植物时刻暴露在各种环境条件下，恶劣的环境条件阻碍着植物的生理性生长过程，这些恶劣的环境条件被称为非生物胁迫/生物逆境，包括干旱、土壤盐浓度、重金属、低温、放射性物质和不同类型的氧化还原反应病虫害等[1]。植物体通过分子、细胞、形态建成各个层次产生对环境的适应性响应[2]，这些复杂的调控网络操纵着细胞和植物个体对环境的响应、对气候的适应性[3]。病原体的入侵引起植物内源信号分子，如植物激素水杨酸（salicylic acid，SA）和茉莉酸（jasmonic acid，JA）以及他们的衍生物含量的迅速升高，这对下游防御基因的表达有着重要的调控作用[4]。其中SA触发植物体对于活营养体寄生病原体的防御反应，JA则是参与对死营养体病原菌的抗性[5]。ABA（abscisic acid）和乙烯（ethylene）对JA调控起协同作用，但他们都拮抗SA。生长素（auxin）、赤霉素（gibberellins）和细胞分裂素（cytokinins）则是优先促进植物的生长过程，抑制胁迫响应基因的表达；但是这个过程可以被SA和JA所抑制，以牺牲植物生长的代价来进行逆境防御和抵抗[4]。
在过去的20年中，人们对WRKY转录因子（TF）家族参与植物对生物和非生物逆境响应的调控有了很多研究和认识[6]，其在高等植物中是最大的转录因子家族之一，并且存在于所有绿色植物基因组中[7]，也被称为非生物胁迫响应的“中心调控因子”[8]。关于WRKY家族转录因子参与SA、JA逆境胁迫响应信号转导过程的报道逐年增多。WRKYs调节植物对多种非生物胁迫响应，例如盐胁迫[9]、干旱胁迫[10]、冷胁迫[11]、伤口反应[12]；且不仅仅局限于模式植物拟南芥，还包括很多其他的物种[13]。WRKY蛋白在产生生物胁迫的病原体防御[14, 15]和昆虫防御[16, 17]中起重要作用。本文主要总结了近年来报道的WRKYs参与植物胁迫响应的作用，希望对WRKY家族在植物逆境响应中的角色，有一个全面的认识。
1 WRKY转录因子的结构特点、分类和分布WRKY家族转录因子具有相同的结构特征，N端都有包含WRKYGQK七肽序列的WRKY结构域，C端则含有C2H2-或C2HC-类型的锌指结构[15]。根据这些特点，WRKYs可以分成三个家族：第Ⅰ家族含两个WRKY结构域和两个C2H2锌指结构，第Ⅱ家族含一个WRKY结构域和一个C2H2锌指结构，第Ⅲ家族含一个WRKY结构域和一个C2HC锌指结构。第Ⅱ家族又被分成a，b，c，d和e五个小亚族。第Ⅱ家族的WRKY蛋白参与调控植物的生长发育，例如衰老、种子休眠和萌发等；还参与植物对干旱、盐胁迫和冷害响应过程[18]。WRKYs如果没有LZ（leucine zipper）基序，则不能形成同源或者异源二聚体[19]。
不同物种中WRKY家族基因数量也是不同的，黄瓜（Cucumis sativus）中57个，麻风树（Jatropha curcas）中58个，葡萄藤（Vitis vinifera）中9个，白梨（Pyrus bretschneideri）中103个，谷子（Setaria italica）中105个，蓖麻子（Ricinus communis L.）中58个，拟南芥（Arabidopsis thaliana）中74个，水稻（rice）中102个，杨树（poplar）中104个，二穗短柄草（Brachypodium distachyon）中86个成员，182个成员在大豆中，116和102个WRKY基因在两个不同的棉花种。油菜（Brassica napus）中有287个WRKY家族基因，桑树（Morus notabilis）中有54个WRKY家族基因，甜木薯（Manihot escule-nta）中被鉴定出来85个WRKY家族基因[20-29]。
2 WRKY转录因子参与调控植物逆境胁迫响应 2.1 WRKY转录因子响应生物逆境胁迫AtWRKY50和AtWRKY51促进SA的生物合成[30]。AtWRKY17和AtWRKY33在JA处理过后被诱导表达[31]。过表达AtWRKY28和AtWRKY46经由SA信号通路可以诱导ICS1和PBS3[32]。此外，从长春花中分离到的12个WRKY基因都可以响应JA信号[33]，丹参（Salvia miltiorrhiza）中的49个WRKY基因可以显著被JA上调或者下调表达[34]。从杨树（Populus trichocarpa）中分离的WRKY第Ⅲ家族成员PtrWRKY89可以被SA快速诱导[35]。PtrWRKY89的过表达转基因株系中检测到PR基因持续表达，且该株系对P. syringae和B. cinerea更敏感。PtrWRKY89参与SA与JA的协同信号转导过程[36]。在烟草中，WRKY 3/4基因可以被TMV、SA和SA类似物所快速诱导，且表达量足够启动PR蛋白合成，增强抵抗力[37]。我们的研究结果证实AtWRKY8通过直接调控ABI4、ACS6和ERF104的表达参与植物对TMV的防御响应过程中，并且介导了TMV和拟南芥之间ABA和乙烯的信号交叉传递[38]。香蕉VQ基因通过抑制冷害响应转录因子MaWRKY26参与到JA生物合成基因的调节[39]。人参中WRKY转录因子对于胁迫的响应有6个PgWRKY基因（PgWRKY2、PgWRKY3、PgWRKY4、PgWRKY5、PgWRKY6、PgWRKY7）参与。SA处理后3个WRKY基因（PgWRKY3、PgWRKY5、PgWRKY9）明显表达量下调。ABA处理后5个PgWRKYs（PgWRKY2、PgWRKY4、PgWRKY5、PgWRKY8、PgWRKY9）一直明显的上调表达[40]。
在水稻中，OsWRKY71[41]、OsWRKY31[42]、Os-WRKY45-1、OsWRKY45-2[43]都被报道在细菌病原菌侵染过程中被诱导。相似的，在拟南芥中，AtWRKY8[44]、AtWRKY33[45]、AtWRKY25[46]、AtWR-KY11和AtWRKY17[31]在细菌病原体侵染时候基因下调表达。WRKY参与菜豆对于SCN大豆胞囊线虫病（Soybean Cyst Nematode）的侵染胁迫响应[47]。CmWRKY15通过调控ABA信号途径可以促进细极链格孢（Alternaria tenuissima）对于植物体的感染作用[48]。但是，CmWRKY48过表达的转基因菊花却可以抑制蚜虫的群体数量[49]。
油菜在响应核盘菌侵染24 h内快速诱导的关键病原体响应基因，包括葡聚糖酶、几丁质酶、过氧化物酶和WRKY转录因子等，这些都是参与宿主早期病原体响应的基因。其中，WRKY 11在24 hpi被诱导（3倍）但是在48 hpi被抑制（-2倍）[50]；WRKY33之前被报道过正调控植物对于营养体坏死型真菌的抗性[51]；而且在甘蓝型油菜中过表达WRKY33导致抗性响应基因的持续表达，包括PR1、PDF1.2，增加了植株的抵抗力[52]。WRKY11、18、53则表现出了负调控或者是对病原菌侵染的延迟响应。在之前的报道中BnWRKY11在侵染早期6 hpi的时候，表达水平同时被JA和ET所抑制[53]。
在拟南芥中过表达AtWRKY28和AtWRK-Y75都能增强植株对病菌的抗性反应[54]。实验结果证明，13个BnWRKYs都明显地被S. sclerotiorum诱导；包括WRKY6、8、11、15、28、33、40、69和75，在所有烟草株系中都能够检测到表达量的变化；其中6个被大幅上调，分别是BnaA08g12420D（WRKY11）、BnaC04g35770D（WRKY15）、BnaC06g-19560D（WRKY40）、BnaC06g40170D（WRKY40）、BnaA08g180-40D（WRKY65）和BnaA09g55250D（W-RKY69），同时5个WRKYs被下调[55]。
WRKY40和铜离子转运蛋白是调节棉花对于橘黄粉虱侵袭防御的中心调控基因[56]。OsWRKY53可以被咀嚼食草动物高粱条螟（SSB）啃食所诱导，负调控转录调节子OsMPK3/OsMPK6导致JA、JA-Ile和乙烯水平下降从而诱发水稻对SSB的抗性。褐飞虱（BPH）侵袭的8 h之内OsWRKY53转录水平上调，在水稻对于啃食性昆虫BPH的抵抗起到重要作用。实验发现，BPH可以导致水稻中H2O2的显著减少，而在oe-wrky植物体中BPH诱导的H2O2含量明显低于WT；说明OsWRKY53通过调节H2O2的水平来正调控水稻对啃食性昆虫的防御方应[57]。
2.2 WRKY转录因子调控非生物胁迫响应干旱是所有非生物胁迫类型中对植物体伤害最大的，缺水使植株生长缓慢且矮小。WRKY家族转录因子在植物对干旱的耐受起到至关重要的作用[58]。CmWRKY10通过ABA途径来调控菊花的干旱耐受性；在其高表达植株中DREB1A、DREB2A、CuZnSOD、NCED3A、NCED3B等基因转录活跃，说明该株系的干旱耐受机制与ABA信号途径有关联。另外，在高表达株系中ROS的积累明显低于野生型，过氧化物酶、超氧歧化酶、过氧化氢酶的酶活性则是高于野生型，这些高酶活都对提高缺水耐受性有帮助[59]。CmWRKY1是从菊花重克隆出来的WRKY Ⅱb亚家族的转录因子，它和拟南芥AtWRKY6高度同源，外施ABA下调内源CmWRKY1，但是湿润条件可以明显的诱导CmWRKY1的表达[60]。CmWRKY1通过调节ABA相关基因表达增强杭菊的脱水耐受性。AtWRKY6调控有正调控和负调控两种调控方式，而CmWRKY1经过证实同样如此[61]。相反，过表达CmWRKY17则增加了菊花对于盐胁迫的敏感性[62]。
AtWRKY46可以明显地被干旱、H2O2、盐胁迫等所诱导，它的突变体相比野生型来说对渗透胁迫更敏感[63]。TaWRKY44在烟草中表达可以提高其对干旱、盐胁迫、渗透胁迫的抗性[64]。研究结果显示，OsWRKY11[65]、HvWRKY38[66]、TaWRKY2和TaWRKY19[67]都能提高植物对于干旱胁迫的抵抗能力。被HSP101调控的OsWRKY11可以增强水稻对高温和干旱的耐受性[65]。相似的，在大豆中过表达GmWRKY54使得植物体对干旱的耐受性有明显的提高[68]。WRKY基因还参与到大豆干旱和洪涝胁迫的响应过程中[69]。
