Immune Receptors and Co-receptors in Antiviral Innate Immunity in Plants

Abstract

Plants respond to pathogens using an innate immune system that is broadly divided into PTI (pathogen-associated molecular pattern- or PAMP-triggered immunity) and ETI (effector-triggered immunity). PTI is activated upon perception of PAMPs, conserved motifs derived from pathogens, by surface membrane-anchored pattern recognition receptors (PRRs). To overcome this first line of defense, pathogens release into plant cells effectors that inhibit PTI and activate effector-triggered susceptibility (ETS). Counteracting this virulence strategy, plant cells synthesize intracellular resistance (R) proteins, which specifically recognize pathogen effectors or avirulence (Avr) factors and activate ETI. These coevolving pathogen virulence strategies and plant resistance mechanisms illustrate evolutionary arms race between pathogen and host, which is integrated into the zigzag model of plant innate immunity. Although antiviral immune concepts have been initially excluded from the zigzag model, recent studies have provided several lines of evidence substantiating the notion that plants deploy the innate immune system to fight viruses in a manner similar to that used for non-viral pathogens. First, most R proteins against viruses so far characterized share structural similarity with antibacterial and antifungal R gene products and elicit typical ETI-based immune responses. Second, virus-derived PAMPs may activate PTI-like responses through immune co-receptors of plant PTI. Finally, and even more compelling, a viral Avr factor that triggers ETI in resistant genotypes has recently been shown to act as a suppressor of PTI, integrating plant viruses into the co-evolutionary model of host-pathogen interactions, the zigzag model. In this review, we summarize these important progresses, focusing on the potential significance of antiviral immune receptors and co-receptors in plant antiviral innate immunity. In light of the innate immune system, we also discuss a newly uncovered layer of antiviral defense that is specific to plant DNA viruses and relies on transmembrane receptor-mediated translational suppression for defense.

Virus perception at the cell surface: revisiting the roles of receptor‐like kinases as viral pattern recognition receptors

“…In resistant genotypes, however, the resistance (R) proteins specifically recognize, directly or indirectly, the viral effectors, called avirulence (Avr) factors, activating ETI and conferring resistance (13). Adapted from Gouveia et al , .…”

“…The BRASSINOSTEROID INSENSITIVE1 (BRI1)‐ASSOCIATED KINASE 1 (BAK1) functions as a coreceptor that interacts with multiple PAMP‐interacting immune receptors (RLKs and RLPs) to assemble active PTI signalling complexes (Ma et al , ). Like BAK1, other members of the subfamily II of LRR‐RLKs, including SERK1, SERK4/BKK1 (BAK1‐LIKE KINASE 1) and the NUCLEAR SHUTTLE PROTEIN‐INTERACTING KINASE 1 (NIK1), function in antiviral immunity (Gouveia et al , ). Accordingly, inactivation of the PTI regulator BAK1 or BKK1 enhances susceptibility to RNA virus infection, demonstrating that they are required to build an effective defence against RNA viruses in Arabidopsis (Kørner et al ., ; Yang et al , ; Fig.…”

Molecular dialogues between viruses and receptor‐like kinases in plants

“…). Interestingly, recent works have unveiled that a number of RLKs indeed influence plant susceptibility to viruses, in some cases being direct targets of viral proteins (Korner et al , ; Zorzatto et al , ; Gouveia et al , ; Niehl et al , ; Calil and Fontes, ; Carluccio et al , ; Li et al , ; Rosas‐Diaz et al , ); some of these RLKs are well‐known players in plant immunity, while others may exert novel functions in antiviral defence (Fig. ).…”

Perspectives on intracellular perception of plant viruses

“…The first TIR‐NLR cloned was the tobacco N gene, which confers resistance to Tobacco mosaic virus (TMV) (Whitham et al , ). Since the cloning of N , at least 15 NLRs that confer resistance to various viruses have been cloned or identified, many of which encode CC‐NLRs (Gouveia et al , ; Padmanabhan and Dinesh‐Kumar, ).…”