Review Tansley review Sebacinales – one thousand and one interactions with land plants Author for correspondence: Michael Weiß1,2, Frank Waller3, Alga Zuccaro4,5 and Marc-Andre Selosse6,7 Marc-Andre Selosse 1 € Tel: +33 607123418 Steinbeis-Innovationszentrum Organismische Mykologie und Mikrobiologie, Vor dem Kreuzberg 17, 72070 Tubingen, Germany; Email: [email protected] 2Department of Biology, University of Tubingen,€ Auf der Morgenstelle 1, 72076 Tubingen,€ Germany; 3Pharmaceutical Biology, Julius Received: 9 October 2015 von Sachs Institute for Biosciences, Biocenter, Wurzburg€ University, Julius-von-Sachs Platz 2, 97082 Wurzburg,€ Germany; 4Botanical Accepted: 5 February 2016 Institute, Cluster of Excellence on Plant Sciences (CEPLAS), BioCenter, University of Cologne, 50674 Cologne, Germany; 5Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany; 6Departement Systematique et Evolution (UMR 7205 ISYEB), Museum national d’Histoire naturelle, CP 50, 45 rue Buffon, 75005 Paris, France; 7Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Gdansk, Poland Contents Summary 20 V. Endophytism in Serendipitaceae: a fungal adaptation to biotrophy 33 I. Introduction 21 VI. Conclusion and future directions 35 II. Phylogeny and systematics of Sebacinales 21 Acknowledgements 36 III. Ecology and diversity of Sebacinales interactions with plants 23 Author contributions 36 IV. Endophytism in Serendipitaceae: changing phenotype of the host plants 29 References 36 Summary New Phytologist (2016) 211: 20–40 Root endophytism and mycorrhizal associations are complex derived traits in fungi that shape doi: 10.1111/nph.13977 plant physiology. Sebacinales (Agaricomycetes, Basidiomycota) display highly diverse interac- tions with plants. Although early-diverging Sebacinales lineages are root endophytes and/or Key words: endophytism, mycorrhizae, have saprotrophic abilities, several more derived clades harbour obligate biotrophs forming mycorrhizal evolution, Phylogeny, mycorrhizal associations. Sebacinales thus display transitions from saprotrophy to endophytism Piriformospora, Sebacinaceae, and to mycorrhizal nutrition within one fungal order. This review discusses the genomic traits Serendipitaceae, stress resistance. possibly associated with these transitions. We also show how molecular ecology revealed the hyperdiversity of Sebacinales and their evolutionary diversification into two sister families: Sebacinaceae encompasses mainly ectomycorrhizal and early-diverging saprotrophic species; the second family includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal abilities. We propose the name Serendipitaceae for this family and, within it, we transfer to the genus Serendipita the endophytic cultivable species Piriformospora indica and P. williamsii. Such cultivable Serendipitaceae species provide excellent models for root endophytism, especially because of available genomes, genetic tractability, and broad host plant range including important crop plants and the model plant Arabidopsis thaliana.We review insights gained with endophytic Serendipitaceae species into the molecular mechanisms of endophytism and of beneficial effects on host plants, including enhanced resistance to abiotic and pathogen stress. 20 New Phytologist (2016) 211: 20–40 Ó 2016 The Authors www.newphytologist.com New Phytologist Ó 2016 New Phytologist Trust New Phytologist Tansley review Review 21 concerning their interactions with plants (e.g. based on genomics I. Introduction and transcriptomics), especially as endophytes. Moreover, we At the beginning of the 2000s, only taxonomists were interested in formally propose a new family Serendipitaceae (Box 1). After a the fungi today known as Sebacinales, then a few species of mostly summary of phylogeny and systematics, we describe the diversity of inconspicuous basidiomycetes with septate basidia (Fig. 1) and Sebacinales interactions with plant roots. We then focus on the unknown ecology. Data from molecular ecology and biology of well-studied endophytic interaction, starting with a review of the interactions with plants drastically changed that outlook, and impact of Sebacinales on plant physiology (i.e. the host side), and Sebacinales turned out to be highly diverse root symbionts, then linking these observations with adaptation to endophytism forming various mycorrhizae and endophytic interactions with (i.e. the fungal side), based on the latest genomic data. high abundance. Endophytes grow in living plant tissues without causing symptoms or morphological modifications, and the impact II. Phylogeny and systematics of Sebacinales of endophytism on the host plant ranges from mildly negative to neutral or even beneficial (Wilson, 1995). Sebacinales illustrate 1. Taxonomic