姜生秀，李德祿

(甘肅省治沙研究所，民勤沙生植物園，甘肅民勤 733300)

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植物絲裂原活化蛋白激酶級聯(lián)信號轉導通路研究進展

姜生秀，李德祿*

(甘肅省治沙研究所，民勤沙生植物園，甘肅民勤 733300)

摘要:絲裂原活化蛋白激酶(MAPK)是酵母、動物和植物等真核生物中普遍存在和高度保守的一類信號轉導通路，由MAPKKK、MAPKK和MAPK等3部分組成，在應對生物非生物脅迫、激素、細胞分裂調控及植物生長發(fā)育等過程中發(fā)揮重要作用。該文對近年來國內外有關MAPK級聯(lián)通路的組成、在植株體內的生物學功能以及MAPK通路的失活進行了概述，旨在為今后MAPK通路介導的信號轉導機制的研究提供參考依據。

關鍵詞:絲裂原活化蛋白激酶(MAPK)；信號轉導；生物學功能

各種外界和內部信號分子調節(jié)著植物的生長和發(fā)育，細胞內的受體蛋白通過識別胞外信號分子并將其向下游傳遞，從而引起一系列的生物化學反應及蛋白之間的相互作用，這個過程被叫做細胞信號轉導[1]。信號轉導是真核細胞應對外界信號及調節(jié)復雜胞內變化的一種重要途徑，在調控細胞增殖、新陳代謝、變異和生存等細胞過程中發(fā)揮重要作用[2]。

外界環(huán)境脅迫下，植物信號轉導通路可分為四大主要類型：絲裂原活化蛋白激酶級聯(lián)途徑、Ca2+依賴信號轉導通路、Ca2+依賴的鹽過敏感(SOS)信號通路和ABA信號轉導通路[3]。其中，絲裂原活化蛋白激酶(MAPK)級聯(lián)途徑是酵母、動物和植物等真核生物中普遍存在和高度保守的一類信號轉導通路[4]。MAPK級聯(lián)途徑包括三個功能性串聯(lián)的蛋白激酶：絲裂原活化蛋白激酶激酶激酶(MAPKKK)、絲裂原活化蛋白激酶激酶(MAPKK)和絲裂原活化蛋白激酶(MAPK)[5]。不同的MAPK通路感應不同的外界信號刺激?，F已證明，在植物中，MAPK通路在應對生物非生物脅迫、激素、細胞分裂調控及植物生長發(fā)育等過程中發(fā)揮著重要作用[4]。

1MAPK級聯(lián)通路的組成

MAPK級聯(lián)途徑由MAPKKK-MAPKK-MAPK三級激酶系統(tǒng)組成，MAPKK被上游的MAPKKK磷酸化，磷酸化位點為Ser/Thr殘基，該位點氨基酸序列為SXXXS/T(X代表任何氨基酸)，反過來，MAPKK磷酸化MAPK，磷酸化位為Thr或Thr殘基，由此使信號逐級放大并傳遞到下游[5]。

1.1絲裂原活化蛋白激酶激酶激酶(MAPKKK)

MAPKKK是級聯(lián)反應的第一部分，被認為是目前MAPK級聯(lián)途徑中最復雜和數量最多的部分。擬南芥(Arabidopsisthaliana)中已被確認有80多種，被分為3個亞族：MEKKs亞族，有21個；Rafs亞族，有48個；ZIKs亞族，有11個成員[6]。在Rafs亞族中，各蛋白激酶的結構域十分保守，其中功能缺失突變基因CTRl(Constitutive triple response 1)在乙烯介導的信號轉導途徑中組成性表達，編碼負調節(jié)子，抑制乙烯誘導基因的表達[7]，Raf型CTR1基因EDR1在植物防御響應中起到負調節(jié)作用[8]，At1g73660是一種Raf型MAPKKK成員，可以減弱擬南芥的耐鹽性[9]。MAP3K中的MEEK可以被磷酸化激活(即為MAP4K)，也可以被Ras或Rho家族的小GTP結合蛋白結合而產生活性[10]。MEKKK型ANP1基因具有應對氧化脅迫、誘導特異脅迫應答基因的表達及阻止植物激素的功能[11]，如煙草(Nicotianatabacum)MEKKK型基因NPK1能增強轉基因植物對非生物脅迫的耐受性[12]。AtMEKK1和AtMEKK4可受到滲透、機械損傷和病原的誘導[6]，AtMEKKs亞組中的ANPKls與調控H2O2的信號傳導有關[13]。NPKl蛋白激酶大量存在于側根原基和根莖頂端分生組織之間，與植物細胞的分裂和增殖有關[14]。ZIKs亞族中的蛋白激酶主要與MAPKs途徑的調節(jié)子ZRl的表達作用有關[15]。

