全 文 ：植物学报 Chinese Bulletin of Botany 2015, 50 (2): 241–254, www.chinbullbotany.com
doi: 10.3724/SP.J.1259.2015.00241
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收稿日期: 2014-08-06; 接受日期: 2014-11-02
基金项目: 国家自然科学基金(No.91017002, No.31070247, No.31271460)
* 通讯作者。E-mail: housw@lzu.edu.cn
光敏色素信号通路中磷酸化修饰研究进展
岳晶, 管利萍, 孟思远, 张静, 侯岁稳*
兰州大学生命科学学院, 细胞活动与逆境适应教育部重点实验室, 兰州 730000
摘要 光是植物的唯一能量来源, 植物在进化过程中产生不同的光敏色素来感知光信号。光信号通路中元件通常被特异翻译
后修饰调节。光敏色素是一种自磷酸化的丝氨酸/苏氨酸蛋白激酶, 可以被一些蛋白磷酸酶去磷酸化。通过对光敏色素A
(phyA)和光敏色素B (phyB)的自磷酸化位点研究, 发现自磷酸化对光敏色素的功能及其介导的信号通路起着非常重要的作
用。光激活的光敏色素诱导光敏色素作用因子(PIF)磷酸化, 这对于PIF的正常降解及光形态建成的起始是必需的。该文主
要介绍了光敏色素信号通路磷酸化修饰的最新进展, 以期为深入研究光敏色素信号转导机制提供参考。
关键词 光敏色素, 光敏色素作用因子, 磷酸化修饰
岳晶, 管利萍, 孟思远, 张静, 侯岁稳 (2015). 光敏色素信号通路中磷酸化修饰研究进展. 植物学报 50, 241–254.
植物种子萌发后, 在生长发育过程中需要适应多
种环境因子, 包括温度、光、湿度和盐度等。在这些
因子中, 光最为重要。植物依赖光受体接收不同的光,
光敏色素(phytochrome, phy)作为红光/远红光受体
接受光信号后, 将其传递到核内光响应因子, 最终调
控植物的光形态建成。在光信号通路中, 磷酸化和去
磷酸化作为一种重要的翻译后修饰被广泛研究。本文
基于前人的研究成果, 对光敏色素信号通路的磷酸化
修饰进行了综述和讨论。
1 光敏色素调控植物发育
光敏色素作为一类光受体, 以红光/远红光(R/FR)依
赖的形式存在。在模式植物拟南芥 (Arabidopsis
thaliana)中, 光敏色素调控3 000多个基因的表达,
并且在植物适应光环境的急剧变化中起非常重要的
作用(Chen et al., 2004)。光敏色素是植物体内合成的
一种调节生长发育的蛋白, 含2个主要结构域: N端感
光区和信号区及C端二聚化区和定位区(又称光调节
区) (Rockwell et al., 2006; Fankhauser and Chen,
2008; Nagatani, 2010; Ulijasz et al., 2010)。光感受
区和光调节区通过铰链区连接在一起(王静和王艇,
2007)。phys以2种相对稳定的形式存在: 红光吸收无
活性形式Pr和远红光吸收激活形式Pfr。有活性的光敏
色素A (phyA)和光敏色素B (phyB)可以与一些特异的
细胞分子相互作用, 这对于它们转运到细胞核内是
必需的(Hiltbrunner et al., 2005; Rockwell et al.,
2006; Pfeiffer et al., 2012)。在此互作过程中光敏色
素信号被级联传递(Bae and Choi, 2008), 表明有活
性的光敏色素分子与细胞分子间的相互作用程度决
定了光敏色素信号的强弱。在拟南芥中, phys家族包
括5个成员, 即从phyA到phyE, 它们可以相互形成同
源和异源二聚体(Clack et al., 2009)。phyA和phyB是
最主要的光敏色素, 参与调节植物生长发育的各个方
面(Franklin and Quail, 2010; Kami et al., 2010)。
phyA作为一种远红光感受器, 调节从暗形态建成到
光形态建成的转变。phyB作为红光调节分子开关, 在
红光信号通路中起着非常关键的作用(Nagy and Schä-
fer, 2002)。光敏色素不同的作用模式为黄化幼苗在远
红光或者红光下产生不同的形态学响应提供了一定
的分子基础。
在拟南芥中, 发现了许多与光敏色素信号分子相
关的突变体(Chory, 2010)。这些光形态突变体可以分
成2大类。第1类突变体表现去黄化和持续光形态表
型, 包括下胚轴短、子叶膨大和部分叶绿体分化, 以
及在黑暗条件下光诱导基因的表达去抑制等。这些突
变体包括de-etiolated 1 (det1) (Chory et al., 1989)、
constitutively photomorphogenic 1 (cop1) (Deng et
·专题论坛·
242 植物学报 50(2) 2015

