An Updated Phylogeny of Sordariomycetes Based on Phylogenetic and Molecular Clock Evidence

Fungal Diversity DOI 10.1007/s13225-017-0384-2 An updated phylogeny of Sordariomycetes based on phylogenetic and molecular clock evidence 1,2 3 1,2 Sinang Hongsanan • Sajeewa S. N. Maharachchikumbura • Kevin D. Hyde • 2 4 1 3 Milan C. Samarakoon • Rajesh Jeewon • Qi Zhao • Abdullah M. Al-Sadi • Ali H. Bahkali5 Received: 30 April 2017 / Accepted: 17 May 2017 Ó School of Science 2017 Abstract The previous phylogenies of Sordariomycetes by divergence period (i.e. 200–300 MYA) can be used as M.E. Barr, O.E. Eriksson and D.L. Hawksworth, and T. criteria to judge when a group of related taxa evolved and Lumbsch and S. Huhndorf, were mainly based on mor- what rank they should be given. In this paper, we provide phology and thus were somewhat subjective. Later outlines an updated classification of accepted subclasses, orders of by T. Lumbsch and S. Huhndorf, and Maharachchikum- Sordariomycetes and use divergence times to provide bura and co-authors, took into account phylogenetic evi- additional evidence to stabilize ranking of taxa in the class. dence. However, even these phylogenetic driven We point out and discuss discrepancies where the phylo- arrangements for Sordariomycetes, were somewhat sub- genetic tree conflicts with the molecular clock. jective, as the arrangements in trees depended on many variables, such as number of taxa, different gene regions Keywords Class Á Classification Á Divergence times Á and methods used in the analyses. What is needed is extra Phylogenetics Á Ranking evidence to help standardize ranking in the fungi. Esti- mation of divergence times using molecular clock methods Introduction has been proposed for providing additional rational for higher ranking of taxa. Thus, in Sordariomycetes, a Sordariomycetes is an important class of ascomycetes, mainly characterized by non-lichenized, flask-shaped fruit- ing bodies (perithecia) and unitunicate asci (Lumbsch 2000; Electronic supplementary material The online version of this article (doi:10.1007/s13225-017-0384-2) contains supplementary Zhang et al. 2006; Maharachchikumbura et al. 2015, 2016). material, which is available to authorized users. However, this simple definition could change upon the growth form and habitat. Most members of Xylariomyceti- & Qi Zhao dae and some of Sordariomycetidae have dark perithecia, [email protected] amyloid asci, true paraphyses and periphysate ostioles, while 1 Key Laboratory of Plant Diversity and Biogeography of East most taxa of Hypocreomycetidae have light coloured Asia, Kunming Institute of Botany, Chinese Academy of perithecia, nonamyloid ascal apical rings (when apical rings Sciences, Kunming 650201, Yunnan, People’s Republic of are present) and lack true paraphyses. Some groups of Sor- China dariomycetes have cleistothecia (Zhang et al. 2006; Tang 2 Center of Excellence in Fingal Research, Mae Fah Luang et al. 2007; Senanayake et al. 2015). The class Sordari- University, Chiang Rai 57100, Thailand omycetes has a cosmopolitan distribution and accommo- 3 Department of Crop Sciences, College of Agricultural and dates mostly terrestrial taxa, although several taxa can be Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khod 123, Oman found in aquatic habitats (Hyde and Jones 1989; Tsui et al. 2000; Ho et al. 2001; Cai et al. 2002; Jones et al. 4 Department of Health Sciences, Faculty of Science, University of Mauritius, Reduit, Mauritius 2009a, b, 2015). They are also pathogens of plants, arthro- pods and mammals (Sung et al. 2007; Maharachchikumbura 5 Department of Botany and Microbiology, College of Science, King Saud University, P.O. Box: 2455, Riyadh 1145, Saudi et al. 2012, 2015; Hyde et al. 2014, 2016) and have been Arabia isolated as endophytes from various plants (Guo et al. 2001; 123 Fungal Diversity Promputtha et al. 2005), while many are saprobes involved proposed changes, including new introductions and discuss in decomposition and nutrient cycling (Prados-Rosale et al. discrepancies between divergent times and phylogenetic 2012; Keim et al. 2014; Liu et al. 2015; Ariyawansa et al. results, when they are inconsistent. 