Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity

作者：Jiale Shi, He Wang, Mengping Li, Liru Mi, Yazhi Gao, Sheng Qiang, Yu Zhang, Dan Chen, Xinbin Dai, Hongyu Ma, Huan Lu, Chanhong Kim, Shiguo Chen · 发表于：Plant Communications · 年份：2023 · DOI：10.1016/j.xplc.2023.100775 · 被引用次数：21 · 研究领域：Plant-Microbe Interactions and Immunity、Insect-Plant Interactions and Control、Photosynthetic Processes and Mechanisms

The chloroplast is a critical battleground in the arms race between plants and pathogens. Among microbe-secreted mycotoxins, the tenuazonic acid (TeA), produced by the genus Alternaria and other phytopathogenic fungi, inhibits photosynthesis, leading to a burst of photosynthetic singlet oxygen (1O2) implicated in damage and chloroplast-to-nucleus retrograde signaling. Despite the potent adversity of Alternaria pathogens on crop production, the molecular mechanism of TeA-caused pathogenicity and cognate plant defense responses remain fragmented. We now reveal that A. alternata induces necrotrophic foliar lesions by harnessing an EXECUTER1 (EX1)/EX2-mediated chloroplast-to-nucleus retrograde signaling (RS), activated by TeA toxin-derived photosynthetic 1O2 in Arabidopsis thaliana. Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1 compromises the expression of 1O2-responsive nuclear genes and foliar lesions. Remarkably, we further noticed that the TeA toxin rapidly induces nuclear genes implicated in jasmonic acid (JA) synthesis and signaling, for which EX1-mediated RS appeared to be critical in establishing a signaling cascade from 1O2 to JA. Our present study sheds new light on A. alternata-caused foliar pathogenicity, where EX1-dependent 1O2 signaling induces JA-dependent foliar cell death.