Contribution of small RNA pathway components in plant immunity

Abstract

Small RNAs regulate a multitude of cellular processes, including development, stress responses, metabolism, and maintenance of genome integrity, in a sequence-specific manner. Accumulating evidence reveals that host endogenous small RNAs and small RNA pathway components play important roles in plant immune responses against various pathogens, including bacteria, fungi, oomycetes, and viruses. Small-RNA-mediated defense responses are regulated through diverse pathways and the components of these pathways, including Dicer-like proteins, RNA-dependent RNA polymerases, Argonaute proteins, and RNA polymerase IV and V, exhibit functional specificities as well as redundancy. In this review, we summarize the recent insights revealed mainly through the examination of two model plants, Arabidopsis and rice, with a primary focus on our emerging understanding of how these small RNA pathway components contribute to plant immunity.

Fig. 1

Plant small RNAs (sRNAs) and RNA interference pathway components contribute to plant immunity. Plants modulate sRNA pathways upon recognition of pathogen-associated molecular patterns or effectors of pathogens. Each pathway involves a distinct context of sRNA pathway components. FLS2, a flagellin-sensitive receptor kinase; TTSS, type III secretion system; miRNA, microRNA; siRNA, short interfering RNA; viRNA, virus-derived siRNA; DCL, Dicer-like protein; AGO, Argonaute; RDR, RNA-dependent RNA polymerase; nat-siRNA, natural antisense transcript-derived siRNA.

Fig. 2

Role of Argonaute (AGO) proteins in plant immunity. A, MicroRNA (miRNA)/miRNA* pair contributes to plant antibacterial immunity through two distinct AGO proteins, miR393 and miR393b*, which are induced by Pseudomonas syringae pv. tomato infection, specifically associate with AGO1 and AGO2, respectively. The miR393/AGO1 complex contributes to pathogen-associated molecular-pattern-triggered immunity by targeting TRANSPORT INHIBITOR RESPONSE1 (TIR1) and related proteins, thereby suppressing auxin signaling; the miR393*-AGO2 complex targets a Golgi-localized SNARE gene, MEMB12, resulting in increased exocytosis of antimicrobial proteins which directly confer resistance against bacteria. PR1, pathogenesis-related protein 1. B, Hierarchical and synergistic contribution of AGO proteins to plant antiviral immunity. AGO1 acts as a major antiviral RNA slicer in antiviral defense against Cucumber mosaic virus (CMV) and Turnip crinkle virus (TCV), while AGO2 functions as a surrogate of AGO1. AGO5 is known to bind to CMV-derived virus-derived siRNAs (viRNAs), although its function in antiviral defense is not clear. AGO7 has a different mode of action from AGO1 in antiviral defense against TCV. AGO2 mediates viRNA-directed defenses against Potato virus X (PVX) in Arabidopsis. Some DNA viruses are targeted by AGO4 for the methylation of viral DNAs. AGO1-associated 21- and 22-nucleotide viRNAs are also considered to be involved in antiviral defense against DNA viruses. Thickness of the lines indicates relative hierarchical contribution of each AGO protein to antiviral immunity.