全 文 ：植物生理学报 Plant Physiology Journal 2016, 52 (4): 394–400　　doi: 10.13592/j.cnki.ppj.2016.0014394
收稿 2016-01-14　　修定 2016-03-07
资助 国家科技支撑计划(2014BAD16B06)。
* 通讯作者(E-mail: ypguo@nwsuaf.edu.cn)。
高等植物6-磷酸海藻糖信号调控研究进展
张雯, 王宇斐, 郭延平*
西北农林科技大学园艺学院, 陕西杨凌712100
摘要: 6-磷酸海藻糖(T6P)在植物体内广泛分布, 对植物的生长发育起着重要的调节作用, 其信号途径伴随植物胚胎发育直
至衰老的整个过程。T6P是海藻糖的代谢前体物质, 其主要通过抑制蔗糖非酵解相关激酶1 (SnRK1)的催化活性, 进而调控
植物生长代谢, 故称为T6P/SnRK1信号。在T6P/SnRK1信号调控植物代谢过程中, 转录因子bZIP11、己糖激酶HXK及PIF
信号途径也参与到植物T6P/SnRK1信号调控路径。
关键词: 植物生长; 逆境; 蔗糖非酵解相关激酶1 (SnRK1); 海藻糖; 6-磷酸海藻糖
海藻糖是2个葡萄糖分子以1,1-糖苷键构成的
非还原性二糖, 其代谢前体物质为6-磷酸海藻糖
(trehalose-6-phosphate, T6P)。T6P主要存在于植物
的细胞质, 液泡和叶绿体中也少量存在(Marina等
2013)。T-6-P的主要代谢途径(图1)为: 尿苷二磷酸
葡萄糖(UDPG)和6-磷酸葡萄糖(G6P)经6-磷酸海
藻糖合成酶(TPS)催化合成T6P, T6P被6-磷酸海藻
糖磷酸酶(TPP)进一步催化合成海藻糖(trehalose),
海藻糖又可被海藻糖酶(TRE)催化分解形成两分
子的葡萄糖(glucose) (Eastmond和Graham 2003)。
间的基因结构类似, 其中拟南芥TPPA和TPPB基因
可影响TPP的活性。
由于海藻糖在高等植物中较难分离、提取,
且在植物体内含量很低, 因此测定比较困难, 而植
物体中T6P的含量更低, 测定更困难。直到Lunn等
(2006)建立串联四极杆-液质联用方法测定T6P后,
有关高等植物中T6P的生物学功能分析逐渐成为
研究热点。从近年的研究报告看, 关于T6P的研究
多集中在T6P/SnRK1信号途径, T6P与蔗糖、淀粉
等代谢物质间的相互关系, T6P的抗逆性功能等方
面(Wingler等2012; Yadav等2014; Kretzschmar等
2015)。本文对近年来有关T6P的研究报告进行了
系统分析, 旨在探讨T6P对植物的生长调控作用,
生物、非生物抗逆功能, T6P与SnRK1信号通路以
及与HXK、IAA、bZIP11的生理调节作用等, 为今
后T6P的研究提供借鉴。
1 T6P及关键酶对植物生长发育的调控
10多年来, 对T6P的研究日渐深入, 取得了不
少成果。早先, Romero等(1997)在TPS转基因烟草
上发现T6P可提高植物抗旱性。之后, Pellny等
(2004)进一步发现T6P与烟草叶面积及光合作用相
关。还有研究表明植物体内T6P含量与蔗糖含量
存在一定比例, 并能影响淀粉合成等多个植物生
理活动(Kolbe等2005; Yadav等2014)。
1.1 T6P与植物生长发育的关系
在碳代谢中, 维持T6P含量与碳含量比例平衡
对植物生长十分重要(Yadav等2014)。当植物处于
在上述的代谢途径中, TPS基因所编码的TPS
蛋白是催化T6P的生物合成酶, 而TPP基因所编码
的TPP是催化T6P生物分解的蛋白酶。研究发现,
拟南芥TPS基因家族有11个基因, TPP基因家族有
10个基因。其中AtTPS基因家族可进一步划归为
AtTPS1~4 (具有编码TPS酶活性的结构)和AtTPS5~11
(不具有编码TPS酶活性的结构)两个亚族。虽然拟
南芥TPS基因家族成员间的基因序列和氨基酸序
列基本一致, 但由于基因特异性较大, 使得TPS
家族成员间的生物学功能有很大不同(Avonce等
2010)。目前仅AtTPS1基因被证实可以明显影响
TPS酶活性, 且AtTPS1也对植物生长代谢过程有影