al., 1991)、COP9的信号组分突变体 (Serino and
Deng, 2003)、suppressor of phytochrome A-1051-4
(spa1-4) (Laubinger et al., 2004)和phytochrome in-
teracting factors 1,3,4,5 (pifQ) (Leivar et al., 2008b,
2009; Shin et al., 2009)。鉴于它们的基因突变都是
隐性的, 被定义为光信号通路中的负向调节组分。此
外, 这些突变体的表型与组成型激活phyB等位基因
的突变体YHB (Y276H mutant of phyB)非常相似(Su
and Lagarias, 2007; Hu et al., 2009), 表明phys通过
抑制这些负调节子来启动光形态建成。
第2类突变体表型都与phyA和phyB功能缺失突
变体类似, 在光下均表现出下胚轴变长和子叶紧闭表
型, 这些突变体在phyA或phyB信号中存在缺陷, 或
者在2个信号通路中都存在缺陷。例如: far-red elon-
gated hypocotyl 1 (fhy1) (Whitelam et al., 1993;
Desnos et al., 2001)、fhy3 (Whitelam et al., 1993;
Wang and Deng, 2002)、long after far-red light 1
(laf1) (Ballesteros et al., 2001)、far-red impaired
response 1 (far1) (Hudson et al., 1999)和long hy-
pocotyl in far-red 1 (hfr1) (Fairchild et al., 2000)等,
在phyA信号通路中存在缺陷, 而the elongated hy-
pocotyl 5 (hy5)突变体在phyA和phyB信号通路中都
表现出缺陷(Koornneef et al., 1980; Oyama et al.,
1997)。最近报道的hemera (hmr)是一种新的phy信号
突变体, 它不仅在红光和远红光下表现出长的下胚
轴, 而且在叶绿体发育方面也存在缺陷(Chen et al.,
2010)。由于HMR在细胞核和叶绿体都有定位, 所以
可能是一个双重功能蛋白。
上述2类突变体中许多基因编码光响应基因的转
录调节子, 包括正向调节因子(HY5、LAF1、HFR1、
FHY3和FAR1)和负向调节因子(PIFs)。光敏色素调节
转录调节子的稳定性是调节基因表达的一个关键机
制(Chen and Chory, 2011)。
2 光敏色素磷酸化修饰在光信号通路中
的作用
2.1 phyA的磷酸化与去磷酸化作用
光敏色素是一类光调节的His激酶(Yeh et al., 1997)。
自磷酸化的燕麦(Avena sativa) phyA在体外是由生
色团调节的(Yeh and Lagarias, 1998)。通过研究纯化
的光敏色素提取物, Hunt和Pratt (1980)发现光敏色
素是一类磷蛋白。另有学者对燕麦幼苗进行了研究,
鉴定出光敏色素的3个磷酸化位点 (Lapko et al.,
1996, 1997, 1999)。其中, 2个磷酸化位点(Ser8和
Ser18)位于phyA的N端延伸区(N-terminal extension,
NTE); 另一个位点(Ser598)位于N端和C端之间的铰
链区域。通过比对单子叶和双子叶植株中phyA的这3
个磷酸化位点 , 发现它们很保守 (图1)。Cherry等
(1992)报道NTE区域对于phyA的生物活性是必需的。
将NTE区域的Ser8和Ser18位点替代为Ser8Ala和
Ser18Ala可以抑制phyA的磷酸化作用 , 从而增强
phyA的生物活性。在转基因植物中表达这2个突变的
phyA蛋白, 植株表现出对远红光敏感, 并且出现矮
化表型(Stockhaus et al., 1992)。这些研究结果说明,
NTE区域的磷酸化导致了phyA信号衰减, 是光敏色
素信号转导的脱敏过程(Emmler et al., 1995; Jordan
et al., 1996, 1997; Casal et al., 2002), 但是这些磷
酸化位点的替代使得信号衰减的机制仍不清楚。Han
等(2010)的研究发现模拟持续磷酸化的phyASer8-
Asp和phyASer18Asp在植物中的降解速率变快。对
水稻(Oryza sativa)中phyA的研究表明, 水稻phyA N
端区域的Ser替换为Ala后转入烟草 (Nicotiana ta-
bacum), 同样可以导致转基因烟草对远红光非常敏
感(Stockhaus et al., 1992)。该结果可以进一步解释
为什么在拟南芥中将phyA的Ser8和Ser18位点模拟
磷酸化, 可以减弱远红光调控的光响应, 而模拟去磷
酸化的效应正好相反。
将燕麦phyA的另一个磷酸化位点Ser598替换为
Ala的转基因植株phyAser598Ala是一种有活性的特
异性磷酸化位点突变体, 它对光表现出非常强的敏感
性, 说明光敏色素Ser598位点磷酸化对于植物的光
敏感性起抑制作用。有研究表明, phyA在体外被PKA
(protein kinase A)催化发生磷酸化后, 其蛋白光谱和
构象都没有发生变化(Lapko et al., 1996)。同时检测
野生型燕麦phyA与phyASer598Ala中phyA的降解,
发现蛋白降解也没有变化, 说明Ser598Ala替换并不
影响phyA的蛋白降解。在黑暗条件下燕麦phyA-GFP
与phyAser598Ala-GFP没有表现出核定位, 在红光
条件下, 2种phyA-GFP融合蛋白都表现出核定位, 并
且形成核斑点, 这些核斑点之间没有定性和定量的变
化。这些研究结果表明, Ser598Ala突变没有影响phyA
岳晶等: 光敏色素信号通路中磷酸化修饰研究进展 243

