma collariae (Figs 5–7). Newly preliminary taxonomic conclusions from the multi-gene phylo- added sequences substantially expanded the following clades genetic analysis. Twenty-six of them represent currently recognised in Wang et al. (2015a), viz. Curvibasidium (Fig. 7), described genera. The others are proposed as new genera Glaciozyma (Fig. 6), Ruinenia (Fig. 4) and Slooffia (Fig. 6). (Fig. 1) based on the phylogenetic analyses, PRBO analysis and phenotypic comparisons (Table 1, Table 3 and Figs 2, 3) pre- sented in this study. TAXONOMY

Phylogenetic analyses Class Agaricostilbomycetes R. Bauer et al., Mycol. Progr. 5: 45. 2006. Only 156 species from 184 ones used in the seven genes-based tree (Wang et al. 2015a) were selected to construct the phylo- Type order: Agaricostilbales Oberw. & R. Bauer genetic network, because some protein genes were not available for all species. As a result all clades recognised in the seven This class contains the order Agaricostilbales. Our previous genes-based tree could be recognised in the network approach. multi-gene sequence analyses indicated that nine well support The network result showed that the five classes containing yeast clades, namely Agaricostilbum, Bensingtonia, Chionos- species, viz. Agaricostilbomycetes, Cystobasidiomycetes, phaera, Kondoa, Kurtzmanomyces, ingoldii, lactophilus, Microbotryomycetes, Mixiomycetes and Spiculogloeomycetes, ruber, sasicola, and two species Bensingtonia sakaguchii and remain separated (Fig. 2A). The 51 clades in the seven genes- Mycogloea nipponica, occurred in the Agaricostilbales (Wang based tree are also separated without any reticulation et al. 2015a). These clades which are delimited at the generic (Fig. 2B–D). This result confirmed the reliability of the combined rank are supported by the PRBO analysis (Table 1), the phylo- phylogenetic analysis of the seven genes. genetic network analysis (Fig. 2B), and the analysis of the For a better understanding of the phylogenetic relationships enlarged LSU rRNA gene dataset (Fig. 4). The genera Chio- between Agaricostilbomycetes, Cystobasidiomycetes, Micro- nosphaera and Kurtzmanomyces are well-established genera. botryomycetes, Mixiomycetes and Spiculogloeomycetes, and to The genera Sterigmatomyces, Cystobasidiopsis and Kondoa are include recently described species, an enlarged LSU rRNA gene emended to include both teleomorphic and anamorphic species dataset was analysed. Thereby, the LSU dataset analysed by in the Agaricostilbum, lactophilus and Kondoa clades, respec- Wang et al. (2015a) was enlarged from 184 to 242 sequences tively. Ballistosporomyces is emended and reintroduced to containing both sexual (e.g. Camptobasidium, Cystobasidium, include species in the sasicola clade. Jianyunia gen. nov., Glaciozyma, Kondoa and Ustilentyloma) and asexual (e.g. Pseudobensingtonia gen. nov. and Ruinenia gen. nov. are pro- Rhodotorula, Sporobolomyces and Occultifur) genera and spe- posed to accommodate the species in the Bensingtonia cies (Figs 4–8). The constrained ML analysis of the enlarged sakaguchii, ingoldii and ruber clades, respectively. Ruin- LSU dataset was used to place species known from LSU rRNA eniaceae fam. nov. is proposed to accommodate the genus gene sequences in the phylogenetic clades previously recog- Ruinenia based on results from the phylogenetic analysis of nised in the analysis based on the seven DNA-loci. Results from seven genes (Fig. 1) and GMYC analyses (Table 2). the LSU analysis were not used to challenge the results of the multi-gene study (Wang et al. 2015a), but to investigate the Order Agaricostilbales Oberw. & R. Bauer, Sydowia 41: 240. stability of the taxonomy in undersampled clades. 1989. The enlarged analysis of the LSU rRNA gene dataset sug- gests that the number of single-species lineages in Micro- Type family: Agaricostilbaceae Oberw. & R. Bauer. botryomycetes is likely to increase in the future, since many sequences representing potentially new species could not be This order was proposed to accommodate the family Agar- assigned to any of the clades recognised (Figs 4–8). In agree- icostilbaceae (Oberwinkler & Bauer 1989). The Agar- ment with previous studies (Scorzetti et al. 2002, Weiß et al. icostilbaceae, Chionosphaeraceae and Kondoaceae were 2004, Boekhout et al. 2011, Wang et al. 2015a), our results accepted in this order by Bauer et al. (2006). Here we propose showed that LSU alone is not sufficient to resolve many clades in Ruineniaceae and Jianyunia as ‘incertae sedis’ in the Microbotryomycetes (Fig. 6). Agaricostilbales. The addition of the supplemental species or sequences representing potential new species resulted in the enlargement Family Agaricostilbaceae Oberw. & R. Bauer, Sydowia 41: 240. of several clades, especially single species lineages recognised 1989. in the phylogenetic analysis of seven genes (Wang et al. 2015a), e.g. Fellozyma, Glaciozyma, Occultifur and Rhodotorula hordea Type genus: Agaricostilbum J.E. Wright. (Figs 5–7). In addition, a few new clades and single-species lineages were identified such as Camptobasidium hydrophilum, This family is characterised by septal pores without microbodies, Meredithblackwellia eburnea and Rhodotorula svalbardensis aseptate basidiospores produced in a yeast-like manner and lack (Fig. 6). Most supplemental sequences (34 out of 58) were of tremelloid haustorial cells (Oberwinkler & Bauer 1989, Bauer located in Microbotryomycetes (Figs 6, 7). The following type et al. 2006).

156 Table 3. Selected physiological and biochemical characteristics of different clades within the Pucciniomycotina. www.studiesinmycology.org Genus or species d - α -Inositol -Arabinose -Arabinose Sucrose Raffinose Lactose Trehalose Maltose Melezitose Methyl- -glucoside Soluble Starch l d Glycerol myo dl -glucoside Nitrate Nitrite CoQ

Agaricostilbomycetes Agaricostilbales Kondoaceae Kondoa vvv+vvv vvv+ − vvv9 Bensingtonia vvvvvv− vvv+ − v+v9 Agaricostilbaceae Sterigmatomyces (Agaricostilbum clade) v v v + − vv − v++ − vvv9 Pseudobensingtonia (ingoldii clade) v v v + − v − vv++ − vvv9 Chionosphaeraceae Ballistosporomyces (sasicola clade) + v v + + v v + v −−−− vv10 Cystobasidiopsis (lactophilus clade) + v v + + v v + v + + − +vv10 Kurtzmanomyces vvvvvv−−vvvvv ++10 Chionosphaera −−−vv−− vvvvvv −−10 Jianyunia (Bensingtonia sakaguchii) −−++++v +−−−−− −−9

Ruinenia (ruber clade) + + v v v + v v v − v −− −−10 P YOEEI LSIIAINO ESSADRLTDTAXA RELATED AND YEASTS OF CLASSIFICATION HYLOGENETIC Spiculogloeales Phyllozyma (subbrunneus clade) v v v v −−− −−vv − v+v10 Cystobasidiomycetes Cystobasidiales Cystobasidium (minuta clade) v v v v v v v v v v + v v −−9,10 Occultifur externus + − ++++−−+++ − + −−n Erythrobasidiales 2) −− − − ErythrobasidiumBannoa + ++v+++v+++ v+++ +vv+ vv v v−− v 10(H 10 (H2) Hasegawazyma (Rhodotorula lactosa) ++++++− ++++ − +++9 Cyrenella elegans ++− +++− ++− + −− ++n Microsporomyces (magnisporus clade) v v v + v + v v v v v v v v v 10 Buckleyzyma (aurantiaca clade) v v − vvv−−+++ − vvv10 157 (continued on next page) W 158

Table 3. (Continued). ANG

Genus or species AL ET . d - α -Inositol -Arabinose -Arabinose Sucrose Raffinose Lactose Trehalose Maltose Melezitose Methyl- -glucoside Soluble Starch l d Glycerol myo dl -glucoside Nitrate Nitrite CoQ

Symmetrospora (marina clade) v v v v v v v v v v + − vvv10 Sakaguchia vv− +vv− vvv+ − v −−10 Naohideales Naohidea sebacea −−−−−−− −−−+ − + −−n Mixiomycetes Mixia osmundae −−−−−−− + − v −−− −−10 Microbotryomycetes Sporidiobolales Rhodotorula (Rhodosporidium clade) + v − +vvv − vv+ − v v v 9,10 Rhodosporidiobolus (mixed Rhodosporidium/Sporidiobolus clade) v v − +vvv vvv+ − v + + 9,10 Sporobolomyces (Sporidiobolus clade) + v − vvvv vvvv − vvv10 Leucosporidiales Leucosporidium vv− vvvv − vv+ − v v v 9,10 Kriegeriales Kriegeriaceae Phenoliferia (glacialis clade) + + −−−+ − n −−−−− + − n Meredithblackwellia eburnea + −−++++ − w++ − + −−n Yamadamyces (Rhodotorula rosulata)+−−w++− w −−w+d ++n − +++n Kriegeria eriophori + −−++++ − +v+ Camptobasidiaceae Glaciozyma antarctica v −−−v −− v −−v −− ++10 Sampaiozyma (vanillica clade) + + + + + + v + − v+ − +++10 Curvibasidium vvvvvv−−+vvvv −−9 Chrysozyma (griseoflavus clade) v −−+++v v− vv −− vv10 Bannozyma (yamatoana clade) + −−+v+− v −−+ −− −−9 Hamamotoa (singularis clade) −−++−−− −vv+ − + −−n Fellozyma (Sporobolomyces inositophilus)+−−+++−−−−++− ++10 Colacogloea vv− +vvv −−vv − vvv10 Udeniozyma (Rhodotorula ferulica)+− +++++ −−++ − v++10 Pseudohyphozyma (buffonii clade) −−−vvv− vv++ − vvv10 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Genera accepted: Sterigmatomyces Fell, Pseudobensingtonia CoQ F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout. n 7

Sterigmatomyces Fell, Antonie van Leeuwenhoek 32: 101.

Nitrite 1966. emend. F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout.

= Agaricostilbum J.E. Wright, Mycologia 62: 679. 1970. Nitrate

−− ++10 ++9 Type species: Sterigmatomyces halophilus Fell.

-glucoside This genus is emended to include species of Agaricostilbum and dl Sterigmatomyces, which occurred as a well supported Agar- + vvvn +++10 +++n +++n

icostilbum clade within Agaricostilbaceae (Figs 1, 4). The name

-Inositol myo Sterigmatomyces was published before Agaricostilbum (Fell − −− −− − − − − 1966, 2011, Wright 1970, Bandoni & Boekhout 2011), so the

merged genus is named Sterigmatomyces. Glycerol + + + + Sexual reproduction observed in some species. Basidia occur

predominantly in synnemata-like basidiomata. Hyphae, basidia

-Arabinose d

v+ v+++ ++9 and basidiospores relatively thick-walled. Basidiospores often

attached to a budding locus (Bandoni & Boekhout 2011). Col-

-Arabinose l onies cream and butyrous. Budding cells present or not, some of vv+ − −− −− them produce one or more stalk-like conidiophores with blasto-

conidia separating at a septum in the mid-region of the stalk on oul Starch Soluble ++++ −− the parent cell. Ballistoconidia not produced. Major CoQ system

Q-9.

-glucoside

- Methyl- d α Species accepted: −− −−−− 1) Sterigmatomyces elviae Sonck & Yarrow, Antonie van

Leeuwenhoek 35: 172. 1969. Melezitose 2) Sterigmatomyces halophilus Fell, Antonie van Leeu-

−− wenhoek 32: 101. 1966. Maltose 3) Sterigmatomyces hyphaenes (Har. & Pat.) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, comb. nov.

MycoBank MB813385. Trehalose Basionym: Pilacre hyphaenes Har. & Pat., Bull. Mus. Hist. ++ +++ +vv +++v v Nat. 17: 370. 1911.

≡ Agaricostilbum hyphaenes (Har. & Pat.) Oberw. & Bandoni. Lactose − v+++v − +++++ + +++++ + 4) Sterigmatomyces pulcherrimus (J.E. Wright) F.Y. Bai,

Q.M. Wang, M. Groenew. & Boekhout, comb. nov. Raffinose MycoBank MB813386. + −− − − − −− Basionym: Isaria pulcherrima Berk. & Broome, J. Linn.

Soc. Bot. 14: 96. 1873. Sucrose ≡ Agaricostilbum pulcherrimum (Berk. & Broome) B.L. Brady, − −−−−−−− −−− −− −−−−−− −−−−−−− + B. Sutton & Samson. = Agaricostilbum palmicola J.E. Wright. 5) Sterigmatomyces novozelandicus (W.B. Kendr. & X.D. Gong) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, comb. nov. MycoBank MB813388. Basionym: Agaricostilbum novozelandicum (as nova- zelandica) W.B. Kendr. & X.D. Gong, Mycotaxon 54: 21. )+

) 1995.

)+ Pseudobensingtonia F.Y. Bai, Q.M. Wang, M. Groenew. &

) Boekhout, gen. nov. MycoBank MB813078. : negative; w: weak; d: delay; n: not tested. − Rhodotorula hordea ( Etymology: The genus is named because of a similar Rhodotorula hylophila (

(yarrowii clade) +morphology + as present in the genus Bensingtonia. Rhodotorula crocea (

(sonckii clade)This genus v is proposed to accommodate the ingoldii clade Rhodotorula javanica (Continued). (

(tsugae clade)containing + two species that previously belonged to the genus a

fi Bensingtonia (Wang et al. 2015a). Member of the Agar- : V: variable; +: positive; icostilbaceae. The genus is mainly circumscribed by the Vonarxula Reniforma strues Spencerozyma Trigonosporomyces Table 3. Genus or species Sloof Oberwinklerozyma Microbotryum Ustilentyloma graminis Yunzhangia Note

www.studiesinmycology.org 159 WANG ET AL.

A

Microbotryomycetes

Cystobasidiomycetes

Mixiomycetes Ustilaginomycotina

Spiculogloeomycetes

1.0

Agaricostilbomycetes

Bensingtonia B B. pseudonaganoensis B.B subrosea B. miscanthii

Mixiomycetes Kondoa

B. naganoensis B. sosorbirbi

clade

clade

subbrunneus clade K. malvinella Spiculogloeales Mixia osmundae B. ciliata S. dimmenae S.S novazealandicus B. changbaiensis

B. phylladus B. thailandica Ustilaginomycotina Ustilago maydisdi B. sakaguchii Rhodotorula phylloplana ingoldii clade B. ingoldii B. musae SS.. clavatuclavatuss ruber clade St. elviae SS.. diospdiospyrorisyroris A.A hyphaenes

S. dracophdracophylliylli AgaricostilbumA clade

S. xanthus S. S. xanthus S. Ch. cuniculicola

S. sasicola S. S. pyrrosiae sasicola S. Ku. nectaireiKurtzmanomyces

Ch. cuniculicola

S. lophatheri lophatheri S. S.

sasicola clade Mycogloea nipponica

lactophilus cladea Chionosphaera Ku.Ku. tardustardus KKu.u. insolitusinsolitus

1.0 clade

Fig. 2. Phylogenetic network of the yeast species within Pucciniomycotina. Single gene ML trees inferred with RAxML were investigated in Splitstree 4.13.1 using the ConsensusNetwork algorithm under default settings. A): the phylogenetic network of the Agaricostilbomycetes, Mixiomycetes, Microbotryomycetes, Cystobasidiomycetes and Spiculogloeomycetes; B): the phylogenetic network of Agaricostilbomycetes, Mixiomycetes and Spiculogloeomycetes; C): the phylogenetic network of Cystobasidiomycetes; D): the phylogenetic network of Microbotryomycetes. Abbreviations: A: Agaricostilbum; B: Bensingtonia; C: Curvibasidium; Ch: Chionosphaera; K: Kondoa; Ku: Kurtzmanomyces; L: Leucosporidium; Le: Leucosporidiella; M: Microbotryum; Ma: Mastigobasidium; R: Rhodotorula; Rh: Rhodosporidium; S: Sporobolomyces; Sa: Sakaguchia; Sp: Sporidiobolus; Sph: Sphacelotheca; Ster: Sterigmatomyces.

160 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

C marina clade R.R. marinamarina

R. calyptogenae (minuta clade)R. slooffiae

R. minuta

Cytstobasidium R. lysiniphila R. laryngis R. benthica S.S oryzicola R. pinicola S. vermiculatus

R. pallida S. foliicola S. coprosmae

S. gracilis S. symmetricus Occultifur externus Naohideales S. kluyveri-nielii Naohidea sebacea S. phyllomatisphyllomatis

R. aurantiaca R.R. aarmeniacarmeniaca aurantiaca clade R. oryzea R. oryzea R. orientis R. ppini Sakaguchia dacryoidea S. magnisporus Sakaguchia dacryoidea magnisporus clade R. sp. JCM8162 S. elongatus R. meli e R. lactosa Erythrobasidium

S. yunnanensis

Cyrenella elegans Erythrobasidium hasegawianum

S. bischofiae bischofiae S. S. Bannoa hahajimensis hahajimensis Bannoa Bannoa R. lamellibrachiae S. syzygii Sakaguchia clade

clade

S. ogasawarensis ogasawarensis S. S.

1.0 Bannoa clade

D Rhodosporidium clade

Rh. kratochvilovaeRh. diobovatum R. araucariaeR. graminis

R. mucilaginosa Curvibasidium clade S. alborubescens C. pallidicorallinuC. cygneicollum R. pacifica

sonckii clade Rh. paludigenum Rh. sphaerocarpum yamatoana clade R. taiwanensis u griseoflavus clade s m Rh. toruloides R. auriculariae clade Rh. toruloides B. yamatoanaR. arctica R. sonckii L. fasciculatum S. carnicolor S. griseoflavus S. ruberrimus clade tsugae S. fushanensis Sporidiobolus us r S. phaffii Heterogastridium pycnidioideum Colacogloea

Reniforma strues R. diffluens

R. pilati pilati R. R.

Sp. salmonicolor S. salmoneus hylophila R. S. falcatus S. marcillae S. koalae R. foliorum marcillae r R. cycloclastica clade s S. roseus R.R. eucalypticaeucalyptica Sp. metaroseus S. jilinensis clade R. javanica Sp. longiusculuslongiusculus R. philyla R.R. retinophilaretinophila is R. ferulica S. inositophilus RR.. terpenoidalisterpenoidalis S. bannaensiss SSp.p. microsporumicrosporuss R. crocea S. beijingensis SS.. nnylandiiylandii Rhodosporidium/Sporidobolus R. lignophila SS.. odoratuodoratuss S. singularis mixed R.R. cocolostrilostri S. poonsookiae R. silvestris singularis clade Rh.Rh. fluvialefluviale R. straminea R. buffonii

R. rosulata yarrowii clade Rh. azoricumm R. hordea R. psychrophenolica R. ingeniosa R. vanillica R. bogoriensis

R. pustula buffonii clade

M. violaceum M. vanillica clade violaceum M.

Ma. intermedium intermedium Ma. Ma. L. fellii L. L. golubevii fellii L. glacialis clade L. scottiii L. fragaria L.L. ffragariaragaria L.L. yyakuticaakutica

L.L. ccreatinivorareatinivora M.M. reticulatumreticulatum L.L. ccreatinovorareatinovora Sph.Sph. hhydropiperisydropiperis M. scabiosae 1.0 M. scabiosae Leucosporidium Microbotryum clade

Fig. 2. (Continued).

www.studiesinmycology.org 161 WANG ET AL.

