The Bacterial Effector AvrPto Targets the Regulatory Coreceptor SOBIR1 and Suppresses Defense Signaling Mediated by the Receptor-Like Protein Cf-4

Abstract

Receptor-like proteins (RLPs) and receptor-like kinases (RLKs) are cell-surface receptors that are essential for detecting invading pathogens and subsequent activation of plant defense responses. RLPs lack a cytoplasmic kinase domain to trigger downstream signaling leading to host resistance. The RLK SOBIR1 constitutively interacts with the tomato RLP Cf-4, thereby providing Cf-4 with a kinase domain. SOBIR1 is required for Cf-4-mediated resistance to strains of the fungal tomato pathogen Cladosporium fulvum that secrete the effector Avr4. Upon perception of this effector by the Cf-4/SOBIR1 complex, the central regulatory RLK SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3a (SERK3a) is recruited to the complex and defense signaling is triggered. SOBIR1 is also required for RLP-mediated resistance to bacterial, fungal ,and oomycete pathogens, and we hypothesized that SOBIR1 is targeted by effectors of such pathogens to suppress host defense responses. In this study, we show that Pseudomonas syringae pv. tomato DC3000 effector AvrPto interacts with Arabidopsis SOBIR1 and its orthologs of tomato and Nicotiana benthamiana, independent of SOBIR1 kinase activity. Interestingly, AvrPto suppresses Arabidopsis SOBIR1-induced cell death in N. benthamiana. Furthermore, AvrPto compromises Avr4-triggered cell death in Cf-4-transgenic N. benthamiana, without affecting Cf-4/SOBIR1/SERK3a complex formation. Our study shows that the RLP coreceptor SOBIR1 is targeted by a bacterial effector, which results in compromised defense responses.

Kinase activity of SOBIR1 and BAK1 is required for immune signalling

“…To determine whether in planta phosphorylation of SOBIR1 plays a role in signalling for constitutive immunity induced by this RLK (Wu et al. , ), we transiently overexpressed full‐length enhanced green fluorescent protein (eGFP)‐tagged Arabidopsis and tomato SOBIR1 proteins, and the corresponding kinase‐dead mutants in which the catalytic aspartic acid (Asp, D) is mutated to asparagine (Asn, N), in N. benthamiana in combination with P19. Subsequently, we analysed their overall phosphorylation status by Pro‐Q staining.…”

“…A, see Supporting Information) (Wu et al. , ). The lack of a Pro‐Q signal for kinase‐dead At SOBIR1 suggests that the wild‐type RD‐kinase of At SOBIR1 trans‐autophosphorylates in planta , as it has previously been shown to do in vitro (Leslie et al.…”

“…Recently, we have observed that transient heterologous overexpression of Arabidopsis thaliana ( At )SOBIR1 in Nicotiana tabacum (tobacco, Nt ) and N. benthamiana ( Nb ), in contrast with transient overexpression of Sl SOBIR1 and Nb SOBIR1, also results in constitutive immunity (Wu et al. , ). This constitutive immunity is typically manifested by the induction of cell death [the hypersensitive response (HR)] and mitogen‐activated protein kinase (MAPK) activation (Wu et al.…”

“…This constitutive immunity is typically manifested by the induction of cell death [the hypersensitive response (HR)] and mitogen‐activated protein kinase (MAPK) activation (Wu et al. , ). Kinase‐dead At SOBIR1 D498N does not induce constitutive immunity, indicating that SOBIR1 kinase activity is essential for this phenomenon.…”

“…However, these phosphatases might not be able to keep At SOBIR1 in check, for example, because of the lower affinity for this heterologous SOBIR1 orthologue (Wu et al. , ).…”