引用本文
李冬月, 原文霞, 郑超, 王栩鸣, 周洁, 严成其, 陈剑平. bZIP转录因子在植物激素介导的抗病抗逆途径中的作用[J]. 浙江农业学报, 2017,29(1): 168-175.
LI Dongyue, YUAN Wenxia, ZHENG Chao, WANG Xuming, ZHOU Jie, YAN Chengqi, CHEN Jianping. Roles of bZIP transcription factors in phytohormone-mediated disease resistance and stress tolerance[J]. ACTA AGRICULTURAE ZHEJIANGENSIS, 2017,29(1): 168-175.
  
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bZIP转录因子在植物激素介导的抗病抗逆途径中的作用
李冬月1,2, 原文霞1,2, 郑超1,2, 王栩鸣2, 周洁2, 严成其1,2,*, 陈剑平1,2,*
1.浙江师范大学 化学与生命科学学院,浙江 金华321004
2.浙江省农业科学院 病毒学与生物技术研究所,浙江省有害生物防控国家重点实验室培育基地,农业部植保生物技术重点实验室,浙江省植物病毒重点实验室,浙江 杭州310021
*通信作者,严成其,E-mail:yanchengqi@163.com;陈剑平,E-mail:jpchen2001@126.com

作者简介:李冬月(1990—),女,河南南阳人,硕士研究生,主要从事植物病理学研究。E-mail:dongyueli2015@163.com

收稿日期: 2016-04-22
基金资助: 国家科技部973前期(2014CB160309); 浙江省自然科学基金(2014C140001,2013C11009)
摘要

植物体内有一套复杂精细且交叉调控的激素信号网络,在植物应对不良环境胁迫的过程中起着至关重要的作用。bZIP转录因子作为基因表达的关键调控因子,在植物抗病抗逆相关基因的表达中行使着重要的功能。文章首先介绍了bZIP转录因子的结构和功能,阐述了其在几种主要的激素抗性调控途径中的作用机理,之后对各种激素信号通路之间的交叉调控途径及其关键调控节点蛋白进行了概括,以期阐明植物激素介导的抗性调控网络,并为新的抗性相关基因的挖掘和利用提供理论依据。

关键词: bZIP转录因子; 植物激素; 抗病; 抗逆; 信号调控
中图分类号:S184;Q945.8 文献标志码:A 文章编号:1004-1524(2017)01-0168-08 doi: 10.3969/j.issn.1004-1524.2017.01.23
Roles of bZIP transcription factors in phytohormone-mediated disease resistance and stress tolerance
LI Dongyue1,2, YUAN Wenxia1,2, ZHENG Chao1,2, WANG Xuming2, ZHOU Jie2, YAN Chengqi1,2,*, CHEN Jianping1,2,*
1. College of Chemistry and Life Sciences,Zhejiang Normal University,Jinhua 321004,China
2. State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control,MOA Key Laboratory for Plant Protection and Biotechnology,Zhejiang Provincial Key Laboratory of Virology,Institute of Virology and Biotechnology,Zhejiang Academy of Agricultural Sciences,Hangzhou 310021,China
Abstract

The elaborate phytohormone regulating networks in plants and their crosstalk pathways play critical roles in adapting to various environmental stresses of plants. As the key regulators in gene expression, bZIP transcription factors control important processes in relation to plant biotic and abiotic stress responses. In this review, we firstly introduced the structure and functions of the bZIP transcription factors, expounded their regulation mechanism in several major hormone-mediated signaling pathways. Subsequently, we discussed the crosstalk pathways between different hormones and made a summary of the key crosstalk integrators in defense processes. The aim of this review was to illuminate plant hormone-mediated signal interactions under stress and provide theoretical bases for exploring and utilizing new resistance genes.

Keyword: bZIP transcription factors; plant hormones; disease resistance; stress tolerance; signal regulation

植物激素不仅在植物的生长发育过程中担任重要角色, 在植物的抗病抗逆信号传导途径中也发挥着重要的作用[1]。目前, 在植物体内研究较多的与抗性相关的激素有水杨酸(salicylic acid, SA)、茉莉酸(jasmonic acid, JA)、乙烯(ethylene, ET)、脱落酸(abscisic acid, ABA)、细胞分裂素(cytokinin, CTK)和油菜素内酯(brassinosteroid, BR)等。植物体内直接参与抗病和抗逆的基因并不多, 但是调控这些基因表达的途径却十分复杂。每一条抗性信号通路的开启都需要许多上游关键调控因子的共同作用。当植物体受到外界病原菌和环境等的胁迫时, 其体内的激素、NO[2]和Ca2+等特定信号分子会与植物细胞内的受体蛋白结合, 通过调节各种胞内转录因子, 进而启动相应的抗性基因表达。转录因子是一类调控基因表达的蛋白, 常常参与植物的生长发育、抗病抗逆等调控途径[3], 它通过识别并结合在目标基因上游的启动子区域来激活或抑制靶基因的表达。

