Article(id=1319998769962266725, tenantId=1146029695717560320, journalId=1316781310003478668, issueId=1319998767835754596, articleNumber=null, orderNo=null, doi=10.11983/CBB25106, pmid=null, cstr=32102.14.CBB25106, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1749139200000, receivedDateStr=2025-06-06, revisedDate=null, revisedDateStr=null, acceptedDate=1751299200000, acceptedDateStr=2025-07-01, onlineDate=1792641831149, onlineDateStr=2026-10-22, pubDate=1757433600000, pubDateStr=2025-09-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1792641831149, onlineIssueDateStr=2026-10-22, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1792641831149, creator=13701087609, updateTime=1792641831149, updator=13701087609, issue=Issue{id=1319998767835754596, tenantId=1146029695717560320, journalId=1316781310003478668, year='2025', volume='60', issue='5', pageStart='669', pageEnd='853', issueExtLink='null', onlineDate='null', pubDate='1757433600000', pubDateStr='2025-09-10', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1792641830643, creator='13701087609', updateTime=1792641943258, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1319999240240222831, tenantId=1146029695717560320, journalId=1316781310003478668, issueId=1319998767835754596, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1319999240240222832, tenantId=1146029695717560320, journalId=1316781310003478668, issueId=1319998767835754596, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=749, endPage=758, ext={EN=ArticleExt(id=1319998771187003496, articleId=1319998769962266725, tenantId=1146029695717560320, journalId=1316781310003478668, language=EN, title=Research Progress on SUMOylation in Plant-Pathogen Interactions, columnId=1319998770868236391, journalTitle=Chinese Bulletin of Botany, columnName=INVITED REVIEWS, runingTitle=null, highlight=null, articleAbstract=

SUMOylation is a crucial post-translational modification in plants, playing a pivotal role in plant immune regulation by mediating substrate protein functions, the activation and transduction of immune signals, and hormonal signaling networks. This review systematically summarizes recent research advances in SUMOylation during plant-pathogen interactions, focusing on the enzymatic cascade mechanisms of the SUMOylation system, the involvement of SUMOylation in plant immune regulation, and the interference/activation of the SUMOylation system by pathogen effector proteins. We highlight the SUMOylation-mediated regulatory networks of plant immunity and provide a reference for developing novel disease resistance strategies in crops based on SUMO modification.

, authors=Li Wenliang1, Feng Hanqing1, *, Lai Jianbin2, *, authorsList=Li Wenliang, Feng Hanqing, Lai Jianbin, authorCompany=null, correspAuthors=Feng Hanqing, Lai Jianbin, authorNote=null, correspAuthorsNote=
*E-mail: ;
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SUMO化修饰是植物中重要的翻译后修饰, 通过介导底物蛋白的功能、免疫信号的激活与转导以及激素信号网络, 在植物免疫调控中发挥关键作用。该文从SUMO化修饰系统的酶联反应机制、SUMO化修饰参与植物免疫调控以及病原体效应蛋白对SUMO化系统的干扰等方面, 系统综述了SUMO化修饰在植物与病原互作中的功能最新研究进展, 旨在解析SUMO化介导的植物免疫调控网络, 为开发基于SUMO化修饰的作物抗病新策略提供参考。

, authors=李文亮1, 冯汉青1, *, 赖建彬2, *, authorsList=李文亮, 冯汉青, 赖建彬, authorCompany=null, correspAuthors=冯汉青, 赖建彬, authorNote=null, correspAuthorsNote=
赖建彬, 华南师范大学生命科学学院教授, 广东省特支计划科技创新青年拔尖人才。长期从事棕榈酰化和SUMO化等翻译后修饰调控植物抗逆研究。以通讯作者(含共同)在Trends in Plant Science、EMBO Journal、Proceedings of the National Academy of Sciences of the United States of America、Developmental Cell、Plant Cell、Molecular Plant、EMBO Reports、New Phytologist和Plant Physiology等国际期刊发表论文30余篇。冯汉青, 西北师范大学生命科学学院教授, 入选甘肃省“飞天学者”特聘人才计划。长期从事植物学理论及应用研究工作。以第一或通讯作者在New Phytologist、Molecular Plant Pathology、Planta、BMC Plant Biology、Bioresources and Bioprocessing、Ecotoxicology and Environmental Safety以及《植物学报》和《植物生理学报》等国内外学术期刊发表论文50余篇。
*E-mail: ;
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During plant-pathogen interactions, SUMOylation regulates the immune functions of fungal pathogenicity proteins, effector proteins and immunity-associated proteins in plant cells, as well as key transcription factors. S: SUMOylation; P: Phosphorylation; Mo: Magnaporthe oryzae (rice blast fungus); Bc: Botrytis cinerea (gray mold fungus); Vd: Verticillium dahliae (verticillium wilt fungus); SA: Salicylic acid; JA: Jasmonic acid; HR: Hypersensitive response; ROS: Reactive oxygen species; BR: Brassinosteroids; ETI: Effector-triggered immunity; X: Inhibition. Solid lines indicate direct targeting regulatory effects; Dash lines indicate the bidirec tional nature of molecular regulation.