光诱导的入核以及核斑点的形成。虽然phyAser598Ala
仍然保持自磷酸化能力 , 但是phyA突变为phyA-
ser598Ala后会影响其与nucleoside-diphosphate
kinases (NDPK2)的相互作用(Choi et al., 1999), 同


图1
Figure 1
244 植物学报 50(2) 2015


图1 单子叶和双子叶植物中phyA蛋白的多序列对比
At: 拟南芥phyA; As: 燕麦phyA; As3: 燕麦phyA 3型; Os: 水稻phyA; Hv: 大麦亚种phyA; Ta: 小麦phyA 1型; Bd: 二穗短柄草
phyA 3型; Zm: 玉米phyA; Sb: 高粱phyA; Sp: 拟高粱phyA; St: 马铃薯phyA。*表示燕麦phyA中已鉴定的磷酸化位点Ser8、Ser18
和Ser598

Figure 1 Multiple sequence alignments of monocot and dicot phyA proteins
At: Arabidopsis thaliana phyA; As: Avena sativa phyA; As: Avena sativa phyA type 3; Os: Oryza sativa phyA; Hv: Hordeum vul-
gare subsp. vulgare phyA; Ta: Triticum aestivum phyA type 1; Bd: Brachypodium distachyon phyA type 3-like; Zm: Zea mays
phyA; Sb: Sorghum bicolor phyA; Sp: Sorghum propinquum phyA; St: Solanum tuberosum phyA. * indicates phosphorylation
sites at Ser8, Ser18 and Ser598 identified in oat phyA
岳晶等: 光敏色素信号通路中磷酸化修饰研究进展 245



时光敏色素的磷酸化还影响其与PIF3的相互作用
(Kim et al., 2004)。phyA铰链区位点处于去磷酸化时
与下游转导子的结合比较强, 当该位点被磷酸化后,
这种结合能力显著降低(图2), 说明光敏色素的铰链
区作为一个磷酸化信号调节位点调控phyA与信号分
子之间的相互作用(Kim et al., 2004)。
在拟南芥中已发现phyA可以被磷酸化并且phyA
的磷酸化可以调节其与COP1/SPA1和FHY1/FHY3
的聚集(Saijo et al., 2008), 但是这些功能的重要性
还不是很清楚。与燕麦和水稻phyA类似 , 拟南芥
phyA N端区域对于信号的传递也非常重要(Cherry et
al., 1992; Jordan et al., 1997), 但是分析拟南芥
phyA N端突变体并没有发现磷酸化可以调节燕麦
phyA信号。在拟南芥中, 将野生型燕麦PHYA转入
phyA-201突变体中, 发现它可以恢复phyA的缺陷表
型, 将突变的燕麦PHYAser598Ala转入phyA-201突
变体, 发现转基因植株表现出对光非常敏感, 说明光
敏色素在铰链区Ser598位点发生磷酸化存在一种抑
制机制(Kim et al., 2004)。但是目前还没有证据证实
拟南芥中Ser598位点的具体功能, 所以还需要深入
研究拟南芥phyA磷酸化对其信号通路的影响。
目前, 对于植物phyA是否磷酸化其它蛋白还有
相当多的争议。体外证据表明 , phyA可以磷酸化
_____________________________________________
←

