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Roles of RNA silencing in viral and non-viral plant immunity and in the crosstalk between disease resistance systems

Abstract

RNA silencing is a well-established antiviral immunity system in plants, in which small RNAs guide Argonaute proteins to targets in viral RNA or DNA, resulting in virus repression. Virus-encoded suppressors of silencing counteract this defence system. In this Review, we discuss recent findings about antiviral RNA silencing, including the movement of RNA through plasmodesmata and the differentiation between plant self and viral RNAs. We also discuss the emerging role of RNA silencing in plant immunity against non-viral pathogens. This immunity is mediated by transkingdom movement of RNA into and out of the infected plant cells in vesicles or as extracellular nucleoproteins and, like antiviral immunity, is influenced by the silencing suppressors encoded in the pathogens’ genomes. Another effect of RNA silencing on general immunity involves host-encoded small RNAs, including microRNAs, that regulate NOD-like receptors and defence signalling pathways in the innate immunity system of plants. These RNA silencing pathways form a network of processes with both positive and negative effects on the immune systems of plants.

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Fig. 1: The various antiviral RNA silencing pathways.
Fig. 2: Modes of action of viral suppressors of RNA silencing.
Fig. 3: Strategies for attaining RNA silencing specificity towards viral RNA.
Fig. 4: Small RNA movement in symbiotic (pathogenic or mutualistic) interactions.
Fig. 5: Layers of defence in plants.
Fig. 6: RNA silencing integrates different layers of the plant immune system.

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Acknowledgements

The authors’ research has been supported by European Research Council Advanced Investigator grant ERC-2013-AdG 340642 (Transgressive Inheritance in Plant Breeding and Evolution (TRIBE)), the Royal Society (RP170001), the Balzan Foundation, the Biological Sciences and Biotechnology Research Council (BB/R018529/1) and the Broodbank Fund. S.L.-G. is a Senior Broodbank Research Fellow. D.C.B. is the Royal Society Edward Penley Abraham Research Professor.

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Glossary

Virulence

A quantitative measure of the degree of pathogenicity; it corresponds with the extent to which the pathogen accumulates in the infected host. There is often a correlation between virulence and the severity of disease.

DNA viruses

Viruses affecting plants that have DNA genomes. They are divided in two groups: geminiviruses, whose genome is replicated as DNA, and pararetroviruses, in which replication involves an RNA phase and is performed by reverse transcriptase.

Retrotransposons

Virus-like transposable elements, whose replication involves reverse transcriptase. Retrotransposons are integrated into the plant nuclear genome but have extrachromosomal phases and, unlike retroviruses, do not have an envelope gene.

Plasmodesmata

Membrane channels in which the plasma membranes of adjacent plant cells are fused. These structures span the cell wall and are the conduit for movement between cells of metabolites, macromolecules, viruses and viroids.

Replication intermediates of RNA viruses

Double-stranded RNA molecules, usually of transient existence, formed by a virus-encoded RNA-dependent RNA polymerase as part of the virus replication process.

Satellite RNA

Coding or non-coding RNA that is replicated by RNA polymerases of the helper viruses and that is transmitted between host organisms as part of the helper virus particles. It is not part of the virus genome and has a distinct nucleotide sequence identity.

Autophagy

The processes by which cells degrade and recycle their components, including proteolytic mechanisms that are specifically targeted.

Mycorrhizal

Refers to mutualistic symbioses in which fungi colonize the roots of plants. The plant provides photosynthate-derived nutrients for the fungus and the fungus mobilizes and transports mineral nutrients to the plant.

Target mimic RNA

RNA designed to bind and sequester microRNAs. A target mimic typically has base-pairing mismatches with the microRNA, which prevent Argonaute (AGO) from cleaving the target mimic, thereby permanently inactivating the microRNA.

NOD-like receptors

(NLRs). Cellular receptors of pathogen-derived factors. Direct or indirect interaction of these factors with NLRs results in effector-triggered immunity, most likely by stimulating components of the pathogen-associated molecular pattern-triggered immunity pathway.

Plasmalemma

The lipid-bilayer membrane bounding a cell, inside the cell wall.

Membrane tubules

Paramural tubules of fungal origin associated with mutualistic and pathogenic fungal symbionts of plants. They may be associated with molecular exchanges between the two interacting organisms.

P-loop motif

The phosphate-binding loop or Walker A motif is common in nucleoside triphosphate-binding proteins. It is rich in Gly, with conserved Lys and Ser or Thr.

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Lopez-Gomollon, S., Baulcombe, D.C. Roles of RNA silencing in viral and non-viral plant immunity and in the crosstalk between disease resistance systems. Nat Rev Mol Cell Biol (2022). https://doi.org/10.1038/s41580-022-00496-5

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