植物冷驯化相关信号机制

ISS N 100727626C N 1123870ΠQ中国生物化学与分子生物学报Chinese Journal of Biochemistry and M olecular Biology2008年4月24(4):295～301・综述・植物冷驯化相关信号机制夏金婵,　吕　强,　郭梅芳,　何奕昆3(首都师范大学生命科学学院,北京　100037)摘要　植物经过非致死温度的处理可以获得更强的抗冷能力叫做冷驯化,主要包括寒驯化和冻驯化.在冷驯化过程中,质膜首先感受冷信号,调节胞质中IP 3的含量,诱导胞质Ca 2+浓度的升高,从而激活CB F 基因的表达.至今已经克隆了大量的冷调控基因,组成了复杂的信号传导网络,其中ICE12C BF 2C OR 通路在植物的冷驯化过程中起到重要的作用.ICE 1基因编码一个MY B 类型的碱性螺旋2环2螺旋(bH LH )转录因子,在上游调节CB F 和其它转录因子的表达,提高抗冷性.H OS1蛋白通过泛素化介导的蛋白降解负调控ICE1,另外,C BF 还通过转录的自我调控保持恰当的表达水平.基因的分析研究证明,RNA 修饰和核质转运在植物的抗冷过程中也具有重要作用.在不依赖于C BF 的途径中,转录因子H OS9和H OS10在调节抗冷有关基因的表达和提高抗冷能力方面具有至关重要的作用.关键词　植物;冷驯化;C BF ΠDRE B ;转录因子中图分类号　Q78Cold Acclimation of H igher PlantsXI A Jin 2Chan ,L ΒQiang ,G UO Mei 2Fang ,HE Y i 2K un3(College o f Life Sciences ,Captal Normal University ,Beijing 100037,China )Abstract C old acclimation ,including cool acclimation and freezing acclimation ,is a process through which certain plants increase their freezing tolerance after being exposed to chilling tem perature.Plant cells can sensecold stress at the cell membrane ,then increase cytos olic Ca 2+and trigger the expression of CB F s during cold acclimation.Many of the C BF genes have been identified and is olated.They participate in a com plex regulatory netw ork ,am ong which the ICE12C BF 2C OR takes an im portant role in the signal transduction regulatory processes.ICE 1encodes a MYC 2type basic helix 2loop 2helix transcription factor and is able to activate the expression of C BFs and other regulon by binding to MYC cis 2element to its prom oter upon cold stress.Protein ubiquitination in cold stress response is als o known to regulate the expression of C BF upstream regulon.Ubiquitinated ICE1by H OS1is targeted for proteos omal degradation.H OS9and H OS10play im portant roles in the regulation of cold 2responsive genes by a C BF 2independent pathway.The expression levels of C BFs are self 2regulated for their optimized transcription.M oreover ,genetic analyses have revealed that the RNA processing and the nucleocytoplasmic transport of C BFs played crucial roles in the responses of plants to cold stress.K ey w ords plant ;cold acclimation ;C BF ΠDRE