2. 四川大学生命科学学院 生物资源与生态环境教育部重点实验室，成都 610065
2. Ministry of Education Key Laboratory of Bio-Resource and Eco-Environment, College of Life Sciences, Sichuan University, Chengdu 610065
水稻作为一种主要粮食作物，养活了世界上一半以上的人口，预计到2050年世界人口将增加到90亿左右，而水稻产量至少需要翻一番[1-2]。但是在水稻生产过程中，稻瘟病、稻曲病、纹枯病、白叶枯病、细菌性条斑病和黑条矮缩病等病害，严重危害着水稻的生长发育，进而造成了极大的产量损失和品质降低，威胁着全球的粮食安全。
为了抵御各种病原物的感染，植物已经进化出复杂的防御系统，其主要由各种信号转导途径组成的复杂分子网络所构成，其中植物激素及其信号转导网络占据着重要的地位[3-5]。大量研究表明，水杨酸(Salicylates，SAs)、茉莉酸(Jasmonates，JAs)和乙烯(Ethylene，ET)在植物与病原物互作过程中发挥了关键的作用；油菜素内酯(Brassinosteroids，BRs)、赤霉素(Gibberellins，GAs)、脱落酸(Abscisic acid，ABA)、生长素(Auxin，IAA)和细胞分裂素(Cytokinins，CKs)等植物生长发育相关的激素也直接或间接地参与了植物抗病或感病反应。不同的植物激素信号通路在植物和病原物互作中行使不同的功能，且各通路之间相互关联，相互影响，协同调控着植物的生长发育以及对外防御反应，使植物无时不处在一种生理平衡之中，最大程度地保护自身。另一方面，植物病原菌入侵植物时，通过分泌多种效应蛋白、或直接分泌激素或激素类似物至植物细胞内，干扰植物激素的合成、代谢及其信号分子网络，减弱植物的抗病防御反应，达到致病目的。效应蛋白与激素网络的互作，在一定程度上决定了病原菌与寄主植物在斗争时的此消彼长。
拟南芥一直是解析植物病原物互作中植物激素分子信号网络的模式植物。然而，愈来愈多的证据表明，作为单子叶农作物的模式植物，水稻有着其独特的一面，其对于指导水稻、小麦、大麦、玉米等农作物的生产育种有着重要意义。尤其是最新开发的基因组定点编辑技术，利用其对激素信号通路关键基因的改造，直接进行分子育种，对现代水稻农业生产具有极大的推动作用。因此，本文从以上提到的几种植物激素出发，论述它们及其涉及的信号组分在水稻与病原物互作中的作用，为下一步的研究发展和生产应用提供理论依据。
1 水杨酸(SA)White等[5-7]在烟草中首次发现了SA在植物抗病中的作用。此后，SA与植物抗病性的关系逐渐得到研究者的广泛重视，目前研究表明SA参与拟南芥、烟草、水稻等多种植物的抗病性。SA是一类简单的酚类化合物，在植物的防御系统中具有重要作用，尤其是系统获得性抗性(Systemic acquired resistance，SAR)。在受到病原物侵染后，植物体内的SA大量积累，导致病程相关蛋白(Pathogenesis-related proteins，PRs)的表达，增加了植物对病原菌侵染的抗性[8-10]。
1.1 水杨酸合成代谢途径参与水稻抗病反应水稻植株内源基础SA含量较高(5 000-30 000 ng/g植株鲜重)，甚至高于受侵染的拟南芥、烟草等植物组织，高含量的SA可以作为一个内源抗氧化剂，保护水稻免受由老化、病原菌侵染及非生物胁迫带来的损伤[11-15]。Isochorismate synthase(ICS)和Phenylalanine ammonialyase(PAL)基因的同源基因负责水稻植株内SA的合成[16-18]，其中，ICS途径被认为是持续合成SA的主要来源，而PAL途径仅仅只是在局部坏死的细胞内快速的形成SA[9, 19]。当水稻被线虫(Meloidogyne graminicola和Hirschm-anniella oryzae)侵染后，OsICS在植株体内不同部位不同时期内的表达均显著下调，而OsPAL则在线虫侵染部位显著上调，在其他部位则表达不明显或者出现下调[20]，但这并不能排除PAL途径对合成SA的重要性。SA参与植物对生物和非生物胁迫响应过程，明确其合成途径的关键酶及其合成机制非常重要。
1.2 OsNPR1参与水稻抗病反应SA途径的主调控蛋白NPR1位于SA生物合成的下游，PRs基因上游。过表达OsNPR1或其同源基因，能增加水稻抗病性[21-27]。核内NPR1的表达水平对于植物诱导抗病至关重要，当植物缺失OsNPR1时，会导致SA诱导的转录缺陷，不能激活SAR反应。在没有病原物侵染时，NPR1蛋白的C端转录激活结构域被其N端BTB/POZ结构域抑制，使NPR1处于失活状态，而SA的存在使NPR1蛋白构像发生改变，解除自身抑制作用，激活NPR1[28-29]。在拟南芥中，NPR1及其同源蛋白NPR3、NPR4都具有结合SA的能力，但NPR1只在合适的平衡溶液中才能结合SA[30-33]。NPR3和NPR4都能直接结合SA，但是NPR3结合亲和力较NPR4弱。在SA浓度低时，SA与NPR4结合，通过26S蛋白酶体降解NPR1，而当病原物侵染诱导SA浓度增加时，NPR3被激活并结合SA形成NPR3-SA复合体，促进NPR1的降解。只有当SA处于合适浓度时，才能实现NPR1蛋白的积累，从而激活SA介导的转录活性，调控植物防御反应[32-36]。NPR1、NPR3和NPR4相互作用，形成植株感受并传递SA信号的模型。但是目前影响NPRs与SA结合能力的因素暂不清楚。
1.3 OsWRKY45参与水稻抗病反应除NPR1之外，水稻中SA信号途径还含有一个主调控因子WRKY45，当用SA类似物Benzothiad-iazole(BTH)处理水稻植株3 h后，OsWRKY45基因表达上调，过表达OsWRKY45可显著增强水稻对稻瘟病菌Magnaporthe oryzae的抗性[37-41]。OsWRKY45基因在水稻粳稻(OsWRKY45-1)和籼稻(OsWRKY45-2)中存在序列差异，OsWRKY45-1在第一个内含子序列中存在一个含osa-miR815b的502个核苷酸的插入，这也导致了两个WRKY45等位基因发挥着不同的作用[42]。过表达OsWRKY45-1的植株，其接种水稻白叶枯病菌Xanthomonas oryzae pv.oyrzae(Xoo)后病斑面积比野生型高10%以上，增加了植株感病性；而过表达OsWRKY45-2的植株则与之相反，病斑面积减少了30%以上[43]。OsWRKY45两个等位基因在对ABA的敏感度，盐胁迫也呈相反的响应，但是对干旱和低温胁迫则表现出相似的响应[44]。2016年研究发现，来源于OsWRKY45-1的osa-miR815b(TE-siR815b)是造成这种现象的主要原因[42]。在水稻受到Xoo侵染后，在含OsWRKY45-1的品种Dongjin中osa-miR815b(TE-siR815b)的积累增加，而含OsWRKY45-2的品种Minghui 63则无显著变化。同时在过表达OsWRKY45-1的植株(WRKY45-1-oe)中，TE-siR815b和OsWRKY45-1的转录显著增加，而在过表达OsWRKY45-2的植株(WRKY45-2-oe)中，只有OsWRKY45-2的转录显著增加，说明TE-siR815b的表达与OsWRKY45-1激活表达相关。含有W-box或类似于W-box序列的siR815 Target 1(ST1)是TE-siR815b的靶标基因，该基因在WRKY45-1-oe中的表达被抑制，而在WRKY45-2-oe中的表达却被激活，且WRKY45-1-oe中的ST1的DNA甲基化水平显著高于WRKY45-2-oe中，ST1的表达并不依赖于TE-siR815b。结果揭示了TE-siR815b通过增加ST1 DNA甲基化的水平，抑制了ST1的表达，进而导致了OsWRKY45在不同品种水稻的防御反应中具有不同作用。OsWRKY45受到MAPKs的调节作用。MAPKs偏好利用Ser/Thr-Pro作为其磷酸化靶标位点，而WRKY45含有3个作用位点。研究发现OsMPK4和OsMPK6可以在离体条件下磷酸化WRKY45蛋白，而且在SA处理后水稻细胞中OsMPK6活性迅速提高，磷酸化并激活WRKY45蛋白以应对病原侵染。Ser294和Ser299磷酸化负责激活OsWRKY45，而Thr266磷酸化则负调控OsWRKY45介导的抗病性[45-47]。这种激活效应会被由ABA调控的OsPTP1/2抑制[46]。此外，细胞核内OsWRKY45的降解也受到泛素蛋白酶系统(Ubiquitin proteasome system，UPS)调控[48]。其它WRKYs基因也参与调控水稻对病原物的抗病反应，如OsWRKY42、OsWRKY51、OsWRKY68、OsWRKY13和OsWRKY62等[49-53]。
