Cross-kingdom RNAi in plant-oomycete interaction

Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. It remained unknown if other classes of pathogens evolved small RNAs for host immune suppression. Oomycetes comprise devastating plant pathogens and are phylogenetically far distant from fungi. Here, we showed that Arabidopsis thaliana mutants compromised in the AGO1-RISC function including the argonaute (ago)1-27 and ago1-45, resisted infection against the oomycete Hyaloperonospora arabidopsidis, whereas other miRNA biogenesis mutants (se-2, hst-6) are not. We investigated infection-specific small RNAs by next generation sequencing and revealed >100 Arabidopsis AGO1-bound oomycete small RNAs. Plant target genes of these oomycete small RNAs were silenced during infection, including members of the Arabidopsis thaliana With No Lysine(K) (AtWNK) Kinase family, AtWNK2 and AtWNK5. Mutant lines atwnk2-2 and atwnk2-3, and atwnk5-3 exhibited enhanced susceptibility to H. arabidopsidis infection. The evidence of oomycete small RNAs trigger host immunity gene suppression proves that cross-kingdom RNAi is a widespread virulence mechanism among distinct microbial pathogens.