响。而TPS2~4仅能推测出对十字花科植物的TPS
蛋白酶有作用。此外, TPS5~11基因的生物学功能
仍不明确(Lunn 2007)。拟南芥TPP基因家族成员
图1 6-磷酸海藻糖代谢途径示意图
Fig.1 T6P metabolic pathways
张雯等: 高等植物6-磷酸海藻糖信号调控研究进展 395
正常生长条件下, 若植物中T6P大量积累, T6P与碳
含量比例随之失衡, 此时植物会通过调节自身碳
积累使它们间比例失衡得以恢复。当植物体内碳
源大量积累而未被利用时, 植物正常生长便会被
抑制, 在过量的碳源中, 过量的蔗糖会引起植物中
T6P的大量积累, 其失衡比例得到恢复, 植物得以
正常生长(Wingler等2000; Zhang等2009)。可见,
T6P是碳源充足与否的信号物质。此外, 植物体内
积累过多T6P, 还会因激发UDPG脱氢酶上游基因,
而影响植物正常代谢(Klinghammer和Tenhaken
2007; Paul等2010)。
在植物胚胎发育中, T6P是种子萌发不可缺少
的物质。对于缺少TPS基因(T6P合成基因)的突变
体种子来说, 该种子在胚胎“鱼雷期”便已终止发
育, 但可以通过过量表达TPS基因解除种子萌发抑
制因素。当然, 即使种子萌发限制解除, 该种子萌
发植株的生长势依然不如野生型(Eastmond等
2002; Schluepmann等2003)。
植物淀粉代谢中, T6P与淀粉代谢息息相关。
叶片积累大量T6P后, 体内AGPase活性受到影响,
进而促进淀粉合成(Kolbe等2005)。但Marina等
(2013)研究认为T6P不是通过影响AGPase调节淀
粉合成与分解的, 而是通过影响植物生物钟进行
调节。可见, T6P调节淀粉代谢的机理仍不明了。
此外, T6P还有延缓叶片衰老、影响果实座果率等
其他植物生理功能(Wingler等2012; Botton等2011)。
1.2 TPS与植物生长发育的关系
TPS催化UDPG和G6P生成T6P的过程中, 低
浓度Ca2+、K+、Mg2+、Na+、果糖、6-磷酸果糖和
葡萄糖可增强TPS酶活性, 而脯氨酸对TPS蛋白酶
活性却有抑制作用(Elisa等2004)。拟南芥的TPS基
因家族包含基因AtTPS1~11, AtTPS1到AtTPS4为第
一类TPSS亚族, AtTPS5到AtTPS11为第二类TPSS亚
族。第一类TPSS亚族与酵母ScTPS1有高度同源
性, AtTPS1基因由于N末端延展区结构与其它第
一类TPSS亚族不同, AtTPS1的生物活性较低, 但可
以表达TPS蛋白酶活性(Van等2002; Zang等2011)。
AtTPS2~4目前只发现在长角果中存在(Paul等
2008), 而全部第二类TPSS亚族都缺少TPS活性
(Harthill等2006; Ramon等2009)。此外, TPS除了有
催化合成T6P的生物功能外, TPS蛋白在氧化戊糖
磷酸途径中对G6P和NADPH分别有感应和激活的
作用(Wilson等2010)。
目前对TPS的研究, 主要集中在基因功能评价
方面(Chary等2008; 付凤玲等2011)。史健志等
(2015)研究发现坛紫菜PhTPS基因在高温胁迫下呈
现先上调、后下降、再上调的起伏趋势。且在高
度失水条件下PhTPS1和PhTPS2-1基因表达显著上
调, 因此推测PhTPS基因在高度失水胁迫下发挥应
激调节作用。另有多种TPS研究是通过TPS1-GUS
检测花芽、角果、叶子与胚胎等的生理功能(Van
等2004; Gómez等2010)。
1.3 TPP与植物生长发育的关系
TPP催化T6P生成海藻糖。TPS和TPP酶基因
均广泛出现在高等植物中, 有着庞大的基因家族
(Leyman等2001; Schluepmann等2004)。在拟南芥
中现有10个TPP家族基因(AtTPPA~J), 其中拟南芥
TPPA和TPPB基因可表达TPP活性。
TPP对植物生长与发育均有一定的影响。Sa-
toh-Nagasawa等(2006)发现在TPP作用下玉米突变
体的花序结构发生了变异。Ge等(2008)发现水稻
中OsTPP1基因过量表达后, 水稻的耐盐性和耐冷
