Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.
Key Laboratory of Plant Hormone Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing, China.
Nat Commun. 2024 Aug 22;15(1):7212. doi: 10.1038/s41467-024-51515-2.
N-hydroxy pipecolic acid (NHP) plays an important role in plant immunity. In contrast to its biosynthesis, our current knowledge with respect to the transcriptional regulation of the NHP pathway is limited. This study commences with the engineering of Arabidopsis plants that constitutively produce high NHP levels and display enhanced immunity. Label-free proteomics reveals a NAC-type transcription factor (NAC90) that is strongly induced in these plants. We find that NAC90 is a target gene of SAR DEFICIENT 1 (SARD1) and induced by pathogen, salicylic acid (SA), and NHP. NAC90 knockout mutants exhibit constitutive immune activation, earlier senescence, higher levels of NHP and SA, as well as increased expression of NHP and SA biosynthetic genes. In contrast, NAC90 overexpression lines are compromised in disease resistance and accumulated reduced levels of NHP and SA. NAC90 could interact with NAC61 and NAC36 which are also induced by pathogen, SA, and NHP. We next discover that this protein triad directly represses expression of the NHP and SA biosynthetic genes AGD2-LIKE DEFENSE RESPONSE PROTEIN 1 (ALD1), FLAVIN MONOOXYGENASE 1 (FMO1), and ISOCHORISMATE SYNTHASE 1 (ICS1). Constitutive immune response in nac90 is abolished once blocking NHP biosynthesis in the fmo1 background, signifying that NAC90 negative regulation of immunity is mediated via NHP biosynthesis. Our findings expand the currently documented NHP regulatory network suggesting a model that together with NHP glycosylation, NAC repressors take part in a 'gas-and-brake' transcriptional mechanism to control NHP production and the plant growth and defense trade-off.
N-羟基哌啶酸（NHP）在植物免疫中起着重要作用。与生物合成相比，我们目前对 NHP 途径的转录调控知之甚少。本研究首先对拟南芥植物进行工程改造，使其持续产生高水平的 NHP 并表现出增强的免疫力。无标记蛋白质组学揭示了一种 NAC 型转录因子（NAC90），该因子在这些植物中强烈诱导。我们发现 NAC90 是 SAR DEFICIENT 1（SARD1）的靶基因，并受病原体、水杨酸（SA）和 NHP 的诱导。NAC90 敲除突变体表现出组成型免疫激活、更早的衰老、更高水平的 NHP 和 SA 以及 NHP 和 SA 生物合成基因的表达增加。相比之下，NAC90 过表达系在疾病抗性方面受到损害，并且积累了较低水平的 NHP 和 SA。NAC90 可以与 NAC61 和 NAC36 相互作用，这两种基因也受病原体、SA 和 NHP 的诱导。我们接下来发现，这个蛋白三聚体直接抑制 NHP 和 SA 生物合成基因 AGD2-LIKE DEFENSE RESPONSE PROTEIN 1（ALD1）、FLAVIN MONOOXYGENASE 1（FMO1）和 ISOCHORISMATE SYNTHASE 1（ICS1）的表达。一旦在 fmo1 背景下阻断 NHP 生物合成，nac90 中的组成型免疫反应就会被消除，这表明 NAC90 对免疫的负调控是通过 NHP 生物合成介导的。我们的发现扩展了目前记录的 NHP 调控网络，提出了一个模型，即与 NHP 糖基化一起，NAC 抑制剂参与“油门和刹车”转录机制，以控制 NHP 的产生和植物生长与防御的权衡。