图2 光敏色素信号通路的磷酸化修饰模式图(Ryu et al., 2005;
Galvão et al., 2012)
(A) 燕麦phyA结构域和磷酸化位点。N端结构域(N)和C端结构
域(COOH)用矩形表示 , Φ表示植物后胆色素 , 它与氨基酸
Cys321 (C321)共价连接。中间的小矩形表示铰链区(H), 中间
箭头指示的位置为铰链区域一个磷酸化位点Ser598。目前已经
报道燕麦phyA有3种翻译后修饰: N-乙酰化(Ac-N), 植物后胆色
素连接到phyA 321位的半胱氨酸上以及磷酸化N端区域的第7
位丝氨酸。光敏色素的自磷酸化位点在N端区域(Lapko et al.,
1999); (B) 光促使无活性的光敏色素转变为有活性的光敏色
素, 从而开启了光敏色素调节的光信号, 有活性的光敏色素可
以自磷酸化以及被一些光敏色素相关的激酶磷酸化。磷酸化的
光敏色素会被一些磷酸酶(PAPP5和PAPP2C)去磷酸化。有活
性的光敏色素在N端和铰链区被去磷酸化从而缓解了磷酸化介
导的去稳定作用, 进而与下游信号分子结合能力增强, 而没有
磷酸化的有活性的光敏色素反之。此外, 磷酸化的没有活性的
光敏色素与下游信号分子结合能力非常低。这些机制导致下游
PIF存在2种状态, 一种是PIF被光敏色素磷酸化从而负向调控
光信号; 另一种是光敏色素由于被去磷酸化所以不能磷酸化
PIF, 最终导致正向调节光信号。

Figure 2 A proposed model of phosphorylation modification
in the phytochrome signaling pathway (Ryu et al., 2005;
Galvão et al., 2012)
(A) Domain structure and phosphorylation sites in oat phyA.
The N-terminal (N) and C-terminal domains (COOH) are
shown by rectangles. Φ indicates phytochromobilin, cova-
lently attached to Cys321 (C321). The middle of the small
rectangle represents “hinge region (H)”, the phosphorylation
site at Ser598 is shown by arrow in the middle. Three types of
posttranslational modification of oat phyA have been reported
previously: N-acetylation (ac-N), phytochromobilin ligation to
Cys321 and phosphorylation in the N-terminal region at Ser7.
Phosphorylation at the N-terminus was suggested to be the
site of phytochrome “autophosphorylation” (Lapko et al.,
1999); (B) Light triggers photoconversion of the Pr-phyto-
chromes to the Pfr-phytochromes, which initiates the phyto-
chrome-mediated photosignaling. Pfr-phytochromes are pho-
sphorylated by their intrinsic kinase activity as well as by
phytochromes-associated kinase(s) and are reversibly
dephosphorylated by phosphatase, such as, PAPP5, PAP-
P2C. The Pfr-phytochromes dephosphorylates in the N-ter-
minal extension and the hinge region is relieved from phosphory-
lation mediated destabilization, exhibiting a high affinity to signal
transducers. However, the unphosphorylated Pfr-phytochromes
were not. Furthermore, the phosphorylated Pr-phytochromes
possess a very lower affinity toward signal transducers. These
mechanisms lead to the existence of two state of PIF. One is PIF
was phosphorylated by phytochromes results in the negative
regulation of light signaling. Another is phytochromes were
dephosphorylated and could not phosphorylate PIF, which results
in the positive regulation of light signaling.
246 植物学报 50(2) 2015


图3
Figure 3
岳晶等: 光敏色素信号通路中磷酸化修饰研究进展 247


图3 单子叶和双子叶植物中phyB蛋白的多序列对比
At: 拟南芥phyB; As: 燕麦phyB; Os: 水稻phyB; Hv: 大麦亚种phyB; Ta: 小麦phyB; Bd: 二穗短柄草类phyB; Zm: 玉米phyB 2;
Sb: 高粱phyB; Sp: 拟高粱phyB; St: 马铃薯phyB。*表示拟南芥phyB中已鉴定的磷酸化位点Ser86和Tyr104