从羊草（Leymus chinensis）中分离的LcWRKY5，在拟南芥中过表达LcWRKY5可以强烈地增强植物体的耐受性[70]。从短柄草（Brachypodium distachyon）中克隆到的BdWRKY36有增强干旱期间植株的适应性的功能。此外，过表达BdWRKY36蛋白的转基因烟草对干旱的抵抗力显著提高，这种增强作用是通过减少活性氧ROS的积累，激活抗性相关基因NtLEA5、ABA生物合成相关基因NtNCED1和调节基因NtDREB3等途径来实现的[71]。与AtWRKY60同源的BhWRKR1，可以被缺水和ABA短暂而快速的诱导表达。BhWRKY1与BhGolS1互作，依赖ABA途径来增加转基因烟草对于水分缺失的耐受性[72]。大豆遭受水分胁迫时，GmWRKY17和GmWRKY67的转录激活作用增强。GmWRKY161在叶片中可被快速短暂诱导表达，在诱导3 h后达到峰值71倍。GmWRKY112在叶片中短暂上调，在处理2 h后达到最大值21倍。GmWRKY17和GmWRKY67转入大豆根系中，干旱处理后分别有12.7倍和4.8倍的表达量。之前的研究已经表明GmWRKY53和GmWRKY112启动子正响应外施用盐和PEG[73]。烟草的转录因子NtWRKY69能够直接被水分胁迫所诱导[74]。WRKY70还参与落花生的低温胁迫响应[75]。互花米草珧冷胁迫响应中，WRKY起始了PR蛋白和AFP蛋白（anti-freezing protein）的表达[76]。WRKY44在烟草对多种非生物胁迫的耐受性起到重要作用[77]。
最近的一个研究显示，来自于棉花（G. hirsutum L.）的GhWRKY68，在烟草中过表达该蛋白，可以通过ABA信号途径来提高转基因植物体对干旱和盐胁迫的敏感性[78]。人参用NaCl处理时除了PgWRKY5之外所有的PgWRKYs转录水平都明显的上调或者下调表达[79]。遏蓝菜（Thlaspi caerulescens）的WRKY53[80]和拟南芥中AtMYB4[81]有可能参与到植物对于重金属镉（Cd）的胁迫响应过程中。怪柳（Tamarix hispida）的ThWRKY7可以特异性的结合到ThVHAc1启动子的W-box上并且具有转录激活活性，而且在Cd处理条件下ThWRKY7与ThVHAc1具有相同的表达模式，表明ThWRKY7能够提高植物对Cd的耐受性[82]。低氧浓度诱导属于AUX/IAA、WRKY、HB、锌指家族的转录因子的高表达，属于WRKYs第Ⅰ家族的WRKY23和WRKY33在0.4 kPa时被诱导[83]，他们可能与VQ蛋白协同作用[84]。在马樱丹（V. lantana）中WRKY蛋白对于O3胁迫在转录水平的响应，诱导一个参与O3胁迫感受/信号转导途径的基因表达并且参与氧化还原反应[85]。WRKY基因可能参与两个杨树杂交克隆受到O3间断式胁迫条件下的氧化还原反应调控[86]。同样的在Col-0拟南芥WRKY转录因子可以被O3（350 ppb，2 h）处理高度诱导，该现象也能在番茄被B. cinerea侵染和被P. syringae感染[87]、O3处理过后观察到[88]。WRKY蛋白还参与毛竹（Phyllostachys edulis）对强光照的响应调控中[89]。
3 WRKY转录因子的其他功能WRKY蛋白已经被证明参与植物的生长发育过程的调节，例如毛状体形态发生[90]，开花[91]，种子发育[92]、休眠和萌发[93]，衰老[94]。拟南芥WRKY13通过直接结合于NST2的启动子上正调控茎中木质素的生物合成[95]。在木髓部细胞中AtWRKY12直接抑制NST2的表达来负调控次级细胞壁（SCW）的形成，次级细胞壁相关的NAC结构域蛋白SND1/NST3和它的功能同源基因NST1和NST2、维管特异性VND6和VND7是一个关键的调控节点，对于下游SCW生物合成基因SND3、MYB46、MYB83、MYB103等次级转录因子的转录具有开关作用[96, 97]。PtrWRKY19与AtWRKY12具有高度同源性，都负调控木质部髓细胞的SCW发育[98]。WRKY还参与苜蓿（Medicago truncatula）的次级细胞壁形成以及表皮转移细胞发育[99]的调控，调节小麦的抽穗期[100]。GsWRKY20正调控开花反应，通过调控开花相关基因和花分生组织基因的表达来促进植物开花过程[101]。同样，芒草（Miscanthus）的MlWRKY12转录因子也被报道控制开花[102]。WRKY还参与到了大豆叶片脱落的器官极性和细胞命运的转录调控中[103]。
我们研究发现，AtWRKY25很有可能对ABA调控种子萌发和萌发后生长有拮抗作用[104]。WRKY40通过直接抑制ABA敏感基因例如ABI5的转录，作为ABA响应途径的中心转录抑制子来起作用[106]。AtWRKY41通过直接调控ABI3在成熟种子中的表达来控制早期的种子休眠和热抑制[107]，CaWRKY6可以激活CaWRKY40，使其作为一个正调控因子调节Ralstonia solanacearum抗性和对热的耐受性[108]。WRKY参与到水稻叶片早衰和种子休眠中，通过对WRKY的上调表达来激活信号转导[109]。在P. trichocarpa中约有100个WRKY基因，他们中的大部分都可以被JA、SA、冷胁迫、干旱胁迫、盐胁迫或者伤口胁迫所诱导[110]。
AtWRKY6、AtWRKY22、AtWRKY53参与到植物衰老过程调控中[111-113]。WRKY53被报道加快了叶片的衰老过程[114]。AtWRKY54、AtWRKY57和AtWRKY70 同样在叶片衰老中起调控作用[115]。我们的研究结果显示AtWRKY57在JA诱导的衰老过程中，作为一个关节点来调控生长素和JA的信号转导过程[116]。在水稻中过表达OsWRKY42导致叶片早衰[117]。之前报道过SA和H2O2可以刺激WRKY基因的表达，包括（WRKY-6、-42、-53、-71、-72、-77、-79和-97）在叶片衰老中起到重要作用，并且这些WRKY转录因子在ospls1中的表达量明显高于野生型[118, 119]。在小麦基因组中，共有116个WRKY基因，其中30个确定为衰老相关WRKY基因，TaWRKY7、16、24、36、39、68、71、74、89、96、114、115和116很可能是调节衰老的SAGs。在拟南芥中异位过表达TaWRKY7，在黑暗处理条件下观察到叶片衰老过程的明显加快；它还可以被ABA诱导，同时阻止了叶片的水分流失提高植株对干旱的忍耐性[120]。AtWRKY6可以直接结合到W-box上从而调控衰老诱导的类受体激酶基因的转录活性，atwrky6突变体和过表达AtWRKY6转基因植株分别表现出早衰和延迟衰老的表型[121]。此外，在铁缺失的条件下WRKY46转录因子通过调节液泡Fe转运基因的表达，来调控Fe元素在植物体内从根到茎叶的转运[122]。
WRKYs转录因子例如GaWRKY1、AaWRKY1、WRKY3、WRKY6和WRKY33都参与控制多种生物合成过程的调节中，包括棉子酚、青蒿素和植物抗毒素的生物合成调控[123-125]。在紫杉醇的生物合成过程中，从红豆杉（Taxus chinensis）中分离的MeJA响应转录因子TcWRKYA1，在体外可以特异性地与两个DBAT基因启动子上W-box元件结合，而DBAT编码紫杉醇生物合成过程中的关键酶[126]。CjWRKY1属于IIc亚家族且响应JA信号，在生物碱异喹啉的生物合成过程中，过表达CjWRKY1能够增强多种黄连素生物合成基因的转录激活[127]。雌性蛇麻草（Humulus lupulus L.）中的HlWRKY1调控蛇麻素生物合成的最后步骤，通过激活黄腐酚和苦酸生物合成的关键基因，例如查耳酮合酶H1，己酰苯合酶，异戊烯转移酶1、1L和2，O-甲基转移酶的转录来完成调控过程[128]。
4 WRKY转录因子的转录后调控 4.1 可变剪接在病原体防御反应中，水稻WRKY62和WRKY76转录因子的基因存在可变剪接。短的可变剪接OsWRKY62.2和OsWRKY76.2亚型可以彼此互作，也可以和全长的蛋白互作。OsWRKY62.2在植物中转录抑制作用减弱，OsWRKY62.2和OsWRKY76.2的剪接使得其对W-box的结合能力有所下降[129]。
4.2 磷酸化量光谱测定显示，体外WRKY46能够被MPK3磷酸化S168和S250位点。磷酸化位点的突变减慢了PAMP诱导的WRKY46降解的过程。在原生质体中过表达WRKY46可以增加PAMP响应提高植物基础抗性[130]。WRKY8和WRKY48作为植物对丁香假单胞菌（P. syringae）基础防御的负调控因子又作为ETI的正调控因子，他们的生物突变体表现出抗性减弱和防御基因表达量的减少[131]。WRKY8、WRKY28和WRKY48的WRKY结构域可以直接被CPKs磷酸化，增强HR反应中WRKY46对细胞程序性死亡相关的标记基因启动子区W-box元件的结合能力[132]。WRKY53可以直接被MAPK信号途径的MEKK1蛋白磷酸化从而参与到植物的基础防御反应的信号转导过程中[133]，WRKY53的磷酸化状态可以加强靶基因的启动和转录能力[134]。在响应B. cinerea侵染的过程中，WRKY33可以被两个明显受病原菌诱导的MAPKs所磷酸化，启动植物抗菌剂-植保素的生物合成[135]。在本生烟中MAPK介导NbWRKY8的磷酸化，NbWRKY8与AtWRKY33同源，参与PTI和ETI可以激活NADPH氧化酶的表达[136]。OsWRKY70可以被MAPK3和MAPK6磷酸化参与GA的生物合成，并且对植物生长和发育的动态平衡起重要作用。目前的报道显示，在不同物种间MAPK是作为通用磷酸酶来磷酸化WRKY家族的蛋白质，并且最终作用到他们的靶基因上[137]。
