Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways

RNA on the Attack Plant microbial pathogens often work through protein effectors that are delivered into the plant cells to disrupt critical cellular functions. Weiberg et al. (p. 118; see the Perspective by Baulcombe) have now found that small RNAs (sRNAs) of the fungus Botrytis cinerea can play a similar role. After fungal infection of tomato or Arabidopsis leaves, the plant cells contained a suite of fungal-derived sRNAs. Three sRNAs were found to bind to the plant's own Argonaute protein, thereby silencing the plant's fungal defense genes. A pathogenic fungus delivers small RNA molecules to disable gene regulatory systems in the target plant. [Also see Perspective by Baulcombe] Botrytis cinerea, the causative agent of gray mold disease, is an aggressive fungal pathogen that infects more than 200 plant species. Here, we show that some B. cinerea small RNAs (Bc-sRNAs) can silence Arabidopsis and tomato genes involved in immunity. These Bc-sRNAs hijack the host RNA interference (RNAi) machinery by binding to Arabidopsis Argonaute 1 (AGO1) and selectively silencing host immunity genes. The Arabidopsis ago1 mutant exhibits reduced susceptibility to B. cinerea, and the B. cinerea dcl1 dcl2 double mutant that can no longer produce these Bc-sRNAs displays reduced pathogenicity on Arabidopsis and tomato. Thus, this fungal pathogen transfers “virulent” sRNA effectors into host plant cells to suppress host immunity and achieve infection, which demonstrates a naturally occurring cross-kingdom RNAi as an advanced virulence mechanism.