植物丝裂原活化蛋白激酶级联信号转导通路研究进展

姜生秀，李德禄

(甘肃省治沙研究所，民勤沙生植物园，甘肃民勤 733300)



植物丝裂原活化蛋白激酶级联信号转导通路研究进展

姜生秀，李德禄*

(甘肃省治沙研究所，民勤沙生植物园，甘肃民勤 733300)

摘要:丝裂原活化蛋白激酶(MAPK)是酵母、动物和植物等真核生物中普遍存在和高度保守的一类信号转导通路，由MAPKKK、MAPKK和MAPK等3部分组成，在应对生物非生物胁迫、激素、细胞分裂调控及植物生长发育等过程中发挥重要作用。该文对近年来国内外有关MAPK级联通路的组成、在植株体内的生物学功能以及MAPK通路的失活进行了概述，旨在为今后MAPK通路介导的信号转导机制的研究提供参考依据。

关键词:丝裂原活化蛋白激酶(MAPK)；信号转导；生物学功能

各种外界和内部信号分子调节着植物的生长和发育，细胞内的受体蛋白通过识别胞外信号分子并将其向下游传递，从而引起一系列的生物化学反应及蛋白之间的相互作用，这个过程被叫做细胞信号转导[1]。信号转导是真核细胞应对外界信号及调节复杂胞内变化的一种重要途径，在调控细胞增殖、新陈代谢、变异和生存等细胞过程中发挥重要作用[2]。

外界环境胁迫下，植物信号转导通路可分为四大主要类型：丝裂原活化蛋白激酶级联途径、Ca2+依赖信号转导通路、Ca2+依赖的盐过敏感(SOS)信号通路和ABA信号转导通路[3]。其中，丝裂原活化蛋白激酶(MAPK)级联途径是酵母、动物和植物等真核生物中普遍存在和高度保守的一类信号转导通路[4]。MAPK级联途径包括三个功能性串联的蛋白激酶：丝裂原活化蛋白激酶激酶激酶(MAPKKK)、丝裂原活化蛋白激酶激酶(MAPKK)和丝裂原活化蛋白激酶(MAPK)[5]。不同的MAPK通路感应不同的外界信号刺激。现已证明，在植物中，MAPK通路在应对生物非生物胁迫、激素、细胞分裂调控及植物生长发育等过程中发挥着重要作用[4]。

1MAPK级联通路的组成

MAPK级联途径由MAPKKK-MAPKK-MAPK三级激酶系统组成，MAPKK被上游的MAPKKK磷酸化，磷酸化位点为Ser/Thr残基，该位点氨基酸序列为SXXXS/T(X代表任何氨基酸)，反过来，MAPKK磷酸化MAPK，磷酸化位为Thr或Thr残基，由此使信号逐级放大并传递到下游[5]。

1.1丝裂原活化蛋白激酶激酶激酶(MAPKKK)

MAPKKK是级联反应的第一部分，被认为是目前MAPK级联途径中最复杂和数量最多的部分。拟南芥(Arabidopsisthaliana)中已被确认有80多种，被分为3个亚族：MEKKs亚族，有21个；Rafs亚族，有48个；ZIKs亚族，有11个成员[6]。在Rafs亚族中，各蛋白激酶的结构域十分保守，其中功能缺失突变基因CTRl(Constitutive triple response 1)在乙烯介导的信号转导途径中组成性表达，编码负调节子，抑制乙烯诱导基因的表达[7]，Raf型CTR1基因EDR1在植物防御响应中起到负调节作用[8]，At1g73660是一种Raf型MAPKKK成员，可以减弱拟南芥的耐盐性[9]。MAP3K中的MEEK可以被磷酸化激活(即为MAP4K)，也可以被Ras或Rho家族的小GTP结合蛋白结合而产生活性[10]。MEKKK型ANP1基因具有应对氧化胁迫、诱导特异胁迫应答基因的表达及阻止植物激素的功能[11]，如烟草(Nicotianatabacum)MEKKK型基因NPK1能增强转基因植物对非生物胁迫的耐受性[12]。AtMEKK1和AtMEKK4可受到渗透、机械损伤和病原的诱导[6]，AtMEKKs亚组中的ANPKls与调控H2O2的信号传导有关[13]。NPKl蛋白激酶大量存在于侧根原基和根茎顶端分生组织之间，与植物细胞的分裂和增殖有关[14]。ZIKs亚族中的蛋白激酶主要与MAPKs途径的调节子ZRl的表达作用有关[15]。