研究人员发现，在拟南芥中WRKYs基因受到OsNPR1基因的调控，与之不同的是，在BTH诱导的防御反应中，水稻中OsNPR1和OsWRKY45是两个独立的调控途径[37-41]，但这也并不表明OsNPR1和OsWRKY45是两个绝对独立的途径。据报道，OsDjA6的RNAi植株能够显著增加水稻对M.oryzae的防御能力，且RNAi植株中OsWRKY45、OsNPR1和OsPR5的RNA水平是野生型TG394的2-4倍。同时用flg22和Chitin处理OsDjA6的RNAi植株发现，RNAi植株中活性氧(Reactive oxygen species，ROS)积累显著增加，结果表明OsDjA6作为负调控因子调控水稻PTI(PRR-triggered immunity)和SA途径[54]。这也说明在其上游可能存在能同时调控它们的基因，但仍需要进一步的研究证实。
2 茉莉酸(JA)JA及其衍生物存在于多种高等植物，参与调节植物的生长发育和植物免疫反应[55]。在拟南芥中，JA能够增强对死体营养型病原物的抗性；相反，对活体营养型病原物的敏感性增强，抗性减弱[56-59]。丁香假单胞菌Pseudomonas syringae侵染时，通过向细胞内分泌JA类似物—coronatine毒素，去干扰寄主植物的激素信号通路，达到致病的目的[60]。JA途径通过调节活性效应物JA-Ile、JA受体复合物SCFCOI1、JA转录抑制子JAZ蛋白、JA途径主要转录因子MYC2、JA衍生物MeJA、JA合成相关基因AOC和WRKY等其他信号通路转录因子之间的相互作用来调控植物防御反应[61-67]。
2.1 茉莉酸合成代谢途径参与水稻抗病反应JA能够从多方面增强水稻对植物病原真菌、细菌和病毒的抗性。如外源喷施JA能增强水稻对黄单胞杆菌Xanthomonas oryzae的抗性[68]，还能增强小麦对白粉病的抗性[69-70]；JA通过苯丙氨酸途径诱导水稻对立枯丝核菌Rhizoctonia solani的抗性，外源喷施JA 5 d后，选择完整的叶鞘接种R.solani，接种4 d后发现JA处理的植株能够形成木质素以抑制病原菌扩展[71]；此外，叶面喷施茉莉酸甲酯(MeJA)降低了水稻黑条矮缩病(Rice black-streaked dwarf virus，RBSDV)的发病率，证实JA能够增加水稻对RBSDV的抗性[72]。与野生型相比，JA合成途径基因OsAOC缺失突变体对M.oryzae抗性降低，表现为菌丝生长更快且JA含量降低，揭示OsAOC能通过JA信号途径调控水稻对M.oryzae的免疫反应[73]；另一方面，过表达OsWRKY30可诱导JA途径中OsLOX，OsAOS2表达，同时伴随内源JA积累，对M.oryzae和R.solani的抗性增强[74]。
2.2 茉莉酸信号转导参与水稻抗病反应在拟南芥中，当受到病原物侵染时，JA水平上升，在活性信号分子JA-Ile的作用下，COI1与JAZ蛋白结合，在泛素连接酶复合体(SCFCOI1)的作用下使JAZ蛋白泛素化并通过26S蛋白酶体途径被降解，JAZ蛋白对转录因子或信号转导蛋白的抑制作用被解除，从而激活JA调控的防御反应[75-76]。在水稻中，通过酵母双杂交试验发现水稻OsCOIs与OsJAZs存在相互作用，且过表达OsCOI1a或OsCOI1b可恢复拟南芥coi1-1突变体中被抑制的JA信号[77]。此外，外源JA显著上调JAZ8表达，通过SCFCOI1 E3泛素连接酶复合体降解JAZ8，增强水稻对Xoo的抗性，JAZ8作为JA途径的防御抑制子负调节JA诱导的水稻对Xoo的抗性[78]，随后的研究表明JAZ通过调节芳樟醇的合成来进一步调控水稻对Xoo的抗性[55]。OsMYC2作为早期JA信号的正调控因子，能够与OsJAZ10的启动子结合激活JA途径，OsMYC2过表达植株表现出对Xoo更强的抗病性，RNA-seq分析表明在OsMYC2 RNAi突变体中，依赖于JA途径的抗病基因、JA合成基因表达量显著下降，这些结果显示OsMYC2在JA调控水稻抗病过程中具有重要作用[79-80]。但是要解析JA的合成及调控途径在水稻抗病性中的作用机制，还有待进一步研究。
3 乙烯(ET)ET是植物体内的一种重要气态激素，主要调控种子的萌发和生长、叶片和组织的衰老、果实的成熟等植物生长发育过程，在植物响应生物和非生物胁迫中也具重要作用。大量研究表明乙烯参与调控拟南芥、烟草、番茄、水稻和大豆等多种植物的免疫反应。在植物免疫反应中，乙烯通常被认为是和JA一起协同参与诱导植物对死体营养型病原菌的抗性，而拮抗SA介导的对活体营养型病原菌的抗性[81]。
3.1 乙烯正调控水稻抗病反应在M.oryzae侵染水稻过程中，与感病材料相比，抗病材料中乙烯信号途径被激活，乙烯积累量显著提高；乙烯合成抑制剂氨基氧乙酸(Aminooxyacetic acid，AOA)和受体结合抑制剂1-甲基环丙烯(1-methylcyclopropene，1-MCP)处理可显著降低寄主的抗病性[82-83]。进一步研究显示，在水稻抗稻瘟病的过程中，乙烯信号下游转录因子OsEIL1可激活OsrbohA/OsrbohB和OsOPRs基因表达，继而激活ROS迸发和植保素积累[83]。而将乙烯信号的中心传递者OsEIN2b沉默后，增加了水稻对稻瘟病的感病性，表现为病原菌生长更快[84]。乙烯也参与调控水稻系统获得性抗性。叶片喷施乙烯利可诱导激活水稻根部的PRs基因和JA信号响应基因OsJAmyb表达，接种实验证实其对根结线虫抗性显著提高；OsEIN2b RNAi突变体也比野生型更感病，且乙烯利处理并不能恢复其表型；AOA处理也能降低水稻抗病性，即乙烯信号传导参与了乙烯诱导的对根结线虫系统获得性抗性[85]。
此外，乙烯的合成在水稻抗病反应中也具有非常重要的作用。Helliwell等[86]发现过表达乙烯生物合成限速酶基因OsACS2后，水稻对M.oryzae和R.solani的抗性显著增强。在过表达水稻抗稻瘟病蛋白Pik-H4的互作蛋白OsBIHD1植株中，OsBIHD1结合在OsACO3的启动子区域激活OsACO3，促进OsACOs表达，这表明乙烯合成在OsBIHD1正调控水稻抗病反应中具有重要作用[87]。
3.2 乙烯负调控水稻抗病反应也有研究表明乙烯可负调控水稻免疫反应。如外源喷施乙烯利会增加水稻对Cochliobolus miyabeanus的感病性[88]，而这种负调控作用能够被硅处理抑制[89]。Shen等[90-91]发现水稻OsEDR1(Enhanced disease resistance 1)基因敲除突变体表现出对Xoo明显的抗性，在OsEDR1敲除突变体中乙烯合成基因ACSs家族的5个基因表达均受到抑制且乙烯的含量也降低，而乙烯合成前体ACC处理可抑制OsEDR1敲除突变对Xoo的抗性。结果表明OsEDR1基因介导乙烯负调控水稻对Xoo的防御反应，同时促进ET的合成，抑制SA和JA相关的防御反应。
和拟南芥一样，乙烯在水稻抗病过程中既可作为正调控因子也可是负调控因子，这种调节作用可能取决于植物-病原菌之间的互作模式及特定的环境条件[92-93]。
4 油菜素内酯(BR)BR是调控植物生长和发育的一类重要的类甾醇激素，在植物全生育期均具有广泛的生理作用。而近年来研究发现，BR在植物应答非生物和生物胁迫反应中也具有非常重要的作用。BR受体BRI1在识别结合BR后与其共受体BAK1形成异源二聚体，激活二者激酶活性并通过一系列磷酸化作用将信号传递至负调控因子GSK3类激酶BIN2，解除BIN2对转录因子BZR1和BES1磷酸化；去磷酸化的BZR1和BES1可进入细胞核并调控BR响应基因表达[94]。BR和PTI信号通路间存在许多共同组分，如BAK1、BSK1和BIK1等，而且PTI途径中的FLS2感知flg22后的也需要和BAK1形成异源二聚体并激活下游信号途径[95-96]。这些相似之处暗示着BR和PTI信号之间可能存在交联互作，即BR也可能参与植物免疫反应。
4.1 BR信号通路相关类受体激酶正调控水稻的抗病性早在2003年，Nakashita等[97]研究发现BR处理可减轻水稻稻瘟病和白叶枯病症状。此外，OsSERK2可正调控类受体激酶Xa21介导的免疫反应，降低OsSERK2表达量可抑制Xa21介导的水稻对Xoo的抗病性[98]。而对于BR信号途径的另一共受体OsSERK1是否参与水稻的免疫反应，目前存在争议。Zuo等[99]研究发现OsSERK1并不参与水稻对M.oryzae和Xoo的防御反应；而Liao等[100]的结果显示OsSERK1正调控水稻对Xoo的抗性。BSKs(BR-signaling kinase)家族中的OsBSK1-2也参与水稻对稻瘟病的抗病反应，但并不参与水稻对BR的响应[101]。这些结果表明在水稻中，BR信号途径中的类受体激酶可能正调控水稻的抗病反应。
