SBP-box/SPL基因在植物表皮毛发育中的作用

汪 斌, 林格格, 宋海冰, 陈壬杰, 兰 涛

(1.福建农林大学作物遗传育种与综合利用省部共建教育部重点实验室;2.福建农林大学生命科学学院;3.福建农林大学,福建省作物设计育种重点实验室,福建 福州 350002)

SBP-box/SPL基因在植物表皮毛发育中的作用

汪 斌1,2, 林格格1,3, 宋海冰1,3, 陈壬杰1,3, 兰 涛1,3

(1.福建农林大学作物遗传育种与综合利用省部共建教育部重点实验室;2.福建农林大学生命科学学院;3.福建农林大学,福建省作物设计育种重点实验室,福建 福州 350002)

植物表皮毛作为表皮细胞的特有组织在分类、减少热量和水分散失、抵御昆虫和微生物侵害方面发挥作用，同时也是生长发育时相转换的一个重要指标.而且表皮毛在提高产量等农艺性状方面也发挥重要作用，如棉花纤维组织的产量和品质.SBP-box/SPL基因是植物特有的一个较小的基因家族，在生长发育多个方面扮演重要角色，涉及花期、育性、果实成熟、蓝光信号传导、器官大小等性状.其中，在调控植物“年龄”相关的时相转换中作用明显.本文对表皮毛发育调控中SPL基因功能、涉及的microRNA，及它们与其他表皮毛发育调控途径的关系进行综述，以期为植物表皮毛发育的深入研究及应用奠定基础.

植物表皮毛; SBP-box/SPL基因; microRNA; 发育调控

植物表皮毛(trichome)是大多数植物地上组织的表皮细胞向外延生的发状结构，由单细胞或多细胞构成，有些具有分支，有些则拥有腺体.植物表皮毛的主要功能是增加表皮层厚度，减少热量和水分散失，保护植物免受昆虫和病原体侵害及某些机械损伤[1].有些植物表皮毛还是一种具有重要经济价值的农艺性状[2].植物表皮毛的形态发生与周围表皮细胞明显不同，因此是研究植物细胞分化调控的一种重要模式.植物表皮毛也是植物生长发育的一个重要标记，尤其是研究植物发育时相转换的一个有力工具[3～5].SBP-box/SPL(SQUAMOSA promoter binding protein-like)基因家族是植物特有的一个较小的转录因子家族，最初在研究植物生殖发育时发现.现有研究表明其在植物花期、育性、果实成熟、器官大小和表皮毛发育等方面扮演重要角色[6～9].本文对SBP-box/SPL基因在植物表皮毛发育中的作用及其与相关miRNA的互作机制进行综述，希望为植物细胞分化调控和植物发育时相转换研究提供参考.

1 植物表皮毛发育的分子基础概述

目前，双子叶模式植物拟南芥表皮毛发育的分子基础已有较多报道，其受多个转录因子调控.其中，表皮毛起始的正调控基因已有较为详细的研究，包括GLABRA1(GL1)[10]、GLABRA2(GL2)[11]、GLABRA3(GL3)、ENHANCEROFGLABRA3(EGL3)[12]和TRANSPARENTTESTAGLABRA1(TTG1)[13].GL1、GL3/EGL3和TTG1是正调控蛋白，形成一个MYB-bHLH-WD40(MBW)三蛋白复合体激活子，诱导下游基因GL2的表达[14].TTG2是TTG1和GL1的下游基因，在控制表皮毛生长中与GL2功能相似[15].表皮毛发育调控中第一个被鉴定的负调节因子是TRIPTYCHON (TRY)[16]，MYB转录因子TRICHOMELESS1(TCL1)和TCL2在表皮毛发育中也起负调节作用，而且TRY、TCL1和TCL2受MBW蛋白复合体诱导表达，产物进入邻近细胞从而抑制周围细胞表皮毛起始[4,9].另外，AtMYC1是bHLH转录因子的IIIf亚家族成员，也是表皮毛起始的一个重要调节因子[12].SPL基因在microRNA的调控下调控表皮毛的起始与分布，表现出与“年龄”相关的表型特征[3,4]，后面第3部分对其进行详细介绍.最近发现植物特有的RAV家族的两个转录因子TEM1和TEM2在表皮毛起始中起负调控作用，而且其作用的组织部位也涉及表皮层下面的叶肉层[17].表皮毛起始也受非转录因子调控，β类输入蛋白SAD2通过影响GL3的功能从而调控表皮毛起始[18]，胞质类受体激酶AtRLCK VI_A3和26S蛋白酶体亚基RPN1a也通过各自途径影响表皮毛分支[19,20].另外，番茄表皮毛形成的调控模式不同于拟南芥，其中Wo基因起关键作用[21].