性均有明显提升。岳思思等(2014)也发现丹参
SmTPS基因有提升植物抵御干旱及低温胁迫能力
的作用。
2 T6P与SnRK1信号调控
Thevelein和Hohmann (1995)发现酵母中T6P
与己糖激酶(hexokinase, HXK)对植物进行协同调
控; 然而Eastmond等(2002)研究表明, T6P并没有通
过HXK对植物进行调节。在随后的研究中发现,
T6P与SnRK1在植物上存在拮抗作用(Zhang等
2009)。SnRK1是碳代谢和氮代谢的重要调控因子,
与养分胁迫等多个响应途径相关(Halford和Hey
2009; Smeekens等2010)。T6P与SnRK1能协同调
节植物的生长与发育(Baena-Gonzalez等2007)。在
植物的生长代谢过程中, HXK有可能参与了T6P/
SnRK1途径(Nägele等2014)。
2.1 SnRK1的植物功能特性
SnRK家族包含SnRK1、SnRK2和SnRK3三个
亚族。其中, SnRK1包含α亚基、β亚基和γ亚基, α
亚基是SnRK1的催化亚基。SnRK1的α亚基由
(KIN10和KIN11)编码, 另有基因编码β亚基和γ亚
植物生理学报396
基。此外, 在拟南芥中还发现了一个植物特有基
因, 可编码βγ亚基(Polge和Thomas 2007)。
SnRK1是植物糖信号调节通路上的关键激
酶。目前研究发现SnRK1与蔗糖磷酸合成酶、硝
酸还原酶和TPS酶等均有联系(Polge和Thomas
2007; Halford和Hey 2009)。虽然李光洁等(2009)
将编码平邑甜茶SnRK1的α亚基以及βγ亚基的基因
序列转入番茄中, 未发现果实糖含量、酸含量以
及淀粉含量有显著变化; 但Wang等(2012)将平邑
甜茶植株中的MhSnRK1基因转入番茄使其过量表
达, 发现该转基因番茄株系中叶片和未成熟果实
中的淀粉含量明显高于野生型, 叶片中蔗糖合酶
分解方向活性和AGPase活性均明显增加。此外,
植物在低糖条件下, 过量表达SnRK1基因, 可通过
依赖蔗糖氧化还原型AGPase促进淀粉合成(McK-
ibbin等2006; Tiessen等2003); 在低氧、黑暗、碳源
缺乏等条件下 , SnRK1也可以影响植物的生长
(BaenaGonzález等2007; Cho等2012)。可见, 当植
物的生长环境、生长时期或种类不同时, SnRK1对
植物有多种不同的生长调节响应方式。
2.2 T6P与SnRK1间作用及信号通路
T6P与SnRK1之间存在某未知中间因子(图2),
且仅存在于幼嫩器官或组织中。T6P对大麦谷粒中
的SnRK1活性抑制作用贯穿整个生长期(Martínez-
Barajas等2011)。Zhang等(2009)通过对拟南芥植
物中不同发育阶段SnRK1的活性测定, 也发现T6P
抑制幼嫩叶片中的SnRK1活性, 而对成熟叶片中的
SnRK1活性没有抑制作用; 该研究还通过在免疫
沉淀反应中添加无SnRK1的α亚基幼嫩组织悬浮
液于成熟组织液后, T6P开始对SnRK1活性表现出
抑制作用; 但将煮沸后的幼嫩组织悬浮液加于成
熟组织液后, T6P则对SnRK1的活性不再产生作
用。说明该未知因子不耐热, 很可能属于蛋白类
物质。今后, 对该因子仍有待进一步寻找和深入
探究。
T6P/SnRK1信号通路在植物糖代谢的信号调
节中起着极其重要的作用(陈素丽等2014)。如参
与了植物呼吸、淀粉合成、淀粉和蔗糖等代谢,
甚至还参与了ABA的积累(Liam等2013)。Baena-
González等(2007)通过AtKIN10基因过量表达, 不
仅观察到拟南芥花序结构受到了影响, 而且也观
察到花期延迟。Martínez-Barajas等(2011)通过研
究花后10 d大麦的生长情况, 指出T6P/SnRK1信号
途径参与到大麦多个生长与发育阶段, 其中包括
对谷粒、种皮以及胚胎等的生理调控。T 6 P /
SnRK1信号途径同样能调节土豆、甘蔗和黄瓜等
植物的“库”器官或细胞(Wu和Birch 2010; Debast等
2011; Zhang等2015)。此外, 研究还发现缺乏TPS6
基因的拟南芥突变体, 其花序分枝会增多(Chary等
