水杨酸介导的植物免疫反应: 从代谢、感知到免疫激活

doi:10.11983/CBB25149

摘要/Abstract

摘要： 水杨酸(SA)是一种植物酚类天然合成产物, 对免疫反应具有重要的调控作用。植物主要通过异分支酸合酶(ICS)途径和苯丙氨酸解氨酶(PAL)途径合成水杨酸, 并被水杨酸受体NPR1等感知, 激活植物免疫反应。拟南芥(Arabidopsis thaliana)等十字花科植物主要通过ICS途径合成水杨酸, 而单子叶植物和非十字花科双子叶植物则主要通过PAL途径合成水杨酸。长期以来, 人们对水杨酸PAL合成途径的认识不完整, 导致水稻(Oryza sativa)等作物中水杨酸介导的植物免疫反应研究滞后, 极大地制约了作物抗病育种改良进程。近期, 我国3个研究团队独立破解了水杨酸在水稻等作物中的PAL合成途径。该文以此为契机, 综述了水杨酸介导的植物免疫反应研究进展, 着重梳理了植物体内的水杨酸合成途径, 总结了水杨酸被植物感知并激活免疫反应的机制, 展望了水杨酸调控植物免疫反应研究中存在的问题和未来的研究方向, 以期为相关理论研究和抗病育种应用提供新思路和新方向。

关键词: 水杨酸, 合成途径, 水杨酸感知, NPR1, 免疫反应

Abstract: Salicylic acid (SA) is a natural phenolic compound in plants that plays a crucial regulatory role in plant immune responses. Plants primarily synthesize SA through two pathways: the isochorismate synthase (ICS) pathway and the phenylalanine ammonia-lyase (PAL) pathway. The synthesized SA is perceived by receptors such as nonexpressor of pathogenesis-related genes 1 (NPR1), which subsequently activate immune responses. In Brassicaceae species like Arabidopsis thaliana, SA is mainly synthesized via the ICS pathway, whereas monocots and non-Brassicaceae dicots predominantly rely on the PAL pathway. For a long time, understanding of SA biosynthesis via the PAL pathway has been incomplete, hindering research on SA-mediated immunity in crops and significantly limiting progress in crop disease-resistant breeding. Recently, three research groups from China independently elucidated the PAL-mediated SA biosynthesis pathway in crops. Building on these breakthroughs, this review summarizes recent advances in the study of SA-mediated plant immune responses. We primarily focus on the biosynthetic pathways of SA within plants, the mechanisms by which SA is perceived and activates immune responses, and discuss current challenges and future directions in SA-mediated immunity research. We hope this review provides new insights and perspectives for both theoretical studies and practical applications in crop disease-resistant breeding.

Key words: salicylic acid, biosynthesis pathway, salicylic acid perception, NPR1, immune responses

朱孝波, 王立印, 陈学伟. 水杨酸介导的植物免疫反应: 从代谢、感知到免疫激活. 植物学报, 2025, 60(5): 679-692.

Zhu Xiaobo, Wang Liyin, Chen Xuewei. Salicylic Acid-mediated Plant Immune Responses: From Metabolism and Perception to Immune Activation. Chinese Bulletin of Botany, 2025, 60(5): 679-692.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB25149

