Fungal Small RNAs Suppress Plant Host Immunity by Hijacking Host RNAi Machinery

Small RNAs are a class of short non-coding regulators that mediate gene silencing by loading into Argonaute protein (AGO) to target complementary genes. Small RNAs have been shown to play an important role in host-microbial interaction.

In fungi, studies in the fission yeast and Neurospora crassa revealed functions of small RNAs in genome defense, heterochromatin formation, and gene regulation. However, it has not been demonstrated that small RNAs or RNAi are directly involved in pathogenicity.

Genome-wide small RNA profiling on an aggressive fungal pathogen Botrytis cinerea-infected Arabidopsis and tomato identified a group of small RNAs from Botrytis cinerea that can potentially target important regulatory genes in plant hosts, including Arabidopsis and tomato. Genetic and biochemical studies have demonstrated that some B. cinerea small RNAs (Bc-sRNAs) can hijack the host RNA interference (RNAi) machinery by loading into Arabidopsis Argonaute 1 (AGO1) to selectively silence host immunity genes. These small RNAs are largely generated from transposon regions, such as LTRs, which are the hot spots undergoing rapid evolution. Many fungal or oomycete protein effector genes are also enriched in the transposon regions, including LTRs. Here, we demonstrate that a fungal pathogen transfers “virulent” sRNA effectors into host cells to achieve infection, which reveals a naturally occurring cross-kingdom RNAi as an advanced virulence mechanism.

Funding support: NSF Career, NSF IOS, and NIH R01 to H. Jin.