, figureFileSmall=HApfnfYL9P15A9yO5pxC8A==, figureFileBig=5JgkakFdfbWF4lTQJ338Lw==, tableContent=null), ArticleFig(id=1319998776924811404, tenantId=1146029695717560320, journalId=1316781310003478668, articleId=1319998769962266725, language=CN, label=图1, caption=SUMO化修饰在植物与病原互作中的免疫调控网络

在植物与病原互作中, SUMO化修饰调控真菌细胞致病蛋白、植物细胞中效应蛋白和免疫相关蛋白以及关键转录因子的免疫功能。S: SUMO化修饰; P: 磷酸化; Mo: 水稻稻瘟病菌; Bc: 灰霉菌; Vd: 大丽轮枝菌; SA: 水杨酸; JA: 茉莉酸; HR: 超敏反应; ROS: 活性氧; BR: 油菜素甾醇; ETI: 效应子触发免疫; X: 抑制作用。实线表示直接靶向调控作用; 虚线表示分子调控的双向性。

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SUMO化修饰在植物与病原互作中的功能研究进展
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李文亮 1 , 冯汉青 1, * , 赖建彬 2, *
植物学报 | 特邀综述 2025,60(5): 749-758
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植物学报 |特邀综述 2025 , 60 (5) : 749 -758
SUMO化修饰在植物与病原互作中的功能研究进展
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李文亮1, 冯汉青1, * , 赖建彬2, *
作者信息
  • 1西北师范大学生命科学学院, 兰州 730070
  • 2华南师范大学生命科学学院, 广东省植物发育生物技术重点实验室, 广州 510631
通讯作者:
赖建彬, 华南师范大学生命科学学院教授, 广东省特支计划科技创新青年拔尖人才。长期从事棕榈酰化和SUMO化等翻译后修饰调控植物抗逆研究。以通讯作者(含共同)在Trends in Plant Science、EMBO Journal、Proceedings of the National Academy of Sciences of the United States of America、Developmental Cell、Plant Cell、Molecular Plant、EMBO Reports、New Phytologist和Plant Physiology等国际期刊发表论文30余篇。冯汉青, 西北师范大学生命科学学院教授, 入选甘肃省“飞天学者”特聘人才计划。长期从事植物学理论及应用研究工作。以第一或通讯作者在New Phytologist、Molecular Plant Pathology、Planta、BMC Plant Biology、Bioresources and Bioprocessing、Ecotoxicology and Environmental Safety以及《植物学报》和《植物生理学报》等国内外学术期刊发表论文50余篇。
Research Progress on SUMOylation in Plant-Pathogen Interactions
Li Wenliang1, Feng Hanqing1, * , Lai Jianbin2, *
Affiliations
  • 1College of Life Sciences, Northwest Normal University, Lanzhou 730070, China
  • 2Guangdong Provincial Key Laboratory of Plant Development Biotechnology, College of Life Sciences, South China Normal University, Guangzhou 510631, China
  • Corresponding Author:
出版时间: 2025-09-10 doi: 10.11983/CBB25106
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SUMO化修饰是植物中重要的翻译后修饰, 通过介导底物蛋白的功能、免疫信号的激活与转导以及激素信号网络, 在植物免疫调控中发挥关键作用。该文从SUMO化修饰系统的酶联反应机制、SUMO化修饰参与植物免疫调控以及病原体效应蛋白对SUMO化系统的干扰等方面, 系统综述了SUMO化修饰在植物与病原互作中的功能最新研究进展, 旨在解析SUMO化介导的植物免疫调控网络, 为开发基于SUMO化修饰的作物抗病新策略提供参考。

SUMO化修饰  /  病原体  /  免疫信号  /  激素信号  /  效应蛋白

SUMOylation is a crucial post-translational modification in plants, playing a pivotal role in plant immune regulation by mediating substrate protein functions, the activation and transduction of immune signals, and hormonal signaling networks. This review systematically summarizes recent research advances in SUMOylation during plant-pathogen interactions, focusing on the enzymatic cascade mechanisms of the SUMOylation system, the involvement of SUMOylation in plant immune regulation, and the interference/activation of the SUMOylation system by pathogen effector proteins. We highlight the SUMOylation-mediated regulatory networks of plant immunity and provide a reference for developing novel disease resistance strategies in crops based on SUMO modification.