1.2絲裂原活化蛋白激酶激酶(MAPKK)

植物MAPKK在MAPK級聯(lián)途徑中的成員數量最小，到目前為止，擬南芥基因組中已報道了至少60個MAPKKK和20個MAPK，但只有10個MAPKK被發(fā)現。上游的MAPKKK感應外界信號，通過10個MAPKK傳遞到20個MAPK中，表明MAPKK是上游逆境信號的聚集點，也是下游MAPK的分枝點[5]。MAPKK是雙重特異性激酶，植物MAPKK最少的信號序列是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，而動物激酶的序列為S/T-X3-S/T；根據氨基酸序列比對將擬南芥的MAPKK分為4個組，分別為A、B、C和D，其中C組和D組的MAPKK的編碼基因不含內含子。植物MAPKK 的N端延伸表明了有一個假定的MAPK切入點，序列為[K/R][K/R][K/R]x(1-5)[L/I]x[L/I] ，類似在動物MAPKK中發(fā)現的序列[15]。另外，MAPKK有很高的底物特異性。

1.3絲裂原活化蛋白激酶(MAPK)

MAPK是級聯(lián)反應的最后一部分，在連接上游組分和下游底物中起到重要作用[16]，MAPK能磷酸化特異效應蛋白，從而激活細胞的響應元件。自從苜蓿(MedicagosativaLinn.)中首次發(fā)現MAPK以來，至今在植物中已有大量MAPK被發(fā)現，基因組測序技術顯示在擬南芥中有20個 MAPK[17]，水稻(Oryzasativa)有17個[18]，楊樹(Populus)有21個[19]。根據編碼的蛋白序列的TXY基序的不同，可將其分為TEY類和TDY類，根據系統(tǒng)發(fā)生關系將TEY類進而劃分為A、B、C組，TDY類單獨列為D組[20]。據報道，A類有AtMPK3、AtMPK6和OsMAPK5；B類有AtMPK4和ZmSIMK1；C類有AtMPK1、AtMPK2、PsMPK2和GhMPK7。這些MAPK在植物脅迫響應和生長發(fā)育過程中都發(fā)揮著重要作用[21]，如擬南芥的AtMPK3可被多種環(huán)境脅迫激活，氧化脅迫也能激活該激酶[22]；應用MPK4的特異性抗體分析顯示AtMPK4參加生物和非生物脅迫應答[23]；PsMPK2在擬南芥中過表達其活性受機械傷害以及其他脅迫信號諸如ABA、H2O2等誘導[24]。從單子葉植物中獲得了詳細的D類MAPK功能資料，如OsBWMK1誘導PR基因的表達，并增強了植物抵抗真菌和細菌感染的能力[25]；AtMPK9優(yōu)先在保衛(wèi)細胞中表達，具有功能冗余性，在ABA信號通路中對活性氧下游起到正調控的作用[26]；AtMPK18有能調節(jié)植物細胞皮層微管的功能[27]；棉花(Gossypiumspp.)GhMPK16的表達受化學和生物信號的誘導[28]。