2008)。不过, 有研究报告指出TPS6并不能表达有
活性的TPS蛋白, 我们分析认为TPS和TPP蛋白主
要通过信号调控途径而非生物催化功能来影响植
物生长与发育。
T6P/SnRK1信号通路还与植物生长素和PIF
光信号通路相关。Paul等(2010)通过微阵列技术分
析发现, 在拟南芥植株中T6P可下调Aux/IAA基因
表达, Aux/IAA是影响植物生长素含量的重要基
因。当过量表达TIR1 (植物生长素受体转运抑制
子1)时, 植物体内T6P含量增加, 通过抑制SnRK1活
性使TIR1亚基磷酸化, 进而保证植物的正常生长
(Farras等2001; Dos等2009)。此外, Paul等(2010)还
发现T6P可调控PIF4基因, PIF4基因是参与光信号
图2 高等植物T6P/SnRK1信号调控途径示意图
Fig.2 Three strategies of T6P/SnRK1 signal pathway to cope with different environment
张雯等: 高等植物6-磷酸海藻糖信号调控研究进展 397
调节的光敏色素相关基因。该基因能参与调节植
物多个生长与发育过程(Franklin 2008; Koini等
2009), 在胚胎处于弱光或高温条件下, 下胚轴在
PIF4信号调节下会伸长 , 诱导植物生长素合成
(Franklin等2011); 当植物内蔗糖含量增多后, 会导
致PIF4和PIF5基因轻微下调, 其中PIF4的下调则
与T6P增加有关(Paul等2010)。
3 T6P及其抗逆性
Schluepmann等(2004)利用基因芯片分析T6P
含量变化对植物的影响时, 发现T6P与植物生物逆
境和非生物逆境相关基因均存在一定的关联。所
以, 全面透彻地探究T6P对植物生物以及非生物逆
境的调节作用, 可以更清晰地理解植物对逆境的
多种适应性。
3.1 T6P与生物逆境
在大麦中海藻糖可诱导植物自身保护机制启
动, 从而抵抗白粉病(Blumeria graminis)对其侵害
(Reignault等2001; Renard-Merlier等2007)。当植物
内源海藻糖含量增加, 会使T6P含量也随之增加,
由此推测可能是T6P对大麦白粉病起到抵制作
用。此外, TPS1基因是稻瘟病(Magnaporthe grisea)
在植物体内繁殖所必需的基因。目前, T6P与生物
逆境的研究报告还很少。
3.2 T6P/ SnRK1的信号途径与非生物逆境
当碳源缺乏时, 植物体内T6P含量会减少, 随
之SnRK1活性增加, 进而降低植物碳源消耗, 增加
碳同化进程和光合作用, 最终使植物体内积累大
量碳水化合物(Baena-González等2007; Baena-
González和Sheen 2008)。在适度干旱条件下, 植物
体内会积累碳水化合物以适应干旱环境(Hummel
等2010; Muller等2011)。同样, 冷害也会使得植物
体内积累碳水化合物, 抵御低温胁迫(Fernandez等
2012)。因而在旱害和冷害时, 植物体内T6P含量
增加, 从而SnRK1活性降低, 促进碳水化合物的合
成积累。
3.3 bZIP11参与与T6P/SnRK1信号途径
T6P抑制SnRK1活性, 进而影响bZIP11启动子
调控相关基因表达(Smeekens 2015)。转录子bZIPs
在抗逆性方面的作用 , 通常与蔗糖含量变化有
关。蔗糖可通过调控bZIPs阅读框(SC-uORF)增强
其转录功能, 并同时抑制其翻译表达(Rook等1998;
Wiese等2004)。此后Baena-González和Sheen
(2008)在研究多个转录子功能时发现SnRK1与转
录子bZIP也存在一定关联。Delatte等(2011)表明
拟南芥的bZIP11基因过量表达时, 在体内积累大量
的T6P后, 植物不再出现生长抑制现象。此外, 研
究还发现bZIP11可以通过诱导一段基因片段, 而对
KIN10进行调控, 以致影响SnRK1活性。
4 结论与展望
糖不仅是代谢物质, 还能作为信号物质调节
植物生长与发育。T6P信号调节途径可直接参与
到种子萌发、幼苗生长、开花结实以及衰老等多