5 总结与展望WRKYs参与到植物生命周期的多个方面，在植物正常的生命活动中有着重要的不可或缺的作用。通过调控植物细胞壁的合成、开花时间、种子储藏物质代谢、种子萌发和休眠和植物衰老等过程参与植物的生长发育的各个阶段。WRKYs和SA、JA等植物激素之间存在复杂的信号转导调控网络，并且在植物受到环境中的各种胁迫因素，例如干旱、盐、缺氧、低温、强光照等非生物胁迫的威胁和病原体、昆虫、食草性或杂食性动物的入侵等生物胁迫的影响时，WRKY家族的转录调控蛋白通过激活或者抑制相关胁迫响应基因的转录激活，来增加植物对于环境的适应性和耐受性。WRKYs转录因子家族广泛存在于绿色植物中，已经有关于不同物种中WRKYs相关作用的报道，但是大部分的调控网络还不清晰，仍然还有很多内容需要进一步的研究证实和完善。
| [1] | Aditya B, Aryadeep R. WRKY Proteins:Signaling and regulation of expression during abiotic stress responses. Scientific World Journal Volume , 2015 : 807560. |
| [2] | Gray SB, Brady SM. Plant developmental responses to climate change. Dev Biol , 2016, S0012-1606 (16) : 30264-0. |
| [3] | Oracz K, Karpinski S. Phytohormones signaling pathways and ROS involvement in seed germination. Plant Sci , 2016, 7 : 864. |
| [4] | Pieterse MC, Van der Does D, Zamioudis C, et al. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol , 2012, 28 : 489–521. DOI:10.1146/annurev-cellbio-092910-154055 |
| [5] | Schluttenhofer C, Pattanaik S, Patra B, et al. Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genomics , 2014, 15 : 502. DOI:10.1186/1471-2164-15-502 |
| [6] | Schuttenhofer C, Yuan L. Regulation of specialized metabolism by WRKY transcription factors. Plant Physiology , 2015, 167 (2) : 295–306. DOI:10.1104/pp.114.251769 |
| [7] | Ulker B, Somssich IE. WRKY transcription factors:from DNA binding towards biological function. Current Opinion in Plant Biology , 2004, 7 (5) : 491–498. DOI:10.1016/j.pbi.2004.07.012 |
| [8] | Tripathi P, Rabara RC, et al. A systems biology perspective on the role of WRKY transcription factors in drought responses in plants. Planta , 2014, 239 : 255–266. DOI:10.1007/s00425-013-1985-y |
| [9] | Wu X, Shiroto Y, Kishitani S, et al. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep , 2009, 28 (1) : 21–30. DOI:10.1007/s00299-008-0614-x |
| [10] | Ren X, Chen Z, Liu Y, et al. ABO3, a?WRKY?transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J , 2010, 63 (3) : 417–29. DOI:10.1111/tpj.2010.63.issue-3 |
| [11] | Zou C, Jiang W, Yu D. Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot , 2010, 61 (14) : 3901–3914. DOI:10.1093/jxb/erq204 |
| [12] | Chen L, Zhang L, Yu D. Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. Mol Plant Microbe Interact , 2010, 23 (5) : 558–565. DOI:10.1094/MPMI-23-5-0558 |
| [13] | Rinerson CI, Rabara RC, Tripathi P, et al. The evolution of WRKY transcription factors. BMC Plant Biology , 2015, 15 : 66. DOI:10.1186/s12870-015-0456-y |
| [14] | Eulgem T, Somssich IE. Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol , 2007, 10 (4) : 366–371. DOI:10.1016/j.pbi.2007.04.020 |
| [15] | Rushton PJ, Somssich IE, Ringler P, et al. WRKY?transcription factors. Trends In Plant Sci , 2010, 15 (5) : 247–258. DOI:10.1016/j.tplants.2010.02.006 |
| [16] | Grunewald W, Karimi M, Wieczorek K, et al. A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol , 2008, 148 (1) : 358–368. DOI:10.1104/pp.108.119131 |
| [17] | Skibbe M, Qu N, Galis I, et al. Induced plant defenses in the natural environment:Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell , 2008, 20 (7) : 1984–2000. DOI:10.1105/tpc.108.058594 |
| [18] | Rushton DL, Tripathi P, Rabara RC, et al. WRKY transcription factors:key components in abscisic acid signaling. Plant Biotechnology Journal , 2012, 10 : 2–11. DOI:10.1111/pbi.2011.10.issue-1 |
| [19] | Narusaka M, Toyoda K, Shiraishi T, et al. Leucine zipper motif in RRS1 is crucial for the regulation of Arabidopsis dual resistance protein complex RPS4/RRS1. Sci Rep , 2016, 6 : 18702. DOI:10.1038/srep18702 |
| [20] | Ling J, Jiang W, Zhang Y, et al. Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics , 2011, 12 : 471. DOI:10.1186/1471-2164-12-471 |
| [21] | Xiong W, Xu X, Zhang L, et al. Genome-wide analysis of the WRKY gene family in physic nut(Jatropha curcas L. ). Gene , 2013, 524 (2) : 124–132. DOI:10.1016/j.gene.2013.04.047 |
| [22] | Guo C, Guo R, Xu X, et al. Evolution and expression analysis of the grape(Vitis vinifera L. )WRKY gene family. J Exp Bot , 2014, 65 (6) : 1513–1528. DOI:10.1093/jxb/eru007 |
| [23] | Eulgem T, Rushton PJ, Robatzek S, et al. The WRKY superfamily of plant transcription factors. Trends Plant Sci , 2000, 5 (5) : 199–206. DOI:10.1016/S1360-1385(00)01600-9 |
| [24] | Huang X, Li K, Xu X, et al. Genome-wide analysis of WRKY transcription factors in white pear(Pyrus bretschneideri)reveals evolution and patterns under drought stress. BMC Genomics , 2015, 16 (1) : 1104. DOI:10.1186/s12864-015-2233-6 |
