全 文 ：植物生理学报 Plant Physiology Journal 2015, 51 (5): 623~632　　doi: 10.13592/j.cnki.ppj.2015.0186 623
收稿 2015-04-02　　修定 2015-05-09
资助 国家自然科学基金(31272028)。
* 通讯作者(E-mail: fmsong@zju.edu.cn; Tel: 0571-88982481)。
植物NF-Y转录因子的生物学功能及其研究进展
宋秋明, 李大勇, 张慧娟, 宋凤鸣*
浙江大学生物技术研究所, 杭州310058
摘要: 核因子Y (NF-Y), 又称CCAAT盒结合因子(CBF)或亚铁血红素激活蛋白(HAP), 是一种普遍存在于酵母、哺乳动物及
植物等真核生物中的转录因子, 由三种不同的亚基组成, 即NF-YA (CBF-B或HAP2)、NF-YB (CBF-A或HAP3)和NF-YC
(CBF-C或HAP5)。近年来的研究发现NF-Y在植物胚胎发育、光合作用、开花时间调控、逆境胁迫响应等诸多方面起重
要作用。本文简要阐述植物NF-Y的生化、互作与家族特性、基因表达调控、生物学功能等方面的研究进展。
关键词: NF-Y转录因子; 生长发育; 逆境胁迫反应
NF-Y Transcription Factors and Their Biological Functions in Plants
SONG Qiu-Ming, LI Da-Yong, ZHANG Hui-Juan, SONG Feng-Ming*
Institute of Biotechnology, Zhejiang University, Hangzhou 310058, China
Abstract: Nuclear factor Y (NF-Y), also known as CCAAT-binding factor (CBF) or Heme Activator Protein
(HAP), is a conserved heterotrimeric complex composed of three subunits, NF-YA (also termed CBF-B or
HAP2), NF-YB (CBF-A or HAP3) and NF-YC (CBF-C or HAP5). During the last decade, extensive studies
have revealed that subunits of NF-Y complex play important roles in embryonic development, photosynthesis,
flowering and stress response. This review summarizes the recent research progress on the biological function
of NF-Y in plants.
Key words: NF-Y transcription factors; growth and development; stress response
核因子Y (nuclear factor Y, NF-Y), 又称
CCAAT盒结合因子(CCAAT-binding factor, CBF)或
亚铁血红素激活蛋白(heme activator protein, HAP),
是一类普遍存在于酵母、动物、植物等真核生物
中的转录因子, 通常由三种不同亚基组成, 即NF-
YA (CBF-B或HAP2)、NF-YB (CBF-A或HAP3)和
NF-YC (CBF-C或HAP5) (Mantovani 1999)。但在
酿酒酵母(Saccaromyces cerevisiae)和乳酸克鲁维
酵母(Kluyveromyces lactis)等少数真菌中还存在第
四类亚基HAP4 (Forsburg和Guarente 1989; Mc-
Nabb等1997)。NF-YA、NF-YB和NF-YC通过形成
异源三聚体复合物, 并与其他调控因子相互作用,
激活或抑制下游基因的表达 (Coust ry等1998;
Wright等1995; Benatti等2008)。在酵母和哺乳动
物中, 每个基因编码一个亚基(Laloum等2013), 但
植物NF-Y家族在进化上不断扩张, 通常是由多个
基因编码同一类亚基(Yang等2005), 因而植物
NF-Y所形成的异源三聚体数目十分庞大。近年来
的研究发现植物NF-Y在胚胎发育、光合作用、开
花时间调控、逆境胁迫响应等诸多方面起重要作
用。本文简要阐述植物NF-Y的生化与家族特性及
其生物学功能等方面的研究进展。
1 NF-Y转录因子
1.1 NF-Y的生化与结构特征
NF-Y分为NF-YA、NF-YB和NF-YC三个亚
基, 均包含一个十分保守的区域。这些保守区域
是DNA结合或蛋白-蛋白互作的功能域(Gusmaroli
等2001), 其中NF-YB和NF-YC具有一段类似于组
蛋白折叠元件(HFM)的保守域, 形成紧密二聚体
(Luger等1997; Petroni等2012)。NF-YB在三聚体与
DNA的特异性结合中起作用(Zemzoumi等1999)。
植物NF-YA蛋白在长度和结构上各不相同,
均包含一个由53个氨基酸组成的保守核心区域,
在这个核心区域中存在两个功能上保守的结构域
A1和A2 (Petroni等2012)。A1位于核心区域的N端,
由20个氨基酸构成一个α螺旋, 主要调控同NF-
植物生理学报624
YB、NF-YC亚基的互作; A2位于核心区域的C端,
由21个氨基酸组成, 在与CCAAT盒的特异性结合
中起重要作用。在植物NF-YA中, 这些保守核心区
域位于蛋白的中间位置, N端通常呈酸性(Coustry
等1996)。
植物NF-YB蛋白长度也各不相同, 但一般小
于NF-YA, 均具有一个中心结构域, 在结构、氨基
酸数目上与核心组蛋白H2B中的HFM相似(Dolfini
等2012)。NF-YB由3个α螺旋组成, 中间被2个β链
环域分隔, 这些结构参与蛋白-DNA及蛋白-蛋白的
互作(Arents和Moudrianakis 1993)。植物NF-YB转
录因子可分为LEC-1和非LEC-1两类, 其中LEC-1
和L1L (LEC-1-like)同源性很高, 是植物胚胎形成
的中枢调控因子(Lee等2003; Hilioti等2014)。
NF-YB由N端的A结构域、中心B结构域和C端的C
结构域三部分组成, 其中LEC-1和L1L类NF-YB蛋
白的B结构域中存在着一段由16个氨基酸组成的
特异序列(Kwong等2003; Holdsworth等2008)。这
段极度保守的特异序列区分了LEC-1和非LEC-1两
类NF-YB蛋白。在LEC类NF-YB蛋白的B结构域
中有一个天冬氨酸Asp-55残基, 是LEC类NF-YB蛋
白的功能位点, 参与调控种子的胚胎形成(Lee等
2003)。拟南芥中除了L1L外, 其他NF-YB成员均
不能替代LEC-1执行其生理功能(Lee等2003)。研
究显示, LEC-1和L1L基因是在种子植物分化之前,
由维管植物的基因组进化而来(Cagliari等2014)。
NF-YC蛋白的大小通常介于NF-YA和NF-YB
蛋白之间。和NF-YB相似, NF-YC蛋白也含有一个
HFM结构域, 但该结构域与核心组蛋白H2A的关
系更近(Dolfini等2012)。
NF-Y三聚体与真核生物启动子区域中一段
常见的CCAAT盒结合, 从而激活或抑制基因的转
录(Ceribelli等2008)。CCAAT盒是一种普遍存在于
真核生物中的启动子元件, 一般位于转录起始位
点上游60~100 bp的区域内(Dolfini等2009)。NF-Y
复合体的转录活性位于NF-YA的N端和NF-YC的C
端 , 均由一段富含谷氨酰胺的疏水结构域组成
(Coustry等1996)。
1.2 NF-Y家族及其特性
