全 文 ：植物生理学报 Plant Physiology Journal 2014, 50 (10): 1435~1444　　doi: 10.13592/j.cnki.ppj.2014.0197 1435
收稿 2014-04-28　　修定 2014-08-20
资助 国家自然科学基金(31370313、91317304和31171520)和浙
江省科技厅公益性项目(2013C32010)。
* 通讯作者(E-mail: jwpan@zjnu.cn; Tel: 0579-82287105)。
拟南芥下胚轴伸长与向光性的分子调控机理
姜楠, 王超, 潘建伟*
浙江师范大学化学与生命科学学院, 浙江金华321004
摘要: 下胚轴快速伸长和向光性是高等植物进行固着生活的重要适应性机制, 是子叶钻出土层进行光形态发生和光合作用
的必要前提。拟南芥下胚轴因其简单的生理形态结构和特异的生理功能而成为剖析植物细胞伸长和向性生长的理想模式
系统。本文主要介绍光和植物激素调控拟南芥下胚轴伸长和向光性弯曲的生理基础、遗传学功能及其分子调控机理的最
新进展。
关键词: 拟南芥; 下胚轴; 细胞伸长; 向光性; PIFs; 激素
Molecular Regulatory Mechanisms of Hypocotyl Elongation and Phototropism in
Arabidopsis
JIANG Nan, WANG Chao, PAN Jian-Wei*
College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, Zhejiang 321004, China
Abstract: Rapid elongation and phototropism of the hypocotyl, which are essential for the young seedling to
perceive light and undergo photomorphogenesis and photosynthesis, are important adaptive mechanisms for
plant sessile life. The Arabidopsis hypocotyl is an ideal model system to dissect cell elongation and tropic
growth in plants due to its simple physiological and morphological structure and specific physiological roles.
This review focused on physiological basis and genetic functions of light- and phytohormone-regulated hypo-
cotyl elongation and phototropism, and recent progresses on their regulatory molecular mechanisms in
Arabidopsis thaliana.
Key words: Arabidopsis thaliana; hypocotyl; cell elongation; phototropism; PIFs; hormones
综　述 Reviews
高等植物种子在土层中萌发后, 下胚轴(hypo-
cotyl)迅速向上伸长, 将子叶推出土层, 并转向阳光
一侧, 开始光合作用, 为幼苗植株后续生长发育提
供充足的养分。下胚轴的快速向上伸长和向光性
生长是高等植物长期进化的结果。如果下胚轴失
去这些生长特性, 萌发的种子会因子叶或胚乳中
的养分耗尽而死于土层中, 无法完成生活周期。
因此, 下胚轴对高等植物尤其是双子叶植物的生
命延续具有特殊的生理意义。下胚轴独特的生长
特性引起了植物学家浓厚的兴趣, 具有重要的科
学研究价值。大量的实验证据表明, 高等植物下
胚轴是研究植物细胞伸长(cell elongation)和向光
性(phototropism)分子机理的经典材料(Vanden-
bussche等2005)。最近几年, 植物学家利用遗传、
细胞和生理生化等现代分析手段, 从分子细胞水
平上剖析了下胚轴伸长和向光性的分子机理, 取
得了长足的进展(Nozue等2007; de Lucas等2008;
Feng等2008; Ding等2011; Sun等2013)。因此, 本文
在介绍一些光和激素调控下胚轴的研究背景的基
础上, 重点介绍最近几年有关下胚轴伸长和向光
性生长的最新进展。
1 下胚轴的生理与形态结构基础
下胚轴是高等植物胚胎和胚后期的幼苗茎,
是连接根系和茎叶的重要结构, 也是水、矿质元
素、养分和信号分子运输的重要通道; 同时, 对内
源信号分子(如激素)和环境刺激(如光、温度和重
力等)非常敏感, 并作出快速响应(Nozue等2007; de
Lucas等2008; Feng等2008; Christie等2011; Ding等
植物生理学报1436
2011; Franklin等2011; Bai等2012; Sun等2012,
2013; Kami等2014)。因此, 下胚轴是一个可塑性
很强的器官, 对高等植物幼苗的生长发育具有重
要生物学功能。双子叶模式植物拟南芥(Arabidop-
sis thaliana)下胚轴形态结构简单, 从顶端到基部
(纵向)共由20多个细胞组成, 大多在胚胎期形成,
仅少数在种子萌发后通过细胞分裂产生, 因此下
胚轴伸长主要起因于细胞伸长。拟南芥下胚轴从
内到外(横向)由中柱维管束、内皮层、皮层和表
皮层等组成(Gendreau等1997)。拟南芥下胚轴因
具有简单的形态结构和特异的生理功能而成为研
究植物细胞伸长和向性生长的重要模式系统。
2 下胚轴伸长的调控机理
已知下胚轴的快速伸长受环境因子和多种内
源激素的综合调控。最近的遗传与生化证据表明,
环境信号和内源激素通过转录因子光敏色素互作
蛋白PIFs (PHYTOCHROME-INTERACTING FAC-
TORs)整合调控下胚轴伸长(Nozue等2007; de
Lucas和Prat 2014; Leivar和Monte 2014)。
2.1 光和激素调控下胚轴伸长的遗传学证据
在土壤中, 黑暗诱导萌发的种子下胚轴快速
伸长, 导致子叶破土而出接受阳光, 标志着暗形态
发生(skotomorphogenesis)的终止和光形态发生
(photomorphogenesis)的开始。光抑制下胚轴伸长
主要依赖于五类光受体: 光敏色素PHYA-E (PHY-
TOCHROMEs, 远红光或红光受体)、向光素PHOT
(PHOTOTROPINs, UV-A/蓝光受体)、隐花色素
CRY (CRYPTOCHROMEs, UV-A/蓝光受体)、
ZTL/FKF1/LKP2家族(ZEITLUPE/FLAVIN BIND-
ING KELCH-REPEATF-BOX1/LOV KELCH PRO-
TEIN2, UV-A/蓝光受体)和UVR8 (UV-B RESIS-