Figure 3 Multiple sequence alignments of monocot and dicot phyB proteins
At: Arabidopsis thaliana phyB; As: Avena sativa phyB; Os: Oryza sativa phyB; Hv: Hordeum vulgare subsp. vulgare phyB; Ta:
Triticum aestivum putative phyB; Bd: Brachypodium distachyon phyB-like; Zm: Zea mays phyB 2; Sb: Sorghum bicolor phyB; Sp:
Sorghum propinquum phyB; St: Solanum tuberosum phyB. * indicates phosphorylation sites at Ser86 and Tyr104 identified in
Arabidopsis phyB

cryptochrome1 (Cry1)、phytochrome kinase sub-
strate 1 (PKS1)和auxin/indole-3-acetic acid (Aux/
IAA), 但是还没有在植物中证明这些结论(Ahmad et
al., 1998; Fankhauser et al., 1999; Colón-Carmona
et al., 2000)。对于拟南芥phyA的磷酸化作用, 最近
研究表明 , 一个光诱导phyA入核的关键调节子
FHY1, 在R/FR光转换过程中被磷酸化, 在红光下磷
酸化FHY1需要phyA参与(Shen et al., 2009; Chen et
al., 2012), 同时磷酸化FHY1降低了有活性形式的
phyA入核速率及phyA与HY5和PIF3的相互作用, 结
果导致phyA在远红光下转录复合体的组装失活
(Yang et al., 2009; Chen et al., 2012)。这些结果说
明, phyA磷酸化其它蛋白对其信号传递非常重要。
目前, 有研究表明, 一些蛋白可以与phyA相互
作用并去磷酸化phyA, 这些蛋白包括flower-specific
phytochrome-associated protein phosphatase (Fy-
PP) (Kim et al., 2002)、phytochrome-associated pro-
tein phosphatase type 2C (PAPP2C) (Phee et al.,
2008)和phytochrome-associated protein phospha-
tase 5 (PAPP5) (Ryu et al., 2005)。转基因植株超表
达FyPP后在开花和下胚轴伸长方面增强了光敏色素
活性, 抑制FyPP表达则导致转基因植株中光敏色素
活性降低(Kim et al., 2002)。phy与PIF3在细胞核内
相互作用并将PIF3磷酸化从而负向调节光信号, 而
PAPP2C可以与phyA相互作用并将phyA去磷酸化,
这个互作优先于phyA与PIF3的结合, 从而导致PIF3
不能被磷酸化 , 最终对光信号通路起正调节作用
(Phee et al., 2008)。PAPP5是一类5型磷酸酶, 其与
燕麦phyA结合形成一类特殊的构象, 可以对phyA的
3个已知磷酸化位点进行去磷酸化, 从而调节幼苗的
去黄化, 影响phyA蛋白的稳定性, 并且去磷酸化的
燕麦phyA增加了其与NDPK2和PIF3的结合能力。在
拟南芥中超表达磷酸酶PAPP5可导致其对远红光敏
感, papp-5突变体则表现出对远红光敏感性降低(Ryu
et al., 2005)。这些发现证明, phyA的去磷酸化在光敏
色素调节的光信号通路中起重要作用。
2.2 phyB的磷酸化与去磷酸化作用
相比phyA, 目前关于phyB磷酸化的研究较少。研究
发现, PAPP5无义突变体papp-5对红光敏感, PAPP5
磷酸酶在体外pull-down实验中可以与phyB相互作
用, 并且在转基因植株中phyB与PAPP5共定位在光
体中。进一步实验证明 , phyB作为PAPP5的底物,
PAPP5在体外可以将phyB去磷酸化 (Ryu et al.,
2005)。随后有许多报道表明, phyB与另一类磷酸酶
PAPP2C在体外也可以相互作用, 并且这个磷酸酶优
先与有活性的phyB相互作用 , 在红光照射下PA-
PP2C与phyB共定位于细胞核内, 在黑暗条件下则无
此现象。自磷酸化的phyB可以被PAPP2C去磷酸化,
并且缺失突变体papp2c对红光响应降低(Phee et al.,
248 植物学报 50(2) 2015