SUMOylation  /  pathogen  /  immune signaling  /  hormonal signaling  /  effector protein
李文亮, 冯汉青, 赖建彬. SUMO化修饰在植物与病原互作中的功能研究进展. 植物学报, 2025 , 60 (5) : 749 -758 . DOI: 10.11983/CBB25106
Li Wenliang, Feng Hanqing, Lai Jianbin. Research Progress on SUMOylation in Plant-Pathogen Interactions[J]. Chinese Bulletin of Botany, 2025 , 60 (5) : 749 -758 . DOI: 10.11983/CBB25106
植物在生长发育过程中一直面临病原微生物(如细菌、真菌和病毒)介导的生物胁迫。为了适应并应对这些生物胁迫, 植物进化出复杂的调控网络。其中, SUMO化修饰(small ubiquitin-like modifier, SUMOylation)作为一种重要的翻译后修饰方式, 通过调节蛋白质的活性、稳定性、定位以及蛋白互作, 赋予细胞内蛋白质多样化的功能, 在植物生长发育与防御反应中发挥关键作用(Han et al., 2022)。SUMO化修饰是将SUMO分子共价结合在底物蛋白上, 该过程高度可逆。在特定条件下, 植物通过SUMO蛋白酶(SUMO-specific proteases, SENPs)移除底物蛋白上的SUMO分子, 将其恢复到未修饰状态, 维持SUMO化修饰的动态平衡, 从而精确调控细胞生命过程(Srivastava et al., 2021)。
病原菌与植物在长期的协同演变中, 进化出多种策略来破坏植物免疫系统。细菌、卵菌和真菌等病原菌利用其分泌的效应蛋白作为分子武器, 通过干扰宿主细胞正常的生理过程实现免疫逃避(Harris et al., 2023)。植物病毒通过表达必需的病毒蛋白借助宿主的翻译机制来抑制其免疫(Li et al., 2024a)。尽管植物利用SUMO化修饰等复杂的调控机制增强免疫响应, 但病原菌效应蛋白的频繁变异以及在宿主体内广泛的靶点, 仍使植物的免疫系统面临重大威胁(An and Zhang, 2024)。本文系统综述了SUMO化修饰在植物与病原相互作用中的功能最新研究进展, 重点讨论了SUMO化修饰与植物免疫调控网络以及病原菌效应子的SUMO化干扰策略, 以期揭示SUMO化修饰在植物免疫中的分子调控网络(图1)。
SUMO化修饰是真核生物中高度保守且可逆的蛋白质翻译后修饰, 通过E1激活酶(activating enzyme E1)、E2结合酶(conjugating enzyme E2)和E3连接酶(ligase E3)介导的级联酶促反应实现底物蛋白的特异性修饰(韩丹璐等, 2018)。SUMO化修饰过程始于SUMO前体蛋白被SUMO蛋白酶切割后暴露出C末端双甘氨酸基序(Gly-Gly, GG), 形成可被E1激活酶识别的成熟结构SUMO-GG。成熟的SUMO分子经E1活化、E2催化结合形成SUMO-E2硫酯中间体, 最终在E3的催化下将SUMO转移至底物蛋白赖氨酸(Lys, K)残基上, 完成底物蛋白的SUMO化修饰(Park et al., 2011)。同时SUMO蛋白酶(ubiquitin-like proteins, ULPs)切割修饰蛋白上的SUMO分子, 使其重新参与新的SUMO化修饰循环, 保持SUMO化修饰的动态平衡(Morrell and Sadanandom, 2019)。此外, E4连接酶(PIALs)可催化底物蛋白与多个SUMO分子结合形成多聚SUMO链, 扩展SUMO化修饰的功能复杂性(Han et al., 2021b)。Ghosh等(2024)指出, E4连接酶的出现是单细胞植物转变为多细胞植物的关键节点, 揭示了SUMO化修饰系统的演变与植物适应性进化密切相关。
研究表明, 利用原核系统重组真核SUMO化组分可实现底物蛋白SUMO化的体外高效检测与功能研究。黄俊文等(2022)利用大肠杆菌重组系统引入植物E3连接酶SIZ1, 可显著提高底物蛋白的SUMO化修饰效率。此外, Huang等(2025)通过大肠杆菌系统重构植物底物蛋白对应的ULP蛋白酶, 成功实现体外底物蛋白的去SUMO化修饰检测。同样, Lai等(2023)建立了玉米(Zea mays) E1、E2和成熟SUMO1分子重构的体外SUMO化检测系统, 并通过质谱分析验证了底物蛋白的SUMO化修饰。这些SUMO化修饰检测系统为深入探索植物蛋白质SUMO化修饰功能提供了有效的外源工具。