植物激素在表皮毛发育中起重要作用.赤霉素生物合成和信号转导途径中GAL-3、SPY、RGA和GAI等基因在表皮毛起始和形成中起正向或负向调控作用[22～24].茉莉酸途径中JAZ(jasmonate-ZIM-domain)蛋白通过与MBW蛋白复合体互作，调节表皮毛起始[25].细胞分裂素在表皮毛发育中起正向调节作用[26]，通过诱导GL1、MYB23、GL3和EGL3基因表达从而参与表皮毛发育调控，生殖生长期花序茎表皮毛形成有关的C2H2类型锌指蛋白基因GIS2、ZFP5、ZFP8和ZFP6表达也受细胞分裂素影响[27,28]，其中GIS和GIS2是GIS3的直接靶基因[29].赤霉素和茉莉酸协同调节表皮毛形成[30]，赤霉素和细胞分裂素在表皮毛发育中表现为调节正相关[28]，而茉莉酸和水杨酸在调节表皮毛发育方面表现出某种拮抗现象[31].

2 SBP-box/SPL基因简述

SQUAMOSA是金鱼草(Antirrhinummajus)的一个MADS-box基因，编码转录因子，调控花的早期发育[32].SQUAMOSA-pROMOTER BINDING PROTEIN(SBP1)和SBP2蛋白可以和SQUAMOSA基因的启动子相互作用，推测是调控SQUAMOSA基因表达的转录因子，二者具有高度相似的SBP-box结构域[33].SPL基因是SBP类似基因，推测它们编码转录因子，且为植物所特有[34,35].SPL基因家族不大，大多数植物基因组中只有十几个成员，如苔藓(Physcomitrellapatens)[36]、番茄(Solanumlycopersicum)[37]、扇叶文心兰(Erycinapusilla)[38]、丹参(Salviamiltiorrhiza)[39]、拟南芥(Arabidopsisthaliana)[40]、葡萄(Vitisvinifera)[41]和水稻(Oryzasativa)[6]分别有13～19个成员不等；而杨树(Populustrichocarpa)[42]、陆地棉(Gossypiumhirsutum)[43]和玉米(Zeamays)[44]则分别有27～31个家族成员.在同一物种中，SPL家族成员的基因结构表现出多样化，但SBP-box结构域是保守的[35].

如其他转录因子一样，SPL基因在植物发育调控中扮演重要角色，性状涉及花期[34]、育性[3]、叶边缘锯齿状缺刻[43]、果实成熟[45,46]、蓝光信号[36]、成年态建立[47]、叶时(plastochron)、器官大小[8]、花青素合成[48]、穗发育[7]、理想株型[49]、谷粒尺寸[50]和颖片结构[51]等.其中，SPL基因在植物表皮毛发育调控中作用明显[8,9].SPL基因是miR156的唯一靶标，拟南芥和水稻都有11个SPL基因受miR156调控[5,6]；扇叶文心兰[38]、杨树[42]和陆地棉[43]有9～18个SPL基因转录物含有miR156结合位点；而番茄[37]、葡萄[41]和丹参[39]有8～12个成员是miR156/157的可能靶标.因此，SPL基因在表皮毛发育调控中直接或间接受到microRNA(miRNA)的影响.

3 SBP-box/SPL基因在植物表皮毛发育中的作用

植物表皮毛发育调控与地上部发育息息相关，从营养生长期到生殖生长期，随着“年龄”增长，地上部不断成熟，表皮毛的空间分布特征则相应改变.以拟南芥为例，在营养生长期，幼嫩叶仅在近轴面有表皮毛，而成熟叶在近轴面和远轴面皆有表皮毛.而在生殖生长期，茎、茎生叶及生殖器官上表皮毛的分布特征又表现出逐渐减少、甚至光滑的特点.因此，表皮毛空间分布特征经常作为植物地上部处于何种发育阶段的标志[46].与“年龄”有关的植物地上部表皮毛发育调控途径中，SBP-box/SPL基因扮演重要角色.而SPL基因的时空表达丰度则受到丰度与“年龄”有关的miRNA调控[4,8].有些SPL基因还会对miRNA表达进行反馈调节[5]，最终实现对表皮毛发育调控.关于SPL基因参与表皮毛发育的研究，目前绝大部分报道集中在双子叶模式植物拟南芥上.