在酵母、动物等真核生物中, NF-Y三个亚基
一般有1个或2个基因编码, 但是植物NF-Y家族则
有很大的扩张。全基因组生物信息学分析表明,
植物NF-Y组成一个基因家族, 而NF-Y的3个亚基
则形成了数量不等的亚家族, 如拟南芥中有10个
NF-YA亚基、13个NF-YB亚基和13个NF-YC亚基
(Siefers等2009), 水稻中NF-YA、NF-YB和NF-YC
分别有10、11和7个(Thirumurugan等2008), 小麦中
先后鉴定了10个NF-YA、11个NF-YB和14个NF-
YC (Stephenson等2007), 大豆中有20个NF-YA、39
个NF-B和27个NF-YC (Laloum等2013)。在大豆、
苜蓿等豆科植物中, NF-YB和NF-YC亚家族分别存
在NC2β和NC2α类特殊成员, 这些特殊成员具有不
同的HFM (Rípodas等2015)。
2 NF-Y在植物生长发育中的作用
2.1 在胚胎和种子发育中的作用
在很多单子叶和双子叶植物中, LEC1和L1L
参与调控植株从胚胎到成熟的转变过程, lec1突变
体表现出多效性表型, 如子叶上毛状体、胚柄的
异常发育及种子在淀粉、蛋白质和油脂积累上的
缺陷等(Zhang等2002; Yazawa等2004; Fambrini等
2006; Alemanno等2008; Cao等2011; Tan等2011;
Salvini等2012)。拟南芥中LEC1 (AtNF-YB9)和L1L
(AtNF-YB6)基因具有调控植物胚胎发育的功能
(Kwong等2003; Junker等2012)。AtLEC1基因通过
激活一些胚胎形成基因和细胞分化基因的转录来
诱导营养细胞的胚胎发育(Lotan等1998)。染色体
免疫沉淀、基因表达谱分析发现, LEC1是作为光
信号和激素信号的一个调控枢纽从而在植物胚胎
发育过程中起作用(Junker等2012)。同样, 水稻Os-
HAP3E (OsLEC1)在营养生长和生殖发育中具有多
效性功能, OsHAP3E影响叶片、圆锥花序和穗粒
的发育, 通过调控分生组织的形态发生在营养生
长和生殖发育中起作用。OsHAP3E可与一些
MADS转录因子互作, 当OsHAP3E蛋白积累水平
上升时 , 会干扰MADS的功能 , 如在水稻中Os-
HAP3E过表达时, OsMADS1启动子特定区域甲基
化水平升高, OsMADS1的表达水平下调, 最终调控
叶片、花序和小穗的发育(Zhang和Xue 2013);
RNAi抑制OsHAP3E表达或过量表达嵌合抑制子
抑制OsHAP3E活性导致在遗传转化时细胞死亡,
无法获得转基因植株(Ito等2011)。OsNF-YB7 (Os-
L1L)的过量表达植株则出现矮化、直立状叶片、
宋秋明等: 植物NF-Y转录因子的生物学功能及其研究进展 625
紧密圆锥花序、异常花轴及重瓣花等表型(Ito等
2011)。此外, 在玉米和油菜中分别过量表达Zm-
LEC1和ZmWRI1或BnLEC1和BnL1L可以提高种子
含油量。玉米ZmWRI1是ZmLEC1下游的一个转录
因子, 过表达ZmWRI1可提高种子含油量, 但不影
响种子萌芽、幼苗生长和作物产量等农艺性状
(Shen等2010; Tan等2011)。在拟南芥中, LEC1/L1L
和NF-YC2通过与种子特异性ABA响应元件结合
因子bZIP67的互作, 从而激活种子储藏蛋白基因
CRUCIFERIN C的表达(Yamamoto等2009)。
除LEC1外, 一些其他NF-Y基因也参与了植物
营养生长和生殖发育的调控。拟南芥 N F -
YA1/5/6/9存在功能冗余现象, 因为单个基因或两个
基因同时突变后并不表现出任何表型变化, 但过
量表达NF-YA1/5/6/9后影响雄配子发育、胚胎发
育、种子形态及种子萌发等(Mu等2013)。At-
NF-YA3和AtNF-YA8也存在功能冗余, 并在胚胎形
成的早期阶段起调控作用(Fornari等2013)。At-
NF-YB2在拟南芥根尖部位特异性表达, 过量表达
AtNF-YB2会加快细胞分裂和伸长, 促进主根伸长,
这个过程可能与细胞分裂和伸长相关(Ballif等
2011)。在水稻中, RNAi抑制OsNF-YB1表达后, 细
胞周期途径的一些基因表达发生变化, 导致胚乳
等缺陷(Sun等2014)。小麦TaNF-YA-B1和管涔山青
扦(Picea wilsoni) PwNF-YC分别在根和花粉管中起
作用, 其中PwNF-YC的作用受Ca2+诱导(Yu等2011;
Qu等2015)。另外, 一些拟南芥NF-Y转录因子在种
子萌发过程中存在相似或相反的功能, 其作用可
能与ABA信号途径有关(Kumimoto等2013; Siri-
wardana等2014)。
2.2 NF-Y在调控植物开花中的作用
在拟南芥中, AtNF-YB2和AtNF-YB3通过感
受长光照来调控开花调控子FLOWERING LOCUS
T (FT)并促进开花(Kumimoto等2008)。过表达At-
NF-YC1和AtNF-YC2能提高FT的转录水平, 加速开
花进程(Hackenberg等2012a); 相反, AtHAP3b突变
体中FT表达水平下降, 开花延迟(Chen等2007)。
AtNF-YC3/4/9通过与AtNF-YB2/3互作, 共同参与
CONSTANS (CO)介导的开花过程(Kumimoto等
2010), 由此推测NF-Y复合体元件结合到FT基因启
动子远端增强子元件, 把CO引导到启动子近端的
顺式元件上, 从而启动向生殖生长的转换(Cao等
2014)。CO是一个关键的光诱导开花时间调控子,
通过保守CCT结构域与NF-Y互作(Ben-Naim等
2006; Wenkel等2006)。CCT类基因与NF-YA基因
具有相似的功能。研究表明, 拟南芥中CCT结构域
基因CO可替代AtNF-YA1/2亚基, 形成CO/AtHAP3/
AtHAP5复合体, 并调控开花时间(Wenkel等2006),
NF-Y复合体为CO提供DNA结合位点(Tiwari等
2010)。当NF-Y缺失时过表达CO会削弱或丧失其
对FT因子的活化能力 , 导致不能提前开花(Ku-
mimoto等2010); 反之, 当CO缺失时过表达NF-Ys则
降低其调控开花的效率(Tiwari等2010)。最新研究
发现, NF-Y蛋白同时与光周期途径中的CO和赤霉
素途径中的DELLA互作, 共同调控花器官调控因
子SOC1基因表达, 其中NF-Y复合体结合到SOC1
基因启动子中特定顺式元件并调控其三甲基化
H3K27水平, 表明NF-Y复合体能起到表观遗传标
记的关键因子作用(Hou等2014)。
在长日照条件下, 水稻OsNF-YB11 (DTH8/
Ghd8/LHD1)通过下调表达开花调控子, 抑制光周
期诱导开花的信号转导网络(Wei等2010; Yan等
2011; Dai等2012)。过量表达HvNF-YB1的大麦植
株能提前开花时间(Liang等2012), 小麦NF-Ys通过
与VRN2、CO中的CCT结构域相结合, 参与春化和
季节性光周期等生长发育信号和环境信号的集成,
从而调控开花进程(Li等2011)。
2.3 NF-Y在叶绿体形成和光合作用中的作用
在拟南芥中, AtNF-YA5、AtNF-YB9和At-
NF-YC9形成的复合体与GCR1 (G蛋白偶联受
体)、GPA1 (G蛋白α亚基)和Pirin1 (一个cupin家族
成员)组成一个信号传递链, 参与拟南芥黄化苗植
株中叶绿素A/B结合蛋白基因的表达(Warpeha等
2007)。水稻OsHAP3A丧失功能突变体中, 叶绿素
含量降低, 叶绿体退化, 说明水稻OsHAP3A参与叶
绿体的发育 ( K u s n e t s o v等 1 9 9 9 ) ; 水稻O s -
NF-YB2/3/4 (OsHAP3A/B/C)调控许多编码核酮
糖-1,5-二磷酸羧化酶/氧合酶小亚基和叶绿素a/b结