2008)。这些结果说明, 可逆磷酸化在phyB调节的信
号通路和光形态建成中起重要作用。
最近, Ferenc Nagy实验室通过质谱实验发现了
拟南芥phyB的磷酸化位点, 证明了phyB在植物体内
能被磷酸化。无论在黑暗或红光条件下, phyB N端的
Ser86位点都可被磷酸化。通过比对单子叶和双子叶
植物中phyB的Ser86位点, 发现该位点在不同物种中
是高度保守的 (图3)。通过研究模拟磷酸化植株
phyBSer86Asp-YFP, 发现其对红光比较敏感, 但是这
种敏感度的差异, 仅在低强度的红光下比较明显。在
phyB中Ser86替换为Ala或Asp并没有改变这些融合
蛋白的稳定性。研究还发现在体外非饱和光照条件下,
模拟磷酸化的phyB与PIF3的结合能力降低(图2)。同
时, phyBSer86Asp-YFP中光诱导光体在细胞核内的积
累和积聚减少了(Medzihradszky et al., 2013)。目前,
还不清楚是由于phyB的自磷酸化还是由于未知激酶
的作用使phyB磷酸化, 从而显著改变phyB的亚核分
布。上述结果表明, 磷酸化光受体可能会调节光体的
形成(Medzihradszky et al., 2013)。
最近的研究还发现, 在phyB的N端存在一个含有
23个氨基酸残基的区域, 叫做PCSM (phosphoryla-
tion cluster of signaling modulation)区域, 当植物受
到光照后, PCSM区域中许多氨基酸被磷酸化, 这些
位点中除了丝氨酸和苏氨酸外, 还包括一个酪氨酸位
点(Tyr104) (Nito et al., 2013), 该位点在不同物种中
都完全保守(图3)。研究发现在拟南芥中模拟磷酸化的
phyBTyr104Glu不能恢复phyB的相关表型, 并且该突变
蛋白没有phyB活性。phyBTyr104Glu不能与信号分子
PIF3相互结合, 也不能形成稳定的光体。在植株中稳
定表达不能磷酸化的phyBTyr104Phe, 会使植株表现出
对光超敏感。在光环境的急剧变化过程中, 由于植物
适应环境对其存活非常关键 , 所以酪氨酸磷酸化
phyB作为在光信号机制中新发现的一种翻译后修饰,
对研究光敏色素信号通路有非常重要的意义(Nito et
al., 2013)。
3 PIFs的磷酸化修饰
3.1 PIFs转录因子的功能
PIFs是一类bHLH转录因子 , 负向调节光形态建成
(Leivar and Quail, 2011)。1998年, Peter Quail实验
室发现了PIFs家族成员PIF3, 这为全面开展PIFs在
光形态建成中的作用研究奠定了很重要的基础(Ni et
al., 1998)。目前 , 鉴定到的PIFs包括PIF3、PIF1/
PIL5、PIF4、PIF5/PIL6和PIF7, 它们可以与光调节
基因的G-box区域结合, 作为转录激活子或转录抑制
子起作用(Huq and Quail, 2002; Huq et al., 2004; De
Lucas et al., 2008; Leivar et al., 2008b, 2009; Moon
et al., 2008; Hornitschek et al., 2009)。PIFs在光敏
色素介导的光响应中起着不同的作用。在去黄化过程
中, PIF1、PIF3、PIF4、PIF5和PIF7抑制植物的下胚
轴伸长(Huq and Quail, 2002; Fujimori et al., 2004;
Huq et al., 2004; Khanna et al., 2004; Oh et al.,
2004; Al-Sady et al., 2008; Lorrain et al., 2009)。在
叶绿体发育过程中, PIF1、PIF3和PIF5抑制叶绿体的
发育, 下调编码叶绿素关键合成酶基因的表达(Huq
et al., 2004; Moon et al., 2008; Leivar et al., 2009;
Shin et al., 2009; Stephenson et al., 2009)。另外,
PIF1还下调类胡萝卜素的表达(Toledo-Ortiz et al.,
2010)。pifQ突变体在黑暗条件下表现出去黄化的表
型(Hu et al., 2009; Leivar et al., 2009)。这些结果说
明, PIFs家族在黑暗条件下可以促进暗形态建成, 抑
制光形态建成, 且在功能上存在冗余(Leivar et al.,
2008b; Shin et al., 2009)。
3.2 PIF蛋白磷酸化修饰的功能
PIF蛋白的N端区域包含光敏色素的作用区域, C端包
含bHLH DNA结合区域和二聚化区域。N端的保守区
域 , 称为激活phyB结合区域 (the active phytoch-
rome B-binding region, APB), 该区域对于与phyB的
特异性结合是必需的(Khanna et al., 2004)。PIF1和
PIF3包含一个独立的区域称为激活phyA结合区域
(the active phytochrome A-binding region, APA), 该
区域对与phyA的结合是必需的(Al-Sady et al., 2006;
Shen et al., 2008)。PIF1和PIF3能与光敏化的phyA
和phyB结合 (Al-Sady et al., 2006; Shen et al.,
2008), 而PIF4、PIF5、PIF6和PIF7只能与phyB结合
(Ni et al., 1998; Huq et al., 2004; Khanna et al.,
2004; Leivar et al., 2008a)。光激活phys后, phys积
聚在细胞核内与PIFs蛋白相互作用, 使得PIFs被磷
酸化并通过泛素蛋白酶体途径迅速降解(Al-Sady et
al., 2006)。光诱导PIFs磷酸化和降解需要与有活性的
岳晶等: 光敏色素信号通路中磷酸化修饰研究进展 249

