全 文 ：植物生理学报 Plant Physiology Journal 2013, 49 (9): 833~846 833
收稿 2013-05-07　　修定 2013-06-27
资助 转基因生物新品种培育重大专项(2011ZX08009-003-003)
和“十二五”农村领域国家科技计划(2012AA10A302-2)。
* 通讯作者(E-mail: zyshi@sippe.ac.cn; Tel: 021-54924078)。
高等植物特有的LBD基因的分子生物学功能研究进展
卢寰1,2, 时振英1,*
1中国科学院上海生命科学研究院植物生理生态研究所, 上海200032; 2中国科学院大学, 北京100039
摘要: LATERAL ORGAN BOUNDARIES DOMAIN (LBD)基因家族是在拟南芥中发现的高等植物所特有的一类基因, 编码的
蛋白中含有LATERAL ORGAN BOUNDARIES (LOB)结构域。LBD基因一般在侧生器官与茎尖分生组织的边界处、侧生
器官的近轴面一侧的基部表达, 并呈现出在多种组织内特异性表达的特征, 暗示该类基因可能在植物的多种发育过程中发
挥功能。LBD蛋白结构中除含有上述LOB结构域以外, 尚未发现其它已知功能的结构域的存在。目前, 已经在拟南芥中发
现43个LBD基因, 而在玉米和水稻中各有35和43个LBD基因。根据LBD蛋白结构中是否含有亮氨酸拉链类似基序, 将LBD
基因分为两类: 第一类(class I) LBD蛋白结构域中包含完整亮氨酸拉链基序; 第二类(class II) LBD蛋白结构域中不含亮氨酸
拉链基序。本文就LBD基因的结构以及它们对高等植物生长发育的影响、LBD基因和植物激素的关系、LBD基因与
miRNA的关系进行了系统的总结。
关键词: LBD基因; LOB结构域; 高等植物; 茎尖分生组织; 表达模式; 蛋白结构; 植物激素; miRNA
Research Progress on the Molecular Function of Plant-Specific LBD Gene
LU Huan1,2, SHI Zhen-Ying1,*
1Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai
200032, China; 2University of Chinese Academy of Sciences, Beijing 100039, China
Abstract: The LATERAL ORGAN BOUNDARIES DOMAIN (LBD) gene family, which was firstly discovered
in Arabidopsis thaliana, encodes a conserved higher plant-specific LATERAL ORGAN BOUNDARIES (LOB)
domain-containing protein. LBD gene is expressed in a band of cells between lateral organs and the shoot apical
meristem (SAM) or at the adaxial base of lateral organs formed from the SAM. The LBD genes show a variety
of tissue-specific expression patterns, suggesting that they may function in diverse developmental processes.
LBD protein doesn’t contain other recognizable functional motifs except for the LOB domain. Up to now, 43
members of the LBD gene family have been identified in Arabidopsis, whereas in rice (Oryza sativa) and maize
(Zea mays), there are 35 and 43 LBD genes respectively. LBD genes contain two major classes which are
characterized by the presence (class I) or absence (class II) of functional leucine-zipper-like motifs. In this
review, we described the structure of LBD proteins, and functions of them on plant development are discussed.
At the same time, the relationships among LBD genes, and those between LBD genes, plant hormones and
miRNA were clarified systematically.
