An RXLR effector disrupts vesicle trafficking at ER-Golgi interface for Phytophthora capsici pathogenicity

Mol Cells. 2024 Nov 20:100158. doi: 10.1016/j.mocell.2024.100158. Online ahead of print.

Abstract

Phytophthora species, an oomycetes plant pathogen, secrete effectors into plant cell throughout their life cycle for manipulating host immunity to achieve successful colonization. However, the molecular mechanisms underlying effector-triggered necrotic cell death remain elusive. In this study, we identified an RXLR effector (Pc12) from Phytophthora capsici which contributes to virulence and induces necrosis by triggering a distinct endoplasmic reticulum (ER) stress response through its interaction with Rab13-2. The necrotic cell death induced by Pc12 did not exhibit conventional effector-triggered immunity (ETI)-mediated hypersensitive cell death, including the involvement of NLR downstream signaling components and transcriptional reprogramming of defense-related genes. Instead, it alters the localization of ER-resident proteins and confines secretory proteins within the ER. Pc12 directly interacts with Rab13-2, which is primarily localized to the ER and Golgi apparatus, resulting in a diminished Rab13-2 signal on the Golgi apparatus. Furthermore, Rab13-2 exhibits increased affinity for its interactor, Rab escort protein 1 (REP1), in the presence of Pc12. Structural predictions revealed that a specific residue of Rab13-2 is crucial for binding to the C-terminus of Pc12. Substitution of this residue reduced its interaction with Pc12 and impaired P. capsici infection, while maintaining its interaction with REP1 and prenylated Rab acceptor (PRA1). These findings provide insight into how a pathogen effector induces a distinct form of necrotic cell death to facilitate colonization of the host plant by disrupting the recycling of Rab13-2, a protein involved in vesicle trafficking at the ER-Golgi interface.

Keywords: ER stress; Necrotic cell death; Phytophthora capsici; RXLR effector; Rab Small GTPase; Vesicle trafficking.