1.2丝裂原活化蛋白激酶激酶(MAPKK)

植物MAPKK在MAPK级联途径中的成员数量最小，到目前为止，拟南芥基因组中已报道了至少60个MAPKKK和20个MAPK，但只有10个MAPKK被发现。上游的MAPKKK感应外界信号，通过10个MAPKK传递到20个MAPK中，表明MAPKK是上游逆境信号的聚集点，也是下游MAPK的分枝点[5]。MAPKK是双重特异性激酶，植物MAPKK最少的信号序列是S-T-XX-G-T-X-X-Y-M-X-P-E-R，植物MAPKK有保守的S/T-X5-S/T序列，而动物激酶的序列为S/T-X3-S/T；根据氨基酸序列比对将拟南芥的MAPKK分为4个组，分别为A、B、C和D，其中C组和D组的MAPKK的编码基因不含内含子。植物MAPKK 的N端延伸表明了有一个假定的MAPK切入点，序列为[K/R][K/R][K/R]x(1-5)[L/I]x[L/I] ，类似在动物MAPKK中发现的序列[15]。另外，MAPKK有很高的底物特异性。

1.3丝裂原活化蛋白激酶(MAPK)

MAPK是级联反应的最后一部分，在连接上游组分和下游底物中起到重要作用[16]，MAPK能磷酸化特异效应蛋白，从而激活细胞的响应元件。自从苜蓿(MedicagosativaLinn.)中首次发现MAPK以来，至今在植物中已有大量MAPK被发现，基因组测序技术显示在拟南芥中有20个 MAPK[17]，水稻(Oryzasativa)有17个[18]，杨树(Populus)有21个[19]。根据编码的蛋白序列的TXY基序的不同，可将其分为TEY类和TDY类，根据系统发生关系将TEY类进而划分为A、B、C组，TDY类单独列为D组[20]。据报道，A类有AtMPK3、AtMPK6和OsMAPK5；B类有AtMPK4和ZmSIMK1；C类有AtMPK1、AtMPK2、PsMPK2和GhMPK7。这些MAPK在植物胁迫响应和生长发育过程中都发挥着重要作用[21]，如拟南芥的AtMPK3可被多种环境胁迫激活，氧化胁迫也能激活该激酶[22]；应用MPK4的特异性抗体分析显示AtMPK4参加生物和非生物胁迫应答[23]；PsMPK2在拟南芥中过表达其活性受机械伤害以及其他胁迫信号诸如ABA、H2O2等诱导[24]。从单子叶植物中获得了详细的D类MAPK功能资料，如OsBWMK1诱导PR基因的表达，并增强了植物抵抗真菌和细菌感染的能力[25]；AtMPK9优先在保卫细胞中表达，具有功能冗余性，在ABA信号通路中对活性氧下游起到正调控的作用[26]；AtMPK18有能调节植物细胞皮层微管的功能[27]；棉花(Gossypiumspp.)GhMPK16的表达受化学和生物信号的诱导[28]。

2MAPK级联反应的功能

植物在整个生命周期中经常受到各种生物和非生物胁迫，干旱、盐和低温等是造成植物减产的主要因素，为应对它们生存的限定因素，植物具有感知和传递刺激信号的能力，其中，MAPK级联通路将感知到的刺激信号传递到细胞中，然后生物体通过蛋白质的磷酸化和去磷酸化实现对逆境的调控[29]。

2.1MAPK参与的植物化学信号途径

目前已有很多证据证明MAPK途径参与了植物化学信号途径，研究较多的植物内源信号分子中，有水杨酸(SA)、茉莉酸(JA)和吲哚乙酸(IAA)等。OsBIMK1基因的表达受化学分子如JA、BTH的诱导[30]；OsMSRMK2表达受JA诱导[31]；OsSIPK稳定期的mRNA分析表明该基因在2周大的水稻幼苗中微弱组成型表达，当用环己酰亚胺(CHX)、JA和SA处理时，OsSIPK的转录水平会增强[32]；AtMPK4在SA通路中起到负调控作用，而在JA通路中起到正调控作用[33]。SA含量的积累不仅造成细胞的死亡，也会激活MAPK信号通路。如Liu等[34]发现大豆(Glycinemax)中GmMPK4s的沉默导致叶片细胞的死亡和SA含量的升高。

