Plant immunity against viruses: antiviral immune receptors in focus

Abstract

Background: Among the environmental limitations that affect plant growth, viruses cause major crop losses worldwide and represent serious threats to food security. Significant advances in the field of plant-virus interactions have led to an expansion of potential strategies for genetically engineered resistance in crops during recent years. Nevertheless, the evolution of viral virulence represents a constant challenge in agriculture that has led to a continuing interest in the molecular mechanisms of plant-virus interactions that affect disease or resistance.

Scope and conclusion: This review summarizes the molecular mechanisms of the antiviral immune system in plants and the latest breakthroughs reported in plant defence against viruses. Particular attention is given to the immune receptors and transduction pathways in antiviral innate immunity. Plants counteract viral infection with a sophisticated innate immune system that resembles the non-viral pathogenic system, which is broadly divided into pathogen-associated molecular pattern (PAMP)-triggered immunity and effector-triggered immunity. An additional recently uncovered virus-specific defence mechanism relies on host translation suppression mediated by a transmembrane immune receptor. In all cases, the recognition of the virus by the plant during infection is central for the activation of these innate defences, and, conversely, the detection of host plants enables the virus to activate virulence strategies. Plants also circumvent viral infection through RNA interference mechanisms by utilizing small RNAs, which are often suppressed by co-evolving virus suppressors. Additionally, plants defend themselves against viruses through hormone-mediated defences and activation of the ubiquitin-26S proteasome system (UPS), which alternatively impairs and facilitates viral infection. Therefore, plant defence and virulence strategies co-evolve and co-exist; hence, disease development is largely dependent on the extent and rate at which these opposing signals emerge in host and non-host interactions. A deeper understanding of plant antiviral immunity may facilitate innovative biotechnological, genetic and breeding approaches for crop protection and improvement.

Keywords: Antiviral immunity; LRR-RLK; NBS-LRR resistance protein; NIK-mediated translation suppression; NSP-interacting kinase; PAMP-triggered immunity; antiviral RNA silencing; antiviral immune receptors; effector-triggered immunity; hormone-mediated defence; proteasome degradation; receptor-like kinase.

Fig. 1.

Antiviral innate immunity in plants. (A) PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI) in virus–host interactions. During viral infection, the replication and expression of the viral genome lead to the accumulation of virus-derived nucleic acids with features of pathogen-associated molecular patterns (PAMPs), which may be recognized by host pattern recognition receptors (PRRs) that, in turn, heterooligomerize with co-receptors, such as BAK1 and BKK1, to trigger PTI. Alternatively, PTI may be activated upon PRR recognition of damage-associated molecular patterns (DAMPs), which are induced by infection and delivered to the apoplast by the host cells via the secretory apparatus. In a successful infection, expression of the viral genome results in accumulation of virus effectors to suppress PTI, leading to disease. In resistant genotypes, however, the resistance genes specifically recognize, directly or indirectly, the viral effectors, called avirulence (Avr) factors, activating ETI and conferring resistance. (B) The translational control arm of the NIK1-mediated signalling in antiviral innate immunity. Virus infection-induced oligomerization of NIK1 promotes transphosphorylation at the crucial Thr474, activating the kinase. Alternatively, NIK1 interacts with an unknown ligand-binding LRR-RLK in a stimulus-dependent manner. Although viral infection triggers NIK1-mediated antiviral signalling, the molecular basis of this elicitation is unknown and may be either intracellular virus-derived nucleic acid PAMPs or endogenous DAMPs released in the apoplasts by the host cells. Upon activation, NIK1 indirectly mediates the RPL10 phosphorylation, promoting its translocation to the nucleus, where it interacts with LIMYB to down-regulate the expression of translation-related genes. Therefore, the propagation of the antiviral signal culminates with suppression of host global protein synthesis, which also impairs translation of viral mRNA, as a defence mechanism. In begomovirus–host compatible interactions, the binding of begomovirus NSP to the NIK1 kinase domain (A-loop) inhibits autophosphorylation at Thr474, thereby preventing receptor kinase activation and RPL10 phosphorylation, overcoming this layer of defence. The viral single-stranded DNA replicates via double-stranded DNA intermediates that are transcribed in the nucleus of plant-infected cells. NSP binds to the nascent viral DNA and facilitates its movement to the cytoplasm and acts in concert with the classical movement protein MP to transport the viral DNA to the adjacent, uninfected cells.

Fig. 2.

Adaptive antiviral immunity in plants: general model of antiviral RNA silencing and its suppression by viral suppressors of RNA silencing (VSRs). The Silencing response is triggered by viral dsRNA molecules (vsRNA, ds-siRNA, 21, 22 rr 24 nt) from different sources, which are produced by Dicer-like proteins (DCLs). These vsRNAs are subsequently loaded into Argonaute (AGO)-containing silencing complexes. In post-transcriptional gene silencing (PTGS), viral RNA is targeted by the RNA-induced silencing complex (RISC) for degradation or translational repression, while the RNA-induced transcriptional silencing complex (RITS) causes histone and/or DNA methylation, leading to transcriptional gene silencing (TGS). The effector phase can also result in the amplification of silencing response through the action of RNA-dependent RNA polymerase (RDR) proteins, which produce more dsRNA substrates for DCL processing. VSRs can target multiple steps of the RNA silencing pathway, defeating host antiviral mechanisms by interfering in dicing, vsRNA loading, AGO activation and amplification.