3.1 非miRNA靶标基因SPL8对植物表皮毛发育的影响

拟南芥SPL8是被发现参与表皮毛生长调控的第一个SPL基因.spl8突变体花序顶端萼片远轴面表皮毛数目少于野生型，无论第一朵花还是第十朵花皆如此[3].SPL8过量表达导致萼片远轴面表皮毛密度和复杂性(星形的)明显提高，表型与spl8突变体正好相反.野生型、SPL8过量表达植株和spl8突变体中GA合成和响应标记基因GA5和γ-TIP的转录水平有所改变[52].已知表皮毛生长和发育受GA调控[26]，在生殖生长期，SPL8可能通过依赖GA途径影响表皮毛发育(图1).

图1 miRNA-SPL在表皮毛发育调控途径中的作用模式图

拟南芥中11个SPL基因受miR156调控，SPL8不是miR156靶标基因.35S∶MIR156b转基因植株萼片远轴面具有表皮毛，然而spl8和35S∶MIR156b双突变体，其萼片远轴面几乎没有表皮毛，反而在近轴面出现表皮毛[53]，同时在子房上部内表皮处发现表皮毛[54].显然，在生殖生长期一些miR156的靶标SPL基因与SPL8在调控表皮毛发育方面有功能冗余.

3.2 miR156靶标基因SPL对植物表皮毛发育的调控

拟南芥表皮毛起始和分布具有时间和空间特异性[4]，其中miR156及其靶标SPL基因在调控网络中扮演重要角色.从营养生长期到生殖生长期，miR156表达水平逐渐降低，其靶标SPL基因的表达水平则逐渐升高[8].同一物种中SPL家族成员的SBP-box结构域是高度保守的，但SBP-box结构域以外部分的基因序列变化较大[35].根据这些靶标SPL基因的序列相似性及其在表皮毛发育调控中的功能特征，将它们分为以下几组.

3.2.1SPL3、SPL4和SPL5 拟南芥SPL3、SPL4和SPL5是SPL基因家族中关系相近的三个成员，它们的3′UTR都有miR156的靶标位点[53,55].在营养生长期，35S∷SPL3植株表皮毛发育模式与野生型无异[55]，而35S∷rSPL3(miR156不敏感型SPL3)植株远轴面表皮毛出现提早了1.5个叶片[8].35S∷MIR156A植株在持续光照条件下，无远轴面表皮毛叶片显著增多，而35S∷MIR156A和35S∷rSPL3双转基因植株无远轴面表皮毛叶片显著少于35S∷MIR156A植株[55].可见在营养生长期，拟南芥随着SPL3表达量增加，逐渐产生有远轴面表皮毛叶片，在生殖生长期，随着SPL3转录物的增加，主茎和花器官上表皮毛数目逐渐降低[4].而SPL3转录物丰度取决于miR156的表达量(图1).SPL4和SPL5与SPL3在调控表皮毛发育方面功能冗余[55].

3.2.2SPL9和SPL15 拟南芥SPL9和SPL15是横向同源基因.在营养生长期，与野生型相比，spl9和spl15单突变体和双突变体皆推迟出现第一片有远轴面表皮毛叶片，双突变体更为明显.可见，SPL15和SPL9功能冗余，且SPL15弱于SPL9[8,47].pSPL9∷rSPL9(miR156不敏感型SPL9)加速了有远轴面表皮毛叶片出现[8]，SPL15突变体msc1(miR156不敏感型)也加速了从幼年期向成熟期转换[56].可见，SPL9和SPL15对表皮毛发育调控也受miR156影响.与SPL8不同，在营养生长期SPL9和SPL15对表皮毛发育调控不依赖赤霉素途径[47].

在生殖生长期，单重复R3 MYB转录因子TRICHOMELESS1(TCL1)和TRIPTYCHON(TRY)是表皮毛发育负调节因子，SPL9通过结合到TCL1和TRY启动子上直接激活它们表达，从而导致主茎和花序上表皮毛逐渐减少，花器官甚至是光滑的[4].另一个单重复R3 MYB转录因子TCL2和TCL1在控制花序表皮毛形成上功能冗余，但不完全等价，而且TCL2转录也受SPL9诱导.TCL1和TCL2通过抑制GL1表达从而抑制茎和花序上表皮毛形成[9].细胞分裂素和赤霉素调控C2H2型转录因子GIS、GIS2和ZFP8，这些转录因子促进GL1表达，最终诱导茎和花序上表皮毛形成[4].而且，该GIS途径没有影响SPL9对TCL1和TRY的调控.因此，miR156调控SPL9基因在发育进程与表皮毛分布上建立了一个直接联系[4]，这一点与营养生长期相似[47].