A B Ballistosporomyces Erythrobasidium

Cystobasidiopsis Bannoa

Kurtzmanomyces

Jianyunia Symmetrospora

Ruinenia

Buckleyzyma

Sterigmatomyces

Sakaguchia

Kondoa

Cystobasidium

Bensingtonia

Microsporomyces Phyllozyma

Naohidea

Fig. 3. Comparison of the colony characteristics in different clades within the Pucciniomycotina. All strains were cultured on slants with potato dextrose agar (PDA) medium for one month at 17 °C. The tree was inferred using maximum likelihood analysis from the combined seven genes (Wang et al. 2015a). A): The colony characteristics in different clades of the classes Agaricostilbomycetes and Spiculogloeomycetes; B): The colony characteristics in different clades of the class Cystobasidiomycetes; C): The colony characteristics in different clades of the order Sporidiobolales of Microbotryomycetes; D): The colony characteristics in different clades of the class Microbotryomycetes, except those belonging to order Sporidiobolales.

162 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

C D Pseudohyphozyma

Slooffia

Oberwinklerozyma

Rhodotorula

Colacogloea

Udeniozyma Bannozyma Chrysozyma Hamamotoa Fellozyma

Rhodosporidiobolus Kriegeriales

Glaciozyma

Leucosporidium

Sampaiozyma

Curvibasidium

Sporobolomyces Microbotryum

Ustilentyloma Yunzhangia

Fig. 3. (Continued).

www.studiesinmycology.org 163 WANG ET AL.

Kurtzmanomyces tardus AF177410 97/99 Kurtzmanomyces insolitus AF177408 99/99 Kurtzmanomyces shapotouensis KC836088 Kurtzmanomyces 98/95 Kurtzmanomyces nectairei AF177409 97/65 Mycogloea nipponica KJ708456 100/100 Kurtzmanomyces sp. JF706573 100/99 Chionosphaera cuniculicola KJ708465 100/72 Chionosphaera apobasidialis AF177407 Kurtzmanomyces sp. EU00854 100/100 96/100 Sporobolomyces taupoensis AF177413 100/100 Sporobolomyces xanthus AF177414 Ballistosporomyces Sporobolomyces sasicola AF177412 Chionosphaera Sporobolomyces sp. AY313055 AB124561 100/100 Sporobolomyces lophatheri AF177411 87/83 Sporobolomyces lactophilus Cystobasidiopsis 99/100 Cystobasidiopsis nirenbergiae FJ536254 Bensingtonia sakaguchi AF363646 Jianyunia Bensingtonia sp. EU678947 62/95 Sporobolomyces sp. DQ404467 87/76 Sporobolomyces clavatus AY364839 Sporobolomyces sp. AY313037 Sporobolomyces sp. AY313041 Sporobolomyces sp. AY313049 sp. AY313043 Ruinenia 100/100 Sporobolomyces Sporobolomyces ruber AF189992 96/88 100/100 Sporobolomyces dracophylli AF189982 Sporobolomyces pyrrosiae AB124562 100/100 Sporobolomyces diospyroris AB124560 Rhodotorula acuta KP216512 100/100 Sterigmatomyces elviae AF177415 AF177406 100/100 Agaricostilbum hyphaenes Sterigmatomyces Agaricostilbum pulcherrimum GU291289 100/100 Sterigmatomyces halophilus AF177416 100/100 Bensingtonia musae AF189892 Bensingtonia ingoldii AF189888 Pseudobensingtonia 99/99 Kondoa malvinella AF189903 93/100 Kondoa aeria AF189901 Bensingtonia subrosea AF189895 Bensingtonia miscanthi AF189891 100/100 Bensingtonia sorbi AY233343 93/ns AF189897 Bensingtonia yuccicola Kondoa 100/100 Bensingtonia changbaiensis AY233339 Bensingtonia phyllada AF189894 Kondoa sp. FN428954 Kondoa “myxariophila” AF189904 EF384207 84/ns Bensingtonia thailandica Bensingtonia bomiensis JN620351 99/96 Bensingtonia naganoensis AF189893 99/100 Bensingtonia pseudonaganoensis DQ224374 Bensingtonia Bensingtonia rectispora JN620355 99/100 Bensingtonia ciliata AF189887 82/94 Sporobolomyces coprosmicola AF189981 Sporobolomyces subbrunneus AF189997 100/100 Sporobolomyces linderae AF189989 100/100 Sporobolomyces productus AB638334 Phyllozyma 98/100 Sporobolomyces corallinus AB638335 100/100 AB644404 96/65 Sporobolomyces dimmenae 100/96 Sporobolomyces novazealandicus KJ708467 Mixia osmundae DQ831009 97/99 Cystobasidiomycetes (100/100) Naohidea sebacea DQ831020 Microbotryomycetes (96/94) (100/100) 100/100 Pucciniomycetes Tritirachiomycetes (100/100) Classiculomycetes (100/100) Platygloea vestita AY512872 Atractiellomycetes (68/100) Rhodotorula phylloplana AF190004 0.2 100/96 Ustilago maydis AY854090

Fig. 4. Phylogenetic relationships of yeasts and related taxa from the Agaricostilbomycetes and Mixiomycetes lineages obtained by Maximum-Likelihood analysis of the LSU (D1/D2 domains) rRNA gene. Tree topology was constrained according to the topology of the seven genes-based tree (Wang et al. 2015a) with nodes showing bootstrap values >85 % inforced to be monophyletic. The type species of each genus is in bold. Taxa not included in the phylogenetic analysis of the seven genes (Wang et al. 2015a) are indicated in red. Note: ns, not supported (BP < 50 %). 164 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

98/95 Kurtzmanomyces (99/99) 97/65 Mycogloea nipponica KJ708456 100/100 Kurtzmanomyces sp. JF706573 100/72 (100/99) 100/100 Chionosphaeria Kurtzmanomyces sp. EU002854 Ballistosporomyces (100/100) Sporobolomyces sp. AY313055 87/83 100/100 Cystobasidiopsis (99/100) 87/66 Bensingtonia sakaguchi AF363646 sp. EU678947 96/88 Bensingtonia Ruinenia (99/100) 99/99 100/100 Sterigmatomyces (100/100) Pseudobensingtonia (100/100) 84/ns Kondoa (100/100) 99/96 Bensingtonia (99/100) Phyllozyma (100/100) 96/65 Mixia osmundae DQ831009 AB082571 100/100 Bannoa hahajimensis Bannoa sp. DQ631898 100/100 Sporobolomyces syzygii AB082573 Bannoa Sporobolomyces ogasawarensis AB082570 100/100 100/100 Sporobolomyces bischofiae AB082572 AB127358 100/100 Sporobolomyces yunnanensis Erythrobasidium hasegawianum AF189899 Erythrobasidium 73/90 Sporobolomyces elongatus AF189983 Rhodotorula lactosa AF189936 Hasegawazyma Cyrenella elegans KJ708454 Sporobolomyces vermiculatus AF460176 100/100 100/100 Sporobolomyces symmetricus AY364836 100/100 Rhodotorula marina AF189944 Sporobolomyces gracilis AF189985 Symmetrospora 71/74 Sporobolomyces coprosmae AF189980 Sporobolomyces oryzicola AF189990 Sporobolomyces foliicola AF189984 100/100 Sporobolomyces kluyveri-nielii AF189988 88/96 Rhodotorula aurantiaca AF189921 Sporobolomyces salicinus AF189995 Buckleyzyma 60/ns 100/100 Rhodotorula armeniaca AF189920 Sporobolomyces phyllomatis AF189991 Rhodotorula orientalis HM559718 100/100 Rhodotorula pini EU075188 100/100 Microsporomyces Sporobolomyces magnisporus AB111954 Rhodotorula bloemforteinensis EU075187 Rhodotorula cladiensis FJ008049 100/100 100/100 Sakaguchia dacryoidea AF189972 AY335161 Rhodotorula oryzicola Sakaguchia Rhodotorula lamellibrachiae AB025999 Rhodotorula meli KJ708452 Rhodotorula sp. JCM 8162 KJ708453 100/100 100/100 Rhodotorula portillonensis JQ769312 Rhodotorula pallida AF189962 Rhodotorula sp. LM644065 100/96 Rhodotorula benthica AB026001 Rhodotorula lysiniphila AB078501 Rhodotorula laryngis AB078500 Cystobasidium ritchiei LM644066 Rhodotorula pinicola AF444293 Cystobasidium 88/89 Rhodotorula oligophaga AB702967 Cystobasidium psychroaquaticum FN868153 97/99 Cystobasidium fimetarium EF450542 Rhodotorula minuta AF189945 Rhodotorula slooffiae AF444722 100/100 Rhodotorula calyptogenae AB025996 98/77 Occultifur kilbournensis KP413160 Occultifur externus AF189910 100/100 Occultifur brasiliensis KM248525 Occultifur Occultifur tropicalis AB921280 Naohidea sebacea DQ831020 Microbotryomycetes (96/94) Pucciniomycetes (100/100) Tritirachiomycetes (100/100) Classiculomycetes (100/100) Platygloea vestita AY512872 Atractiellomycetes (68/100) Ustilago maydis AY854090 0.2 100/96 Rhodotorula phylloplana AF190004

Fig. 5. Phylogenetic relationships of yeasts and related taxa from the Cystobasidiomycetes lineage obtained by Maximum-Likelihood analysis of the LSU (D1/D2 domains) rRNA gene. Tree topology was constrained according to the topology of the seven genes-based tree (Wang et al. 2015a) with nodes showing bootstrap values >85 % inforced to be monophyletic. The type species of each genus is in bold. Taxa not included in the phylogenetic analysis of the seven genes (Wang et al. 2015a) are indicated in red. Note: ns, not supported (BP < 50 %).

www.studiesinmycology.org 165 WANG ET AL.

Agaricostilbomycetes - Mixiomycetes (84/ns) Cystobasidiomycetes (97/99) Microbotryales (93/100) Leucosporidiales (97/69) Sampaiozyma (91/99) Curvibasidium - Pseudoleucosporidium (90/95) Sporidiobolales (85/90) - Rhodotorula sonckii Rhodotorula terpenoidalis AF444729 94/94 Rhodotorula retinophila AF444730 Rhodotorula philyla AF075471 88/98 Colacogloea peniophorae AY629313 Rhodotorula eucalyptica EU075183 Rhodotorula cycloclastica AF444631 86/99 Rhodotorula sp. EU002850 Colacogloea sp. FN428953 68/74 Rhodotorula Rhodotorula sp. FN428968 Rhodotorula diffluens AF075485 Sporobolomyces falcatus AF075490 Rhodotorula foliorum AF317804 Rhodotorula hylophila AF363645 Trigonosporomyces Rhodotorula javanica AF189935 Vonarxula Reniforma strues AF189912 Heterogastridium pycnidioideum GU291290 99/100 Rhodotorula ferulica AF363653 Udeniozyma Rhodotorula cresolica AF189926 Slooffia Rhodotorula sp. DQ531946 98/100 Rhodotorula sp. EF450537 AF189922 99/100 Rhodotorula auriculariae Yunzhangia Rhodotorula buffonii AF189924 Rhodotorula bogoriensis AF189923 Pseudohyphozyma Rhodotorula pustula AF189964 90/89 Rhodotorula sp. AB552933 100/96 Sporobolomyces fushanensis AB176591 Chrysozyma 100/100 Sporobolomyces griseoflavus AF189986 Rhodotorula sp. DSM 101778 (RP-231-13) Bensingtonia yamatoana AF189896 Bannozyma Rhodotorula arctica AB478858 Rhodotorula sp. FN428970 100/100 Sporobolomyces tsugae AF189998 100/100 Rhodotorula pilati AF189963 Rhodotorula sp. AF444728 Slooffia 82/100 Rhodotorula sp. FN428962 Rhodotorula sp. FN428972 sp. FN868158 100/100 Sporobolomyces Fellozyma Sporobolomyces inositophilus AF189987 Sporobolomyces singularis AF189996 Hamamotoa Rhodotorula sp. AM039679 Rhodotorula sp. FN428971 82/99 Rhodotorula svalbardensis JF805370 Rhodotorula glacialis EF151258 Rhodotorula psychrophila EF151252 Phenoliferia Rhodotorula himalayensis AM410635 Rhodotorula psychrophenolica EF151255 Rhodotorula rosulata EU872490 Yamadamyces Kriegeria eriophori AF189905 99/100 Glaciozyma martinii HQ676604 Glaciozyma litorale HF934009 Glaciozyma 68/95 Glaciozyma antarctica AF189906 Glaciozyma watsonii HQ432817 Camptobasidium hydrophilum AY212991 Rhodotorula sp. AY040647 Camptobasidium 92/96 Rhodotorula sp. FJ841888 Rhodotorula silvestris GQ121044 96/94 Rhodotorula straminea EU872489 Oberwinklerozyma Rhodotorula yarrowii AF189971 Rhodotorula sp. FN401525 Meredithblackwellia eburnea JX508798 Rhodotorula crocea AY372179 Spencerozyma Pucciniomycetes (100/100) Tritirachiomycetes (100/100) Classiculomycetes (100/100) Platygloea vestita AY512872 Atractiellomycetes (68/100) 100/96 Rhodotorula phylloplana AF190004 0.2 Ustilago maydis AY854090

Fig. 6. Phylogenetic relationships of yeasts and related taxa from the Microbotryomycetes (‘incertae sedis’ lineages) obtained by Maximum-Likelihood analysis of the LSU (D1/ D2 domains) rRNA gene. Tree topology was constrained according to the topology of the seven genes-based tree (Wang et al. 2015a) with nodes showing bootstrap values >85 % inforced to be monophyletic. The type species of each genus is in bold. Taxa not included in the phylogenetic analysis of the seven genes (Wang et al. 2015a) are indicated in red. Note: ns, not supported (BP < 50 %).

166 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Agaricostilbomycetes - Mixiomycetes (84/ns) Cystobasidiomycetes (97/99) Microbotryum (81/91) 83/87 Sphacelotheca polygoni-persicariae AF189974 63/68 Sphacelotheca koordersiana DQ832219 Liroa emodensis AY212992 Bauerago vuyckii DQ363321 67/73 Fulvisporium restifaciens AF009860 Microbotryales Microbotryozyma collariae JN849460 93/100 Aurantiosporium subnitens AF009846 Ustilentyloma fluitans AF009882 Rhodotorula hordea AF189933 Ustilentyloma 100/100 Ustilentyloma brefeldii EF622016 Leucosporidiella creatinivora AF189925 88/89 Leucosporidium scottii AF070419 L. scottii 98/100 Rhodotorula creatinovora KJ708455 species complex 98/80 Leucosporidiella yakutica AY213001 97/69 Leucosporidiella fragaria AF070428 Leucosporidium golubevii AY212999 Leucosporidium Leucosporidiales Leucosporidium escuderoi JN181009 100/100 Leucosporidiella muscorum AF070433 Leucosporidium fellii AF189907 Mastigobasidium intermedium AF189889 91/99 Rhodotorula ingeniosa AF189934 Rhodotorula vanillica AF189970 Sampaiozyma Rhodotorula sp. AY383751 Rhodotorula futronensis KP216511 Curvibasidium cygneicollum AF189928 AF444736 100/100 Curvibasidium pallidicorallinum Curvibasidium Rhodotorula sp. DQ531939 90/95 100/96 Curvibasidium rogersii JX188232 Leucosporidium fasciculatum AY212993 Pseudoleucosporidium Rhodotorula sp. EU002852 Sporidiobolales (85/90) Rhodotorula sonckii (Yuzangia) AF189969 Colacogloea - Trigonosporomyces - Vonarxula 99/99 Reniforma strues AF189912 Heterogastridium pycnidioideum GU291290 Rhodotorula ferulica AF363653 Slooffia cresolica clade (99/100) Rhodotorula auriculariae (Yuzhangia) AF189922 Pseudohyphozyma (98/100) Chrysozyma (90/89) Bannozyma (100/100) Rhodotorula sp. FN428970 Slooffia (100/100) Rhodotorula sp. FN428972 Fellozyma (82/100) Hamamotoa (100/100) Rhodotorula sp. AM039679 Rhodotorula sp. FN428971 Rhodotorula svalbardensis JF805370 Phenoliferia (ns/ns) Rhodotorula rosulata EU872490 Kriegeria eriophori AF189905 Glaciozyma (99/100) Camptobasidium (86/95) Rhodotorula sp. FJ841888 96/94 Oberwinklerozyma (92/96) Rhodotorula sp. FN401525 Meredithblackwellia eburnea JX508798 Rhodotorula crocea AY372179 Pucciniomycetes (100/100) Tritirachiomycetes (100/100) Classiculomycetes (100/100) Platygloea vestita AY512872 Atractiellomycetes (68/100) AY854090 Ustilago maydis 0.2 100/96 Rhodotorula phylloplana AF190004

Fig. 7. Phylogenetic relationships of yeasts and related taxa from the Microbotryomycetes (Microbotryales, Leucosporidiales and related ‘incertae sedis’ lineages) obtained by Maximum-Likelihood analysis of the LSU (D1/D2 domains) rRNA gene. Tree topology was constrained according to the topology of the seven genes-based tree (Wang et al. 2015a) with nodes showing bootstrap values >85 % inforced to be monophyletic. The type species of each genus is in bold. Taxa not included in the phylogenetic analysis of the seven genes (Wang et al. 2015a) are indicated in red. Note: ns, not supported (BP < 50 %).

www.studiesinmycology.org 167 WANG ET AL.