B ;transcription factor收稿日期:2007209218;接受日期:2007212212国家自然科学基金资助(NO.30328003)和北京市教委科技发展计划面上项目(N o.2007C B948200)3联系人　T el :010*********;E 2mail :yhe @Received :September 18,2007;Accepted :December 12,2007Supported by National Natural Science F oundation of China (N o.30328003)and G eneral Program for Science and T echnology C ommission F oundation of Beijing (N o.2007C B948200)3C orresponding author T el :010*********;E 2mail :yhe @ 低温是植物经常遭受的一种逆境胁迫.它限制作物的产量,影响植物的自然分布.剖析植物对低温的应答机制、提高其抗低温能力在农业生产上有重要意义.为了适应和抵抗低温胁迫,植物在长期进化过程中形成了“冷驯化”(cold acclimation )应答保护机制:植物经过非致死温度的处理可以获得更强的抗冷能力叫做冷驯化.冷驯化又可细分为寒驯化(cold acclimation ,喜温植物在中度低温10～12℃环境中的冷驯化)和冻驯化(freezing acclimation,植物在0℃以上环境中的冷驯化).目前,通过各种筛选和克隆的方法已得到一系列与冷驯化信号途径相关的基因.例如:CB F,COR,KIN,L TI或RD基因.对这些基因的分离和功能分析为我们绘出了植物冷驯化信号通路的大致轮廓.1　第二信使C a2+在脱落酸(abscisic acid,ABA)非依赖冷驯化信号传导过程中,细胞首先通过膜的流动性和蛋白构象的变化感受冷信号,并且激活Ca2+通道,诱导胞质Ca2+的瞬时增加,上调冷驯化信号途径中CB F和COR基因的表达[1,2].拟南芥中与冷、ABA信号有关的fry1基因编码多磷酸肌醇12磷酸,可使1,4,52三磷酸肌醇(IP3)脱磷酸,负调控细胞中IP3的水平.在冷或ABA胁迫下fry1突变体中积累较多的IP3,并且持续保持较高水平的IP3含量,因此比野生型中更加强烈地诱导COR基因(RD29A,KIN1, COR15A,COR47A和ADH)的表达,而野生型中IP3含量的升高是瞬间的[3].hos2突变体是由FRY1蛋白的单个氨基酸被置换所生成的,在冷胁迫下突变体中COR基因的表达显著高于野生型,而对ABA 没有反应[4].而且,拟南芥的Cax1(calcium exchanger 1)突变体的液泡上缺少Ca2+ΠH+反向运输,从而导致CB F和COR基因的高表达提高抗冷能力[5].这些结果暗示,在冷信号传导过程中,IP3作为重要的信号分子介导细胞内钙库储存的Ca2+释放到胞质,从而调控CB F和COR基因的表达.冷驯化可以诱导ROS(例如H2O2)的产生.ROS 可能影响Ca2+信号,激活有丝分裂原激活的蛋白激酶(M APK)和氧化反应转录因子.FRO1基因编码线粒体中电子传递链复合物1(NADH脱氢酶)的Fe2S 亚单位(非生物胁迫下一个可能的ROS的产生位点).因此,fro1突变体中累积了较多的ROS,在没有冷的胁迫下fro1突变体中高水平的ROS激活Ca2+信号,使细胞对冷诱导的钙信号不敏感,导致COR 基因的下调,降低冷驯化[6].在ABA依赖的冷驯化信号传导过程中,ABA作为第二信使传导冷信号在los5突变体中部分的得到证明.在冷处理下,los5 (ABA合成缺陷)降低了COR基因的诱导表达水平,所以不能抵抗低温[7].植物冷驯化的信号传导网络如Fig.1所示[8].T able1　Abbreviations of genes related to cold acclim ation and othersAbbreviationsG enes related to cold acclimationAZF2Arabidopsis zinc2finger2CB F s C2repeat(CRT)2binding factorsCOR C old2regulatedDRE B Dehydration2response element2bindingES K1ESKI M O1FRY FIERY,inositol polyphosphate12phosphatase FRO1FROST BITE1H OS High expression of osm otically responsive genes ICE1Inducer of C BF expression1IP3Inositol21,4,52triphosphateKIN C old2inducedLTI Low2temperature2inducedLOS Low expression of