Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi

Abstract

Pathogens secrete effector proteins to suppress host immune responses. Recently, we showed that an aggressive plant fungal pathogen Botrytis cinerea can also deliver small RNA effectors into host cells to suppress host immunity. B. cinerea sRNAs (Bc-sRNAs) translocate into host plants and hijack the plant RNAi machinery to induce cross-kingdom RNAi of host immune responsive genes. Here, we functionally characterized another Bc-sRNA effector Bc-siR37 that is predicted to target at least 15 Arabidopsis genes, including WRKY transcription factors, receptor-like kinases, and cell wall-modifying enzymes. Upon B. cinerea infection, the expression level of Bc-siR37 was induced, and at least eight predicted Arabidopsis target genes were downregulated. These target genes were also suppressed in the transgenic Arabidopsis plants overexpressing Bc-siR37, which exhibited enhanced disease susceptibility to B. cinerea. Furthermore, the knockout mutants of the Bc-siR37 targets, At-WRKY7, At-PMR6, and At-FEI2, also exhibited enhanced disease susceptibility to B. cinerea, giving further support that these genes indeed play a positive role in plant defense against B. cinerea. Our study demonstrates that analysis of pathogen sRNA effectors can be a useful tool to help identify host immunity genes against the corresponding pathogen.

Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection

“…Upon infection, B. cinerea delivers a group of sRNAs into host plant cells. These transferred sRNAs are loaded into the host Arabidopsis AGO1 protein to silence host immunity genes, such as mitogen activated protein kinases (MAPKs) and a cell wall associated kinase, etc [35-37]. It has been long known that pathogens deliver effectors, mostly proteins, into host cells to suppress host immunity [38].…”

“…It has been long known that pathogens deliver effectors, mostly proteins, into host cells to suppress host immunity [38]. These sRNAs from B. cinerea function as a novel class of pathogen effectors [35,37], which have the characteristic features that allow them to be loaded into host Arabidopsis AGO1 protein. Consistent with this finding, B. cinerea causes much less disease symptoms on the Arabidopsis ago1-27 mutant compared to wild type plants because sRNA effectors could no longer function without host AGO1 [35,37].…”

“…These sRNAs from B. cinerea function as a novel class of pathogen effectors [35,37], which have the characteristic features that allow them to be loaded into host Arabidopsis AGO1 protein. Consistent with this finding, B. cinerea causes much less disease symptoms on the Arabidopsis ago1-27 mutant compared to wild type plants because sRNA effectors could no longer function without host AGO1 [35,37]. Less severe disease symptoms were also observed on Arabidopsis ago1-27 mutants infected with another fungal pathogen, Verticillium dahliae , which causes Verticillium wilt disease on many plants [39,40].…”

RNA-based disease control as a complementary measure to fight Fusarium fungi through silencing of the azole target Cytochrome P450 Lanosterol C-14 α-Demethylase

“…Some sRNA effectors can target multiple host defence genes to enhance Bc pathogenicity. For example, Bc-siR37 suppresses host immunity by targeting at least 15 Arabidopsis genes, including WRKY transcription factors, receptor-like kinases, and cell wall-modifying enzymes (Wang et al 2017a). Bc sRNAs utilize the host RNAi machinery by binding to Arabidopsis ARGONAUTE1 (AGO1) to silence host defense genes.…”

RNA as a means of inter-species communication and manipulation: Progresses and shortfalls

“…Regulation of host genes by pathogens mediated by small ncRNAs (sncRNAs) has been a recent topic of interest in hostpathogen interactions. Wang et al 4 found that a small RNA, Bc-siR37, produced by the plant pathogenic fungus, Botrytis cinerea, is translocated into the host plant, Arabidopsis, suppressing at least 8 host genes, some of which appear to play a role in plant defense against the fungus. While this finding is not the first instance of a sncRNA effector shown to regulate a host gene in plant or animal hosts, it further supports the role of sncRNAs in inter-kingdom communications between hosts and pathogens.…”