合蛋白的光合相关基因(Miyoshi等2003)。在小麦
中, 过量表达TaNF-YB3后显著提高叶绿素含量、
光合速率及早期生长率(Stephenson等2011), TaNF-
YC11受光照调控, 且参与光合作用相关基因表达
植物生理学报626
的调控(Stephenson等2010)。
3 NF-Y在非生物胁迫反应中的作用
3.1 在干旱胁迫响应中的作用
有学者系统研究了拟南芥和小麦NF-Y基因在
干旱胁迫下的表达变化 , 发现在拟南芥中大多
NF-YA基因呈上调表达, 但在小麦中NF-YA基因的
表达则相反(Stephenson等2007; Hackenberg等
2012a)。转基因研究表明, 过表达AtNF-YB1和
ZmNF-YB2的转基因拟南芥和玉米植株显著提高
干旱抗性(Nelson等2007)。同样, 在拟南芥中过表
达大豆GmNF-YA3或白杨PdNF-YB7可以减少叶片
水分损失 , 提高植株抗旱性(Ni等2013; Han等
2013)。NF-Y调控植物抗旱性的机制可能比较复
杂, 一般通过影响叶绿素含量、气孔电导率、叶
面温度、蒸腾效率及光合作用等几个因素进行调
控。过表达AtNF-YB1的转基因拟南芥中大批干旱
反应相关基因如DREB和ABA途径基因的表达并
无显著变化, 因此AtNF-YB1可能通过其他未知信
号途径来调控抗旱反应(Nelson等2007)。同时, 小
RNA可能通过影响NF-Y基因转录本丰度来调控
NF-Y在抗旱反应中的作用。干旱胁迫下, 拟南芥
AtNF-YA5在维管组织和保卫细胞中的表达水平显
著上调, 其表达受ABA途径调控, 但在转录后则受
miR169调控, 在气孔保卫细胞中AtNF-YA5的上调
表达改变气孔的孔径等 , 而在非保卫细胞中At-
NF-YA5可以激活一些胁迫响应基因的表达(Li等
2008); 利用人工miRNA方法抑制ERF (NF-YA5 En-
hancing RING FINGER)基因表达后增加miR169丰
度, 但显著降低NF-YA5的转录本积累水平(Gao等
2015)。
3.2 在高盐胁迫响应中的作用
在拟南芥芽后生长的早期阶段, AtNF-YA1过
表达植株增加对高盐胁迫和ABA的敏感性(Li等
2013)。过量表达小麦TaNF-YA10-1的拟南芥植株
显著增加对盐胁迫的敏感性, 降低ABA敏感性, 同
时AtRAB18、AtRD29B、AtABI5、AtCBF1和
AtCBF3等胁迫相关基因的表达水平显著下降(Ma
等2015)。但过表达百慕大草CdtNF-YC1的转基因
水稻植株增强抗盐性。研究表明, ABA、H2O2和
NO参与盐胁迫诱导CdtNF-YC1基因的转录表达,
当抑制ABA合成或去除H2O2、NO分子时Cdt-
NF-YC1的转录表达就会终止(Chen等2014)。高盐
胁迫下, 水稻miR169首先上调表达, 然后选择性降
解NF-YA基因, 抑制其表达(Zhao等2009)。
3.3 在其他胁迫响应中的作用
在拟南芥中 , 研究发现A t N F - Y C 2、A t -
NF-YA4、AtNF-YB3和AtbZIP28形成转录复合体,
从而诱导内质网胁迫响应基因的上调表达(Liu和
Howell 2010)。拟南芥AtHAP5A通过结合AtXTH21
的CCAAT元件来正调控抗冷性, 抑制活性氧积累,
激活ABA途径基因的表达 (Sh i等2014)。At-
NF-YC10能与DREB2A互作 , 在热胁迫中At-
NF-YC10与AtNF-YA2、AtNF-YB3形成三聚体复
合物, 并与DREB2A协同调控热胁迫诱导基因的启
动子, 从而提高植株的耐热性(Sato等2014)。
4 NF-Y在植物-微生物互作中的作用
研究表明NF-Y在豆科植物-根瘤菌互作中起
重要作用。在菜豆-Rhizobium etli互作中, RNAi沉
默PvNF-YC1基因表达后导致根瘤菌不能侵染、抑
制根瘤形成, 而过量表达后则显著提高结瘤效率,
表明PvNF-YC1在根瘤菌侵染和根瘤形成中起重
要作用(Zanetti等2010)。在蒺藜状苜蓿中, Mt-
NF-YA1和MtNF-YA2存在功能冗余, 在豆科植物-根
瘤菌共生系统形成的早期阶段起作用(Laloum等
2014)。MtNF-YA1在共生关系建立时上调表达, 其
转录本丰度受miRNA169调控(Reynoso等2013), 进
一步研究表明, MtNF-YA1通过影响侵染索的形成
来调控根瘤菌的侵染(Laporte等2014)。NF-YC1和
一个GRAS转录因子SIN1间的互作在根瘤形成发
挥重要作用。NF-Y三聚体中的NF-YC1与SIN1发
生互作, 并特异性结合到CCAAT框序列上, 激活细
胞周期相关基因及其下游基因的表达, 最终调控
根瘤菌的侵染和根瘤的形成(Soyano等2013; Batta-
glia等2014; Rípodas等2014)。
NF-Y在植物抗病反应中的作用鲜有研究。
最近发现, 过量表达OsHAP2E的水稻植株显著提
高对稻瘟病和白叶枯病的抗病性, 芯片表达谱分
析显示在过量表达OsHAP2E的植株中大量防卫基
因表达上调(Alam等2015)。因此, NF-Y在植物抗病
反应中起重要作用, 但其作用机制有待研究阐明。
5 miR169对NF-YA转录本丰度的转录后调控
研究发现 , m iR169在转录后水平上调控
宋秋明等: 植物NF-Y转录因子的生物学功能及其研究进展 627
NF-YA基因转录本的积累水平(Jones-Rhoades和
Bartel 2004)。在干旱胁迫响应中, 水稻miR169成
员上调表达(Zhao等2007, 2009), 而拟南芥中
miR169则多数下调表达(Li等2008)。在干旱、盐
胁迫及缺乏氮素条件下, 拟南芥miR169表达上调,
而一些NF-YA基因转录本的积累水平则显著下降
(Zhao等2011; Leyva-González等2012); miR169a比
miRA169c对AtNF-YA5转录本积累的抑制作用更
为显著, 导致AtNF-YA5转录本水平下降, 使得植株
对干旱胁迫更为敏感(Li等2008)。这与番茄中的
结果相反, 过量表达SlymiR169c后SlNF-YA1/2/3等
基因转录本的积累水平显著下调, 却提高抗旱性
(Zhang等2011)。在短期干旱、盐胁迫中, 大部分
玉米ZmNF-YA基因转录本积累量增加, 但在长期
胁迫时其转录本积累量下降; 相应的miR169在干
旱胁迫中下调表达, 在盐胁迫中先上调后下调表
达(Luan等2015)。在氮素缺乏时, 拟南芥miR169强
烈下调, 而其靶标AtNF-YA的转录本积累水平则显
著上调 , 过量表达miR169a的拟南芥植株中At-
NF-YA的转录本积累水平显著下降, 导致植株对氮
素胁迫更为敏感(Zhao等2011)。 此外, 拟南芥At-
NF-YA2、蒺藜状苜蓿MtNF-YA1和MtHAP2-1、白
杨PtrHAP2及矮牵牛和金鱼草NF-YA等在根系发
育、根瘤形成、叶芽休眠、花器官形态等的作用
均受到miRNA169的调控(Combier等2006; Cartola-
no等2007; Liu和Howell 2010; Potkar等2013; Sorin
等2014)。
6 NF-Y亚基间的互作及其复合体
NF-Y的功能需要NF-YA/B/C形成异源三聚体
复合体 , 但是NF-Y亚基间的互作十分复杂 , 且
NF-Y亚基间的互作存在一定的特异性。最近, 采
用酵母双杂交技术分析拟南芥中NF-YB成员和
NF-YC成员的互作关系, 除AtNF-YB9 (LEC1)不与
任何一个AtNF-YC成员发生互作外, 两个家族间
绝大部分成员均存在一定的互作关系, 其中At-
NF-YB/AtNF-YC间均存在较强的互作关系(Cal-
venzani等2012)。胡萝卜一个NF-YB (LEC1)和两
个NF-YC间具有互作关系 (Yazawa和Kamada