Agaricostilbomycetes - Mixiomycetes (84/ns) Cystobasidiomycetes (97/99) 84/92 Microbotryales (93/100) Leucosporidiales (97/69) Sampaiozyma (91/99) Curvibasidium - Pseudoleucosporidium (90/95) Rhodotorula sp. EU002852 Rhodotorula graminis AF070431 Rhodotorula araucariae AF070427 Rhodosporidium babjevae AF070420 Rhodotorula glutinis AF070429 Rhodosporidium diobovatum AF070421 Rhodotorula evergladiensis FJ008048 Rhodosporidium kratochvilovae AF071436 Rhodotorula mucilaginosa AF070432 Sporobolomyces alborubescens AF207886 Rhodotorula Rhodotorula dairenensis AY033552 Rhodotorula pacifica AB026006 100/100 Rhodosporidium sphaerocarpum AF070425 Rhodotorula taiwanensis GU646863 Rhodosporidium toruloides AF070426 Rhodotorula sinensis KP216510 AF070424 87/84 Rhodosporidium paludigenum Rhodotorula colostri AY372177 67/ns Rhodosporidium lusitaniae AF070423 AF387125 98/100 Sporobolomyces odoratus Sporobolomyces nylandii AF387123 Rhodosporidiobolus Sporobolomyces poonsookiae AF387124 Rhodosporidium azoricum AF321977 Rhodosporidium fluviale AF189915 Sporidiobolus microsporus AF070436 Sporidiobolus ruineniae AF070434 Sporobolomyces jilinensis AY364838 100/100 Sporobolomyces beijingensis AY364837 85/90 Sporidiobolus metaroseus EU003461 Sporobolomyces roseus AF070441 93/ns Sporidiobolus pararoseus AF189977 Sporobolomyces patagonicus AY158655 AY070017 100/96 Sporobolomyces salmoneus Sporobolomyces marcillae AF070440 81/ns Sporobolomyces phaffii AY070011 Sporobolomyces ruberrimus AF070442 Sporobolomyces 95/79 Sporobolomyces shibatanus AF070437 Sporobolomyces carnicolor AY070008 95/ns Sporobolomyces koalae EU276011 KJ708464 93/75 Sporidiobolus longiusculus Sporobolomyces bannaensis AY274823 100/100 Sporobolomyces blumeae AY213010 AF070439 95/ns Sporidiobolus salmonicolor Sporidiobolus johnsonii AF070435 100/100 Sporobolomyces holsaticus AF189975 Rhodotorula sonckii (Yuzangia) AF189969 Colacogloea - Trigonosporomyces - Vonarxula 99/99 Reniforma strues AF189912 Heterogastridium pycnidioideum GU291290 Rhodotorula ferulica AF363653 Slooffia cresolica clade (99/100) Rhodotorula auriculariae (Yuzhangia) AF189922 Pseudohyphozyma (98/100) Chrysozyma (90/89) Bannozyma (100/100) Rhodotorula sp. FN428970 Slooffia (100/100) Rhodotorula sp. FN428972 Fellozyma (82/100) Hamamotoa (100/100) Rhodotorula sp. AM039679 Rhodotorula sp. FN428971 Rhodotorula svalbardensis JF805370 Phenoliferia (ns/ns) Rhodotorula rosulata EU872490 Kriegeria eriophori AF189905 Glaciozyma (99/100) Camptobasidium (86/95) Rhodotorula sp. FJ841888 96/94 Oberwinklerozyma (92/96) Rhodotorula sp. FN401525 Meredithblackwellia eburnea JX508798 Rhodotorula crocea AY372179 Pucciniomycetes (100/100) Tritrachiomycetes (100/100) Classiculomycetes (100/100) Platygloea vestita AY512872 Atractiellomycetes (68/100) Ustilago maydis AY854090 0.2 100/96 Rhodotorula phylloplana AF190004

Fig. 8. Phylogenetic relationships of yeasts and related taxa from the Microbotryomycetes (Sporidiobolales and selected ‘incertae sedis’ lineages) obtained by Maximum- Likelihood analysis of the LSU (D1/D2 domains) rRNA gene. Tree topology was constrained according to the topology of the seven genes-based tree (Wang et al. 2015a) with nodes showing bootstrap values >85 % inforced to be monophyletic. The type species of each genus is in bold. Taxa not included in the phylogenetic analysis of the seven genes (Wang et al. 2015a) are indicated in red. Note: ns, not supported (BP < 50 %).

168 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA phylogenetic analysis of seven genes, in which it formed a a well-supported clade related to the genus Cystobasidiopsis sister lineage to the genus Sterigmatomyces within Agar- within Chionosphaeraceae (Figs 1, 4). The genus Ballisto- icostilbaceae (Figs 1, 4). This genus is phylogenetically sporomyces was erected by Nakase et al. (1989) and distinct from the Bensingtonia clade that contains the type included Ba. xanthus (= Sporobolomyces xanthus), the type species of Bensingtonia, B. ciliata, that belongs to the family of Ballistosporomyces,andBa. ruber (= Sporobolomyces Kondoaceae (Wang et al. 2015a, Fig. 4 of this study). ruber). This genus was treated as a synonym of Spor- obolomyces (Boekhout 1991). Our analyses showed that Ba. Sexual reproduction not known. Colonies greyish-yellow or dark xanthus (S. xanthus) is located in the sasicola clade, yellow and butyrous. Budding cells present. Pseudohyphae whereas Ba. ruber (S. ruber)occursintheruber clade that is present or not. Ballistoconidia present, ellipsoidal or kidney- phylogenetically distinct from the family Chionosphaeraceae shaped. Major CoQ system Q-9. (Fig. 1). Thus, here we emend and reintroduce Ballistospor- omyces as a genus to include the species of the sasicola Type species: Pseudobensingtonia ingoldii (Nakase & Itoh.) F.Y. clade. Bai, Q.M. Wang, M. Groenew. & Boekhout. Sexual reproduction unknown. Colonies orange to pale Note: The species of Pseudobensingtonia do not form con- yellowish-brown and butyrous. Budding cells present. Hyphae idiogenous stalks, which are present in the anamorphic species and pseudohyphae not formed. Ballistoconidia present, allantoid. of Sterigmatomyces (Nakase et al. 1989, 2011, Takashima et al. Major CoQ system Q-10. 1995). Note: Sporobolomyces ruber (Ba. ruber), which is located in the Species accepted: ruber clade (Fig. 1), is proposed as a new combination in 1) Pseudobensingtonia ingoldii (Nakase & Itoh.) F.Y. Bai, Ruinenia (Fig. 4). Q.M. Wang, M. Groenew. & Boekhout, comb. nov. MycoBank MB813079. Species accepted: Basionym: Bensingtonia ingoldii Nakase & Itoh., J. Gen. 1) Ballistosporomyces sasicola (Nakase & M. Suzuki) F.Y. Appl. Microbiol. 35: 53. 1989. Bai, Q.M. Wang, M. Groenew. & Boekhout, comb. nov. 2) Pseudobensingtonia musae (M. Takash., S.O. Suh & MycoBank MB813081. Nakase) F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, Basionym: Sporobolomyces sasicola Nakase & M. Suzuki, comb. nov. MycoBank MB813080. J. Gen. Appl. Microbiol. 33: 171. 1987. Basionym: Bensingtonia musae M. Takash. et al., J. Gen. 2) Ballistosporomyces taupoensis (Hamam. & Nakase) Appl. Microbiol. 41: 143. 1995. F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout, comb. nov. MycoBank MB813082. Family Chionosphaeraceae Oberw. & Bandoni, Can. J. Bot. 60: Basionym: Sporobolomyces taupoensis Hamam. & 1732. 1982. Nakase, Antonie van Leeuwenhoek 67: 163. 1995. 3) Ballistosporomyces xanthus Nakase et al., J. Gen. Appl. Type genus: Chionosphaera D.E. Cox. Microbiol. 35: 292. 1989.

This family is characterised by teleomorphic members with Chionosphaera D.E. Cox, Mycologia 68: 503. 1976. gasteroid basidia with simultaneous basidiospore production per basidium (Oberwinkler & Bandoni 1982, Bauer et al. 2006). Type species: Chionosphaera apobasidialis D.E. Cox.

Genera accepted: Ballistosporomyces Nakase et al. emend. F.Y. Species accepted: Bai, Q.M. Wang, M. Groenew. & Boekhout, Chionosphaera D.E. 1) Chionosphaera apobasidialis D.E. Cox, Mycologia 68: Cox, Cystobasidiopsis R. Bauer et al. emend. F.Y. Bai, Q.M. 503. 1976. Wang, M. Groenew. & Boekhout, Kurtzmanomyces Y. Yamada 2) Chionosphaera coppinsii P. Roberts, Mycotaxon 63: 195. et al., Stilbum Tode. 1997. 3) Chionosphaera cuniculicola R. Kirschner et al., Mycol. Notes: Mycogloea nipponica was placed in this family based on a Res. 105: 1404. 2001. multi-gene analyses (Wang et al. 2015a) and an analysis of the 4) Chionosphaera erythrinae (Hansf.) R. Kirschner, Fungal enlarged LSU rRNA gene dataset (Fig. 4). The species of the Science Taipei 23: 50. 2008. genus Stilbum are not listed here because living cultures of 5) Chionosphaera lichenicola Alstrup et al., Graphis Scripta Stilbum are not available at present. 5: 97. 1993. 6) Chionosphaera phylaciicola (Seifert & Bandoni) R. Ballistosporomyces Nakase et al., J. Gen. Appl. Microbiol. 35: Kirschner & Oberw., Mycol. Res. 105: 1406. 2001. 291. 1989. emend. F.Y. Bai, Q.M. Wang, M. Groenew. & Boekhout. Note: Living cultures have been obtained only from Ch. apobasidialis and Ch. cuniculicola, which have an asexual Type species: Ballistosporomyces xanthus Nakase et al. yeast stage.

This genus is emended and reintroduced to include species Cystobasidiopsis R. Bauer et al., Mycol. Res. 113: 962. 2009. of the sasicola clade (Wang et al. 2015a), which occurred as emend. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout.

www.studiesinmycology.org 169 WANG ET AL.

Type species: Cystobasidiopsis nirenbergiae R. Bauer et al. Family Kondoaceae R. Bauer et al., Mycol. Progr. 5: 45. 2006.

This genus is emended to include species of Cystobasidiopsis Type genus: Kondoa Y. Yamada et al. and anamorphic species of the lactophilus clade (Wang et al. 2015a), which occurred as a well supported clade related to This family was proposed to accommodate the genus Kondoa the genus Ballistosporomyces within Chionosphaeraceae (Figs that has ballistosporic phragmobasidia, as well as members of 1, 4). the genus Bensingtonia (Bauer et al. 2006). Genera accepted: Bensingtonia Ingold, Kondoa Y. Yamada et al. Sexual reproduction observed in some species. Teleomorphic emend. Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout. taxa produce probasidia with stipitate, transversely septate basidia. Basidiospores sessile. Colonies cream white and Bensingtonia Ingold, Trans. Br. mycol. Soc. 86: 325. 1986. butyrous. Budding cells present or not. Ballistoconidia present or not, ellipsoidal, amygdaliform or falcate. Major CoQ system Q- Type species: Bensingtonia ciliata Ingold 10. Species accepted: Species accepted: 1) Bensingtonia bomiensis F.Y. Bai & Q.M. Wang, Int. J. Syst. 1) Cystobasidiopsis lactophilus (Nakase, M. Itoh, M. Evol. Microbiol. 62: 2043. 2012. Suzuki & Bandoni) Q.M. Wang, F.Y. Bai, M. Groenew. & 2) Bensingtonia ciliata Ingold, Trans. Br. mycol. Soc. 86: 325. Boekhout, comb. nov. MycoBank MB813083. 1986. Basionym: Sporobolomyces lactophilus Nakase et al., 3) Bensingtonia naganoensis (Nakase & M. Suzuki) Nakase Trans. Mycol. Soc. 31: 161. 1990. & Boekhout, J. Gen. Appl. Microbiol. 34: 435. 1988. 2) Cystobasidiopsis lophatheri (Nakase, Tsuzuki, F.L. Lee, 4) Bensingtonia pseudonaganoensis F.Y. Bai & Q.M. Wang, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. Antonie van Leeuwenhoek 89: 262. 2006. & Boekhout, comb. nov. MycoBank MB813084. 5) Bensingtonia rectispora F.Y. Bai & Q.M. Wang, Int. J. Syst. Basionym: Sporobolomyces lophatheri Nakase et al.,J. Evol. Microbiol. 62: 2042. 2012. Gen. Appl. Microbiol. 51: 282. 2005. 3) Cystobasidiopsis nirenbergiae R. Bauer et al., Mycol. Res. Note: B. rectispora and B. bomiensis were not included in our 113: 962. 2009. previous phylogenetic study (Wang et al. 2015a), but the ITS and the D1/D2 domains of LSU rRNA sequences analysis demon- Note: The emended genera Cystobasidiopsis and Ballistospor- strated that they belong to Bensingtonia (Wang et al. 2012, Fig. 4 omyces can be distinguished by colony morphology and some of this study). physiological characteristics (Table 3, Fig. 3A). The species of Cystobasidiopsis form white colonies and assimilate D-arabi- Kondoa Y. Yamada et al., J. Gen. Appl. Microbiol. 35: 383. 1989. nose, glycerol and DL-lactate, whereas the species of Ballisto- emend. Q.M. Wang, M. Groenew., F.Y. Bai & Boekhout. sporomyces form yellow-brown colonies and do not assimilate these three carbon sources. Type species: Kondoa malvinella (Fell & Hunter) Y. Yamada et al.

Kurtzmanomyces Y. Yamada et al., J. Gen. Appl. Microbiol. 34: This genus is emended to include species of the genera Kondoa 505. 1988. and Bensingtonia hitherto classified in the Kondoa clade (Wang et al. 2015a), which occurred as a well supported clade that is Type species: Kurtzmanomyces nectairei (Rodr. Mir.) Y. Yamada phylogenetically distinct from the genus Bensingtonia within et al. Kondoaceae (Figs 1, 4). Thus all Bensingtonia species included in the Kondoa clade will be transferred into the genus Kondoa Species accepted: based on the “One Fungal = One Name” principle (Hawksworth 1) Kurtzmanomyces insolitus J.P. Samp. & Fell, Syst. Appl. 2011, Taylor 2011, McNeill et al. 2012). Microbiol. 22: 62. 1999. 2) Kurtzmanomyces nectairei (Rodr. Mir.) Y. Yamada et al.,J. Sexual reproduction observed in some species. Transversely Gen. Appl. Microbiol. 34: 505. 1988. septate basidia arise directly on the hyphae. Sexual structures 3) Kurtzmanomyces shapotouensis T. Zhang & L.Y. Yu, Int. not known on agar media. Teliospores are not formed. Colonies J. Syst. Evol. Microbiol. 63: 3894. 2013. cream to pinkish-cream and butyrous. Budding cells present. 4) Kurtzmanomyces tardus Gim.-Jurado & van Uden, Anto- Pseudohyphae or true hyphae present or not. Septal pores in nie van Leeuwenhoek 58: 130. 1990. true hyphae ‘simple’ and uniperforate. Major CoQ system Q-9.

Note: Kurtzmanomyces shapotouensis was not included in our Species accepted: previous phylogenetic study (Wang et al. 2015a); the 1) Kondoa aeria A. Fonseca, J.P. Samp. & Fell, Antonie van sequence analysis of the LSU rRNA D1/D2 domains and ITS Leeuwenhoek 77: 295. (including 5.8S rRNA) region indicated that it belongs to the 2) Kondoa changbaiensis (F.Y. Bai & Q.M. Wang) Q.M. genus Kurtzmanomyces (Zhang et al. 2013, Fig. 4 of this Wang, M. Groenew., F.Y. Bai & Boekhout, comb. nov. study). MycoBank MB813085.

170 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Basionym: Bensingtonia changbaiensis F.Y. Bai & Q.M. Genus accepted: Ruinenia Q.M. Wang, F.Y. Bai, M. Groenew. & Wang, Int. J. Syst. Evol. Microbiol. 53: 2086. 2003. Boekhout. 3) Kondoa malvinella (Fell & Hunter) Y. Yamada et al.,J. Gen. Appl. Microbiol. 35: 384. 1989. Ruinenia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. 4) Kondoa miscanthi (Nakase & M. Suzuki) Q.M. Wang, M. nov. MycoBank MB813093. Groenew., F.Y. Bai & Boekhout, comb. nov. MycoBank MB813086. Etymology: The genus is named in honour of J. Ruinen for her Basionym: Sporobolomyces miscanthi Nakase & M. contributions to the biology of yeasts from the phyllosphere. Suzuki, J. Gen. Appl. Microbiol. 33: 183. 1987. ≡ Bensingtonia miscanthi (Nakase & M. Suzuki) Nakase & This genus agrees with the ruber clade (Wang et al. 2015a). Boekhout. 5) Kondoa phyllada (van der Walt & Y. Yamada) Q.M. Member of Ruineniaceae (Agaricostilbales, Agar- Wang, M. Groenew., F.Y. Bai & Boekhout, comb. nov. icostilbomycetes). The genus is mainly circumscribed by the MycoBank MB813087. phylogenetic analysis of seven genes, in which it occurred as a well Basionym: Sporobolomyces phylladus van der Walt & Y. supported clade distinct from the other genera within Agar- Yamada, Antonie van Leeuwenhoek 55: 190. 1989. icostilbales (Figs 1, 4). ≡ Bensingtonia phyllada (van der Walt & Y. Yamada) van der Walt et al. ex Boekhout. Sexual reproduction not known. Colonies orange-red or salmon- ≡ Bensingtonia phylladus (van der Walt & Y. Yamada) van pink, and butyrous. Budding cells present. Hyphae and pseu- der Walt et al., Nom. inval. dohyphae present or not. Ballistoconidia present, ellipsoidal, 6) Kondoa sorbi (F.Y. Bai & Q.M. Wang) Q.M. Wang, M. reniform to falcate. Major CoQ system Q-10. Groenew., F.Y. Bai & Boekhout, comb. nov. MycoBank MB813088. Type species: Ruinenia rubra (Nakase, Oakada & Sugiy.) Q.M. Basionym: Bensingtonia sorbi F.Y. Bai & Q.M. Wang, Int. Wang, F.Y. Bai, M. Groenew. & Boekhout. J. Syst. Evol. Microbiol. 53: 2087. 2003. 7) Kondoa subrosea (Nakase & M. Suzuki) Q.M. Wang, M. Species accepted: Groenew., F.Y. Bai & Boekhout, comb. nov. MycoBank 1) Ruinenia clavata (F.Y. Bai & Q.M. Wang) Q.M. Wang, F.Y. MB813089. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Basionym: Sporobolomyces subroseus Nakase & M. MB813094. Suzuki, J. Gen. Appl. Microbiol. 33: 186. 1987. Basionym: Sporobolomyces clavatus F.Y. Bai & Q.M. ≡ Bensingtonia subrosea (Nakase & M. Suzuki) Nakase & Wang, FEMS Yeast Res. 4: 583. 2004. Boekhout. 2) Ruinenia diospyroris (Nakase, Tsuzuki, F.L. Lee, Jin- 8) Kondoa thailandica (Fungsin, Hamam. & Nakase) Q.M. dam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Wang, M. Groenew., F.Y. Bai & Boekhout, comb. nov. Boekhout, comb. nov. MycoBank MB813095. MycoBank MB813090. Basionym: Sporobolomyces diospyroris (as diospyri) Basionym: Bensingtonia thailandica Fungsin et al., Int. J. Nakase et al., J. Gen. Appl. Microbiol. 51: 280. 2005. Syst. Evol. Microbiol. 51: 1209. 2001. 9) Kondoa yuccicola (Nakase & M. Suzuki) Q.M. Wang, M. 3) Ruinenia dracophylli (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Groenew., F.Y. Bai & Boekhout, comb. nov. MycoBank MB813096. MB813091. Basionym: Sporobolomyces dracophylli (as dracophyllus) Basionym: Sporobolomyces yuccicola Nakase & M. Hamam. & Nkase, Antonie van Leeuwenhoek 67: 168. Suzuki, Antonie van Leeuwenhoek 54: 48. 1988. 1995. ≡ Bensingtonia yuccicola (Nakase & M. Suzuki) Nakase & Boekhout. 4) Ruinenia pyrrosiae (Nakase, Tsuzuki, F.L. Lee, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813097. Note: Two sequences representing the not yet described species Basionym: Sporobolomyces pyrrosiae Nakase et al.,J. Kondoa myxariophila (Scorzetti et al. 2002, Fonseca 2011) were Gen. Appl. Microbiol. 51: 284. 2005. obtained from public databases (Fig. 4). 5) Ruinenia rubra (Nakase, G. Oakada & Sugiy.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Family Ruineniaceae Q.M. Wang, F.Y. Bai, M. Groenew. & MycoBank MB813098. Boekhout, fam. nov. MycoBank MB813092. Basionym: Ballistosporomyces ruber Nakase et al.,J. Gen. Appl. Microbiol. 35: 295. 1989. Member of Agaricostilbales (Agaricostilbomycetes). The diag- ≡ Sporobolomyces ruber (Nakase et al.) Boekhout. nosis of the family Ruineniaceae is based on the description of the genus Ruinenia. The nomenclature of the family is based on the genus Ruinenia. Note: The species of Ruinenia (i.e. ruber clade) form salmon- orange to red colonies, which are a unique feature in the Agaricostilbomycetes (Fig. 3A). Additionally, five sequences Type genus: Ruinenia Q.M. Wang, F.Y. Bai, M. Groenew. & representing potential new species of this genus were obtained Boekhout. from public databases (Fig. 4).

www.studiesinmycology.org 171 WANG ET AL.