2.2MAPK参与植物生物胁迫下的信号传导

自然界各种病原体威胁着植物的生长，植物自身形成了多种防御措施，除了化学和物理障碍措施外，还通过病原体诱导措施来保护自己，包括细胞壁增厚、产生植物抗毒素、激活防御基因活性等[35]。Suzuki等[36]用从疫霉菌(Phytophthorainfestans)衍生而来的一种诱导子处理烟草悬浮细胞时发现，47 kDa的 MAPK快速而短暂地被激活。Zhang等[37]发现当烟草感染花叶病毒时，烟草中有2种MAPK被激活，分别是 48 kD的水杨酸(SA)诱导蛋白激酶(SIPK)和44 kD的创伤诱导蛋白激酶(WIPK)。He等[38]从水稻中克隆获得了一种MAPK基因BWMK1，该基因在水稻感染稻瘟菌4 h后表达。据最近的报道，AhMPK3在转基因烟草中过表达增强了烟草对斜纹夜蛾(Spodopteralitura)的耐受性[39]，GhMPK16在拟南芥中的异位表达增强了植物的抗病性[38]。Northern杂交显示，GhMPK7的转录水平受病原体诱导，转化烟草后，转基因烟草表现出了很强的抵抗烟草炭疽病菌(Colletotrichumnicotiana)和病毒PVY的能力，并且SA通路基因的转录水平也得到了快速的增强[40]。可见，MAPK参与植物生物胁迫下的信号传导。

2.3MAPK途径在植物激素信号转导通路中的作用

脱落酸(ABA)在种子萌发、气孔调节和干旱、盐、低温等非生物胁迫中都起到一定的作用，ABA对逆境胁迫的适应作用主要是通过诱导必要的胁迫相关基因的表达来实现。在糊粉层细胞中，ABA快速而短暂地激活MAPK的活性，而赤霉素(GA)则抑制MAPK的转录水平。PsMAPK3在豌豆(Pisumsativum)中的表达受GA、6-BA诱导[41]，而转PsMPK2基因拟南芥中PsMPK2和AtMPK1 及AtMPK2一样具有ABA和H2O2耐受性[42]；拟南芥中ABA激活AtMPK3和p46MAPK的活性[43]，而水稻中OsMAPK5的活性受ABA的激活[44]；棉花GhMPK6基因参与ABA诱导的CAT1的表达[45]；ABA可以诱导玉米ZmMPK5少量表达[46]；GhMPK2在烟草中过表达致使植物降低对ABA的敏感性[47]。

乙烯是植物生命活动中的重要调节物质，参与植物的果实成熟和花叶衰老等过程，也有诱导防御体系的功能，例如，当烟草受到病原体侵害时，其叶片就会快速诱导蛋白的磷酸化，从而对病原菌起抑制作用[48]。TR1、ETR2和EIN4是乙烯的受体，CTR1编码一种和Raf家族相似的蛋白；CTR1在乙烯信号通路中作为负调控因子，它在乙烯受体的下游，乙烯受体结合并激活CTR1[49]。很多人认为MAPK通路参与了乙烯信号转导，如用乙烯处理烟草叶片后会激活一种50 kD大的 MBP激酶，这种激酶是CTR1下游的一种MAPK激酶[50]。

植物生长素在植物生长和发育过程中也起到很重要的调节作用，如顶端优势、侧根和根须的形成及微管的变异等。很多研究发现了蛋白激酶和磷酸酶在生长素信号通路中的作用，首先证明了MAPK是参与生长素信号转导的一种激酶，将缺少生长素的烟草BY-2细胞用合成生长素，即2,4-二氯苯乙酸 (2,4-D)进行处理，结果46 kD的 MBP激酶被快速激活[51]；此外，用生长素处理后，一种磷酸化重组AtMPK2蛋白激酶的活性也得到了增强。这些结果表明MAPKK和 MAPK在生长素介导的信号转导中发挥着一定的作用[52]。