2015; Li et al. 2016). The classification of Sordariomycetes has changed Materials and methods drastically over the past decades because of the plasticity and variability in phenotype characters (Alexopoulos et al. 1996; Barr 1983, 1987, 1990; Eriksson and Hawksworth Phylogenetic analysis 1993). In addition, morphology alone is unable to provide Representative LSU, SSU, TEF1 and RPB2 sequence evidence for the natural origins and patterns of evolution data from each family in Sordariomycetes and some strains among these fungi (Mitchell et al. 1995; Vijaykrishna et al. of Leotiomycetes (346 taxa) were downloaded from Gen- 2006; Tang et al. 2007). Molecular studies on Sordari- Bank to supplement the dataset (Supplementary Table 1). omycetes began in the early 1990s and SSU and LSU Representative strains from Eurotiomycetes were used as sequence data was mostly used as markers (Berbee and outgroup taxa. The data set was aligned by using MAFFT Taylor 1992; Spatafora and Blackwell 1993; Spatafora (Katoh et al. 2009), checked and aligned manually using 1995). However, SSU and LSU alone, are not sufficient to Bioedit (Hall 1999). Maximum likelihood analysis using resolve the most of the groups in Sordariomycetes as they RAxML was performed by using raxmlGUIv.0.9b2 (Sil- have a low resolution in ranking taxa (Tang et al. 2007). vestro & Michalak 2012). The GTRGAMMA model was The higher ranking of Sordariomycetes is not yet stable. used in the analysis, the search strategy was set to 1000 Eriksson and Winka (1997) introduced three subclasses, rapid bootstrapping. The number of replicates was inferred Hypocreomycetidae, Sordariomycetidae and Xylari- using the stopping criterion (Pattengale et al. 2009). The omycetidae based on morphology (perithecial ascomata, trees from analysis were viewed in FigTree (Rambaut hamathecium composed of paraphyses, ostioles with peri- 2006). The bootstrap values equal or greater than 50% are physes and unitunicate or pseudoprotunicate asci) and given as the first set of numbers above the nodes (Fig. 1). nrDNA sequence data. However, it has been found that assemblages of protein genes yield a higher phylogenetic Molecular clock analysis resolution, as compared to ribosomal regions (Schoch et al. Data for the molecular clock analysis of Sordari- 2009). In most recent studies, in addition to ribosomal omycetes is provided in Hyde et al. (2017). We use the data genes, the phylogenetic relationships among Sordari- from the molecular clock evidence in this paper and omycetes were investigated using partial translation elon- compare it with the phylogenetic tree presented here. The gation factor 1-alpha, the second largest subunit of RNA conflicts found between the MCC tree in Hyde et al. (2017) polymerase (RPB2) and beta-tubulin genes (Zhang et al. and the phylogenetic tree in this study are discussed below. 2006; Tang et al. 2007). In a revision of Sordariomycetes, Maharachchikumbura et al. (2015) introduced three new subclasses; Diaporthomycetidae, Lulworthiomycetidae, Results and discussion and Meliolomycetidae based on morphology and combined analysis of LSU, SSU, TEF and RPB2 sequence data. Representative strains of LSU, SSU, TEF1 and RPB2 According to the outline by Maharachchikumbura et al. sequence data of Sordariomycetes and Leotiomycetes were (2016), Sordariomycetes currently has six subclasses, 32 included in the phylogenetic analysis; representative strains orders, 105 families and 1331 genera. of Eurotiomycetes were selected as an outgroup (Figs. 1, Fossil calibration data and divergence time estimates are 2). Phylogenetic analysis generated by RAxML analysis being used as additional evidence for the ranking of fungi indicates Sordariomycetes share a common ancestor with (Beimforde et al. 2014; Hongsanan et al. 2016;Pe´rez- Leotiomycetes with high support (94% ML). In the tree, Ortega et al. 2016; Samarakoon et al. 2016; Zhao et al. Diaporthomycetidae, Hypocreomycetidae, Lulwor- 2016) and studies have shown that Sordariomycetes had a thiomycetidae, Sordariomycetidae, Savoryellomycetidae higher speciation process over time, when compared to and Xylariomycetidae are well-supported. Meliolomyceti- Dothideomycetes and Leotiomycetes (Wang et al. 2010). dae belongs to Sordariomycetidae, and is no longer treated In this paper, we provide an updated backbone tree for as subclass. Savoryellomycetidae is introduced formally in Sordariomycetes based on the analysis of LSU, SSU, TEF this study based on phylogenetic analysis (100% ML) and and RPB2 sequence data. Based on the new phylogenies its stem age (267 MYA) reported in Hyde et al. (2017). The and additional evidence from divergence times published internal classification of each subclass is discussed in this in Hyde et al. (2017), several taxonomic changes to Sor- paper based on phylogenetic (this study) and the MCC dariomycetes are necessary. We therefore provide a list of trees (Hyde et al. 2017). Moreover, some conflicts between 123 Fungal Diversity Fig. 1 RAxML maximum likelihood phylogenetic tree Diaporthales (LSU, SSU, TEF1 and RPB2) of Calosphaeriales Sordariomycetes tree (compressed overview tree) Togniniales from 345 taxa with all lineages Magnaporthales collapsed to order level where Distoseptisporaceae possible. Subclasses are indicated in coloured blocks Myrmecridiales Annulatascales Diaporthomycedae Thyridiaceae Phomatosporales Ophiostomatales Papulosaceae Trichosphaeriaceae Sporidesmiaceae Amplistromatales

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