Key words: LBD gene; LOB domain; higher plant; shoot apical meristem (SAM); expression pattern; protein
structure; miRNA; plant hormone
Lateral Organ Boundaries Domain gene family
(LBD)基因家族是一类植物特有的基因家族。该
家族的基因调控植物侧生器官原基的启动、侧生
器官的近—远轴极性建立、侧生器官与顶端分生
组织之间边界的建立(Iwakawa等2002; Shuai等
2002; Chalfun-Junior等2005; Liu等2005), 部分基因
还可以与顶端分生组织、侧生器官与顶端分生组
织的边界处特异表达的其它基因如KNOX基因、
CUP-SHAPED COTELYDON (CUC)基因、PETAL
LOSS (PTL)基因相互作用(Byrne等2000; Semiarti
等2001; Lin等2003; Xu等2003; Xu等2008), 参与调
控植物体内的激素积累以及植物花青素和氮素的
代谢途径等 (Scheib le等2004; Rub in等2009;
Albinsky等2010; Bell等2012)。侧生器官和分生组
织中央区的分离对于维持器官分化和分生组织分
生特性之间的相对平衡是必须的, 这种平衡有利
特约综述 Invited Review
植物生理学报834
于保证器官的持续发育和分生组织细胞分生特性
的发挥。通过确定器官-器官及器官-分生组织的
边界, 既可以把将要发育的侧生器官与顶端分生
组织的中央区隔离, 同时又能保证侧生器官和分
生组织的相对整体性, 是一种调节植物形态建成
的有效方式(Aida和Tasaka 2006)。
1 LBD蛋白的结构和分类
1.1 LBD蛋白的结构
LBD蛋白由氨基端的LOB结构域和羧基端的
可变C末端组成。LOB结构域包含一个典型的由4
个保守的半胱氨酸残基组成的CX2CX6CX3C (X代
表非保守的氨基酸残基)基序、一个保守的甘氨酸
残基和一个亮氨酸拉链类似基序(图1)。其中 ,
CX2CX6CX3C基序对于结合DNA是必需的; 亮氨酸
拉链基序LX6LX3LX6L可能与蛋白二聚化有关, 负
责LBD蛋白和其它蛋白的相互作用(Shuai等2002;
Matsumura等2009; Majer和Hochholdinger 2010; 图
1)。由于LBD蛋白的LOB结构域中存在核定位信
号, 因此LBD蛋白被推测是一种转录因子(Hus-
bands等2007; Okushima等2007; Lee等2009)。
1.2 LBD蛋白的分类
对拟南芥、水稻、玉米全基因组的LBD基因
进行系统进化分析, 发现根据LOB结构域中亮氨
酸拉链类似基序的存在与否可以将LBD基因归为
两类: 含有亮氨酸拉链类似基序的一类是第一类
(class I); 而缺失亮氨酸拉链类似基序的是第二类
(class II) (Shuai等2002; Iwakawa等2002; Majer和
Hochholdinger 2010; 图2)。LBD基因家族中的大部
分成员属于第一类。LBD蛋白一般不形成同源二
聚体, 而是与其它LBD蛋白或非LBD蛋白形成异
源二聚体(Evans等2007), 如 : ASYMMETRIC
LEAVES2 (AtAS2)蛋白和MYB结构域蛋白AtAS1
能够相互作用形成异源二聚体(Xu等2003), 玉米
LBD蛋白ZmIG1 (ZmLBD19)能够与AtAS1在玉米
中的同源蛋白ROUGH SHEATH2 (RS2)异二聚化
(Evens等2007)。第二类(class II) LBD蛋白由于缺
乏完整亮氨酸拉链基序, 不能形成coiled-coil结构,
所以它们在调控植物发育的功能上的作用机制区
别于第一类。
在双子叶模式植物拟南芥中, LBD基因家族
包括43个成员(Shuai等2002, 图2), 其中7个属于第
二类。在单子叶模式植物水稻中, 共有35个LBD基
因(Yang等2006, 图2), 其中5个属于第二类; 而在玉
米基因组中则有43个LBD基因(Schnable等2009; 图
2), 其中7个属于第二类。水稻和玉米的LBD基因
之间能够形成17个同源基因对 , 而拟南芥与水
稻、玉米的LBD基因之间只分别形成6个和5个同
源基因对, 说明LBD基因在单子叶植物间的亲缘关