Taxa incertae sedis in the Agaricostilbales Spiculogloeaceae Denchev, Mycol. Balcanica 6: 87. 2009.

Jianyunia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. Type genus: Spiculogloea P. Roberts. nov. MycoBank MB813099. The name Spiculogloeaceae was validated by Denchev (2009) Etymology: The genus is named in honour of Jian-Yun Zhuang, to include the taxa of Spiculogloeales (Bauer et al. 2006). former professor at the Institute of Microbiology, Chinese Academy of Sciences, for his contributions to the taxonomic Genera accepted: Spiculogloea P. Roberts, Phyllozyma Q.M. study of Pucciniales in China. Wang, F.Y. Bai, M. Groenew. & Boekhout, Mycogloea L.S. Olive (pro parte). This genus agrees with the Bensingtonia sakaguchii lineage (Wang et al. 2015a). Member of Agaricostilbales (Agar- Note: The species of the genus Spiculogloea and Mycogloea are icostilbomycetes). The genus is mainly circumscribed by the not listed here because cultures of Spiculogloea and Mycogloea, phylogenetic analysis of seven genes, in which it occurred as a except for Mycogloea nipponica that is located in the Chionos- single-species lineage distinct from the other genera within phaeraceae, are presently not available. Moreover, nucleotide Agaricostilbales (Figs 1, 4). sequence data for type species of these genera are not available from public databases. Sexual reproduction not known. Colonies ivory and butyrous. Budding cells present. Pseudohyphae present. Ballistoconidia Phyllozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, present, kidney-shaped. Major CoQ system Q-9. gen. nov. MycoBank MB813102.

Type species: Jianyunia sakaguchii (Sugita, M. Takash., Hamam. Etymology: The genus is named based on the habitat as all & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. species from this clade were isolated from the leaves of plants.

Species accepted: This genus agrees with the subbrunneus clade (Wang et al. 1) Jianyunia sakaguchii (Sugita, M. Takash., Hamam. & 2015a). Member of the Spiculogloeaceae (Spiculogloeales, Spi- Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, culogloeomycetes). The genus is mainly circumscribed by the comb. nov. MycoBank MB813100. phylogenetic analysis of seven genes and the analysis of the Basionym: Bensingtonia sakaguchii Sugita et al., J. Gen. enlarged LSU rRNA gene dataset, in which it occurred as a well Appl. Microbiol. 43: 232. 1997. supported clade (Figs 1, 4). Species in the subbrunneus clade are associated with plant leaves (Hamamoto et al. 2011) and are Class Spiculogloeomycetes Q.M. Wang, F.Y. Bai, M. Groenew. ecologically different from the teleomorphic species Spiculogloea & Boekhout, class. nov. MycoBank MB813101. spp. and Mycogloea spp., which are mycoparasites with tremelloid haustorial cells (Roberts 1996, Bauer 2004, Weiß et al. 2004). Type order: Spiculogloeales R. Bauer et al. Sexual reproduction not known. Colonies pale yellowish- brown, reddish-orange and butyrous. Budding cells present. Hy- Member of Pucciniomycotina. The class is mainly circumscribed pha and pseudohyphae present or not. Ballistoconidia present, by the phylogenetic analysis of seven genes, in which it formed a ellipsoidal, fusiform or sickle-shaped. Major CoQ system Q-10. deep well supported lineage with affinity to Mixiomycetes within Pucciniomycotina (Fig. 1). The diagnosis of the class Spiculo- Type species: Phyllozyma subbrunnea (Nakase & M. Suzuki) gloeomycetes is based on the description of the order Spiculo- Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout gloeales (Bauer et al. 2006). The nomenclature of this class is based on the Spiculogloeales. Species accepted: This class contains species of Spiculogloea and some species 1) Phyllozyma coprosmicola (Hamam. & Nakase) Q.M. of Mycogloea and Sporobolomyces (Aime et al. 2006, 2014, Bauer Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. et al. 2006, Wang et al. 2015a). Phyllozyma gen. nov. is proposed to MycoBank MB813103. accommodate the Sporobolomyces species in the subbrunneus Basionym: Sporobolomyces coprosmicola Hamam. & clade based on the phylogenetic analysis of seven genes (Fig. 1), Nakase, Antonie van Leeuwenhoek 67: 162. 1995. PRBO (Table 1), phylogenetic network analysis (Fig. 2B) and the 2) Phyllozyma corallina (N. Furuya & M. Takash.) Q.M. analysis of the enlarged LSU rRNA gene dataset (Fig. 4). Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813321. Order Spiculogloeales R. Bauer et al., Mycol. Prog. 5: 41. 2006. Basionym: Sporobolomyces corallinus N. Furuya & M. Takash., Mycoscience 53: 261. 2012. Type family: Spiculogloeaceae Denchev. 3) Phyllozyma dimennae (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank This order is characterised by teleomorphic members that may form MB813104. tremelloid haustorial cells (nanometer-fusion mycoparasitism) and Basionym: Sporobolomyces dimennae Hamam. & includes species of the sexual genera Spiculogloea and Myco- Nakase, Antonie van Leeuwenhoek 67: 159. 1995. gloea, as well as asexual species previously classified in the genus 4) Phyllozyma linderae (Nakase, M. Takash. & Hamam.) Sporobolomyces (Bauer et al. 2006). Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813105.

172 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Basionym: Sporobolomyces linderae Nakase et al.,J. Genera accepted: Cystobasidium Lagerh. emend. A.M. Yurkov Gen. Appl. Microbiol. 40: 98. 1994. et al., Occultifur Oberw. 5) Phyllozyma novozealandica (Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Cystobasidium (Lagerh.) emend. A.M. Yurkov et al., Antonie MycoBank MB813106. van Leeuwenhoek 107: 179. 2015. Basionym: Sporobolomyces novazealandicus Hamam. & = Jola subgen. Cystobasidium Lagerh., Bihang till Kungliga svenska Nakase, Antonie van Leeuwenhoek 67: 156. 1995. Vetenskaps-Akademiens Handlingar 24: 15. 1898. 6) Phyllozyma producta (N. Furuya & M. Takash.) Q.M. fi Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Type species: Cystobasidium metarium (Schumach.) P. Roberts MycoBank MB813322. Species accepted: Basionym: Sporobolomyces productus N. Furuya & M. 1) Cystobasidium benthicum (Nagah. et al.) A.M. Yurkov Takash., Mycoscience 53: 261. 2012. et al., Antonie van Leeuwenhoek 107: 180. 2015. 7) Phyllozyma subbrunnea (Nakase & M. Suzuki) Q.M. 2) Cystobasidium calyptogenae (Nagah. et al.)A.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Yurkov et al., Antonie van Leeuwenhoek 107: 181. MycoBank MB813107. 2015. Basionym: Sporobolomyces subbrunneus Nakase & M. 3) Cystobasidium fimetarium (Schumach.) P. Roberts, Suzuki, J. Gen. Appl. Microbiol. 31: 468. 1985. Mycologist 13: 171. 1999. 4) Cystobasidium hypogymniicola Diederich & Ahti, Note: S. productus and S. corallinus were not included in our Biblthca Lichenol. 61: 21. 1996. previous phylogenetic study (Wang et al. 2015a). These two 5) Cystobasidium laryngis (Reiersöl) A.M. Yurkov et al., species were placed in the subbrunneus lineage closely related Antonie van Leeuwenhoek 107: 181. 2015. to S. subbrunneus and S. dimnenae based on the sequence 6) Cystobasidium lysinophilum (Nagah. et al.) A.M. Yurkov analysis of the D1/D2 domains of LSU rRNA (Furuya et al. 2012, et al., Antonie van Leeuwenhoek 107: 181. 2015. Fig. 4 of the present study), and hence, they are recombined in 7) Cystobasidium minuta (Saito) A.M. Yurkov et al., Antonie the genus Phyllozyma. van Leeuwenhoek 107: 180. 2015. 8) Cystobasidium oligophagum (Satoh & Makimura) A.M. Class Cystobasidiomycetes R. Bauer et al., Mycol. Progr. 5: Yurkov et al., Antonie van Leeuwenhoek 107: 181. 46. 2006. 2015. 9) Cystobasidium pallidum (Lodder) A.M. Yurkov et al., Type order: Cystobasidiales R. Bauer et al. Antonie van Leeuwenhoek 107: 181. 2015. 10) Cystobasidium pinicola (F.Y. Bai et al.) A.M. Yurkov et al., Three orders, namely Cystobasidiales, Erythrobasidiales and Antonie van Leeuwenhoek 107: 181. 2015. Naohideales,aswellastheaurantiaca, magnisporus, marina 11) Cystobasidium portillonense (F. Laich, I. Vaca & R. and Sakaguchia clades occur within Cystobasidiomycetes (Wang Chavez) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout et al. 2015a). As the relative positioning of these five groups could comb. nov. MycoBank MB813108. not be resolved with certainty (Fig. 1) we suggest to treat the four Basionym: Rhodotorula portillonensis F. Laich et al., Int. clades as families but not to assign them to any order. Instead, we J. Syst. Evol. Microbiol. 63: 3889. 2013. place them as ‘incertae sedis’ within Cystobasidiomycetes. 12) Cystobasidium proliferans L.S. Olive, Mycologia 44: 564. Buckleyzymaceae fam. nov. with Buckleyzyma gen. nov, 1952. Microsporomycetaceae fam. nov. with Microsporomyces gen. 13) Cystobasidium psychroaquaticum A.M. Yurkov et al., nov., Symmetrosporaceae fam. nov. with Symmetrospora gen. Antonie van Leeuwenhoek 107: 181. 2015. nov., and Sakaguchiaceae fam. nov. are proposed to accom- 14) Cystobasidium ritchiei A.M. Yurkov et al., Antonie van modate the taxa in the aurantiaca, magnisporus, marina and Leeuwenhoek 107: 182. 2015. Sakaguchia clades, respectively (Figs 1, 5). 15) Cystobasidium sebaceum G.W. Martin, Mycologia 31: 507. 1939. Order Cystobasidiales R. Bauer et al., Mycol. Progr. 5: 46. 2006. 16) Cystobasidium slooffiae (E.K. Novak & Vörös-Felkai) A.M. Yurkov et al., Antonie van Leeuwenhoek 107: 180. Type family: Cystobasidiaceae G€aum. 2015. 17) Cystobasidium usneicola Diederich & Alstrup, Biblthca This order was proposed to accommodate the family Cys- Lichenol. 61: 25. 1996. tobasidiaceae that is characterised by nanometer-fusion myco- parasitism with tremelloid haustorial cells and septal pores with Note: R. portillonensis that is phylogenetically located in the cystosomes (Bauer et al. 2006). Cystobasidium clade was recently proposed by Laich et al. (2013). This species was placed in this genus in the analysis Family Cystobasidiaceae G€aum., Vergl. Morph. Pilze (Jena): of the enlarged LSU rRNA gene dataset (Fig. 5) and we transfer 411. 1926. R. portillonensis to the genus Cystobasidium.

Type genus: Cystobasidium Lagerh. emend. A.M. Yurkov et al. Occultifur Oberw., Rep. Tottori Mycol. Inst. 28: 119. 1990.

The family comprises the genera Occultifur and Cystobasidium, Type species: Occultifur internus (L.S. Olive) Oberw. as well as species previously classified in the genus Rhodotorula in Bauer et al. (2006).

www.studiesinmycology.org 173 WANG ET AL.

Species accepted: Sexual reproduction observed in some species. Clamp con- 1) Occultifur brasiliensis Gomes et al., Antonie van Leeu- nections present. Teliospores not formed. Unicellular basidia wenhoek 107: 608. 2015. arise laterally on a clamp connection, or terminally at the hyphae. 2) Occultifur corticiorum P. Roberts, Mycotaxon 63: 202. Cells of the basidia germinate with hyphae, from which yeast 1997. cells originate. Colonies orange to salmon-red. Budding cells 3) Occultifur externus J.P. Samp. et al., Mycologia 91: 1095. present. Pseudohyphae absent. Ballistoconidia present or not, 1999. ovoid and ellipsoidal. Major CoQ system Q-10(H2). 4) Occultifur internus (L.S. Olive) Oberw., Rep. Tottori Mycol. Inst. 28: 120. 1990. Species accepted: 5) Occultifur kilbournensis Kurtzman & Robnett, Antonie Van 1) Bannoa bischofiae (Hamam., Thanh & Nakase) Q.M. Leeuwenhoek 107: 1325. 2015. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. 6) Occultifur tropicalis Khunnamwong et al., Int. J. Syst. Evol. MycoBank MB813109. Microbiol. 65: 1580. 2015. Basionym: Sporobolomyces bischofiae Hamam. et al., Int. J. Syst. Evol. Microbiol. 52: 1029. 2002. Notes: Three species of the genus Occultifur, O. corticiorum, 2) Bannoa hahajimensis Hamam. et al., Int. J. Syst. Evol. O. externus and the generic type O. internus, were accepted by Microbiol. 52: 1028. 2002. Sampaio & Oberwinkler (2011), but only O. externus was included 3) Bannoa syzygii (Hamam., Thanh & Nakase) Q.M. Wang, in our previous phylogenetic study (Wang et al. 2015a) as neither F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank living cultures nor molecular data are available for the other two MB813110. species. Three new asexual members of the genus Occultifur Basionym: Sporobolomyces syzygii Hamam. et al., Int. J. (Fig. 5), namely O. brasiliensis, O. kilbournensis and O. tropicalis, Syst. Evol. Microbiol. 52: 1031. 2002. were recently described by Gomes et al. (2015), Kurtzman & 4) Bannoa ogasawarensis (Hamam., Thanh & Nakase) Robnett (2015) and Khunnamwong et al. (2015), respectively. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813111. Order Erythrobasidiales R. Bauer et al., Mycol. Progr. 5: 46. Basionym: Sporobolomyces ogasawarensis Hamam. 2006. et al., Int. J. Syst. Evol. Microbiol. 52: 1030. 2002.

Type family: Erythrobasidiaceae Denchev. Note: Our analyses suggest that Bannoa sp. MP3490 (AFTOL-ID 1921) represents a potentially new species of this genus (Wang This order accommodates the genera Erythrobasidium and Ban- et al. 2015a, Fig. 5 of this study). noa that have non-tremelloid haustorial cells, septal pores without cystosomes, and coenzyme CoQ10 (H2), as well as some Rho- Erythrobasidium Hamam., Sugiy. & Komag., J. Gen. Appl. dotorula and Sporobolomyces species (Bauer et al. 2006). The Microbiol. 34: 285. 1988. emend. Q.M. Wang, F.Y. Bai, M. genus Cyrenella was not placed in this order by Aime et al. (2006), Groenew. & Boekhout Bauer et al. (2006) and Hibbett et al. (2007). This genus, however, formed a well supported clade with the genera Erythrobasidium and Type species: Erythrobasidium hasegawianum Hamam. et al. Bannoa,andRhodotorula lactosa, which is placed in a new genus Hasegawazyma (Fig. 1). Thus, this order includes the family This genus is emended to include species of Erythrobasidium Erythrobasidiaceae and the genera Cyrenella and Hasegawazyma, and related Sporobolomyces species that hitherto were classified which are treated as ‘incertae sedis’ in the Erythrobasidiales. in the Erythrobasidium clade (Wang et al. 2015a), which occurred as a well supported clade closely related to Bannoa Family Erythrobasidiaceae Denchev, Mycol. Balcanica 6: 87. within Erythrobasidiales (Figs 1, 5). 2009. Sexual reproduction observed in some species. Hyphae Type genus: Erythrobasidium Hamam. et al. form from single cells without mating. Clamp connections pre- sent or absent. Septal pores ‘simple’. Teliospores not formed. The name Erythrobasidiaceae was validated by Denchev (2009) Unicellular basidia (holobasidia) arise by the formation of lateral to include the taxa of Erythrobasidiales (Bauer et al. 2006). protrusions on the hyphae. Sessile basidiospores produced terminally on the holobasidia and not forcibly discharged. Col- Genera accepted: Bannoa Hamam., Erythrobasidium Hamam. onies orange-red. Budding cells present. Pseudohyphae ab- et al. sent. Ballistoconidia present or not, ellipsoidal or ovoid. Major CoQ system Q-10(H2). Bannoa Hamam., Int. J. Syst. Evol. Microbiol. 52: 1027. 2002. emend. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Species accepted: 1) Erythrobasidium elongatum (R.G. Shivas & Rodr. Mir.) Type species: Bannoa hahajimensis Hamam. et al. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813112. This genus is emended to include species of Bannoa and related Basionym: Sporobolomyces elongatus R.G. Shivas & Sporobolomyces species that hitherto were classified in the Rodr. Mir., Antonie van Leeuwenhoek 49: 160. 1983. Bannoa clade (Wang et al. 2015a), which occurred as a well 2) Erythrobasidium hasegawianum Hamam. et al., J. Gen. supported clade related to Erythrobasidium within Eryth- Appl. Microbiol. 37: 131. 1991. robasidiales (Figs 1, 5).