bZIP、NAC、MYB、AP2/ERF、WRKY等是植物中常见的转录因子家族。这些转录因子通常作为正向或负向的调控因子在植物激素介导的抗病抗逆信号调控中起作用。VNI2是NAC转录因子家族基因之一, 通过调控响应寒冷和脱水等相关的一系列基因的表达来参与ABA介导的非生物胁迫信号转导[4]。MYB转录因子家族的S1亚家族基因MYB60和MYB96通过ABA介导的信号调控通路来调节拟南芥保卫细胞的运动和植株的抗病性[5, 6]。AP2/ERF转录因子家族庞大, 响应植株的生物和非生物胁迫, 且常常在ET、JA、SA等激素介导的信号转导及信号交叉调控中起作用。WRKY转录因子为植物特有的锌指型转录因子, 在SA介导的抗病途径中起着重要作用。用水杨酸的衍生物BTH(benzothiodiazole)处理水稻3 h后, 其体内的WRKY45基因的表达明显上调, 过表达WRKY45的转基因水稻对稻瘟菌的抗性明显增强, 将WRKY45基因敲除后, 由BTH诱导的植物对稻瘟菌的抗性受到抑制[7]。

植物bZIP转录因子功能繁多, 因而广泛参与各种激素介导的信号转导通路。有时, bZIP转录因子也通过与其他转录因子相互作用, 共同调控激素介导的信号转导途径。本文就bZIP转录因子的分类、功能以及其在各种激素信号途径中的作用进行系统综述, 以期为抗病抗逆相关基因及其功能的挖掘和应用提供理论基础。

1 植物bZIP转录因子的结构及功能

随着生物信息学的快速发展, 科研工作者对水稻[8]、拟南芥[9]、高粱、苹果[10]等测序完成的植物进行了全基因组转录因子的预测和统计。结合大多数bZIP转录因子家族成员的功能特点, 将其结构分为两大部分:一是其N端均包含由一个不间断的α -螺旋组成的结合DNA的结构域, 该结构域由大约20个碱性氨基酸残基组成, 主要是能够识别启动子上的特定元件, 并与之结合; 二是C端的亮氨酸拉链寡聚结构域, 其以每7个氨基酸为一个单位, 第7位为一个亮氨酸, 两个bZIP转录因子在其亮氨酸结构域的寡聚作用下结合在一起, 形成拉链状的螺旋结构[11, 12], 该结构域主要是行使转录激活功能或者抑制基因转录表达的功能。由于bZIP转录因子是对基因的转录进行调控, 因此其通常定位于细胞核[13]。此外, 有些含有寡聚化结构域的转录因子通常形成二聚体或多聚体复合物, 在细胞核中行使功能[14]。根据拟南芥中bZIP转录因子的结构域特点和功能特性将其再细分为10个亚家族, 名为A-I和S亚家族[15, 16], 包括与ABA和非生物胁迫相关的ABF亚家族[17], 与抗病相关的TGA亚家族[18], 与光信号调控相关的GBF亚家族和HY亚家族等[19], 在此不作一一阐述。

作为最大的转录因子家族之一, 不同植物bZIP转录因子监管着各种转录调控机制, 如植物的生长发育、衰老[20]、激素调控[17]、能量代谢[21]、病原防御[22]和非生物胁迫[23]等。Zou等[24]从水稻圆锥花序中分离出了OsABI5基因, 抑制该基因的表达会降低水稻的育性。辣椒的CAbZIP1基因, 其仅在根和花中表达, 在叶片、茎和果实中不表达。且CAbZIP1转基因拟南芥出现矮化的表型, 由此推测该基因可能与植物的生长发育相关[11]。关于bZIP转录因子在植株的生物、非生物胁迫中的功能研究, Lee等[12]研究认为, 辣椒CAbZIP1基因不仅在植株中组成型表达, 对感染辣椒斑点病菌(Xanthomonas.campestris pv.vesicatoria)的辣椒植株进行检测, 发现CAbZIP1基因还受病原菌诱导表达。在拟南芥中超表达CAbZIP1基因, 可以增强植株对番茄丁香假单胞杆菌(Pseudomonas syringae pv. tomato, DC3000)的抗性, 还能诱导拟南芥抗性相关基因AtRP-4和AtRD29A的表达。水稻的OsbZIP71基因, 在干旱、PEG以及ABA处理后, 其基因表达量显著增高, 而盐处理后其表达受到抑制。过表达OsbZIP71基因可提高水稻植株对干旱、盐和ABA等的耐受性。对该基因进行沉默, 发现水稻对干旱、盐、PEG和ABA胁迫的敏感度增高, 说明OsbZIP71基因在水稻的非生物胁迫中起着重要的作用[25]。