| [25] | He H, Dong Q, Shao Y, et al. Genome-wide survey and characteri-zation of the WRKY gene family in Populus trichocarpa. Plant Cell Rep , 2012, 31 (7) : 1199–1217. DOI:10.1007/s00299-012-1241-0 |
| [26] | Muthamilarasan M, Bonthala VS, Khandelwal R, et al. Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci , 2015, 6 : 910. |
| [27] | Ross CA, Liu Y, Shen QJ. The WRKY gene family in rice(Oryza sativa). J Integr Plant Biol , 2007, 49 : 827–842. DOI:10.1111/jipb.2007.49.issue-6 |
| [28] | Zou Z, Yang?L, Wang D, et al. Gene structures, evolution and transcriptional profiling of the WRKY gene family in Castor Bean(Ricinus communis L. ). PLoS One , 2016, 11 (2) : e0148243. DOI:10.1371/journal.pone.0148243 |
| [29] | Ulker B, Somssich IE. WRKY transcription factors:from DNA binding towards biological function. Curr Opin Plant Biol , 2004, 7 (5) : 491–498. DOI:10.1016/j.pbi.2004.07.012 |
| [30] | Gao QM, Venugopal S, Navarre D, Kachroo A. Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiol , 2011, 155 (1) : 464–476. DOI:10.1104/pp.110.166876 |
| [31] | Journot-Catalino N, Somssich IE, Roby D, Kroj T. The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell , 2006, 18 (11) : 3289–3302. DOI:10.1105/tpc.106.044149 |
| [32] | Verk MC, Bol JF, Linthorst HJ. WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol , 2011, 11 : 89. DOI:10.1186/1471-2229-11-89 |
| [33] | Schluttenhofer C, Pattanaik S, Patra B, et al. Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genomics , 2014, 15 : 502. DOI:10.1186/1471-2164-15-502 |
| [34] | Gong L, Zhang H, Gan X. Transcriptome profiling of the potato(Solanum tuberosum L. )Plant under drought stress and water-stimulus conditions. PLoS One , 2015, 10 (5) : e0128041. DOI:10.1371/journal.pone.0128041 |
| [35] | Jiang Y, Guo L, Liu R, et al. Overexpression of poplar PtrWRKY89 in transgenic Arabidopsis leads to a reduction of disease resistance by regulating defense related genes in salicylate- and jasmonate dependent signaling. PLoS One , 2016, 11 (3) : e0149137. DOI:10.1371/journal.pone.0149137 |
| [36] | Jiang YZ, Duan YJ, Yin J, et al. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot , 2014, 65 (22) : 6629–6644. DOI:10.1093/jxb/eru381 |
| [37] | Chen C, Chen Z. Isolation and characterization of two pathogen- and salicylic acid-induced genes encoding?WRKY?DNA-binding proteins from tobacco. Plant Mol Biol , 2000, 42 (2) : 387–396. DOI:10.1023/A:1006399311615 |
| [38] | Chen LG, Zhang LP, Li DB, et al. WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA , 2013, 110 : E1963–1971. DOI:10.1073/pnas.1221347110 |
| [39] | Ye YJ, Xiao YY, Han YC, et al. Banana fruit VQ motif-containing protein5 represses cold-responsive transcription factor MaWRKY26 involved in the regulation of JA biosynthetic genes. Sci Rep , 2016, 6 : 23632. DOI:10.1038/srep23632 |
| [40] | Xiu H, Nuruzzaman M, Guo X, et al. Molecular cloning and expression analysis of eight PgWRKY genes in Panax ginseng responsive to salt and hormones. Int J Mol Sci , 2016, 17 (3) : 319. DOI:10.3390/ijms17030319 |
| [41] | Liu X, Bai X, Wang X, Chu C. OsWRKY71, a rice transcription factor, is involved in rice defense response. Plant Physiol , 2007, 164 : 969–979. DOI:10.1016/j.jplph.2006.07.006 |
| [42] | Zhang J, Peng Y, Guo Z. Constitutive expression of pathogen- inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res , 2008, 18 (4) : 508–521. DOI:10.1038/cr.2007.104 |
| [43] | Tao Z, Kou Y, Liu H, et al. OsWRKY45 alleles play different roles in abscisic acid signaling and salt stress tolerance but similar roles in drought and cold tolerance in rice. Exp Bot , 2011, 62 (14) : 4863–4874. DOI:10.1093/jxb/err144 |
| [44] | Chen L, Zhang L, Yu D. Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. Mol Plant Micro , 2011, 23 : 558–565. |
| [45] | Zheng Z, Qamar SA, Chen Z, Mengiste T. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J , 2006, 48 (4) : 592–605. DOI:10.1111/tpj.2006.48.issue-4 |
| [46] | Zheng Z, Mosher SL, Fan B, et al. Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringe. BMC Plant Biol , 2007, 7 : 2. DOI:10.1186/1471-2229-7-2 |
| [47] | Jain S, Chittem K, Brueggeman R, et al. Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection. PLoS One , 2016, 11 (7) . |