在完整的SUMO化修饰过程中, E1激活酶负责活化SUMO分子, 其在植物中由1对异源二聚体SAE1 (SUMO activating enzyme subunit 1)和SAE2构成(Castaño-Miquel et al., 2013)。E2结合酶(SUMO conjugation enzyme, SCE)是SUMO转移的核心, 其催化活性依赖于高度保守的半胱氨酸残基。在特殊情况下, E2结合酶可单独介导底物蛋白与SUMO分子的共价结合, 增强底物蛋白的特异性(Ghimire et al., 2021)。拟南芥(Arabidopsis thaliana)仅包含1个E2结合酶SCE1, 其保守的半胱氨酸残基突变导致SUMO偶联复合物减少, 且AtSCE1敲除突变体表现出发育停滞和胚胎致死, 表明该酶不仅在SUMO化修饰中具有核心作用, 还与植物发育密切相关(Saracco et al., 2007; Tomanov et al., 2013)。与拟南芥相比, SUMO E2结合酶在其它作物中存在多种拷贝。例如, 水稻(Oryza sativa)含有3个E2结合酶(OsSCE1、OsSCE2和OsSCE3), 这些酶在进化过程中表现出高度保守, 其中OsSCE1为调节水稻SUMO化修饰整体水平的关键基因(Yu et al., 2024)。玉米含有7个E2结合酶(ZmSCE1a-ZmSCE1g), 其活性中心的半胱氨酸位点高度保守, 同一亚族的E2结合酶序列相似性较高。然而, 仅ZmSCE1b和ZmSCE1d参与ZmSUMO1对底物蛋白的修饰(Augustine et al., 2016; Lai et al., 2022)。马铃薯(Solanum tuberosum)含有9个E2结合酶(StSCE1-StSCE9), 这些酶具有不同的组织特异性, 分别参与细胞的多种生理过程, 是目前发现含E2最多的植物(Ghimire et al., 2020)。由此可见, 不同植物SCE基因存在家族扩张。推测这种基因家族扩张可能使不同SCE成员响应不同病原体攻击和非生物胁迫, 或在特定组织器官中发挥作用, 从而增强植物适应复杂环境的能力。同时, 这种功能分化可能源于植物在长期进化过程中对多样化环境压力的适应性进化, 使得SUMO化修饰系统能够更精细地调控植物的生长发育与逆境响应之间的平衡。未来可探索不同SCE蛋白在多种环境条件下功能的分化与协调, 以及它们如何通过SUMO化修饰影响植物的生长发育与防御能力。
同样, E3连接酶亦是增强底物特异性与修饰效率的核心组分。植物中主要的E3连接酶包括SIZ1 (SAP AND MIZ1 DOMAIN-CONTAINING LIGASE 1)、MMS21/HPY2 (HIGH PLOIDY 2)和PIALs (PIAL1/ PIAL2), 它们均含有1个保守的SP-RING结构域(Ghosh et al., 2024)。其中SIZ1在植物中的表达丰度较高, 介导大多数底物蛋白的SUMO化修饰; 而MMS21仅介导少数低丰度蛋白的SUMO化修饰(Rytz et al., 2018); PIALs主要负责将多个SUMO化链添加到底物蛋白上, 但对SUMO化链形成并非必需。E2结合酶在缺少PIALs的情况下仍能形成SUMO化链(Ghosh et al., 2024)。研究发现, SIZ1的SP-RING结构域突变严重损害体内SUMO化修饰水平(Cheong et al., 2009)。同时SIZ1对维持植物全基因组SUMO化修饰水平至关重要(Han et al., 2021a), 表明SIZ1在调控SUMO化修饰中起关键作用。
Colignon等(2017)发现在致病疫霉感染的马铃薯中, SUMO化修饰通路核心基因(SAE1、SCE1和SIZ1)的表达水平显著上升, 表明植物会激活SUMO化修饰系统响应病原入侵。同时, Castaño-Mique等(2017)通过在拟南芥中过表达E1 SAE2UFDCt结构域破坏SUMO E1与E2之间的相互作用, 导致转基因植物对灰葡萄孢菌和黄瓜葡萄孢菌的易感性增强, 证实SUMO化修饰参与植物免疫调节。Skelly等(2019)进一步发现, SUMO化修饰组分E2结合酶SCE1第139位半胱氨酸的巯基亚硝基化(S-nitrosylation)可通过解除SUMO1/ 2的抑制作用, 调节植物整体的SUMO化修饰水平, 驱动免疫信号的激活, 暗示SUMO化修饰调控植物免疫网络的复杂性(Skelly et al., 2019)。综上, SUMO化修饰在植物免疫调控中具有重要作用。
植物先天免疫的激活依赖于模式识别受体对病原信号的精准识别及其触发的胞内信号转导。受体激酶FLS2 (FLAGELLIN SENSING 2)与共受体BAK1 (BRI1 (BRASSINOSTEROID INSENSITIVE 1) ASSOCIATED RECEPTOR KINASE 1)形成复合物是启动基础免疫信号级联的核心事件。Orosa等(2018)发现细菌鞭毛蛋白flg22可特异性诱导模式识别受体FLS2发生SUMO化修饰, 促进胞质激酶BIK1 (BOTRYTIS-INDUCED KINASE 1)从细胞质膜FLS2-BAK1复合物释放到细胞质中, 激活下游免疫信号通路, 推测SUMO化修饰可直接介导受体蛋白调控植物免疫信号转导。有趣的是, 油菜素甾醇(brassinosteroids, BR)与免疫的共受体BAK1在感知BR处理后, 自身SUMO化修饰水平明显提高, 进而促进BR受体BRI1 (BRASSINOSTEROID INSENSITIVE 1)在质膜上与BAK1的解离, 激活BR下游信号; 但BAK1感知细胞外免疫信号分子Pep1 (plant elicitor peptide 1)并不影响其SUMO化修饰, 说明共受体BAK1的信号激活途径受到SUMO化修饰的特异性调控(Xia et al., 2025)。同时, 免疫信号分子Pep1作为损伤相关分子模式可触发植物免疫应答。
