A core Plasmopara viticola effector attenuates the DNA-binding activity of bZIP transcription factor to compromise plant immunity

Abstract

Grapevine (Vitis vinifera L.) frequently faces challenges from various pathogens, among which Plasmopara viticola is the most devastating one hindering grape production. During infection, P. viticola secretes a series of effectors into host cells to manipulate plant immune responses. Here, an RXLR effector of P. viticola, PvRXLR13, was identified as one that could disrupt immune processes and thus promote pathogen colonization. PvRXLR13 contained a functional signal peptide and was highly conserved across different destructive oomycetes. PvRXLR13 was significantly induced during P. viticola infection and could suppress elicitor chitin-induced reactive oxygen species (ROS), callose deposition, and INF1-triggered cell death. Furthermore, PvRXLR13 could also inhibit P. viticola- and P. capsici-triggered H₂O₂ accumulation and promote pathogen colonization in both grapevine and Nicotiana benthamiana, respectively. VvHY5, a basic leucine zipper (bZIP) transcription factor, was found to be the host target of PvRXLR13. Further analysis revealed that overexpression of VvHY5 enhanced grapevine resistance to P. viticola and P. viticola-triggered H₂O₂ accumulation. Furthermore, we found that VvHY5 directly bound to the promoter of the positive immune factor VvEDS1 and activated its expression, whereas PvRXLR13 attenuated the DNA-binding activity of VvHY5 during P. viticola infection. Further analysis revealed that other members of grape bZIPs, VvbZIP6/9/21/32/34/37, were also involved in the defense response against P. viticola invasion. Just like HY5/HYH, all these bZIP family members were targeted by the effector PvRXLR13. Collectively, our findings suggest that P. viticola secretes a key effector PvRXLR13 to compromise the function in immune regulation of bZIP transcription factors to promote infection in grapevine.