phys直接相互作用(Al-Sady et al., 2006; Shen et al.,
2008)。PIF3与光敏化的phys共定位形成光体也需要
与有活性的phys直接相互作用(Bauer et al., 2004;
Al-Sady et al., 2006; Chen and Chory, 2011)。突变
的PIF3蛋白不能与phyA和phyB结合, 所以检测不到
phys诱导的PIF3磷酸化以及降解 (Al-Sady et al.,
2006)。光诱导PIF3磷酸化可以通过检测PIF3迁移率
的变化来证明(Al-Sady et al., 2006)。这些结果表明,
光敏化的phys是介导PIF3磷酸化并最终通过泛素化
途径降解的主要因子。目前, 已经证明PIF1、PIF4和
PIF5在光诱导降解之前都会被磷酸化修饰(Shen et
al., 2007; Lorrain et al., 2008; Shen et al., 2008)。因
此 , 光诱导的PIFs蛋白磷酸化是信号从光敏化的
phys传递到转录因子PIFs最主要的生物学机制。然
而, 目前还不清楚PIFs的磷酸化是哪个激酶在起作
用。最近报道证明 , PIF1可以被CK2 (casein kin-
ase II)以及可能没有发现的激酶磷酸化(Bu et al.,
2011a)。PIF4可以与BZR1 (brassinazole-resistant 1)
相互作用, 它们在响应BR、黑暗以及热激时相互独立
地调控细胞伸长, 并且可以共同调控一些光合激素响
应的基因, 进而证明BZR1-PIF4相互作用, 从而控制
了一个核心的转录网络, 使得植株生长受到甾醇和环
境因子的共同调控(Oh et al., 2012)。但是对于PIF4
通过什么机理与BR信号共同调控下胚轴伸长尚不清
楚。有报道显示BR信号通路中BIN2 (brassinosteroid-
insensitive 2)可以将PIF4磷酸化, 这就找到了PIF4
的一个激酶。研究发现, 转基因植株PIF41A中, PIF4
与BIN2结合区域中的关键位点突变, 结果导致PIF4
不能被BIN2磷酸化, 最终使得植株中PIF4的磷酸化
和降解都明显受到抑制。BR通过抑制BIN2活性拮抗
地参与光信号 , 从而调节PIF4的去稳定性。同时 ,
PIF4的磷酸化对于其调节周期性的下胚轴生长也非
常重要(Bernardo-Garcia et al., 2014)。但截至目前,
已知的可以磷酸化PIFs的激酶还很少, 所以尚需要
进一步研究。
为了更好地分析信号分子从光敏化的phy到PIF
转录因子转移过程的分子本质, 2013年, Quail实验室
找到了PIF3的磷酸化位点, 并将该位点定点突变, 结
果发现当13个磷酸化位点全部突变为Ala时, 突变的
PIF3 (PIF3-A13)表现出明显光诱导的迁移率降低以
及光诱导的降解变慢(Ni et al., 2013)。将其余磷酸化
位点全部突变后, PIF3迁移率降低且降解抑制作用更
明显。同时检测这些转基因植株的泛素化水平, 结果
表明泛素化修饰蛋白的积累需要光诱导的PIF3磷酸
化。PIF3磷酸化位点的突变不能影响其与phyB的结
合, 也不影响其与特异的DNA序列结合。经过红光诱
导后, PIF3与phyB在亚核结构中共定位形成核斑点,
检测PIF3磷酸化位点突变转基因植株PIF3-A14、
PIF3-A20和PIF3-A26, 发现明显存在光体定位, 但
PIF3-A14和PIF3-A20中PIF3形成的光体消失的速率
变慢, 表明光诱导的磷酸化对于PIF3光体定位不是
必需的。检测模拟磷酸化植株PIF3-D6和PIF3-D19的
磷酸化, 发现这些植株在黑暗条件下已经发生磷酸
化, 并且部分蛋白发生降解, 进一步说明PIF3磷酸化
对于其降解是必要的(Ni et al., 2013)。
单基因突变体pif以及PIF超表达突变体幼苗均表
现出复杂的形态模式(Leivar and Quail, 2011)。pif突
变体对持续红光照射非常敏感(Huq and Quail, 2002;
Kim et al., 2003; Fujimori et al., 2004; Monte et al.,
2004; Khanna et al., 2007; Nozue et al., 2007; de
Lucas et al., 2008; Leivar et al., 2008a; Lorrain et
al., 2008, 2009; Shin et al., 2009)。这些突变体对红
光的响应 , 在某种程度上是由于phyB的大量积累 ,
从而导致了它们对光的超敏感性。phyB大量积累主要
是因为PIF蛋白降解反馈调节光敏化的phyB降解, 而
在突变体中这种反馈作用降低, 使phyB的降解减少,
最终导致phyB的积累(Khanna et al., 2007; Al-Sady
et al., 2008; Leivar et al., 2008a, 2012)。通过检测转
基因植株PIF3-WT、PIF3-A14、PIF3-A20和PIF3-A26
体内的phyB含量 , 发现PIFs反馈调节phyB不仅与
phyB相互作用的PIFs含量有关, 而且与体内光诱导
PIFs降解的速率有关(Ni et al., 2013)。目前, 光诱导
PIF3磷酸化并最终影响其降解的机制尚不清楚(Bu et
al., 2011a, 2011b)。最新研究表明, PIF的磷酸化可以
招募一种光响应的LRB (light-response bric-a-brack/
tramtrack/broad (BTB)) E3泛素连接酶结合到PIF3和
phyB的复合物上。招募的LRBs可以促使PIF3和phyB
泛素化以及降解。这些结果揭示了光受体及其所调节
的信号分子之间存在一种相互保护且相互抑制的信
号传递和信号终止机制, 该机制与以往的报道不同。
然而, 尽管在LRB的突变体lrb123中光诱导的phyB泛
素化以及降解下游PIF基本消除, 但是PIF3的泛素化
250 植物学报 50(2) 2015

