Beyond its role in cellular homeostasis, autophagy plays anti-and promicrobial roles in host-microbe interactions, both in animals and plants. One prominent role of antimicrobial autophagy is to degrade intracellular pathogens or microbial molecules, in a process termed xenophagy. Consequently, microbes evolved mechanisms to hijack or modulate autophagy to escape elimination. Although well-described in animals, the extent to which xenophagy contributes to plant-bacteria interactions remains unknown. Here, we provide evidence that Xanthomonas campestris pv. vesicatoria (Xcv) suppresses host autophagy by utilizing type-III effector XopL. XopL interacts with and degrades the autophagy component SH3P2 via its E3 ligase activity to promote infection. Intriguingly, XopL is targeted for degradation by defense-related selective autophagy mediated by NBR1/Joka2, revealing a complex antagonistic interplay between XopL and the host autophagy machinery. Our results implicate plant antimicrobial autophagy in the depletion of a bacterial virulence factor and unravel an unprecedented pathogen strategy to counteract defense-related autophagy in plant-bacteria interactions.

As a critical part of plant immunity, cells that are attacked by pathogens undergo rapid transcriptional reprogramming to minimize virulence. Many bacterial phytopathogens use type III effector (T3E) proteins to interfere with plant defense responses, including this transcriptional reprogramming. Here, we show that XopS, a T3E of Xanthomonas campestris pv. vesicatoria (Xcv), interacts with and inhibits proteasomal degradation of WRKY40, a transcriptional regulator of defense gene expression. Virus-induced gene silencing of WRKY40 in pepper (Capsicum annuum) enhanced plant tolerance to Xcv infection, indicating that WRKY40 represses immunity. Stabilization of WRKY40 by XopS reduces the expression of its targets, which include salicylic acid (SA)-responsive genes and the jasmonic acid (JA) signaling repressor JAZ8. Xcv bacteria lacking XopS display significantly reduced virulence when surface inoculated onto susceptible pepper leaves. XopS delivery by Xcv, as well as ectopic expression of XopS in Arabidopsis thaliana or Nicotiana benthamiana, prevented stomatal closure in response to bacteria and biotic elicitors. Silencing WRKY40 in pepper or N. benthamiana abolished XopS’s ability to prevent stomatal closure. This suggests that XopS interferes with both preinvasion and apoplastic defense by manipulating WRKY40 stability and downstream gene expression, eventually altering phytohormone crosstalk to promote pathogen proliferation.

Beyond its role in cellular homeostasis, autophagy is considered to play anti- and pro-microbial roles in host-microbe interactions, both in animals and plants. One of the prominent roles of anti-microbial autophagy in animals is to degrade intracellular pathogens or microbial molecules, in a process termed “xenophagy”. Consequently, microbes evolved mechanisms to hijack or modulate autophagy to escape elimination. However, the extent to which xenophagy contributes to plant-bacteria interactions remains unknown. Here, we provide evidence that NBR1/Joka2-dependent selective autophagy functions in plant defence by degrading the bacterial type-III effector (T3E) XopL from Xanthomonas campestris pv. vesicatoria (Xcv). We show how XopL associates with the autophagy machinery and undergoes self-ubiquitination, subsequently triggering its own degradation by the NBR1/Joka2-mediated selective autophagy. Intriguingly, Xcv is also able to suppress autophagy in a T3E-dependent manner by utilizing the same T3E XopL that interacts and degrades the autophagy component SH3P2 via its E3 ligase activity. Thus, XopL is able to escape its own degradation and promote pathogenicity of Xcv by inhibiting autophagy through SH3P depletion. Together, we reveal a novel phenomenon how NBR1/Joka2 contributes to anti-microbial autophagy that we termed “effectorphagy”. We provide a unique mechanism how a T3E undergoes self-modification to act as a bait to trap host cellular degradation machineries.Significant statementAutophagy has anti- and pro-microbial roles in host-microbe interactions. Its anti-microbial role is derived from its ability to degrade intracellular pathogens, termed “xenophagy”. The contribution of xenophagy to host-bacteria interactions in plants and its substrates remains elusive. Here, we reveal that NEIGHBOR OF BRCA1 (NBR1)-mediated autophagy has an anti-microbial role towards bacteria by degrading the type-III effector (T3E) XopL from Xanthomonas campestris pv. vesicatoria (Xcv), a process we termed “effectorphagy”. We unveil that the same T3E is able to perturb autophagy to escape its own degradation and to boost bacterial virulence. These findings highlight a novel role of xenophagy that is conserved across kingdoms and we offer new perspectives on how T3Es undergo self-modification to trap host cellular degradation pathways.

A critical component of plant immunity against invading pathogens is the rapid transcriptional reprogramming of the attacked cell to minimize virulence. Many adapted plant bacterial pathogens use type III effector (T3E) proteins to interfere with plant defense responses, including the induction of immunity genes. The elucidation of effector function is essential to understanding bacterial pathogenesis. Here, we show that XopS, a T3E of Xanthomonas campestris pv. vesicatoria (Xcv), interacts with and inhibits the proteasomal degradation of the transcriptional regulator of defense gene expression WRKY40. Virus-induced gene silencing of WRKY40 in pepper enhanced plant tolerance towards Xcv infection, indicating it represses immunity. Stabilization of WRKY40 by XopS reduces the expression of its targets including salicylic acid (SA)-responsive genes and the jasmonic acid (JA) signaling repressor JAZ8. Xcv bacteria lacking XopS display significantly reduced virulence when surface inoculated onto susceptible pepper leaves. XopS delivery by Xcv, as well as ectopic expression of XopS in Arabidopsis or Nicotiana benthamiana prevented stomatal closure in response to bacteria and biotic elicitors in a WRKY40 dependent manner. This suggests that XopS interferes with preinvasion as well as with apoplastic defense by manipulating WRKY40 stability and gene expression eventually altering phytohormone crosstalk to promote pathogen proliferation.