https://www.chinbullbotany.com/CN/Y2025/V60/I5/679

图/表 2

图1 水杨酸(SA)的生物合成与转录调控和代谢 (A) 水杨酸的生物合成途径(植物通过分支酸合酶(ICS)途径和苯丙氨酸解氨酶(PAL)途径合成水杨酸, 2条合成途径均起始于叶绿体, 以分支酸为前体。ICS1: 异分支酸合酶1; ICS2: 异分支酸合酶2; EDS5: 异分支酸转运蛋白; PBS3: 酰胺转移酶, EPS1: 酰基转移酶; OSD1/CNL: 肉桂酰辅酶A连接酶; AIM1/CHD: 肉桂酰辅酶A水合酶/脱氢酶; KAT: 3-酮酰辅酶A硫解酶; OSD2/BEBT: 苯甲醇苯甲酰转移酶; OSD3/BB2H/BBH/BBO: 苯甲酸苄酯2-羟化酶; OSD4/BSH/BSE: 水杨酸苄水解酶; ER: 内质网; 问号圆圈表示未知转运蛋白); (B) 水杨酸合成的转录调控(转录因子SARD1和CBP60g是ICS1、PBS3和EDS5基因表达的主要调控因子, 转录因子EIN3和多个ANAC可以抑制ICS1的表达, DEL1能够抑制EDS5的表达。PHB3可以稳定ICS1蛋白, 水杨酸可抑制PBS3的酶活性, 从而反馈调控水杨酸的合成。转录因子D53、WRKY75和OsMYB30可以调控多个PALs基因的表达。RNA结合蛋白BSR-K1可结合PAL基因的mRNA并降解, 在mRNA水平调控其表达); (C) 水杨酸的代谢(水杨酸可由水杨酸羟化酶S5H转化为2,5-二羟基苯甲酸(2,5-DHBA), 由S3H转化为2,3-二羟基苯甲酸(2,3-DHBA); 被UGT74F1和UGT76B1转化为水杨酸葡萄糖苷(SAG), 被UGT74F2转化为水杨酸葡萄糖酯(SGE), SAG和SGE可转运到液泡中进行储存; 还可被羧基甲基转移酶BSMT1甲基化, 生成甲基水杨酸(MeSA), MeSA可由甲基酯酶MES9转化为水杨酸; 水杨酸可在磺基转移酶SOT12的催化下生成磺基化的水杨酸; 还可在酰基酸氨基合成酶GH3.5的作用下, 与天门冬氨酸(Asp)结合, 生成SA-Asp)。

Figure 1 Biosynthesis, transcriptional regulation, and metabolism of salicylic acid (SA) (A) Biosynthetic pathways of SA (plants synthesize SA via two main pathways: the isochorismate synthase (ICS) pathway and the phenylalanine ammonia-lyase (PAL) pathway. Both originate in the chloroplast, using chorismate as the precursor. ICS1: Isochorismate synthase 1; ICS2: Isochorismate synthase 2; EDS5: Isochorismate transporter; PBS3: Amide transferase; EPS1: Acyl transferase; OSD1/CNL: Cinnamoyl-CoA ligase; AIM1/CHD: Cinnamoyl-CoA hydratase/dehydrogenase; KAT: 3-ketoacyl- CoA thiolase; OSD2/BEBT: Benzyl alcohol O-benzoyltransferase; OSD3/BB2H/BBH/BBO: Benzyl benzoate 2-hydroxylase; OSD4/BSH/BSE: Benzyl salicylate hydrolase; ER: Endoplasmic reticulum; question marked circles indicate unknown transporter); (B) Transcriptional regulation of SA biosynthesis (transcription factors SARD1 and CBP60g are major regulators of ICS1, PBS3, and EDS5 gene expression. EIN3 and several ANAC transcription factors repress ICS1 expression, while DEL1 suppresses EDS5 expression. PHB3 stabilizes the ICS1 protein. SA itself inhibits the enzymatic activity of PBS3, forming a feedback loop to regulate its own synthesis. Transcription factors D53, WRKY75, and OsMYB30 regulate the expression of multiple PAL genes. RNA-binding protein BSR-K1 can bind to the mRNA of the PAL genes and degrade them, thereby regulating their expression at the mRNA level); (C) Metabolism of SA (SA can be hydroxylated by salicylic acid 5-hydroxylase (S5H) to form 2,5-dihydroxybenzoic acid (2,5-DHBA), and by S3H to produce 2,3-dihydroxybenzoic acid (2,3-DHBA). It can also be glycosylated by UGT74F1 and UGT76B1 to form salicylic acid glucoside (SAG), or by UGT74F2 to form salicylic acid glucose ester (SGE). SAG and SGE are transported into vacuoles for storage. SA can also be methylated by the carboxyl methyltransferase BSMT1 to produce methyl salicylate (MeSA), which is converted back to SA by methyl esterase MES9. SA can be converted into sulfonated SA under the catalysis of sulfite transferase SOT12. Additionally, SA can conjugate with aspartic acid (Asp) via the action of acyl acid amido synthetase GH3.5 to form SA-Asp).