已知细胞内钙离子浓度升高可促进II型MC蛋白酶的自加工激活, 进而对定位于液泡膜表面的PROPE- P1进行加工, 使Pep1从液泡膜释放进入细胞质, Pep1被PEPR受体识别后激活或强化植物免疫反应(Shen et al., 2019)。Zhang等(2025)发现植物细胞壁损伤造成胞内钙离子浓度升高, 诱导SUMO E3连接酶SIZ1的表达, 促进免疫信号分子Pep1前体蛋白PROPEP1发生SUMO化修饰, 进而增强PROPEP1与钙离子依赖蛋白酶MC4的互作, 加速免疫信号分子Pep1的切割生成, 提高植物对细胞壁损伤的抗性。此外, 在胞内免疫信号转导中, Verma等(2021)发现MPK3/6通过SUMO互作基序(SUMO interacting motif, SIM)特异性识别被SUMO化修饰的转录因子WRKY33, 介导其磷酸化以激活转录活性, 诱导植物的抗病反应。由此可见, SUMO化修饰已成为调控植物免疫信号转导的核心, 确保植物快速精准地响应病原危险信号。
尽管免疫反应的激活可增强植物抗病性, 但过度防御常伴随着能量消耗和生长受抑制。为此, 植物演化出SUMO化修饰依赖的“免疫刹车”系统, 以精确调控免疫与生长的动态平衡。早期研究表明, 拟南芥SIZ1功能缺失突变体因整体SUMO化修饰水平下降, 导致植物体内水杨酸(salicylic acid, SA)过度积累以及抗病相关基因表达上调, 进而产生植株矮小和自身免疫表型, 并对丁香假单胞菌番茄致病变种DC3000 (Pseudomonas syringae pv. tomato DC3000, Pst DC3000)的抗性增强(Lee et al., 2007)。研究发现SIZ1自身免疫表型源于其介导细胞核中转录抑制因子TPR1 (TOPLESS-RELATED 1) SUMO化修饰对植物免疫反应的抑制作用(Niu et al., 2019)。当SIZ1缺失时, TPR1与组蛋白去乙酰化酶HDA19 (HISTONE DEACETYLASE 19)的互作增强, 导致抗病蛋白SNC1 (SUPPRESSOR OF NPR1-1 CONSTITUTIVE 1)与TPR1激活免疫反应; 在野生型中, SIZ1通过SUMO化修饰抑制TPR1蛋白活性, 以维持SNC1/TPR1复合物的非活性状态, 从而避免因过度激活免疫而抑制植物生长发育(Gou et al., 2017; Niu et al., 2019)。类似地, Xie等(2024)发现SIZ1与核孔蛋白NUA (NUCLEAR PORE ANCHOR)及SUMO蛋白酶EDS4 (EARLY IN SHORT DAYS 4)协同调控TPR1的SUMO化修饰, 实现免疫与生长的平衡。当NUA缺失时, TPR1过度SUMO化导致其活性降低, 降低SA的积累及抗病基因表达; 在野生型中, NUA与ESD4互作促进TPR1的去SUMO化, SIZ1控制TPR1的SUMO化稳态, 以维持适当的免疫输出强度, 确保植物正常生长发育。此外, 在高温条件下, SIZ1通过调控COP1 (CONSTITUTIVE PHO-TOMORPHOGENIC 1)的SUMO化修饰作为SNC1依赖性免疫反应的负调节因子, 在植物免疫与生长发育之间建立动态平衡(Hammoudi et al., 2018)。这种通过SUMO化修饰调控免疫与生长平衡的机制在单子叶植物中是否保守尚不明确。最近, 在玉米中的研究为我们提供了线索。研究发现, 玉米ZmSIZ1a/b在维持这种平衡中发挥关键作用。Liao等(2023)发现ZmSIZ1a/b功能缺失突变体表现出生长发育受阻的表型, 且在高温下SUMO化修饰水平明显降低, 双突变体对玉米穗粒腐病的抗性显著减弱, 推测其可能与ZmSIZ1介导的SUMO化修饰调控黄酮类化合物合成受阻有关, 进而参与调控抗病与生长发育的平衡。综上, SIZ1介导的SUMO化修饰通过对关键免疫因子和信号节点进行动态可逆的修饰, 精细调控免疫反应的信号强度。这种机制可能在不同物种中具有保守性和特异性。在特定时间内底物蛋白的SUMO化修饰对生物体免疫信号产生不同的影响, 而植物免疫信号强度的正向或负向输出取决于底物蛋白的SUMO化修饰。