2007); 水稻OsHAP3A与2个OsHAP2、6个Os-
HAP5s间具有互作关系(Thirumurugan等2008)。酵
母三杂交实验结果表明, 在AtNF-YB2/3/4/5存在
时, AtNF-YA4与AtNF-YC2存在互作(Liu和Howell
2010)。
在作用上, NF-YB和NF-YC最初在细胞质中
形成异源二聚体, 后穿梭至细胞核中并与NF-YA结
合 , 形成成熟的异源三聚体复合体 ( K a h l e等
2005)。研究证明, 拟南芥AtNF-YB、AtNF-YC亚
基间形成异源二聚体, 但不能形成同源二聚体; At-
NF-YA只能与含HFD亚基形成的二聚体组装成异
源三聚体复合体, 但是不能与单个AtNF-YA或At-
NF-YB亚基相结合(Hackenberg等2012b)。
7 小结和展望
自在油菜中第一次报道植物NF-YA以来(Al-
bani和Robert 1995), 有关植物NF-Y及其生物学功
能的研究已经取得显著进展。研究显示, NF-Y的
生物学功能十分多样 , 涉及胚胎形成、光合作
用、开花时间调控及各种胁迫响应等重要生理过
程(表1)。相比而言, NF-Y在植物抗病反应中的作
用尚需研究阐明。目前NF-Y的研究主要集中在拟
南芥等少数模式植物中, 其他植物特别是农作物
中NF-Y的功能鉴定和作用研究尚有待深入。已有
研究证明, 改变NF-Y亚基基因的表达水平可以提
高植物种子含油量及对各种逆境胁迫的抗逆性。
因此, NF-Y在作物农艺性状的改良及分子育种中
具有巨大的潜力。
在体内, NF-Y组装形成异源三聚体复合体, 从
而发挥其调控胚胎发育、开花时间、光合效率及
逆境胁迫响应等方面的功能。NF-Y在植物生长发
育和各种逆境胁迫反应中的作用机制极为复杂,
今后有关NF-Y作用机制的研究包括: (1) NF-Y不
同亚基之间的互作形成的异源三聚体组成与特异
性及其在不同生物学过程中的功能; (2) NF-Y异源
三聚体与其他调控因子(如转录因子)互作形成的
转录复合体及其协同作用; (3) miR169等小RNA调
控NF-YA基因转录本积累及其对NF-Y异源三聚体
组成与功能的影响; (4)分离鉴定上游调控NF-Y基
因表达和异源三聚体形成的因子、NF-Y异源三聚
体所调控的下游靶标基因及其功能。这些研究将
有助于全面认识NF-Y的生物学功能、作用机制及
其调控网络。
植物生理学报628
参考文献
Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K,
Yaeno T, Yamaoka N, Shimomoto K, Takayama K, Nishina H
et al (2015). Overexpression of a rice heme activator protein
gene (OsHAP2E) confers resistance to pathogens, salinity and
drought, and increases photosynthesis and tiller number. Plant
Biotechnol J, 13: 85~96
Albani D, Robert LS (1995). Cloning and characterization of a Bras-
sica napus gene encoding a homologue of the B subunit of a
heteromeric CCAAT-binding factor. Gene, 167: 209~213
Alemanno L, Devic M, Niemenak N, Sanier C, Guilleminot J, Rio M,
Verdeil JL, Montoro P (2008). Characterization of leafy cotyle-
don1-like during embryogenesis in Theobroma cacao L.. Planta,
表1 已知功能的植物NF-Y亚基及其生物学功能
Table 1 Plant NF-Y subunits with known biological functions
基因 植物 功能分析方法 生物学性状 参考文献
AtNF-YA1 拟南芥 过量表达 胚胎发育; 盐胁迫相关 Li等2013; Mu等2012
AtNF-YA3 拟南芥 RNAi 胚胎发育 Fornari等2013
AtNF-YA4 拟南芥 T-DNA插入突变体 内质网逆境胁迫 Liu和Howell 2010
AtNF-YA5 拟南芥 T-DNA插入突变体 胚胎发育; 干旱胁迫 Warpeha等2007; Li等
2008; Mu等2013
AtNF-YA8 拟南芥 T-DNA插入突变体; RNAi 胚胎发育 Fornari等2013
AtNF-YB1 拟南芥 过量表达 干旱胁迫耐受性 Nelson等2007
AtNF-YB2 拟南芥 过量表达 促进主根伸长; 调控花期 Ballif等2011; Kumimoto
等2008
AtNF-YB3 拟南芥 过量表达; T-DNA插入突变体 调控花期; 内质网逆境胁迫 Kumimoto等2008; Liu
和Howell 2010
AtNF-YB6 拟南芥 RNAi 胚胎发育 Kwong等 2003
AtNF-YB9 拟南芥 T-DNA插入突变体 胚胎发育 Junker等2012; Warpeha
等2007
AtHAP3b 拟南芥 T-DNA插入突变体 调控花期 Chen等2007
AtHAP5A 拟南芥 过量表达 冷胁迫耐受性 Shi和Chan 2014
AtNF-YC1 拟南芥 过量表达 调控花期 Hackenberg等2012a
AtNF-YC2 拟南芥 过量表达 调控花期; 内质网逆境胁迫 Hackenberg等2012a;
Liu和Howell 2010
AtNF-YC10 拟南芥 过量表达 热胁迫耐受性 Sato等2014
OsHAP2E 水稻 过量表达 抗病性 Alam等2015
OsHAP3E 水稻 过量表达 营养和生殖发育 Zhang和Xue 2013
OsNF-YB1 水稻 过量表达; RNAi 胚乳发育; 调控细胞周期 Sun等2014
OsNF-YB2 水稻 RNAi 叶绿素合成与叶绿体发育 Kusnetsov等1999
OsNF-YB7 水稻 过量表达 营养和生殖发育 Ito等2011
OsNF-YB11 水稻 QTL位点 抑制开花 Wei等2010; Yan等2011;
Dai等2012
TaNF-YA10-1 小麦 过量表达 盐胁迫相关 Ma等2015
TaNF-YB3 小麦 过量表达 叶绿素含量; 光合作用 Stephenson等2011
BnLEC1 油菜 过量表达 脂肪酸生物合成 Tan等2011
BnL1L 油菜 过量表达 脂肪酸生物合成 Tan等2011
BdNF-YB6 二穗短柄草 过量表达 提前开花 Cao等2011
ZmLEC1 玉米 过量表达 脂肪酸生物合成 Shen等2010
ZmNF-YB2 玉米 过量表达 干旱胁迫耐受性 Nelson等2007
PvNF-YC1 菜豆 过量表达; RNAi 根瘤发育 Zanetti等2010
PwNF-YCs 管涔山青扦 过量表达; RNAi 花粉管发育 Yu等2011
GmNF-YA3 大豆 过量表达 干旱胁迫耐受性 Ni等2013
PdNF-YB7 白杨 过量表达 干旱胁迫耐受性 Han等2013
CdtNF-YC1 百慕大草 过量表达 耐盐性; 耐旱性 Chen等2014
HvNF-YB1 大麦 过量表达 提前开花 Liang等2012
MtHAP2-1 蒺藜状苜蓿 RNAi 促进根瘤发育 Combier等2006

宋秋明等: 植物NF-Y转录因子的生物学功能及其研究进展 629
227: 853~866
Arents G, Moudrianakis EN (1993). Topography of the histone octam-