TANCE 8, UV-B受体) (Yang等2000; Möglich等
2010; Wu等2012)。遗传分析表明, 突变体phyA和
phyB分别在远红光和红光下具有长胚轴表型(Reed
等1998), 表明PHYA/B介导远红光或红光对下胚轴
伸长的抑制效应。在特定的UV-B照射下, 突变体
uvr8具有长胚轴表型(Favory等2009), 表明UVR8介
导UV-B对下胚轴伸长的抑制作用。在蓝光下, 突
变体phot1下胚轴长度与野生型相似(Kang等2008),
而cry1下胚轴明显比野生型长(Parks等1998), 表明
CRY1介导蓝光对下胚轴伸长的抑制作用。然而,
蓝光能瞬时抑制黑暗生长的野生型、phot2和cry1
下胚轴伸长, 但未能瞬时抑制phot1和phot1cry1下
胚轴伸长; 相反, 蓝光能持续抑制野生型和phot1,
但不能持续抑制cry1 (Folta等2001), 暗示PHOT1介
导蓝光对下胚轴的快速抑制。ztl-1突变体下胚轴
在蓝光下比野生型长3倍, 但在红光下其伸长受到
抑制(Somers等2000), 表明ZTL介导蓝光对下胚轴
伸长的调控作用。
植物激素是下胚轴伸长的重要调控信号分
子。已知外源生长素、赤霉素(GA)和油菜素甾醇
(BR)处理促进下胚轴伸长(Vandenbussche等2005),
暗示这些生长物质正调控下胚轴伸长。生长素转
录信号突变体axr1-12 (auxin resistant 1-12) (Leyser
等1993)和核受体突变体 tir1afb2afb3 (transport in-
hibitor response 1/auxin signaling f-box protein 2/3)
均表现为短胚轴, 并且对外源生长素处理不敏感
(Chapman等2012), 表明生长素转录信号途径对下
胚轴伸长是必需的。GA合成突变体ga1和信号突
变体gai具有短胚轴表型, 外源GA4处理能恢复ga1
短胚轴表型, 但未能恢复gai短胚轴表型(Cowling
和Harberd 1999)。同样, BR合成突变体dwf1/dim/
cbb1 (dwarf 1/dimunito/cabbage 1)和det2 (de-etio-
lated 2)和BR信号突变体bri1 (brassinosteroid-in-
sensitive 1)均表现为短胚轴表型(Clouse 1996)。这
些分析结果表明, GA和BR合成与信号传导对下胚
轴伸长也是必需的。
2.2 下胚轴伸长的分子调控机理
早期的遗传与生化证据表明, 拟南芥下胚轴
伸长主要受外界光信号和内源激素拮抗调控, 但
具体的拮抗调控机制一直不清楚。最近的研究发
现, 转录因子PIFs通过整合胞内外信号来调控下胚
轴伸长(图1)。PIFs是一类含bHLH (basic he-
lix-loop-helix)结构域的转录因子家族, 最初的生物
信息学分析暗示, 在PIF亚家族中, 共有15个同源成
员(Toledo-Ortiz等2003), 但至今仅7个成员(PIF1、
3、4、5、6、7和8)被证实能与PHYA或PHYB互
作(Leivar和Monte 2014) (图1)。这7个PIFs蛋白主
要由bHLH结构域(与DNA结合)、APB结构域(ac-
tive PHYB binding; 与PHYB活性形式Pfr结合)和
APA结构域(active PHYA binding, 与PHYA活性形
式Pfr结合)组成(Leivar和Monte 2014)。
姜楠等: 拟南芥下胚轴伸长与向光性的分子调控机理 1437
最近的研究表明, 黑暗生长的幼苗受到外界
光信号刺激后, PHYA和PHYB分别被远红光和红
光激活后以Pfr形式进入细胞核, PHYA与PIF1/3/4/6
结合, 而PHYB与PIF1/3/4/5/6/7/8都能结合, 以诱导
这些PIFs磷酸化和快速降解, 从而抑制由这些PIFs
介导的暗形态发生和下胚轴伸长(Nozue等2007;
Shen等2007; Leivar等2008; Shen等2008; Jeong等
2013)。四突变体pif1pif3pif4pif5 (pifq)在黑暗下表
现出与组成型光形态发生突变体cop1 (constitutive
photomorphogenesis 1)相似的表型, 如短胚轴、子
叶展开等(Leivar等2008), 同样, PIF1/3/4/5功能同
时缺失抑制了phyB长胚轴表型(de Lucas等2008;
Leivar等2012); 相反, 分别过表达PIF3、PIF4、PIF5
导致长胚轴等暗形态发生表型(Khanna等2007; Sun
等2012; Jeong等2013)。以上遗传与生化证据表明
光通过激活PHYA/B的活性来促进PIFs降解从而抑
制下胚轴伸长, 而黑暗通过抑制PHYA/B的活性来
促进PIFs的积累和下胚轴伸长(图1)。
已知光信号能调控植物内源激素的生物合
成。PHYA/B或CRY1功能缺失促进GA含量上升
和下胚轴伸长(Reed等1998; Foo等2006; Kunihiro
等2010)。GA促进受体GID1 (GA INSENSITIVE
DWARF 1)与其底物转录阻碍蛋白DELLAs结合,
导致DELLAs泛素化和降解。最近的研究发现,
PHYB和CRY1通过调控GA含量来调控DELLAs水
平, 而DELLAs通过与PIF3/4/5互作从而抑制这些
PIFs与DNA的结合能力和转录活性(de Lucas等
2008; Feng等2008; Kunihiro等2010), 表明PIFs位于
DELLAs下游起作用(图1), 暗示光通过下调GA含
量促进DELLAs积累, 从而导致PIF3/4/5转录活性
的下调和下胚轴伸长; 相反, 黑暗促进GA合成和
DELLAs降解, 从而释放PIF3/4/5的转录活性和下
图1 下胚轴伸长的分子调控机理
Fig.1 Molecular regulatory mechanisms of hypocotyl elongation
参考de Lucas等(2008)、 Feng等(2008)、Bai等(2012)、Sun等(2012)、Leivar和Monte (2014)文献并作修改。
植物生理学报1438
胚轴伸长。因此, 光信号通过PHYA/B-或CRY1-
GA-DELLA途径来调控PIF3/4/5的转录活性和下
胚轴伸长(图1), 推测della多突变体长胚轴表型可
被PIF3/4/5功能同时缺失所抑制。
最近的生化分析表明, PIF4与调控BR信号传
导的转录因子BES1/BZR1 (BRI1-EMS-SUPPRES-
SOR 1/BRASSINAZOLE RESISTANT 1)结合, 以
异源二聚体(BZR1-PIF4)的形式激活下游靶基因的
表达(Oh等2012; de Lucas和Prat 2014) (图1)。pifq
下胚轴对外源BR不敏感, 并且抑制了功能获得性
突变体bzr1-D (组成型非磷酸化活性形式)长胚轴
表型(Oh等2012), 表明BES1/BZR1介导下胚轴伸长
位于PIFs的上游。遗传与生化证据表明, DELLAs
通过同时与BZR1和PIF4互作从而抑制BZR1-PIF4
二聚体的转录活性; 相反, GA释放DELLA对BZR1
