A fungal RNA-dependent RNA polymerase is a novel player in plant infection and cross-kingdom RNA interference

PLoS Pathog. 2023 Dec 20;19(12):e1011885. doi: 10.1371/journal.ppat.1011885. eCollection 2023 Dec.

Abstract

Small RNAs act as fungal pathogen effectors that silence host target genes to promote infection, a virulence mechanism termed cross-kingdom RNA interference (RNAi). The essential pathogen factors of cross-kingdom small RNA production are largely unknown. We here characterized the RNA-dependent RNA polymerase (RDR)1 in the fungal plant pathogen Botrytis cinerea that is required for pathogenicity and cross-kingdom RNAi. B. cinerea bcrdr1 knockout (ko) mutants exhibited reduced pathogenicity and loss of cross-kingdom small RNAs. We developed a "switch-on" GFP reporter to study cross-kingdom RNAi in real-time within the living plant tissue which highlighted that bcrdr1 ko mutants were compromised in cross-kingdom RNAi. Moreover, blocking seven pathogen cross-kingdom small RNAs by expressing a short-tandem target mimic RNA in transgenic Arabidopsis thaliana led to reduced infection levels of the fungal pathogen B. cinerea and the oomycete pathogen Hyaloperonospora arabidopsidis. These results demonstrate that cross-kingdom RNAi is significant to promote host infection and making pathogen small RNAs an effective target for crop protection.

MeSH terms

  • Arabidopsis* / genetics
  • Arabidopsis* / microbiology
  • Botrytis / genetics
  • Plant Diseases / genetics
  • Plant Diseases / microbiology
  • Plants / genetics
  • RNA Interference
  • RNA, Fungal / genetics
  • RNA, Plant
  • RNA, Small Interfering / genetics
  • RNA-Dependent RNA Polymerase* / genetics
  • Virulence / genetics

Substances

  • RNA, Small Interfering
  • RNA-Dependent RNA Polymerase
  • RNA, Fungal
  • RNA, Plant

Grants and funding

AW received funding for this study from the German Research Foundation (DFG, www.dfg.de), grant award no. WE5707/2-1 as part of the Research Unit FOR5116. The funder did not play any role in the study design, data collection and analysis, decision to publish, or presentation of the manuscript.