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.

Keywords: ETI; NSP-Interacting kinase 1; PAMP-triggered immunity; PTI; antiviral immunity; effector-triggered immunity; receptor NIK1; resistance genes.

FIGURE 1

Antiviral innate immunity with conserved features with antibacterial and antifungal immune responses. Plant viruses are obligate, biographic parasites and as such their life cycles start with the penetration of the virions in the host cells via wound sites (lightening arrow). Within the host cells, the virion is disassembled and then host cells mediate the expression of the viral genome by providing a translation apparatus for all viruses and transcription machinery for DNA viruses (Figure 2). The viral mRNAs are translated into the cytoplasm, producing at least three viral proteins absolutely required for completion of the viral life cycle, replication protein (Rep), movement protein (MP) and coat protein (CP). The viral replication proteins combine with cellular proteins to produce multiple copies of the virus genome. These newly made genomes interact with CPs to form new virions or viral ribonucleoprotein complexes (vRNP). The next step is movement of the virus into neighboring cells, which requires the MP. The intracellular translated viral proteins (Avr) may also provide recognition sites for cytosolic NB-LRR receptors (e.g., R proteins), triggering ETI, which results in HR, necrosis or SAR similarly to non-viral ETI. R proteins, R co-factors (CF) and Avr factors form an interacting complex with the SGT1/RAR1/HSP90, and EDS1/PAD4/SAG101 modules to mediate downstream changes in SA, JA, ET, NO and H₂O₂ levels or signaling via MAP Kinases cascades, culminating in the induction of defense genes. NPR1 complexes TF to induce defense genes via SA signaling, whereas EIN2 is a regulator of ET signaling. Virus infection may also trigger epigenetic changes. At the first line of defense, replication of viral RNA genomes may provide non-self RNA motifs (ssRNA or dsRNA) as virus-derived PAMPs to activate PTI. Alternatively, plant cells may sense viral infection and secrete plant-derived DAMPs, recognized by PRRs extracellularly. Members of the SERK family also function as co-receptors in viral PTI. Arrows denote unknown or putative paradigms in viral innate immunity. Adapted from Mandadi and Scholthof (2013).

FIGURE 2

Similarities between viral PTI and NIK1-mediated antiviral signaling. Replication and expression of viral genomes lead to the accumulation of non-self DNA or RNA motifs (virus-derived PAMPs), which may be recognized by PRRs that in turn heteromultimerize with co-receptors (BAK1 or SERK1) to trigger viral PTI. Alternatively, PTI may be activated by endogenous DAMPs, which are induced by virus infection and delivered to the apoplast via the secretory apparatus. In addition to PTI, in the case of DNA viruses (begomoviruses), plant cells may also elicit the translational control branch of the NIK1-mediated antiviral signaling as an innate defense. The mechanism of NIK1 transmembrane receptor activation is unknown. Structural organization and biochemical properties of NIK1 may suggest an activation mechanism dependent on recognition of viral PAMPs or endogenous DAMPs by PRR partners, similarly to a typical viral PTI. In this case, one may consider virus derived-dsDNA as possible PAMPs. The viral single-stranded DNA form begomoviruses 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 MP to transport the viral DNA to the adjacent, uninfected cells. Activation of NIK1 in incompatible interactions promotes phosphorylation and subsequent translocation of RPL10 to the nucleus, where it interacts with LIMYB to fully repress the expression of RP genes, leading to global translation suppression, which also impairs viral mRNA (vmRNA) translation. In begomovirus-host compatible interactions, NSP binds to NIK1 and suppresses its activity. In any case, RNA or DNA viruses, a successful infection implicates in accumulation of virus effectors (for example, CP from PPV and NSP from begomoviruses) 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. Adapted from Machado et al. (2015).