Verma等(2018)发现SUMO化修饰在细胞内与植物激素信号网络重合, 可动态调控植物免疫信号。SA和茉莉酸(jasmonic acid, JA)是调控植物抗病反应的核心信号分子, 其拮抗关系构成植物免疫信号网络的核心框架。其中SA正向调节活体营养型病原体的免疫反应, 而JA有助于增强对坏死性病原体的防御能力。此外, 在某些病理系统中, JA也作为效应子触发免疫(effector-triggered immunity, ETI)的正调节因子(Sharma et al., 2021)。在拟南芥中, NPR1 (nonexpressor of pathogenesis-related (PR) genes 1)与其旁系同源物NPR3/NPR4以不同的亲和力结合SA, 已证实其是SA的受体(Fu et al., 2012; Wu et al., 2012)。有趣的是, SA的结合导致NPR1的构象发生变化, 促进NPR1二聚体的锚蛋白重复序列ANK (Ankyrin repeats) C末端SBD (salicylic acid-binding domain)发生折叠并与ANK相互作用, 而SBD-ANK对接构象可以实现翻译后修饰, 促进未知转录调节因子的募集, 提高NPR1重编程防御转录组的活性(Kumar et al., 2022)。这暗示翻译后修饰可能在NPR1转录活性中发挥作用。Saleh等(2015)发现SA积累会诱导NPR1的SUMO化修饰, 导致其与WRKY70解离, 而SUMO化修饰激活NPR1 Ser11/15的磷酸化, 产生更多激活的NPR1与转录激活因子TGA3相互作用, 从而诱导PR1基因的表达; 同时, SUMO化修饰的NPR1与NPR3-CRL3 (Cullin 3 RING E3 ligase)相互作用后被泛素化降解, 确保免疫诱导的瞬时性, 从而实现对植物免疫反应的精确控制。Zavaliev等(2020)发现病原感染部位SA浓度的升高可诱导细胞核中NPR1单体SUMO化修饰, 促进其被NPR3/4-CRL3复合物降解, 解除对ETI的抑制, 进而激活超敏反应, 形成物理防御屏障, 以限制病原菌扩散。由此可见, SA信号输出强度依赖于SUMO化修饰对NPR1蛋白的动态调控, 也表明动态的翻译后修饰可调控单个蛋白与不同伙伴蛋白合作并执行多重功能或响应多重应激反应。Srivastava等(2018)发现, 在JA信号通路中, SUMO蛋白酶OTS1/2 (OVERLY TOLERANT TO SALT 1/2)通过介导JA信号抑制因子JAZ (jasmonate ZIM- domain)蛋白的SUMO化修饰, 形成SUMO化JAZ与JA受体COI1 (CORONATINE- INSENSITIVE 1)互作, 阻断COI1对非SUMO化JAZ蛋白的降解, 在不改变JA水平的前提下抑制JA信号转导, 进而增强植物对坏死性病原体的敏感性。这暗示SUMO化修饰在调控JA信号通路中表现出一种独特的分子制动机制。由此可见, SUMO化修饰在SA和JA激素信号通路中发挥“分子开关”作用, 确保免疫响应的精确性与平衡性。
植物与病原体长期相互作用驱动了双方的协同进化, 植物进化出多层级的免疫系统以抵御病原体入侵, 而病原体也相应地发展出多种策略来劫持或干扰宿主的免疫反应。其中, 病原体劫持宿主SUMO化修饰系统的策略尤为关键, 病原体通过靶向宿主SUMO化修饰途径抑制植物的防御反应, 增强自身的致病能力。
在细菌病原体中, 依赖分泌系统入侵宿主的效应蛋白是其致病性的关键武器。研究表明, 有些细菌效应蛋白能够直接靶向植物SUMO化修饰途径。已证实黄单胞菌(Xanthomonas campestris pv. vesicatoria, Xcv)效应蛋白AvrXv4和XopD能够直接调节宿主的SUMO化修饰途径。AvrXv4具有SUMO蛋白酶活性, 其在植物细胞内过表达导致宿主SUMO化修饰蛋白的丰度降低(Roden et al., 2004)。XopD则通过去SUMO化酶活性, 特异性靶向番茄(Lycopersicon esculentum)细胞核中的转录因子SIERF4, 从而抑制乙烯介导的免疫反应, 为病原体的生长创造有利条件(Kim et al., 2013)。类似地, 在植物叶片气孔成功定殖的丁香假单胞菌, 其效应蛋白HopB1切割共受体BAK1的能力受到宿主SUMO化修饰的抑制, 而效应蛋白HopG1则借助植物SUMO化修饰系统, 抑制细胞线粒体活性和产生活性氧(reactive oxygen species, ROS), 削弱宿主的免疫防御(Li et al., 2024b)。这表明细菌效应蛋白可通过模拟宿主SUMO蛋白酶活性、利用SUMO化修饰底物以及干扰宿主SUMO化修饰底物功能等策略, 直接破坏植物的免疫反应。
