Functional role of DREB and ERF transcription factors: regulating stress-responsive network in plants

Acta Physiologiae Plantarum

Volumn 37, Issue 9, 2015, Pages

  Rehman, Shazia ^a   Mahmood, Tariq ^a  

^a QUAID I AZAM UNIVERSITY   (Pakistan)

Author keywords

AP2 ERF transcription factors; Diverse functions; Plant tolerance; Stress regulation

Indexed keywords

DICOTYLEDONEAE; LILIOPSIDA;

EID: 84938692494     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-015-1929-1     Document Type: Review

References (107)

1. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645
2. Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37:1125–1135
3. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479
4. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, León P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14:2085–2096
5. Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966
6. Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353(2):299–305
7. Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198
8. Chen M, Xu Z, Xia L, Li L, Cheng X, Dong J, Wang Q, Ma Y (2009) Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). J Exp Bot 60(1):121–135
9. Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787
10. Cong L, Chai T, Zhang Y (2008) Characterization of the novel gene BjDREB1B encoding a DRE-binding transcription factor from Brassica juncea L. Biochem Biophys Res Commun 371:702–706
11. De Boer K, Tilleman S, Pauwels L, Vanden Bossche R, De Sutter V, Vanderhaeghen R, Hilson P, Hamill JD, Goossens A (2011) APETALA2/Ethylene response factor and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J. doi:10.1111/j.1365-313X.2011.04566.x[Epub ahead of print]
12. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984
13. Dong CJ, Liu JY (2010) The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biol 10:47
14. Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103:8281–8286
15. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, 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 33:751–763
16. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168
17. Fischer U, Dröge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Inter 17:1162–1171
18. Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23:412–427
19. Gao S, Zhang H, Tian Y, Li F, Zhang Z, Lu X, Chen X, Huang R (2008) Expression of TERF1 in rice regulates expression of stress-responsive genes and enhances tolerance to drought and high-salinity. Plant Cell Rep 27:1787–1795
20. Gao SQ, Chen M, Xia LQ, Xiu HJ, Xu ZS, Li LC, Zhao CP, Cheng XG, Ma YZ (2009) A cotton (Gossypium hirsutum) DRE-binding transcription factor gene, GhDREB, confers enhanced tolerance to drought, high salt, and freezing stresses in transgenic wheat. Plant Cell Rep 28(2):301–311
21. Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the over-expression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68:533–555
22. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471
23. Haake V, Cook D, Riechmann J, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648
24. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030
25. Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R (2010) ArabidopsisRAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 153:757–772
26. Huang B, Jin L, Liu JY (2008) Identification and characterization of the novel gene GhDBP2 encoding a DRE-binding protein from cotton (Gossypium hirsutum). J Plant Physiol 165:214–223
27. Hubbard KE, Siegel RS, Valerio G, Brandt B, Schroeder JI (2012) Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses. Ann Bot 109:5–17
28. Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, Zheng SH, Yuasa T, Iwaya-Inoue M (2012) Reactive Oxygen Species Are Involved in Gibberellin/Abscisic Acid Signaling in Barley Aleurone Cells. Plant Physiol 158:1705–1714
29. 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 47:141–153
30. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467
31. Jin LG, Liu JY (2008) Molecular cloning, expression profile and promoter analysis of a novel ethylene responsive transcription factor gene GhERF4 from cotton (Gossypium hirsutum). Plant Physiol Biochem 46:46–53
32. Jin TC, Chang Q, Li WF, Yin DX, Li ZJ, Wang DL, Liu B, Liu LX (2010) Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell, Tissue and Organ Culture 100(2):219–227
33. Jin X, Xue Y, Wang R, Xu R, Bian L, Zhu B, Han H, Peng R, Yao Q (2013) Transcription factor OsAP21 gene increases salt/drought tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 40:1743–1752
34. Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y, Hwang I, Kim M (2007) The barley ERF-type tran-scription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 225:575–588
35. Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282–294
36. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
37. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350
38. Kobayashi F, Ishibashi M, Takumi S (2007) Transcriptional activation of Cor/Lea genes and increase in abiotic stress tolerance through expression of a wheat DREB2 homolog in transgenic tobacco. Transgen Res 17:755–767
39. Krishnaswamy S, Verma S, Rahman MH, Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127
40. Lee JH, Kim DM, Lee JH, Kim J, Bang JW, Kim WT, Pai HS (2005) Functional characterization of NtCEF1, an AP2/EREBP-type transcriptional activator highly expressed in tobacco callus. Planta 222:211–224
41. Licausi F, Giorgi FM, Zenoni S, Osti F, Pezzotti M, Perata P (2010) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genom 11:719–734
42. Lim CJ, Hwang JE, Chen H, Hong JK, Yang KA, Choi MS, Lee KO, Chung WS, Lee SY, Lim CO (2007) Over-expression of the Arabidopsis DRE/CRT-binding transcription factor DREB2C enhances thermotolerance. Biochem Biophys Res Commun 362:431–436
43. Lin RC, Park HJ, Wang HY (2008) Role of ArabidopsisRAP2.4 in regulating light and ethylene-mediated developmental processes and drought stress tolerance. Mol Plant 1:42–57
44. Lindemose S, O’Shea C, Jensen M, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878
45. 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 10:391–406
46. Liu N, Zhong N, Wang G, Li L, Liu X, He Y, Xia G (2007) Cloning and functional characterization of PpDBF1 gene encoding a DRE binding transcription factor from Physcomitrella patens. Planta 226:827–838
47. Lucas S, Durmaz E, Akpınar BA, Budak H (2011) The drought response displayed by a DRE-binding protein from Triticum dicoccoides. Plant Physiol Biochem 49:346–351
48. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the ArabidopsisDREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993
49. Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics 283:185–196
50. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96
51. Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249
52. Movahedi S, Sayed Tabatabaei BE, Alizade H, Ghobadi C, Yamchi A, Khaksar G (2012) Constitutive expression of Arabidopsis DREB1B in transgenic potato enhances drought and freezing tolerance. Biol Plant 56:37–42
53. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432
54. Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363
55. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two ArabidopsisDREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
56. Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575
57. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim MJ, Kim YK, Nahm BH, Kim JK (2005) ArabidopsisCBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351
58. Oh SJ, Kwon CW, Choi DW, Song SIK, Kim JK (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. J Plant Biotechnol 5:646–656
59. Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968
60. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081
61. Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thalianaDREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493–500
62. Perata P, Voesenek LA (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci 12:43–46
63. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi- Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052
64. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69
65. Qin F, Sakuma Y, Tran LSP, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi- Shinozaki K (2008) ArabidopsisDREB2A interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693–1707
66. Rashid M, Guangyuan H, Guangxiao Y, Hussain J, Xu Y (2012) A 2/RF transcription factor in rice: genome-wide canvas and syntenic relationships between monocots and eudicots. Evol Bioinform 8:321–355
67. Sakuma Y, Liu Q, Dubouzet JG, 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. Biophys Res Commun 290:998–1009
68. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309
69. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi- Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827
70. Sharma M, Kumar R, Solanke A, Sharma R, Tyagi A, Sharma A (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284:455–475
71. Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360
72. Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003a) An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106:923–930
73. Shen YG, Zhang WK, Yan DQ, Du BX, Zhang JS, Liu Q, Chen SY (2003b) Characterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis. Theor Appl Genet 107:155–161
