Molecular characterization and roles of AP2 transcription factors on drought tolerance in plants

Abstract

The APETALA2 (AP2) domain defines a large family of DNA binding proteins. It has been demonstrated that the AP2 proteins have important functions in the transcriptional regulation of a variety of biologic processes related to growth and development in various responses to drought and other abiotic stresses. In this essay, recent researches on the AP2 transcription factors, such as the molecular characterization, expression patterns in responses to drought and other abiotic stresses, the roles of ABA on drought responding which were mediated by AP2 transcription factors, transcription regulation mechanisms, and the roles of overexpression of AP2 transcription factor on plant drought tolerance, etc. have been overviewed. Deepening the understanding of signaling and the corresponding transduction pathways that are initiated via drought stress stimuli will play crucial roles for providing the theoretical basis for variety breeding with promising drought tolerance in the future.

Keywords

transcription factor / AP2 domain / molecular characterization / transcriptional activation / drought tolerance

References

[1] Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004). The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell, 16(9): 2463–2480

[2] Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y S, Amasino R, Scheres B (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell, 119(1): 109–120

[3] Allen G J, Kuchitsu K, Chu S P, Murata Y, Schroeder J I (1999). Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell, 11(9): 1785–1798

[4] Allen M D, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998). A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J, 17(18): 5484–5496

[5] Alonso J M, Stepanova A N, Leisse T J, Kim C J, Chen H, Shinn P, Stevenson D K, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers C C, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter D E, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby W L, Berry C C, Ecker J R (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301(5633): 653–657

[6] Assmann S M (2003). OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells. Trends Plant Sci, 8(4): 151–153

[7] Assmann S M, Wang X Q (2001). From milliseconds to millions of years: guard cells and environmental responses. Curr Opin Plant Biol, 4(5): 421–428

[8] Baker S S, Wilhelm K S, Thomashow M F (1994). The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol, 24(5): 701–713

[9] Banno H, Ikeda Y, Niu Q W, Chua N H (2001). Overexpression of ArabidopsisESR1 induces initiation of shoot regeneration. Plant Cell, 13(12): 2609–2618

[10] Boutilier K, Offringa R, Sharma V K, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C M, van Lammeren A A, Miki B L, Custers J B, van Lookeren Campagne M M (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell, 14(8): 1737–1749

[11] Bowman J L, Alvarez J, Weigel D, Meyerowitz E M, Smyth D R (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development, 119: 721–743

[12] Choi D W, Rodriguez E M, Close T J (2002). Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol, 129(4): 1781–1787

[13] Chuck G, Meeley R B, Hake S (1998). The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev, 12(8): 1145–1154

[14] Chuck G, Muszynski M, Kellogg E, Hake S, Schmidt R J (2002). The control of spikelet meristem identity by the branched silkless1 gene in maize. Science, 298(5596): 1238–1241

[15] Connolly K M, Wojciak J M, Clubb R T (1998). Site-specific DNA binding using a variation of the double stranded RNA binding motif. Nat Struct Biol, 5(7): 546–550

[16] Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996). A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science, 273(5279): 1239–1241

[17] Dubouzet J G, Sakuma Y, Ito Y, Kasuga M, Dubouzet E G, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003). OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J, 33(4): 751–763

[18] Elliott R C, Betzner A S, Huttner E, Oakes M P, Tucker W Q, Gerentes D, Perez P, Smyth D R (1996). AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell, 8(2): 155–168

[19] Finkelstein R R, Gampala S S, Rock C D (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell, 14(Suppl): S15–S45

[20] Finkelstein R R, Lynch T J (2000). The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell, 12(4): 599–609

[21] Finkelstein R R, Wang M L, Lynch T J, Rao S, Goodman H M (1998). The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell, 10(6): 1043–1054

[22] Fujimoto S Y, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell, 12(3): 393–404