系比在单子叶和双子叶植物间的亲缘关系近
(Majer和Hochholdinger 2010)。
2 LBD基因家族对植物发育和代谢的影响
LBD基因家族作为一类专门界定植物器官边
界的特殊基因 , 对植物发育的影响已经渗入至
叶、花序、根和小孢子的发育过程等各方面
(Borghi等2007)。
2.1 LBD基因对叶发育的影响
LBD基因调控植物叶片发育的机制中研究得
最早的是拟南芥AtASL4 (AtLOB)基因。AtASL4在
侧生器官的近轴面基部表达, 并且其表达依赖于
KNAT1蛋白和AtAS1蛋白(Shuai等2002)。当
BREVIPEDICELLUS (BP)蛋白和homeobox转录因
子SHOOT MERISTEMLESS (STM)蛋白分别结合
到AtASL4基因的5区段与3区段时, AtASL4仅在正
发育的叶原基与茎尖分生组织边界处表达, 从而
实现对拟南芥叶片早期发育的调控(Dolan和Lang-
dale 2004, 图3)。
图1 LBD蛋白结构(修改自Majer和Hochholdinger 2010)
Fig.1 Structure of LBD proteins
卢寰等: 高等植物特有的LBD基因的分子生物学功能研究进展 835
图2 拟南芥、水稻和玉米LBD蛋白的系统进化分析(Majer和Hochholdinger 2010)
Fig.2 Phylogeny of LBD proteins in Arabidopsis, rice and maize
植物生理学报836
AtAS2 (AtLBD6)也是调控叶片发育的LBD基
因, 该基因在子叶原基的近轴面表达(Iwakawa等
2002), 通过抑制近轴面区域的细胞增殖(Iwakawa
等2007), 使叶片的近-远轴两面对称发育成平展叶
(Semiarti等2001)。当用另一LBD蛋白的LOB结构
域代替AtAS2的LOB结构域时, AtAS2蛋白就会丧
失活性(Matsumura等2009), 说明LOB结构域在
AtAS2中的功能专一性。在STM基因调控下, AtAS2
基因仅在茎尖分生组织内表达, 但当它受BLADE
—ON—PETIOLE1 (BOP1)蛋白和BOP2蛋白诱导
后, 会扩散至茎尖分生组织和新叶原基的边界处
表达。同时, STM蛋白和AtAS1蛋白互为负调控因
子(Byrne等2000; Semiarti等2001, 图4)。在拟南芥
叶片中, BOP1蛋白直接诱导AtAS2基因先后在小叶
原基(Jun等2010)、叶片近轴面、近轴面与远轴面
交界的维管组织内表达(Iwakawa等2007)。类似这
种受特定蛋白诱导后表达位置迁移的例子还有
AtASL4和AtASL1等其它LBD基因(Uchida等2007;
Ha等2007)。
茎尖分生组织细胞的分生活力由KNOX基因
(KNAT1和KNAT2)决定(Long等1996; Vollbrecht等
2000; Scofield和Murray等2006)。只有在KNOX基
因的表达被抑制的情况下, 侧生器官如叶原基等
才会在茎尖分生组织的一侧起始发育(Jackson等
1994; Long等1996), 而KNOX基因过高的表达活性
则促使分生组织细胞持续增殖 (Sinha等1993;
Chuck等1996; Kidner等2002)。AtAS2基因不仅自
身直接调控拟南芥叶片的发育, 而且还可以通过
与其互作蛋白AtAS1结合形成异源二聚体在转录
水平上影响叶片的发育 (图4)。AtAS2蛋白和
AtAS1蛋白形成的异源二聚体直接同KNAT1启动
子序列内的两个顺式调控元件CWGTTD和KMK-
TTGAHW结合, 产生一个DNA环, 这个DNA环与
染色质重构因子HIRA协同抑制KNAT1的表达活
性促进叶原基的发育(Guo等2008)。此外, AS1-
AS2蛋白二聚体还能通过抑制KNOX基因如KNAT2
和KNAT6; 远轴化决定因子ETT/ARF3和KANADI2
(KAN2)的表达 , 使得叶片细胞维持在被决定
(determinated)的状态(Iwakawa等2007; Jun等2010;
Lin等2003; Ori等2000)。拟南芥叶中的KNOX基因
也能以类似的机制被AtARF6和AtA-RF8沉默
(Tabata等2010)。除第一类LBD基因中的AtAS2外,
图3 AtASL4调控拟南芥叶片发育模式图
Fig.3 Regulation model of AtASL4 on Arabidopsis leaf development
