Comparative genome analyses of sebacinoid taxa

The sebacinoid orchid mycorrhizal fungus S. vermifera (MAFF 305830) was first isolated from the Australian orchid Cyrtostylis reniformis. This fungus displays similar root colonization strategies as described for P. indica and the ability to establish beneficial interactions with different hosts. Colonization by S. vermifera results in enhanced seed germination and biomass production as well as increased resistance against biotic and abiotic stresses in its experimental hosts barley, Arabidopsis and switchgrass.

To identify and characterize conserved sebacinoid genes as key determinants in the Sebacinales symbioses we used comparative genomics and transcriptomic analyses, by means of RNA-seq technology and microarrays. The genome of S. vermifera was sequenced in cooperation with the DOE Joint Genome Institute (JGI) in Walnut Creek (CA), USA in the frame of the sequencing program “Exploring the genome diversity of mycorrhizal fungi”. Similar to P. indica genome, SNPs with two variants could be identified in the S. vermifera genome assembly suggesting that this fungus is also heterokaryotic. P. indica and S. vermifera are particularly well equipped with genes encoding protein- and carbohydrate-active enzymes, peptidases and lectins that potentially degrade plant cell walls and modify the fungal cell wall. These expanded arsenals are more similar to those of hemibiotrophic and necrotrophic pathogens than to the highly reduced set found in ectomycorrhizal fungi and biotrophic pathogens. The majority of these enzymes are activated in the late colonization stages during barley-P. indica interaction but to a lesser extent in Arabidopsis. Similarly, just few S. vermifera genes encoding glycosyl hydrolases and peptidases are induced during interaction with Arabidopsis, suggesting an extended biotrophic interaction with this host. The global transcriptional responses showed a tightly controlled expression of the lifestyle-associated gene sets during the onset of the symbioses.
Recently, it has been demonstrated by phylogenomic analysis that ectomycorrhizal biotrophy emerged from white rot ancestry and is accompanied by reduction or complete losses in glycoside hydrolases and peroxidases families and by expansion of pectinases and hemicellulases, suggesting adaptation to colonization of living plant cells. We could show by comparative genomics that the sebacinoid hydrolytic machinery is similar to that of white rot saprophytes. The findings provide a significant advance in understanding development of biotrophy in root symbionts and suggest a series of incremental shifts along the continuum from saprotrophy towards biotrophy in the evolution of mycorrhizal association from decomposer fungi.