2 植物bZIP转录因子与激素介导的抗性途径
2.1 植物bZIP转录因子与水杨酸(SA)介导的抗病途径

水杨酸(SA)介导的抗病信号通路主要是针对活体营养型或者半活体营养型病原菌的侵袭, 也就是所谓的系统获得性抗性(system acquired resistance, SAR)[26]。SAR是一种高效的先天性免疫应答反应, 能抵御多种病原菌, 由水杨酸或者它的衍生物INA(2, 6-dichloroisonicotinic acid)和BTH(benzothiodiazole)诱导产生[27, 28]。SA介导的抗病通路与NPR1蛋白和TGA转录因子密切相关[29]。TGA类转录因子是bZIP家族的重要亚家族之一, 在植物SA激素介导的抗病信号转导中起重要的调控作用。当病原菌侵入植物细胞后, 植物体内的水杨酸(SA)快速积累, 致使细胞内的还原势增加, 多聚体NPR1蛋白中的二硫键断裂形成单体的NPR1分子, 进入细胞核与二聚体化的TGA转录因子结合, 联合NAC、WRKY等转录调控蛋白, 分别结合在PR基因启动子区域的特定位点上, 共同调控下游PR基因的表达[30]。目前, 在拟南芥的10个TGA转录因子中, 有7个TGA(TGA1-TGA7)基因已被成功克隆并证明在SA信号途径中起到正向或负向调控作用[18]。拟南芥中的TGA2、TGA5、TGA6中任何一个基因的功能缺失, 用水杨酸衍生物INA(2, 6-二氯异烟酸)处理, 都可诱导PR1基因的表达, 而同时敲除3个基因则INA不能诱导PR1基因表达, 说明TGA2、TGA5、TGA6转录因子均参与植株的抗性调控[31]。有些TGA转录因子在植株抗病途径中起负调控作用。在水稻中分离出rTGA2.1基因, 通过两种手段对rTGA2.1基因进行改造, 一是破坏该基因的DNA结合结构域, 使其变成无结合功能的rTGA2.1, 另一种是用dsRNA沉默水稻内源rTGA2.1基因, 分别超表达上述2个基因获得转基因植株, 研究发现, 转基因水稻对白叶枯病菌(Xoo)的抗性明显增强, 且转基因植株中PR-1b、PR10等基因的表达量也发生改变。说明rTGA2.1基因属于水稻抗病中的负调控因子[32]。

除了TGA亚家族基因, 其他的bZIP转录因子基因的表达也会受到SA激素信号的影响。在苹果中, MdbZIP34和MdbZIP48基因的表达均受SA诱导。在SA处理后的不同时间点取样, 两基因的表达量均呈现上调趋势[33]。用稻瘟病菌(Magnaporthe grisea)或SA处理水稻植株后, OsbZIP1基因的表达量迅速提高, 推测其可能参与由水杨酸介导的防御反应[34]。