的抑制效应(图1); pifq bzr1-1D突变体对GA不敏感
(Bai等2012), 表明激活的BZR1对GA诱导下胚轴伸
长是必需的, 并且DELLA-BZR1-PIF4之间的互作
是光信号、GA和BR调控下胚轴伸长的重要机制
之一(图1)。另有研究表明, BZR1结合于IAA19和
ARF7启动子(Zhou等2013), 而PIF4与IAA19和
IAA29启动子结合(Sun等2013), 暗示BZR1-PIF4对
生长素下游基因的转录调控是BR与生长素交互对
话(crosstalk)的重要机理之一。
另外, 其他激素如乙烯、细胞分裂素(CK)和
独脚金内酯(SL)抑制黑暗诱导的下胚轴伸长(Van-
denbussche等2005; Jia等2014)。乙烯在光下能促
进下胚轴伸长 , 但在黑暗下却抑制下胚轴伸长
(Smalle等1997)。在黑暗中, 乙烯过量合成突变体
eto1 (ethylene overproducer 1)、信号传导突变体
ctr1 (constitutive triple response 1)和受体三突变体
etr1etr2ein4 (ethylene response 1/2/ethylene insensi-
tive 4)均表现为短胚轴(Guzman和Ecker 1990; Hua
和Meyerowitz 1998), 而乙烯信号传导突变体ein2
具有长胚轴表型, 对乙烯不敏感(Cary等1995)。因
此, 乙烯受体ETR1激活CTR1从而抑制下游EIN2
和EIN3/EIL1 (ETHYLENE INSENSITIVE 3/EIN3
like 1)介导的乙烯信号途径(Guo等2003)。最新研
究表明 , 光通过促进PIF3降解和提高转录因子
ERF1 (ETHYLENE RESPONSE FACTOR 1, 负调
控下胚轴伸长) 稳定性来抑制下胚轴伸长(Zhong
等2014)。在光下, 乙烯通过促进EIN3/EIL1介导的
PIF3转录活性从而促进下胚轴伸长; 而在黑暗下,
乙烯通过提高EIN3/EIL1介导的ERF1稳定性从而
抑制下胚轴伸长(Zhong等2012, 2014) (图1), 暗示
在光和黑暗下乙烯对下胚轴伸长的截然相反的调
控作用主要通过调控EIN3/EIL1介导的PIF3转录活
性和ERF1稳定性来实现的。细胞分裂素CK在黑
暗下抑制下胚轴伸长但在光下不影响下胚轴伸
长。突变体ckr1 (cytokinin resistant 1)/ein2和ein1下
胚轴伸长对细胞分裂素BA (6-benzylaminopurine)
和乙烯不敏感(Cary等1995), 表明细胞分裂素通过
乙烯来间接影响下胚轴伸长(图1)。SL在黑暗下抑
制下胚轴伸长(Cheng等2013)。光受体突变体
cry1、cry2、phyA和phyB及其下游cop1和 pifq在相
应的单色光下对独脚金内酯类似物GR24超敏(Jia
等2014), 暗示CRY和PHYA/B介导的光信号途径负
调控SL对下胚轴伸长的影响。GR24 (<10 μmol·L-1)
能有效抑制光下野生型下胚轴伸长, 而SL信号突
变体max2 (more axillary growth 2)下胚轴伸长对
GR24不敏感(Jia等2014), 暗示SL通过MAX2介导
的信号途径负调控下胚轴伸长。另外, SL通过促
进MAX2介导的bZIP转录因子HY5 (ELONGATED
HYPOCOTYL 5)的转录活性和光依赖的HY5积累
来抑制下胚轴伸长(Jia等2014) (图1)。尽管已知
PIF1或PIF3能与HY5形成异源二聚体(Chen等
2013), 但这种异源二聚体在下胚轴伸长中的作用
仍有待于进一步证实(图1)。
已知高温(29 ℃)促进下胚轴局部生长素合成
从而诱导下胚轴伸长(Gray等1998)。最近的遗传
与生化证据表明, PIF4、PIF5和PIF7能与生长素合
成酶基因TAA1 (TRYPTOPHAN AMINOTRANSFER-
ASE OF ARABIDOPSIS 1)和YUC8 (YUCCA 8)启动
子结合从而来激活TAA1和YUC8的表达(Franklin等
2011; Hornitschek等2012; Sun等2012)。YUC8功能
缺失显著抑制由PIF4过表达或高温诱导的长胚轴
表型(Sun等2012), 表明高温通过促进PIF4的表达
从而激活YUC8的转录, 最终导致下胚轴IAA含量
上升和下胚轴伸长(图1)。除促进下胚轴IAA合成
外 , 高温也间接诱导B R合成酶基因D W F 4
(DWARF4)的表达和BR合成, 从而促进了BR介导
的下胚轴伸长(Maharjan和Choe 2011) (图1)。另外,
姜楠等: 拟南芥下胚轴伸长与向光性的分子调控机理 1439
外源蔗糖能诱导野生型下胚轴伸长, 但未能诱导
pifq下胚轴伸长且外源GA未能弥补这一缺陷(Liu
等2011), 暗示PIF1/3/4/5和GA共同介导蔗糖诱导
的下胚轴伸长(图1)。
综上所述, 虽然PIF家族中的成员对下胚轴伸
长都有一定的作用, 但不同PIFs在不同环境或激素
信号传导中起作用, 它们之间的功能并不是完全
冗余。在黑暗中, PIF1参与抑制种子萌发、下胚轴
顶钩的形成和子叶的打开; 而在光下, PIF3参与调
控乙烯诱导的下胚轴伸长(Jeong等2013)。PIF4介
导高温诱导下胚轴伸长, 而PIF7介导下胚轴避荫反
应(Li等2012); PIF3/4/5与DELLA互作, 而PIF4/5/7
调控生长素的合成。
3 下胚轴向光性调控机理
植物向光性是植物根据光源方向通过下胚轴
或茎的向光面和背光面的差异生长来改变自身的
生长方向(Sakai和Haga 2012)。这是植物为了争夺
有限光源和生存空间, 在进化过程中逐渐形成的
一种环境适应性机制。已知单侧蓝光或白光诱导
的下胚轴向光性弯曲主要由质膜定位的PHOT来
介导, 由三个关键性步骤组成: (1) PHOT感受并传
导蓝光信号, (2)下胚轴向光面与背光面生长素不
对称分布, (3)下胚轴细胞不对称伸长和向光性弯
曲(Hohm等2013)。在此过程中, 其他光信号受体
和激素也参与调控下胚轴向光性弯曲。
3.1 PHOT介导蓝光诱导的向光性
拟南芥蓝光受体PHOT家族共有两个同源成员
PHOT1和PHOT2。遗传分析表明, 在单侧弱蓝光下,
突变体phot1和phot1phot2下胚轴均无向光性表型,
但phot2仍有向光性; 在单侧强蓝光下, phot1phot2仍
无向光性, 但phot1和phot2均有向光性(Sakai等
2001), 表明PHOT1和PHOT2之间存在部分功能冗
余, PHOT1是强弱蓝光诱导向光性弯曲所必需的,
而PHOT2仅在强蓝光下起作用。
PHOT主要由N端的光感受结构域和C端的
Ser/Thr激酶域组成。Ser/Thr激酶域主要催化蓝光
激发的PHOT自体磷酸化(Cho等2007), 而N端含有
LOV1 (light oxygen voltage 1)和LOV2光感受结构
域(Demarsy和Fankhauser 2009), 其中LOV2是
PHOT1自体磷酸化和PHOT1介导下胚轴向光性不
