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The Phylocode Applied to <I>Cintractiellales</I>, a New Order

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The Phylocode Applied to <I>Cintractiellales</I>, a New Order VOLUME 6 DECEMBER 2020 Fungal Systematics and Evolution PAGES 55–64 doi.org/10.3114/fuse.2020.06.04 The PhyloCode applied to Cintractiellales, a new order of smut fungi with unresolved phylogenetic relationships in theUstilaginomycotina A.R. McTaggart1,2, C.J. Prychid3,4, J.J. Bruhl3, R.G. Shivas5* 1Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Ecosciences Precinct, GPO Box 267, Brisbane 4001, Australia 2Department of Plant and Soil Sciences, Tree Protection Co-operative Programme (TPCP), Forestry and Agricultural Biotechnology Institute (FABI), Private Bag X20, University of Pretoria, Pretoria, Gauteng, South Africa 3School of Environmental and Rural Science, University of New England, Armidale 2351, New South Wales, Australia 4Current address: Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK 5Centre for Crop Health, University of Southern Queensland, Toowoomba 4350, Queensland, Australia *Corresponding author: [email protected] The first two authors contributed equally to the manuscript Key words: Abstract: The PhyloCode is used to classify taxa based on their relation to a most recent common ancestor as recovered Cyperaceae pathogens from a phylogenetic analysis. We examined the first specimen of Cintractiella (Ustilaginomycotina) collected from fungal systematics Australia and determined its systematic relationship to other Fungi. Three ribosomal DNA loci were analysed both ITS with and without constraint to a phylogenomic hypothesis of the Ustilaginomycotina. Cintractiella did not share a LSU most recent common ancestor with other orders of smut fungi. We used the PhyloCode to define theCintractiellales , new taxa a monogeneric order with four species of Cintractiella, including C. scirpodendri sp. nov. on Scirpodendron ghaeri. obligate biotroph The Cintractiellales may have shared a most recent common ancestor with the Malasseziomycetes, but are otherwise Editor-in-Chief Prof. dr P.W. Crous, Westerdijk Fungal Biodiversity unresolved Institute, P.O. at Box the 85167, rank 3508 of AD class. Utrecht, The Netherlands. E-mail: [email protected] Citation: McTaggart AR, Prychid CJ, Bruhl JJ, et al. (2020). The PhyloCode applied to Cintractiellales, a new order of smut fungi with unresolved phylogenetic relationships in the Ustilaginomycotina. Fungal Systematics and Evolution 6: 55–64. doi: 10.3114/fuse.2020.06.04 Effectively published online: 26 March 2020 Corresponding editor: P.W. Crous INTRODUCTION (i) undiscovered biodiversity (missing data in phylogenetic analyses); (ii) few speciation events, and (iii) many extinctions Higher taxonomic ranks of smut fungi and their asexual yeast- between extant species and their most recent common like morphs (Ustilaginomycotina, Basidiomycota) were first ancestors. Several monogeneric classes and orders are known classified by patterns of teliospore germination (Tulasne & in the Ustilaginomycotina, namely, Malasseziomycetes, Tulasne 1847), later by ultrastructural characters (Bauer et al. Ceraceosorales, Golubeviales, Robbauerales, Uleiellales and 1997), and most recently by their evolutionary relationships Violaceomycetales (Begerow et al. 2006, Wang et al. 2014, Albu based on genes (Begerow et al. 2006, Wang et al. 2015) et al. 2015, Wang et al. 2015, Riess et al. 2016). and genomes (Kijpornyongpan et al. 2018). Confidence Hibbett et al. (2018) used the PhyloCode to define higher in the phylogenetic relationships and taxonomy of the taxonomic ranks of Fungi with known phylogenetic relationships. Ustilaginomycotina has increased as genomes of more taxa are The PhyloCode transcends descriptive taxonomy in that it delimits sequenced (Kijpornyongpan et al. 2018). taxa by their most recent common ancestor in a phylogenetic The smut fungi are evolutionary divergent and polyphyletic analysis, rather than by characters that may be homoplasious or (Begerow et al. 2006, McTaggart et al. 2012). The sexual difficult to recognise. Phylogenetic taxon definitions are suited phenotype of smut fungi, when known, replaces the to monotypic yeasts of the Ustilaginomycotina, as there are reproductive or other organs (leaves, roots) of their host plants few apomorphies, whether morphological or biological, and with powdery masses of fungal spores. Phylogenetic studies their current taxonomies are based on phylogenetic hypotheses have re-classified some traditional groups of smut fungi into (Wang et al. 2014, Wang et al. 2015). higher taxonomic ranks outside of the Ustilaginomycotina, e.g. Species of Cintractiella (Ustilaginomycotina) form foliar the Entorrhizomycota (Entorrhizomycota) (Aime et al. 2006, pseudo-spikelets or modify the reproductive units (see Prychid Bauer et al. 2015) and Microbotryales (Pucciniomycotina) & Bruhl 2013) of some tropical sedges (Cyperaceae, subfamily (Aime et al. 2006). The unresolved relationships between Mapanioideae). Three species of Cintractiella have been some taxa in the Ustilaginomycotina can be explained by described, the type, C. lamii on an unidentified species of Fungal Systematics and Evolution is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License © 2020 Westerdijk Fungal Biodiversity Institute 55 McTaggart et al. Wallemia sebi 0.99/98/33.3 AGARICOMYCOTINA 1.0/100/100 Tremella mesenterica Cryptococcus neoformans Georgefischeria riveae 1.0/100/100 Tilletiaria anomala Georgefischeriales Phragmotaenium flavum Entyloma calendulae 100/100/100 Entylomatales Editor-in-Chief Entyloma arnoseridis Prof. dr P.W. Crous, Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Rhamphospora nymphaeae 0.98/100/100 Doassansiales 0.99/98/33.3 Doassansia hygrophilae USTILAGINOMYCOTINA 0.98/95/66.7 Laurobasidium hachijoense 0.97/99/100 0.98/100/100 Exobasidium pachysporum 0.97/100/100 Exobasidium vaccinii Exobasidiales 0.97/100/100 Meira miltonrushii Exobasidiomycetes Graphiola phoenicis Robbauera albescens Robbaurerales Golubevia pallescens Golubeviales Erratomyces patelii 1.0/100/100 Conidiosporomyces ayresii 1.0/100/100 0.92/–/0 Tilletiales –/100/100 Ingoldiomyces hyalosporus Tilletia caries Jaminaea rosea 0.99/100/66.7 Volvocisporium triumfetticola Quambalaria cyanescens Microstromatales Microstroma bacarum 0.99/100/66.7 Pseudomicrostroma juglandis Pseudomicrostroma glucosiphilum Cintractiella scirpodendri BRIP 60160 1.0/100/100 Cintractiellales Cintractiella scirpodendri BRIP 59264 Malassezia furfur 1.0/100/100 Malasseziomycetes Malassezia sympodialis 0.95/99/33.3 Malasseziales 0.99/100/100 Malassezia globosa Malassezia restricta 0.95/99/100 Violaceomyces palustris Violaceomycetales Uleiella chilensis Uleiellales Ceraceosorus guamensis 0.96/–/33.3 1.0/100/100 Ceraceosorales Ceraceosorus bombacis Thecaphora amaranthi 0.94/91/66.7 Doassansiopsis limnocharidis 0.94/97/50 Urocystidales 0.97/100/50 Urocystis colchici 1.0/100/33.3 Fereydounia khargensis Ustilaginomycetes 1.0/100/100 Melanotaenium endogenum Melanotaenium euphorbiae 1.0/94/66.7 Anthracoidea karii 1.0/100/100 Testicularia cyperi –/96/100 Cintractia axicola 0.93/97/33.3 Moesziomyces bullatus Ustilago tritici 1.0/100/100 Ustilaginales 1.0/100/66.7 Ustilago hordei 0.96/–/66.7 Melanopsichium pennsylvanicum Incongruent branch with phylogenomic 0.96/98/66.7 Sporisorium scitamineum hypothesis of Kijpornyongpan et al. (2018) Sporisorium reilianum Tranzscheliella hypodytes aLRT>0.9 / UFBoot>95% / gCF –/99/50 Pseudozyma hubeiensis 0.04 Mycosarcoma maydis Fig. 1. Phylogram obtained from a maximum likelihood search in IQTree v. 1.7 beta, with a GTR gamma FreeRate heterogeneity model of evolution and a different rate for each partition of ribosomal DNA. aRLT values (≥ 0.9) and ultrafast bootstrap values (≥ 95 %) from 10 000 replicates, and genealogical concordance factors for three ribosomal DNA loci above nodes. Dashed lines indicate incongruence between the topology obtained from a phylogenomic dataset by Kijpornyongpan et al. (2018). 56 © 2020 Westerdijk Fungal Biodiversity Institute The PhyloCode applied to Cintractiellales Hypolytrum in Irian Jaya, Indonesia (Boedijn 1937); C. diplasiae et al. 2015) with a GTR gamma FreeRate heterogeneity model on Diplasia karataefolia in South America (Piepenbring 2001); of evolution and a different rate for each partition (command and C. kosraensis on Mapania pacifica in the Caroline Islands, -spp -m GTR+R), 10 000 ultrafast bootstraps (Hoang et al. 2018), Federated States of Micronesia (Aime et al. 2018). an approximate likelihood ratio test with 10 000 replicates Boedijn (1937) did not propose a higher taxonomic rank for (Guindon et al. 2010) and genealogical concordance factors Cintractiella. Vánky (2003) established the Cintractiellaceae in calculated from each locus (Minh et al. 2018). the Ustilaginales for two species of Cintractiella. Begerow et We used two approaches to determine the phylogenetic al. (2018) were uncertain of the relationship of Cintractiella to relationships of Cintractiella. A maximum likelihood search Editor-in-Chief Prof. dr P.W. Crous, Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] other genera of the Ustilaginomycotina and treated the group on the concatenated alignment i) without constraint, and with an unknown taxonomic affiliation. Our aim was to resolve ii) constrained to the class rank topology recovered by the systematic placement of Cintractiella within Fungi. We used Kijpornyongpan
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