history how organismal interactions, long-studied observationally and rarely experimentally, have been unexpectedly clarified by molec- This story starts with the French mycologists Charles and Louis- ular methods and are now known to connect ecology and Rene Tulasne, who transferred Corticium incrustans into a new systematics, physiology and genomics. However, we are only genus Sebacina based on longitudinally septate basidia (Tulasne & beginning to understand the impact and mechanisms of these Tulasne, 1871; Fig. 1c). Until recently, the genus Sebacina plant–fungal interactions. included fungi with resupinate or absent fruitbodies (the basid- This review summarizes the results of rapidly expanding research iospore-bearing structures). Roughly a century later the family that includes systematics, ecology, biogeography, physiology and Sebacinaceae was erected (Wells & Oberwinkler, 1982) based on genomics, to depict the current knowledge of Sebacinales interac- micromorphology, such as longitudinally septate basidia, absence tions with plants. We update previous reviews and focus on of clamp connections and often thick-walled hyphae, particularly evolutionary patterns in Sebacinales and on recent advances within the substrate (Fig. 1a,c). The family then contained the (a) (b) (c) (d) (e) (f) (g) Fig. 1 Sebacinales morphology and anatomy. (a) Micromorphology of Serendipita vermifera (from type material): hyphae, clusters of longitudinally septate basidia in various stages, some with branched sterigmata (arrowheads), worm-like basidiospores (to the left; bar, 20 lm; modified from Oberwinkler et al., 2014). (b) Crust-like fruitbody of Sebacina incrustans (bar, 1 cm; from Oberwinkler et al., 2013b). (c) Micromorphology of Sebacina dimitica (from type material): longitudinal section through the whole fruitbody, with thick-walled hyphae colonizing the substrate, longitudinally septate basidia, branched sterile hyphal elements (dikaryophyses), and basidiospores (bar, 20 lm; modified from Oberwinkler et al., 2014). (d) Transmission electron micrograph of a dolipore with continuous parenthesomes (arrowheads; bar, 150 nm; from Setaro et al., 2006b). (e) Cushion-shaped fruitbody of Craterocolla cerasi (Sebacinaceae; from Hibbett et al., 2014). (f) Clavarioid-erect fruitbody of Sebacina candida (= Tremellodendron candidum; bar, 2 cm; from Oberwinkler et al., 2013b). (g) Funnel-shaped fruitbodies of Tremelloscypha gelatinosa (Sebacinaceae; bar, 2 cm; from Bandala et al., 2011). Ó 2016 The Authors New Phytologist (2016) 211: 20–40 New Phytologist Ó 2016 New Phytologist Trust www.newphytologist.com New 22 Review Tansley review Phytologist More than 1000 Sebacinales species, most of which correspond to Box 1 Taxonomic novelties. species yet to be described, are currently available in the UNITE database (based on a threshold of 1% divergence of internal First, we formally establish here a name for the Sebacinales ‘Group transcribed spacer (ITS) barcode sequences; K~oljalg et al., 2013). B’ (Weiß et al., 2004; see Supporting Information Table S1) that For this review, available sequences were used to build a tree has a sister position to Sebacinaceae (Weiß et al., 2011; Figs 2, 3): (displayed in Supporting Information Fig. S1, see alignment in Serendipitaceae M. Weiß, Waller, A. Zuccaro & Selosse, fam.n. Notes S1), from which selected sections are shown in Fig. 3. (MycoBank MB809112). Equivalent to ‘Sebacinales Group B’ sensu Weiß et al. (2004). Members of Sebacinales that lack macroscop- ically visible fruitbodies. Signature nucleotides of internal tran- 2. Sebacinaceae scribed spacer (ITS) and 28S rDNA sequences for this group are given in Oberwinkler et al. (2014). Fruitbodies are only known from this family, but molecular Second, molecular phylogenetic analyses have shown that phylogenies (Weiß et al., 2004, 2011) have suggested that gross Piriformospora cannot be separated taxonomically from morphology (Fig. 1), once the basis for generic concepts in the Serendipita without rendering the latter paraphyletic (e.g. Weiß Sebacinales, is a poor marker to distinguish monophyletic groups. et al., 2004, 2011; Basiewicz et al., 2012; Oberwinkler et al., 2014; Species with erect fruitbodies (hitherto classified in Tremellodendron) Fig. 3h,k). We thus propose that Piriformospora be merged with evolved independently from crust-like forms several times within the Serendipita. Serendipita was based on a teleomorph (= sexual stage; Roberts, 1993), whereas Piriformospora was proposed as an Sebacinaceae. To render Sebacina a monophyletic crown group, anamorph genus (= asexual stage; Verma et al., 1998). Merging Oberwinkler et al. (2014) merged Tremellodendron (see Fig. 1f) with both types of taxa was not possible