Ralstonia solanacearum effector RipAK suppresses homodimerization of the host transcription factor ERF098 to enhance susceptibility and the sensitivity of pepper plants to dehydration.

Abstract

Plants have evolved a sophisticated immune system to defend against invasion by pathogens. In response, pathogens deploy copious effectors to evade the immune responses. However, the molecular mechanisms used by pathogen effectors to suppress plant immunity remain unclear. Herein, we report that an effector secreted by Ralstonia solanacearum, RipAK, modulates the transcriptional activity of the ethylene-responsive factor ERF098 to suppress immunity and dehydration tolerance, which causes bacterial wilt in pepper (Capsicum annuum L.) plants. Silencing ERF098 enhances the resistance of pepper plants to R. solanacearum infection not only by inhibiting the host colonization of R. solanacearum but also by increasing the immunity and tolerance of pepper plants to dehydration and including the closure of stomata to reduce the loss of water in an abscisic acid signal-dependent manner. In contrast, the ectopic expression of ERF098 in Nicotiana benthamiana enhances wilt disease. We also show that RipAK targets and inhibits the ERF098 homodimerization to repress the expression of salicylic acid-dependent PR1 and dehydration tolerance-related OSR1 and OSM1 by cis-elements in their promoters. Taken together, our study reveals a regulatory mechanism used by the R. solanacearum effector RipAK to increase virulence by specifically inhibiting the homodimerization of ERF098 and reprogramming the transcription of PR1, OSR1, and OSM1 to boost susceptibility and dehydration sensitivity. Thus, our study sheds light on a previously unidentified strategy by which a pathogen simultaneously suppresses plant immunity and tolerance to dehydration by secreting an effector to interfere with the activity of a transcription factor and manipulate plant transcriptional programs.

• Authors: Kaisheng Liu, Lanping Shi, Hongli Luo, Kan Zhang, Jianxin Liu, Shanshan Qiu, Xia Li, Shuilin He, Zhiqin Liu
• Journal: The Plant journal : for cell and molecular biology (Plant J) Vol. 117 Issue 1 Pg. 121-144 (Jan 2024) ISSN: 1365-313X [Electronic] England
• PMID: 37738430 (Publication Type: Journal Article)
• Copyright: © 2023 Society for Experimental Biology and John Wiley & Sons Ltd.

Chemical References

• Transcription Factors
• Plant Proteins

Topics

• Transcription Factors (genetics, metabolism)
• Ralstonia solanacearum (physiology)
• Dehydration
• Plant Proteins (genetics, metabolism)
• Plants (metabolism)
• Plant Immunity (genetics)
• Gene Expression Regulation, Plant
• Plant Diseases (microbiology)
• Capsicum (metabolism)
• Disease Resistance (genetics)