Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum

Abstract

The most frequently encountered symbiont on tree roots is the ascomycete Cenococcum geophilum, the only mycorrhizal species within the largest fungal class Dothideomycetes, a class known for devastating plant pathogens. Here we show that the symbiotic genomic idiosyncrasies of ectomycorrhizal basidiomycetes are also present in C. geophilum with symbiosis-induced, taxon-specific genes of unknown function and reduced numbers of plant cell wall-degrading enzymes. C. geophilum still holds a significant set of genes in categories known to be involved in pathogenesis and shows an increased genome size due to transposable elements proliferation. Transcript profiling revealed a striking upregulation of membrane transporters, including aquaporin water channels and sugar transporters, and mycorrhiza-induced small secreted proteins (MiSSPs) in ectomycorrhiza compared with free-living mycelium. The frequency with which this symbiont is found on tree roots and its possible role in water and nutrient transport in symbiosis calls for further studies on mechanisms of host and environmental adaptation.

Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists

“…(). Genes and gene clusters involved in secondary metabolism were predicted for the 60 species using a pipeline based on Smurf (Peter et al ., ). Potential transporters were predicted using the Transport TP online tool (http://bioinfo3.noble.org/transporter/; Li et al ., ).…”

Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis?

“…Another striking and convergent trait in ECM and AM fungal genomes is the very small repertoire of genes encoding enzymes involved in plant cell wall degradation (PCWDEs) and secondary metabolism (Martin et al, 2016;Kamel et al, 2017). Phylogenomics indicates that the small repertoire of PCWDEs in the genome of ECM fungi, which evolved repeatedly and independently from diverse ancestral saprotrophs in both Basidiomycetes and Ascomycetes, is the consequence of substantial gene loss (Kohler et al, 2015;Peter et al, 2016), and the same evolutionary trend is probably also true for AM fungi. Gene loss may occur when a gene becomes dispensable because of functional redundancy, or when it is no longer needed because the organism lost the physiological requirement in which the gene was involved (i.e.…”

“…Gene loss is very well documented for microbes that specialised as obligate biotrophs, with extremely reduced genomes being reported for bacteria living in association with different eukaryotes (McCutcheon & Moran, 2012). The same is true for fungi, even though the lower gene content may be concealed in a large genome by a high proportion of repetitive elements (Peter et al, 2016). Extensive loss of genes encoding CAZymes and key enzymes in secondary metabolism characterises the genome of many specialised biotrophic plant pathogens (Kemen et al, 2011;Spanu, 2012).…”

The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics

“…Tuber melanosporum (Martin et al ., ); Cenococcum geophilum (Peter et al ., )) and Glomeromycotina (see Part II). An additional shared evolutionary feature of mycorrhizal fungal genomes is the induction of MiSSP gene expression upon symbiosis (Martin et al ., ; Kohler et al ., ; Peter et al ., ). As shown in R. irregularis (see Part II), MiSSPs can modulate the host gene expression and dampen defence reactions triggered by root colonization.…”