osm otically responsive genes MAPK Mitogene2activated protein kinaseRD Responsive to dehydrationSTZ Salt2tolerance zinc fingerSCOF1S oybean cold2inducible zinc finger proteinSG B F1S oybean G2Box2binding factor1OthersABA Abscisic acidbZIP Basic2leucine zipperbH LH Basic helix2loop2helixC2H2Cysteine22and histidine22EP2A cis2element originally identified in52enolpyruvylshikimate232phosphate synthase geneprom oterMYB MyeloblastosisMYC Myelocytomatosis2　CBF调控的信号通路与表达的自我调控研究发现,冷驯化过程同时涉及依赖ABA和非依赖ABA的信号传导过程[9～11],但依赖ABA的具体调控机制尚未阐明.在非依赖ABA的信号转导途径中,C BFΠDRE B脱水响应元件结合因子类基因是近年来植物冷驯化研究方面的突破性进展.该类基因受冷的诱导表达,属AP2/ERE BP转录因子家族,有保守的AP2ΠERE BP结构域[12,13],该结构域由约58个氨基酸组成,能与DREΠCRT DNA调节元件相互作用,调节启动子区域含该顺式作用元件的基因的表达,主要在低温和短日照下启动表达,使细胞表现出抗冷能力[14,15].超表达CB F1和CB F3能强烈诱导COR基因表达,提高植物对冷胁迫的耐受能力.ICE1基因编码1个MY B类型的碱性螺旋2环2螺旋(bH LH)转录因子,为组成性表达并定位在核692中国生物化学与分子生物学报24卷内,受冷刺激后表达稍有增强.在冷胁迫下,它与CB F3启动子区的MY C顺式作用元件结合激活CB F3基因的表达.拟南芥ice1突变体抑制CB F3基因的表达,进而降低许多CB F目的基因的表达,削弱了植物的寒冷耐受和冷驯化的能力.过量表达ICE1基因能提高CB F和COR基因的表达及对冷的抵抗能力.ICE1需要经过冷诱导的构型变化(可能是通过磷酸化和去磷酸化作用)调节活性从而激活下游基因的表达[16].ice1突变体的ICE1多肽链第236位的精氨酸被组氨酸替代,可能会影响附近243和245位的丝氨酸(潜在的磷酸化和去磷酸位点)磷酸化和去磷酸,从而影响与CB F3启动子区域的MY C 顺式作用元件结合,致使靶基因(CB F3)表达 量下降[16].最近,发现1个R2R3类型的MY B转录因子能与ICE1相互作用,在冷胁迫下负调控CB F 基因的表达[17].另外,通过对CB F2启动子突变体的分析鉴定了2个作用于冷驯化调节CB F2表达的片段(ICEr1和ICEr2)[18],这些证明或许有类似ICE1的bH LH转录因子或者是MY B转录因子调节CB F 基因的表达[18,19],这些转录因子间或许相互作用.拟南芥中的HOS1基因编码1个915个氨基酸的蛋白,在N末端有一段很短的序列与动物中I AP (inhibitor of apoptosis)中所含有的RI NG(really interesting new gene)2finger domain相似.体外泛素化研究证明,H OS1是1个有功能的RI NG2finger蛋白,具有泛素E3连接酶的活性,催化特定的信号蛋白水Fig.1　Schem atic illustration of regulatory netw ork involved in cold acclim ation in plant[8]C old2stress activates the ICE protein,which triggers the expression of CB F s,and in turn induces expression of down2steam genes.H OS1negatively regulates ICE1by proteos omal degradation,C BFs als o self regulate their transcription to optimize their expression levels.RNA processing and nucleocytoplasmic transport play crucial roles in plant responses to cold stress.H OS9and H OS10regulons negatively regulate C BF2target genes by aC BF2independent pathwayD otted line(→)indicate possible regulation;Arrow( ),active or induction of expression;Line ending with cross line(),repression 792第4期夏金婵等:植物冷驯化相关信号机制　解.