Plum pox virus capsid protein suppresses plant pathogen‐associated molecular pattern (PAMP)‐triggered immunity

Abstract

The perception of pathogen-associated molecular patterns (PAMPs) by immune receptors launches defence mechanisms referred to as PAMP-triggered immunity (PTI). Successful pathogens must suppress PTI pathways via the action of effectors to efficiently colonize their hosts. So far, plant PTI has been reported to be active against most classes of pathogens, except viruses, although this defence layer has been hypothesized recently as an active part of antiviral immunity which needs to be suppressed by viruses for infection success. Here, we report that Arabidopsis PTI genes are regulated upon infection by viruses and contribute to plant resistance to Plum pox virus (PPV). Our experiments further show that PPV suppresses two early PTI responses, the oxidative burst and marker gene expression, during Arabidopsis infection. In planta expression of PPV capsid protein (CP) was found to strongly impair these responses in Nicotiana benthamiana and Arabidopsis, revealing its PTI suppressor activity. In summary, we provide the first clear evidence that plant viruses acquired the ability to suppress PTI mechanisms via the action of effectors, highlighting a novel strategy employed by viruses to escape plant defences.

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

“…One of the best studied PRRs in mammals, Toll-like receptors (TLR), have important roles in antiviral defense via recognition of a different range of MAMPs, such viral RNA and DNA (Song and Lee, 2012). In contrast, the PTI pathway in plants remains unclear with regard to resistance against viruses, although studies describing an association of PTI in antiviral immunity have been recently reported (Yang et al, 2010; Kørner et al, 2013; Nicaise, 2014; Machado et al, 2015; Nicaise and Candresse, 2016; Niehl et al, 2016). Indeed, a complex set of typical PTI responses is induced in plants upon virus infection, including SA accumulation, ROS production, ion fluxes, defense gene (e.g., PR-1) activation, and callose deposition (for a review, see Nicaise, 2014).…”

“…Consistently, Arabidopsis bak-1 mutants show increased susceptibility to three different RNA viruses, and crude extracts of virus-infected leaf tissues induce typical PTI responses in a BAK1-dependent manner (Kørner et al, 2013). The Arabidopsis double mutant bak1-5 bkk1 displays increased viral accumulation when inoculated with Plum pox virus (PPV; Nicaise and Candresse, 2016). Furthermore, MAPK4, a negative regulator of plant PTI signaling, suppresses soybean defense against Bean pod mottle virus (BPMV; Liu et al, 2011), and chitosan, a deacetylated chitin derivative elicitor, is able to stimulate the plant immune response against viruses (Iriti and Varoti, 2014).…”

“…The PTI pathway also contributes to antiviral immunity against PPV in Arabidopsis (Nicaise and Candresse, 2016). As a counteraction strategy, the CP from PPV appears to act as a PTI suppressor, impairing early immune responses such as the oxidative burst and enhanced expression of PTI-associated marker genes in planta during infection (Nicaise and Candresse, 2016).…”

Cross-Talk in Viral Defense Signaling in Plants

“…However, a few recent publications indicate that the known PTI components are involved in dsRNA recognition and that the reaction is an immune response distinct from the RNA silencing pathway. Therefore, these studies claim that PTI against viral pathogens is preserved in plants and animals (Korner et al, 2013; Nicaise, 2014; Nicaise and Candresse, 2016; Niehl et al, 2016). However, there is no direct evidence to explain how dsRNAs are recognized in plants; therefore, further studies are needed to determine whether an animal-like mechanism underlies dsRNA-mediated PTI in plants.…”

“…PTI against viral pathogens has been primarily described in mammalian cells, but not in plant cells (Calil and Fontes, 2016). However, several recent studies provided evidence that PTI and related components are also involved in antiviral defense responses in plants (Korner et al, 2013; Nicaise, 2014; Iriti and Varoni, 2015; Calil and Fontes, 2016; Nicaise and Candresse, 2016; Niehl et al, 2016). In general, plants defense responses triggered against viral pathogens are based on RNA- or protein-mediated resistance.…”