[23] Garg A K, Kim J K, Owens T G, Ranwala A P, Choi Y D, Kochian L V, Wu R J (2002). Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA, 99(25): 15898–15903

[24] Gilmour S J, Zarka D G, Stockinger E J, Salazar M P, Houghton J M, Thomashow M F (1998). Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J, 16(4): 433–442

[25] Gu Y Q, Yang C, Thara V K, Zhou J, Martin G B (2000). Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell, 12(5): 771–786

[26] Guo Y, Xiong L, Song C P, Gong D, Halfter U, Zhu J K (2002). A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell, 3(2): 233–244

[27] Gutterson N, Reuber T L (2004). Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol, 7(4): 465–471

[28] Haake V, Cook D, Riechmann J L, Pineda O, Thomashow M F, Zhang J Z (2002). Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol, 130(2): 639–648

[29] Hao D, Yamasaki K, Sarai A, Ohme-Takagi M (2002). Determinants in the sequence specific binding of two plant transcription factors, CBF1 and NtERF2, to the DRE and GCC motifs. Biochemistry, 41(13): 4202–4208

[30] Hao D Y, Ohme-Takagi M, Sarai A (1998). Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem, 273(41): 26857–26861

[31] Himmelbach A, Yang Y, Grill E (2003). Relay and control of abscisic acid signaling. Curr Opin Plant Biol, 6(5): 470–479

[32] Hoth S, Morgante M, Sanchez J P, Hanafey M K, Tingey S V, Chua N H (2002). Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci, 115(24): 4891–4900

[33] Hsieh T H, Lee J T, Charng Y Y, Chan M T (2002). Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol, 130(2): 618–626

[34] Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006). Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA, 103(35): 12987–12992

[35] Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008). Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol, 67(1-2): 169–181

[36] Hu Y X, Wang Y X, Liu X F, Li J Y (2004). Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development. Cell Res, 14(1): 8–15

[37] Hugouvieux V, Kwak J M, Schroeder J I (2001). An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell, 106(4): 477–487

[38] Ingram J, Bartels D (1996). The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol, 47(1): 377–403

[39] Irish V F, Sussex I M (1990). Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell, 2(8): 741–753

[40] Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006). Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol, 47(1): 141–153

[41] Jaglo K R, Kleff S, Amundsen K L, Zhang X, Haake V, Zhang J Z, Deits T, Thomashow M F (2001). Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol, 127(3): 910–917

[42] Jang I C, Oh S J, Seo J S, Choi W B, Song S I, Kim C H, Kim Y S, Seo H S, Choi Y D, Nahm B H, Kim J K (2003). Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol, 131(2): 516–524

[43] Jiang C, Iu B, Singh J (1996). Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol, 30(3): 679–684

[44] Jofuku K D, den Boer B G, Van Montagu M, Okamuro J K (1994). Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell, 6(9): 1211–1225

[45] Jung J, Won S Y, Suh S C, Kim H, Wing R, Jeong Y, Hwang I, Kim M (2006). The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta, 225(3): 575–588

[46] Kagaya Y, Ohmiya K, Hattori T (1999). RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res, 27(2): 470–478

[47] Karin M (1990). Too many transcription factors: positive and negative interactions. New Biol, 2(2): 126–131

[48] Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004). A combination of the ArabidopsisDREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol, 45(3): 346–350

[49] Khandelwal A, Elvitigala T, Ghosh B, Quatrano R S (2008). Arabidopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor. Plant Physiol, 148(4): 2050–2058

[50] Rice Full-Length cDNA Consortium; National Institute of Agrobiological Sciences Rice Full-Length cDNA Project Team, Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T; Foundation of Advancement of International Science Genome Sequencing & Analysis Group, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K; RIKEN, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003). Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science, 301(5631): 376–379

[51] Kizis D, Pagès M (2002). Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J, 30(6): 679–689

[52] Klucher K M, Chow H, Reiser L, Fischer R L (1996). The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell, 8(2): 137–153