| [48] | Fan Q, Song A, Xin J, et al. CmWRKY15 facilitates Alternaria tenuissima infection of chrysanthemum. PLoS One , 2015, 10 : e0143349. DOI:10.1371/journal.pone.0143349 |
| [49] | Li P, Song A, Gao C, et al. The over-expression of a chrysanthemum WRKY transcription factor enhances aphid resistance. Plant Physiology and Biochemistry , 2015, 95 : 26–34. DOI:10.1016/j.plaphy.2015.07.002 |
| [50] | Joshi RK, Megha S, Rahman MH, et al. A global study of transcriptome dynamics in canola(Brassica napus L. )responsive to Sclerotinia sclerotiorum infection using RNA-Seq. Gene , 2016, 590 (1) : 57–67. DOI:10.1016/j.gene.2016.06.003 |
| [51] | Yang B, Jiang Y, Rahman MH, et al. Identification and expression analysis of?WRKY?transcription factor genes in canola(Brassica napus L. )in response to fungal pathogens and hormone treatments. BMC Plant Biol , 2009, 9 : 68. DOI:10.1186/1471-2229-9-68 |
| [52] | Wang Z, Fang H, Chen Y, et al. Overexpression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol Plant Pathol , 2014, 15 (7) : 677–689. DOI:10.1111/mpp.2014.15.issue-7 |
| [53] | Wang Z, Mao H, Dong C, et al. Overexpression of Brassica napus MPK4 enhances resistance to Sclerotinia sclerotiorum in oilseed rape. Mol Plant Microbe In , 2009, 22 (3) : 235–244. DOI:10.1094/MPMI-22-3-0235 |
| [54] | Chen XT, Liu T, Lin G, et al. Overexpression of AtWRKY28 and AtWRKY75 in Arabidopsis enhances resistance to oxalic acid and Sclerotinia sclerotiorum. Plant Cell Rep , 2013, 32 (10) : 1589–1599. DOI:10.1007/s00299-013-1469-3 |
| [55] | Jiang YZ, Duan YJ, Yin J, et al. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response tobiotic and abiotic stresses. Exp Bot , 2014, 65 (22) : 6629–6644. DOI:10.1093/jxb/eru381 |
| [56] | Li J, Zhu J, Hull JJ, et al. Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem feeding insect Bemisia tabaci(whitefly). Plant Biotechnol , 2016, 14 (10) : 1956–1975. DOI:10.1111/pbi.2016.14.issue-10 |
| [57] | Hu L, Ye M, Li R, Lou Y. OsWRKY53, a versatile switch in regulating herbivore-induced defense responses in rice. Plant Signal Behav , 2016, 11 (4) : e1169357. DOI:10.1080/15592324.2016.1169357 |
| [58] | Satapathy L, Singh D, Ranjan P, et al. Transcriptome-wide analysis of WRKY transcription factors in wheat and their leaf rust responsive expression profiling. Molecular Genetics Genomics , 2014, 289 : 1289–1306. DOI:10.1007/s00438-014-0890-9 |
| [59] | Jaffar MA, Song A, Faheem M, et al. Involvement of CmWRKY10 in drought tolerance of Chrysanthemum through the ABA-signaling pathway. Int J Mol Sci , 2016, 17 (5) : E693. DOI:10.3390/ijms17050693 |
| [60] | Song A, Li P, Jiang J, et al. Phylogenetic and transcription analysis of chrysanthemum WRKY transcription factors. International Journal Molecular Science , 2014, 15 : 14442–14455. DOI:10.3390/ijms150814442 |
| [61] | Fan Q, Song A, Jiang J, et al. CmWRKY1 enhances the dehydration tolerance of Chrysanthemum through the regulation of ABA-associated genes. PLoS One , 2016, 11 (3) : e0150572. DOI:10.1371/journal.pone.0150572 |
| [62] | Li P, Song A, Gao C, et al. Chrysanthemum WRKY gene CmWRK- Y17 negatively regulates salt stress tolerance in transgenic chrysa-nthemum and Arabidopsis plants. Plant Cell Reports , 2015, 34 : 1365–1378. DOI:10.1007/s00299-015-1793-x |
| [63] | Ding ZJ, Yan JY, Xu XY, et al. Transcription factor?WRKY46?reg-ulates osmotic stress responses and stomatal movement independ-ently in Arabidopsis. Plant J , 2014 (1) : 13–27. |
| [64] | Han Y, Zhang X, Wang W, et al. Correction:the suppression of?WRKY44?by GIGANTEA-miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS One , 2015, 10 (4) : e0124854. DOI:10.1371/journal.pone.0124854 |
| [65] | Wu X, Shiroto Y, Kishitani S, et al. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep , 2009, 28 (1) : 21–30. DOI:10.1007/s00299-008-0614-x |
| [66] | Xiong X, James VA, Zhang H, Altpeter F. Constitutive expression of the barley HvWRKY38 transcription factor enhances drought tol-erance in turf and forage grass(Paspalumnotatum Flugge). Mol Breed , 2010, 25 (3) : 419–432. DOI:10.1007/s11032-009-9341-4 |
| [67] | Niu CF, Wei W, Zhou QY, et al. Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ , 2012, 35 (6) : 1156–1170. DOI:10.1111/pce.2012.35.issue-6 |