2.4MAPK与非生物胁迫信号的关系

植物在生存的过程中要应对各种非生物胁迫，包括干旱、高温低温和渗透胁迫等。例如，在拟南芥中，冷和盐胁迫能诱导完整的MAPK级联途径：MEKK1-MKK2-MPK4[53]，MAPKK4和MAPKK6被冷和盐诱导，而MAPKK1被盐和干旱诱导，MAPKK10-2只被冷胁迫诱导[54]；烟草的一个MAPKK家族SIPKK，当植物受到创伤之后其表达量升高[55]；大豆GMK1的活性在盐胁迫下被激活[56]；黄瓜(CucumissativusLinn.)CsNMAPK在转基因烟草中受到盐胁迫和渗透胁迫诱导[57]；苹果砧木山定子(MalushupehensisRehd. var.pinyiensisJiang)的叶和根中MhMAPK的mRNA水平被干旱和盐所诱导[58]；在盐和渗透胁迫下，TMKP1在小麦(TriticumaestivumLinn.)中被诱导表达[59]；海蓬子 (Salicorniabrachiata)SbMAPKK的转录水平被旱、冷和盐诱导，并在盐诱导下的转录水平最高[60]。ZmSIMK1在拟南芥中的过表达增强了植物的耐盐性，并且诱导了胁迫相关基因RD29和P5CS1的表达[61]。水稻中OsMAPK44的活性受盐、干旱和氧化胁迫诱导，但不受冷胁迫诱导[62]，而OsMAPK33在干旱胁迫下其转录水平升高，而在盐胁迫下转录水平下降[63]。棉花中，GhMPK2和GhMPK16具有耐受渗透胁迫的能力[64]，将GhMPK3转化烟草中增强了转基因烟草的耐旱性和耐氧化性[65]。

活性氧(ROS)是多种胁迫信号通路的中间信号分子，非生物胁迫导致ROS在植物体内的积累，MAPK级联通路不仅可以被ROS诱导，也可以调节ROS含量。在渗透胁迫下，烟草中过表达的ZmMPK7基因通过调节过氧化物酶(POD)活性降低ROS造成的伤害[66]。水稻中，MAPKKK的DSM1通过ROS的清除参与和干旱胁迫有关的信号通路[67]。当植物受到创伤时，AtMPK8通过整合ROS、Ca2+和蛋白的磷酸化作用对ROS的体内平衡起到调节作用[68]。

另外，已有证据表明低温影响许多植物蛋白的磷酸化位点。Northern杂交结果表明，ZmMPK17的转录水平受多种逆境胁迫诱导，在烟草中的过表达增强了植物对低温的耐受性[69]。Berberich 等[70]从玉米中分离出了ZmMPK4，转入烟草中发现该基因增强了转基因植株对低温的耐受性。马郁兰(OriganumonitesL.)OoMAPKK1在低温胁迫下表达量明显升高[71]。在低温条件下，OsMAPK2的mRNA积累量显著升高[72]。

3MAPK通路的失活

MAPK级联途径的失活和活化同等重要，MAPK的失活是通过TXY 域里Ser或Tyr的去磷酸化来调节。目前，已克隆获得了一些酵母和动物的磷酸化酶，发现它们具有使MAPK失活的功能，这类酶至少可以被分为3类：双特异性磷酸酶(DsPTPases)，能使MAPK在Ser或Tyr位点去磷酸化；酪氨酸磷酸化酶(PTPases)，只在Tyr位点去磷酸化；丝氨酸/苏氨酸磷酸化酶(PPases)[52]。DsPTPases具有活性位点VXVHCXXGXSRSXTXXXAY(L/I)M，这个特异的域和PTPase有同源性，因此，又可把PTPase和DsPTPases归为同一类[73]。

迄今，有很多研究证明了高等植物中MAPK 的激活伴随蛋白激酶中Tyr的磷酸化，这些研究为MAPK自磷酸化或Tyr位点被磷酸化提供了证据，同时也证明了植物具有酪氨酸磷酸化酶，在Tyr位点去磷酸化并且使MAPK失活[74]。拟南芥双特异性磷酸酶AtDsPTP1在Tyr位点去磷酸化，并使AtMPK4失活，导致AtDsPTP1在不同的胁迫下于不同组织中组成型表达[73]。另外，编码PTPase的一些基因的表达并不受MAPK通路的调节[75]。拟南芥AtPTP1的转录水平受到高盐胁迫诱导和低温的抑制，AtPTP1具有去磷酸化功能，在体外能使一种MAPK失活[76]。Gupta等[77]在研究MAPK活性的实验中发现，AtMPK6的活性受H2O2调节， 在体外AtPTP1 能使AtMPK6失活；最近从豌豆和大豆中也分离得到AtPTP1[78]。Haring等[79]从衣藻属(Chlamydomonas)中分离出了一种双特异性磷酸酶VH-PTP13，具有去磷酸化的功能，因此在体外能使紫花苜蓿中的SIMK和MMK2失活。