真菌病原体同样进化出依赖宿主SUMO化修饰系统的效应蛋白。SUMO化修饰对水稻稻瘟病菌(Magnaporthe oryzae)的菌丝生长、孢子形成、效应蛋白分泌及致病性至关重要(Liu et al., 2018)。此外, 灰霉菌(Botrytis cinerea)热休克蛋白(Hsp70) BcSsb和E3泛素连接酶BcRad18是SUMO化修饰的底物, BcSsb通过SUMO化修饰调控微管蛋白的积累, 从而影响微管的稳定性, 进而调控菌丝的低温适应性; BcRad18则通过SUMO化修饰调控滑动夹蛋白增殖细胞核抗原(PCNA)的单泛素化, 调控其氧化损伤耐受性(Shao et al., 2023)。大丽轮枝菌(Verticillium dahliae)烯醇酶VdEno (V. dahliae Enolase)通过SUMO化修饰介导自身核质分布, 协调其作为转录抑制因子和糖酵解酶的双重功能, 控制效应蛋白VdSCP8的表达以促进致病毒力(Wu et al., 2023)。稻瘟病菌的效应蛋白MoHTR1则借助宿主SUMO化修饰系统维持自身稳定性与细胞核定位, 促进水稻免疫相关基因的转录重编程, 进而抑制水稻免疫(Lim et al., 2024)。研究表明, 真菌病原体对宿主的致病性依赖SUMO化修饰, 这为探明真菌与植物互作提供了切入点, 也表明SUMO化修饰在植物与病原互作中起关键作用。
与细菌和真菌病原体不同, 病毒与植物SUMO化修饰存在复杂的双向博弈机制。病毒不仅通过表达蛋白靶向SUMO化通路核心组分, 破坏SUMO化修饰稳态, 还直接靶向破坏植物关键激素受体的SUMO化修饰, 实现免疫逃避。例如, 双生病毒蛋白Rep和AL1通过结合宿主SUMO E2结合酶SCE1, 促进病毒复制。但AL1只改变宿主底物蛋白的SUMO化修饰状态, 不影响整体的SUMO化水平(Sánchez-Durán et al., 2011)。而Rep与SCE1结合可以特异性干扰植物增殖细胞核抗原(proliferating cell nuclear antigen, PCNA)的SUMO化修饰, 进而增强病毒感染能力(Arroyo-Mateos et al., 2018)。胡萝卜(Daucus carota)斑驳病毒蛋白ORF4通过劫持宿主SUMO化修饰系统靶向胞间连丝, 促进病毒在植物体内的扩散(Jiang et al., 2021)。值得注意的是, 芜菁花叶病毒RNA依赖性RNA聚合酶(NUCLEAR INCLUSION B, NIb)直接靶向SA受体NPR1, 依赖SCE1介导的SUMO化修饰抑制宿主免疫反应并促进病毒RNA复制(Xiong and Wang, 2013; Cheng et al., 2017)。研究表明, NIb通过靶向NPR1的SIM结构域, 阻碍NPR1的SUMO化修饰, 进而抑制NPR1磷酸化及PR基因表达, 实现免疫逃避(Liu et al., 2023)。面对芜菁花叶病毒的侵染, 植物同样进化出精密的SUMO化反制策略。SCE1通过介导植物Pelota蛋白的SUMO化修饰, 促进Pelota蛋白募集伴侣蛋白Hbs1 (GTPase Hsp70 subfamily B suppressor 1), 特异性识别芜菁花叶病毒RNA的GA基序并触发其降解(Ge et al., 2023)。有趣的是, 病毒亦演化出对抗机制。NIb通过自身保守的SIM3结构域充当SUMO化修饰诱饵靶向SCE1, 通过破坏植物Pelota蛋白依赖SCE1的SUMO化修饰, 抑制Pelota介导的RNA识别与降解, 从而逃避宿主RNA质量监控系统以促进感染(Ge et al., 2025)。由此可见, SUMO化修饰的核心组分SUMO E2结合酶SCE1是病毒实现感染和传播的关键靶标。推测病毒可能将SUMO化修饰系统作为其调节生命周期的辅助工具加以利用, 而不同病毒对植物SUMO化修饰系统的干扰是否具有普遍性或特异性? 植物是否进化出新的机制来应对病毒的干扰? 这些问题需要深入研究。
SUMO化修饰作为植物免疫调控的核心因子, 通过精确修饰免疫受体、信号转导节点及激素信号通路成分, 使植物的免疫与生长保持动态平衡(Verma et al., 2018; Xie et al., 2024)。然而, 在与植物长期共进化过程中, 病原微生物进化出多维度劫持策略来破坏宿主SUMO化稳态以促进自身侵染。特别是病毒精准靶向SUMO E2结合酶SCE1, 实现对SCE1功能的双向操纵, 既促进自身复制, 又抑制其对免疫蛋白的修饰, 从而巧妙地实现免疫逃避, 显示出SUMO化修饰系统在植物与病原互作中“武器化”的复杂性(Soni et al., 2024)。
植物细胞拥有丰富的模式识别受体(pattern recognition receptors, PRRs)和NLR免疫受体(nucleotide-binding domain and leucine-rich repeats, NLRs), 这些蛋白构成了精细的植物免疫网络。尽管已有受体免疫相关的SUMO化修饰底物蛋白(如FLS2和BAK1)被报道, 但大量的免疫受体是否受到SUMO化修饰仍不清楚。虽然Ingole等(2021)对病原诱导拟南芥防御反应进行质谱分析, 鉴定出261种SUMO1底物, 但其中仅有29种免疫候选底物。Sang等(2024)利用高灵敏SUMO化组学鉴定技术, 在拟南芥中鉴定出 1 300个底物蛋白, 其中包括49种SUMO化修饰蛋白激酶, 显著扩展了对植物SUMO化修饰底物的理解。