4.2 油菜素内酯负调控水稻抗病性也有研究发现BR在水稻与病原互作中起负调控作用。外施BL(Brassinolide)可显著抑制水稻对Pythium graminicola的基础免疫反应；而BR合成抑制剂BRZ(Brassinazole)处理则可提高其抗病性，相应地，BR合成缺陷突变体的抗病性也明显减弱；此外，P.graminicola侵染也可激活BR合成途径和信号，暗示着P.graminicola可能会利用水稻BR系统并作为毒性因子来致病[102]。RBSDV侵染水稻的过程中，BR合成基因表达下调；同时外施BL在激活BR信号后寄主更感病，而外施BRZ可增强水稻对RBSDV抗病性；此外，与野生型相比，BR信号负调控基因OsGSK2过表达突变体也更感病；综上表明BR信号在水稻对RBSDV的免疫反应中起负调控作用[72]。此外，BR在调控水稻对M.graminicola的免疫反应时是依赖于BL浓度的，即外施低浓度BL可增加寄主的感病性，而高浓度BL则提高寄主的抗病性；而BRZ处理和BR合成缺陷均可提高水稻对M.graminicola的抗病性，但仅低浓度BL处理可抑制BR合成缺陷突变体的抗病性[103]。
在拟南芥中BR和PTI信号之间存在拮抗效应[104-106]。这和BR负调控水稻对P.graminicola、M.graminicola和RBSDV的免疫反应一致。至于BR信号途径中的类受体激酶表现出的正调控水稻抗病反应，可能是这些类受体激酶也直接参与了水稻PTI信号激活传导。在拟南芥中，关于BAK1协调BR和PTI信号的机理目前存在争论，一种结果是BRI1和FLS2募集BAK1的过程是独立的，BR信号抑制PTI信号可能存在其他方式[104]，而另一结果显示BRI1可能通过和FLS2竞争BAK1以抑制PTI信号[105]。此外，BZR1在BR抑制植物免疫反应中也具有重要作用[107]；同时BES1可被PTI信号中的MPK6磷酸化，但磷酸化位点和BR信号中不同[108]，这些现象显示BZR1或BES1在权衡生长和免疫中可能是一个重要的调节子。植物在面对外界信号时，生长还是免疫的选择是需要进行精细调控的。BR信号也很可能调控权衡水稻的生长发育和免疫防御反应。
5 其他激素(GAs) 5.1 赤霉素GAs是一类属于四环二萜化合物的植物激素，主要调控植物的生长发育过程。在水稻中，GA受体OsGID1结合具生物活性的GA后可与转录抑制子DELLA蛋白OsSLR1互作，形成的GA-OsGID1-OsSLR1三聚体可被OsGID2多聚泛素化，随后OsSLR1被26S蛋白酶系统降解，进而激活GA响应的转录因子[109]。尽管GA最早是在水稻恶苗病的研究过程中发现的，但是直到近年才逐渐发现其也参与调控植物免疫反应。GA可诱导水稻对不同病原物产生抗病性和感病性。在水稻和卵菌P.graminicola互作过程中，与野生型相比，GA合成受阻、GA不敏感以及SLR1功能获得性突变体均表现出增强的感病性，SLR1功能丧失突变体slr1-1的抗病性增强；药理实验显示GA和GA合成抑制剂Uniconazole处理可分别提高和降低水稻的抗病性[103]。Hossain等[110]发现外源GA的使用可以增加水稻对H.oryzae的抗性。相反地，也有研究报道发现GA信号可负调控水稻免疫反应，外源GA和GA合成抑制剂处理可分别降低和提高水稻对M.oryzae和Xoo的抗病性[111-114]。GA合成基因OsGA20ox3和GA失活蛋白EUI的过表达植株对M.oryzae和Xoo更感病，反之其RNAi干扰植株更抗病[112-113]；GA不敏感突变体和OsSLR1的功能获得性突变体对M.oryzae或Xoo的抗病性增强[111, 114]。
5.2 脱落酸(ABA)ABA是一种最先从棉桃中分离出来的物质，它不仅调控植物生长发育的各个阶段，还能增强植物的抗逆性。研究发现ABA处理能显著抑制水稻对M.oryzae的抗性，ABA不敏感突变体Osabi3表现出对M.oryzae的抗性，表明ABA作为负调控因子调控水稻对M.oryzae的抗病性[115-116]。此外，ABA在水稻对Xoo的抗病反应中也起负调控作用[117]。外源喷施ABA，可以抑制C.miyabeanus的生长而增强抵抗能力[118]。
5.3 生长素(IAA)IAA是最早被发现的植物激素，其不仅参与了水稻的生长发育过程，在免疫反应中也起着重要的作用。有证据表明，IAA负调控水稻对病原菌侵染的抗性。用IAA或2，4-D处理水稻后，会刺激Xoo的增殖，导致水稻更感病；同时Xoo的侵染会诱导水稻的IAA积累[120]。在植物中，GH3类蛋白可催化IAA-氨基酸的合成从而抑制生长素的作用。在水稻中，过表达GH3-8、OsGH3.1和GH3-2基因，会降低IAA的含量，导致水稻植株矮小，但增强了水稻对Xoo、Xanthomonas oryzae pv.oyrzicola(Xoc)和M.oryzae的抗病性[119-121]。此外，过表达OsCYP71Z2也可通过抑制IAA信号以增强对Xoo抗病性[122]。作为平衡植物体内生长素的IAA酰胺合成酶GH3s可能作为一个重要的交叉点精细地调控水稻的生长发育和防御反应。
5.4 细胞分裂素(CKs)CKs是最早在玉米种子中发现的能够促进细胞分裂的植物激素。尽管目前对CK参与抗病功能研究较少，但也有研究表明CK在植物免疫反应中发挥着重要的作用[123]。研究发现，在接种稻瘟病后的水稻苗中可明显检测到CK的积累，同时还发现病原菌也能产生CK；CK还能协同SA激活防御反应，即与水杨酸单独处理相比，CK和SA共处理更能大幅地提高OsPR1b和PBZ1的表达量，而沉默OsNPR1和OsWRKY45表达后可显著减弱这种效应；表明稻瘟病菌能通过提高寄主的CK含量以有利于其侵染，而水稻可能将CK含量的提高作为病原侵染的信号以激活防卫反应[124]。此外，CK参与调控番茄、拟南芥和烟草的抗病性[125-129]，如在拟南芥中，CK受体AHK3和ARR2调节保卫细胞的活性氧稳态，促进由病原相关分子模式(PAMP)触发的气孔关闭，导致拟南芥对丁香假单胞杆菌的抗性增强[127, 131]。
6 不同激素信号间的互作在参与水稻抗病反应中，植物激素并不是独立作用于病原物，而是通过激素间的相互拮抗或协同作用更有效地抵御病原物的侵染。据报道，过表达OsNPR1增加了植株对水稻对M.oryzae和Xoo的抗性，同时提高了对虫害的敏感性。OsNPR1过表达植株中OsPR1b的表达被激活，而JA调控通路的基因OsJAI1的表达被抑制，而且在这个过程中SA和JA的水平并没有显著变化，这些结果暗示OsNPR1调节了SA和JA途径的拮抗作用。ABA可通过抑制SA和ET信号以降低水稻对稻瘟病菌的抗病性，且ABA的负调控信号位于SA信号途径WRKY45与NPR1和ET信号EIN2的上游[84]。BR能通过负调控SA和GA信号而抑制水稻对P.graminicola的基础免疫反应[102]，还可通过抑制JA介导的防卫反应增强对M.graminicola的感病性[104]。在RBSDV侵染水稻过程中，JA信号通路诱导寄主产生的抗病性可通过JA受体COI1抑制BR信号对寄主抗病性的负调控作用[72]。GA信号中的eui突变体可通过抑制JA信号来负调控水稻对稻瘟病菌的抗病反应[113]，SLR1可通过整合和放大依赖于SA和JA的防御反应来正调控对半活体营养型病原菌的防御反应[114]，即GA可抑制SA和JA介导的防御反应。与上述拮抗作用不同的是，JA信号通路和ET信号通路依赖于ERF转录因子在抵御死体营养型病原菌方面存在协同作用[131]。
7 总结与展望植物激素在植物免疫反应中具有重要作用，除了传统的SA、JA和ET这3种激素，近年来BR和GA等也越来越受到研究者的青睐。几种植物激素调控的防御反应构成了植物抵抗病原物侵染的有效防线，因此，明确植物激素在水稻内的调控机制对水稻病害的防治具有重要意义。现代生化和遗传学方法的结合，使各种激素的合成，信号转导等机制逐渐清晰化，但现有的研究并没有解决所有问题。例如:SA合成基因OsICS和OsPAL在内源SA的合成和抗病中的作用机制，为什么NPRs与SA结合的亲和力不同？对于JA信号通路而言，其参与调控防虫的机理和抗病有何不同？而对于其他植物激素ABA、IAA、CK、BR和GA的研究虽然不多，但是也同样暴露了研究中存在的不足，虽然现有研究已显示BR信号途径参与了调节植物免疫反应，但是关于其具体调节作用和调控机理仍存在许多不清楚和有争议之处，尤其是BR信号在水稻中的调控作用更是需要进一步研究，例如，在水稻免疫反应中，BR信号是否也会抑制PTI信号，以及BR信号如何调控权衡水稻的生长发育和免疫反应。揭示和明确植物激素如何协调自身生长发育和响应外界胁迫及其调控机理，也将有助于促进农业生产，保障粮食安全。