| [68] | Zhou QY, Tian AG, Zou HF, et al. Soybean WRKY-type transcrip-tion actor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic tresses in transgenic Arabid-opsis plants. Plant Biotechnology Journal , 2008, 6 : 486–503. DOI:10.1111/pbi.2008.6.issue-5 |
| [69] | Chen W, Yao Q, Patil GB, et al. Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and flooding stress revealed by RNA-Seq. Front Plant Sci , 2016, 7 : 1044. |
| [70] | Ma T, Li M, Zhao A, et al. LcWRKY5:an unknown function gene from sheep grass improves drought tolerance in transgenic Arabidopsis. Plant Cell Reports , 2014, 33 : 1507–1518. DOI:10.1007/s00299-014-1634-3 |
| [71] | Sun J, Hu W, Zhou R, et al. The Brachypodium distachyon BdWRKY36 gene confers tolerance to drought stress in transgenic tobacco plants. Plant Cell Reports , 2015, 34 : 23–35. DOI:10.1007/s00299-014-1684-6 |
| [72] | Wang Z, Zhu Y, Wang L, et al. A WRKY transcription factor participates in dehydrationtolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase(BhGolS1)promoter. Planta , 2009, 230 : 1155–1166. DOI:10.1007/s00425-009-1014-3 |
| [73] | Tripathi P, Rabara RC, Reese RN, et al. A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics , 2016, 17 : 102. DOI:10.1186/s12864-016-2420-0 |
| [74] | Rabara RC, Tripathi P, Reese RN, et al. Tobacco drought stress responses reveal new targets for Solanaceae crop improvement. BMC Genomics , 2015, 16 : 484. DOI:10.1186/s12864-015-1575-4 |
| [75] | Bonthala VS, Mayes K, Moreton J, et al. Identification of gene mod- ules associated with low temperatures response in bambara ground-nut by network-based analysis. PLoS One , 2016, 11 (2) : e0148771. DOI:10.1371/journal.pone.0148771 |
| [76] | Nah G, Lee M, Kim DS, et al. Transcriptome Analysis of Spartina pectinate in Response to Freezing Stress. PLoS One , 2016, 11 (3) : e0152294.. DOI:10.1371/journal.pone.0152294 |
| [77] | Wang X, Zeng J, Li Y, et al. Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances. Front Plant Sci , 2015, 6 : 615. |
| [78] | Jia H, Wang C, Wang F, et al. GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana benthamiana. PLoS One , 2015, 10 : e0120646. DOI:10.1371/journal.pone.0120646 |
| [79] | Xiu H, Nuruzzaman M, Guo Xet A. Molecular cloning and express-ion analysis of eight PgWRKY genes in Panax ginseng responsive to salt and hormones. Int J Mol Sci , 2016, 17 (3) : 319. DOI:10.3390/ijms17030319 |
| [80] | Wei W, Zhang Y, Han L, et al. A novel WRKY transcriptional factor from THLASPI CAERULESCENS negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Rep , 2008, 27 : 795–803. DOI:10.1007/s00299-007-0499-0 |
| [81] | Hemm MR, Herrmann KM, Chapple C. AtMYB4:a transcription factor general in the battle against UV. Trends Plant Sci , 2001, 6 (4) : 135–136. DOI:10.1016/S1360-1385(01)01915-X |
| [82] | Gao C, Wang Y, Jiang B, et al. A novel vacuolar membrane H+-ATPase c subunit gene(ThVHAc1)from Tamarix hispida confers tolerance to several abiotic stresses in Saccharomyces cerevisiae. Mol Biol Rep , 2011, 38 (2) : 957–963. DOI:10.1007/s11033-010-0189-9 |
| [83] | Rushton PJ, Somssich IE, Ringler P, et al. WRKY transcription factors. Trends Plant Sci , 2010, 15 : 247–258. DOI:10.1016/j.tplants.2010.02.006 |
| [84] | Cheng Y, Zhou Y, Yang Y, et al. Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. PlantPhysiol , 2012, 159 (2) : 810–825. |
| [85] | Tosti N, Pasqualini S, Borgogni A, et al. Gene expression profiles of O3-treated Arabidopsis plants. Plant Cell Environ , 2006 (9) : 1686–702. |
| [86] | Rizzo M, Bernardi R, Salvini M, et al. Identification of differentially expressed genes induced by ozone stress in sensitive and tolerant poplar hybrids. J Plant Physiol , 2007, 164 (7) : 945–949. DOI:10.1016/j.jplph.2006.07.012 |
| [87] | Birkenbihl RP, Diezel C, Somssich IE. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol , 2012, 159 (1) : 266–285. DOI:10.1104/pp.111.192641 |
| [88] | Journot-Catalino N, Somssich IE, Roby D, Kroj T. The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell , 2006 (11) : 3289–302. |
| [89] | Zhao H, Lou Y, Sun H. Transcriptome and comparative gene expression analysis of Phyllostachys edulis in response to high light. BMC Plant Biology , 2016, 16 : 34. DOI:10.1186/s12870-016-0720-9 |
| [90] | Johnson CS, Kolevski B, Smyth DR. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a?WRKY?transcription factor. Plant Cell , 2002, 14 (6) : 1359–1375. DOI:10.1105/tpc.001404 |
