Abstract
The exchange of small RNAs (sRNAs) between hosts and pathogens can lead to gene silencing in the recipient organism, a mechanism termed cross-kingdom RNAi (ck-RNAi). While fungal sRNAs promoting virulence are established, the significance of ck-RNAi in distinct plant pathogens is not clear. Here, we describe that sRNAs of the pathogen Hyaloperonospora arabidopsidis, which represents the kingdom of oomycetes and is phylogenetically distant from fungi, employ the host plant's Argonaute (AGO)/RNA-induced silencing complex for virulence. To demonstrate H. arabidopsidis sRNA (HpasRNA) functionality in ck-RNAi, we designed a novel CRISPR endoribonuclease Csy4/GUS reporter that enabled in situ visualization of HpasRNA-induced target suppression in Arabidopsis. The significant role of HpasRNAs together with AtAGO1 in virulence was revealed in plant atago1 mutants and by transgenic Arabidopsis expressing a short-tandem-target-mimic to block HpasRNAs, that both exhibited enhanced resistance. HpasRNA-targeted plant genes contributed to host immunity, as Arabidopsis gene knockout mutants displayed quantitatively enhanced susceptibility.
Highlights
Plant small RNAs regulate gene expression via the Argonaute (AGO)/RNA-induced silencing complex (RISC), which is crucial for tissue development, stress physiology and activating immunity (Chen, 2009; Huang et al, 2016; Khraiwesh et al, 2012)
We presumed that H. arabidopsidis can produce sRNAs, as sRNA biogenesis genes like RNA-dependent RNA polymerases (RDRs) and Dicer-like (DCL) were discovered in the genome (Bollmann et al, 2016)
The identified HpasRNAs mapped in different amounts to distinct regions of a H. arabidopsidis reference genome including ribosomal RNA, transfer RNA, small nuclear/nucleolar RNA, protein-coding messenger RNA and non-annotated regions (Figure 1—figure supplement 1a)
Summary
Plant small RNAs (sRNAs) regulate gene expression via the Argonaute (AGO)/RNA-induced silencing complex (RISC), which is crucial for tissue development, stress physiology and activating immunity (Chen, 2009; Huang et al, 2016; Khraiwesh et al, 2012). The fungal plant pathogen Botrytis cinerea, secretes sRNAs that hijack the plant AGO/RISC in Arabidopsis, and B. cinerea sRNAs induce host gene silencing to support virulence (Weiberg et al, 2013), a mechanism known as cross-kingdom RNA interference (ck-RNAi) (Weiberg et al, 2015). In fungal-plant interactions, ck-RNAi is bidirectional, as plant-originated sRNAs are secreted into fungal pathogens and trigger gene silencing of virulence genes (Cai et al, 2018; Zhang et al, 2016). It is currently not known, how important ck-RNAi is for pathogen virulence in general and whether other kingdoms of microbial pathogens, such as oomycetes, transfer sRNAs into hosts to support virulence. RISC and that these mobile oomycete sRNAs are crucial for virulence by silencing plant host defence genes
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