图4 AtAS2调控拟南芥叶片发育模式图
Fig.4 Regulation model of AtAS2 on Arabidopsis leaf development
卢寰等: 高等植物特有的LBD基因的分子生物学功能研究进展 837
第二类LBD基因中的AtASL38 (AtLBD41)基因在鸡
冠花中超表达后能引起叶的远轴化, 因此, 推测它
也可能参与调控叶发育过程的近—远轴极性决定
(Meng等2009)。而类似这种LBD蛋白通过与其它
蛋白之间形成异源二聚体调控植物叶片极性的机
制在单子叶植物中也存在, 如: AtAS1在玉米中的
同源蛋白RS2也能和AtAS2在玉米中的同源蛋白
及染色质重构因子HIRA相互作用(Phelps-Durr等
2005), 在叶原基发育过程中抑制KNOX基因的表
达(Timmermans等1999)。AtAS2在水稻中的同源基
因OsAS2基因也参与调控水稻叶的形成(Ma等
2009)。Luo等(2006)发现, 百脉根中的LBD基因
LjLOB1和LjLOB3在小叶原基的基部表达, 似乎暗
示着它们可能在百脉根的叶发育过程中发挥一定
功能。
2.2 LBD基因对花序发育的影响
AtAS2基因除了在拟南芥叶片极性建立的过
程中发挥关键功能外, 也能调控花序的发育(Xu等
2008)。AtAS2基因在幼嫩花器官的近轴面一侧特
异表达, 同时AtAS1基因和JAGGED (JAG)基因的
协同作用确立花器官中边界细胞的具体位置。双
突变体as2jag和as1jag的萼片和花瓣显著缩小, 在
这些明显缩小了的萼片和花瓣中, 一些边界特异
表达基因如CUC1基因、CUC2基因和PTL基因的
表达明显上调, 表达区域明显扩大; 在as1jag双突
变体背景中将CUC1基因、CUC2基因和PTL基因
功能缺失可以部分回复as1jag双突变体萼片和花
瓣缩小的表型, 说明AtAS2基因、AtAS1基因和JAG
基因三者可以通过在拟南芥的萼片和花瓣内协同
抑制CUC1基因、CUC2基因和PTL基因等边界特
异表达基因的表达, 来保证萼片和花瓣等花器官
的正常发育(Xu等2008, 图5)。拟南芥中与AtAS2基
因进化关系最近的AtASL1基因也以类似机制抑制
KNAT1基因的过量表达, 从而调控拟南芥花瓣的
近-远轴极性(Chalfun-Junior等2005)。水稻LBD基
因家族中的DH1基因可以控制水稻颖壳的发育,
DH1转录本在腋芽、幼穗、花序内的柱头和雄蕊
中有较高的积累, dh1突变体种皮不能正常发育,
柱头和浆片完全缺失, 雄蕊数目减少(Li等2008)。
玉米中的LBD基因Indeterminate gameto-phyte1
(Ig1)可以控制雌配子体增殖期的长短(Evans等
2007)。玉米RAMOSA2基因在花序的腋生分生组
织起始处表达, ramosa2突变体雄穗枝梗数增加, 并
且雄穗较上部的枝梗增长(Bortiri等2006)。百脉根
LjLOB4在发育中的花芽不同轮之间的边界表达,
似乎也暗示LjLOB4可能参与调控百脉根的花序发
育(Luo等2006)。我们课题组也克隆到一个水稻
LBD蛋白编码基因, 该基因的超表达转基因植株
的花序整体缩小, 而表达下调的转基因植株的花
序则变长(未发表工作)。
2.3 LBD基因对根发育的影响
高等植物侧根的发育过程受一系列细胞周期
相关的基因调控, E2F/DIMERIZATION PART-
NER(DP)/RETINOBLASTOMA-RELATED (RBR)
信号通路是一套在高等真核生物之间高度保守的
调控细胞周期起始的机制。通过激活G1/S期特异
性细胞周期蛋白依赖性激酶/细胞周期蛋白复合体
(cyclin-dependent kinase genes/cyclin complexes,
CDK/cyclin complexes)后, 转录抑制蛋白RBR被高
度磷酸化, 使得其从E2F/DP复合体中脱离, 进而激
活下游DNA复制特异调控基因的表达, 进入细胞
周期循环(Inze和De Veylder 2006; Berkmans和De
Veylder 2009)。拟南芥共包括六个E2F转录因子:
E2Fa、E2Fb、E2Fc、E2Fd、E2Fe/ DPa和E2Ff/
DPb。其中, E2Fa和E2Fb是细胞周期的转录激活
因子, 二者超表达后能促进细胞增殖(De Veylder等