4展望

MAPK级联途径作为细胞信号转导途径中重要的组成部分，已有越来越多的MAPK基因从植物中克隆获得，并对其功能开展了研究。目前，对于MAPK基因功能和作用原理的研究只是现象描述，还存在很多问题，因此，对MAPK级联途径的诸多方面还有待进一步探讨。主要包括以下几个方面：(1)植物在进化过程中形成了一套非常完善的感应外界刺激的机制，各种各样的蛋白激酶及同一类激酶的不同亚类之间在信号传递过程中有交叉作用，所以在现有研究基础上需要进一步弄清各种蛋白激酶之间的相互关系；(2)进一步阐明MAPK级联途径的下游事件及在植株体内介导的生化代谢和生理调控过程；(3)阐明植物中与MAPK级联途径相关的信号转导分子途径，以及MAPK级联途径与植物细胞中其他信号途径的动态互作关系。

参考文献:

[1]NARINDER K, ANIL K. Signal transduction pathways under abiotic stresses in plants[J].CurrentScience, 2005, 6:1 771-1 780.

[2]LIU Y, ZHAO H Y. A computational approach for ordering signal transduction pathway components from genomics and proteomics Data[J].BMCBioinformatics, 2004, 10:1-6.

[3]XIONG L, SCHUMAKER K S, ZHU J K. Cell signalling during cold, drought and salt stress[J].PlantCell, 2002, 1:165-163.

[4]HWA CH M, YANG X C. The AtMKK3 pathway mediates ABA and salt signaling inArabidopsis[J].ActaPhysiol.Plant, 2008, 30:277-286.

[5]XU H N, LI K Z, YANG F J. Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses[J].Mol.Biol.Rep., 2010, 37:3 157-3 163.

[6]MIZOGUCHI T, IRIE K, HIRAYAMA T,etal. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen·activated protein kinase and an S6 ribosomal protein kinase by touch,cold,and water stress inArabidopsisthaliana[J].NationalAcadSciences,1996,93(2): 765-769.

[7]DAMS P L, BRRY C, KANNAN P,etal, GIOVANNONI J. Evidence that CTR1 mediated ethylene signal transduction in tomato is encoded by a multigene family whose members display distinct regulatory features[J].PlantMol.Biol., 2004, 54:387-404.

[8]FRYE C A, TANG D, INNES R W. Negative regulation of defense responses in plants by a conserved MAPKK kinase[J].Proc.Natl.Acad.Sci., 2001, 98:373-378.

[9]GAO L, XIANG C B. The genetic locusAt1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance inArabidopsis[J].PlantMol.Biol., 2008, 67:125-134.

[10]JOHNSON G L, LAPADAT R. Mitogen-activated protein kinase pathways mediated by ERK,JNK,and p38 protein kinases[J].Science, 2002,298(5 600):1 911-1 912.

[11]KOVTUN Y, CHIU W L, ZENG W,etal. Suppression of auxin signal transduction by a MAPK cascade in higher plants[J].Nature, 1998, 395:716-720.

[12]SHOU H, BORDALLO P, WANG K. Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize[J].J.Exp.Bot., 2004, 55:1 013-1 019.

[13]KOVTUN Y,CHIU W L,TENA G,etal.Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in Plants[J].Proc.Natl.Acad.Sci.USA,2000,97(6):2 940-2 945.

[14]NISHIHAMA R,SOYANO T,ISHIKAWA M,etal.Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex[J].Cell,2002,109(1):87-99.

[15]ZWERGER K, HIRT H. Recent advances in plant MAP kinase signaling[J].Biol.Chem., 2001, 382:1 123-1 131.

[16]ZHU N, SHAO Y, XU L,etal. Gadd45-alpha and Gadd45-gamma utilize p38 and JNK signaling pathways to induce cell cycle G2/M arrest in Hep-G2 hepatoma cells[J].Mol.Biol.Rep., 2009, 36:2 075-2 085.

[17]KAZUYA I, KAZUO S, GUILLAUME T. Mitogen-activated protein kinase cascades in plants: a new nomenclature[J].TrendsPlantSci., 2002, 10:1 360-1 385.