在生殖生长期，SPL15依然与SPL9功能冗余，在miR156调控下一起影响表皮毛发育.此外，在sk156突变体(MIR156B过量表达)中过量表达rSPL15(miR156不敏感型SPL15)导致MIR156B转录水平大量降低，而且在MIR156B转录起始位点附近有多个SPL结合核心序列GTAC，说明SPL15对MIR156B表达也许存在反馈调节[5](图1).

3.2.3SPL10、SPL11和SPL2 拟南芥SPL10、SPL11和SPL2是SBP-box基因家族中关系相近成员，序列和表达都比较相似.在营养生长期，spl10、spl11和spl2单突变体，表皮毛分布与野生型无异，猜测它们之间存在功能冗余[46].pSPL10∷rSPL10/11(miR156不敏感型SPL10/11)加速叶片远轴面表皮毛出现[8]，可见它们调节表皮毛发育时也受miR156控制.拟南芥内生开花途径研究表明FRUITFULL(FUL)是SPL的直接下游靶基因[57,58].ful突变体拥有更多无远轴面表皮毛叶片，35S∷mSPL10/11/2转基因植株叶片FUL表达量明显高于野生型[46].因此，SPL10/11/2也许通过FUL途径实现调控地上部表皮毛发育(图1).

在生殖生长期，抑制SPL10/11/2的表达，则茎生叶和花上出现许多表皮毛，虽然后续花上表皮毛数目逐渐减少，但时期迟于野生型.三个基因单突变体萼片表皮毛数目皆显著增加，spl10spl2和spl11spl2双突变体在茎生叶和花上也出现许多表皮毛，且效应强于单突变体，说明这三个基因在生殖生长期控制表皮毛发育的功能冗余[46].

3.3 SPL介导的miRNA互作在表皮毛发育中的作用

3.2部分在阐述SPL基因对表皮毛发育调控时不可避免地提到miR156/157，然而除miR156/157之外，miR172和miR171在SPL调控表皮毛发育中也发挥重要作用.

miR156和miR172通过SPL产生互作或信号交叉，从而在表皮毛发育调控中扮演不同角色.在短日条件下，miR156过量表达拟南芥植株产生约90片缺少远轴面表皮毛叶片；反之，MIM156(miR156靶基因模拟)过量表达植株，其前两片莲座叶就已经有远轴面表皮毛.miR172过量表达植株产生有远轴面表皮毛叶片比正常植株早2个叶时，而MIR172B突变体则延迟了约3个叶时.因此，miR172对表皮毛发育调控与miR156正好相反.此外，通过MIR156、MIR172B、TOE1、TOE2(TOE1和TOE2是miR172的靶标)和SPL9单突变体、三突变体、过量表达和抑制表达分析，发现miR156抑制SPL9/10表达，而SPL9/10又促进MIR172B表达[8].可见，在表皮毛发育调控途径中，SPL9/10在miR156和miR172之间起承上启下作用.35S∶MIR172转基因植株第二(甚至第一)莲座叶远轴面出现表皮毛，同时SPL3/4/5转录水平显著提高，该调控是miR172通过其靶标基因在SPL3/4/5转录水平实现的[59].可见，在表皮毛发育调控途径中，SPL3/4/5在miR156和miR172之间仅扮演一个信号交叉点角色，不同于SPL9/10所起的承上启下作用(图2).马铃薯表皮毛发育似乎也存在与拟南芥相似的miR156-SPL9-miR172调控模式[60]，而苜蓿中过量表达miR156增加了叶片表皮毛密度，但没有明确提出营养生长期和生殖生长期之间的差异，似乎与拟南芥调控模式有所不同[61].

miR156也与miR171发生互作，从而在表皮毛发育调控中发挥作用.GRAS家族成员LOSTMERISTEM1(LOM1)、LOM2和LOM3是miR171的靶标基因.miR171过量表达减少LOM丰度，导致茎和花器官上表皮毛密度降低；相反，组成型表达rLOM(miR171不敏感型LOM)则促进表皮毛产生，可见LOM在生殖生长期增强表皮毛起始.遗传分析显示LOM决定茎上表皮毛分布依赖于SPL途径.这样两个与时间有关的miRNA通过它们靶标的直接互作而实现拮抗，从而实现对植物生长、时相转换和形态发生进行调控[62].不难看出，miR171和miR156在调控表皮毛发育中通过SPL建立的互作关系与miR172通过SPL3/4/5与miR156建立的互作关系是相似的.此外miR171表达受其靶标LOM调节，形成一个自我平衡的反馈环[62](图2).同样的反馈调控也出现在miR156和其靶标SPL之间[5].