在hos1缺失突变体中CB F基因过量表达,说明H OS1可能是CB F基因上游的负调解物.H OS1与ICE1相互作用证明,H OS1通过催化ICE1蛋白的水解来负调节ICE1靶基因的表达[20].在冷的胁迫下泛素化或许也调节蛋白的合成.拟南芥中1个受冷热上调的F2box蛋白AtF BP7(At1g21760)是温度胁迫下蛋白合成所必需的[21].但其作用机制还不太清楚.在ICE12C BF2C OR途径中,除了未知的受体、Ca2+、IP3等,Ca2+受体、Ca2+依赖的蛋白激酶和有丝分裂原蛋白激酶(例如:M APKK2、M APK4和M APK6)级联反应也参与其中[22～24].冷驯化通过上调和下调许多基因的表达调整植物的生长代谢[25].因此,通过反馈抑制保持恰当的冷诱导蛋白水平是必须的.1个C2H2锌指结构蛋白和1个双链的RNA结合蛋白已被证明是冷信号传导途径中的负调控因子.在拟南芥中受冷、ABA、干旱和盐胁迫诱导的C2H2锌指蛋白AZF2和盐耐受锌指蛋白Z AT10(STZ)的启动子区含有DRE、MY B和MY C识别位点[26].所以,这些基因的表达受到与这些顺式作用元件结合的转录因子的调控.CB F3的超表达能增强ZAT10(STZ)的表达[27].相反,在ice1突变体中,CB F3的缺失降低了A ZF2和ZAT10 (STZ)的表达[16],所以,ICE1诱导CB F3的表达或许可能通过DRE顺式作用元件正调控A ZF2和ZAT10(STZ)的表达.ZAT10(STZ)基因的诱导在los2突变体中是强烈持久的,而在野生型中是快速瞬时的,因此,LOS2是ZAT10(STZ)的负调节因子[28].另外,Z AT10(STZ)可以通过与RD29A启动子区-554到-522的STZ识别位点(ACT AG TG AN13TCT AG T AAG)结合抑制RD29A的表达[28].所以,los2突变体中COR基因的表达受到调控.凝胶移位分析表明,AZF2和Z AT10(STZ)能与EP2序列(与负调节因子结合的顺式作用元件)中的A(GΠC)T顺式作用元件特异结合.因此,对含有EP2序列的基因表达起抑制作用.超表达CB F的转基因植株中诱导STZ的高表达,STZ抑制一些参与光合和碳代谢的基因,抑制转基因植物的生长[26].CB F 诱导的锌指蛋白可反馈抑制C BF的表达[29].另外, fry2突变体对冷超敏感,在冷和ABA的处理下,强烈诱导CB F和COR基因的表达,这说明FRY2也是CB F和COR基因的负调控因子[30].基因分析证明, FRY2RNA聚合酶Ⅱ的C端磷酸酶是通过RNA聚合酶Ⅱ的去磷酸化控制转录和mRNA的延伸,从而调控COR基因的表达[30,31].但是,fry2突变体对冷的敏感性说明FRY2或许正调控抗冷性的某些基因.锌指蛋白Z AT12编码1个转录抑制因子,它的超表达能够阻遏冷诱导CB F基因的表达,对CB F冷驯化途径起负调控作用[32].在冷信号传导过程中,C BF蛋白的自身反馈调节也具有重要的作用.拟南芥los1突变体缺失转录延伸因子2,影响蛋白的合成,不能通过C BF蛋白抑制CB F基因的表达.因此,在冷的胁迫下强烈诱导CB F基因的表达,而低水平的诱导COR基因的表达[33].与野生型相比,CB F2突变体中CB F1和CB F3的表达量升高,表现出更强的冷冻抵抗能力,说明CB F2蛋白在冷驯化过程中调节CB F1和CB F3的表达[34].而CB F2的表达水平可能通过CB F3来调节,因为在ice1突变体中,CB F3的表达受到抑制的同时,CB F2的表达升高[16].但对CB F 基因在自身相互调节和在冷驯化中的作用仍需要进一步分析研究.拟南芥sfr6(sensitive to freezing6)突变体在低温条件下,CB F1、CB F2、CB F3表达水平与野生型相比并未下降,而下游靶基因COR的表达却显著减少,推测SFR6可能调控C BF蛋白对COR基因的转录激活能力或COR基因转录后调节[35].利用A ffymetrix拟南芥24K芯片发现,在受冷诱导的514个基因中,302个基因上调,212个下调[29,36].在CB F2超表达植株中,85个基因上调,8个基因下调.所以,除了C BF外,还有其他的转录因子在冷驯化过程中起作用.但是,在25个显著上调的基因中,21个是受CB F2异位表达调控的,而且, Z AT12调节因子比C BF转录因子调控的基因少得多.这些结果表明,冷诱导大量基因的表达,其中CB F信号转导途径起着重要的作用.对去春化的基因表达研究发现,212个基因上调,320个基因下调,因此在冷驯化中,主要是诱导基因上调,而不是下调[37].