微管参与的植物激素信号转导研究进展

陈炳佑，刘广志，侍福梅

(聊城大学 生命科学学院，山东 聊城 252059)

微管参与的植物激素信号转导研究进展

陈炳佑，刘广志，侍福梅*

(聊城大学 生命科学学院，山东 聊城 252059)

微管骨架和植物激素都参与多个植物生长发育过程的调控和多种胁迫应答。以生长素、赤霉素、油菜素内酯和脱落酸为代表，综述了植物激素发挥生理功能的同时与微管骨架的交叉联系，以期寻找参与微管骨架和植物激素对话互作的关键分子及其共性，为进一步完善植物激素信号网络和微管骨架功能提供参考。

植物激素； 微管； 信号转导； 周质微管

微管(microtubule,MT)的基本组成单位是微管蛋白(tubulin)。其中，包括α微管蛋白和β微管蛋白。植物微管在漫长的进化过程中形成了4种不同的微管列阵形式，包括周质微管、早前期带、有丝分裂纺锤体和成膜体[1]。这些微管列阵调控细胞分裂和生长的方向。植物的周质微管列阵对于植物形态建成和生长发育十分重要[2]。周质微管列阵具有高度动态的组织特性，始终处于解聚和聚合的动态过程中，并在多种信号转导过程中发挥功能[3-5]，同时受到许多微管结合蛋白(microtubule-associated proteins，MAPs)的调控，其中植物的微管结合蛋白包括Csi1p(CSI1)、Spr2p(SPR2)、Microtubule-associated protein 70(MAP70)、WAVE-DAMPENED 2(WVD2/WDL)、Ribosome-inactivating protein(RIP/MIDD)、SPIRAL1(SPR1)、Microtubule-associated protein 18(MAP18/PCaP)、ENDOSPERM DEFECTIVE 1(EDE1)、renin 2 tandem duplication of Ren1(REN2) 和Centrosomal protein 190kD(MAP190) 等[2,6]。

植物激素和微管骨架共同参与植物生长发育和逆境胁迫应答过程。在生长素、赤霉素和油菜素内酯调节植物细胞伸长生长的过程中，微管骨架应答上游的信号转导发生周质列阵的重排[7-9]。脱落酸作为重要的植物抗逆激素，通过调节保卫细胞的微管动态变化，从而调控植物叶片的气孔开度，使植物更好地应对来自外界的逆境变化[10]。有研究表明，在以上植物激素信号通路中，微管骨架是其中重要的参与者[10]。综述了近年来微管骨架参与的植物激素信号转导研究成果，以期寻找参与微管骨架和植物激素对话互作的关键分子及共性，为进一步完善植物激素信号网络和微管骨架功能提供参考。

1 微管参与生长素的信号转导

吲哚乙酸(IAA)是生长素(AUX)的主要化学成分。植物生长和发育的幼嫩部位为AUX在植物中的主要分布位置，而在其他成熟的器官或衰老的器官中分布很少[11-12]。AUX主要调控植株的顶端优势、根的向地生长、器官的形态建成、维管组织的分化和细胞的伸长等生理活动[13-15]。由4个亚基(Skp1、Cdc53、F-box和RBX1)组成的SCF泛素连接酶复合体，是AUX信号转导途径的关键蛋白[16]。当植物体内的AUX含量减少时，转录因子ARF的活性被AUX和信号转运抑制因子TPL蛋白抑制。当植物体内AUX含量增加时，AUX和SCFTR1结合，使其泛素化后降解。此后，TPL蛋白脱离复合体，ARF转录因子恢复活性，整个信号通路重新畅通[17-18]。

微管和AUX共同参与植物遮光条件下的生长。植物在遮荫条件下，茎和叶柄会快速伸长[19]。AUX主要的功能是调控植物的生长。周质微管列阵的动态变化也影响细胞的定向伸长。研究发现，AUX通过调控周质微管列阵的排布而影响植物在遮荫条件下的生长。其机制：AUX在调控细胞定向伸长的过程中不仅将细胞壁软化，而且还通过周质微管影响纤维素的沉积方向，从而诱导植物细胞的生长。但AUX并非直接作用于周质微管，而是作用于微管调控蛋白，如ABP1、KATANIN 1以及一系列下游的原件如ROP6 GTPase和RIC1(ROP-interactive protein)等[20-24]。木葡聚糖内转糖苷酶(XTHs)也参与AUX在遮荫条件下调控周质微管列阵动态的变化。周质微管通过调节细胞壁修饰蛋白的表达，影响AUX的分布，而AUX调节XTHs的表达，进而影响周质微管列阵的排布，即AUX和周质微管通过XTHs和细胞壁修饰蛋白共同调节叶柄伸长的过程[19]。此外，在早前期带和成膜体中发现了AUX和其载体PIN2蛋白的积累，说明AUX参与调控这些过程[25]，但具体机制目前还不清楚。生长素反应因子ARF8也参与调控拟南芥下胚轴和雄蕊的伸长，模型为光→光受体→ARF8→AUX→下胚轴和雄蕊的生长，而这些过程中微管都参与，但目前缺乏其参与调控的直接证据[26]。