2MAPK級聯(lián)反應的功能

植物在整個生命周期中經常受到各種生物和非生物脅迫，干旱、鹽和低溫等是造成植物減產的主要因素，為應對它們生存的限定因素，植物具有感知和傳遞刺激信號的能力，其中，MAPK級聯(lián)通路將感知到的刺激信號傳遞到細胞中，然后生物體通過蛋白質的磷酸化和去磷酸化實現對逆境的調控[29]。

2.1MAPK參與的植物化學信號途徑

目前已有很多證據證明MAPK途徑參與了植物化學信號途徑，研究較多的植物內源信號分子中，有水楊酸(SA)、茉莉酸(JA)和吲哚乙酸(IAA)等。OsBIMK1基因的表達受化學分子如JA、BTH的誘導[30]；OsMSRMK2表達受JA誘導[31]；OsSIPK穩(wěn)定期的mRNA分析表明該基因在2周大的水稻幼苗中微弱組成型表達，當用環(huán)己酰亞胺(CHX)、JA和SA處理時，OsSIPK的轉錄水平會增強[32]；AtMPK4在SA通路中起到負調控作用，而在JA通路中起到正調控作用[33]。SA含量的積累不僅造成細胞的死亡，也會激活MAPK信號通路。如Liu等[34]發(fā)現大豆(Glycinemax)中GmMPK4s的沉默導致葉片細胞的死亡和SA含量的升高。

2.2MAPK參與植物生物脅迫下的信號傳導

自然界各種病原體威脅著植物的生長，植物自身形成了多種防御措施，除了化學和物理障礙措施外，還通過病原體誘導措施來保護自己，包括細胞壁增厚、產生植物抗毒素、激活防御基因活性等[35]。Suzuki等[36]用從疫霉菌(Phytophthorainfestans)衍生而來的一種誘導子處理煙草懸浮細胞時發(fā)現，47 kDa的 MAPK快速而短暫地被激活。Zhang等[37]發(fā)現當煙草感染花葉病毒時，煙草中有2種MAPK被激活，分別是 48 kD的水楊酸(SA)誘導蛋白激酶(SIPK)和44 kD的創(chuàng)傷誘導蛋白激酶(WIPK)。He等[38]從水稻中克隆獲得了一種MAPK基因BWMK1，該基因在水稻感染稻瘟菌4 h后表達。據最近的報道，AhMPK3在轉基因煙草中過表達增強了煙草對斜紋夜蛾(Spodopteralitura)的耐受性[39]，GhMPK16在擬南芥中的異位表達增強了植物的抗病性[38]。Northern雜交顯示，GhMPK7的轉錄水平受病原體誘導，轉化煙草后，轉基因煙草表現出了很強的抵抗煙草炭疽病菌(Colletotrichumnicotiana)和病毒PVY的能力，并且SA通路基因的轉錄水平也得到了快速的增強[40]?？梢?，MAPK參與植物生物脅迫下的信號傳導。

2.3MAPK途徑在植物激素信號轉導通路中的作用

脫落酸(ABA)在種子萌發(fā)、氣孔調節(jié)和干旱、鹽、低溫等非生物脅迫中都起到一定的作用，ABA對逆境脅迫的適應作用主要是通過誘導必要的脅迫相關基因的表達來實現。在糊粉層細胞中，ABA快速而短暫地激活MAPK的活性，而赤霉素(GA)則抑制MAPK的轉錄水平。PsMAPK3在豌豆(Pisumsativum)中的表達受GA、6-BA誘導[41]，而轉PsMPK2基因擬南芥中PsMPK2和AtMPK1 及AtMPK2一樣具有ABA和H2O2耐受性[42]；擬南芥中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基因參與ABA誘導的CAT1的表達[45]；ABA可以誘導玉米ZmMPK5少量表達[46]；GhMPK2在煙草中過表達致使植物降低對ABA的敏感性[47]。