个植物生理活动中。在植物正常生长条件下, T6P
与蔗糖含量成一定比例, 存在相互调节的关系。
当植物体内蔗糖含量增加时, T6P与蔗糖含量比例
平衡被打破, 进而T6P含量随蔗糖含量增加而增加,
植物体内重新达到T6P与蔗糖含量比例的平衡
(Yadav等2014)。因而, 可以理解为T6P有调节养分
胁迫的生理功能。此外, T6P通过调节SnRK1活性,
作用于bZIP11、光敏色素以及植物生长激素等, 确
保了植物生长与发育的正常进行, 提高了植物对
环境的适应性。
近几年, 尽管高等植物中T6P信号物质的研究
日益增多, 但还有很多不足, 主要是由于T6P在植
物内含量低, 又与多个信号物质协同调节植物代
谢, 因而较难准确地阐明T6P的生理调控机制, 并
且T6P是植物生长代谢的重要物质, 难以在不影响
植物正常生长条件下对T6P进行分子生物学分
析。今后, 要通过双分子荧光互补、免疫共沉淀
等实验技术手段找出T6P与SnRK1中间未知的蛋
白因子, 明确T6P/SnRK1信号途径除了参与PIF4光
敏信号途径外, 是否还参与到其他信号调控中, 进
一步阐明T6P/SnRK1信号调控途径。
总之, 对T6P的研究仍需要不断创新和完善研
究手段和实验技术, 并结合多领域如细胞生物学,
植物生理学、遗传学和基因组学等进一步研究,
从而更加深入地了解T6P信号调节方式、分子机
理与植物信号响应等。
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Review on crosstalk regulation involving in trehalose-6-phosphate signal in
plant
ZHANG Wen, WANG Yu-Fei, GUO Yan-Ping*
College of Horticulture, Northwest Agriculture and Forestry University, Yangling, Shaanxi 712100, China
Abstract: Trehalose-6-phosphate (T6P) is an essential signaling metabolite which is involved in the regulation
of plant growth and development. Developmental processes are regulated by T6P that range from embryo de-
velopment to leaf senescence. T6P is a substance of trehalose metabolism, and regulates metabolism of plant
growth mainly by inhibiting sucrose non-fermenting related kinase-1 (SnRK1) activity, which is called T6P/
SnRK1 signal. The transcription factor bZIP11, HXK and PIF signal pathway has been identified as a new play-
er in the T6P/SnRK1 regulatory pathway.
Key words: plant development; stress; sucrose non-fermenting related kinase-1 (SnRK1); trehalose; treha-
lose-6-phosphate; review.
Received 2016-01-14 Accepted 2016-03-07
This work was supported by the National Natural Science and Technology Support Program (Grant No. 2014BAD16B06).
*Corresponding author (E-mail: ypguo@nwsuaf.edu.cn).