174 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

3) Erythrobasidium yunnanense (F.Y. Bai, M. Takash., Naohidea Oberw., Rep. Tottori Mycol. Inst. 28: 114. 1990. Hamam. & Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813113. Type species: Naohidea sebacea (Berk. & Broome) Oberw. Basionym: Sporobolomyces yunnanensis F.Y. Bai et al., Int. J. Syst. Evol. Microbiol. 51: 234. 2001. The genus Naohidea, representing the order Naohideales,pro- duces cream-coloured cultures that are different from all other Taxa incertae sedis in the Erythrobasidiales taxa in the Cystobasidiomycetes, which form pink to orange-red pigmented colonies (Sampaio & Chen 2011, Fig. 3B of this study). Cyrenella Goch., Mycotaxon 13: 268. 1981. Species accepted: 1) Naohidea sebacea (Berk. & Broome) Oberw., Rep. Tottori Type species: Cyrenella elegans Goch. Mycol. Inst. 28: 114. 1990. Species accepted: 1) Cyrenella elegans Goch., Mycotaxon 13: 268. 1981. Taxa incertae sedis in the Cystobasidiomycetes

Hasegawazyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Family Symmetrosporaceae Q.M. Wang, F.Y. Bai, M. Groenew. gen. nov. MycoBank MB813114. & Boekhout, fam. nov. MycoBank MB813116.

Etymology: The genus is named in honour of T. Hasegawa who Member of the Cystobasidiomycetes. The diagnosis of the family firstly described the species Rhodotorula lactosa. Symmetrosporaceae is based on the description of the genus Symmetrospora. The nomenclature of the family is based on the This genus corresponds to the Rhodotorula lactosa lineage genus Symmetrospora. (Wang et al. 2015a, Fig. 5 of this study). Member of Eryth- robasidiales (Cystobasidiomycetes). The genus is mainly circum- Type genus: Symmetrospora Q.M. Wang, F.Y. Bai, M. Groenew. scribed by the phylogenetic analysis of seven genes and the & Boekhout. analysis of the enlarged LSU rRNA gene dataset, in which it occurred as a single-species lineage distinct from the other genera Genus accepted: Symmetrospora Q.M. Wang, F.Y. Bai, M. within Cystobasidiomycetes (Figs 1, 5). This genus differs from Groenew. & Boekhout. Bannoa, Cyrenella and Erythrobasidium by having ubiquinone Q-9. Symmetrospora Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sexual reproduction not known. Colonies pink-coloured and gen. nov. MycoBank MB813117. butyrous. Budding cells present. Pseudohyphae and true hyphae not observed. Ballistoconidia absent. Major CoQ system Q-9. Etymology: The genus is named by the (almost) symmetrical ballistoconidia that are formed by ballistoconidia-forming species Type species: Hasegawazyma lactosa (Hasegawa) Q.M. Wang, of this clade. F.Y. Bai, M. Groenew. & Boekhout This genus agrees with the marina clade (Wang et al. Species accepted: 2015a). Member of the Symmetrosporaceae (Cys- 1) Hasegawazyma lactosa (Hasegawa) Q.M. Wang, F.Y. tobasidiomycetes). The genus is mainly circumscribed by the Bai, M. Groenew. & Boekhout, comb. nov. MycoBank phylogenetic analysis of seven genes and the analysis of the MB813115. enlarged LSU rRNA gene dataset, in which it occurred as a Basionym: Rhodotorula lactosa Hasegawa, J. Gen. Appl. sister clade to Erythrobasidiales within Cystobasidiomycetes Microbiol. 5: 31. 1959. (Figs 1, 5).

Order Naohideales R. Bauer et al., Mycol. Progr. 5: 46. 2006. Sexual reproduction not known. Colonies orange-red and butyrous. Budding cells present. Hypha and pseudohyphae not Type family: Naohideaceae Denchev observed. Ballistoconidia present or not, symmetrical or nearly symmetrical, ellipsoidal or ovoidal. Major CoQ system Q-10. This order was proposed to accommodate the genus Naohidea, which is characterised by nanometer-fusion mycoparasitism with Type species: Symmetrospora gracilis (Derx) Q.M. Wang, F.Y. intracellular haustoria (tremelloid) and septal pores without Bai, M. Groenew. & Boekhout cystosomes (Bauer et al. 2006). Species accepted: 1) Symmetrospora coprosmae (Hamam. & Nakase) Q.M. Family Naohideaceae Denchev, Mycol. Balcanica 6: 87. 2009. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813118. Type genus: Naohidea Oberw. Basionym: Sporobolomyces coprosmae Hamam. & The name Naohideaceae was validated by Denchev (2009) to Nakase, Antonie van Leeuwenhoek 67: 166. 1995. 2) Symmetrospora foliicola (R.G. Shivas & Rodr. Mir.) include the taxa of Naohideales (Bauer et al. 2006). Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813119. Genus accepted: Naohidea Oberw.

www.studiesinmycology.org 175 WANG ET AL.

Basionym: Sporobolomyces foliicola R.G. Shivas & Rodr. Basionym: Rhodotorula armeniaca R.G. Shivas & Rodr. Mir., Antonie van Leeuwenhoek 49: 162. 1983. Mir., Antonie van Leeuwenhoek 49: 163. 1983. 3) Symmetrospora gracilis (Derx) Q.M. Wang, F.Y. Bai, M. 2) Buckleyzyma aurantiaca (Saito) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Groenew. & Boekhout, comb. nov. MycoBank MB813128. MB813120. Basionym: Torula aurantiaca Saito, Jap. J. Bot. 1: 45. 1922. Basionym: Sporobolomyces gracilis Derx, Annls mycol. ≡ Rhodotorula aurantiaca (Saito) Lodder 28: 18. 1930. 3) Buckleyzyma kluyveri-nielii (van der Walt) Q.M. Wang, 4) Symmetrospora vermiculata (M. Takash. & Nakase) F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. MB813130. nov. MycoBank MB813121. Basionym: Sporobolomyces kluyveri-nielii van der Walt, Basionym: Sporobolomyces vermiculatus M. Takash. & Antonie van Leeuwenhoek 52: 432. 1986. Nakase, Mycoscience 41: 367. 2000. 4) Buckleyzyma phyllomatis (van der Walt & Y. Yamada) 5) Symmetrospora marina (Phaff, Mrak & Williams) Q.M. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. nov. MycoBank MB813131. MycoBank MB813123. Basionym: Sporobolomyces phyllomatis van der Walt & Y. Basionym: Rhodotorula marina Phaff et al., Mycologia 44: Yamada, Antonie van Leeuwenhoek 54: 202. 1988. 436. 1952. 5) Buckleyzyma salicina (B.N. Johri & Bandoni) Q.M. 6) Symmetrospora symmetrica (F.Y. Bai & Q.M. Wang) Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. MycoBank MB813132. nov. MycoBank MB813125. Basionym: Bullera salicina B.N. Johri & Bandoni, Taxon- Basionym: Sporobolomyces symmetricus F.Y. Bai & Q.M. omy of Fungi (Proc. int. Symp. Madras 1973) Part 2 Wang, FEMS Yeast Res. 4: 584. 2004. (Madras) 2: 544. 1984. ≡ Sporobolomyces salicinus (B.N. Johri & Bandoni) Nakase Family Buckleyzymaceae Q.M. Wang, F.Y. Bai, M. Groenew. & & M. Itoh Boekhout, fam. nov. MB813126. Family Microsporomycetaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, fam. nov. MycoBank MB813134. Member of the Cystobasidiomycetes. The diagnosis of the family Buckleyzymaceae is based on the description of the genus Member of Cystobasidiomycetes. The diagnosis of the family Buckleyzyma. The nomenclature of the family is based on the Microsporomycetaceae is based on the description of the genus genus Buckleyzyma. Microsporomyces. The nomenclature of the family is based on the genus Microsporomyces. Type genus: Buckleyzyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Type genus: Microsporomyces Q.M. Wang, F.Y. Bai, M. Groe- new. & Boekhout. Genus accepted: Buckleyzyma Q.M. Wang, F.Y. Bai, M. Groe- new. & Boekhout. Genus accepted: Microsporomyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Buckleyzyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. nov. MycoBank MB813127. Microsporomyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. nov. MycoBank MB813135. Etymology: The genus is named in honour of Helen R. Buckley for her contributions to yeast taxonomy. Etymology: The genus name relates to the type species, Spor- obolomyces magnisporus that produces small (micro-) This genus agrees with the aurantiaca clade (Wang et al. 2015a). ballistoconidia. Member of Buckleyzymaceae (Cystobasidiomycetes). The genus is mainly circumscribed by the phylogenetic analysis of seven This genus agrees with the magnisporus clade (Wang et al. genes and the analysis of the enlarged LSU rRNA gene dataset, 2015a). Member of the Microsporomycetaceae (Cys- in which it occurred as a sister clade to Erythrobasidiales and tobasidiomycetes). The genus is mainly circumscribed by the Symmetrospora within Cystobasidiomycetes (Figs 1, 5). phylogenetic analysis of seven genes and the analysis of the enlarged LSU rRNA gene dataset, in which it occurred as a sister Sexual reproduction not known. Colonies brownish-orange or clade to Cystobasidiales and Sakaguchia within the Cys- orange and butyrous. Budding cells present. Hyphae and tobasidiomycetes (Figs 1, 5). pseudohyphae present or not. Ballistoconidia present or not, ellipsoidal allantoid to amygdaliform. Major CoQ system Q-10. Sexual reproduction not known. Colonies orange or salmon- coloured and butyrous. Budding cells present. Pseudohyphae Type species: Buckleyzyma aurantiaca (Saito) Q.M. Wang, F.Y. present or not. Ballistoconidia present or not, ellipsoidal, allantoid Bai, M. Groenew. & Boekhout to amygdaliform. Major CoQ system Q-10. Species accepted: Type species: Microsporomyces magnisporus (Nakase, Tsuzuki, 1) Buckleyzyma armeniaca (R.G. Shivas & Rodr. Mir.) Q.M. F.L. Lee, Sugita, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Groenew. & Boekhout. MycoBank MB813133.

176 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Species accepted: Basionym: Rhodotorula cladiensis Fell et al., Antonie van 1) Microsporomyces bloemfonteinensis (Pohl, M.S. Smit Leeuwenhoek 99: 546. 2011. & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekh- 2) Sakaguchia dacryoidea (Fell et al.) Y. Yamada et al., out, comb. nov. MycoBank MB814789. Biosc. Biotechn. Biochem. 58: 102. 1994. Basionym: Rhodotorula bloemfonteinensis Pohl et al., Int. 3) Sakaguchia lamellibrachiae (Nagah., Hamam., Nakase J. Syst. Evol. Microbiol. 61: 2324. 2011. & Horikoshi) Q.M. Wang, F.Y. Bai, M. Groenew. & 2) Microsporomyces magnisporus (Nakase, Tsuzuki, F.L. Boekhout, comb. nov. MycoBank MB813147. Lee, Sugita, Jindam. & M. Takash.) Q.M. Wang, F.Y. Bai, Basionym: Rhodotorula lamellibrachiae (as lamellibrachii) M. Groenew. & Boekhout, comb. nov. MycoBank Nagah. et al., Antonie van Leeuwenhoek 80: 320. 2001. MB813137. 4) Sakaguchia meli (Libkind, van Broock & J.P. Samp.) Basionym: Sporobolomyces magnisporus Nakase et al.,J. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. Gen. Appl. Microbiol. 49: 341. 2003. nov. MycoBank MB813148. 3) Microsporomyces pini (Pohl, M.S. Smit & Albertyn) Q.M. Basionym: Rhodotorula meli Libkind et al., Int. J. Syst. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Evol. Microbiol. 60: 2253. 2010. MycoBank MB813138. 5) Sakaguchia oryzae (F.Y. Bai & Y.M. Cai) Q.M. Wang, F.Y. Basionym: Rhodotorula pini Pohl et al., Int. J. Syst. Evol. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Microbiol. 61: 2323. 2011. MB813150. 4) Microsporomyces orientalis (Pohl, M.S. Smit & Alber- Basionym: Rhodotorula oryzae F.Y. Bai & Y.M. Cai, tyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Antonie van Leeuwenhoek 86: 296. 2004. comb. nov. MycoBank MB813327. Basionym: Rhodotorula orientalis (as orientis) Pohl et al., Note: Our analyses suggest that Rhodotorula sp. JCM 8162 Int. J. Syst. Evol. Microbiol. 61: 2325. 2011. represents a potential new species of this genus, as revealed by the multi-gene analyses (Wang et al. 2015a) and the analysis of Family Sakaguchiaceae Q.M. Wang, F.Y. Bai, M. Groenew. & the enlarged LSU rRNA gene dataset (Fig. 5). Boekhout, fam. nov. MycoBank MB813142. Class Microbotryomycetes R. Bauer et al., Mycol. Progr. 5: 47. Member of the Cystobasidiomycetes. The diagnosis of the family 2006. Sakaguchiaceae is based on the description of the genus Sakaguchia. The nomenclature of the family is based on the Type order: Microbotryales R. Bauer & Oberw. genus Sakaguchia. This class presently contains four orders that contain yeast Type genus: Sakaguchia Y. Yamada et al. species, namely Kriegeriales, Leucosporidiales, Microbotryales and Sporidiobolales (Aime et al. 2006, 2014, Bauer et al. 2006, Genus accepted: Sakaguchia Y. Yamada et al. emend. Q.M. Hibbett et al. 2007, Toome et al. 2013). Ten clades and seven Wang, F.Y. Bai, M. Groenew. & Boekhout. single-species lineages do not belong to the above listed orders (Wang et al. 2015a), and they may be assigned into eleven Sakaguchia Y. Yamada et al., Biosc. Biotechn. Biochem. 58: families based on modified GMYC analysis (Table 2)in 102. 1994. emend. Q.M. Wang, F.Y. Bai, M. Groenew. & conjunction with the phylogenetic analysis of seven genes (Fig. 1). Boekhout. However, most of these suggested families are monotypic or poorly sampled (Table 2). Thus, we propose Chrysozymaceae Type species: Sakaguchia dacryoidea (Fell et al.) Y. Yamada fam. nov. to accommodate the griseoflavus, yamatoana, sin- et al. gularis and Sporobolomyces inositophilus clades, and Cola- cogloeaceae fam. nov. to cover the Colacogloea clade because This genus is emended to include Sakaguchia dacryoidea these two proposed families have more taxa than the other clades and related Rhodotorula species that hitherto were classified and have strong support values (Fig. 1). The other six clades and in the Sakaguchia clade (Wang et al. 2015a), which occurred six single-species lineages are proposed to be included in twelve as a well supported clade within the Cystobasidiomycetes genera that at the higher rank are considered as ‘incertae sedis’ (Figs 1, 5). within the Microbotryomycetes at present. The species Rhodo- torula svalbardensis (Singh et al. 2014) was not included in the Sexual reproduction in some species. Clamp connections seven genes-based phylogenetic analysis (Wang et al. 2015a) present. Teliospores laterally or terminally on the hyphae. Te- and has no proper placement in the constrained LSU analysis liospores germinate with two- to four-celled metabasidium with (Fig. 6). The phylogenetic placement of this species needs to be lateral and terminal basidiospores. Colonies red or orange-red addressed by a robust molecular analysis. Thus, we leave it as and butyrous. Budding cells present. Pseudohyphae or true Rhodotorula svalbardensis pro tem.inthisstudy.Theterm“pro hyphae present or not. Ballistoconidia not produced. Major CoQ tem.” (pro tempore) was proposed in Wang et al. (2015b) and system Q-10. indicates a temporary taxonomic placement.

Species accepted: Order Kriegeriales Toome & Aime, Mycologia 105: 489. 2013. 1) Sakaguchia cladiensis (Fell, Statzell & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Type family: Kriegeriaceae Toome & Aime. MycoBank MB813144.

www.studiesinmycology.org 177 WANG ET AL.

This order was proposed to contain the families Kriegeriaceae Type species: Phenoliferia psychrophenolica (Margesin & J.P. and Camptobasidiaceae (Toome et al. 2013). The teleomorphic Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout members of this order are characterised by the presence of ‘simple’ septal pores and subgloboid spindle pole bodies (Toome Species accepted: et al. 2013). 1) Phenoliferia psychrophenolica (Margesin & J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. Family Kriegeriaceae Toome & Aime, Mycologia 105: 489. 2013. nov. MycoBank MB813153. Basionym: Rhodotorula psychrophenolica Margesin & J.P. Type genus: Kriegeria Bres. Samp., Int. J. Syst. Evol. Microbiol. 57: 2183. 2007. 2) Phenoliferia psychrophila (Margesin & J.P. Samp.) Q.M. This family was proposed to accommodate the sexual plant Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. parasite Kriegeria, the asexual genus Meredithblackwellia, and MycoBank MB813154. six related Rhodotorula species (Toome et al. 2013). The species Basionym: Rhodotorula psychrophila Margesin & J.P. R. pilati was placed in the Kriegeriaceae by Toome et al. (2013), Samp., Int. J. Syst. Evol. Microbiol. 57: 2181. 2007. fi but this af liation was not supported in the muligene study by 3) Phenoliferia glacialis (Margesin & J.P. Samp.) Q.M. Wang et al. (2015a). This species was located in the tsugae Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. fi clade (Wang et al. 2015a). The other ve Rhodotorula species in MycoBank MB813155. fi the Kriegeriaceae are reclassi ed into two new genera Pheno- Basionym: Rhodotorula glacialis Margesin & J.P. Samp., liferia and Yamadamyces. Int. J. Syst. Evol. Microbiol. 57: 2183. 2007. 4) Phenoliferia himalayensis (Shivaji, Bhadra & Rao) Q.M. Genera accepted: Kriegeria Bres., Meredithblackwellia Toome & Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Aime, Phenoliferia Q.M. Wang, F.Y. Bai, M. Groenew. & MycoBank MB813156. Boekhout, Yamadamyces Q.M. Wang, F.Y. Bai, M. Groenew. & Basionym: Rhodotorula himalayensis Shivaji et al., Boekhout Extremophiles 12: 380. 2008.