| [1] |
余四斌, 熊银, 肖景华, 等. 杂交稻与绿色超级稻[J]. 科学通报, 2016, 61(35): 3797-3803. |
| [2] |
Skamnioti P, Gurr S. Against the grain:safeguarding rice from blast disease[J]. Trends in Biotechnology, 2009, 27(3): 141-150. DOI:10.1016/j.tibtech.2008.12.002 |
| [3] |
Grant M, Kazan K, Manners J. Exploiting pathogens' tricks of the trade for engineering of plant disease resistance:challenges and opportunities[J]. Microbial Biotechnology, 2013, 6(3): 212-222. DOI:10.1111/1751-7915.12017 |
| [4] |
Berens M, Berry H, Mine A, et al. Evolution of hormone signaling networks in plant defense[J]. Annu Rev Phytopathol, 2017, 55(1): 401-425. DOI:10.1146/annurev-phyto-080516-035544 |
| [5] |
丁丽娜, 杨国兴. 植物抗病机制及信号转导的研究进展[J]. 生物技术通报, 2016, 32(10): 109-117. |
| [6] |
White RF. Acetylsalicylic acid(aspirin)induces resistance to tobacco mosaic virus in tobacco[J]. Virology, 1979, 99(2): 410-412. DOI:10.1016/0042-6822(79)90019-9 |
| [7] |
Antoniw JF, Dunkley AM, White RF, et al. Soluble leaf proteins of virus-infected tobacco(Nicotiana tabacum)cultivars[J]. Biochemical Society Transactions, 1980, 8(1): 70-71. DOI:10.1042/bst0080070 |
| [8] |
Shah J. The salicylic acid loop in plant defense[J]. Current Opinion in Plant Biology, 2003, 6(4): 365-371. DOI:10.1016/S1369-5266(03)00058-X |
| [9] |
Vlot AC, Dempsey DA, Klessig DF. Salicylic acid, a multifaceted hormone to combat disease[J]. Annu Rev Phytopathol, 2009, 47: 177-206. DOI:10.1146/annurev.phyto.050908.135202 |
| [10] |
Grant M, Lamb C. Systemic immunity[J]. Current Opinion in Plant Biology, 2006, 9(4): 414-420. DOI:10.1016/j.pbi.2006.05.013 |
| [11] |
Silverman P, Seskar M, Kanter D, et al. Salicylic acid in rice:biosynthesis, conjugation, and possible role[J]. Plant Physiology, 1995, 108(2): 633-639. DOI:10.1104/pp.108.2.633 |
| [12] |
Raskin I, Skubatz H, Tang W, et al. Salicylic acid levels in thermogenic and non-thermogenic plants[J]. Ann Bot, 1990, 66(4): 369-373. DOI:10.1093/oxfordjournals.aob.a088037 |
| [13] |
Malamy J, Carr JP, Klessig DF, et al. Salicylic acid:a likely endogenous signal in the resistance response for tobacco mosaic viral infection[J]. Science, 1990, 250(4983): 1002-1004. DOI:10.1126/science.250.4983.1002 |
| [14] |
Chen Z, Iyer S, Caplan A, et al. Differential accumulation of salicylic acid and salicylic acid sensitive catalase in different rice tissue[J]. Plant Physiology, 1997, 114(1): 193-201. DOI:10.1104/pp.114.1.193 |
| [15] |
Yang Y, Qi M, Mei C. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress[J]. The Plant Journal, 2004, 40(6): 909-919. DOI:10.1111/tpj.2004.40.issue-6 |
| [16] |
Wildermuth M, Dewdney J, Wu G, et al. Isochorismate synthase is required to synthesize salicylic acid for plant defence[J]. Nature, 2001, 414(6863): 562-565. DOI:10.1038/35107108 |
| [17] |
Lee H, Leon J, Raskin I. Biosynthesis and metabolism of salicylic acid[J]. Proceedings of the National Academy of Sciences, 1995, 92(10): 4076-4079. DOI:10.1073/pnas.92.10.4076 |
| [18] |
Zhang X, Chen S, Mou Z. Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis[J]. Journal of Plant Physiology, 2010, 167(2): 144-148. DOI:10.1016/j.jplph.2009.08.002 |
| [19] |
Durrant W, Dong X. Systemic acquired resistance[J]. Annu Rev Phytopathol, 2004, 42: 185-209. DOI:10.1146/annurev.phyto.42.040803.140421 |
| [20] |
Kyndt T, Nahar K, Haegeman A, et al. Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice[J]. Plant Biology, 2012, 14(s1): 73-82. |
| [21] |
Cao H, Glazebrook J, Clarke J, et al. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats[J]. Cell, 1997, 88(1): 57-63. DOI:10.1016/S0092-8674(00)81858-9 |