2.2 植物bZIP转录因子与茉莉酸/乙烯(JA/ET)介导的抗病途径

茉莉酸(JA)和乙烯(ET)在植物的生长和对抗环境胁迫中起重要作用[35]。尤其是当植物受到食草动物伤害或机械损伤时, 其体内的JA含量会急剧上升, 同时调控体内靶基因在伤口处表达来防止外源致病菌的侵入[36, 37]。JA介导的信号途径常常和ET介导的信号通路协同调控植株对腐殖营养病原菌的抗性[38]。PDF1.2基因是拟南芥中的抗性基因, 其表达受病原菌诱导, 在JA应答途径突变或ET应答途径突变的植株中, 该基因对病原菌的响应被阻断, 说明该基因响应由JA/ET介导的抗病防御反应[39]。另外一种甾类激素油菜素内酯(BR)也与植物的生长和抗逆途径密切相关[40], 且与JA信号途径存在着协同作用。DWF4基因是BR合成的关键基因, Kim等[41]在拟南芥中过表达DWF4基因, 对其接种番茄丁香假单胞杆菌(Pst DC3000)后, 分析植株中JA介导的抗病相关基因如MYC2和PDF1.2的表达量, 发现DWF4基因通过调控MYC2和PDF1.2基因的表达来激活JA介导的抗病信号转导途径。除了JA途径之外, BR途径与SA[41]、ABA[42]等介导的抗性信号途径之间也存在着一定的关联性。另外, SA途径与JA/ET抗病信号途径在一定条件下既相互协同又相互拮抗。在SA途径中参与植株抗病性的TGA2、TGA5和TGA6转录因子在由JA/ET介导的抵抗腐殖营养病原菌的防御反应中也起调控作用[38]。水稻tga256突变体植株中由JA/ET诱导的PDF1.2基因和b-CHI基因的表达受到了影响, 使得植株对灰霉病菌变得易感。ORA59(octadecanoid-responsive Arabidopsis, AP2/ERF59)蛋白是JA和ET两条信号途径的整合者, 也是PDF1.2基因表达的调控者。SA会通过其信号途径的下游基因强烈抑制ORA59蛋白积累, 致使抗性基因PDF1.2的表达降低[43]。

2.3 植物bZIP转录因子与脱落酸(ABA)介导的抗逆途径

脱落酸(ABA)作为植物生长抑制因子, 有助于植物度过干旱、低温、高盐等不良环境[17]。通常情况下, 许多逆境胁迫相关基因受ABA信号诱导表达[34]。许多bZIP转录因子如OsbZIP46[44]、OsAREB1/OsABF2[45]、OSBZ8[46]、OsABI5/OREB1[47, 48, 49]和OsbZIP52/RISBZ5[50]等均与ABA响应元件(ABA-responsive elements, ABRE)结合并且对这些ABA响应基因的转录进行调控。水稻OsbZIP46转录因子是一个ABRE结合蛋白, 受干旱、高温、氧化应激胁迫和ABA诱导表达, 过表达内源性的OsbZIP46基因可增强植株对ABA的敏感性。对OsbZIP46基因进行一系列的敲除和结构改造, 去除其D-结构域(一个活性负调控区域), 改成一个组成型表达的基因OsbZIP46CA1。在水稻中过表达OsbZIP46CA1基因可以显著提高植物对干旱和渗透胁迫的耐受性, 芯片分析显示, OsbZIP46CA1转基因水稻中大量胁迫相关基因的表达受到激活, 其中许多为ABF/AREBs下游基因, 且OsbZIP46基因还能够与SnRK2蛋白激酶(磷酸化ABF元件)的同源物结合, 证明活化状态下的OsbZIP46转录因子是ABA信号途径和干旱胁迫应答中的正向调控因子。水稻bZIP转录因子OsABF1和OsbZIP72均为ABRE结合因子, 对ABA信号高度敏感, 且能够增强植株的耐受性[45, 51]; OSBZ8基因受ABA诱导表达, 对盐胁迫处理的水稻进行OSBZ8基因表达分析, 结果显示, OSBZ8基因在籼稻耐盐品种中表达量远远高于盐敏感的品种[46]。

另有一些bZIP转录因子负向调控ABA介导的抗病抗逆途径。OsbZIP52基因编码一个受低温(4 ℃)诱导表达的蛋白。在OsbZIP52基因过表达的水稻植株中, OsLEA3、OsTPP1、Rab25等非生物胁迫相关基因的表达量下调, 使转基因植株对寒冷和干旱的耐受力减弱, 说明OsbZIP52基因是水稻应对寒冷和干旱胁迫中的负向调控因子[50]。水稻的另一个逆境胁迫负调控基因— OsABI5, 在苗期该基因受ABA和高盐诱导表达。构建OsABI5基因过表达和干涉材料, 对其进行盐处理和PEG干旱模拟处理, 结果显示, OsABI5干涉材料具有较强的耐盐性和耐旱性, 而过表达植株经盐处理后与对照相比表现出明显的黄萎病[48]。