图2 营养生长期miR156、miR171和miR172对表皮毛发育调控途径模式图

HYPONASTIC LEAVES1(HYL1)是miRNA生物发生的一个重要调控因子.拟南芥hyl1突变体远轴面表皮毛提早出现，hyl135S∷MIR156A植株和hyl1spl9spl15植株都能完全或部分弥补hyl1突变体表皮毛发育缺陷，而且SPL9基因在hyl1突变体内过量表达导致其幼年期完全消失[63].可见，HYL1通过miR156-SPLs途径(主要是SPL9和SPL15)控制表皮毛发育，从而实现幼年期到成熟期的正常转换(图2).

4 结语

植物表皮毛是覆盖于植物组织表面、由表皮细胞层分化出的单细胞或多细胞毛状结构，其形态多样，经常作为植物分类的特征之一.不同植物的表皮毛功能相去甚远，涉及抗虫、抗病和抗逆等性状.随着分子生物学发展，表皮毛生长和发育研究深入到分子机理水平，发现了许多相关基因，其中包括SBP-box/SPL基因.SPL基因中多数是miRNA的靶标，预计随着SPL基因和miRNA互作研究的深入，表皮毛生长、发育及调控的分子机理会越来越清晰.然而除了双子叶模式植物拟南芥外，其它植物表皮毛发育调控也许存在不同机制.作者通过对单子叶模式植物水稻不同生长时期不同叶片上表皮毛的观察，没有发现与拟南芥相似的发育特征(未发表).Zheng等将水稻OsTCL1在拟南芥中异位表达，对表皮毛影响与拟南芥TCL1的效果相似，但在水稻中异位表达却没有类似效应[64].可见水稻在表皮毛发育方面有不同的调控机制.随着对多种植物和相关基因的深入研究，植物表皮毛发育特征及调控机理将更加明晰，这些研究成果为植物发育的理论研究奠定基础，同时也为某些重要农艺性状(如植物纤维的产量和质量)的深入研究和合理利用提供帮助.

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(责任编辑:吴显达)

The role of SBP-box/SPLgenes in the formation and development of trichomes in plants

WANG Bin1,2, LIN Gege1,3, SONG Haibing1,3, CHEN Renjie1,3, LAN Tao1,3

(1.Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Agriculture and Forestry University; 2.College of Life Science, Fujian Agriculture and Forestry University; 3.Fujian Provincial Key Laboratory of Crop Breeding by Design, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China)

As a special tissue structure of epidermal cells, plant trichomes play crucial roles in plant classification, reduction of heat and moisture loss from plant leaves, plant resistances to insects, microorganisms and abiotic stresses. The trichomes are also important indicators for phase transition of plant growth and development and significantly influence crop important agronomic traits, such as yield and quality of cotton fiber. The SBP-box/SPLgenes belong to a relatively small and specific gene family in plants, and play important roles in several processes during plant growth and development, including flowering time, fertility, fruit ripping, blue light signal transduction, and organ size, especially in regulating phase transition during aging. In this paper, the function and mechanism ofSPLgenes in regulating trichomes development, including microRNA and their relationship with other pathways regulating trichomes development are summarized, which would afford supports in further study on plant trichomes development and application.

plant trichome; SBP-box/SPLgenes; microRNA; developmental regulation

2016-02-29

2016-07-28

国家自然科学基金(31671668);福建省自然科学基金(2015J01094);福建省教育厅科技计划项目(JK2012014).

汪斌(1966-),女,博士,副教授.研究方向:植物抗逆分子遗传.Email:wangbin_doc@163.com.通讯作者兰涛(1975-),男，博士,副教授.研究方向:作物逆境机理及改良.Email:tlan@fafu.edu.cn.

Q341;Q344+.4

A

1671-5470(2017)02-0121-08

10.13323/j.cnki.j.fafu(nat.sci.).2017.02.001