和降解只是变慢并没有完全消失, 说明可能还有一些
未知E3连接酶在调控PIF3的降解过程中与LRBs存在
功能冗余(Ni et al., 2014)。
4 展望
过去十多年中, 光敏色素信号机制的研究已经取得了
巨大的进展。然而, 对于光敏色素调控信号网络的本
质和范围所知甚少。在光敏色素信号通路中, 磷酸化
修饰作为一种重要的机制还未被完全解析清楚。光敏
色素除了自磷酸化外, 是否还有激酶参与其去磷酸
化; 光敏色素的去磷酸化如何影响其信号传递和功能
等; 诸如此类的问题还有待解决。同时, 光敏色素需
通过磷酸化PIF蛋白传递信号, PIF自身磷酸化对于其
降解至关重要, 但具体分子本质目前还不是很清楚。
此外, PIF蛋白的去磷酸化到现在还一无所知。未来的
挑战将是寻找调控光敏色素以及PIF蛋白磷酸化水平
的激酶和磷酸酶。
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Research Progress in Phosphorylation Modification of Phyto-
chrome Signaling
Jing Yue, Liping Guan, Siyuan Meng, Jing Zhang, Suiwen Hou*
MOE Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou 730000
Abstract Light is the unique source of energy for plants. Plants have evolved a variety of photoreceptors to sense light
information. The elements in the light signaling pathway are mainly regulated by several post-translational modifications
such as phosphorylation and dephosphorylation. Photochromes, the known auto-phosphorylating serine/threonine
kinases, can be dephosphorylated by a few protein phosphatases. Investigation of the autophosphorylation sites in phy-
tochrome A (phyA) and phytochrome B (phyB) has revealed that the autophosphorylation of phy is essential for their
function and plays a significant role in regulating phytochrome-mediated signaling. The phosphorylation of phyto-
chrome-interacting factor (PIF) induced by the light-activated photoreceptor is critical for PIF degradation and photo-
morphogenesis initiation. This review focuses on the recent progress in understanding phosphorylation modification in
phytochrome signaling, providing valuable information for further research in this field.
Key words phytochrome, PIF, phosphorylation modification
Yue J, Guan LP, Meng SY, Zhang J, Hou SW (2015). Research progress in phosphorylation modification of phyto-
chrome signaling. Chin Bull Bot 50, 241–254.
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* Author for correspondence. E-mail: housw@lzu.edu.cn
(责任编辑: 孙冬花)