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Evolution of Nutritional Modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) As Revealed from Publicly Available ITS Sequences

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Evolution of Nutritional Modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) As Revealed from Publicly Available ITS Sequences fungal ecology 6 (2013) 256e268 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/funeco Evolution of nutritional modes of Ceratobasidiaceae (Cantharellales, Basidiomycota) as revealed from publicly available ITS sequences Vilmar VELDREa, Kessy ABARENKOVa, Mohammad BAHRAMa, Florent MARTOSc,1, ~ Marc-Andre SELOSSEb, Heidi TAMMa, Urmas KOLJALGa, Leho TEDERSOOa,d,* aInstitute of Ecology and Earth Sciences, University of Tartu, 40 Lai, 51005 Tartu, Estonia bCentre d’Ecologie Fonctionnelle et Evolutive, CNRS, UMR 5175, 1919 Route de Mende, 34293 Montpellier cedex 5, France cUniversitedeLaReunion, Peuplements Vegetaux et Bioagresseurs en Milieu Tropical (UMR C53), Equipe Dynamiques ecologiques au sein des ecosystemes naturels, 15 Avenue Rene Cassin, BP 7151, 97715 Saint-Denis cedex 9, France dNatural History Museum of Tartu University, 46 Vanemuise, 51046 Tartu, Estonia article info abstract Article history: Fungi from the Ceratobasidiaceae family have important ecological roles as pathogens, Received 1 September 2012 saprotrophs, non-mycorrhizal endophytes, orchid mycorrhizal and ectomycorrhizal sym- Revision received 5 March 2013 bionts, but little is known about the distribution and evolution of these nutritional modes. Accepted 6 March 2013 All public ITS sequences of Ceratobasidiaceae were downloaded from databases, annotated Available online 24 April 2013 with ecological and taxonomic metadata, and tested for the non-random phylogenetic Corresponding editor: distribution of nutritional modes. Phylogenetic analysis revealed six main clades within Havard€ Kauserud Ceratobasidiaceae and a poor correlation between molecular phylogeny and morphologi- calecytological characters traditionally used for taxonomy. Sequences derived from soil Keywords: (representing putative saprotrophs) and orchid mycorrhiza clustered together, but Ceratobasidium remained distinct from pathogens. All nutritional modes were phylogenetically conserved Ectomycorrhiza in the Ceratobasidiaceae based on at least one index. Our analyses suggest that in general, Evolutionary ecology autotrophic orchids form root symbiosis with available Ceratobasidiaceae isolates in soil. Orchid mycorrhiza Ectomycorrhiza-forming capability has evolved twice within the Ceratobasidiaceae and it Phylogeny had a strong influence on the evolution of mycoheterotrophy and host specificity in certain Rhizoctonia orchid taxa. Saprotrophepathogen continuum ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved. Thanatephorus Introduction decomposers of dead organic matter, provide mineral nutri- tion to plants as mycorrhizal symbionts, or devastate plant Fungi play a fundamental role in nutrient and carbon cycling populations as phytopathogens. Despite their major eco- in terrestrial ecosystems and sediments. They act as logical and economic importance, the taxonomic and * Corresponding author. Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai, 51005 Tartu, Estonia. Tel./fax: þ372 7376222. E-mail address: [email protected] (L. Tedersoo). 1 Current address: School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa. 1754-5048/$ e see front matter ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved. http://dx.doi.org/10.1016/j.funeco.2013.03.004 Evolution of nutritional modes in Ceratobasidiaceae 257 ecological complexity of many important taxa remains poorly currently considered a peripheral member of the order Can- understood because of the ephemeral habit, and the lack of tharellales, although its phylogenetic relations to other fruit bodies in most fungal groups. members of this group are not well resolved (Moncalvo et al. The family Ceratobasidiaceae (Cantharellales, Basidiomy- 2006; Hibbett et al. 2007). cota) consists of the two closely related sexual genera, Cera- Most attention to the members of the Ceratobasidiaceae tobasidium and Thanatephorus along with their Rhizoctonia has been sparked by their role as widespread soil-borne crop asexual forms. They form one of such ‘cryptic’ fungal groups pathogens. Their necrotrophic capability is remarkably non- that play important ecological roles as crop pathogens, orchid specific and affects a multitude of plant taxa. There is a con- mycorrhizal symbionts, saprotrophs and endophytes tinuum between the necrotrophic parasitism and saprotrophy (Parmeter 1970; Sneh et al. 1996; Roberts 1999). These fungi in the Ceratobasidiaceae. Most strains possess some sapro- spend most of their life cycle in the morphologically simple trophic capability, but aggressive pathogens are poor sapro- asexual (i.e. ‘anamorphic’) stage during which they can only trophic competitors and depend on nutrients acquired from be observed macroscopically as irregular sclerotia or, for living plant tissue (Papavizas 1970). By contrast, strains that phytopathogens, as necrotic lesions in the tissues of a tre- have lost their ability to infect and cause serious damage to mendous range of host plants. Even when the sexual (i.e. living organs, may function as commensal or even mutualistic ‘teleomorphic’) stage occurs, it represents an inconspicuous, endophytes (i.e. fungi that grow diffusely in tissues, without fragile, web-like layer of generative hyphae covering living causing any visible symptoms; Sen et al. 1999) and increase leaves and stems of hosts, or plant debris (Roberts 1999). Dif- their hosts’ resistance to pathogenic strains (Sneh 1998). ficulties with the induction of fruiting in culture and the lack However, little is known about the frequency and role of of morphological characters to distinguish among biological Ceratobasidiaceae endophytes (Sen et al. 1999). species have considerably complicated taxonomic and eco- As a further major interaction, the Ceratobasidiaceae logical research on these fungi. includes a large number of taxa that form orchid mycorrhiza To provide a practical method for identification, plant (OrM). Orchids have an unusual relationship with their pathologists implemented a tractable test based on number of mycorrhizal fungi compared to other mycorrhizal plants: they nuclei per cell and anastomosis compatibility in co-culture receive all nutrients, including carbon, from their fungi during instead of morphology-based binomial taxonomy (Carling their heterotrophic germination (Smith & Read 2008; 1996; Sharon et al. 2008). Traditionally, strains of binucleate Dearnaley et al. 2012). At the adult stage, most orchids develop Rhizoctonia (BNR; binucleate strains are occasionally placed in photosynthetic capability, but clearly continue to benefit from the anamorphic genus Ceratorhiza) and multinucleate Rhi- their mycobionts by receiving mineral nutrients. Some spe- zoctonia (MNR) are considered anamorphs of Ceratobasidium cies associated with Ceratobasidium allow a net carbon flow and Thanatephorus, respectively, although a few species of from adult orchids to the fungus (Cameron et al. 2006, 2008), Thanatephorus are binucleate (Roberts 1999). Both the MNR and while in some other species, adult orchids still obtain carbon BNR are separated into anastomosis groups (AG), including 13 from fungi (Selosse & Roy 2009; Yagame et al. 2012). Thus, the MNR AGs (AG-1 to AG-13) and 16 BNR AGs (AG-A to AG-S, balance between costs and benefits for fungi remains poorly excluding AG-J, AG-M and AG-N; Sharon et al. 2008), some of understood in OrM (Dearnaley et al. 2012), and we treat here which are further divided into anastomosis subgroups based the association between autotrophic orchids and their on more detailed analysis of anastomosis compatibility, mycorrhizal fungi as symbiotic along the mutualismeparasi- morphology, pathogenicity and other criteria. All multi- tism continuum (Egger & Hibbett 2004). As a side finding in the nucleate AGs correspond to the teleomorphic species T. research on OrM, it was discovered that some Ceratobasidia- cucumeris (anamorph Rhizoctonia solani). The binucleate AG-A, ceae isolates also form ectomycorrhiza (EcM) (Warcup 1991; AG-B(o), AG-D, AG-P and AG-Q correspond to Ceratobasidium Yagame et al. 2008, 2012; Bougoure et al. 2009), and indeed cornigerum, whereas AG-Ba and AG-Bb correspond to some Ceratobasidiaceae have been sporadically reported in Ceratobasidium setariae. However, teleomorphs of the remain- community analyses of EcM fungi (e.g. Rosling et al. 2003). ing binucleate AGs remain unknown (Roberts 1999). However, the phylogenetic and biogeographic distribution of Teleomorphs of Ceratobasidiaceae are characterized by these relatively uncommon EcM groups remains poorly aseptate basidia (a derived, apomorphic feature), but also self- understood (Tedersoo et al. 2010). replicating spores and large indeterminate sterigmata Development of molecular methods has led to rapid (ancestral features; Roberts 1999). Numerous minor genera unravelling of the systematics and ecology of microbes in the have been described within the Ceratobasidiaceae, but later past few decades. Barcoding with the Internal Transcribed synonymized with either Ceratobasidium (characterized by a Spacer (ITS) region of the ribosomal DNA locus has become a single layer of basidia arising from horizontally branching standard means of identification in fungi (Schoch et al. 2012). hyphae of <10 mm in diameter) or Thanatephorus (charac- ITS sequences offer suitable resolution for identification of the terized by multiple layers of basidia arising from vertically Ceratobasidiaceae strains and provide an
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