可或缺的(Cho等2007), 但LOV1的功能目前仍不清
楚。在LOV2和激酶区域之间的活性环中, PHOT1
Ser851残基非常保守, 它的自体磷酸化是光信号转
导的主要分子事件(Inoue等2008)。Ser/Thr蛋白磷
酸酶2A (PP2A)功能缺失引起PHOT2去磷酸化抑
制和向光性弯曲的加强(Tseng和Briggs 2010), 表明
PP2A对PHOT2介导的向光性具有负调控作用。
质膜定位的PHOT1通过网格蛋白介导的内吞
CME (clathrin-mediated endocytosis)途径进入胞腔
内, 蓝光促进PHOT1内吞(Kaiserli等2009), 而这一
过程被红光诱导的PHYA活性所抑制, 从而促进向
光性弯曲(Han等2008)。此外, PHOT1与生长素运
输载体PIN (PIN FORMED)和ABCB (ATP-BIND-
ING CASSETTE B)蛋白共定位于质膜(Wan等
2008; Titapiwatanakun等2009), 暗示PHOT1可能与
PIN和ABCB之间存在一定的互作关系。目前已知
拟南芥有四种PHOT互作蛋白: NPH3 (NON-PHO-
TOTROPIC HYPOCOTYL 3)、RPT2 (ROOT PHO-
TOTROPISM 2)、PKS1 (PHYTOCHROME KI-
NASE SUBSTRATE 1)和14-3-3 (Chen等2008;
Hohm等2013)。
NPH3和RPT2属于NRL (NPH3/RPT2-like)家
族成员 , 拥有BTB/POZ (BROAD COMPLEX,
TRAMTRACK, BRIC A BRAC/POX VIRUS AND
ZINC FINGER)和coiled-coil结构域, 参与蛋白与蛋
白之间的互作(Motchoulski和Liscum 1999)。质膜
定位的NPH3与PHOT1/2互作(Sakamoto和Briggs
2002)。蓝光分别诱导NPH3去磷酸化和PHOT1磷
酸化(Pedmale和Liscum 2007), NPH3参与调控PIN
的亚细胞定位(Wan等2012), NPH3功能缺失抑制了
下胚轴生长素的不对称分布和向光性弯曲(Haga等
2005; Roberts等2011), 表明NPH3去磷酸化对于
PHOT1介导的向光性具有重要调控作用。然而,
强蓝光诱导的phot1单突变体的向光性应答中 ,
NPH3并没有去磷酸化(Tsuchida-Mayama等2010),
暗示PHOT2介导的向光性不需要NPH3去磷酸
化。同样, 质膜定位的RPT2与PHOT1共定位(Ina-
da等2004)。酵母双杂交分析表明, RPT2与NPH3
互作(Lariguet等2006)。RPT2参与调控PHOT1介
导的向光性弯曲, 尤其在强蓝光下(Sakai等2000;
Inada等2004; Sakai和Haga 2012), 但并不参与
PHOT2介导的向光性弯曲(Zhao等2013)。这些分
植物生理学报1440
析结果暗示PHOT1和PHOT2通过不同调控机制来
介导下胚轴向光性。PKS也是质膜定位蛋白, 共有
4个同源成员PKS1~PKS4 (Lariguet等2006), 其中
PKS4主要在下胚轴伸长区表达, 体外磷酸化分析
暗示PKS4很可能是PHOT1的磷酸化底物(Demarsy
等2012)。pks1、pks2和pks4的单和双突变体均有
向光性缺陷表型, 而pks1pks2pks4向光性缺陷更加
严重(Lariguet等2006), 且在该突变体的黄化幼苗
顶钩区域, 生长素侧向运输及其信号传导发生改
变(Kami等2014), 表明PKS之间存在功能冗余。有
研究表明PKS1均能与PHOT1/2和PIN1相互作用
(Lariguet等2006; Zhao等2013), 暗示PHOT1/2可能
通过PKS1来调控PIN1的亚细胞定位(图2)。另外,
14-3-3λ主要与PHOT介导的气孔开启相关, 是否参
与调控下胚轴向光性仍缺乏证据。以上结果表明,
NPH3、RPT2和PKS是PHOT介导向光性的重要互
作蛋白。
除PHOT外, 其他光受体也参与向光性弯曲。
在蓝光处理之前, 用UV-A、红光、远红光预处理
或和蓝光一起处理能够增强下胚轴向光性弯曲
(Liscum和Briggs 1996)。遗传分析表明, PHYA功
能缺失抑制了红光对向光性的促进作用, 但PHYB
功能缺失并没有影响红光的增强作用(Parks等
1996)。最近的分析表明, phyAphyBphyCphyDphyE
五突变体仍有90%的向光性反应, 但phyBphyCphy-
DphyE四突变体仍有正常向光性(Kami等2012), 表
明向光性的增强效应主要由PHYA来介导。更有
意思的是, phyAcry1cry2和phyAphyBcry1cry2具有
严重的向光性缺陷(Tsuchida等2010), 表明PHYA和
CRY具有协同调控向光性的功能(图2)。
3.2 生长素介导的向光性弯曲
生长素不对称分布是导致向性生长的主要原
因, 这种不对称分布主要由生长素运输载体AUX1/
LAX (AUXIN RESISTANT 1/LIKE AUXIN RESIS-
TANT)、ABCB19和PIN协同完成(Christie等2011;
Ding等2011; Zhang等2013)。最近的遗传与生理分
析表明, 单侧蓝光或白光诱导野生型下胚轴伸长区
PIN3的重定位, 引起内皮层细胞背光一侧有更多
的PIN3定位(侧向定位), 导致下胚轴生长素的不对
称分布和向光性弯曲; 相反, PHOT1功能缺失抑制
了单侧光诱导的下胚轴PIN3重定位、生长素不对
称分布和向光性弯曲, 同样, pin3下胚轴生长素不
对称分布和向光性弯曲也均被抑制(Ding等2011),
而且 pin3pin4pin7和pin1pin3pin7下胚轴向光性缺
陷比pin3pin7更严重(Haga和Sakai 2012)。此外, 在
Ser/Thr蛋白激酶PID (PINOID)过表达突变体和
wag1wag2pid缺失突变体中, 单侧光诱导的PIN3侧
图2 下胚轴向光性分子调控机理
Fig.2 Molecular regulatory mechanisms
of hypocotyl phototropism
参考Zourelidou等(2009)、Christie等(2011)、Ding等(2011)、
Sun等(2013)文献并作修改。
姜楠等: 拟南芥下胚轴伸长与向光性的分子调控机理 1441
向定位和向光性弯曲均被抑制; 进一步分析表明,
蓝光显著抑制野生型植株PID的转录水平, 而在
phot1phot2双突变体中这种抑制作用明显减弱
(Ding等2011), 暗示PHOT介导的蓝光信号通过抑
制PID的转录水平和PIN3磷酸化来促进PIN3侧向
重定位, 从而诱导生长素不对称分布和向光性弯曲
(图2)。然而, 另有研究认为, 单侧蓝光诱导下胚轴
生长素不对称分布最初发生在下胚轴顶部(子叶
节) (Christie等2011)。在下胚轴顶部, 蓝光促进
PHOT1介导的ABCB19磷酸化从而抑制ABCB19的
输出活性, 引起下胚轴垂直生长停止和顶部背光面
