Sugarcane smut caused by Sporisorium scitamineum is a destructive disease responsible for significant losses in sugarcane production worldwide. However, the mechanisms underlying the pathogenicity of this fungus remain largely unknown. In this study, we found that the disruption of the SsRSS1 gene, which encodes a salicylic acid (SA) sensing regulator, does not affect phenotypic traits such as the morphology, growth rate, and sexual mating ability of haploid basidiospores, but rather reduces the tolerance of basidiospores to SA stress by blocking the induction of SsSRG1, a gene encoding a SA response protein in S. scitamineum. SsRSS1 deletion resulted in the attenuation of the virulence of the fungus. In addition to a significant reduction in whip formation, a portion of plantlets (18.3%) inoculated with the ΔSsRSS1 strains were found to be infected but failed to produce whips for up to 90 days post-inoculation. However, the development of hyphae and teliospore from the ΔSsRSS1-infected plants that formed whips seemed indistinguishable from that in the wild-type-infected plants. Combined, our findings suggested that SsRss1 is required for maintaining fungal fitness in planta by counteracting SA stress.

The basidiomycetous fungus Sporisorium scitamineum causes sugarcane smut that leads to severe economic losses in the major sugarcane growing areas in China, India and Brazil, etc.  Autophagy is a conserved pathway in eukaryotes for bulk degradation and cellular recycling, and was shown to be important for fungal cell growth, development, and pathogenicity.  However, physiological function of autophagy has not been studied in S. scitamineum.  In this study, we identified a conserved Atg8 protein, named as SsAtg8 and characterized its function. Our results showed that autophagy was blocked in the ssatg8Δ mutant, in nitrogen starvation.  The ssatg8Δ mutant formed pseudohypha frequently and was hypersensitive to oxidative stress.  However, mating or filamenation was unaffected in the ssatg8Δ mutant in vitro.  Overall we demonstrate that autophagy is dispensable for S. scitamineum mating/filamentation, while critical for oxidative stress tolerance and proper morphology in sporidial stage.