值得注意的是,冷胁迫还可以诱导2个AP2类蛋白RAP211和RAP216的表达[12],RAP211的启动子区含有CRTΠDRE元件,所以,CB F的异位表达强烈诱导RAP211的表达,可能是C BF转录因子的靶基因[36].3　不依赖于CBF的调节因子在依赖ABA的信号传导途径中,调节基因表达的转录因子属于bZIP(ABRE结合因子或ARE B)、MY C或MY B家族.在拟南芥中克隆了1个受冷和ABA诱导的bZIP基因,其下游基因还不清楚,但是892中国生物化学与分子生物学报24卷发现了一个激活bZIP转录因子的C2H2类型的锌指蛋白,通过ABRE元件调节COR基因的表达.在拟南芥中过表达大豆中的1个冷诱导的锌指蛋白SC OF1能够诱导COR基因的表达,提高抗冷性.大豆中的1个冷诱导的bZIP转录因子SG BF1(G2box 结合因子),在冷驯化中依赖ABA诱导COR基因的表达.S OCF1能提高SG BF1的DNA结合活性[38].最近,在拟南芥中通过正向遗传学鉴定了2个转录因子H OS9和H OS10,参与抗冷过程[39,40].HOS9和HOS10分别编码1个推测的同源转录因子和R2R3类型的MY B类转录因子,转录不受冷的诱导,基因的缺失突变体降低本底和获得性的抗冷能力.与野生型相比,在hos9和hos10突变体中,尽管CB F的表达没有改变,但是对冷的胁迫敏感,因此,HOS9和HOS10在调节冷驯化的过程中是不依赖于CB F 的,并起重要的作用[39].1个未知功能的蛋白ESK1的突变导致对冷的抵抗,但影响的基因与C BF转录因子不同[41].同样,转录调节因子ADA2的突变也增强抗冷能力,但不是COR基因的变化所引起的[42].4　RNA的修饰和核质转运在冷胁迫中的重要作用 在冷驯化过程中,基因的诱导和组成性表达的转录都需要加工、运输到细胞质保持一种适合翻译的构型.RNA可被折叠成二级结构从而影响它的功能.低温加剧了这种干扰.在细菌中,与核酸结合的冷激蛋白(CSP)在低温的条件下积累,作为一种转录增强子降低RNA二级结构的稳定性,并且抑制转录的终止[43].在冷的胁迫下植物中一些含有CSP结构域的蛋白上调,也可能是作为RNA伴侣调节翻译[44,45].RZ21a是拟南芥中的一个锌指结构、甘氨酸含量丰富的RNA结合蛋白,在冷的胁迫下上调.基因分析证明它在抗冷方面具有作用[46].另外一类RNA伴侣,RNA解旋酶,也参与RNA 的代谢.在蓝细菌中,参与冷胁迫过程的一个DE AD2 box RNA解旋酶可能通过5′非翻译区伸展RNA的二级结构[47].在植物中有一大类DE AD2box RNA解旋酶.在拟南芥中其中的一个DE AD2box RNA解旋酶LOS4在植物的抗冷反应中起重要的作用[48],参与RNA有效的从核转运到胞质[49].拟南芥中的核蛋白AtNUP160(Arabidopsis nucleoporin)控制RNA的运输,在抗冷过程中是至关重要的[50].因为los4和atnup160突变体没有生长和发育上的缺陷,在其他非生物胁迫下也没有明显的变化,所以LOS4和AtNUP160蛋白只有在冷的胁迫下才会影响RNA的核质转运.有趣的是两个突变体中都影响C BF基因的表达.5　研究展望对植物冷驯化过程的研究已经成为目前科学研究的热门领域.植物细胞或许通过膜的流动性或结构的变化感受冷信号,但到目前为止具体的机制还不清晰;冷胁迫诱导过氧化氢的产生,过氧化氢通过M APK信号级联反应传递冷信号,可M APK信号途径如何与转录调节因子发生作用,调节冷诱导基因的表达还不知道;在C BF不依赖的信号途径中,一个未知功能的蛋白ESK1的突变导致对冷的抵抗,但是影响的基因与C BF转录因子不同,同样,转录调节因子ADA2的突变也增强抗冷能力,但不是COR基因的变化,2个转录因子H OS9和H OS10也参与植物的抗冷反应,他们的上下游基因都还不是十分清楚,这些都还需要进一步的研究.另一方面通过转化冷驯化过程中的关键基因,在很大程度上改善了植物的抗冷能力.但是植物对冷的耐受能力是有微效多基因控制的数量性状[51],单个基因的转入根本不能全面提高植物的抗冷能力.因此通过正向和反向遗传学的方法和生物化学的方法、或许建立和应用一种全新的研究方法研究冷驯化的精细网络信号转导过程迫在眉睫,从而利用相应的基因改良作物的抗冷能力.参考文献(R eferences)[1]　Orvar B L,Sangwan V,Omann F,et al.Early steps in cold sensingby plant cells:the role of actin cytoskeleton and membrane fluidity[J].Plant J,2000,23(6):7852794[2]　Sangwan V,F oulds I,S ingh J,et al.C old2activation of Brassicanapus BN115prom oter is mediated by structural changes 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