2 微管参与赤霉素的信号转导

赤霉素(GA)是一类环状的双萜类化合物的统称。GA促进植物从营养生长向生殖生长的过渡。GA还影响植物种子萌发、花粉成熟和茎的生长等生长发育过程[27-28]。GA的信号转导通路包括关键蛋白DELLA[29-30]， 还有GA受体GID1[31]、F-box型蛋白GID2和SLY1 等主要的组成部分[32-33]。植物体内没有GA时，DELLA蛋白结合调控植物生长的转录因子，抑制植物生长。当植物体内有GA时，GA受体GID1蛋白识别并结合GA，之后再结合DELLA蛋白形成复合体，特异的E3 连接酶复合物 SCFSLY1/GID2作用于复合物，使DELLA蛋白发生泛素化降解，解除靶基因的抑制，进一步促发植物的GA应答，表现促进生长作用。相反，没有GA时不发生后面的一系列反应，DELLA不能降解，植物生长发育受阻[34-38]。

微管和GA共同参与调节植物的胚轴生长和花器官的发育。GA显著诱导下胚轴轴向的伸长[8]。GA与在细胞核中的DELLA蛋白和前折叠素复合体相互作用调节微管走向[39]。在有GA的条件下，DELLA蛋白被分解，前折叠素复合体在细胞质中行使功能。在没有GA的条件下，前折叠素复合体则定位于细胞核中，并显著抑制α/β微管蛋白二聚体的活性，从而影响微管列阵的排布[40]。类激酶蛋白BC12/GDD1有转录因子活性，通过调控GA合成调节细胞伸长；微管免疫共沉淀试验进一步表明，在有ATP存在时，BC12/GDD1与微管结合， 表明GA信号和微管都位于BC12/GDD1的下游，存在潜在的互作关系[41]。向日葵的舌状花发育过程中，决定花大小的主要因素是细胞的体积而非细胞数目。而周质微管调控细胞的定向伸长和异向扩张[42]。研究发现，GA信号类似光信号，诱导舌状花细胞周质微管出现明显的垂直于伸长方向的列阵，进而促进了舌状花细胞的伸长生长，表明GA通过影响微管列阵调节舌状花细胞的生长过程[42-43]。另外，在非洲菊(Gerberahybrida)的舌状花的发育中也发现GA和光信号参与调控周质微管，影响细胞的伸长，当光和GA同时作用时舌状花既有纵向伸长又有横向扩展，而GA作用时只发生纵向伸长，不发生横向扩展，进一步研究发现在微管抑制剂氨璜乐灵(oryzalin)作用下细胞纵向伸长明显受到抑制，说明微管和GA共同参与调控非洲菊舌状花的伸长生长[44]。

3 微管参与油菜素内酯的信号转导

油菜素甾醇类化合物(BR)是一类甾醇类化合物的统称[45]。其中,油菜素内酯(BL)活性最强[46]。BR在植物的各个器官中都有分布，特别是在幼嫩的器官如芽、幼叶中含量较高[47-48]。BR参与多种植物生长发育的过程，如细胞的伸长[49]、种子萌发[50]、气孔的开闭[51]、植物抗逆性的提高[52]、植物育性的调节[53-54]以及光形态的建成[9,55]等。BR的信号转导过程中，受体激酶(BRI1)的作用十分关键[9]，其位于细胞膜的表面。当不存在BR时，BR负调控蛋白BKI1与其结合，无法启动下游反应。当存在BR时，BRI1感知并结合BR，启动下游反应，调控植株生长[56-57]。

微管和BR都参与调节胚轴细胞的伸长。MDP40是微管去稳定蛋白，正调节下胚轴细胞的伸长。BRI1是一个在BR信号通路中关键的转录因子，特异上调MDP40的表达。MDP40的表达使得BR缺失突变体de-etiolated-2幼苗下胚轴短的表型部分消除，更接近野生型的表型。然而，RNA干扰MDP40的转基因突变体的细胞周质微管对BR不敏感。表明在下胚轴生长过程中，MDP40是BR调控周质微管列阵的关键调节因子[58-59]。此外，最近的研究表明，BR还参与调控有丝分裂的终止，但是否与微管相互作用有待进一步研究[60]。

4 微管参与脱落酸的信号转导

脱落酸(ABA)是含有15个碳原子的倍半萜烯化合物，参与调节植物的抗逆性应答[61-62]和生长发育[63]。ABA信号转导研究过程中发现了许多ABA的受体，其中目前研究较为详细的2个受体是PYR/PYL/RCAR和ABAR/CHLH。在以PYR/PYL/RCAR为受体的ABA信号通路中，当植物体内ABA不存在时，由于ABA受体PYR/PYL/RCAR的存在形式为二聚体，不能与蛋白磷酸激酶PP2Cs结合，植物生长发育正常。相反，当植物体内存在ABA，ABA与PYR/PYL/RCAR结合，使其结合PP2Cs，进一步激活下游的信号流，抗逆基因表达[64-65]，植物表现抗逆性生长。在以ABAR/CHLH为受体的ABA信号通路中，ABAR/CHLH与ABA结合，转录因子WRKY40从细胞核中转移出来，影响其转录表达，解除ABI5、MYB2和ABI4等ABA下游因子的抑制，植物表现ABA应答[66]。