| [22] |
Fitzgerald H, Chern M, Navarre R, et al. Overexpression of(At)NPR1 in rice leads to a BTH-and environment-induced lesion-Mimic/Cell death phenotype[J]. Molecular Plant-Microbe Interactions, 2004, 17(2): 140-151. DOI:10.1094/MPMI.2004.17.2.140 |
| [23] |
Chern M, Fitzgerald H, Canlas P, et al. Overexpression of a rice NPR1 Homolog leads to constitutive activation of defense response and hypersensitivity to light[J]. Molecular Plant-Microbe Interactions, 2005, 18(6): 511-520. DOI:10.1094/MPMI-18-0511 |
| [24] |
Yuan Y, Zhong S, Li Q, et al. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility[J]. Plant Biotechnology Journal, 2007, 5(2): 313-324. DOI:10.1111/pbi.2007.5.issue-2 |
| [25] |
Chern M, Canlas P, Fitzgerald H, et al. Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1[J]. The Plant Journal, 2005, 43(5): 623-635. DOI:10.1111/tpj.2005.43.issue-5 |
| [26] |
Chern M, Fitzgerald H, Yadav R, et al. Evidence for a disease resistance pathway in rice similar to the NPR1 mediated signaling pathway in Arabidopsis[J]. The Plant Journal, 2001, 27(2): 101-113. DOI:10.1046/j.1365-313x.2001.01070.x |
| [27] |
Weigel R, Bäuscher C, Pfitzner AP, et al. NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants[J]. Plant Mol Biol, 2001, 46(2): 143-160. DOI:10.1023/A:1010652620115 |
| [28] |
Despres C, Chubak C, Rochon A, et al. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1[J]. Plant Cell, 2003, 15(9): 2181-2191. DOI:10.1105/tpc.012849 |
| [29] |
Lindermayr C, Sell S, Müller B, et al. Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide[J]. Plant Cell, 2010, 22(8): 2894-2907. DOI:10.1105/tpc.109.066464 |
| [30] |
Lu HT, Greenberg J, Holuigue L. Editorial:salicylic acid signaling[J]. Frontiers in Plant Science, 2016. DOI:10.3389/fpls.2016.00238 |
| [31] |
Kuai X, MacLeod B, Després C. Integrating data on the Arabidopsis NPR1/NPR3/NPR4 salicylic acid receptors; a differentiating argument[J]. Frontiers in Plant Science, 2015. DOI:10.3389/fpls.2015.00235 |
| [32] |
Fu Z, Yan S, Saleh A, et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants[J]. Nature, 2012, 486(7402): 228-232. |
| [33] |
Wu Y, Zhang D, Chu J, et al. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid[J]. Cell Reports, 2012, 1(6): 639-647. DOI:10.1016/j.celrep.2012.05.008 |
| [34] |
Yan S, Dong X. Perception of the plant immune signal salicylic acid[J]. Current Opinion in Plant Biology, 2014, 20: 64-68. DOI:10.1016/j.pbi.2014.04.006 |
| [35] |
Spoel S, Mou Z, Tada Y, et al. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity[J]. Cell, 2009, 137(5): 860-872. DOI:10.1016/j.cell.2009.03.038 |
| [36] |
Withers J, Dong X. Posttranslational modifications of NPR1:a Single protein playing multiple roles in plant immunity and physiology[J]. PLoS Pathogens, 2016, 12(8): e1005707. DOI:10.1371/journal.ppat.1005707 |
| [37] |
Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants[J]. PLoS Pathogens, 2006, 2(11): e123. DOI:10.1371/journal.ppat.0020123 |
| [38] |
Shimono M, Koga H, Akagi A, et al. Rice WRKY45 plays important roles in fungal and bacterial disease resistance[J]. Mol Plant Pathol, 2012, 13(1): 83-94. |
| [39] |
Shimono M, Sugano S, Nakayama A, et al. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance[J]. Plant Cell, 2007, 19(6): 2064-2076. DOI:10.1105/tpc.106.046250 |
| [40] |
Inoue H, Hayashi N, Matsushita A, et al. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction[J]. Proceedings of the National Academy of Sciences, 2013, 110(23): 9577-9582. DOI:10.1073/pnas.1222155110 |
| [41] |
Shingo G, Fuyuko S, Mai S, et al. Development of disease-resistant rice by optimized expression of WRKY45[J]. Plant Biotechnology Journal, 2015, 13(6): 753-765. DOI:10.1111/pbi.2015.13.issue-6 |