生长素积累, 生长素由此侧向流向下胚轴伸长区背
光面, 最终导致向光性弯曲(Christie等2011)。
ABCB19功能缺失促进向光性弯曲, 可能通过激活
PHY和CRY的功能来实现(Noh等2003; Nagashima
等2008; Christie等2011)。这些结果暗示ABCB19
负调控下胚轴向光性弯曲(图2)。此外, 生长素输
入载体AUX1/LAX功能缺失后也引起下胚轴向光
性缺陷, 表明AUX1/LAX参与调控下胚轴向光性
(Stone等2008), 但具体的调控机理仍不清楚。
除生长素运输载体外, D6PK (D6 PROTEIN
KINASE)和生长素信号传导途径也参与调控下胚
轴向光性弯曲。遗传与生化分析表明, D6PK能磷
酸化PIN3蛋白, D6PK功能缺失多突变体d6pk012
和d6pk0123下胚轴生长素向基运输和向光性弯曲
均被显著抑制(Willige等2013), 表明D6PK通过介
导PIN磷酸化调控下胚轴生长素运输和向光性弯
曲(图2)。阻碍蛋白MSG2/IAA19 (MASSUGU 2/
INDOLE-3-ACETIC ACID 19)通过抑制转录因子
NPH4/ARF7 (AUXIN RESPONSE FACTOR 7)的活
性, 从而参与调控下胚轴向光性弯曲(Zourelidou等
2009)。NPH4/ARF7功能缺失突变体(Harper等
2000)和MSG2/IAA19功能获得性突变体(Tatemat-
su等2004)下胚轴向光性弯曲均被抑制。在单侧光
刺激下, 下胚轴背光面的生长素大量积累促进了
MSG2/IAA19降解, 释放NPH4/ARF7的转录活性
(Stone等2008), 最终导致与向光性生长相关基因的
表达(图2)。最近的遗传与生化证据表明, PIF4通
过与IAA19和IAA29启动子G-box基序结合直接激
活它们的表达, 从而抑制ARF7的活性和向光性弯
曲; PIF4功能缺失促进了下胚轴向光性弯曲(Sun等
2013)。TIR1/AFB介导的信号途径通过调控ARF7
或其他转录因子的表达和生长素不对称分布, 从而
引起向光性弯曲(Sakai和Haga 2012)。tir1afb1af-
b2afb3四突变体下胚轴向光性严重缺陷(Möller等
2010)。因此 , 推测生长素通过TIR1/AFB下调
IAA19水平从而促进ARF7的表达和向光性弯曲, 相
反, PIF4通过促进IAA19的表达来抑制ARF7的转录
活性和向光性弯曲(图2)。
4 展望
近几年来, 人们综合利用遗传学、细胞学和
生理生化等研究手段, 对植物下胚轴伸长和向光
性机制研究已取得了重要进展, 如光信号和内源
生长激素通过PIFs的整合调控作用来介导下胚轴
伸长, ABCB和PIN介导下胚轴向光性弯曲的分子
作用机理等等, 但仍有许多问题有待于进一步研
究: (1)外界环境因子是否都通过PIF的整合功能来
调控下胚轴伸长？(2)除PHYA/B外, PIFs是否与其
他光受体如PHOT、CRY等互作从而调控蓝光信
号途径？(3) PHOT互作蛋白如NPH3、RPT2和
PKS等是否调控ABCB19的活性或PIN的重定位?
(4)生长素胞外受体ABP1 (AUXIN BINDING PRO-
TEIN 1)和网格蛋白是否参与调控下胚轴伸长和向
光性？如何调控？因此, 要真正剖析植物下胚轴
伸长和向光性分子机理仍面临巨大的挑战。
参考文献
Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang
ZY (2012). Brassinosteroid, gibberellin and phytochrome im-
pinge on a common transcription module in Arabidopsis. Nat
Cell Biol, 14 (8): 810~817
Cary AJ, Liu W, Howell SH (1995). Cytokinin action is coupled to
ethylene in its effects on the inhibition of root and hypocotyl
elongation in Arabidopsis thaliana seedlings. Plant Physiol, 107
(4): 1075~1082
Chapman EJ, Greenham K, Castillejo C, Sartor R, Bialy A, Sun TP,
Estelle M (2012). Hypocotyl transcriptome reveals auxin regu-
lation of growth-promoting genes through GA-dependent and
-independent pathways. PLoS One, 7 (5): e36210
Chen X, Lin WH, Wang Y, Luan S, Xue HW (2008). An inositol poly-
phosphate 5-phosphatase functions in PHOTOTROPIN1 signal-
ing in Arabidopsis by altering cytosolic Ca2+. Plant Cell, 20 (2):
353~366
Chen D, Xu G, Tang W, Jing Y, Ji Q, Fei Z, Lin R (2013). Antag-
onistic basic helix-loop-helix/bZIP transcription factors form
transcriptional modules that integrate light and reactive oxygen
species signaling in Arabidopsis. Plant Cell, 25 (5): 1657~1673
植物生理学报1442
Cheng X, Ruyter-Spira C, Bouwmeester H (2013). The interaction be-
tween strigolactones and other plant hormones in the regulation
of plant development. Front Plant Sci, 4 (199): 1~16
Cho HY, Tseng TS, Kaiserli E, Sullivan S, Christie JM, Briggs WR
(2007). Physiological roles of the light, oxygen, or voltage do-
mains of phototropin 1 and phototropin 2 in Arabidopsis. Plant
Physiol, 143 (1): 517~529
Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J,
Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR et al (2011).
