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Ceraceosorus bombacis is an early-diverging lineage of smut fungi and a pathogen of cotton trees (Bombax ceiba). To study the evolutionary genomics of smut fungi in comparison with other fungal and oomycete pathogens, the genome of C. bombacis was sequenced and comparative genomic analyses were performed. The genome of 26.09 Mb encodes for 8,024 proteins, of which 576 are putative-secreted effector proteins (PSEPs). Orthology analysis revealed 30 ortholog PSEPs among six Ustilaginomycotina genomes, the largest groups of which are lytic enzymes, such as aspartic peptidase and glycoside hydrolase. Positive selection analyses revealed the highest percentage of positively selected PSEPs in C. bombacis compared with other Ustilaginomycotina genomes. Metabolic pathway analyses revealed the absence of genes encoding for nitrite and nitrate reductase in the genome of the human skin pathogen Malassezia globosa, but these enzymes are present in the sequenced plant pathogens in smut fungi. Interestingly, these genes are also absent in cultivable oomycete animal pathogens, while nitrate reductase has been lost in cultivable oomycete plant pathogens. Similar patterns were also observed for obligate biotrophic and hemi-biotrophic fungal and oomycete pathogens. Furthermore, it was found that both fungal and oomycete animal pathogen genomes are lacking cutinases and pectinesterases. Overall, these findings highlight the parallel evolution of certain genomic traits, revealing potential common evolutionary trajectories among fungal and oomycete pathogens, shaping the pathogen genomes according to their lifestyle.

A taxonomic re-evaluation of the Ceratobasidium-Rhizoctonia group suggests that Ceratobasidium contains only the type species C. calosporum, which deviates in micromorphological and ultrastructural characters from all other species so far included in that genus. Rhizoctonia species are compared with the type species of Ceratobasidium, Cejpomyces, Oncobasidium, Tofispora, Waitea, and Ypsilonidium. The micromorphology, ultrastructure, cellular interaction with the host, and molecular phylogeny of a Rhizoctonia species parasitic on needles and young shoots of Picea abies have been studied. The parasite has been known for a long time, but misinterpreted, and not named so far. Rhizoctonia butinii is described and compared with related species of the genus.

Patterns of geographic distribution and composition of fungal communities are still poorly understood. Widespread occurrence in terrestrial ecosystems and the unique richness of interactions of Sebacinales with plants make them a target group to study evolutionary events in the light of nutritional lifestyle. We inferred diversity patterns, phylogenetic structures and divergence times of Sebacinales with respect to their nutritional lifestyles by integrating data from fossil-calibrated phylogenetic analyses. Relaxed molecular clock analyses indicated that Sebacinales originated late Permian within Basidiomycota, and their split into Sebacinaceae and Serendipitaceae nom. prov. likely occurred during the late Jurassic and the early Cretaceous, coinciding with major diversifications of land plants. In Sebacinaceae, diversification of species with ectomycorrhizal lifestyle presumably started during the Paleocene. Lineage radiations of the core group of ericoid and cavendishioid mycorrhizal Sebacinales started probably in the Eocene, coinciding with diversification events of their hosts. The diversification of Sebacinales with jungermannioid interactions started during the Oligocene, and occurred much later than the diversification of their hosts. Sebacinales communities associated either with ectomycorrhizal plants, achlorophyllous orchids, ericoid and cavendishioid Ericaceae or liverworts were phylogenetically clustered and globally distributed. Major Sebacinales lineage diversifications started after the continents had drifted apart. We also briefly discuss dispersal patterns of extant Sebacinales.

Background Phylogenetic studies, particularly those based on rDNA sequences from plant roots and basidiomata, have revealed a strikingly high genetic diversity in the Sebacinales. However, the factors determining this genetic diversity at higher and lower taxonomic levels within this order are still unknown. In this study, we analysed patterns of genetic variation within two morphological species, Sebacina epigaea and S. incrustans, based on 340 DNA haplotype sequences of independent genetic markers from the nuclear (ITS + 5.8S + D1/D2, RPB2) and mitochondrial (ATP6) genomes for 98 population samples. By characterising the genetic population structure within these species, we provide insights into species boundaries and the possible factors responsible for genetic diversity at a regional geographic scale. Results We found that recombination events are relatively common between natural populations within Sebacina epigaea and S. incrustans, and play a significant role in generating intraspecific genetic diversity. Furthermore, we also found that RPB2 and ATP6 genes display higher levels of intraspecific synonymous polymorphism. Phylogenetic and demographic analyses based on nuclear and mitochondrial loci revealed three distinct phylogenetic lineages within of each of the morphospecies S. epigaea and S. incrustans: one major and widely distributed lineage, and two geographically restricted lineages, respectively. We found almost no differential morphological or ecological characteristics that could be used to discriminate between these lineages. Conclusions Our results suggest that recombination and negative selection have played significant roles in generating genetic diversity within these morphological species at small geographical scales. Concordance between gene genealogies identified lineages/cryptic species that have evolved independently for a relatively long period of time. These putative species were not associated with geographic provenance, geographic barrier, host preference or distinct phenotypic innovations.

To study the diversity and phylogenetic structure of Sebacinales communities from eight vegetation communities along an altitudinal gradient in the Bavarian Alps (Germany), we analysed 456 thalli or roots of plants. We detected 264 sebacinoid sequences, spanning the intergenic transcribed spacer region, 5.8S and D1/D2 regions of the nuclear rRNA gene, mostly using a nested PCR approach. Based on 97% sequence similarity, 73 Sebacinales molecular taxonomic units were found from 70 host species belonging to 44 plant families. Twenty-six molecular taxonomic units represented singletons, the most frequent of these being restricted exclusively to either wooded or grassland habitats. Although Sebacinales appear to occur in low abundance in plant roots, these microorganisms are phylogenetically diverse and widely spread in the ecosystems studied. Ordination analyses showed that land use, pH and humus content strongly influence the diversity and assembly of Sebacinales. In most cases, Sebacinales communities in ecosystems with extreme soil conditions or intensive land use exhibited significant phylogenetic clustering, whereas in undisturbed plant communities no trend was observed. These results suggest that ecosystem disturbance and environmental forces have an influence on the diversity and structure of Sebacinales community assembly over local and spatial scales.

International audience; Inconspicuous basidiomycetes from the order Sebacinales are known to be involved in a puzzling variety of mutualistic plant-fungal symbioses (mycorrhizae), which presumably involve transport of mineral nutrients. Recently a few members of this fungal order not fitting this definition and commonly referred to as ‘endophytes’ have raised considerable interest by their ability to enhance plant growth and to increase resistance of their host plants against abiotic stress factors and fungal pathogens. Using DNA-based detection and electron microscopy, we show that Sebacinales are not only extremely versatile in their mycorrhizal associations, but are also almost universally present as symptomless endophytes. They occurred in field specimens of bryophytes, pteridophytes and all families of herbaceous angiosperms we investigated, including liverworts, wheat, maize, and the non-mycorrhizal model plant Arabidopsis thaliana. They were present in all habitats we studied on four continents. We even detected these fungi in herbarium specimens originating from pioneering field trips to North Africa in the 1830s/40s. No geographical or host patterns were detected. Our data suggest that the multitude of mycorrhizal interactions in Sebacinales may have arisen from an ancestral endophytic habit by specialization. Considering their proven beneficial influence on plant growth and their ubiquity, endophytic Sebacinales may be a previously unrecognized universal hidden force in plant ecosystems.