Kriegeria Bres., Revue mycol. Toulouse 13: 14. 1891. Notes: Species of Phenoliferia (i.e. the glacialis clade) have = Zymoxenogloea D.J. McLaughlin & Doubles, Mycologia 84: 671. similar assimilation patterns of carbon and nitrogen compounds 1992. (Margesin et al. 2007). They share the ability to grow on raffinose as the sole carbon source but not on maltose. In contrast, closely Type species: Kriegeria eriophori Bres. related taxa, such as Kriegeria eriophori and Rhodotorula rosu- lata, have different assimilation properties and are able to utilise Species accepted: maltose, but not raffinose (Table 3). R. himalayensis was not 1) Kriegeria eriophori Bres., Revue mycol. Toulouse 13: 14. included in our previous phylogenetic study (Wang et al. 2015a). 1891. This species was found to be closely related to R. psychrophila and R. glacialis based on the sequence analyses of LSU rRNA Meredithblackwellia Toome & Aime, Mycologia 105: 490. 2013. D1/D2 domains and ITS (Shivaji et al. 2008, Turchetti et al. 2011, Toome et al. 2013, Singh et al. 2014, Fig. 6 of this study), and, Type species: Meredithblackwellia eburnea Toome & Aime. hence, it is recombined in the genus Phenoliferia. Species accepted: Yamadamyces Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, 1) Meredithblackwellia eburnea Toome & Aime, Mycologia gen. nov. MycoBank MB813326. 105: 491. 2013. Etymology: The genus is named in honour of Y. Yamada Phenoliferia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, because of his contributions to the taxonomy of yeasts. gen. nov. MycoBank MB813152. This genus corresponds to the Rhodotorula rosulata lineage Etymology: The genus is named because the species in this (Wang et al. 2015a). Member of the Kriegeriaceae (Kriegeriales, clade can assimilate phenol. Microbotryomycetes). The genus is mainly circumscribed by the phylogenetic analysis of seven genes and the analysis of the This genus agrees with the glacialis clade (Wang et al. 2015a). enlarged LSU rRNA gene dataset, in which it occurred as a Member of the Kriegeriaceae (Kriegeriales, Micro- single-species lineage within the Kriegeriaceae (Figs 1, 6). botryomycetes). The genus is mainly circumscribed by the phylogenetic analysis of seven genes and the analysis of the Sexual reproduction not known. Colonies greyish-cream and enlarged LSU rRNA gene dataset, in which it occurred as a well butyrous. Budding cells present. Pseudomycelium present. supported clade related to the genus Kriegeria within Krieger- Ballistoconidia not produced. Major CoQ system unknown. iaceae (Figs 1, 6). Type species: Yamadamyces rosulatus (Golubev & Scorzetti) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Sexual reproduction not known. Colonies creamy-white and butyrous. Budding cells present. Pseudomycelium or true hy- Species accepted: phae not observed. Ballistoconidia not produced. Major CoQ 1) Yamadamyces rosulatus (Golubev & Scorzetti) Q.M. system unknown. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813578.

178 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Basionym: Rhodotorula rosulata Golubev & Scorzetti, Int. Note: Only one species of the genus Glaciozyma, namely J. Syst. Evol. Microbiol. 60: 2503. 2010. G. antarctica, was employed in our previous study (Wang et al. 2015a) because G. litoralis, G. martini and G. watsonii were only Notes: The species R. rosulata was found to differ from recently published (Turchetti et al. 2011, Kachalkin 2014). These K. eriophori in the utilisation of three carbon sources, namely species were included in the analysis of the enlarged LSU rRNA methyl-α-D-glucoside, L-arabinose and myo-inositol (Table 3). The gene dataset (Fig. 6), and the genus Glaciozyma received high micromorphology of the species resembles that of Me. eburnea support in ML and MP analyses. and K. eriophori with budding cells remaining connected to each other at the base and forming clusters (or rosettes) of cells. Order Leucosporidiales J.P. Samp. et al., Mycol. Prog. 2: 61. 2003.

Family Camptobasidiaceae R.T. Moore, Mycotaxon 59: 8. Type family: Leucosporidiaceae J.P. Samp. et al. 1996.

This order was proposed to accommodate the asexual or sexual, Type genus: Camptobasidium Marvanova & Suberkr. non-phytoparasitic members of the Microbotryomycetidae with white to cream-coloured colonies (Sampaio et al. 2003). The The family Camptobasidiaceae was described to accommodate order includes Mastigobasidium and Leucosporidium fellii, and a teleomorphic aquatic fungus Camptobasidium (Marvanova& the family Leucosporidiaceae in Sampaio et al. (2003). Members Suberkropp 1990) that was placed in the Atractiellales (Atrac- of this order have colacosomes (lenticular bodies) and represent tiellomycetes)byMoore (1996). Aime et al. (2006) indicated that potential mycoparasites (Sampaio et al. 2003). Camptobasidium belongs to Microbotryomycetes rather than Atractiellomycetes based on rRNA sequence analysis. Family Leucosporidiaceae J.P. Samp. et al., Mycol. Prog. 2: 63. 2003. Genera accepted: Camptobasidium Marvanova & Suberkr., Glaciozyma Turchetti et al. Type genus: Leucosporidium Fell et al. emend. V. de Garcia et al.

Note: Our previous study (Wang et al. 2015a) did not support the This family was proposed to accommodate the genera Leuco- family Camptobasidiaceae as belonging to the Kriegeriales, and, sporidiella and Leucosporidium excluding the species L. fellii and therefore, we consider the family as ‘incertae sedis’ in L. fasciculatum, and Mastigobasidium (Sampaio et al. 2003). The Microbotryomycetes. genera Mastigobasidium and Leucosporidiella were recently proposed as a synonym of Leucosporidium (de García et al. Camptobasidium Marvanova & Suberkr., Mycologia 82: 209. 2015). Thus, the family Leucosporidiaceae presently includes 1990. only the genus Leucosporidium (Fig. 7). = Crucella Marvanova & Suberkr., Mycologia 82: 212. 1990. Genus accepted: Leucosporidium Fell et al. emend. V. de Garcia Type species: Camptobasidium hydrophilum Marvanova& et al. Suberkr. Leucosporidium Fell et al., Antonie van Leeuwenhoek 35: 438. Species accepted: 1969. emend. V. de Garcia et al., FEMS Yeast Res. 15: 9. 2015. 1) Camptobasidium hydrophilum Marvanova & Suberkr., = Mastigobasidium Golubev, Int. J. Syst. Bacter. 49: 49. 1999 Mycologia 82: 209. 1990. = Leucosporidiella Sampaio, Mycol. Progr. 2: 63. 2003

Notes: Camptobasidium hydrophilum is a slow-growing psychro- Type species: Leucosporidium scottii Fell et al. philic fungus without a yeast stage but with a tetraradiate ana- morph, Crucella subtilis. In co-culturing experiments with aquatic Species accepted: hyphomycetes Camptobasidium hydrophilum behaves like a 1) Leucosporidium creatinivorum (Golubev) V. de Garcia contact biotrophic mycoparasite and its hyphae coil around host et al., FEMS Yeast Res. 15: 9. 2015. hyphae or conidia. The penetration of the host by hyphae has, 2) Leucosporidium drummii A.M. Yurkov et al., Int. J. Syst. however, not been reported (Marvanova & Suberkropp 1990). Evol. Microbiol. 62: 730. 2012. 3) Leucosporidium escuderoi Vaca et al., Antonie van Glaciozyma Turchetti et al., Extremophiles 15: 579. 2011. Leeuwenhoek 105: 599. 2013. 4) Leucosporidium fellii Gim.-Jurado & Uden, Antonie van Type species: Glaciozyma antarctica (Fell et al.) Turchetti et al. Leeuwenhoek 55: 134. 1989. 5) Leucosporidium golubevii Gadanho et al., Mycol. Progr. Species accepted: 2: 57. 2003. 1) Glaciozyma antarctica (Fell et al.) Turchetti et al., 6) Leucosporidium scottii Fell et al., Antonie van Leeu- Extremophiles 15: 579. 2011. wenhoek 35: 440. 1969. 2) Glaciozyma litoralis A.V. Kachalkin, Antonie van Leeu- 7) Leucosporidium yakuticum (Golubev) V. de Garcia et al., wenhoek 105: 1080. 2014. FEMS Yeast Res. 15: 9. 2015. 3) Glaciozyma martinii Turchetti et al., Extremophiles 15: 8) Leucosporidium muscorum (Di Menna) V. de Garcia 579. 2011. et al., FEMS Yeast Res. 15: 9. 2015. 4) Glaciozyma watsonii Turchetti et al., Extremophiles 15: 9) Leucosporidium intermedium (Golubev) V. de Garcia 582. 2011. et al., FEMS Yeast Res. 15: 9. 2015.

www.studiesinmycology.org 179 WANG ET AL.

10) Leucosporidium fragarium (J.A. Barnett & Buhagiar) V. 2) Ustilentyloma brefeldii (Krieg.) Vanky, Mycotaxon 41: 491. de Garcia et al., FEMS Yeast Res. 15: 9. 2015. 1991. Basionym: Entyloma brefeldii Krieg., Hedwigia 35(Beibl.): Order Microbotryales R. Bauer & Oberw., Can. J. Bot. 75: 145. 1896. 1309. 1997. 3) Ustilentyloma fluitans (Liro) Vanky, Microbiologia Bucur- esti 1: 328. 1970. Type family: Microbotryaceae R.T. Moore. 4) Ustilentyloma oreochloae (Durrieu) Vanky, Mycotaxon 78: 319. 2001. This order was proposed to accommodate phytoparasitic taxa 5) Ustilentyloma graminis (Rodr. Mir. & H.G. Diem) Q.M. lacking colacosomes (lenticular bodies) and teliospores (Bauer Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. et al. 1997, Bauer et al. 2006). The order includes the families MycoBank MB813157. Microbotryaceae and Ustilentylomataceae. No yeast species are Basionym: Candida graminis Rodr. Mir. & H.G. Diem, Can. included in the family Microbotryaceae, but yeast stages of taxa J. Bot. 52: 279. 1974. in this family occur (Fig. 3D). = Rhodotorula hordea Rodr. Mir. & Weijman.

Family Ustilentylomataceae R. Bauer & Oberw., Can. J. Bot. Notes: The close relatives of R. hordea are plant parasite species 75: 1311. 1997. of Ustilentyloma based on the sequence analysis of the D1/D2 domains of the LSU rRNA (Sampaio 2011, Fig. 7 of this study) and Type genus: Ustilentyloma Savile. the ITS (including 5.8S rRNA) region. Nucleotide sequences of R. hordea differ from Ustilentyloma fluitans (GenBank number: This family was proposed to include taxa with ‘simple’ septal AF009882 and KC994459) and Ustilentyloma brefeldii (GenBank pores in the Microbotryales (Bauer et al. 1997). number: EF622016) by 1 and 15 positions in the D1/D2 domains of the LSU rRNA, respectively. However, R. hordea differs from Genera accepted: Aurantiosporium M. Piepenbr. et al., Fulvis- U. fluitans by 78 mismatches and gaps (12 %) in the ITS region porium Vanky, Ustilentyloma Savile, Microbotryozyma S.O. Suh (GenBank number: AY212990 and KC994460), and by the et al. assimilation of D-galactose, L-sorbose, D-ribose, lactose, erythritol, ribitol and protocatechuic acid (Sampaio 2011). The genus Usti- Note: The species of the genera Aurantiosporium and Fulvispo- lentyloma established by Savile & Parmelee (1964) contains rium are not listed here because no yeast phase has been U. brefeldii, U. fluitans, U. oreochloae and U. pleuropogonis.All observed in these two genera. Representatives of these genera species of this genus are parasites infecting leaves of Poaceae. were included in the analysis of the enlarged LSU rRNA gene R. hordea isolated from the leaves of six-row barley (Hordeum dataset (Fig. 7). vulgare subsp. hexastichium, Poaceae) may have a similar ecology as a phyllosphere inhabitant as the species of Ustilenty- Microbotryozyma S.O. Suh et al., Antonie van Leeuwenhoek loma, although it is not known to be a parasite on barley. One 102: 102. 2012. possibility may be that R. hordea represents a yeast stage of a dimorphic phytoparasite that is distinct from U. fluitans. Sequences Type species: Microbotryozyma collariae S.O. Suh et al. of U. pleuropogonis, the type species of Ustilentyloma, are not available at present, but the above mentioned sequence analysis Species accepted: of U. brefeldii and U. fluitans indicated that this genus may be 1) Microbotryozyma collariae S.O. Suh et al., Antonie van monophyletic (Fig. 7). The morphological characters of this genus Leeuwenhoek 102: 103. 2012. also support its monophyletic nature (Vanky 2002). Based on the above discussion we prefer to propose R. hordea as a new Note: Mi. collariae is a yeast species within Ustilentylomataceae, combination of Ustilentyloma. The name Rhodotorula hordea was which was recently described to accommodate two strains iso- chosen to replace Candida graminis when it was transferred to lated from the intestine of a plant bug (Collaria oleosa, Miridae, Rhodotorula by Weijman et al. (1998) because the specific epithet Heteroptera, Insecta)bySuh et al. (2012). This anamorphic ‘graminis’ was already used for the species Rhodotorula graminis. species is distantly related to any teleomorphic parasitic taxa in Here we reuse this epithet for Ustilentyloma graminis. this family (Fig. 7). Order Sporidiobolales J.P. Samp. et al., Mycol. Progr. 2: 66. Ustilentyloma Savile, Can. J. Bot. 42: 708. 1964. emend. Q.M. 2003. Wang, F.Y. Bai, M. Groenew. & Boekhout. Type family: Sporidiobolaceae (R.T. Moore) J.P. Samp. et al. Type species: Ustilentyloma pleuropogonis Savile. This order was proposed to include the family Sporidiobolaceae (Sampaio et al. 2003). This genus was originally described for teleomorphic fungi occurring on Poaceae (Savile & Parmelee 1964, Vanky 2002). Family Sporidiobolaceae R.T. Moore, Bot. Mar. 23: 361. 1980. Here it is emended to include free-living yeast species with un- emend. J.P. Samp. et al., Mycol. Progr. 2: 66. 2003. known sexual states. Type genus: Sporidiobolus Nyland. Species accepted: 1) Ustilentyloma pleuropogonis Savile, Can. J. Bot. 42: 708. This family was emended to include Sporidiobolus and Rhodo- 1964. sporidium that have colacosomes (lenticular bodies), ‘simple’

180 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA septal pores and teliospores, and some species that are hitherto 9) Rhodotorula kratochvilovae (Hamam., Sugiy. & classified in Sporobolomyces and Rhodotorula (Sampaio et al. Komag.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, 2003). All known species in this family have pink-coloured cul- comb. nov. MycoBank MB813353. tures (Sampaio et al. 2003, Fig. 3C of this study). Basionym: Rhodosporidium kratochvilovae Hamam. et al., J. Gen. Appl. Microbiol. 34: 122. 1988. Genera accepted: Rhodotorula F.C. Harrison emend. Q.M. Wang, 10) Rhodotorula mucilaginosa (A. Jörg.) F.C. Harrison, Proc. F.Y. Bai, M. Groenew. & Boekhout, Rhodosporidiobolus Q.M. & Trans. Roy. Soc. Canada ser. 3 21: 349. 1928. Wang, F.Y.Bai, M. Groenew. & Boekhout, Sporobolomyces Kluyver 11) Rhodotorula pacifica Nagah. & Hamam., Int. J. Syst. & C.B. Niel emend. Q.M. Wang, F.Y.Bai, M. Groenew. & Boekhout. Evol. Microbiol. 56: 297. 2006. 12) Rhodotorula paludigena (Fell & Tallman) Q.M. Wang, Rhodotorula F.C. Harrison, Proc. & Trans. Roy. Soc. Canada F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Myco- ser. 3 21: 349. 1927. emend. Q.M. Wang, F.Y. Bai, M. Groenew. Bank MB813354. & Boekhout. Basionym: Rhodosporidium paludigenum Fell & Tallman, = Rhodosporidium I. Banno, J. Gen. Appl. Microbiol. 13: 192. 1967. Int. J. Syst. Bacteriol. 30: 658. 1980. 13) Rhodotorula sphaerocarpa (S.Y. Newell & Fell) Q.M. Type species: Rhodotorula glutinis (Fresen.) F.C. Harrison. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813356. This genus is emended to include Rhodotorula species and Basionym: Rhodosporidium sphaerocarpum S.Y. Newell their sexual counterpart Rhodosporidium in the Rhodospori- & Fell, Mycologia 62: 276. 1970. dium clade (Wang et al. 2015a), which is a well supported 14) Rhodotorula taiwanensis F.L. Lee & C.H. Huang, Antonie clade within Sporidiobolaceae (Sporidiobolales). The Rhodo- van Leeuwenhoek 99: 300. 2011. sporidium clade is composed of Rhodotorula glutinis,thetype 15) Rhodotorula toruloides (I. Banno) Q.M. Wang, F.Y. Bai, species of Rhodotorula,andRhodosporidium toruloides,the M. Groenew. & Boekhout, comb. nov. MycoBank type species of Rhodosporidium (Figs 1, 8). The name Rho- MB813358. dotorula is older than Rhodosporidium, and has taxonomic Basionym: Rhodosporidium toruloides I. Banno, J. Gen. priority over the latter. Appl. Microbiol. 13: 193. 1967.

Sexual reproduction observed in some species. Clamp con- Rhodosporidiobolus Q.M. Wang, F.Y. Bai, M. Groenew. & nections present. Teliospores may be formed and produce Boekhout, gen. nov. MycoBank MB813359. transversely septate basidia. The basidiospores ovoid, passively released and germinate by budding. Colonies red and butyrous. Etymology: The genus name refers to the fact that the species Budding cells present. Pseudohyphae or true hyphae present or were hitherto classified in the genera Rhodosporidium or not. Ballistoconidia formed or not, ellipsoidal. Major CoQ systems Sporidiobolus. Q-9 or Q-10. This genus agrees with the mixed Rhodosporidium/Spor- Species accepted: idiobolus clade (Wang et al. 2015a) and includes asexual states 1) Rhodotorula alborubescens (Derx) Q.M. Wang, F.Y. classified in the genera Rhodotorula and Sporobolomyces, and Bai, M. Groenew. & Boekhout, comb. nov. MycoBank their sexual counterparts Rhodosporidium and Sporidiobolus MB813323. (Fig. 8). Member of the Sporidiobolaceae (Sporidiobolales). The Basionym: Sporobolomyces alborubescens Derx, Annls genus is mainly circumscribed by the phylogenetic analysis of mycol. 28: 15. 1930. seven genes and the analysis of the enlarged LSU rRNA gene 2) Rhodotorula araucariae Grinb. & Yarrow, Antonie van dataset, in which it occurred as a well supported clade within Leeuwenhoek 36: 455. 1970. Sporidiobolales (Figs 1, 8). Because the type species of the 3) Rhodotorula babjevae (Golubev) Q.M. Wang, F.Y.Bai, M. genera Rhodotorula, Rhodosporidium, Sporobolomyces and Groenew. & Boekhout, comb. nov. MycoBank MB813324. Sporidiobolus are located in other clades, species in this clade Basionym: Rhodosporidium babjevae Golubev, Syst. will be transferred into a new genus. Appl. Microbiol. 16: 445. 1993. 4) Rhodotorula dairenensis (T. Haseg. & I. Banno) Fell, J.P. Sexual reproduction observed in some species. Clamp con- Samp. & Gadanho, FEMS Yeast Res. 2: 56. 2002. nections present. Teliospores may be formed and produce 5) Rhodotorula diobovata (S.Y. Newell & I.L. Hunter) transversely septate basidia. Colonies pink to red and butyrous. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. Budding cells present. Pseudohyphae or true hyphae present or nov. MycoBank MB813325. not. Ballistoconidia formed or not, ellipsoidal, allantoid or Basionym: Rhodosporidium diobovatum S.Y. Newell & amygdaliform. Major CoQ systems Q-9 or Q-10. I.L. Hunter, J. Bact. 104: 504. 1970. = Rhodotorula glutinis (Fresenius) Harrison var. lusitanica Type species: Rhodosporidiobolus nylandii (M. Takash. & Marcilla. Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. 6) Rhodotorula evergladensis Fell, Statzell & Scorzetti, Antonie van Leeuwenhoek 99: 547. 2011. Species accepted: 7) Rhodotorula glutinis (Fresen.) F.C. Harrison, Proc. & 1) Rhodosporidiobolus fluvialis (Fell, Kurtzman, Tallman Trans. Roy. Soc. Canada ser. 3 21: 349. 1928. & J.D. Buck) Q.M. Wang, F.Y. Bai, M. Groenew. & 8) Rhodotorula graminis Di Menna, J. Gen. Microbiol. 18: Boekhout, comb. nov. MycoBank MB813360. 270. 1958.

www.studiesinmycology.org 181 WANG ET AL.