[18]REYNA N S, YANG Y. Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection[J].Mol.PlantMicrobeInteract, 2006, 19:530-540.

[19]NICOLE M C, HAMEL L P, MORENCY M J,etal. MAP-ping genomic organization and organspecific expression profiles of poplar MAP kinases and MAP kinase kinases[J].BMCGenomics, 2006, 7:223-245.

[20]HAMEL L P, NICOLE M C, SRITUBTIM S,etal. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families[J].TrendsPlantSci., 2006, 11:192-198.

[21]ZHANG L, XI D M, LI S W. A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco[J].PlantMol.Biol., 2011, 77:17-31.

[22]KOVTUN Y, CHIU W L,TENA G,etal.Functional analysis of oxidative stress activated mitogen-activated protein kinase cascade in plants[J].Proc.Natl.Acad.Sci.USA,2000,97:2 940-2 945.

[23]DESIKAN R, HANCOCK J T, ICHIMURA K,etal.Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6[J].PlantPhysiol., 2001,126:1 579-1 587.

[24]ORTIZ-MASIA D,PEREZ-AMADOR M A,CARBONELL P,etal. Characterization of PsMPK2,the first C1 subgroup MAP kinase from pea (PisumsativumL.)[J].Planta,2008,227:1 333-1 342.

[25]CHEONG H, MOON B C, KIM J K. BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor[J].PlantPhysiol, 2003, 132:1 961-1 972.

[26]JAMMES F, SONG C, SHIN D,etal. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling[J].Proc.Natl.Acad.Sci., 2009, 106:20 520-20 525.

[27]WALIA A, LEE J S, WASTENEYS G, ELLISl B. Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells[J].PlantJ, 2009, 59:565-575.

[28]SHI J, ZHANG L, AN H L. GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity[J].BMCMolecularBiology, 2011, 12:1-12.

[29]韩静, 罗利军. 水稻MAPKK家族基因克隆及转基因研究[D]. 上海:上海海洋大学, 2009.

[30]SONG F M, ROBERT M G. OsBIMK1, a rice MAP kinase gene involved in disease resistance responses[J].Planta, 2002, 215:997-1 005.

[31]AGRAWAL G K, RAKWAL R, IWAHASHI H. Isolation of novel rice (OryzasativaL.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues[J].Biochem.Biophys.Res.Commun., 2002, 294:1 009-1 016.

[32]LEE M O, CHO K W, SO H K. Novel rice OsSIPK is a multiple stress responsive MAPK family member showing rhythmic expression at mRNA level[J].Planta, 2008, 227:981-990.

[33]SCHWEIGHOFER A, KAZANAVICIUTE V, SCHEIKL E. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels inArabidopsis[J].PlantCell, 2007, 19:2 213-2 224.

[34]LIU J Z, HEIDI D, EDWARD B. Soybean homologs ofMPK4 negatively regulate defense responses and positively regulate growth and development[J].PlantPhysiology, 2011, 11: 1 363-137.

[35]YANG Y, SHAH J, KLESSIG D F. Signal perception and transduction in plant defense responses[J].GenesDev., 1997, 11:1 621-1 639.

[36]SUZUKI K, SHINSHI H. Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with fungal elicitor[J].PlantCell, 1997,7:639-647.

[37]ZHANG S, KLESSIG D F. Resistance gene N-mediated denovo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection[J].Proc.Natl.Acad.Sci.USA, 1998, 95:7 433-7 438.

[38]KLOEPPER J W, TUZUN S, KU J A. Proposed definitions related to induced disease resistance[J].BiocontrolScienceandTechnology, 1992, 2(4):349-351.

[39]HE C, FONG S H, YANG D,etal. BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice[J].Mol.Plant-MicrobeInteract, 1999, 12:1 064-1 073.

[40]SHI J, AN H L, ZHANG L.GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development[J].PlantMol.Biol., 2010, 74:1-17.

[41]KUMAR K R, SRINIVASAN T, KIRTI P B. A mitogen-activated protein kinase gene, AhMPK3 of peanut: molecular cloning, genomic organization, and heterologous expression conferring resistance against Spodoptera litura in tobacco[J].Mol.GenetGenomics, 2009, 282:65-81.

[42]MARCOTE M J, CARBONELL J. Transient expression of a pea MAP kinase gene induced by gibberellic acid and 6-benzyladenine in unpollinated pea ovaries[J].PlantMol.Biol., 2000, 44:177-186.