| [91] | Luo X, Sun X, Liu B, et al. Ectopic expression of a?WRKY?homolog from Glycine soja alters flowering time in Arabidopsis. PLoS One , 2013, 8 (8) : e73295. DOI:10.1371/journal.pone.0073295 |
| [92] | Luo M, Dennis ES, Berger F, et al. MINISEED3(MINI3), a?WR-KY?family gene, and HAIKU2(IKU2), a leucine-rich repeat(L- RR)KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA , 2005, 102 (48) : 17531–17536. DOI:10.1073/pnas.0508418102 |
| [93] | Zhang ZL, Xie Z, Zou X. A rice?WRKY?gene encodes a transcript-ional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol , 2004, 134 (4) : 1500–1513. DOI:10.1104/pp.103.034967 |
| [94] | Robatzek S, Somssich IE. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev , 2002, 16 (9) : 1139–1149. DOI:10.1101/gad.222702 |
| [95] | Li W, Tian Z, Yu D. WRKY13 acts in stem development in Arabi-dopsis thaliana. Plant Sci , 2015, 236 : 205–213. DOI:10.1016/j.plantsci.2015.04.004 |
| [96] | Wang H, Avci U, Nakashima J, et al. Mutation of WRKY transcri-ption factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA , 2010, 107 (51) : 22338–22343. DOI:10.1073/pnas.1016436107 |
| [97] | Yu Y, Hu R, Wang H, et al. MlWRKY12, a novel Miscanthus transcription factor, participates in pith secondary cell wall formation and promotes flowering. Plant Sci , 2013, 212 : 1–9. DOI:10.1016/j.plantsci.2013.07.010 |
| [98] | Li Y, Xin Z, Fa nY, et al. PtrWRKY19, a novel WRKY transcription factor, contributes to the regulation of pith secondary wall formation in Populus trichocarpa. Scientific RepoRts , 2016, 6 : 18643. DOI:10.1038/srep18643 |
| [99] | Arun-Chinnappa KS, McCurdy DW. Identification of candidate transcriptional regulators of epidermal transfer cell development in Vicia faba Cotyledons. Front Plant Sci , 2016, 7 : 717. |
| [100] | Kiseleva, Shcherban AB, Leonova IN, et al. Identification of new heading date determinants in wheat 5B chromosome. BMC Plant Biol , 2016, 16 (1) : 8. |
| [101] | Luo X, Sun X, Liu B, et al. Ectopic expression of a WRKY homolog from Glycine soja alters flowering time in Arabidopsis. PLoS One , 2013, 8 : e73295. DOI:10.1371/journal.pone.0073295 |
| [102] | Yu Y, Hu R, Wang H, et al. MlWRKY12, a novel Miscanthus transcription factor, participates in pith secondary cell wall formation and promotes flowering. Plant Sci , 2013, 212 : 1–9. DOI:10.1016/j.plantsci.2013.07.010 |
| [103] | Kim J, Yang J, Yang R, et al. Transcriptome analysis of soybean leaf abscission identifies transcriptional regulators of organ polarity and cell fate. Plant Sci , 2016, 7 : 125. |
| [104] | Jiang Y, Deyholos MK. Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Molecular Biology , 2009, 69 : 91–105. DOI:10.1007/s11103-008-9408-3 |
| [105] | Shang Y, Yan L, Liu ZQ, et al. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell , 2010, 22 : 1909–1935. DOI:10.1105/tpc.110.073874 |
| [106] | Chen H, Lai Z, Shi J, et al. Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol , 2010, 10 : 281. DOI:10.1186/1471-2229-10-281 |
| [107] | Ding ZJ, Yan JY, Li GX, et al. WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J , 2014, 79 : 810–823. DOI:10.1111/tpj.2014.79.issue-5 |
| [108] | Cai H, Yang S, Yan Y, et al. CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper. J Exp Bot , 2015, 66 : 3163–3174. DOI:10.1093/jxb/erv125 |
| [109] | Yang X, Gong P, Li K, et al. A single cytosine deletion in the OsPLS1 gene encoding vacuolar-type H+-ATPase subunit A1 leads to premature leaf senescence and seed dormancy in rice. J Exp Bot , 2016, 67 (9) : 2761–2776. DOI:10.1093/jxb/erw109 |
| [110] | He HS, Dong Q, Shao Y, et al. Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep , 2012, 31 : 1199–1217. DOI:10.1007/s00299-012-1241-0 |
| [111] | Robatzek S, Somssich E. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev , 2002, 16 (9) : 1139–1149. DOI:10.1101/gad.222702 |
| [112] | Zhou X, Jiang Y, Yu D. WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol Cells , 2011, 31 (4) : 303–313. DOI:10.1007/s10059-011-0047-1 |
| [113] | Miao Y, Laun T, Smykowski A, et al. Arabidopsis MEKK1 can take a short cut:I t can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol , 2007, 65 (1-2) : 63–76. DOI:10.1007/s11103-007-9198-z |