2.4 植物bZIP转录因子与细胞分裂素(CTK)介导的抗逆途径

细胞分裂素(CTK)是一种通过其特有的信号转导途径来调节生长发育和环境响应的植物激素[52]。CTK介导的信号调控途径与三种蛋白相关:用于感知信号的组氨酸激酶(histidine kinases, HK)受体、用于转移信号的磷酸转移酶(his-containing phosphotransfer, HP)受体和用于输出信号的调控因子(response regulators, RR)[53]。在拟南芥中RR应答调控基因分为3类, 其中的B型细胞分裂素应答调控因子(Arabidopsis type B cytokinin response regulators, ARRs)与CTK介导的抗逆途径密切相关[54]。B型ARRs中的ARR1、ARR10和ARR12基因通过其磷酸化作用调控CTK信号通路下游的相关基因的转录表达[55]。同时突变3个调控因子基因的arr1、arr10和arr12植株, 与野生型拟南芥相比, 细胞膜的稳定性增强, 花青素的合成增多, 对干旱的耐受性增强, 说明其负向调控植物对干旱胁迫的响应。

细胞分裂素(CTK)信号调控通路在一定条件下与ABA、SA等激素介导的信号通路存在着联系。CTK在延缓气孔闭合和叶片衰老中起重要作用[56]。拟南芥中ABA处理会抑制植株B类ARRs(ARR2、ARR10、ARR12)基因的表达, 这些基因调控MYB等转录因子, 进而影响CTK基因的表达[57]。在干旱条件下, 植物体内ABA含量上升, 抑制CTK相关基因表达使植物气孔关闭来延缓水分散失[58, 59]。在拟南芥中, Choi等[60, 61]研究发现, 超表达拟南芥细胞分裂素异戊烯基转移酶基因(IPT)能增强SA防御途径标志基因PR1的表达, 并加强了对丁香假单孢杆菌(Pst DC3000)侵染的保护, 且这一过程被证实是由B型生长素反应调节因子ARR2与TGA3转录因子互作并通过SA/NPR1途径来实现对抗病基因的表达调控的。

2.5 不同激素介导的抗性信号转导途径的交叉调控

植物为了生存必须对各种胁迫信号产生快速的应答反应, 而植物激素是这些防御和调控机制的关键调控者。植物通过对各种激素及其信号途径的上调或下调来抵御各种环境压力[62]。在应对各种生物、非生物胁迫时, 不同激素信号调控网络之间既相互拮抗又相互协同。除了上文中介绍到的JA/ET、CTK/SA等信号途径中存在着交叉调控外, 植物体内还存在许多信号交叉途径(表1), 通过调控关键的信号整合蛋白来影响下游抗性相关基因的表达。一定条件下ABA信号途径与CTK和IAA信号途径存在着拮抗作用。拟南芥ABI4转录因子不仅是ABA信号途径和ARR5基因表达的正向调控因子[63], 还是编码生长素极性运输蛋白PIN1的表达抑制子, 而ARR5基因在CTK介导的信号转导途径中起负调控作用[64], 由此证明ABI4基因是ABA、CTK和IAA三条激素信号通路交叉的节点。Wang等[65, 66]发现, 当ABA激素水平上升时, CTK和auxin激素水平以及运输蛋白PIN3和PIN7的表达均受到抑制。在植株生长进程中, ET和CTK途径之间也存在着交叉调控。ET介导的逆境胁迫应答反应受EIN3转录因子的调控, EIN3能抑制CBF1、CBF2、CBF3等冷胁迫相关基因的表达, 此外, 其还能抑制ARR5、ARR7等CTK激素途径抑制子基因的表达[67]。虽然ET途径干扰CTK途径信号的转导, 但其合成却受CTK途径的影响。CTK能够稳定ACS5(1-氨基环丙烷羧酸合成酶5)和ACS9, 将活性腺苷基甲硫氨酸再转换成ACC合酶, 以加快ET的合成和积累, 进而调控植物的生长进程[68]。

表1 几种植物激素介导的与胁迫相关的交叉调控途径 Table 1 The crosstalk pathways among phytohormones in response to stresses
3 小结

随着对bZIP家族基因功能和信号调控通路的深入研究, 各种转录调控因子在激素途径中的调控机理也越来越明晰, 随之也带来了许多新发现和新问题。许多激素介导的胁迫相关途径之间存在着拮抗作用和协同作用, 其通过共同的信号整合蛋白来调控植株对病原菌和环境胁迫的防御应答反应。要探明植物激素介导的完整的抗性调控网络作用机理, 必须找出各种激素信号转导的交叉调控途径, 而其关键在于对各种调控节点蛋白的研究。bZIP转录因子作为基因表达的关键调控因子, 在植物激素介导的抗病抗逆信号途径中行使重要的功能。对bZIP家族基因进行功能研究, 不仅有助于阐明植物激素介导的抗性信号调控网络, 还为新的抗性相关基因的挖掘和应用提供依据。

The authors have declared that no competing interests exist.

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