er surface: repeating structural motifs utilized in the docking of
nucleosomal DNA. Proc Natl Acad Sci USA, 90: 10489~10493
Ballif J, Endo S, Kotani M, MacAdam J, Wu Y (2011). Over-expres-
sion of HAP3b enhances primary root elongation in Arabidopsis.
Plant Physiol Biochem, 49: 579~583
Battaglia M, Rípodas C, Clúa J, Baudin M, Aguilar OM, Niebel A,
Zanetti ME, Blanco FA (2014). A nuclear factor Y interacting
protein of the GRAS family is required for nodule organogene-
sis, infection thread progression, and lateral root growth. Plant
Physiol, 164: 1430~1442
Benatti P, Basile V, Merico D, Fantoni LI, Tagliafico E, Imbriano C
(2008). A balance between NF-Y and p53 governs the pro- and
anti-apoptotic transcriptional response. Nucleic Acids Res, 36:
1415~1428
Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, Coup-
land G, Samach A, Lifschitz E (2006). The CCAAT binding fac-
tor can mediate interactions between CONSTANS-like proteins
and DNA. Plant J, 46: 462~476
Cagliari A, Turchetto-Zolet AC, Korbes AP, dos Santos Maraschin F,
Margis R, Margis-Pinheiro M (2014). New insights on the evolu-
tion of LEAFY COTYLEDON1 (LEC1) type genes in vascular
plants. Genomics, 103: 380~387
Calvenzani V, Testoni B, Gusmaroli G, Lorenzo M, Gnesutta N,
Petroni K, Mantovani R, Tonelli C (2012). Interactions and
CCAAT-binding of Arabidopsis thaliana NF-Y subunits. PLoS
ONE, 7: e42902
Cao S, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt
BF (2014). A distal CCAAT/NUCLEAR FACTOR Y complex
promotes chromatin looping at the FLOWERING LOCUS T pro-
moter and regulates the timing of flowering in Arabidopsis. Plant
Cell, 26: 1009~1017
Cao S, Kumimoto RW, Siriwardana CL, Risinger JR, Holt III BF
(2011). Identification and characterization of NF-Y transcription
factor families in the monocot model plant Brachypodium dis-
tachyon. PLoS ONE, 6: e21805
Cartolano M, Castillo R, Efremova N, Kuckenberg M, Zethof J,
Gerats T, Schwarz-Sommer Z, Vandenbussche M (2007). A con-
served microRNA module exerts homeotic control over Petunia
hybrida and Antirrhinum majus floral organ identity. Nat Genet,
39: 901~905
Ceribelli M, Dolfini D, Merico D, Gatta R, Viganò AM, Pavesi G,
Mantovani R (2008). The histone-like NF-Y is a bifunctional
transcription factor. Mol Cell Biol, 28: 2047~2058
Chen M, Zhao Y, Zhuo C, Lu S, Guo Z (2014). Overexpression of a
NF-YC transcription factor from bermudagrass confers tolerance
to drought and salinity in transgenic rice. Plant Biotechnol J, doi:
10.1111/pbi.12270
Chen NZ, Zhang XQ, Wei PC, Chen QJ, Ren F, Chen J, Wang XC
(2007). AtHAP3b plays a crucial role in the regulation of flow-
ering time in Arabidopsis during osmotic stress. J Biochem Mol
Biol, 40: 1083~1089
Combier JP, Frugier F, De Billy F, Boualem A, El-Yahyaoui F, Moreau
S, Vernié T, Ott T, Gamas P, Crespi M et al (2006). MtHAP2-1 is
a key transcriptional regulator of symbiotic nodule development
regulated by microRNA169 in Medicago truncatula. Genes Dev,
20: 3084~3088
Coustry F, Maity SN, Sinha S, de Crombrugghe B (1996). The
transcriptional activity of the CCAAT-binding factor CBF is
mediated by two distinct activation domains, one in the CBF-B
subunit and the other in the CBF-C subunit. J Biol Chem, 271:
14485~14491
Coustry F, Sinha S, Maity S, Crombrugghe BD (1998). The two acti-
vation domains of the CCAAT-binding factor CBF interact with
the dTAF(II)110 component of the Drosophila TFIID complex.
