Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition
Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition
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病原体对叶绿体功能的操纵触发光依赖性免疫识别
DOI：
10.1073/pnas.2002759117
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发表时间：
2020-04-28
影响因子：
11.1
通讯作者：
Dong, Suomeng
中科院分区：
文献类型：
--
作者：
Gao, Chuyun;Xu, Huawei;Dong, Suomeng
植物病原体，如爱尔兰马铃薯饥荒病原体致病疫霉（Phytophthora infestans），仍然是全球粮食安全的最大威胁。植物抗病性通常由核苷酸结合的富含亮氨酸重复序列（NLR）蛋白赋予，NLR蛋白是识别和消除病原体的细胞内免疫传感器。然而，很少有人知道病原体激活的NLR免疫是如何受到环境因素，如光的影响。在这里，我们表明，致病疫霉操纵植物叶绿体功能触发光依赖性免疫反应。我们的研究结果表明，光诱导的替代启动子选择调节植物免疫识别的病原体毒力因子的农业上重要的NLR型受体蛋白。在植物和动物中，核苷酸结合的富含亮氨酸重复序列（NLR）蛋白是细胞内的免疫传感器，可以识别和消除广泛的入侵病原体。已知NLR介导的免疫受环境因素调节。然而，NLR对病原体的识别如何受到环境因素（如光）的影响仍不清楚。在这里，我们表明，农学上重要的NLR Rpi-vnt 1.1需要光赋予抗病性的爱尔兰马铃薯饥荒病原体致病疫霉分泌的效应蛋白AVRvnt 1的种族。Rpi-vnt 1.1的激活需要核编码的叶绿体蛋白，甘油酸3-激酶（GLYK），其涉及能量产生。病原体效应子AVRvnt 1结合全长叶绿体靶向GLYK同种型，导致Rpi-vnt 1.1的激活。在黑暗中，Rpi-vnt 1.1介导的抗性受到损害，因为植物产生较短的GLYK-缺乏完整的叶绿体转运肽-不被AVRvnt 1结合。全长和较短的植物GLYK转录本之间的转换是由光依赖性的替代启动子选择机制控制的。在缺乏Rpi-vnt 1.1的植物中，AVRvnt 1的存在减少了叶绿体中GLYK的积累，抵消了GLYK对基础免疫的贡献。我们的研究结果表明，病原体操纵叶绿体功能导致了光依赖性免疫反应。
Significance Plant pathogens, such as Irish potato famine agent Phytophthora infestans, remain the most significant threats to global food security. Plant disease resistance is often conferred by nucleotide-binding leucine-rich repeat (NLR) proteins, intracellular immune sensors that recognize and eliminate pathogens. However, little is known about how pathogen-activated NLR immunity is influenced by environmental factors such as light. Here, we show that P. infestans manipulation of plant chloroplast function triggers a light-dependent immune response. Our results reveal that light-induced alternative promoter selection regulates plant immune recognition of a pathogen virulence factor by an agriculturally important NLR-type receptor protein. In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1–mediated resistance is compromised because plants produce a shorter GLYK—lacking the intact chloroplast transit peptide—that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.