[43]DOLORES O M, MIGUEL A, PEREZ A. Characterization of PsMPK2, the Wrst C1 subgroup MAP kinase from pea (PisumsativumL.)[J].Planta, 2008, 227:1 333-1 342.

[44]LU C, HAN M H, GEVARA G A,etal. Mitogene activated protein kinase signaling in postgermination arrest development by abscisic acid[J].Proc.Natl.Acad.Sci.USA, 2002, 99:15 812-15 817.

[45]XIONG L, YANG Y. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid inducible mitogen-activated protein kinase[J].PlantCell, 2003, 15:15 745-15 759.

[46]DING Y, CAO J, NI L,etal. ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signalling in maize[J].J.Exp.Bot., 2013, 64:871-884.

[47]ZHANG L, XI D M, LI S W. A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco[J].PlantMol.Biol., 2011, 77:17-31.

[48]RAZ V, FLUHR R. Ethylene signaling is transduced via protein phosphorylation events in plants[J].PlantCell, 1993, 5:2 359-2 368.

[49]CLARK K L, LARSEN P B, WANG X. Association of theArabidopsisCTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors[J].Proc.Natl.Acad.Sci.USA, 1998, 95:5 401-5 406.

[50]SESSA G, RAZ V, SAVALDI S. PK12, a plant dual-specificity protein kinase of the LAMMER family, is regulated by the hormone ethylene[J].PlantCell, 1996, 8:2 223-2 234.

[51]MIZOGUCHI T, GOTOH Y, NISHIDA E. Characterization of two cDNAs that encode MAP kinase homologues inArabidopsisthalianaand analysis of the possible role of auxin in activating such kinase activities in cultured cells[J].PlantJ., 1994, 5:111-122.

[52]IRUTE M, HERIBERT H. MAP kinase pathways: molecular plug-and-play chips for the cell[J].PlantMolecularBiology, 2000, 42:791-806.

[53]TEIGE M, SCHEIKL E, EULGEM T. The MKK2 pathway mediates cold and salt stress signaling inArabidopsis[J].Mol.Cell, 2004, 15:141-152.

[54]KUMAR K, RAO K P, SHARMA P,etal. Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stresses[J].PlantPhysiol.Bioch., 2008, 46:891-897.

[55]LIUY, ZHANG S, KLESSIG D F. Molecular cloning and characterization of a tobacco MAP kinase that interacts with SIPK[J].Mol.PlantMicrobe, 2000, 13(1):118-124.

[56]JONG H I, HYOUNGSEOK L, JITAE K. A salt stress-activated mitogen-activated protein kinase in soybean is regulated by phosphatidic acid in early stages of the stress response[J].J.PlantBiol., 2012, 55:303-309.

[57]XU H N, LI K Z, YANG F J,etal. Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses[J].Mol.Biol.Rep., 2010, 37:3 157-3 163.

[58]DUAN K X, YANG H Q, RAN K. Characterization of a novel stress-response member of the MAPK family in malus hupehensis rehd[J].PlantMol.Biol.Rep., 2009, 27:69-78.

[59]IKRAM Z, CHANTAL E, MAJDI T. TMKP1 is a novel wheat stress responsive MAP kinase phosphatase localized in the nucleus[J].PlantMol.Biol., 2010, 73:325-338.

[60]PRADEEP K A, KAPIL G, BHAVANATH J. Molecular characterization of theSalicorniabrachiataSbMAPKK gene and its expression by abiotic stress[J].Mol.Biol.Rep., 2010, 37:981-986.

[61]GU L K, LIU Y K, ZONG X J. Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 inArabidopsisincreases tolerance to salt stress[J].Mol.Biol.Rep., 2010, 37:4 067-4 073.

[62]MI J J, SEONG K L, BEOM G K. A rice (OryzasativaL.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses[J].PlantCell,TissueandOrganCulture, 2006, 85: 151-160.

[63]SEONG K, BEOM G K, TAEK R K. Overexpression of the mitogen-activated protein kinase gene OsMAPK33 enhances sensitivity to salt stress in rice (OryzasativaL.)[J].J.Biosci, 2009, 36:139-151.

[64]ZHANG S, KLESSIG D F. MAPK cascades in plant defense signaling[J].TrendsPlantSci., 2001, 6(11):520-527.