Biochem J, 331: 291~297
Dai X, Ding Y, Tan L, Fu Y, Liu F, Zhu Z, Sun X, Gu P, Cai H, Sun
C (2012). LHD1, an allele of DTH8/Ghd8, controls late heading
date in common wild rice (Oryza rufipogon). J Integr Plant Biol,
54: 790~799
Dolfini D, Gatta R, Mantovani R (2012). NF-Y and the transcriptional
activation of CCAAT promoters. Crit Rev Biochem Mol Biol,
47: 29~49
Dolfini D, Zambelli F, Pavesi G, Mantovani R (2009). A perspective
of promoter architecture from the CCAAT box. Cell Cycle, 8:
4127~4137
Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V,
Salvini M, Pugliesi C (2006). Characterization of LEAFY COT-
YLEDON1-LIKE gene in Helianthus annuus and its relationship
with zygotic and somatic embryogenesis. Dev Genes Evol, 216:
253~264
Fornari M, Calvenzani V, Masiero S, Tonelli C, Petroni K (2013). The
Arabidopsis NF-YA3 and NF-YA8 genes are functionally redun-
dant and are required in early embryogenesis. PLoS ONE, 8:
e82043
Forsburg SL, Guarente L (1989). Identification and characterization
of HAP4: a third component of the CCAAT-bound HAP2/HAP3
heteromer. Genes Dev, 3: 1166~1178
Gao W, Liu W, Zhao M, Li WX (2015). NERF encodes a RING E3
ligase important for drought resistance and enhances the expres-
sion of its antisense gene NFYA5 in Arabidopsis. Nucleic Acids
Res, 43: 607~617
Gusmaroli G, Tonelli C, Mantovani R (2001). Regulation of the
CCAAT-binding NF-Y subunits in Arabidopsis thaliana. Gene,
264: 173~185
Hackenberg D, Keetman U, Grimm B (2012a). Homologous NF-
YC2 subunit from Arabidopsis and tobacco is activated by
photooxidative stress and induces flowering. Int J Mol Sci, 13:
3458~3477
Hackenberg D, Wu Y, Voigt A, Adams R, Schramm P, Grimm B
(2012b). Studies on differential nuclear translocation mechanism
and assembly of the three subunits of the Arabidopsis thaliana
transcription factor NF-Y. Mol Plant, 5: 876~888
Han X, Tang S, An Y, Zheng DC, Xia XL, Yin WL (2013). Over-
expression of the poplar NF-YB7 transcription factor confers
drought tolerance and improves water-use efficiency in Arabi-
dopsis. J Exp Bot, 64: 4589~4601
植物生理学报630
Hilioti Z, Ganopoulos I, Bossis I, Tsaftaris A (2014). LEC1-LIKE
paralog transcription factor: how to survive extinction and fit in
NF-Y protein complex. Gene, 543: 220~233
Holdsworth MJ, Bentsink L, Soppe WJ (2008). Molecular networks
regulating Arabidopsis seed maturation, after-ripening, dorman-
cy and germination. New Phytol, 179: 33~54
Hou X, Zhou J, Liu C, Liu L, Shen L, Yu H (2014). Nuclear factor
Y-mediated H3K27me3 demethylation of the SOC1 locus or-
chestrates flowering responses of Arabidopsis. Nat Commun, 5:
4601
Ito Y, Thirumurugan T, Serizawa A, Hiratsu K, Ohme-Takagi M,
Kurata N (2011). Aberrant vegetative and reproductive develop-
ment by overexpression and lethality by silencing of OsHAP3E
in rice. Plant Sci, 181: 105~110
Jones-Rhoades MW, Bartel DP (2004). Computational identification
of plant microRNAs and their targets, including a stress-induced
miRNA. Mol Cell, 14: 787~799
Junker A, Mönke G, Rutten T, Keilwagen J, Seifert M, Thi TMN,
Renou JP, Balzergue S, Viehöver P, Hähnel U et al (2012). Elon-
gation-related functions of LEAFY COTYLEDON1 during the
development of Arabidopsis thaliana. Plant J, 71: 427~442
Kahle J, Baake M, Doenecke D, Albig W (2005). Subunits of the
heterotrimeric transcription factor NF-Y are imported into the
nucleus by distinct pathways involving importin β and importin
13. Mol Cell Biol, 25: 5339~5354
Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion
CM, Hempel FD, Ratcliffe OJ (2008). The Nuclear Factor Y sub-
units NF-YB2 and NF-YB3 play additive roles in the promotion
of flowering by inductive long-day photoperiods in Arabidopsis.