phot1 inhibition of ABCB19 primes lateral auxin fluxes in
the shoot apex required for phototropism. PLoS Biol, 9 (6):
e1001076
Clouse SD (1996). Molecular genetic studies confirm the role of brass-
inosteroids in plant growth and development. Plant J, 10 (1): 1~8
Cowling RJ, Harberd NP (1999). Gibberellins control Arabidopsis hy-
pocotyl growth via regulation of cellular elongation. J Exp Bot,
50 (337): 1351~1357
de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, lglesias-Pe-
draz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E,
Prat S (2008). A molecular framework for light and gibberellin
control of cell elongation. Nature, 451 (7177): 480~484
de Lucas M, Prat S (2014). PIFs get BRright: PHYTOCHROME
INTERACTING FACTORs as integrators of light and hormonal
signals. New Phytol, 202 (4): 1126~1141
Demarsy E, Fankhauser C (2009). Higher plants use LOV to perceive
blue light. Curr Opin Plant Biol, 12 (1): 69~74
Demarsy E, Schepens I, Okajima K, Hersch M, Bergmann S, Christie
J, Shimazaki K, Tokutomi S, Fankhauser C (2012). Phytochrome
Kinase Substrate 4 is phosphorylated by the phototropin 1 pho-
toreceptor. EMBO J, 31 (16): 3457~3467
Ding Z, Galván-Ampudia CS, Demarsy E, Łangowski Ł, Kleine-Vehn
J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R et al
(2011). Light-mediated polarization of the PIN3 auxin transport-
er for the phototropic response in Arabidopsis. Nat Cell Biol, 13
(4): 447~452
Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, Albert
A, Cloix C, Jenkins GI, Oakeley EJ et al (2009). Interaction of
COP1 and UVR8 regulates UV-B-induced photomorphogenesis
and stress acclimation in Arabidopsis. EMBO J, 28 (5): 591~601
Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L,
Yu L, lglesias-Pedraz JM, Kircher S et al (2008). Coordinated
regulation of Arabidopsis thaliana development by light and
gibberellins. Nature, 451 (7177): 475~479
Foo E, Platten JD, Weller JL, Reid JB (2006). PhyA and cry1 act re-
dundantly to regulate gibberellin levels during de-etiolation in
blue light. Physiol Plant, 127 (1): 149~156
Folta KM, Spalding EP (2001). Unexpected roles for cryptochrome
2 and phototropin revealed by high-resolution analysis of blue
light-mediated hypocotyl growth inhibition. Plant J, 26 (5):
471~478
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P,
Breen G, Cohen JD et al (2011). Phytochrome-interacting factor
4 (PIF4) regulates auxin biosynthesis at high temperature. Proc
Natl Acad Sci USA, 108 (50): 20231~20235
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H
(1997). Cellular basis of hypocotyl growth in Arabidopsis thali-
ana. Plant Physiol, 114 (1): 295~305
Gray WM, Östin A, Sandberg G, Romano CP, Estelle M (1998). High
temperature promotes auxin-mediated hypocotyl elongation in
Arabidopsis. Proc Natl Acad Sci USA, 95 (12): 7197~7202
Guo H, Ecker JR (2003). Plant responses to ethylene gas are mediated
by SCF (EBF1/EBF2)-dependent proteolysis of EIN3 transcrip-
tion factor. Cell, 115 (6): 667~677
Guzmán P, Ecker JR (1990). Exploiting the triple response of Ara-
bidopsis to identify ethylene-related mutants. Plant Cell, 2 (6):
513~523
Haga K, Sakai T (2012). PIN auxin efflux carriers are necessary for
pulse-induced but not continuous light-induced phototropism in
Arabidopsis. Plant Physiol, 160 (2): 763~776
Haga K, Takano M, Neumann R, Iino M (2005). The rice COLEOP-
TILE PHOTOTROPISM1 gene encoding an ortholog of Ara-
bidopsis NPH3 is required for phototropism of coleoptiles and
lateral translocation of auxin. Plant Cell, 17 (1): 103~115
Han IS, Tseng TS, Eisinger W, Briggs WR (2008). Phytochrome A
regulates the intracellular distribution of phototropin 1-green
fluorescent protein in Arabidopsis thaliana. Plant Cell, 20 (10):
2835~2847
Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K,
Watahiki MK, Yamamoto K, Liscum E (2000). The NPH4 locus
encodes the auxin response factor ARF7, a conditional regulator
of differential growth in aerial Arabidopsis tissue. Plant Cell, 12
(5): 757~770
Hohm T, Preuten T, Fankhauser C (2013). Phototropism: translating
light into directional growth. Am J Bot, 100 (1): 47~59
Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K,
López-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M,
Pradervand S et al (2012). Phytochrome interacting factors 4 and
5 control seedling growth in changing light conditions by direct-
ly controlling auxin signaling. Plant J, 71 (5): 699~711
Hua J, Meyerowitz EM (1998). Ethylene response are negatively reg-
ulated by a receptor gene family in Arabidopsis thaliana. Cell,
94 (2): 261~271
Inada S, Ohgishi M, Mayama T, Okada K, Sakai T (2004). RPT2 is a
signal transducer involved in phototropic response and stomatal
opening by association with phototropin 1 in Arabidopsis thali-
ana. Plant Cell, 16 (4): 887~896
Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimaza-
ki K (2008). Blue light-induced autophosphorylation of pho-
totropin is a primary step for signaling. Proc Natl Acad Sci USA,
105 (14): 5626~5631
Jeong J, Choi G (2013). Phytochrome-interacting factors have both
shared and distinct biological roles. Mol Cells, 35 (5): 371~380
Jia KP, Luo Q, He SB, Lu XD, Yang HQ (2014). Strigolactone-reg-
ulated hypocotyl elongation is dependent on cryptochrome and
phytochrome signaling pathways in Arabidopsis. Mol Plant, 7 (3):
528~540
Kaiserli E, Sullivan S, Jones MA, Feeney KA, Christie JM (2009).