2002; Sozzani等2006)。Berckmans等(2011)发现拟
南芥AtLBD33和AtLBD18能够通过形成蛋白异源
二聚体结合到E2Fa启动子序列中的顺式元件上,
激活E2Fa的表达, 进而促进根部侧生分生组织细
胞进入细胞周期循环, 最终启动拟南芥侧根的发
育(图6)。同时, lbd16lbd18双突变体的侧根数减少,
图5 AtAS2调控拟南芥花序发育模式图
Fig.5 Regulation model of AtAS2 on
Arabidopsis flower development
植物生理学报838
因此, 在拟南芥侧根基部特异表达的AtLBD18不仅
直接调控拟南芥侧根发育, 还能通过在转录水平
上影响E2Fa进而调控拟南芥侧根发育(Lee等2009;
Berckmans等2011)。拟南芥侧根的发育还依赖于
生长素响应因子AtARF7和AtARF19的活性。arf7-
arf19双突变体的侧根完全不能正常发育, 但在arf7-
arf19双突变体背景中超表达AtLBD16或AtLBD29
可以部分回复侧根发育障碍的表型, 说明AtARF7
和AtARF19影响根的发育可能部分地通过调控
LBD基因实现(Okushima等2007, 图6)。AtLBD29在
水稻、玉米中的同源基因Crl1 (Arl1)和Rtcs分别在
水稻和玉米的根冠原基处表达, 调控其根冠的发
育(Hetz等1996; Inukai等2005; Liu等2005; Taramino
等2007)。
2.4 LBD基因参与调控拟南芥小孢子的分裂
LBD基因不仅广泛地参与调控植物叶片、花
序和根等的发育过程, 还能通过调控细胞分裂影
响小孢子的发育。Oh等(2010)发现拟南芥SIDECAR
POLLEN (SCP)基因编码LBD27 (ASL29)蛋白, 对
于雄配子体发育过程中小孢子在正确时空范围内
的不对称分裂是必需的。
2.5 LBD基因参与调控植物代谢
目前已分离得到的少数几个第二类LBD基因
可能参与调控植物的氮素代谢。在AtASL39 (AtL-
BD37)、AtASL40 (AtLBD38)和AtASL41 (AtLBD39)
分别超表达的asl39、asl40、asl41突变体中, 花青
素合成调节基因PAP1和PAP2及一些氮素响应基因
的表达均受到抑制(Scheible等2004; Rubin等2009)。
Albinsky等(2010)发现水稻OsLBD37也和氮素代谢
相关。
3 LBD基因与植物激素的相互关系
3.1 LBD基因参与调控植物体内油菜素甾醇的积累
油菜素甾醇(brassinosteroid, BR)是一种类固
醇激素, 油菜素甾醇不仅广泛参与调控植物的株
型发育、从营养生长到生殖生长的转换、开花、
籽粒灌浆等生理过程, 而且能增加水稻对病原体
的抗病性, 提高植株的育性(Hanano等2006; Doma-
galska等2007; Li等2010a; Ye等2010; Hartwig等2011;
Makareritch等2012; Wang等2012)。Bell等(2012)发
现超表达拟南芥AtASL4基因可以激活其下游靶基
因PHYBACTIVATION TAGGED SUPPRESSOR1
(BAS1, 编码一类油菜素甾醇去活化酶), 解除油菜
素甾醇在分生组织和侧生器官边界处的积累, 回
复asl4缺失突变体自身的腋茎与茎生叶融合的表
型, 说明油菜素甾醇的高度积累在一定程度上是
引起asl4突变体的分生组织和侧生器官边界消失
的原因。同时AtASL4基因与油菜素甾醇之间通过
形成负反馈循环来调控侧生器官与分生组织边界
处细胞分化。
3.2 LBD基因协同生长素调控植株的形态建成
生长素(auxin)在植物体内的时空分布直接决
定了植物胚发育时期器官的发育和胚发育后期植
株的形态建成(Sabatini等1999; Friml等2002; Benk-
ova等2003; Blilou等2005)。而生长素浓度梯度的
动态分布依赖于生长素极性运输载体蛋白PINF-
ORMED (PIN)在特异类型细胞内表达方式及其多
样性的亚细胞定位方式等调控机制的发挥(Gälw-
eiler等1998; Paponov等2005; Zazímalová等2007;
Feraru和Friml 2008)。PLETHORA (PLT)基因可以
控制PIN基因家族在胚发育及胚胎后期发育过程
图6 AtLBD33、AtLBD18、AtLBD16和AtLBD29调控拟南芥根发育模式图