微管和ABA共同参与调控气孔的开闭。目前已知钙离子、细胞骨架和磷脂酸等参与调节气孔开度。磷脂酶衍生出来的磷脂酸与ABA信号通路中下游的磷酸酶ABI1结合，抑制其活性[67-69]。野生型拟南芥中ABA诱导微管解聚，气孔关闭，而磷脂酶突变体pldα1中这一过程被打断。对野生型和突变体pldα1施加微管破坏药物氨璜乐灵或者炔苯酰草胺(propyzamide)，导致二者微管都解聚但是不影响ABA诱导的气孔关闭。相反，对野生型和pldα1突变体施加微管稳定药物紫杉醇(paclitaxel) ，二者微管都解聚，并且抑制了ABA诱导的气孔关闭。在pldα1突变体中，ABA诱导的细胞质钙离子浓度升高被部分抑制，外源钙离子诱导的微管解聚和气孔关闭也被抑制，说明ABA信号通路中磷脂酶PLDα1和磷脂酸调节微管动态变化和钙离子浓度[10]。

5 微管参与其他植物激素及物质的信号转导

除上述激素之外，乙烯(ETH)具有促进果实成熟的作用。有研究表明其在表皮毛的发育过程中参与调控微管骨架，但是具体的分子机制尚未明确[70-71]。NO与周质微管存在互作，低浓度的NO2-Tyr处理下，发现在拟南芥根的伸长区微管呈现无序分布，并且伴随着细胞的非极性化扩张[72]。此外，NO参与调节植物的紫外胁迫应答和大丽轮枝菌诱导的微管重排[73-74]，这也进一步证明了NO和微管的相关性。

6 展望

生长素、赤霉素和油菜素内酯都有促进植物生长的作用，微管骨架都参与这些激素对植物的调节作用[19,39,58]。生长素通过生长素结合蛋白ABP1、KATANIN 1[20-21]、XTHs和细胞壁修饰蛋白[19]等作用于微管。赤霉素通过类激酶蛋白BC12/GDD1作用于微管[41]。油菜素内酯通过影响微管去稳定蛋白MDP40的表达作用于微管。下一步的研究重点将集中在继续寻找参与微管与植物激素互作的潜在蛋白，分析激素对该类蛋白活性和表达的影响，筛选出目标蛋白，构建靶蛋白的缺失及过表达突变体，进一步分析与激素的关系。

目前对脱落酸的研究主要集中在胁迫应答和气孔的开闭运动[67-69]，而脱落酸在低浓度下也有促进植物生长的作用[62]，与生长素、赤霉素和油菜素内酯的功能类似。聊城大学生命科学学院侍福梅实验室发现低浓度脱落酸与微管骨架在调节植物的生长发育中存在互作(待发表)。此外，除了气孔运动、种子萌发、根生长及胁迫应答之外的生长过程中，成熟和衰老器官中不涉及到细胞定向生长的生理活动中是否有微管骨架的参与有待进一步研究。

除了传统的植物激素外，一些其他的分子，如茉莉酮酸及其酯、水杨酸、独脚金内酯等[75-80]，在调控植物的生长发育等生理活动中也具有重要的作用，它们与微管骨架潜在的互作关联问题可以借鉴已知的研究线索展开调查，有望寻求突破。

随着遗传学和分子生物学的发展，大量模式植物突变体的构建也为研究激素与微管骨架之间的关系提供了良好的材料。对于微管骨架与植物激素的对话及潜在核心信号蛋白的研究有助于进一步完善植物激素的信号转导网络，进而为深入解析植物的生长发育调控提供参考。

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Progresses on Involvement of Microtubule in Plant Hormone Signal Transduction

CHEN Bingyou,LIU Guangzhi,SHI Fumei*

(School of Life Science,Liaocheng University,Liaocheng 252059,China)

Both microtubule and phytohormone are reported to involve many important growth and development regulation and kinds of stresses response in plants.Here we summarized the potential link between microtubules and vital hormones including auxin(AUX),gibberellin(GA),brassinosteroid(BR) and abscisic acid(ABA),so as to screen key components,especially the common characters,concerning microtubule functions as well as the hormone signal transduction,and further provide references for improving the hormones network and microtubule functions.

phytohormone; microtubule; signal transduction; cortical microtubule

2015-07-13

国家自然科学基金项目(31240035)；山东省自然科学基金项目 (ZR2010CQ002)

陈炳佑(1991-)，男，内蒙古包头人，在读硕士研究生，研究方向：细胞生物学。

*通讯作者：侍福梅(1978-)，女，辽宁沈阳人，副教授，博士，主要从事植物分子细胞生物学研究。 E-mail: shifumei@lcu.edu.cn

Q257

A

1004-3268(2016)02-0001-06