Planta, 228: 709~723
Kumimoto RW, Siriwardana CL, Gayler KK, Risinger JR, Siefers N,
Holt BF (2013). NUCLEAR FACTOR Y transcription factors
have both opposing and additive roles in ABA-mediated seed
germination. PLoS ONE, 8: e59481
Kumimoto RW, Zhang Y, Siefers N, Holt BF (2010). NF-YC3, NF-
YC4 and NF-YC9 are required for CONSTANS-mediated, pho-
toperiod-dependent flowering in Arabidopsis thaliana. Plant J,
63: 379~391
Kusnetsov V, Landsberger M, Meurer J, Oelmüller R (1999). The
assembly of the CAAT-box binding complex at a photosynthesis
gene promoter is regulated by light, cytokinin, and the stage of
the plastids. J Biol Chem, 274: 36009~36014
Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB,
Harada JJ (2003). LEAFY COTYLEDON1-LIKE defines a class
of regulators essential for embryo development. Plant Cell, 15:
5~18
Laloum T, Baudin M, Frances L, Lepage A, Billault-Penneteau B,
Cerri MR, Ariel F, Jardinaud MF, Gamas P, de Carvalho-Niebel
F et al (2014). Two CCAAT-box-binding transcription factors
redundantly regulate early steps of the legume-rhizobia endo-
symbiosis. Plant J, 79: 757~768
Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2013). CCAAT-
box binding transcription factors in plants: Y so many? Trends
Plant Sci, 18: 157~166
Laporte P, Lepage A, Fournier J, Catrice O, Moreau S, Jardinaud MF,
Mun JH, Larrainzar E, Cook DR, Niebel A et al (2014). The
CCAAT box-binding transcription factor NF-YA1 controls rhi-
zobial infection. J Exp Bot, 65: 481~694
Lee H, Fischer RL, Goldberg RB, Harada JJ (2003). Arabidopsis
LEAFY COTYLEDON1 represents a functionally specialized
subunit of the CCAAT binding transcription factor. Proc Natl
Acad Sci USA, 100: 2152~2156
Leyva-González MA, Ibarra-Laclette E, Cruz-Ramírez A, Herrera-Es-
trella L (2012). Functional and transcriptome analysis reveals an
acclimatization strategy for abiotic stress tolerance mediated by
Arabidopsis NF-YA family members. PLoS ONE, 7: e48138
Li C, Distelfeld A, Comis A, Dubcovsky J (2011). Wheat flowering
repressor VRN2 and promoter CO2 compete for interactions
with NUCLEAR FACTOR-Y complexes. Plant J, 67: 763~773
Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H,
Zhu JK (2008). The Arabidopsis NFYA5 transcription factor is
regulated transcriptionally and posttranscriptionally to promote
drought resistance. Plant Cell, 20: 2238~2251
Li YJ, Fang Y, Fu YR, Huang JG, Wu CA, Zheng CC (2013). NFYA1
is involved in regulation of postgermination growth arrest under
salt stress in Arabidopsis. PLoS ONE, 8: e61289
Liang M, Hole D, Wu J, Blake T, Wu Y (2012). Expression and func-
tional analysis of NUCLEAR FACTOR-Y, subunit B genes in
barley. Planta, 235: 779~791
Liu JX, Howell SH (2010). bZIP28 and NF-Y transcription factors are
activated by ER stress and assemble into a transcriptional com-
plex to regulate stress response genes in Arabidopsis. Plant Cell,
22: 782~796
Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi
K, Fischer RL, Goldberg RB, Harada JJ (1998). Arabidopsis
LEAFY COTYLEDON1 is sufficient to induce embryo develop-
ment in vegetative cells. Cell, 93: 1195~1205
Luan M, Xu M, Lu Y, Zhang L, Fan Y, Wang L (2015). Expression of
zma-miR169 miRNAs and their target ZmNF-YA genes in re-
sponse to abiotic stress in maize leaves. Gene, 555:178~185
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997).
Crystal structure of the nucleosome core particle at 2.8 Å resolu-
tion. Nature, 389: 251~260
Ma X, Zhu X, Li C, Song Y, Zhang W, Xia G, Wang M (2015). Over-
expression of wheat NF-YA10 gene regulates the salinity stress
response in Arabidopsis thaliana. Plant Physiol Biochem, 86:
34~43
Mantovani R (1999). The molecular biology of the CCAAT-binding
factor NF-Y. Gene, 239: 15~27
McNabb DS, Tseng KA, Guarente L (1997). The Saccharomyces
cerevisiae Hap5p homologue from fission yeast reveals two con-
served domains that are essential for assembly of heterotetrameric
CCAAT binding factor. Mol Cell Biol, 17: 7008~7018
Miyoshi K, Ito Y, Serizawa A, Kurata N (2003). OsHAP3 genes regu-
late chloroplast biogenesis in rice. Plant J, 36: 532~540
Mu J, Tan H, Hong S, Liang Y, Zuo J (2013). Arabidopsis transcrip-
tion factor genes NF-YA1, 5, 6 and 9 play redundant roles in
male gametogenesis, embryogenesis, and seed development.
宋秋明等: 植物NF-Y转录因子的生物学功能及其研究进展 631
Mol Plant, 6: 188~201
Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC,
Anstrom DC, Bensen RJ, Castiglioni PP, Heard JE et al (2007).
Plant nuclear factor Y (NF-Y) B subunits confer drought toler-
ance and lead to improved corn yields on water-limited acres.
Proc Natl Acad Sci USA, 104: 16450~16455
Ni Z, Hu Z, Jiang Q, Zhang H (2013). GmNFYA3, a target gene of
miR169, is a positive regulator of plant tolerance to drought
stress. Plant Mol Biol, 82: 113~129
Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M,
Tonelli C, Holt BF, Mantovani R (2012). The promiscuous life
of plant NUCLEAR FACTOR Y transcription factors. Plant Cell,
24: 4777~4792
Potkar R, Recla J, Busov V (2013). ptr-MIR169 is a posttranscription-
al repressor of PtrHAP2 during vegetative bud dormancy period
of aspen (Populus tremuloides) trees. Biochem Biophys Res
Commun, 431: 512~518
Qu B, He X, Wang J, Zhao Y, Teng W, Shao A, Zhao X, Ma W, Wang
J, Li B et al (2015). A wheat CCAAT box-binding transcription
factor increases the grain yield of wheat with less fertilizer input.
Plant Physiol, 167: 411~423
Reynoso MA, Blanco FA, Bailey-Serres J, Crespi M, Zanetti ME
(2013). Selective recruitment of mRNAs and miRNAs to polyri-
bosomes in response to rhizobia infection in Medicago truncatu-
la. Plant J, 73: 289~301
Rípodas C, Castaingts M, Clúa J, Blanco F, Zanetti ME (2015). Anno-
tation, phylogeny and expression analysis of the nuclear factor Y
gene families in common bean (Phaseolus vulgaris). Front Plant
Sci, doi: 10.3389/fpls
Rípodas C, Clúa J, Battaglia M, Baudin M, Niebel A, Zanetti ME,
Blanco F (2014). Transcriptional regulators of legume-rhizobia
symbiosis: Nuclear Factors Ys and GRAS are two for tango.