Fig.6 Regulation model of AtLBD33, AtLBD18, AtLBD16 and AtLBD29 on Arabidopsis root development
卢寰等: 高等植物特有的LBD基因的分子生物学功能研究进展 839
的表达(Blilou等2005; Galinha等2007)。Bureau等
(2010)克隆到拟南芥中一类LBD基因JAGGED
LATERAL ORGAN (JLO)基因, JLO在根尖分生组
织、发育的茎、花等器官与茎尖分生组织及花分
生组织的边界内特异表达, 并在很大程度上决定
了PLT1、3、4、7等基因的表达水平。当提高JLO
基因表达量时, PIN1和PIN3基因的表达量上调, 同
时PLT基因的表达在glo突变体中被严重下调。因
此, JLO基因通过控制PLT/PIN基因的表达间接调
控拟南芥中生长素信号转导途径, 进而对植株的
基-顶形态的建成及维持发挥关键功能(Bureau等
2010)。Mangeon等(2011)发现拟南芥中存在与
AtASL4基因和AtAS2基因高度同源的另一个LBD基
因DOWN IN DARK AND AUXIN1 (DDA1)。当施加
外源生长素时, DDA1的转录水平被下调, 而DDA1
的T-DNA插入突变体dda1-1对生长素响应的灵敏
度降低, 侧根数目减少。
3.3 LBD基因协同茉莉酮酸酯调控植株的抗病性
茉莉酮酸酯(jasmonate, JA)是一类脂类衍生
激素(Wasternack等2007; Balbi和Devoto 2008;
Katsir等2008)。当弥散性黄萎病原菌侵染宿主植
物时, 会分泌一种细菌毒素——冠菌素(CORONATINE,
COR), 使植物内源性的JA抗病信号通路被激活。
游离的小分子JA在由JASMONATE RESISTANT 1
(JAR1)基因编码产生的JA-氨基合成酶的催化作用
下与异亮氨酸结合形成JA-Ile短肽复合体(Staswick
等2002, 2004; Suza等2008), 该短肽复合体能与
COR竞争结合Jasmonate ZIM domain proteins
(JAZ), 而CORONATINE INSENSITIVE 1 (COI1)
这一F-box蛋白决定了E3泛素连接酶Skp/Cullin/
F-box (SCFCOI1)的靶标特异性(Feys等1994; Xie
等1998; Li等2004), 当JA-Ile结合到JAZ并形成
SCFCOI1-JA-Ile-JAZ后, 就能激活COI蛋白对JAZ蛋白
的泛素化降解(Chini等2007; Thines等2007; Yan等
2007), 进而解除对MYC2蛋白的抑制, 最终激活内
源性的JA早期响应基因THIONIN 2.1 (Thi2.1)和
VEGETATIVE STORAGE PROTEIN2 (VSP2)的表达
(Epple等1997; Chan等2005; Liu等2005)。其中,
Thi2.1编码抗菌小分子多肽——硫堇(thionin), 阻
止细菌毒素对植物的伤害, 而VSP2是JA早期响应
标志基因。Thatcher等(2012)发现拟南芥AtLBD20
基因在根中的表达水平与外源JA浓度呈正相关,
MYC2蛋白则可以通过直接与AtLBD20启动子上
游的顺式元件结合显著激活AtLBD20的表达, 同时
LBD20在coi1突变体和myc2突变体中几乎都不表
达, 说明LBD20的表达水平受JA、COI1蛋白和
MYC2蛋白调控。在lbd20突变体中Thi2.1和VSP2
表达上调 , 而在AtLBD20超表达转基因材料中 ,
Thi2.1和VSP2的表达下调。说明LBD20参与了COI
依赖性的JA介导的植物抗病响应。
3.4 LBD基因协同细胞分裂素调控植物发育
细胞分裂素(cytokinin, CK)是一种可以提高
植物抗逆性的重要激素。环境中的逆境信号如干
旱、高盐会降低内源性的细胞分裂素的合成运输
效率, 此时这些外界逆境因子被组氨酸—天冬氨
酸磷酸中继信号(His-Asp phosphorelay)接收、传
输和放大, 进而释放植物体内细胞分裂素响应基
因, 最终激活细胞分裂系抗逆信号通路(Ha等2011)。
施加外源细胞分裂素能有效增加植物叶片气孔细
胞的孔径和蒸腾作用, 进而通过提高植株的光合
效率增强其抗逆能力(Davis和Zhang 1991; Posp-