图2 水杨酸(SA)信号的感知与激活在低浓度水杨酸条件下, NPR1蛋白通过二硫键(S-S)连接, 以寡聚体的形式存在于细胞质中; 而NPR3/4蛋白则在细胞核中与TGAs转录因子互作, 抑制水杨酸响应基因的表达。当细胞内水杨酸浓度升高时, 一方面NPR3/4可与水杨酸结合, 解除NPR3/4对下游水杨酸响应基因表达的抑制作用。另一方面, 水杨酸诱导细胞氧化还原状态改变, 在TRXh3/5的还原作用下, NPR1间的二硫键被破坏, NPR1解聚为单体; 解聚的NPR1在胞质中与水杨酸结合, 随后作为CRL3 E3泛素连接酶的底物识别蛋白, 与胞质中抗病蛋白(NLRs)及胁迫响应相关蛋白等形成水杨酸诱导的细胞质蛋白聚集体(cSINC), 调控这些蛋白的降解和稳态, 从而调控植物免疫反应。此外, 胞质中的NPR1蛋白还可经过蛋白激酶SnRK2.8的磷酸化(橘黄色圆形P)、未知蛋白磷酸酶对Ser55/99的去磷酸化及类泛素化修饰酶SUMO3的类泛素化修饰(绿色圆形S)等系列蛋白翻译后修饰作用后进入细胞核; 在细胞核中NPR1形成二聚体, Ser11/15被未知激酶磷酸化, 并在CRL3 E3泛素连接酶作用下发生单泛素化或短链泛素化修饰(单个蓝色圆形Ub); NPR1构象改变并与水杨酸结合, 与TGAs转录因子互作激活水杨酸响应基因的表达。在细胞核内, NPR1与TGAs转录因子和蛋白修饰酶及其它转录调控蛋白互作, 形成调控水杨酸响应基因表达的蛋白聚集体, 称为水杨酸诱导的细胞核蛋白聚集体(nSINC)。随后, 在泛素连接酶UBE4/MUSE3的作用下, NPR1的泛素化修饰链延长(多个蓝色圆形Ub), 促使NPR1进入26S蛋白酶体进行降解; 进入蛋白酶体的NPR1蛋白可在蛋白酶体相关去泛素化酶UBP6/7的作用下, 发生去泛素化作用, 解除NPR1的泛素蛋白酶体降解, 恢复其转录激活活性。

Figure 2 Perception and activation of salicylic acid (SA) signaling At low intracellular SA levels, NPR1 proteins are present in the cytosol as oligomers linked by disulfide bonds (S-S). Meanwhile, NPR3 and NPR4 proteins interact with TGA transcription factors in the nucleus to repress the expression of SA-responsive genes. When intracellular SA levels rise, NPR3/4 bind to SA, relieving their repression of downstream SA-responsive gene expression. SA also induces changes in the cellular redox state, and the disulfide bonds between NPR1 molecules are reduced by TRXh3/5, leading to monomerization of NPR1. Cytoplasmic NPR1 binds SA and acts as a substrate recognition protein for the CRL3 E3 ubiquitin ligase. It forms SA-induced NPR1 cytoplasmic protein condensates (cSINC) with disease resistance proteins (NLRs) and stress-related proteins, regulating their degradation and homeostasis to modulate plant immune responses. Additionally, cytoplasmic NPR1 undergoes a series of post-translational modifications before entering the nucleus, such as phosphorylation by protein kinase SnRK2.8 (orange circle labeled “P”), dephosphorylation at Ser55/99 by unknown phosphatases, and SUMOylation by SUMO3 (green circle labeled “S”). When enters in the nucleus, NPR1 forms dimers and is phosphorylated at Ser11/15 by unknown kinases, and undergoes mono- or short-chain ubiquitination (single blue circle labeled “Ub”) mediated by CRL3 E3 ligase. These modifications change NPR1’s conformation, enabling SA binding and interaction with TGA transcription factors to activate SA-responsive genes. Nuclear NPR1, together with TGAs, protein modifiers, and other transcriptional regulators, forms nuclear protein condensates known as SA-induced NPR1 nuclear condensates (nSINC), which orchestrate SA-responsive genes’ expression. Subsequently, NPR1 undergoes polyubiquitination (multiple blue circles labeled “Ub”) mediated by the ubiquitin ligase UBE4/MUSE3, targeting it for degradation via the 26S proteasome. However, NPR1 can be deubiquitinated by proteasome-associated deubiquitinases UBP6/7, preventing its degradation and restoring its transcriptional activation function.

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