由此可见, 利用常规组学手段挖掘出的免疫受体激酶仍然有限, 侧面反映了SUMO化修饰的动态可逆性和对免疫受体调控的节点性。鉴于此, 未来研究可基于时空组学进一步挖掘和鉴定免疫相关的SUMO化修饰底物。目前在SUMO化修饰调控植物免疫的研究中还存在一些疑问。例如, 已知与免疫相关的SUMO化底物蛋白是否具有广谱响应性? 在病原体侵染期间, 植物SUMO化系统如何整合外界环境调控自身免疫信号, 同时病原体侵染植物是否也需要考虑外界环境实现免疫逃避? 植物体内是否存在SUMO code? 即特定的SUMO链是否像泛素化一样, 决定着底物蛋白的特定命运? 对这些问题的解答将有助于我们深入理解SUMO化修饰的多样性和特异性。此外, 在自然环境下, 温度、湿度及光照等环境因素如何动态调节SUMO化修饰系统, 进而影响植物对病原体的抗性? 研究SUMO化修饰响应病原体和植物细胞各种环境胁迫的精确调节机制, 有助于阐明环境-SUMO-免疫三者间的联动机制, 对于培育广谱抗病和环境适应性强的作物品种至关重要。
尽管目前的研究已经揭示了病原体效应子劫持宿主SUMO化修饰系统的多种机制, 但也有许多问题需进一步探索。例如, 不同病原体效应子在宿主细胞内如何精准识别和靶向SUMO化修饰途径的关键组分? 病原体效应子如何在不同的环境条件下动态调节宿主SUMO化修饰以适应自身的生存需求? 植物如何感知并应对病原体对SUMO化修饰系统的劫持? 探明这些问题将有助于揭示植物与病原体之间复杂的互作机制, 并为开发新的植物抗病策略提供理论依据。
李文亮: 构思并撰写论文; 冯汉青: 指导论文构思; 赖建彬: 指导论文构思并修改论文。
  • 国家自然科学基金(32270752)
  • 甘肃省科技计划-自然科学基金重点项目(24JRRA124)
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2025年第60卷第5期
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doi: 10.11983/CBB25106
  • 接收时间:2025-06-06
  • 首发时间:2026-10-22
  • 出版时间:2025-09-10
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  • 收稿日期:2025-06-06
  • 录用日期:2025-07-01
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国家自然科学基金(32270752)
甘肃省科技计划-自然科学基金重点项目(24JRRA124)
作者信息
    1西北师范大学生命科学学院, 兰州 730070
    2华南师范大学生命科学学院, 广东省植物发育生物技术重点实验室, 广州 510631

通讯作者:

赖建彬, 华南师范大学生命科学学院教授, 广东省特支计划科技创新青年拔尖人才。长期从事棕榈酰化和SUMO化等翻译后修饰调控植物抗逆研究。以通讯作者(含共同)在Trends in Plant Science、EMBO Journal、Proceedings of the National Academy of Sciences of the United States of America、Developmental Cell、Plant Cell、Molecular Plant、EMBO Reports、New Phytologist和Plant Physiology等国际期刊发表论文30余篇。冯汉青, 西北师范大学生命科学学院教授, 入选甘肃省“飞天学者”特聘人才计划。长期从事植物学理论及应用研究工作。以第一或通讯作者在New Phytologist、Molecular Plant Pathology、Planta、BMC Plant Biology、Bioresources and Bioprocessing、Ecotoxicology and Environmental Safety以及《植物学报》和《植物生理学报》等国内外学术期刊发表论文50余篇。
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2种不同金属材料的力学参数
科
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属数
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genus
种数
Number of
species
占总种数比例
Percentage of
total species (%)
属
Genus
种数
Number of
species
占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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