[53] Koornneef M, Reuling G, Karssen C M (1984). The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant, 61(3): 377–383

[54] Krizek B A (2003). AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain. Nucleic Acids Res, 31(7): 1859–1868

[55] Latchman D S (1997). Transcription factors: an overview. Int J Biochem Cell Biol, 29(12): 1305–1312

[56] Lee J H, Hong J P, Oh S K, Lee S, Choi D, Kim W T (2004). The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol, 55(1): 61–81

[57] Lee T I, Young R A (2000). Transcription of eukaryotic protein-coding genes. Annu Rev Genet, 34(1): 77–137

[58] Leung J, Giraudat J (1998). Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol, 49(1): 199–222

[59] Leung J, Merlot S, Giraudat J (1997). The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell, 9(5): 759–771

[60] Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 10(8): 1391–1406

[61] Lu C, Fedoroff N (2000). A mutation in the ArabidopsisHYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell, 12(12): 2351–2366

[62] Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004). dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J, 37(5): 720–729

[63] Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001). The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J, 25(3): 295–303

[64] Meyerowitz E M (1994). Flower development and evolution: new answers and new questions. Proc Natl Acad Sci USA, 91(13): 5735–5737

[65] Moose S P, Sisco P H (1996). Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev, 10(23): 3018–3027

[66] Murzin A G, Brenner S E, Hubbard T, Chothia C (1995). SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol, 247(4): 536–540

[67] Mustilli A C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell, 14(12): 3089–3099

[68] Nakano T, Suzuki K, Fujimura T, Shinshi H (2006). Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol, 140(2): 411–432

[69] Nakashima K, Tran L S, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J, 51(4): 617–630

[70] Nikolov D B, Burley S K (1997). RNA polymerase II transcription initiation: a structural view. Proc Natl Acad Sci USA, 94(1): 15–22

[71] Nole-Wilson S, Krizek B A (2000). DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA. Nucleic Acids Res, 28(21): 4076–4082

[72] Oh S J, Kim Y S, Kwon C W, Park H K, Jeong J S, Kim J K (2009). Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol, 150(3): 1368–1379

[73] Oh S J, Kwon C W, Choi D W, Song S I, Kim J K (2007). Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J, 5(5): 646–656

[74] Oh S J, Song S I, Kim Y S, Jang H J, Kim S Y, Kim M, Kim Y K, Nahm B H, Kim J K (2005). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol, 138(1): 341–351

[75] Ohki I, Shimotake N, Fujita N, Nakao M, Shirakawa M (1999). Solution structure of the methyl-CpG-binding domain of the methylation-dependent transcriptional repressor MBD1. EMBO J, 18(23): 6653–6661

[76] Ohme-Takagi M, Shinshi H (1995). Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell, 7(2): 173–182

[77] Ohto M A, Fischer R L, Goldberg R B, Nakamura K, Harada J J (2005). Control of seed mass by APETALA2. Proc Natl Acad Sci USA, 102(8): 3123–3128

[78] Okamuro J K, Caster B, Villarroel R, Van Montagu M, Jofuku K D (1997). The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA, 94(13): 7076–7081

[79] Park J M, Park C J, Lee S B, Ham B K, Shin R, Paek K H (2001). Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell, 13(5): 1035–1046

[80] Pawson T (1993). Signal transduction—a conserved pathway from the membrane to the nucleus. Dev Genet, 14(5): 333–338

[81] Riechmann J L, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R, Creelman R, Pilgrim M, Broun P, Zhang J Z, Ghandehari D, Sherman B K, Yu G (2000). Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290(5499): 2105–2110

[82] Riechmann J L, Meyerowitz E M (1998). The AP2/EREBP family of plant transcription factors. Biol Chem, 379(6): 633–646

[83] Roeder R G (1996). The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci, 21(9): 327–335

[84] Sakuma Y, Liu Q, Dubouzet J G, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun, 290(3): 998–1009