Domain swapping to assess the mechanistic basis of Arabidopsis
姜楠等: 拟南芥下胚轴伸长与向光性的分子调控机理 1443
phototropin 1 receptor kinase activation and endocytosis by blue
light. Plant Cell, 21 (10): 3226~3244
Kami C, Allenbach L, Zourelidou M, Ljung K, Schütz F, Isono E,
Watahiki MK, Yamamoto KT, Schwechheimer C, Fankhauser
C (2014). Reduced phototropism in pks mutants may be due to
altered auxin-regulated gene expression or reduced lateral auxin
transport. Plant J, 77 (3): 393~403
Kami C, Hersch M, Trevisan M, Genoud T, Hiltbrunner A, Bergmann
S, Fankhauser C (2012). Nuclear phytochrome A signaling pro-
motes phototropism in Arabidopsis. Plant Cell, 24 (2): 566~576
Kang B, Grancher N, Koyffmann V, Lardemer D, Burney S, Ahmad
M (2008). Multiple interactions between cryptochrome and pho-
totropin blue-light signalling pathways in Arabidopsis thaliana.
Planta, 227 (5): 1091~1099
Khanna R, Shen Y, Marion CM, Tsuchisaka A, Theologis A, Schäfer E,
Quail PH (2007). The basic helix-loop-helix transcription factor
PIF5 acts on ethylene biosynthesis and phytochrome signaling
by distinct mechanisms. Plant Cell, 19 (12): 3915~3929
Kunihiro A, Yamashino T, Mizuno T (2010). PHYTOCHROME-IN-
TERACTING FACTORS PIF4 and PIF5 are implicated in the
regulation of hypocotyl elongation in response to blue light
in Arabidopsis thaliana. Biosci Biotechnol Biochem, 74 (12):
2538~2541
Lariguet P, Schepens I, Hodgson D, Pedmale UV, Trevisan M, Kami
C, de Carbonnel M, Alonso JM, Ecker JR, Liscum E et al (2006).
PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1
binding protein required for phototropism. Proc Natl Acad Sci
USA, 103 (26): 10134~10139
Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle
M (1993). Arabidopsis auxin-resistance gene AXR1 encodes a
protein related to ubiquitin-activating enzyme E1. Nature, 364
(6433): 161~164
Leivar P, Monte E (2014). PIFs: Systems integrators in plant develop-
ment. Plant Cell, 26 (1): 56~78
Leivar P, Monte E, Cohn MM, Quail PH (2012). Phytochrome sig-
naling in green Arabidopsis seedling: impact assessment of a
mutually negative phyB-PIF feedback loop. Mol Plant, 5 (3):
734~749
Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, Huq E, Quail
PH (2008). Multiple phytochrome-interacting bHLH transcrip-
tion factors repress premature seedling photomorphogenesis in
darkness. Curr Biol, 18 (23): 1815~1823
Liscum E, Briggs WR (1996). Mutations of Arabidopsis in potential
transduction and response components of the phototropic signal-
ing pathway. Plant Physiol, 112 (1): 291~296
Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C,
Cole BJ, Ivans LJ, Pedmale UV, Jung HS et al (2012). Linking
photoreceptor excitation to changes in plant architecture. Genes
Dev, 26 (8): 785~790
Liu Z, Zhang Y, Liu R, Hao H, Wang Z, Bi Y (2011). Phytochrome
interacting factors (PIFs) are essential regulators for sucrose-in-
duced hypocotyl elongation in Arabidopsis. J Plant Physiol, 168
(15): 1771~1779
Maharjan PM, Choe S (2011). High temperature stimulates DWARF4
(DWF4) expression to increase hypocotyl elongation in Arabi-
dopsis. J Plant Physiol, 54 (6): 425~429
Möglich A, Yang X, Ayers RA, Moffat K (2010). Structure and func-
tion of plant photoreceptors. Annu Rev Plant Biol, 61: 21~47
Möller B, Schenck D, Lüthen H (2010). Exploring the link between
auxin receptors, rapid cell elongation and organ tropisms. Plant
Signal Behav, 5 (5): 601~603
Motchoulski A, Liscum E (1999). Arabidopsis NPH3: a NPH1 photo-
receptor-interacting protein essential for phototropism. Science,
286 (5441): 961~964
Nagashima A, Suzuki G, Uehara Y, Saji K, Furukawa T, Koshiba T,
Sekimoto M, Fujioka S, Kuroha T, Kojima M et al (2008). Phy-
tochromes and cryptochromes regulate the differential growth
of Arabidopsis hypocotyls in both a PGP19-dependent and a
PGP19-independent manner. Plant J, 53 (3): 516~529
Noh B, Bandyopadhyay A, Peer WA, Spalding EP, Murphy AS (2003).
Enhanced gravi- and phototropism in plant mdr mutants mis-
localizing the auxin efflux protein PIN1. Nature, 423 (6943):
999~1002
Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer
SL, Maloof JN (2007). Rhythmic growth explained by coinci-
dence between internal and external cues. Nature, 448 (7151):
358~361
Oh E, Zhu JY, Wang ZY (2012). Interaction between BZR1 and PIF4
integrates brassinosteroid and environmental responses. Nat Cell
Biol, 14 (8): 802~809
Parks BM, Cho MH, Spalding EP (1998). Two genetically separable
phases of growth inhibition induced by blue light in Arabidopsis
seedlings. Plant Physiol, 118 (2): 609~615
Parks BM, Quail PH, Hangarter RP (1996). Phytochrome A regulates
red-light induction of phototropic enhancement in Arabidopsis.
Plant Physiol, 110 (1): 155~162
Pedmale UV, Liscum E (2007). Regulation of phototropic signaling
in Arabidopsis via phosphorylation state changes in the pho-
totropin 1-interacting protein NPH3. J Biol Chem, 282 (27):
19992~20001
Reed JW, Elumalai RP, Chory J (1998). Suppressors of an Arabidopsis
thaliana phyB mutation identify genes that control light signal-
ing and hypocotyl elongation. Genetics, 148 (3): 1295~1310
Roberts D, Pedmale UV, Morrow J, Sachdev S, Lechner E, Tang X,
Zheng N, Hannink M, Genschik P, Liscum E (2011). Modulation
of phototropic responsiveness in Arabidopsis through ubiquiti-
nation of phototropin 1 by the CUL3-ring E3 ubiquitin ligase
CRL3 (NPH3). Plant Cell, 23 (10): 3627~3640
Sakai T, Haga K (2012). Molecular genetic analysis of phototropism
in Arabidopsis. Plant Cell Physiol, 53 (9): 1517~1534
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR,
Wada M, Okada K (2001). Arabidopsis nph1 and npl1: blue light
receptors that mediate both phototropism and chloroplast reloca-
tion. Proc Natl Acad Sci USA, 98 (12): 6969~6974
Sakai T, Wada T, Ishiguro S, Okada K (2000). RPT2: A signal trans-
ducer of the phototropic response in Arabidopsis. Plant Cell, 12
(2): 225~236
Sakamoto K, Briggs WR (2002). Cellular and subcellular localization
植物生理学报1444
of phototropin 1. Plant Cell, 14 (8): 1723~1735
Shen H, Zhu L, Castillon A, Majee M, Downie B, Huq E (2008).