Basionym: Rhodosporidium fluviale Fell et al., Mycologia Sexual reproduction observed in some species. Clamp con- 80: 562. 1988. nections present. Teliospores are formed and germinate to 2) Rhodosporidiobolus azoricus (J.P. Samp. & Gadanho) produce transversely septate basidia. Colonies salmon-pink, red Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. and butyrous. Budding cells present. Pseudohyphae or true nov. MycoBank MB813364. hyphae present or not. Ballistoconidia formed, ellipsoidal, Basionym: Rhodosporidium azoricum J.P. Samp. & allantoid or amygdaliform. Major CoQ system Q-10. Gadanho, Can. J. Microbiol. 47: 214. 2001. 3) Rhodosporidiobolus microsporus (Higham ex Fell, Species accepted: 1) Sporobolomyces bannaensis F.Y. Bai & J.H. Zhao, Int. J. Blatt & Statzell) Q.M. Wang, F.Y. Bai, M. Groenew. & Syst. Evol. Microbiol. 53: 2092. 2003. Boekhout, comb. nov. MycoBank MB813366. Basionym: Sporidiobolus microsporus Higham ex Fell 2) Sporobolomyces beijingensis F.Y. Bai & Q.M. Wang, FEMS Yeast Res. 4: 582. 2004. et al., Antonie van Leeuwenhoek 74: 268. 1998. 3) Sporobolomyces blumeae M. Takash. & Nakase, 4) Rhodosporidiobolus nylandii (M. Takash. & Nakase) Mycoscience 41: 366. 2000. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. 4) Sporobolomyces carnicolor Yamasaki & H. Fujii ex F.Y.Bai nov. MycoBank MB813369. & Boekhout, Int. J. Syst. Evol. Microbiol. 52: 2313. 2002. Basionym: Sporobolomyces nylandii M. Takash. & 5) Sporobolomyces longiusculus (Libkind, van Broock & Nakase, Mycoscience 41: 364. 2000. J.P. Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & 5) Rhodosporidiobolus ruineniae (Holzschu, Tredick & Phaff) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Boekhout, comb. nov. MycoBank MB813380. Basionym: Sporidiobolus longiusculus Libkind et al., Int. comb. nov. MycoBank MB813371. J. Syst. Evol. Microbiol. 55: 505. 2005. Basionym: Sporidiobolus ruineniae Holzschu et al., Curr. 6) Sporobolomyces japonicus Iizuka & Goto, J. Gen. Appl. Microbiol. 5: 75. 1981. Microbiol. 11: 333. 1965. 6) Rhodosporidiobolus lusitaniae (A. Fonseca & J.P. 7) Sporobolomyces jilinensis F.Y. Bai & Q.M. Wang, FEMS Samp.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Yeast Res. 4: 584. 2004. comb. nov. MycoBank MB813374. 8) Sporobolomyces johnsonii (Nyland) Q.M. Wang, F.Y. Basionym: Rhodosporidium lusitaniae A. Fonseca & J.P. Samp., Syst. Appl. Microbiol. 15: 48. 1992. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813382. 7) Rhodosporidiobolus colostri (T. Castelli) Q.M. Wang, Basionym: Sporidiobolus johnsonii Nyland, Mycologia 41: F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank 687. 1949. MB813375. 9) Sporobolomyces koalae Satoh & Makimura, Int. J. Syst. Basionym: Mycotorula colostri T. Castelli, Giorn. Biol. App. Evol. Microbiol. 58: 2985. 2008. alla Indust. Chim. ad Alm. 2: 1. 1932. 10) Sporobolomyces patagonicus Libkind et al., Int. J. Syst. 8) Rhodosporidiobolus odoratus (J.P. Samp., A. Fonseca Evol. Microbiol. 55: 506. 2005. &Valerio) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, fi comb. nov. MycoBank MB813377. 11) Sporobolomyces phaf i F.Y. Bai et al., Int. J. Syst. Evol. Microbiol. 52: 2313. 2002. Basionym: Sporobolomyces odoratus J.P. Samp. et al., 12) Sporobolomyces roseus Kluyver & C.B. Niel, Centbl. FEMS Yeast Res. 2: 15. 2002. Bakt. ParasitKde Abt. II 63: 19. 1924. 9) Rhodosporidiobolus poonsookiae (M. Takash. & 13) Sporobolomyces ruberrimus Yamasaki & H. Fujii ex Fell Nakase) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, et al., FEMS Yeast Res. 1: 267. 2002 comb. nov. MycoBank MB813379. 14) Sporobolomyces salmonicolor (B. Fisch. & Brebeck) Basionym: Sporobolomyces poonsookiae M. Takash. & Kluyver & C.B. Niel, Centbl. Bakt. ParasitKde Abt. II 63: Nakase, Mycoscience 41: 365. 2000. 19. 1924. 15) Sporobolomyces salmoneus Derx, Annls mycol. 28: 17. Sporobolomyces Kluyver & C.B. Niel, Centbl. Bakt. ParasitKde 1930. Abt. II 63: 19. 1924. emend. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Taxa incertae sedis in the Microbotryomycetes = Sporidiobolus Nyland, Mycologia 41: 686. 1949. Family Colacogloeaceae Q.M. Wang, F.Y. Bai, M. Groenew. & Type species: Sporobolomyces roseus Kluyver & C.B. Niel Boekhout, fam. nov. MycoBank MB813158. This genus is emended to include Sporobolomyces species and their sexual counterparts Sporidiobolus, which belong to the Member of the Microbotryomycetes. The diagnosis of the family Sporobolomyces clade (Wang et al. 2015a) that occurred as a Colacogloeaceae is based on the description of the genus well supported clade within the Sporidiobolaceae (Spor- Colacogloea. The nomenclature of the family is based on the idiobolales). The Sporidiobolus clade contains the type species genus Colacogloea. of Sporobolomyces, S. salmonicolor, and the type species of Type genus: Colacogloea Oberw. & Bandoni. Sporidiobolus, Sp. johnsonii (Figs 1, 8). From this perspective the name Sporobolomyces has taxonomic priority over Spor- Genus accepted: Colacogloea Oberw. & Bandoni. idiobolus, as the former was published in 1924 and the latter in 1949. Thus we propose to keep the genus name Spor- Colacogloea Oberwinkler & Bandoni, Can. J. Bot. 68: 2532. obolomyces for this clade. 1990. emend. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout.

182 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Type species: Colacogloea peniophorae (Bourdot & Galzin) 9) Colacogloea terpenoidalis (Thanh, M.S. Smit, Moleleki Oberwinkler & Bandoni. & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813169. This genus is emended to include species of Colacogloea and Basionym: Rhodotorula terpenoidalis Thanh et al., FEMS related Rhodotorula species in the Colacogloea clade (Wang Yeast Res. 4: 860. 2004. et al. 2015a), which occurred as a well supported clade within Microbotryomycetes (Figs 1, 6). Note: Additional sequences representing three potential new species of this genus were found in public databases (Fig. 6). Sexual reproduction observed in some species. Teleomorphic taxa mycoparasitic, and the sexual state develops only in the Family Chrysozymaceae Q.M. Wang, F.Y. Bai, M. Groenew. & host. Basidiocarps minute, pulvinate to effuse, and mucoid- Boekhout, fam. nov. MycoBank MB813171. gelatinous. Basidia auricularioid (i.e., transversely septate). Hy- phae thin-walled, hyaline, with clamp connections, and grow Member of the Microbotryomycetes. The diagnosis of the family intrahymenially in host fructifications. Septal pores ‘simple’. Chrysozymaceae is based on the description of the genus Colacosomes (or lenticular body) occur at the interface between Chrysozyma. The nomenclature of the family is based on the the parasite and the host (Sampaio et al. 2011). Colonies cream, genus Chrysozyma. mucoid or butyrous. Budding cells present. Ballistoconidia not formed. Major CoQ system Q-10. Type genus: Chrysozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Species accepted: 1) Colacogloea cycloclastica (Thanh, M.S. Smit, Moleleki Genera accepted: Bannozyma Q.M. Wang, F.Y. Bai, M. Groe- & Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, new. & Boekhout, Chrysozyma Q.M. Wang, F.Y. Bai, M. Groe- comb. nov. MycoBank MB813159. new. & Boekhout, Hamamotoa Q.M. Wang, F.Y. Bai, M. Basionym: Rhodotorula cycloclastica Thanh et al., FEMS Groenew. & Boekhout, Fellozyma Q.M. Wang, F.Y. Bai, M. Yeast Res. 4: 858. 2004. Groenew. & Boekhout. 2) Colacogloea diffluens (Ruinen) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813160. Bannozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, fl Basionym: Candida dif uens Ruinen, Antonie van Leeu- gen. nov. MycoBank MB813173. wenhoek 29: 437. 1963. ≡ fl Rhodotorula dif uens (Ruinen) von Arx & Weijman Etymology: The genus is named in honour of I. Banno for his ≡ fl Vanrija dif uens (Ruinen) R.T. Moore contributions to yeast taxonomy. 3) Colacogloea eucalyptica (C.H. Pohl, M.S. Smit & Albertyn) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, This genus corresponds to the yamatoana clade (Wang et al. comb. nov. MycoBank MB813161. 2015a). Member of Chrysozymaceae (Microbotryomycetes). Basionym: Rhodotorula eucalyptica C.H. Pohl et al., Int. J. The genus is mainly circumscribed by the phylogenetic analysis Syst. Evol. Microbiol. 61: 2326. 2011. of seven genes and the analysis of the enlarged LSU rRNA gene 4) Colacogloea falcata (Nakase, M. Itoh & M. Suzuki) Q.M. dataset, in which it occurred as a well supported clade within Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Microbotryomycetes (Figs 1, 6). MycoBank MB813162. Basionym: Sporobolomyces falcatus Nakase et al., Trans. Sexual reproduction not known. Colonies pale yellow to Mycol. Soc. Japan 28: 296. 1987. greyish-yellow, butyrous. Budding cells present. Pseudohy- 5) Colacogloea foliorum (Ruinen) Q.M. Wang, F.Y. Bai, M. phae and septate hyphae present or not. Ballistoconidia pre- Groenew. & Boekhout, comb. nov. MycoBank sent or not, kidney-shaped, allantoid or elongate. Major CoQ MB813163. system Q-9. Basionym: Candida foliarum Ruinen, Antonie van Leeu- wenhoek 29: 436. 1963. Type species: Bannozyma yamatoana (Nakase, M. Suzuki & M. ≡ Rhodotorula foliorum (Ruinen) Rodr. Mir. & Weijman Itoh) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. 6) Colacogloea peniophorae (Bourdot & Galzin) Oberwinkler & Bandoni, Can. J. Bot. 68: 2532. 1990. Species accepted: 7) Colacogloea philyla (van der Walt, Klift & D.B. Scott) 1) Bannozyma arctica (Vishniac & M. Takash.) Q.M. Wang, Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank nov. MycoBank MB813164. MB813176. Basionym: Torulopsis philyla van der Walt et al., Antonie Basionym: Rhodotorula arctica Vishniac & M. Takash., Int. van Leeuwenhoek 37: 464. 1971. J. Syst. Evol. Microbiol. 60: 1215. 2010. ≡ Rhodotorula philyla (van der Walt et al.) Rodr. Mir. & 2) Bannozyma yamatoana (Nakase, M. Suzuki & M. Itoh) Weijman Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. 8) Colacogloea retinophila (Thanh, M.S. Smit, Moleleki & nov. MycoBank MB813179. Fell) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Basionym: Sporobolomyces yamatoanus Nakase et al.,J. comb. nov. MycoBank MB813166. Gen. Appl. Microbiol. 33: 446. 1987. Basionym: Rhodotorula retinophila Thanh et al., FEMS ≡ Bensingtonia yamatoana (Nakase et al.) Nakase & Yeast Res. 4: 859. 2004. Boekhout.

www.studiesinmycology.org 183 WANG ET AL.

Chrysozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Species accepted: gen. nov. MycoBank MB813180. 1) Fellozyma inositophila (Nakase & M. Suzuki) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Etymology: The genus is named because the type species MycoBank MB813185. produces yellowish colonies. Basionym: Sporobolomyces inositophilus Nakase & M. Suzuki, Antonie van Leeuwenhoek 53: 246. 1987. This genus agrees with the griseoflavus clade (Wang et al. 2015a). Member of Chrysozymaceae (Microbotryomycetes). The Note: Additional sequence representing a potential new species genus is mainly circumscribed by the phylogenetic analysis of of this genus was found in public databases (Fig. 6). seven genes and the analysis of the enlarged LSU rRNA gene dataset, in which it occurred as a well supported clade closely Hamamotoa Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, related to the yamatoana clade within Microbotryomycetes gen. nov. MycoBank MB813186. (Figs 1, 6). Sexual reproduction not known. Colonies greyish-white to Etymology: The genus is named in honour of Dr. Makiko yellowish-cream, butyrous. Budding cells present. Hyphae and Hamamoto for her contributions to yeast taxonomy. pseudohyphae not observed. Ballistoconidia present, ellipsoidal, allantoid or lunate. Major CoQ system Q-10. This genus agrees with the singularis clade (Wang et al. 2015a). Member of Chrysozymaceae (Microbotryomycetes). Type species: Chrysozyma griseoflava (Nakase & M. Suzuki) The genus is mainly circumscribed by the phylogenetic Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. analysis of seven genes and the analysis of the enlarged LSU rRNA gene dataset, in which it occurred as a well Species accepted: supported clade closely related to the griseoflavus and 1) Chrysozyma fushanensis (Nakase, F.L. Lee & M. yamatoana clades within Microbotryomycetes (Figs 1, 6). Takash.) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Sexual reproduction not known. Colonies cream-coloured comb. nov. MycoBank MB813181. to pale yellowish-brown, mucoid. Budding cells present. Basionym: Sporobolomyces fushanensis Nakase et al.,J. Hyphae and pseudohyphae not present. Ballistoconidia Gen. Appl. Microbiol. 51: 43. 2005. present or not, ellipsoidal or kidney-shaped. Major CoQ 2) Chrysozyma griseoflava (Nakase & M. Suzuki) Q.M. system Q-10. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813183. Type species: Hamamotoa singularis (Phaff & do Carmo-Sousa) fl Basionym: Sporobolomyces griseo avus Nakase & M. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Suzuki, J. Gen. Appl. Microbiol. 33: 168. 1987. Species accepted: Note: Species of Chrysozyma and Bannozyma can be distin- 1) Hamamotoa lignophila (Dill, C. Ramírez & Gonzalez) guished from each other by the presence of Q-10 and Q-9, Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. respectively. nov. MycoBank MB813187. Basionym: Candida lignophila Dill et al., Antonie van Fellozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. Leeuwenhoek 50: 220. 1984. nov. MycoBank MB813184. ≡ Rhodotorula lignophila (Dill et al.) Roeijmans et al. 2) Hamamotoa singularis (Phaff & do Carmo-Sousa) Q.M. Etymology: The genus is named in honour of Jack.W. Fell for his Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. contributions to yeast taxonomy. MycoBank MB813188. Basionym: Sporobolomyces singularis Phaff & do Carmo- This genus agrees with the Sporobolomyces inositophilus line- Sousa, Antonie van Leeuwenhoek 28: 205. 1962. age (Wang et al. 2015a). Member of the Chrysozymaceae ≡ Bullera singularis (Phaff & do Carmo-Sousa) Rodr. Mir. (Microbotryomycetes). The genus is mainly circumscribed by the phylogenetic analysis of seven genes and the analysis of the Note: Species of Hamamotoa (i.e. the singularis clade) enlarged LSU rRNA gene dataset, in which it occurred as a assimilate lactose and DL-lactate, but not melezitose and form single-species lineage within the Microbotryomycetes (Figs 1, 6). highly mucoid colonies (Fig. 3D). The species of Chrysozyma S. inositophilus is related to the singularis clade in the MP (i.e. the griseoflavus clade) and Bannozyma (i.e. the analysis of the combined seven genes-based dataset. This, yamatoana clade) are not able to grow on the former two however, was not supported in the ML and Bayesian analyses carbon sources and have colonies with a butyrous texture (Wang et al. 2015a). (Fig. 3D). Sexual reproduction not known. Colonies greyish-cream, butyrous. Budding cells present. Hyphae and pseudohyphae Pseudohyphozyma Q.M. Wang, F.Y. Bai, M. Groenew. & not observed. Ballistoconidia present, amygdaliform to falcate. Boekhout, gen. nov. MycoBank MB813189. Major CoQ system Q-10. Etymology: The name of the genus refers to the presence of Type species: Fellozyma inositophila (Nakase & M. Suzuki) Q.M. pseudohyphae in all known species of this clade. Wang, F.Y. Bai, M. Groenew. & Boekhout