[85] Schroeder J I, Kwak J M, Allen G J (2001). Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature, 410(6826): 327–330

[86] Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002). Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics, 2(6): 282–291

[87] Shen Y G, Zhang W K, Yan D Q, Du B X, Zhang J S, Liu Q, Chen S Y (2003). Characterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis. Theor Appl Genet, 107(1): 155–161

[88] Shinozaki K, Yamaguchi-Shinozaki K (1997). Gene expression and signal transduction in water-stress response. Plant Physiol, 115(2): 327–334

[89] Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003). Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol, 6(5): 410–417

[90] Shukla R K, Raha S, Tripathi V, Chattopadhyay D (2006). Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol, 142(1): 113–123

[91] Skinner J S, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger E J, Thomashow M F, Chen T H, Hayes P M (2005). Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol, 59(4): 533–551

[92] Sohn K H, Lee S C, Jung H W, Hong J K, Hwang B K (2006). Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol Biol, 61(6): 897–915

[93] Song C P, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu J K (2005). Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell, 17(8): 2384–2396

[94] Stockinger E J, Gilmour S J, Thomashow M F (1997). Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA, 94(3): 1035–1040

[95] Thomashow M F (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol, 50(1): 571–599

[96] Trujillo L E, Sotolongo M, Menéndez C, Ochogavía M E, Coll Y, Hernández I, Borrás-Hidalgo O, Thomma B P H J, Vera P, Hernández L (2008). SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant Cell Physiol, 49(4): 512–525

[97] van der Fits L, Memelink J (2000). ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289(5477): 295–297

[98] Wang X Q, Ullah H, Jones A M, Assmann S M (2001). G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science, 292(5524): 2070–2072

[99] Wojciak J M, Sarkar D, Landy A, Clubb R T (2002). Arm-site binding by lambda-integrase: solution structure and functional characterization of its amino-terminal domain. Proc Natl Acad Sci USA, 99(6): 3434–3439

[100] Xiao B, Huang Y, Tang N, Xiong L (2007). Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet, 115(1): 35–46

[101] Xiong L, Gong Z, Rock C D, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu J K (2001b). Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell, 1(6): 771–781

[102] Xiong L, Lee Bh, Ishitani M, Lee H, Zhang C, Zhu J K (2001a). FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev, 15(15): 1971–1984

[103] Xiong L, Schumaker K S, Zhu J K (2002). Cell signaling during cold, drought, and salt stress. Plant Cell, 14(Suppl): S165–S183

[104] Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996). Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol, 110(1): 249–257

[105] Xu Z S, Xia L Q, Chen M, Cheng X G, Zhang R Y, Li L C, Zhao Y X, Lu Y, Ni Z Y, Liu L, Qiu Z G, Ma Y Z (2007). Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol, 65(6): 719–732

[106] Xue G P (2003). The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J, 33(2): 373–383

[107] Yamaguchi-Shinozaki K, Shinozaki K (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell, 6(2): 251–264

[108] Yamaguchi-Shinozaki K, Shinozaki K (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol, 57(1): 781–803

[109] Yamamoto S, Suzuki K, Shinshi H (1999). Elicitor-responsive, ethylene-independent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. Plant J, 20(5): 571–579

[110] Yi S Y, Kim J H, Joung Y H, Lee S, Kim W T, Yu S H, Choi D (2004). The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol, 136(1): 2862–2874

[111] Zhang J Y, Broeckling C D, Blancaflor E B, Sledge M K, Sumner L W, Wang Z Y (2005). Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J, 42(5): 689–707

[112] Zhou J, Tang X, Martin G B (1997). The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J, 16(11): 3207–3218

[113] Zhu J K (2002). Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 53(1): 247–273

Acknowledgements

This work was supported by the Natural Science Foundation of Hebei, China (No. C2010000752), the National Transgenic Major Program, China (No. 2009ZX08002-012B) and the Key Crop Growth Regulation Laboratory of Hebei Province, China.

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