74. Shin R, Park JM, An JM, Paek KH (2002) Ectopic expression of Tsi1 in transgenic hot pepper plants enhances host resistance to viral, bacterial, and oomycete pathogens. Mol Plant Microbe Interact 15:983–989
75. Shukla RK, 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 142:113–123
76. Shukla RK, Tripathi V, Jain D, Yadav RK, Chattopadhyay D (2009) CAP2 enhances germination of transgenic tobacco seeds at high temperature and promotes heat stress tolerance in yeast. FEBS J 276:5252–5262
77. Siddiqua M, Nassuth A (2011) Vitis CBF1 and Vitis CBF4 differ in their effect on Arabidopsis abiotic stress tolerance, development and gene expression. Plant, Cell Environ 34:1345–1359
78. Söderman EM, Brocard IM, Lynch TJ, Finkelstein RR (2000) Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol 124:1752–1765
79. Stockinger EJ, Gilmour SJ, Thomashow MF (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 94:1035–1040
80. Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF (2008) TINY, a dehydration-responsive element (DRE)-binding protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 283:6261–6271
81. Taketa S, Amano S, Tsujino Y, Sato T, Saisho D, Kakeda K, Nomura M, Suzuki T, Matsumoto T, Sato K, Kanamori H, Kawasaki S, Takeda K (2008) Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105:4062–4067
82. Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinusvirginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617
83. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
84. Tong Z, Hong B, Yang Y, Li Q, Ma N, Ma C, Gao J (2009) Overexpression of two chrysanthemum DgDREB1 group genes causing delayed flowering or dwarfism in Arabidopsis. Plant Mol Biol 71:115–129
85. Trujillo LE, Sotolongo M, Menéndez C, Ochogavía ME, Coll Y, Hernández I, Borras-Hidalgo O, Thomma BPHJ, Vera P, Hernandez L (2008) SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant Cell Physiol 49:512–515
86. Vernié T, Moreau S, de Billy F, Plet J, Combier JP, Rogers C, Oldroyd G, Frugier F, Niebel A, Gamas P (2008) EFD Is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20:2696–2713
87. Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602
88. Welling A, Palva ET (2008) Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol 147:1199–1211
89. Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of Tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963
90. Xu ZS, Ni ZY, Li ZY, Li LC, Chen M, Gao DY, Yu XD, Liu P, Ma YZ (2009) Isolation and functional characterization of HvDREB1-a gene encoding a dehydration-responsive element binding protein in Hordeum vulgare. J Plant Res 122:121–130
91. Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585
92. Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326–339
93. Yan HW, Hong L, Zhou YQ, Jiang HY, Zhu SW, Fan J, Cheng BJ (2013) A genome-wide analysis of the ERF gene family in sorghum. Genet Mol Res 12:2038–2055
94. Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219–229
95. Zarei A, Korbes AP, Younessi P, Montiel G, Champion A, Memelink J (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol Biol 75:321–331
96. Zhai Y, Wang Y, Li Y, Lei T, Yan F, Su L, Li X, Zhao Y, Sun X, Li J, Wang Q (2013) Isolation and molecular characterization of GmERF7, a soybean ethylene-response factor that increases salt stress tolerance in tobacco. Gene 513:174–183
97. Zhang Z, Huang R (2010) Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol 73:241–249
98. Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Thomashow MF (2004a) Freezing sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39:905–919
99. Zhang H, Zhang D, Chen J, Yang Y, Huang Z, Huang D, Wang XC, Huang R (2004b) Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol Biol 55:825–834
100. Zhang X, Zhang Z, Chen J, Chen Q, Wang XC, Huang R (2005) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222:494–501
101. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107
102. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796
103. Zhang G, Chen M, Chen X, Xu Z, Li L, Guo J, Ma Y (2010a) Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Mol Biol Rep 37:809–818
104. Zhang H, Liu W, Wan L, Li F, Dai L, Li D, Zhang Z, Huang R (2010b) Functional analyses of ethylene response factor JERF3 with the aim of improving tolerance to drought and osmotic stress in transgenic rice. Transgenic Res 19:809–818
105. Zhang Z, Li F, Li D, Zhang H, Huang R (2010c) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232:765–774
106. Zhou M, Ma J, Pang J, Zhang Z, Tang Y, Wu Y (2010) Regulation of plant stress response by dehydration responsive element binding (DREB) transcription factors. Afr J Biotechnol 9:9255–9279
107. Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH (2008) Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Commun 371:468–474