| [114] | Miao H, Qin Y, da Silva JA, et al. Identification of differentially expressed genes in pistils from self-incompatible Citrus reticulata by suppression subtractive hybridization. Mol Biol Rep , 2013, 40 (1) : 159–169. DOI:10.1007/s11033-012-2045-6 |
| [115] | Ulker B, Shahid Mukhtar M, Somssich IE. The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta , 2007, 226 (1) : 125–137. DOI:10.1007/s00425-006-0474-y |
| [116] | Jiang YJ, Liang G, Yang SZ, et al. Arabidopsis WRKY57 functions as a node of convergence for Jasmonic acid- and Auxin-mediated signaling in Jasmonic acid-induced leaf senescence. Plant Cell , 2014, 26 : 230–245. DOI:10.1105/tpc.113.117838 |
| [117] | Han M, Kim CY, Lee J, et al. OsWRKY42 represses OsMT1d and induces reactive oxygen species and leaf senescence in rice. Mol Cells , 2014, 37 (7) : 532–539. DOI:10.14348/molcells.2014.0128 |
| [118] | Bakshi M, Oelmüller R. WRKY transcription factors:Jack of many trades in plants. Plant Signal Behav , 2014, 9 (2) : e27700. DOI:10.4161/psb.27700 |
| [119] | Nuruzzaman M, Sharoni AM, Satoh K, et al. Comparative transcriptome profiles of the WRKY gene family under control, hormone-treated, and drought conditions in near-isogenic rice lines reveal differential, tissue specific gene activation. J Plant Physiol , 2014, 171 (1) : 2–13. DOI:10.1016/j.jplph.2013.09.010 |
| [120] | Zhang H, Zhao M, Song Q, et al. Identification and function analyses of senescence-associated WRKYs in wheat. Biochem Biophys Res Commun , 2016, 474 (4) : 761–767. DOI:10.1016/j.bbrc.2016.05.034 |
| [121] | Robatzek S, Somssich IE. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev , 2002, 16 : e1139–1149. DOI:10.1101/gad.222702 |
| [122] | Yan JY, Li CX, Sun L, et al. A WRKY transcription factor regulates Fe translocation under Fe deficiency in Arabidopsis. Plant Physiol , 2016, 171 (3) : 2017–2027. |
| [123] | Xu YH, Wang JW, Wang S, et al. Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene(+)-delta-cadinene synthase-A. Plant Physiol , 2004, 135 (1) : 507–515. DOI:10.1104/pp.104.038612 |
| [124] | Skibbe M, Qu N, Galis I, et al. Induced plant defenses in the natural environment:Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell , 2008, 20 : 1984–2000. DOI:10.1105/tpc.108.058594 |
| [125] | Qiu JL, Fiil BK, Petersen K, et al. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J , 2008, 27 : 2214–2221. DOI:10.1038/emboj.2008.147 |
| [126] | Song S, Qi T, Fan M, et al. The bHLH subgroup Ⅲd factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet , 2013, 9 (7) : e1003653. DOI:10.1371/journal.pgen.1003653 |
| [127] | Kato N, Dubouzet E, Kokabu Y. Identification of a?WRKY?protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in Coptis japonica. Plant Cell Physiol , 2007, 48 (1) : 8–18. |
| [128] | Jaroslav M, Tomáš K, Josef P, et al. The “putative” role of transcription factors from HlWRKY family in the regulation of the final steps of prenylflavonid and bitter acids biosynthesis in hop(Humulus lupulus L. ). Plant Mol Biol , 2016, 92 (3) : 263–277. DOI:10.1007/s11103-016-0510-7 |
| [129] | Liu J, Chen X, Liang X, et al. Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense. Plant Physiol , 2016, 171 (2) : 1427–1442. |
| [130] | Sheikh AH, Eschen-Lippold L, Pecher P, et al. Regulation of WRKY46 transcription factor function by mitogen-activated protein kinases in Arabidopsis thaliana. Plant Sci , 2016, 7 : 61. |
| [131] | Xing DH, Lai ZB, Zheng ZY, et al. Stress-and pathogen-induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant , 2008, 1 (3) : 459–470. DOI:10.1093/mp/ssn020 |
| [132] | Gao X, Chen X, Lin W, et al. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog , 2013 : e1003127. |
| [133] | Zhang Z, Wu Y, Gao M, et al. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe , 2012, 11 : 253–263. DOI:10.1016/j.chom.2012.01.015 |
| [134] | Miao Y, Laun TM, Smykowski A, et al. Arabidopsis MEKK1 can take a short cut:it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol , 2007, 65 : 63–76. DOI:10.1007/s11103-007-9198-z |
| [135] | Mao G, Meng X, Liu Y, et al. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell , 2011 : 1639–1653. |
| [136] | Adachi H, Nakano T, Miyagawa N, et al. WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell , 2015, 27 : 2645–2663. DOI:10.1105/tpc.15.00213 |
| [137] | Li R, Zhang J, Li J, et al. Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. Elife , 2015, 4 : e04805. |