Fusarium oxysporum f. sp. cepae small RNAs (Foc-sRNAs) promote disease susceptibility in onion (Allium cepa L.) through cross kingdom RNA interference

Fusarium basal rot (FBR) caused by Fusarium oxysporum f. sp. cepae (Foc), is one of the most vicious fungal phytopathogen infecting onion and allied crops across the world. Small RNAs (sRNAs) are important pathogenicity factor in various fungal phytopathogens that impairs host immune responses. However, the sRNA repertoire from Foc and their roles in onion-Foc interaction is not clear yet. Here, we performed genome-wide small-RNA profiling of Foc post infection of onion and detected three Foc-sRNAs (Fx-sR3, Fx-sR4 and Fx-sR9) that were significantly induced in Foc sensitive onion genotype. Co-transformation assay showed that Foc-sRNAs facilitate cross-kingdom RNA interference (RNAi) cleaving the onion defense genes encoding NLR class R protein, LRR-receptor kinase and F-box transcription factor. Inhibition of the Foc-sRNAs resulted in an increased onion resistance, while knockdown of the targeted defense genes increased the susceptibility of onion to FBR infection. This suggest that Foc-sRNAs represses the host immune response by suppressing the expression of the three targeted immunity specific genes. All together, we propose that Foc-sRNAs are central factors of Foc pathogenicity, and could suppress host immunity by acting as effectors. Our results revealed significant understandings into the pathogenicity of FBR infection in onion.