Plant Signal Behav, 9: e28847
Salvini M, Sani E, Fambrini M, Pistelli L, Pucciariello C, Pugliesi C
(2012). Molecular analysis of a sunflower gene encoding an ho-
mologous of the B subunit of a CAAT binding factor. Mol Biol
Rep, 39: 6449~6465
Sato H, Mizoi J, Tanaka H, Maruyama K, Qin F, Osakabe Y, Morim-
otoa K, Ohoria T, Kusakabea K, Nagata M et al (2014). Arabi-
dopsis DPB3-1, a DREB2A interactor, specifically enhances heat
stress-induced gene expression by forming a heat stress-specific
transcriptional complex with NF-Y subunits. Plant Cell, 26:
4954~4973
Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D,
Tarczynski MC (2010). Expression of ZmLEC1 and ZmWRI1
increases seed oil production in maize. Plant Physiol, 153 (3):
980~987
Shi H, Ye T, Zhong B, Liu X, Jin R, Chan Z (2014). AtHAP5A modu-
lates freezing stress resistance in Arabidopsis through binding to
CCAAT motif of AtXTH21. New Phytol, 203: 554~567
Siefers N, Dang KK, Kumimoto RW, Bynum WE, Tayrose G, Holt BF
(2009). Tissue-specific expression patterns of Arabidopsis NF-Y
transcription factors suggest potential for extensive combinatori-
al complexity. Plant Physiol, 149: 625~641
Siriwardana CL, Kumimoto RW, Jones DS, Holt BF (2014). Gene
family analysis of the Arabidopsis NF-YA transcription factors
reveals opposing abscisic acid responses during seed germina-
tion. Plant Mol Biol Rep, 32:971~986
Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Brière C,
Njo MF, Beeckman T, Crespi M, Hartmann C (2014). A miR169
isoform regulates specific NF-YA targets and root architecture in
Arabidopsis. New Phytol, 202: 1197~1211
Soyano T, Kouchi H, Hirota A, Hayashi M (2013). Nodule inception
directly targets NF-Y subunit genes to regulate essential process-
es of root nodule development in Lotus japonicus. PLoS Genet, 9:
e1003352
Stephenson TJ, McIntyre CL, Collet C, Xue GP (2007). Genome-wide
identification and expression analysis of the NF-Y family of
transcription factors in Triticum aestivum. Plant Mol Biol, 65:
77~92
Stephenson TJ, McIntyre CL, Collet C, Xue GP (2010). TaNF-YC11,
one of the light-upregulated NF-YC members in Triticum aes-
tivum, is co-regulated with photosynthesis-related genes. Funct
Integr Genomics, 10: 265~276
Stephenson TJ, McIntyre CL, Collet C, Xue GP (2011). TaNF-YB3 is
involved in the regulation of photosynthesis genes in Triticum
aestivum. Funct Integr Genomics, 11: 327~340
Sun X, Ling S, Lu Z, Ouyang Y, Liu S, Yao J (2014). OsNF-YB1, a
rice endosperm-specific gene, is essential for cell proliferation in
endosperm development. Gene, 551: 214~221
Tan H, Yang X, Zhang F, Zheng X, Qu C, Mu J, Fu F, Li J, Guan R,
Zhang H et al (2011). Enhanced seed oil production in canola
by conditional expression of Brassica napus LEAFY COTYLE-
DON1 and LEC1-LIKE in developing seeds. Plant Physiol, 156:
1577~1588
Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008). Identi-
fication, characterization and interaction of HAP family genes in
rice. Mol Genet Genomics, 279: 279~289
Tiwari SB, Shen Y, Chang HC, Hou Y, Harris A, Ma SF, McPartland M,
Hymus GJ, Adam L, Marion C et al (2010). The flowering time
regulator CONSTANS is recruited to the FLOWERING LOCUS
T promoter via a unique cis-element. New Phytol, 187: 57~66
Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR,
Anderson MB, Kaufman LS (2007). The GCR1, GPA1, PRN1,
NF-Y signal chain mediates both blue light and abscisic acid re-
sponses in Arabidopsis. Plant Physiol, 143: 1590~1600
Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H,
Wan J (2010). DTH8 suppresses flowering in rice, influencing
plant height and yield potential simultaneously. Plant Physiol,
153: 1747~1758
Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A,
Coupland G (2006). CONSTANS and the CCAAT box binding
complex share a functionally important domain and interact to
regulate flowering of Arabidopsis. Plant Cell, 18: 2971~2984
Wright KL, Moore TL, Vilen BJ, Brown AM, Ting JPY (1995). Major
histocompatibility complex class II-associated invariant chain
gene expression is up-regulated by cooperative interactions of
Sp1 and NF-Y. J Biol Chem, 270: 20978~20986
植物生理学报632
Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hat-
tori T (2009). Arabidopsis NF-YB subunits LEC1 and LEC1-
LIKE activate transcription by interacting with seed-specific
ABRE-binding factors. Plant J, 58: 843~856
Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH,
Zhang YS, Yu SB, Zhang QF et al (2011). A major QTL, Ghd8,
plays pleiotropic roles in regulating grain productivity, plant
height, and heading date in rice. Mol Plant, 4: 319~330
Yang J, Xie Z, Glover BJ (2005). Asymmetric evolution of duplicate
genes encoding the CCAAT-binding factor NF-Y in plant ge-
nomes. New Phytol, 165: 623~631
Yazawa K, Kamada H (2007). Identification and characterization of
carrot HAP factors that form a complex with the embryo-specific
transcription factor C-LEC1. J Exp Bot, 58: 3819~3828
Yazawa K, Takahata K, Kamada H (2004). Isolation of the gene en-
coding carrot LEAFY COTYLEDON1 and expression analysis
during somatic and zygotic embryogenesis. Plant Physiol Bio-
chem, 42: 215~223
Yu Y, Li Y, Huang G, Meng Z, Zhang D, Wei J, Yan K, Zheng C,
Zhang L (2011). PwHAP5, a CCAAT-binding transcription
factor, interacts with PwFKBP12 and plays a role in pollen tube
growth orientation in Picea wilsonii. J Exp Bot, 62: 4805~4817
Zanetti ME, Blanco FA, Beker MP, Battaglia M, Aguilar OM (2010).
A C subunit of the plant nuclear factor NF-Y required for rhizo-
bial infection and nodule development affects partner selection
in the common bean-Rhizobium etli symbiosis. Plant Cell, 22:
4142~4157
Zemzoumi K, Frontini M, Bellorini M, Mantovani R (1999). NF-Y
histone fold α1 helices help impart CCAAT specificity. J Mol
Biol, 286: 327~337
Zhang JJ, Xue HW (2013). OsLEC1/OsHAP3E participates in the
determination of meristem identity in both vegetative and repro-
ductive developments of rice. J Integr Plant Biol, 55: 232~249
Zhang S, Wong L, Meng L, Lemaux PG (2002). Similarity of expres-
sion patterns of knotted1 and ZmLEC1 during somatic and zygot-
ic embryogenesis in maize (Zea mays L.). Planta, 215: 191~194
Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011).
Over-expression of microRNA169 confers enhanced drought
tolerance to tomato. Biotechnol Lett, 33: 403~409
Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009). Members
of miR-169 family are induced by high salinity and transiently
inhibit the NF-YA transcription factor. BMC Mol Biol, 10: 29
Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007).
Identification of drought-induced microRNAs in rice. Biochem
Biophys Res Commun, 354: 585~590
Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011). Involvement of
miR169 in the nitrogen-starvation responses in Arabidopsis.
New Phytol, 190: 906~915