isilova和Batkova 2004; Pospisilova等2005)。Naito
等(2007)从拟南芥中分离到一类时空表达仅受细
胞分裂素特异性调控的LBD基因AtASL9。当有外
源细胞分裂素诱导处理时, AtASL9转录本在叶片
和根中大量积累, 而AtASL9::GUS转基因植株中原
本集中于茎尖分生组织和侧生子叶边界处的GUS
信号强度也显著增加, 说明AtASL9能够响应CK抗
逆信号途径。
3.5 与赤霉素相关的LBD基因
赤霉素(gibberellin acid, GA)是一种双萜类植
物激素, 可以促进植物种子萌发、叶片扩展、茎
节延伸和促进开花等。Ikezaki等(2010)证实AtAS2
可以通过抑制KNOX基因家族的表达促进赤霉素
的合成, 而另一LBD基因AtASL37的表达则受赤霉
素负调控(Zentella等2007)。
4 LBD基因与miRNA的关系
homeodomain/leucine zipper (HD-ZIP)转录因
子是一类植物特有的、广泛参与植物器官和维管
发育以及分生组织的建立与维持等重要发育过程
的调控因子。HD-ZIP转录因子通常分为四类, 依
次为: HD-ZIP I、HD-ZIP II、HD-ZIP III和HD-ZIP
植物生理学报840
IV。这四类HD-ZIP转录因子的结构、DNA结合
元件和功能都各不相同(Ariel等2007)。HD-ZIP I
蛋白结构中只有homeodomain (HD)结构域和leucine
zipper motif (LZ)基序, 其DNA结合元件是CAAT
(A/T)ATTG (Chan等1998; Palena等1999, 2001), 主
要负责脱落酸信号及非生物胁迫响应(Himmelbach
等2002; Henriksson等2005)。HD-ZIP II蛋白结构
中除HD和LZ外, 还有N端保守基序和Cys-Pro-Ser-
Cys-Glu基序(CPSCE基序), 其DNA结合元件是
CAAT(C/G)ATTG, 主要负责光信号、生长素信号
响应并调节植株的耐暗性(Morelli和Ruberti等
2000; Sawa等2002; Sessa等2005)。HD-ZIP III蛋白
结构中除HD和LZ外, 还包括类固醇急性调控蛋白
相关脂类转移结构域(steroidogenic acute regulatory
protein-related lipid transfer domain, START
domain)、START相邻结构域(START-adjacent
domain, SAD)和Met-Glu-Lys-His-Leu-Ala基序
(MEKHLA基序), 其DNA结合元件是GTAAT(G/C)
ATTAC (Sessa等1998), 主要调控胚胎发育、分生
组织的发育分化、侧生器官的起始、叶极性的建
立及维持、维管系统的发育及生长素的极性运输
(Baima等2001; Otsuga等2001; Prigge等2005)。
HD-ZIP IV蛋白结构中则含有HD、LZ、START结
构域和SAD结构域, 其DNA结合元件是CATT(A/T)
AATG (Tron等2001), 主要参与调控拟南芥根、表
皮毛的发育、花青素的积累及茎部表皮细胞的分
化(Kubo等1999; Luo等1999; Abe等2003; Ohashi等
2003; Chew等2013)。
miR165/166的靶基因编码HD-ZIP III转录因
子, 该类转录因子编码基因在拟南芥中有: PHAB-
ULOSA (PHB)、PHAVOLUTA (PHV)、REVOLUTA
(REV)、ATHB8、ATHB15。当靶基因中miR165/
166的识别位点突变后, 叶细胞命运就从远轴化转
为近轴化(McConnel l等2001; Emery等2003;
Mallory等2004; Williams等2005)。因此, 叶片近-
远轴面极性的建立取决于miR165/166在叶片近-远
轴面浓度分布的平衡, miR165/166是一类促进叶片
细胞远轴化的miRNA。ERECTA (ER)基因编码一
类富亮氨酸重复受体激酶(leucine-rich repeat
receptor kinase), ER基因可能通过参与AS1-AS2蛋
白复合体调控拟南芥叶极性建立的途径, 促使叶
细胞近轴化(Xu等2003; Qi等2004)。在as2er双突
变体中, 成熟miR165/166转录本大量积累(Li等