| [42] |
Zhang H, Tao Z, Hong H, et al. Transposon-derived small RNA is responsible for modified function of WRKY45 locus[J]. Nature Plants, 2016, 2: 16016. DOI:10.1038/nplants.2016.16 |
| [43] |
Tao Z, Liu H, Qiu D, et al. A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions[J]. Plant Physiology, 2009, 151(2): 936-948. DOI:10.1104/pp.109.145623 |
| [44] |
Tao Z, Kou Y, Liu H, et al. OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice[J]. Journal of Experimental Botany, 2011, 62(14): 4863-4874. DOI:10.1093/jxb/err144 |
| [45] |
Ueno Y, Yoshida R, Kaboshi M, et al. MAP kinases phosphorylate rice WRKY45[J]. Plant Signaling & Behavior, 2013, 8(6): e24510. |
| [46] |
Ueno Y, Yoshida R, Kaboshi M, et al. Abiotic stresses sntagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6[J]. PLoS Pathogens, 2015, 11(10): e1005231. DOI:10.1371/journal.ppat.1005231 |
| [47] |
Ueno Y, Matsushita A, Inoue H, et al. WRKY45 phosphorylation at threonine 266 acts negatively on WRKY45-dependent blast resistance in rice[J]. Plant Signaling & Behavior, 2017, 12(8): e1356968. |
| [48] |
Matsushita A, Inoue H, Goto S, et al. Nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program[J]. The Plant Journal, 2013, 73(2): 302-313. DOI:10.1111/tpj.12035 |
| [49] |
Hwang S, Kwon S, Jang J, et al. OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv.oryzae[J]. Plant Cell Reports, 2016, 35(9): 1975-1985. DOI:10.1007/s00299-016-2012-0 |
| [50] |
徐文静, 缪刘杨, 李莉云, 等. 五个WRKY转录因子在水稻叶片生长和Xa21介导的白叶枯病抗性反应中的表达研究[J]. 生物化学与生物物理进展, 2013, 40(4): 356-364. |
| [51] |
缪刘杨, 周亮, 杨烁, 等. 水稻转录因子WRKY42的转录、表达及其与W-box的结合特征分析[J]. 生物化学与生物物理进展, 2014, 41(7): 682-692. |
| [52] |
Qiu D, Xiao J, Ding X, et al. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate-and jasmonate-dependent signaling[J]. Molecular Plant-Microbe Interactions, 2007, 20: 492-499. DOI:10.1094/MPMI-20-5-0492 |
| [53] |
Fukushima S, Mori M, Sugano S, et al. Transcription factor WRKY62 plays a role in pathogen defense and hypoxia-responsive gene expression in rice[J]. Plant & Cell Physiology, 2016, 57(12): 2541-2551. |
| [54] |
Zhong X, Yang J, Shi Y, et al. The DnaJ protein OsDjA6 negatively regulates rice innate immunity to the blast fungus Magnaporthe oryzae[J]. Mol Plant Pathol, 2017. DOI:10.1111/mpp.12546 |
| [55] |
Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens[J]. Annu Rev Phytopathol, 2005, 43(1): 205-227. DOI:10.1146/annurev.phyto.43.040204.135923 |
| [56] |
Bari R, Jones J D G. Role of plant hormones in plant defence responses[J]. Plant Mol Biol, 2009, 69(4): 473-488. DOI:10.1007/s11103-008-9435-0 |
| [57] |
Jiang Y, Yu D. The WRKY57 Transcription factor affects the expression of jasmonate ZIM-Domain genes transcriptionally to compromise Botrytis cinerea resistance[J]. Plant Physiology, 2016, 171(4): 2771-2782. |
| [58] |
Vos IA, Moritz L, Pieterse CMJ, et al. Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions[J]. Frontiers in Plant Science, 2015, 6(639): 639. |
| [59] |
Birkenbihl RP, Somssich IE. Transcriptional plant responses critical for resistance towards necrotrophic pathogens[J]. Frontiers in Plant Science, 2011, 2(12): 76. |
| [60] |
Geng X, Cheng J, Gangadharan A, et al. The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense[J]. Plant Cell, 2012, 24(11): 4763-4774. DOI:10.1105/tpc.112.105312 |
| [61] |
Kombrink E. Chemical and genetic exploration of jasmonate biosynthesis and signaling paths[J]. Planta, 2012, 236(5): 1351-1366. DOI:10.1007/s00425-012-1705-z |
| [62] |
Hause B, Mielke K, Forner S. Cell-specific detection of jasmonates by means of an immunocytological approach[M]. Jasmonate Signaling.Humana Press, 2013, 135-144.
