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

• Published in: Molecules and cells 2024-12, Vol.47 (12), p.100158, Article 100158
• Main Authors: Kim, Jihyun, Kaleku, Jesse, Kim, Haeun, Kang, Minji, Kang, Hui Jeong, Woo, Jongchan, Jin, Hongshi, Jung, Seungmee, Segonzac, Cécile, Park, Eunsook, Choi, Doil
• Format: Article
• Language: English
• Subjects: Endoplasmic Reticulum - metabolism; Endoplasmic Reticulum Stress; ER stress; Golgi Apparatus - metabolism; Nicotiana - immunology; Nicotiana - metabolism; Nicotiana - microbiology; Phytophthora - metabolism; Phytophthora - pathogenicity; Phytophthora capsici; Plant Diseases - microbiology; Protein Transport; rab GTP-Binding Proteins - metabolism; Rab small GTPase; RXLR effector; Vesicle trafficking; Virulence
• ISSN: 1016-8478; 0219-1032; 0219-1032
• DOI: 10.1016/j.mocell.2024.100158

Phytophthora species, an oomycete plant pathogen, secrete effectors into plant cells 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 (amino acid residue; Arginine-Any amino acid-Leucine-Arginine motif) 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-mediated hypersensitive cell death, including the involvement of nucleotide-binding site leucine-rich repeat 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, 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 Rab escort protein 1 and prenylated Rab acceptor 1. 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.