Light-induced phosphorylation and degradation of the negative
regulator PHYTOCHROME-INTERACTING FACTOR1 from
Arabidopsis depend upon its direct physical interactions with
photoactivated phytochromes. Plant Cell, 20 (6): 1586~1602
Shen Y, Khanna R, Carle CM, Quail PH (2007). Phytochrome induces
rapid PIF5 phosphorylation and degradation in response to red-
light activation. Plant Physiol, 145 (3): 1043~1051
Smalle J, Haegman M, Kurepa J, Van Montagu M, Straeten DV (1997).
Ethylene can stimulate Arabidopsis hypocotyl elongation in the
light. Proc Natl Acad Sci USA, 94 (6): 2756~2761
Somers DE, Schultz TF, Milnamow M, Kay SA (2000). ZEITLUPE
encodes a novel clock-associated PAS protein from Arabidopsis.
Cell, 101 (3): 319~329
Stone BB, Stowe-Evans EL, Harper RM, Celaya RB, Ljung K, Sand-
berg G, Liscum E (2008). Disruptions in AUX1-dependent auxin
influx alter hypocotyl phototropism in Arabidopsis. Mol Plant, 1
(1): 129~144
Sun J, Qi L, Li Y, Zhai Q, Li C (2013). PIF4 and PIF5 transcription
factors link blue light and auxin to regulate the phototropic re-
sponse in Arabidopsis. Plant Cell, 25 (6): 2102~2114
Sun J, Qi L, Li Y, Chu J, Li C (2012). PIF4 – mediated activation of
YUCCA8 expression integrates temperature into the auxin path-
way in regulating Arabidopsis hypocotyl growth. PLoS Genet, 8
(3): e1002594
Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM,
Liscum E, Yamamoto KT (2004). MASSUGU2 encodes Aux/
IAA19, an auxin-regulated protein that functions together with
the transcriptional activator NPH4/ARF7 to regulate differential
growth responses of hypocotyl and formation of lateral roots in
Arabidopsis thaliana. Plant Cell, 16 (2): 379~393
Toledo-Ortiz G, Huq E, Quail PH (2003). The Arabidopsis basic/
helix-loop-helix transcription factor family. Plant Cell, 15 (8):
1749~1770
Tseng TS, Briggs WR (2010). The Arabidopsis rcn1-1 mutation im-
pairs dephosphorylation of Phot2, resulting in enhanced blue
light responses. Plant Cell, 22 (2): 392~402
Tsuchida-Mayama T, Sakai T, Hanada A, Uehara Y, Asami T, Yama-
guchi S (2010). Role of the phytochrome and cryptochrome
signaling pathways in hypocotyl phototropism. Plant J, 62 (4):
653~662
Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec
J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M et al
(2009). ABCB19/PGP19 stabilises PIN1 in membrane micro-
domains in Arabidopsis. Plant J, 57 (1): 27~44
Vandenbussche F, Verbelen JP, Van Der Straeten D (2005). Of light
and length: regulation of hypocotyl growth in Arabidopsis. Bio-
essays, 27 (3): 275~284
Wan YL, Eisinger W, Ehrhardt D, Kubitscheck U, Baluska F, Briggs
W (2008). The subcellular localization and blue-light-induced
movement of phototropin 1-GFP in etiolated seedlings of Arabi-
dopsis thaliana. Mol Plant, 1 (1): 103~117
Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S,
Baluska F, Lin J (2012). The signal transducer NPH3 integrates
the phototropin 1 photosensor with PIN2-based polar auxin
transport in Arabidopsis root phototropism. Plant Cell, 24 (2):
551~565
Willige BC, Ahlers S, Zourelidou M, Barbosa IC, Demarsy E, Trevis-
an M, Davis PA, Roelfsema MR, Hangarter R, Fankhauser C et
al (2013). D6PK AGCVIII kinases are required for auxin trans-
port and phototropic hypocotyl bending in Arabidopsis. Plant
Cell, 25 (5): 1674~1688
Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P,
Deng H, Wang J et al (2012). Structural basis of ultraviolet-B
perception by UVR8. Nature, 484 (7393): 214~219
Yang HQ, Wu YJ, Tang RH, Liu D, Liu Y, Cashmore AR (2000). The
C termini of Arabidopsis crytochromes mediate a constitutive
light response. Cell, 103 (5): 815~827
Zhang KX, Xu HH, Yuan TT, Zhang L, Lu YT (2013). Blue light-in-
duced PIN3 polarization for root negative phototropic response
in Arabidopsis. Plant J, 76 (2): 308~321
Zhao X, Wang YL, Qiao XR, Wang J, Wang LD, Xu CS, Zhang X
(2013). Phototropins function in high-intensity blue light-in-
duced hypocotyl phototropism in Arabidopsis by altering cytoso-
lic calcium. Plant Physiol, 162 (3): 1539~1551
Zhong S, Shi H, Xue C, Wei N, Guo H, Deng XW (2014). Eth-
ylene-orchestrated circuitry coordinates a seedlings response to
soil cover and etiolated growth. Proc Natl Acad Sci USA, 111
(11): 3913~3920
Zhong S, Shi H, Xue C, Wang L, Xi Y, Li J, Quail PH, Deng XW, Guo
H (2012). A molecular framework of light-controlled phytohor-
mone action in Arabidopsis. Curr Biol, 22 (16): 1530~1535
Zhou XY, Song L, Xue HW (2013). Brassinosteroids regulate the
differential growth of Arabidopsis hypocotyls through auxin sig-
naling components IAA19 and ARF7. Mol Plant, 6 (3): 887~904
Zourelidou M, Müller I, Willige BC, Nill C, Jikumaru Y, Li H,
Schwechheimer C (2009). The polarly localized D6 PROTEIN
KINASE is required for efficient auxin transport in Arabidopsis
thaliana. Development, 136 (2009): 627~636