乙烯是植物生命活動中的重要調節(jié)物質，參與植物的果實成熟和花葉衰老等過程，也有誘導防御體系的功能，例如，當煙草受到病原體侵害時，其葉片就會快速誘導蛋白的磷酸化，從而對病原菌起抑制作用[48]。TR1、ETR2和EIN4是乙烯的受體，CTR1編碼一種和Raf家族相似的蛋白；CTR1在乙烯信號通路中作為負調控因子，它在乙烯受體的下游，乙烯受體結合并激活CTR1[49]。很多人認為MAPK通路參與了乙烯信號轉導，如用乙烯處理煙草葉片后會激活一種50 kD大的 MBP激酶，這種激酶是CTR1下游的一種MAPK激酶[50]。

植物生長素在植物生長和發(fā)育過程中也起到很重要的調節(jié)作用，如頂端優(yōu)勢、側根和根須的形成及微管的變異等。很多研究發(fā)現了蛋白激酶和磷酸酶在生長素信號通路中的作用，首先證明了MAPK是參與生長素信號轉導的一種激酶，將缺少生長素的煙草BY-2細胞用合成生長素，即2,4-二氯苯乙酸 (2,4-D)進行處理，結果46 kD的 MBP激酶被快速激活[51]；此外，用生長素處理后，一種磷酸化重組AtMPK2蛋白激酶的活性也得到了增強。這些結果表明MAPKK和 MAPK在生長素介導的信號轉導中發(fā)揮著一定的作用[52]。

2.4MAPK與非生物脅迫信號的關系

植物在生存的過程中要應對各種非生物脅迫，包括干旱、高溫低溫和滲透脅迫等。例如，在擬南芥中，冷和鹽脅迫能誘導完整的MAPK級聯(lián)途徑：MEKK1-MKK2-MPK4[53]，MAPKK4和MAPKK6被冷和鹽誘導，而MAPKK1被鹽和干旱誘導，MAPKK10-2只被冷脅迫誘導[54]；煙草的一個MAPKK家族SIPKK，當植物受到創(chuàng)傷之后其表達量升高[55]；大豆GMK1的活性在鹽脅迫下被激活[56]；黃瓜(CucumissativusLinn.)CsNMAPK在轉基因煙草中受到鹽脅迫和滲透脅迫誘導[57]；蘋果砧木山定子(MalushupehensisRehd. var.pinyiensisJiang)的葉和根中MhMAPK的mRNA水平被干旱和鹽所誘導[58]；在鹽和滲透脅迫下，TMKP1在小麥(TriticumaestivumLinn.)中被誘導表達[59]；海蓬子 (Salicorniabrachiata)SbMAPKK的轉錄水平被旱、冷和鹽誘導，并在鹽誘導下的轉錄水平最高[60]。ZmSIMK1在擬南芥中的過表達增強了植物的耐鹽性，并且誘導了脅迫相關基因RD29和P5CS1的表達[61]。水稻中OsMAPK44的活性受鹽、干旱和氧化脅迫誘導，但不受冷脅迫誘導[62]，而OsMAPK33在干旱脅迫下其轉錄水平升高，而在鹽脅迫下轉錄水平下降[63]。棉花中，GhMPK2和GhMPK16具有耐受滲透脅迫的能力[64]，將GhMPK3轉化煙草中增強了轉基因煙草的耐旱性和耐氧化性[65]。

活性氧(ROS)是多種脅迫信號通路的中間信號分子，非生物脅迫導致ROS在植物體內的積累，MAPK級聯(lián)通路不僅可以被ROS誘導，也可以調節(jié)ROS含量。在滲透脅迫下，煙草中過表達的ZmMPK7基因通過調節(jié)過氧化物酶(POD)活性降低ROS造成的傷害[66]。水稻中，MAPKKK的DSM1通過ROS的清除參與和干旱脅迫有關的信號通路[67]。當植物受到創(chuàng)傷時，AtMPK8通過整合ROS、Ca2+和蛋白的磷酸化作用對ROS的體內平衡起到調節(jié)作用[68]。

