Key Points
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Coevolution between plants and pathogens has given rise to a large variety of defence pathways and counter-acting virulence pathways. Plant resistance against bacterial and fungal pathogens is largely mediated by a first layer of basal resistance and a second layer of strong race-specific resistance; successful pathogens have evolved effector molecules to suppress both layers of defence. Analogously, virus resistance is mediated broadly by RNA silencing and also by race-specific resistance.
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Viruses actively suppress RNA silencing, which alleviates anti-viral defence but also disrupts endogenous host gene regulation through microRNAs and small-interfering RNAs. Virulent infections thus cause disease partly through disrupting host silencing, while viruses unable to suppress silencing fail to replicate in healthy plants.
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RNA silencing actively contributes to defence against bacterial and eukaryotic pathogens as well, through regulation of host gene expression. These non-viral pathogens have consequently evolved silencing suppressors that contribute to disease.
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Recent work has revealed a crucial role for multiple aspects of host silencing in repressing race-specific defence responses. Thus, resistance and defence-promoting genes are silenced by miRNAs, siRNAs and/or epigenetically through DNA methylation.
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Silencing suppressors deployed by pathogens therefore prevent the first layer of defence responses, but relieve repression of strong race-specific resistance mechanisms, which can contribute to increased host resistance.
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This review synthesizes the intricate interplay between plant resistance pathways, RNA silencing and its manipulation by pathogens.
Abstract
RNA silencing is a central regulator of gene expression in most eukaryotes and acts both at the transcriptional level through DNA methylation and at the post-transcriptional level through direct mRNA interference mediated by small RNAs. In plants and invertebrates, the same pathways also function directly in host defence against viruses by targeting viral RNA for degradation. Successful viruses have consequently evolved diverse mechanisms to avoid silencing, most notably through the expression of viral suppressors of RNA silencing. RNA silencing suppressors have also been recently identified in plant pathogenic bacteria and oomycetes, suggesting that disruption of host silencing is a general virulence strategy across several kingdoms of plant pathogens. There is also increasing evidence that plants have evolved specific defences against RNA-silencing suppression by pathogens, providing yet another illustration of the never-ending molecular arms race between plant pathogens and their hosts.
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Acknowledgements
Work in the O.V. group is supported by a core grant from ETH-Z, Advanced Researcher grant 'Frontiers of RNAi-II' (No. 323071), from the European Research Council, and a grant from the Swiss National Foundation (No. 31003A_132907). N.P. received support from an EMBO Long-Term Fellowship and a Marie-Curie Actions Incoming International Fellowship.
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FURTHER INFORMATION
Glossary
- Pathogen-associated molecular patterns
-
(PAMPs; alternatively, microorganism-associated molecular patterns). Conserved and essential pathogen signature molecules that include flagellin, lipopoly-saccharide, elongation factors and double-stranded RNA.
- Oomycetes
-
Eukaryotic fungal-like organisms of the kingdom Stramenopila that include the causal agent of the Irish potato famine, Phytophthora infestans.
- Viral suppressors of RNA silencing
-
(VSRs). Proteins encoded by viruses that function as virulence factors by inhibiting post-transcriptional gene silencing pathways in plants and invertebrates.
- MicroRNA
-
(miRNA). Discrete 21- or 22-nucleotide small RNAs, arising from genome-encoded imperfect foldback structures processed by DCL1, which negatively regulate endogenous target mRNAs by complementary base-pairing.
- Repeat-associated small interfering RNA
-
(rasiRNA). 24-nucleotide small interfering RNAs generated from genomic repeats and transposon loci by DCL3, which target DNA methylation and chromatin modification at their loci of origin.
- Trans-acting siRNA
-
(tasiRNA). 21-nucleotide small interfering RNAs produced by sequential processing by DCL4 on long, perfectly complementary double-stranded RNA.
- hrcC
-
A mutant of Pseudomonas syringae pv. tomato that lacks a functional type III secretion system, thus making it unable to deliver virulence effectors into its host.
- Type III secretion system
-
(T3SS). A delivery system encoded by a wide range of Gram-negative bacterial pathogens of plants and animals that is used to inject effector proteins into host cells.
- Avirulent
-
A pathogen that elicits a specific effector-triggered immunity response owing to recognition of one of its virulence factors by a cognate host-encoded resistance gene, resulting in an incompatible interaction.
- SNARE
-
Soluble NSF (N-ethylmaleimide-sensitive factor) attachment protein (SNAP) receptor, which regulates secretory vesicle fusion.
- PATHOGENESIS-RELATED 1
-
(PR1). A secreted protein with suspected antimicrobial functions. It is used as a classic defence marker owing to its strong induction during pathogen challenge.
- Hypersensitive response
-
(HR). A specific form of programmed cell death, often induced by effector-triggered immunity and correlated with accumulation of antimicrobial compounds and systemic acquired resistance.
- Bacterial suppressors of RNA silencing
-
(BSRs). Effector molecules used by bacterial pathogens to alter host post-transcriptional gene silencing or, possibly, transcriptional gene silencing.
- Chromocentres
-
Densely packed heterochromatic (silenced) DNA including pericentromeric regions, transposons and repetitive elements.
- Salicylic acid
-
A central plant hormone signal that induces local and systemic defence responses, including systemic acquired resistance.
- Biotrophic
-
Organisms that complete their life cycle on living plant tissue; such organisms actively prevent host cell death.
- Necrotrophic
-
Organisms that kill host cells before invasion and gain nutrients from the dead plant tissue.
- Jasmonic acid
-
A phytohormone that regulates defence against necrotrophic pathogens and herbivores.
- Helitron
-
A DNA transposon that is commonly subjected to repressive DNA methylation and that transposes through rolling circle DNA replication.
- Extreme resistance
-
A plant defence response against viruses that is elicited by effector-triggered immunity. It differs from the hypersensitive response in that it restricts viral accumulation without cell death.
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Pumplin, N., Voinnet, O. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11, 745–760 (2013). https://doi.org/10.1038/nrmicro3120
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DOI: https://doi.org/10.1038/nrmicro3120
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