Song Kai, Li Ruifang, Cui Ying, Chen Bo, Zhou Lian, Han Wenying, Jiang Bo-Le, He Ya-Wen
State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai China.
Guangxi Key Laboratory of Biology for Crop Diseases and Insect Pests, Plant Protection Research Institute Guangxi Academy of Agricultural Sciences Nanning China.
mLife. 2024 Sep 16;3(3):430-444. doi: 10.1002/mlf2.12140. eCollection 2024 Sep.
Salicylic acid (SA) plays an essential role in plant defense against biotrophic and semi-biotrophic pathogens. Following pathogen recognition, SA biosynthesis dramatically increases at the infection site of the host plant. The manner in which pathogens sense and tolerate the onslaught of SA stress to survive in the plant following infection remains to be understood. The objective of this work was to determine how the model phytopathogen pv. (Xcc) senses and effluxes SA during infection inside host plants. First, RNA-Seq analysis identified an SA-responsive operon Xcc4167-Xcc4171, encoding a MarR family transcription factor HepR and an RND (resistance-nodulation-cell division) family efflux pump HepABCD in Xcc. Electrophoretic mobility shift assays and DNase I footprint analysis revealed that HepR negatively regulated expression by specifically binding to an AT-rich region of the promoter of the operon, P. Second, isothermal titration calorimetry and further genetic analysis suggest that HepR is a novel SA sensor. SA binding released HepR from its cognate promoter P and then induced the expression of . Third, the RND family efflux pump HepABCD was responsible for SA efflux. The cluster was also involved in the regulation of culture pH and quorum sensing signal diffusible signaling factor turnover. Finally, the cluster was transcribed during the XC1 infection of Chinese radish and was required for the full virulence of Xcc in Chinese radish and cabbage. These findings suggest that the ability of Xcc to co-opt the plant defense signal SA to activate the multidrug efflux pump may have evolved to ensure Xcc survival and virulence in susceptible host plants.
水杨酸（SA）在植物抵御活体营养型和半活体营养型病原体的防御过程中发挥着重要作用。在病原体被识别后，SA生物合成在宿主植物的感染部位急剧增加。病原体如何感知并耐受SA胁迫的冲击以在感染后的植物中存活，仍有待了解。这项工作的目的是确定模式植物病原体野油菜黄单胞菌（Xcc）在宿主植物体内感染期间如何感知和外排SA。首先，RNA测序分析鉴定出一个SA响应操纵子Xcc4167 - Xcc4171，其在Xcc中编码一个MarR家族转录因子HepR和一个RND（抗性-固氮-细胞分裂）家族外排泵HepABCD。电泳迁移率变动分析和DNase I足迹分析表明，HepR通过特异性结合操纵子P的启动子富含AT的区域来负调控其表达。其次，等温滴定量热法和进一步的遗传分析表明，HepR是一种新型的SA传感器。SA结合使HepR从其同源启动子P上释放，然后诱导其表达。第三，RND家族外排泵HepABCD负责SA外排。该簇也参与了培养物pH的调节和群体感应信号可扩散信号因子的周转。最后，该簇在Xcc感染中国萝卜期间被转录，并且是Xcc在中国萝卜和甘蓝中完全致病力所必需的。这些发现表明，Xcc利用植物防御信号SA来激活多药外排泵的能力可能已经进化，以确保Xcc在易感宿主植物中的存活和致病力。