184 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

This genus agrees with the buffonii clade (Wang et al. 2015a). Etymology: The genus is named in honour of Franz. Oberwinkler Member of the Microbotryomycetes. The genus is mainly cir- for his contributions to the taxonomy of Basidiomycota. cumscribed by the phylogenetic analysis of seven genes and the analysis of the enlarged LSU rRNA gene dataset, in which it This genus agrees with the yarrowii clade (Wang et al. 2015a). occurred as a well supported clade within the Micro- Member of the Microbotryomycetes. The genus is mainly cir- botryomycetes (Figs 1, 6). cumscribed by the phylogenetic analysis of seven genes and the analysis of the enlarged LSU rRNA gene dataset, in which it Sexual reproduction not known. Colonies cream-coloured and occurred as a well supported clade within the Micro- butyrous. Budding cells present. Pseudohyphae of branched botryomycetes (Figs 1, 6). The yarrowii, buffonii and tsugae chains of ovoid to cylindrical cells. Ballistoconidia not produced. clades clustered together with low support in the ML analysis, but Major CoQ system Q-10. were not supported by the MP and BI analyses (Wang et al. 2015a). Type species: Pseudohyphozyma buffonii (C. Ramírez) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Sexual reproduction not known. Colonies cream-coloured. Budding cells present. Pseudohyphae present. Ballistoconidia Species accepted: not produced. Major CoQ system Q-9. 1) Pseudohyphozyma bogoriensis (Deinema) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Type species: Oberwinklerozyma yarrowii (A. Fonseca & van MB813190. Uden) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Basionym: Candida bogoriensis Deinema, J. Econ. Biol. 61: 40. 1961. Species accepted: ≡ Rhodotorula bogoriensis (Deinema) von Arx & Weijman. 1) Oberwinklerozyma silvestris (Golubev & Scorzetti) Q.M. ≡ Candida bogoriensis Deinema var. lipolytica Ruinen. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. ≡ Vanrija bogoriensis (Deinema) Moore. MycoBank MB813194. 2) Pseudohyphozyma buffonii (C. Ramírez) Q.M. Wang, Basionym: Rhodotorula silvestris Golubev & Scorzetti, Int. F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank J. Syst. Evol. Microbiol. 60: 2501. 2010. MB813191. 2) Oberwinklerozyma straminea (Golubev & Scorzetti) Basionym: Torulopsis buffonii C. Ramírez, Microbiol. 10: Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. 236. 1957. nov. MycoBank MB813195. ≡ Rhodotorula buffonii (C. Ramírez) Roeijmans. Basionym: Rhodotorula straminea Golubev & Scorzetti, 3) Pseudohyphozyma pustula (Buhagiar) Q.M. Wang, F.Y. Int. J. Syst. Evol. Microbiol. 60: 2501. 2010. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank 3) Oberwinklerozyma yarrowii (A. Fonseca & van Uden) MB813192. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. Basionym: Torulopsis pustula Buhagiar, J. Gen. Microbiol. nov. MycoBank MB813196. 86: 3. 1975. Basionym: Cryptococcus yarrowii A. Fonseca & van Uden, ≡ Rhodotorula pustula (Buhagiar) Rodr. Mir. & Weijman. Antonie van Leeuwenhoek 59: 177. 1991. ≡ Rhodotorula yarrowii (A. Fonseca & van Uden) Boekhout Note: Species of the genus Pseudohyphozyma (i.e. the buffonii et al. clade) have a butyrous colony texture on slants with potato dextrose agar (PDA) and differ from members of the genus Slooffia (the Note: Species of the genus Oberwinklerozyma (i.e. the yarrowii tsugae clade), which are usually mucoid on PDA (Fig. 3D). clade) have major coenzyme Q system Q-9 and are able to assimilate raffinose and myo-inositol, whereas members of the genera Pseudohyphozyma (i.e. the buffonii clade) and Slooffia Pseudoleucosporidium V. de Garcia et al., FEMS Yeast Res. (i.e. the tsugae clade) have coenzyme Q-10 and do not use 15: 11. 2015. these two carbon sources (Table 3). Type species: Pseudoleucosporidium fasciculatum (Babeva & Sampaiozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Lisichk.) V. de Garcia et al. gen. nov. MycoBank MB813197. Species accepted: 1) Pseudoleucosporidium fasciculatum (Babeva & Lisichk.) Etymology: The genus is named in honour of J.P. Sampaio for V. de Garcia et al., FEMS Yeast Res. 15: 13. 2015. his contributions to yeast taxonomy. This genus agrees with the vanillica clade (Wang et al. 2015a). Note: Our analyses suggest a close relationship between the Member of the Microbotryomycetes. The genus is mainly circum- genera Pseudoleucosporidium and Curvibasidium, as revealed scribed by the phylogenetic analysis of seven genes and the anal- by the multi-gene analyses (Wang et al. 2015a) and the analysis ysis of the enlarged LSU rRNA gene dataset, in which it occurred as of the enlarged LSU rRNA gene dataset (Fig. 7). a well supported clade within Microbotryomycetes (Figs 1, 7). Oberwinklerozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Sexual reproduction not known. Colonies cream or yellowish. Boekhout, gen. nov. MycoBank MB813193. Budding cells present. Pseudohyphae and true hyphae absent. Ballistoconidia not produced. Major CoQ system Q-10.

www.studiesinmycology.org 185 WANG ET AL.

Type species: Sampaiozyma ingeniosa (Di Menna) Q.M. Wang, formed. Ballistoconidia present or not, ellipsoidal. Major CoQ F.Y. Bai, M. Groenew. & Boekhout. system Q-10

Species accepted: Type species: Slooffia tsugae (Phaff & do Carmo-Sousa) Q.M. 1) Sampaiozyma ingeniosa (Di Menna) Q.M. Wang, F.Y. Wang, F.Y. Bai, M. Groenew. & Boekhout Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813198. Species accepted: Basionym: Torulopsis ingeniosa Di Menna, J. Gen. 1) Slooffia cresolica (Middelhoven & Spaaij) Q.M. Wang, Microbiol. 19: 581. 1958. F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank ≡ Rhodotorula ingeniosa (Di Menna) von Arx & Weijman. MB813203. ≡ Candida ingeniosa (Di Menna) Meyer & Yarrow. Basionym: Rhodotorula cresolica Middelhoven & Spaaij, ≡ Vanrija ingeniosa (Di Menna) Moore. Int. J. Syst. Bacteriol. 47: 324. 1997. 2) Sampaiozyma vanillica (J.P. Samp.) Q.M. Wang, F.Y. 2) Slooffia pilati (F.H. Jacob, Faure-Raynaud & Berton) Bai, M. Groenew. & Boekhout, comb. nov. MycoBank Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. MB813199. nov. MycoBank MB813204. Basionym: Rhodotorula vanillica J.P. Samp., Syst. Appl. Basionym: Torulopsis pilati F.H. Jacob et al., Mycopatho- Microbiol. 17: 616. 1994. logia 69: 83. 1979. ≡ Rhodotorula pilati (F.H. Jacob et al.) Barnett et al. Spencerozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, 3) Slooffia tsugae (Phaff & do Carmo-Sousa) Q.M. Wang, gen. nov. MycoBank MB813200. F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank MB813206. Etymology: The genus is named in honour of I. Spencer-Martins Basionym: Bullera tsugae Phaff & do Carmo-Sousa, for her contributions to yeast taxonomy and physiology. Antonie van Leeuwenhoek 28: 205. 1962. ≡ Sporobolomyces tsugae (Phaff & do Carmo-Sousa) This genus agrees with the Rhodotorula crocea lineage (Wang Nakase & M. Itoh. et al. 2015a). Member of the Microbotryomycetes. The genus is mainly circumscribed by the phylogenetic analysis of seven Notes: Species of Slooffia can be distinguished from those of genes and the analysis of the enlarged LSU rRNA gene dataset, Pseudohyphozyma (the buffonii clade) by their colony texture in which it occurred as a single-species lineage within the (see above, Fig. 3D). Additional sequences representing two Microbotryomycetes (Figs 1, 6). potential new species of this genus were found in public data- bases (Fig. 6). Sexual reproduction not known. Colonies yellowish-cream, butyrous. Budding cells present. Pseudohyphae and true hy- Trigonosporomyces Q.M. Wang, F.Y. Bai, M. Groenew. & phae absent. Ballistoconidia not produced. Major CoQ system Q- Boekhout, gen. nov. MycoBank MB813207. 10. Etymology: The genus is named based on the morphology of the Type species: Spencerozyma crocea (Shifrine & Phaff) Q.M. type species that forms triangular cells on pseudohyphae. Wang, F.Y. Bai, M. Groenew. & Boekhout. This genus agrees with the Rhodotorula hylophila (Wang et al. Species accepted: 2015a). Member of the Microbotryomycetes. The genus is mainly 1) Spencerozyma crocea (Shifrine & Phaff) Q.M. Wang, circumscribed by the phylogenetic analysis of seven genes and F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank the analysis of the enlarged LSU rRNA gene dataset, in which it MB813201. occurred as a single-species lineage within the Micro- Basionym: Rhodotorula crocea Shifrine & Phaff, Mycolo- botryomycetes (Figs 1, 6). gia 48: 50. 1956. Sexual reproduction not known. Colonies cream-coloured. Slooffia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. Budding cells present. Pseudohyphae of long, slender cells, nov. MycoBank MB813202. often triangular. Ballistoconidia not produced. Major CoQ system unknown. Etymology: The genus is named in honour of W.C. Slooff for her contributions to yeast taxonomy. Type species: Trigonosporomyces hylophilus (van der Walt, van der Klift & D.B. Scott) Q.M. Wang, F.Y. Bai, M. Groenew. & This genus corresponds to the tsugae clade (Wang et al. Boekhout. 2015a). Member of the Microbotryomycetes. The genus is mainly circumscribed by the phylogenetic analysis of seven Species accepted: genes and the analysis of the enlarged LSU rRNA gene dataset, 1) Trigonosporomyces hylophilus (van der Walt, van der in which it occurred as a well supported clade within Micro- Klift & D.B. Scott) Q.M. Wang, F.Y. Bai, M. Groenew. & botryomycetes (Figs 1, 6). Boekhout, comb. nov. MycoBank MB813208. Basionym: Candida hylophila van der Walt et al., Antonie Sexual reproduction not known. Colonies cream-coloured and van Leeuwenhoek 37: 449. 1971. mucoid. Budding cells present. Hyphae and pseudohyphae not ≡ Rhodotorula hylophila (van der Walt et al.) Rodr. Mir. & Weijman.

186 PHYLOGENETIC CLASSIFICATION OF YEASTS AND RELATED TAXA

Yunzhangia Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Species accepted: gen. nov. MycoBank MB813209. 1) Udeniozyma ferulica (J.P. Samp. & van Uden) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. Etymology: The genus is named in honour of Yun-Zhang Wang, MycoBank MB813214. former professor at the Institute of Microbiology, Chinese Basionym: Rhodotorula ferulica J.P. Samp. & van Uden, Academy of Sciences, for his contributions to the taxonomic Syst. Appl. Microbiol. 14: 146. 1991. study of Pucciniales in China. Vonarxula Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, gen. This genus agrees with the sonckii clade (Wang et al. nov. MycoBank MB813216. 2015a). Member of the Microbotryomycetes. The genus is mainly circumscribed by the phylogenetic analysis of seven Etymology: The genus is named in honour of J.A. von Arx for his genes and the analysis of the enlarged LSU rRNA gene contributions to fungal taxonomy. dataset, in which it occurred as a well supported clade diverged from the other clades within the Microbotryomycetes This genus agrees with the Rhodotorula javanica lineage (Wang (Figs 1, 6). et al. 2015a). Member of the Microbotryomycetes. The genus is mainly circumscribed by the phylogenetic analysis of seven Sexual reproduction not known. Colonies cream-coloured, genes and the analysis of the enlarged LSU rRNA gene dataset, mucoid or butyrous. Budding cells present. Pseudohyphae and in which it occurred as a single-species lineage within the true hyphae not observed. Ballistoconidia not produced. Major Microbotryomycetes (Figs 1, 6). CoQ system unknown. Sexual reproduction not known. Colonies cream-coloured. Type species: Yunzhangia auriculariae (Nakase) Q.M. Wang, Budding cells present. Pseudohyphae of branched chains of F.Y. Bai, M. Groenew. & Boekhout. fusiform cells. Ballistoconidia not produced. Major CoQ system Q-9. Species accepted: 1) Yunzhangia auriculariae (Nakase) Q.M. Wang, F.Y. Bai, Type species: Vonarxula javanica (Ruinen) Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. nov. MycoBank M. Groenew. & Boekhout. MB813210. Basionym: Torulopsis auriculariae Nakase, J. Gen. Appl. Species accepted: Microbiol. 17: 413. 1971. 1) Vonarxula javanica (Ruinen) Q.M. Wang, F.Y. Bai, M. ≡ Rhodotorula auriculariae (Nakase) Rodr. Mir. & Weijman. Groenew. & Boekhout, comb. nov. MycoBank ≡ Candida auriculariae (Nakase) Meyer & Yarrow. MB813218. 2) Yunzhangia sonckii (Hopsu-Havu, Tunnela & Yarrow) Basionym: Candida javanica Ruinen, Antonie van Leeu- Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, comb. wenhoek 29: 436. 1963. nov. MycoBank MB813212. ≡ Rhodotorula javanica (Ruinen) von Arx & Weijman. Basionym: Candida sonckii Hopsu-Havu et al., Antonie van Leeuwenhoek 44: 436. 1978. Mixiomycetes R. Bauer et al., Mycol. Progr. 5: 47. 2006. ≡ Rhodotorula sonckii (Hopsu-Havu et al.) Rodr. Mir. & Weijman. Type order: Mixiales R. Bauer et al. Udeniozyma Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout, Mixiales R. Bauer et al., Mycol. Progr. 5: 47. 2006. gen. nov. MycoBank MB813213. Type family: Mixiaceae C.L. Kramer. Etymology: The genus is named in honour of N.J. van Uden for his contributions to the study and taxonomy of basidiomycetous This order is characterised by multinucleate hyphae and multiple yeasts. spores produced simultaneously on sporogenous cells (Bauer et al. 2006). This genus agrees with the Rhodotorula ferulica lineage (Wang et al. 2015a). Member of the Microbotryomycetes. The genus is Mixiaceae C.L. Kramer, Stud. Mycol. 30: 159. 1987. mainly circumscribed by the phylogenetic analysis of seven genes and the analysis of the enlarged LSU rRNA gene dataset, Type genus: Mixia C.L. Kramer. in which it occurred as single-species lineage within the Micro- botryomycetes (Figs 1, 6). R. ferulica seems to have affiliation to This family was proposed to accommodate the Taphrina-like Colacogloea, but did not receive high bootstrap values and genus Mixia (Kramer 1987), which is an intracellular parasite of Bayesian posterior probability. ferns belonging to the genus Osmunda.

Sexual reproduction not known. Colonies cream-coloured, Genus accepted: Mixia C.L. Kramer mucoid. Budding cells present. Hyphae and pseudohyphae pre- sent or not. Ballistoconidia not produced. Major CoQ system Q-10. Mixia C.L. Kramer, Mycologia 50: 924. 1958.

Type species: Udeniozyma ferulica (J.P. Samp. & van Uden) Type species: Mixia osmundae (Nishida) C.L. Kramer. Q.M. Wang, F.Y. Bai, M. Groenew. & Boekhout. Species accepted:

www.studiesinmycology.org 187 WANG ET AL.

1) Mixia osmundae (Nishida) C.L. Kramer, Mycologia 50: domain sequence analysis. International Journal of Systematic and Evolu- 924. 1958. tionary Microbiology 50: 1351–1371. Fonseca A (2011). Kondoa Y. Yamada, Nakagawa & Banno emend. A. Fonseca, Sampaio & Fell (2000). In: The yeasts, a taxonomic study Suggestion for new species descriptions (Kurtzman CP, Fell JW, Boekhout T, eds), 5th edn. Elsevier, Amsterdam: 1471–1475. In the future descriptions of new species in the genera Rhodo- Furuya N, Takashima M, Shiotani H (2012). Reclassification of citrus pseudo torula, Sporobolomyces and Bensingtonia should be restricted to greasy spot causal yeasts, and a proposal of two new species, Spor- obolomyces productus sp. nov. and S. corallinus sp. nov. Mycoscience 53: the clades containing the respective type species (Figs 1, 4, 8). 261–269. In the case of unclassified Microbotryomycetes or 'incertae Göker M, García-Blazquez G, Voglmayr H, et al. (2009). Molecular taxonomy of sedis’, none of the aforementioned generic names should be phytopathogenic fungi: a case study in Peronospora. PLoS One 4: e6319. used to describe new species, and new genera have to be Göker M, Grimm GW, Auch AF, et al. (2010). A clustering optimisation strategy introduced following a robust phylogenetic analysis utilising for molecular taxonomy applied to planktonic foraminifera SSU rRNA. Evolutionary Bioinformatics 6:97–112. several independent DNA loci or whole-genome comparisons Goloboff PA, Farris JS, Nixon KC (2008). TNT, a free program for phylogenetic (e.g. Wang et al. 2015a). Our results show that using the LSU analysis. Cladistics 24: 774–786. rRNA gene alone is not sufficient to resolve the high-level Gomes FC, Safar SV, Marques AR, et al. (2015). The diversity and extracellular phylogenetic relationships in Microbotryomycetes. enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis f.a., sp. nov. Antonie van Leeuwenhoek 107: 597–611. ACKNOWLEDGEMENTS Hamamoto M, Boekhout T, Nakase T (2011). Sporobolomyces Kluyver & van Niel (1924). In: The yeasts, a taxonomic study (Kurtzman CP, Fell JW, Boekhout T, eds), 5th edn. Elsevier, Amsterdam: 1929–1990. We thank Masako Takashima for providing some strains and Walter Gams for Hamamoto M, Nakase T (2000). Phylogenetic analysis of the ballistoconidium- his advice on nomenclatural matters; we also thank Jose Paulo Sampaio and forming yeast genus Sporobolomyces based on 18S rRNA sequences. In- Diego Libkind for their critical comments for this manuscript and Nathalie van ternational Journal of Systematic and Evolutionary Microbiology 50: der Wiele and Vincent Robert for their help with the registration of taxa in 1373–1380. MycoBank. This study was supported by grants No. 30970013 and No. Hawksworth DL (2011). A new dawn for the naming of fungi: impacts of de- 31010103902 from the National Natural Science Foundation of China (NSFC), cisions made in Melbourne in July 2011 on the future publication and No. 2012078 from the Youth Innovation Promotion Association of the Chinese regulation of fungal names. MycoKeys 1:7–20. Academy of Sciences and No. 10CDP019 from the Royal Netherlands Hibbett DS, Binder M, Bischoff JF, et al. (2007). A higher-level phylogenetic Academy of Arts and Sciences (KNAW). AY acknowledges a grant from the classification of the Fungi. Mycological Research 111: 509–547. Fundaç~ao para a Ci^encia e a Tecnologia, Portugal (grant number PTDC/BIA- Humphreys AM, Barraclough TG (2014). The evolutionary reality of higher taxa BIC/4585/2012). TB is supported by grant NPRP 5-298-3-086 of Qatar in mammals. Proceedings of the Royal Society B: Biological Sciences 281: Foundation. The authors are solely responsible for the content of this work. 20132750. Huson DH, Bryant D (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267. REFERENCES Kachalkin AV (2014). Yeasts of the White Sea intertidal zone and description of Glaciozyma litorale sp. nov. Antonie van Leeuwenhoek 105: 1073–1083. Aime MC, Matheny PB, Henk DA, et al. (2006). An overview of the higher level Khunnamwong P, Surussawadee J, Jindamorakot S, et al. (2015). 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