2005)。AtAS2蛋白可能通过抑制成熟miR165/166
的转录后形成过程, 在拟南芥叶片极性建立的整
体过程中发挥关键调控功能(Ueno等2007)。
5 分生组织和器官原基边界处特异表达的其它基因
组成边界的这类细胞一般体积较小, 相对于
邻近细胞分裂频率较低, 这种特性使边界成为区
别于分生组织和器官原基的独特区域 (Breui l -
Broyer等2004; Rast和Simon 2008), 并且这类细胞
表达特定基因, 借此实现在不影响侧生器官形成
的前提下, 限制器官原基位置的目的。这类特定
基因主要为植物特有的NAM-ATAF1、2-CUC2
(NAC)转录因子家族的CUC基因和GAI-RGA-SCR
(GRAS)转录因子家族的LATERAL SUPPRESSOR
(LAS)基因(Aida等1997; Takada等2001; Takada和
Tasaka 2002; Greb等2003)。
5.1 CUC基因
CUC基因控制胚顶端分生组织的形成及萼片
和雄蕊的分离过程(Aida等1997)。CUC1在营养生
长时期内表达量很低, 而在生殖生长时期的花序
顶端表达较高; CUC2在营养生长时期和生殖生长
时期的顶端分生组织表达都很弱。可能相对于
CUC1而言, CUC2在维持顶端分生组织和花序的
形成方面的功能比较次要。cuc1cuc2双突变体的
两片子叶边界融合成杯状、同一轮内的花器官发
生融合、茎尖分生组织的发育出现严重障碍(Aida
等1997, 1999; Ishida等2000; Takada等2001; Takada
和Tasaka 2002)。将cuc1cuc2双突变体的融合子叶
横切后能观察到与野生型完全相同的4层叶片组
织: 上表皮、栅栏组织、海绵组织和下表皮, 说明
cuc1cuc2双突变体子叶、花器官异常融合的表型
并非由组织分化规律的改变引起, 而是器官原基
和分生组织边界消失引起的, CUC基因是控制并
特化分生组织和器官原基之间边界的重要基因
(Aida等1997)。CUC2基因的表达受到RAX1基因
(编码一类MYB家族转录因子)的促进(Keller等
2006); 同时, CUC1和CUC2受到miR164的转录后
调控(Kasschau等2003; Laufs等2004; Mallory等
2004; Baker等2005; Schwab等2005; Nikovics等
2006)。CUC3基因的转录本起初在球形胚时期的
卢寰等: 高等植物特有的LBD基因的分子生物学功能研究进展 841
顶端部位, 继而集中在心型胚的子叶原基中表达,
最后在子叶原基和子叶分生组织的边界处、小花
原基和花序分生组织的边界处、萼片原基和萼片
分生组织的边界处、小花梗和腋芽的近轴面高度
积累。负责调控多种器官如茎、花梗与叶中的腋
生分生组织间边界的建立与维持(Hibara等2006)。
5.2 LAS基因
拟南芥LAS基因编码一类含GRAS结构域的
转录因子, 是番茄LS基因的同源基因。拟南芥LAS
可以完全回复番茄ls突变体腋生分生组织的发育
缺陷(Rossberg等2001)。LAS基因的表达模式与
CUC基因和LBD基因类似: 一般在子叶原基与茎
尖分生组织的边界处、小花原基与花序分生组织
的边界处表达。营养生长时期内, las突变体莲座
叶的叶腋处的腋生分生组织的发育不能正常起始;
而在生殖生长期内, 茎生叶的叶腋处长出的腋生
枝与主茎融合不能分离(Aida等1999; Takada等
2001; Shuai等2002; Greb等2003)。
6 结语
由于LBD基因作为一类新发现的高等植物特
有的基因家族, 目前仅揭示了在拟南芥、水稻和
玉米等少数几类模式植物中的部分LBD基因的功
能。对于它们在调控植物发育过程中的功能, 现
有的研究表明可能跟植物侧生分生组织的发育密
切相关, 但是理解得还不够深入。围绕着LBD基因
还有很多疑问等待着我们去逐一解释, 如: LBD基
因在其它种类植物中是否发挥功能？发挥怎样的
功能？已知的这些与植物激素有相互关系的或者
对miRNA有调控作用的LBD蛋白会有哪些下游靶
基因呢？LBD基因在定义植物器官与分生组织边
界时的精细调控机制又是什么？随着越来越多的
LBD基因在不同物种中被克隆和研究, 我们对于其
参与调控的发育过程和代谢途径必将有更为清晰
而详尽的认知。
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