|
| [63] |
Sheard LB, Tan X, Mao H, et al. Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor[J]. Nature, 2010, 468(7322): 400-405. DOI:10.1038/nature09430 |
| [64] |
Thines B, Katsir L, Melotto M, et al. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signaling[J]. Nature, 2007, 448(7154): 661-665. DOI:10.1038/nature05960 |
| [65] |
Seo HS, Song JT, Cheong JJ, et al. Jasmonic acid carboxyl methyltransferase:a key enzyme for Jasmonate-Regulated plant responses[J]. Proc Natl Acad Sci USA, 2001, 98(8): 4788-4793. DOI:10.1073/pnas.081557298 |
| [66] |
Riemann M, Haga K, Shimizu T, et al. Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae[J]. Plant Journal for Cell & Molecular Biology, 2013, 74(2): 226-238. |
| [67] |
Yokotani N, Sato Y, Tanabe S, et al. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance[J]. Journal of Experimental Botany, 2013, 64(16): 5085-5097. DOI:10.1093/jxb/ert298 |
| [68] |
Taniguchi S, Hosokawa-Shinonaga Y, Tamaoki D, et al. Jasmonate induction of the monoterpene linalool confers resistance to rice bacterial blight and its biosynthesis is regulated by JAZ protein in rice[J]. Plant Cell & Environment, 2014, 37(2): 451-461. |
| [69] |
Duan Z, Lv G, Shen C, et al. The role of jasmonic acid signalling in wheat(Triticum aestivum L.)powdery mildew resistance reaction[J]. European Journal of Plant Pathology, 2014, 140(1): 169-183. DOI:10.1007/s10658-014-0453-2 |
| [70] |
Ross A, Yamada K, Hiruma K, et al. The Arabidopsis PEPR pathway couples local and systemic plant immunity[J]. The EMBO Journal, 2014, 33(1): 62-75. DOI:10.1002/embj.201284303 |
| [71] |
Taheri P, Tarighi S. Riboflavin induces resistance in rice against Rhizoctonia solani, via jasmonate-mediated priming of phenylpropanoid pathway[J]. Journal of Plant Physiology, 2010, 167(3): 201-208. DOI:10.1016/j.jplph.2009.08.003 |
| [72] |
He Y, Zhang H, Sun Z, et al. Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice[J]. New Phytologist, 2017, 214(1): 388-399. DOI:10.1111/nph.14376 |
| [73] |
Riemann M, Haga K, Shimizu T, et al. Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae[J]. Plant Journal for Cell & Molecular Biology, 2013, 74(2): 226-238. |
| [74] |
Peng X, Hu Y, Tang X, et al. Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice[J]. Planta, 2012, 236(5): 1485-1498. DOI:10.1007/s00425-012-1698-7 |
| [75] |
Howe GA, Jander G. Plant Immunity to Insect Herbivores[J]. Annual Review of Plant Biology, 2008, 59(1): 41-66. DOI:10.1146/annurev.arplant.59.032607.092825 |
| [76] |
Browse J. Jasmonate passes muster:a receptor and targets for the defense hormone[J]. Annual Review of Plant Biology, 2009, 60(1): 183-205. DOI:10.1146/annurev.arplant.043008.092007 |
| [77] |
Lee HY, Seo JS, Cho JH, et al. Oryza sativa COI homologues restore jasmonate signal transduction in Arabidopsis coi1-1 mutants[J]. PLoS One, 2013, 8(1): e52802. DOI:10.1371/journal.pone.0052802 |
| [78] |
Yamada S, Kano A, Tamaoki D, et al. Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice[J]. Plant & Cell Physiology, 2012, 53(12): 2060. |
| [79] |
Uji Y, Taniguchi S, Tamaoki D, et al. Overexpression of OsMYC2 results in the Up-Regulation of early JA-Rresponsive genes and bacterial blight resistance in rice[J]. Plant & Cell Physiology, 2016, 57(9): 1814-1827. |
| [80] |
Ogawa S, Kawaharamiki R, Miyamoto K, et al. OsMYC2 mediates numerous defence-related transcriptional changes via jasmonic acid signalling in rice[J]. Biochemical & Biophysical Research Communications, 2017, 486(3): 796-803. |
| [81] |
Derksen H, Rampitsch C, Daayf F. Signaling cross-talk in plant disease resistance[J]. Plant science, 2013, 207: 79-87. DOI:10.1016/j.plantsci.2013.03.004 |
| [82] |
Iwai T, Miyasaka A, Seo S, et al. Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants[J]. Plant Physiology, 2006, 142(3): 1202-1215. DOI:10.1104/pp.106.085258 |
| [83] |
Yang C, Li W, Cao J, et al. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice[J]. The Plant Journal, 2017, 89(2): 338-353. DOI:10.1111/tpj.2017.89.issue-2 |
| [84] |
Bailey T, Zhou X, Chen J, et al. Role of Ethylene, Abscisic Acid and MAP Kinase Pathways in Rice Blast Resistance[M]. Advances in Genetics, Genomics and Control of Rice Blast Disease, Dordrecht: Springer, 2009, 185-190.
|
| [85] |
Nahar K, Kyndt T, Vleesschauwer DD, et al. The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice[J]. Plant Physiology, 2011, 157(1): 305-316. DOI:10.1104/pp.111.177576 |
| [86] |
Helliwell E, Wang Q, Yang Y. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani[J]. Plant Biotechnology Journal, 2013, 11(1): 33-42. DOI:10.1111/pbi.12004 |
| [87] |
Liu H, Dong S, Gu F, et al. NBS-LRR protein Pik-H4 interacts with OsBIHD1 to balance rice blast resistance and growth by coordinating Ethylene-Brassinosteroid pathway[J]. Frontiers in Plant Science, 2017, 8: 127. |
| [88] |
De Vleesschauwer D, Yang Y, Cruz C V, et al. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling[J]. Plant Physiology, 2010, 152(4): 2036-2052. DOI:10.1104/pp.109.152702 |
| [89] |
Van Bockhaven, Spíchal L, Novák O, et al. Silicon induces resistance to the brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene pathway[J]. New Phytologist, 2015, 206(2): 761-773. DOI:10.1111/nph.13270 |
| [90] |
Shen X, Liu H, Yuan B, et al. OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis[J]. Plant Cell Environ, 2011, 34(2): 179-191. DOI:10.1111/pce.2011.34.issue-2 |
| [91] |
Robert-Seilaniantz A, Grant M, Jones JDG. Hormone crosstalk in plant disease and defense:more than just jasmonate-salicylate antagonism[J]. Annu Rev Phytopathol, 2011, 49: 317-343. DOI:10.1146/annurev-phyto-073009-114447 |
| [92] |
Broekaert WF, Delauré SL, De Bolle MFC, et al. The role of ethylene in host-pathogen interactions[J]. Annu Rev Phytopathol, 2006, 44: 393-416. DOI:10.1146/annurev.phyto.44.070505.143440 |
| [93] |
Van Loon LC, Geraats BPJ, Linthorst HJM. Ethylene as a modulator of disease resistance in plants[J]. Trends in Plant Science, 2006, 11(4): 184-191. DOI:10.1016/j.tplants.2006.02.005 |
| [94] |
Wei Z, Li J. Brassinosteroids regulate root growth, development, and symbiosis[J]. Molecular Plant, 2016, 9(1): 86-100. DOI:10.1016/j.molp.2015.12.003 |
| [95] |
Chinchilla D, Zipfel C, Robatzek S, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence[J]. Nature, 2007, 448(7152): 497-500. DOI:10.1038/nature05999 |
| [96] |
Heese A, Hann DR, Gimenez-Ibanez S, et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants[J]. Proceedings of the National Academy of Sciences, 2007, 104(29): 12217-12222. DOI:10.1073/pnas.0705306104 |
| [97] |
Nakashita H, Yasuda M, Nitta T, et al. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice[J]. The Plant Journal, 2003, 33(5): 887-898. DOI:10.1046/j.1365-313X.2003.01675.x |
| [98] |
Chen X, Zuo S, Schwessinger B, et al. An XA21-associated kinase(OsSERK2)regulates immunity mediated by the XA21 and XA3 immune receptors[J]. Molecular Plant, 2014, 7(5): 874-892. DOI:10.1093/mp/ssu003 |
| [99] |
Zuo S, Zhou X, Chen M, et al. OsSERK1 regulates rice development but not immunity to Xanthomonas oryzae pv.oryzae or Magnaporthe oryzae[J]. Journal of Integrative Plant Biology, 2014, 56(12): 11791-1192. |
| [100] |
Liao H, Xiao X, Li X, et al. OsBAK1 is involved in rice resistance to Xanthomonas oryzae pv.oryzae PXO99[J]. Plant Biotechnology Reports, 2016, 10(2): 75-82. DOI:10.1007/s11816-016-0387-6 |
| [101] |
Wang J, Shi H, Zhou L, et al. OsBSK1-2, an orthologous of AtBSK1, is involved in rice immunity[J]. Frontiers in Plant Science, 2017, 8: 908. DOI:10.3389/fpls.2017.00908 |
| [102] |
De Vleesschauwer D, Van BuytenE, Satoh K, et al. Brassinosteroids antagonize gibberellin-and salicylate-mediated root immunity in rice[J]. Plant Physiology, 2012, 158(4): 1833-1846. DOI:10.1104/pp.112.193672 |
| [103] |
Nahar K, Kyndt T, Hause B, et al. Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway[J]. Molecular Plant-Microbe Interactions, 2013, 26(1): 106-115. DOI:10.1094/MPMI-05-12-0108-FI |
| [104] |
Albrecht C, Boutrot F, Segonzac C, et al. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1[J]. Proceedings of the National Academy of Sciences, 2012, 109(1): 303-308. DOI:10.1073/pnas.1109921108 |
| [105] |
Belkhadir Y, Jaillais Y, Epple P, et al. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns[J]. Proceedings of the National Academy of Sciences, 2012, 109(1): 297-302. DOI:10.1073/pnas.1112840108 |
| [106] |
Jiménez-Góngora T, Kim SK, Lozano-Durán R, et al. Flg22-triggered immunity negatively regulates key BR biosynthetic genes[J]. Frontiers in Plant Science, 2015, 6: 981. |
| [107] |
Lozano-Durán R, Macho AP, Boutrot F, et al. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth[J]. Elife, 2013, 2: e00983. |
| [108] |
Kang S, Yang F, Li L, et al. The Arabidopsis transcription factor BES1 is a direct substrate of MPK6 and regulates immunity[J]. Plant Physiology, 2015, 167: 107. |
| [109] |
Vidhyasekaran P. Plant hormone signaling systems in plant innate immunity[M]. Dordrecht: Springer, 2015, 383-402.