另外，已有證據表明低溫影響許多植物蛋白的磷酸化位點。Northern雜交結果表明，ZmMPK17的轉錄水平受多種逆境脅迫誘導，在煙草中的過表達增強了植物對低溫的耐受性[69]。Berberich 等[70]從玉米中分離出了ZmMPK4，轉入煙草中發(fā)現該基因增強了轉基因植株對低溫的耐受性。馬郁蘭(OriganumonitesL.)OoMAPKK1在低溫脅迫下表達量明顯升高[71]。在低溫條件下，OsMAPK2的mRNA積累量顯著升高[72]。

3MAPK通路的失活

MAPK級聯(lián)途徑的失活和活化同等重要，MAPK的失活是通過TXY 域里Ser或Tyr的去磷酸化來調節(jié)。目前，已克隆獲得了一些酵母和動物的磷酸化酶，發(fā)現它們具有使MAPK失活的功能，這類酶至少可以被分為3類：雙特異性磷酸酶(DsPTPases)，能使MAPK在Ser或Tyr位點去磷酸化；酪氨酸磷酸化酶(PTPases)，只在Tyr位點去磷酸化；絲氨酸/蘇氨酸磷酸化酶(PPases)[52]。DsPTPases具有活性位點VXVHCXXGXSRSXTXXXAY(L/I)M，這個特異的域和PTPase有同源性，因此，又可把PTPase和DsPTPases歸為同一類[73]。

迄今，有很多研究證明了高等植物中MAPK 的激活伴隨蛋白激酶中Tyr的磷酸化，這些研究為MAPK自磷酸化或Tyr位點被磷酸化提供了證據，同時也證明了植物具有酪氨酸磷酸化酶，在Tyr位點去磷酸化并且使MAPK失活[74]。擬南芥雙特異性磷酸酶AtDsPTP1在Tyr位點去磷酸化，并使AtMPK4失活，導致AtDsPTP1在不同的脅迫下于不同組織中組成型表達[73]。另外，編碼PTPase的一些基因的表達并不受MAPK通路的調節(jié)[75]。擬南芥AtPTP1的轉錄水平受到高鹽脅迫誘導和低溫的抑制，AtPTP1具有去磷酸化功能，在體外能使一種MAPK失活[76]。Gupta等[77]在研究MAPK活性的實驗中發(fā)現，AtMPK6的活性受H2O2調節(jié)， 在體外AtPTP1 能使AtMPK6失活；最近從豌豆和大豆中也分離得到AtPTP1[78]。Haring等[79]從衣藻屬(Chlamydomonas)中分離出了一種雙特異性磷酸酶VH-PTP13，具有去磷酸化的功能，因此在體外能使紫花苜蓿中的SIMK和MMK2失活。

4展望

MAPK級聯(lián)途徑作為細胞信號轉導途徑中重要的組成部分，已有越來越多的MAPK基因從植物中克隆獲得，并對其功能開展了研究。目前，對于MAPK基因功能和作用原理的研究只是現象描述，還存在很多問題，因此，對MAPK級聯(lián)途徑的諸多方面還有待進一步探討。主要包括以下幾個方面：(1)植物在進化過程中形成了一套非常完善的感應外界刺激的機制，各種各樣的蛋白激酶及同一類激酶的不同亞類之間在信號傳遞過程中有交叉作用，所以在現有研究基礎上需要進一步弄清各種蛋白激酶之間的相互關系；(2)進一步闡明MAPK級聯(lián)途徑的下游事件及在植株體內介導的生化代謝和生理調控過程；(3)闡明植物中與MAPK級聯(lián)途徑相關的信號轉導分子途徑，以及MAPK級聯(lián)途徑與植物細胞中其他信號途徑的動態(tài)互作關系。

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(編輯:裴阿衛(wèi))

文章編號: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

基金項目:甘肅省自然基金 (1308RJYA091)；典型沙生植物生態(tài)適應機制及其進化策略研究(145RJIA335)

作者簡介:姜生秀(1987-)，女，碩士，研究實習員，主要從事植物抗逆分子生物學研究。E-mail:yanyunjiang1987@163.com *通信作者:李得祿，副研究員，主要從事荒漠植物及荒漠化防止研究。 E-mail:lidlu2008@163.com

中圖分類號:Q257

文獻標志碼: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