[65]LU L, WEI G, LI X.GbMPK3, a mitogen-activated protein kinase from cotton, enhances drought and oxidative stress tolerance in tobacco[J].PlantCellTiss.OrganCult., 2013, 2:153-162.

[66]ZONG X J, LI D P, GU L K. Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species[J].Planta, 2009, 229:485-495.

[67]NING J, LI X H, HICKS L M,etal. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice[J].PlantPhysiol., 2010, 152:876-890.

[68]TAKAHASHI F, MIZOGUCHI T, YOSHIDA R,etal. Calmodulin-dependent activation of MAP kinase for ROS homeostasis inArabidopsis[J].Mol.Cell, 2011, 41(6):649-660.

[69]PAN J W, ZHANG M Y, KONG X P.ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses[J].Planta, 2012, 235:661-676.

[70]BERBERICH T, SANO H, KUSANO T. Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize[J].Mol.Gen.Genet., 1999, 262:534-542.

[71]ISMAIL P. Molecular cloning and characterization of a mitogen-activated protein kinase kinase (OoMAPKK1) inOriganumonitesL.(Lamiaceae)[J].J.PlantBiochem.Biotechnol., 2013, 6:14-22.

[72]HUNG W C, HUANG D D. Reactive oxygen species, calcium and serine/threonine phosphatase are required for copper-induced MAP kinase gene,OsMAPK2, expression in rice[J].PlantGrowthRegulation, 2005, 45:233-241.

[73]GUPTA R, HUANG Y, KIEBER J. Identification of a dual-specificity protein phosphatase that inactivates a MAP kinase fromArabidopsis[J].PlantJ., 1998, 16:581-589.

[74]LUAN SH, TING J L, RAJEEV G. Protein tyrosine phosphatases in higher plants[J].NewPhytologist, 2001, 151:155-160.

[75]HUMBERTO M, MARTA F, CESAR N. Protein phosphatases in MAPK signalling: we keep learning from yeast[J].MolecularMicrobiology, 2005, 58(1):6-16.

[76]XU Q, FU H H, GUPTA R. Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene inArabidopsis[J].PlantCell, 1998, 10: 849-857.

[77]RAJEEV G, SHENG L. Control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants[J].PlantPhysiology, 2003, 7:1 149-1 152.

[78]FORDHAM S, SKIPSEY M, EVEANS I M. Higher plant tyrosine-specific protein phosphatases (PTPs) contain novel amino-terminal domains: expression during embryogenesis[J].PlantMol.Biol., 1999, 39:593-605.

[79]HARING M A, SIDERIUS M, JONAK C. Tyrosine phosphatase signalling in a lower plant: cell-cycle and oxidative stress-regulated expression of the Chlamydomonas eugametos VH-PTP13 gene[J].PlantJ., 1995, 7:981-988.

(编辑:裴阿卫)

文章编号:1000-4025(2016)06-1278-07

doi:10.7606/j.issn.1000-4025.2016.06.1278

收稿日期:2015-12-29;修改稿收到日期:2016-05-19

基金项目:甘肃省自然基金 (1308RJYA091)；典型沙生植物生态适应机制及其进化策略研究(145RJIA335)

作者简介:姜生秀(1987-)，女，硕士，研究实习员，主要从事植物抗逆分子生物学研究。E-mail:yanyunjiang1987@163.com *通信作者:李得禄，副研究员，主要从事荒漠植物及荒漠化防止研究。 E-mail:lidlu2008@163.com

中图分类号:Q257

文献标志码:A

Research Progress of Mitogen-activated Protein Kinase Signal Transduction Pathway

JIANG Shengxiu, LI Delu*

(Gansu Psammophyte Engineering Technology Research Center, Minqin Desert Botanical Garden, Minqin， Gansu 733300，China)

Abstract:Mitogen-activated protein kinase(MAPK) cascades are highly conserved signaling modules found in all eukaryotes, including fungi, plants and animals.A MAPK cascade generally consists of three components:a MAPKKK (MAPKK kinase), a MAPKK (MAPK kinase) and a MAPK, and they play essential roles in abiotic stresses, hormones, cell division and plant growth and development.In this article,we outlined the compositions,biological functions, inactivation of MAPK cascades,which aimed at providing some references basis for the research of MAPK- mediated signal transduction mechanisms.

Key words:Mitogen-activated protein kinase(MAPK); signal transduction pathway; biological functions