|
| [110] |
Hossain M, Nahar K, Gheysen G. The role of Gibberellin in the response of rice to Hirschmanniella oryzae infection[J]. Arabian Journal for Science and Engineering, 2017. DOI:10.1007/s13369-017-2603-2 |
| [111] |
Tanaka N, Matsuoka M, Kitano H, et al. gid1, a gibberellin-insensitive dwarf mutant, shows altered regulation of probenazole-inducible protein(PBZ1)in response to cold stress and pathogen attack[J]. Plant Cell Environ, 2006, 29(4): 619-631. DOI:10.1111/pce.2006.29.issue-4 |
| [112] |
Yang D, Li Q, Deng Y, et al. Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance[J]. Molecular Plant, 2008, 1(3): 528-537. DOI:10.1093/mp/ssn021 |
| [113] |
Qin X, Liu J, Zhao W, et al. Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice[J]. Molecular Plant-Microbe Interactions, 2013, 26(2): 227-239. DOI:10.1094/MPMI-05-12-0138-R |
| [114] |
De VleesschauwerD, Seifi HS, Filipe O, et al. The DELLA protein SLR1 integrates and amplifies salicylic acid-and jasmonic acid-dependent innate immunity in rice[J]. Plant Physiology, 2016, 170(3): 1831-1847. |
| [115] |
Jiang C, Shimono M, Sugano S, et al. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction[J]. Molecular Plant-Microbe Interactions, 2010, 23(6): 791-798. DOI:10.1094/MPMI-23-6-0791 |
| [116] |
Cao J, Yang C, Li L, et al. Rice Plasma membrane proteomics reveals Magnaporthe oryzae promotes susceptibility by sequential activation of host hormone signaling pathways[J]. Molecular Plant-Microbe Interactions, 2016, 29(11): 902-913. DOI:10.1094/MPMI-08-16-0165-R |
| [117] |
Xu J, Audenaert K, Hofte M, et al. Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses[J]. PloS One, 2013, 8(6): e67413. DOI:10.1371/journal.pone.0067413 |
| [118] |
De Vleesschauwer D, Yang Y, Cruz CV, et al. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling[J]. Plant Physiology, 2010, 152(4): 2036-2052. DOI:10.1104/pp.109.152702 |
| [119] |
Ding X, Cao Y, Huang L, et al. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice[J]. Plant Cell, 2008, 20(1): 228-240. DOI:10.1105/tpc.107.055657 |
| [120] |
Domingo C, Andrés F, Tharreau D, et al. Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice[J]. Molecular Plant-Microbe Interactions, 2009, 22(2): 201-210. DOI:10.1094/MPMI-22-2-0201 |
| [121] |
Fu J, Liu H, Li Y, et al. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice[J]. Plant Physiology, 2011, 155(1): 589-602. DOI:10.1104/pp.110.163774 |
| [122] |
Li W, Wang F, Wang J, et al. Overexpressing CYP71Z2 enhances resistance to bacterial blight by suppressing auxin biosynthesis in rice[J]. PLoS One, 2015, 10(3): e0119867. DOI:10.1371/journal.pone.0119867 |
| [123] |
Choi J, Choi D, Lee S, et al. Cytokinins and plant immunity:old foes or new friends?[J]. Trends in Plant Science, 2011, 16(7): 388-394. DOI:10.1016/j.tplants.2011.03.003 |
| [124] |
Jiang C, Shimono M, Sugano S, et al. Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice[J]. Molecular Plant-Microbe Interactions, 2013, 26(3): 287-296. DOI:10.1094/MPMI-06-12-0152-R |
| [125] |
Argueso CT, Ferreira FJ, Epple P, et al. Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity[J]. PLoS Genetics, 2012, 8(1): e1002448. DOI:10.1371/journal.pgen.1002448 |
| [126] |
Choi J, Huh SU, Kojima M, et al. The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis[J]. Developmental Cell, 2010, 19(2): 284-295. DOI:10.1016/j.devcel.2010.07.011 |
| [127] |
Großkinsky DK, Naseem M, Abdelmohsen UR, et al. Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling[J]. Plant Physiology, 2011, 157(2): 815-830. DOI:10.1104/pp.111.182931 |
| [128] |
Sano H, Seo S, Orudgev E, et al. Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection[J]. Proceedings of the National Academy of Sciences, 1994, 91(22): 10556-10560. DOI:10.1073/pnas.91.22.10556 |
| [129] |
Swartzberg D, Kirshner B, Rav-David D, et al. Botrytis cinerea induces senescence and is inhibited by autoregulated expression of the IPT gene[J]. European Journal of Plant Pathology, 2008, 120(3): 289-297. DOI:10.1007/s10658-007-9217-6 |
| [130] |
Arnaud D, Lee S, Takebayashi Y, et al. Regulation of reactive oxygen species homeostasis by cytokinins modulates stomatal immunity in Arabidopsis[J]. Plant Cell, 2017, 29(3): tpc. 00583. 2016.
|
| [131] |
Bari R, Jones JDG. Role of plant hormones in plant defence responses[J]. Plant Mol Biol, 2009, 69(4): 473-488. DOI:10.1007/s11103-008-9435-0 |