In addition, the Dicer (DCL) double mutant strain Bc-dcl1dcl2 can no longer produce these Bc-sRNAs also displays much reduced pathogenicity on various plant species, indicating that sRNA effectors are essential for Bcs pathogenicity. Consistent with this finding, Bc causes less disease symptoms on the Arabidopsis ago1–27 mutant compared to wild type plants. ![]() The Bc sRNAs utilize the host RNAi machinery by binding to Arabidopsis ARGONAUTE1 (AGO1) to silence host immunity genes. 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. ![]() Some sRNA effectors can target multiple host immunity genes to enhance Bc pathogenicity. The grey mold fungal pathogen Botrytis cinerea ( Bc) produces sRNA effectors, the majority of which derived from clusters within long-terminal repeat (LTR) retrotransposons in the fungal genome, which can migrate into and down-regulate Arabidopsis and tomato genes involved in immunity. Pathogen-derived sRNAs can move into host cells to suppress host immunity ( Figure 1a). Pathogen-derived cross-kingdom sRNAs suppressing host immunity We review here the current understanding and application of cross-kingdom RNA trafficking and environmental RNAi. These mechanisms enable us to successfully control crop diseases by transgene-mediated cross-kingdom RNAi or spray-induced gene silencing (SIGS) that spraying pathogen gene-targeting dsRNAs and sRNAs on plant surfaces to suppress pathogen virulence. The novel strategy employs the recent discoveries that sRNAs can move across the cellular boundaries between hosts and interacting pathogens and pests and induce gene silencing in trans, designated ‘cross-kingdom RNA interference (RNAi)’ and that some pathogens and pests are capable of taking up RNAs from the environment, termed ‘environmental RNAi’. The demonstration that eukaryotic pathogens and pests are inhibited by small RNAs (sRNAs) targeting their essential and/or pathogenicity genes has raised the possibility that plants can be protected by a new generation of eco-friendly RNA-based fungicides or insecticides, which are highly specific and can be easily adapted to control multiple diseases simultaneously. Each year, pathogens and pests destroy 20–40% of attainable crop production globally. To meet the increasing food and energy demands of a fast-growing population, it will be necessary to roughly double crop yields worldwide over the next 40–50 years. ![]() This review summarizes the current understanding of cross-kingdom RNA trafficking and environmental RNAi and how these findings can be developed into novel effective strategies to fight diseases caused by microbial pathogens and pests. To circumvent transgenic approaches, direct application of dsRNAs or sRNAs (environmental RNAi) onto host plants or post-harvest products leads to silencing of the target microbe/pest gene (referred to spray-induced gene silencing, SIGS) and confers efficient disease control. Exploiting this new knowledge, host-induced gene silencing (HIGS) by transgenic expression of pathogen gene-targeting double-stranded (ds)RNA has the potential to become an important disease-control method. Strikingly, recent evidence supports that some sRNAs can travel between interacting organisms and induce gene silencing in the counter party, a mechanism termed cross-kingdom RNAi. Similarly, sRNAs from pathogens and pests also play an important role in modulating their virulence. In plants, small RNA (sRNA)-mediated RNA interference (RNAi) is critical for regulating host immunity against bacteria, fungi, oomycetes, viruses, and pests.
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