Identification and functional characterization of ten AP2/ERF genes in potato

Donia Bouaziz1, Mariam Charfeddine2, Rania Jbir1, Mohammed Najib Saidi3, Julien Pirrello4, Safa Charfeddine2, Mondher Bouzayen4, Radhia Gargouri-Bouzid2
1Laboratoire des Biotechnologies Végétales Appliquées à l'Amélioration des Cultures, Ecole Nationale d'Ingénieurs de Sfax, Route Soukra Km 4, BP 1173, 3038 Sfax, Tunisia
2Unité d’Enzymes et Bioconversion, Ecole Nationale d’Ingénieurs de Sfax, Route Soukra Km 4, BP 1173, 3038, Sfax, Tunisia
3Laboratoire de Protection et Amélioration des Plantes, Centre de Biotechnologie de Sfax (CBS), BP 1177, 3018, Sfax, Tunisia
4INP-ENSA Toulouse, Génomique et Biotechnologie des Fruits, Université de Toulouse, Avenue de l’Agrobiopole, BP 32607, 31326, Castanet-Tolosan, France

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Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signaling. Biol Plant 54:201–212

Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

Behnam B, Kikuchi K, Celebi-Toprak F, Yamanaka S, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2006) The Arabidopsis DREB1A gene driven by the stress-inducible rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotechnol 23:169–177

Behnam B, Kikuchi A, Celebi-Toprak F, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2007) Arabidopsis rd29A:DREB1A enhances freezing tolerance in transgenic potato. Plant Cell Rep 26:1275–1282

Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32

Bouaziz D, Pirrello J, Ben Amor H, Hammami A, Charfeddine M, Dhieb A et al (2012) Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiol Biochem 60:98–108

Bouaziz D, Pirrello J, Charfeddine M, Hammami A, Jbir R, Dhieb A et al (2013) Overexpression of StDREB1 transcription factor increases tolerance to salt in transgenic potato plants. Mol Bio 54(3):803–817

Bouaziz D, Jbir R, Charfeddine S, Saidi MN, Gargouri-Bouzid R (2015) The StDREB1 transcription factor is involved in oxidative stress response and enhances tolerance to salt stress. Plant Cell Tissue Organ Cult 121:237–248

Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang LM, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, Campagne MMV (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

Camire ME, Kubow S, Donnelly DJ (2009) Potatoes and human health. Crit Rev Food Sci Nutr 49:823–840

Cao Y, Song F, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163:1167–1178

Celebi-Toprak F, Behnam B, Serrano G, Kasuga M, Yamaguchi-Shinozaki K, Naka H, Watanabe JA, Yamanaka S, Watanabe KN (2005) Tolerance to salt stress of the transgenic tetrasomic tetraploid potato, Solanum tuberosum cv. Desiree appears to be induced by the DREB1A gene and rd29A promoter of Arabidopsis thaliana. Breed Sci 55:31–319

Charfeddine M, Bouaziz D, Charfeddine S, Hammami A, Nouri-Ellouz O, Gargouri Bouzid R (2015a) Overexpression of dehydration responsive element binding 1 protein (DREB1) in transgenic Solanum tuberosum enhances tolerance to biotic stress. Plant Biotechnol Rep 9:79–88

Charfeddine M, Saϊdi MN, Charfeddine S, Hammami A, Gargouri Bouzid R (2015b) Genome-wide analysis and expression profiling of the ERF transcription factor family in potato (Solanum tuberosum L.). Mol Biotechnol 57:348–358

Chuang HW, Harnrak A, Chen YC, Hsu CM (2010) A harpin-induced ethylene-responsive factor regulates plant growth and responses to biotic and abiotic stresses. Biochem Biophys Res Commun 402:414–420

Djébali N, Belhassen T (2010) Field study of the relative susceptibility of eleven potato (Solanum tuberosum L.) varieties and the efficacy of two fungicides against Rhizoctonia solani attack. Crop Prot 29:998–1002

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

Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

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. The Plant J. 33:751–763

Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, 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

Fang YJ, You J, Xie KB, Xie WB, Xiong LZ (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563

Fujimoto SY, 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 12:393–404

Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Proteins identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook. Humana Press, New York, pp 571–607

Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

Hao DY, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethyleneresponsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861

Hemalatha N, Rajesh MK, Narayanan NK (2012) Genome-wide analysis of putative ERF and DREB gene families in Indica Rice (O. sativa L. subsp. Indica). Int J Mach Learn Comput 2:188

Hernandez JA, Ferrer M, Jiménez A, Ros-Barcelo A, Sevilla F (2001) Antioxidant systems and O−2/H2O2 production with NaCl-induced necrotic lesions in minor veins. Plant Cell Environ 23:853–862

HongBo S, ZongSuo L, MingAn S (2006) Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloids Surf B Biointerfaces 47:132–139

Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094

Huang B, Jin L, Liu J (2007) Molecular cloning and functional characterization of a DREB1/CBF-like gene (GhDREB1L) from cotton. Sci China Ser C 50:7–14

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

Jadhao KR, Samal KC, Pradhan SK, Rout GR (2014) Studies on molecular characterization of DREB gene in Indica Rice (Oryza sativa L.). Hered Genet 3:133

Jin LG, Liu JY (2008) Molecular cloning, expression profile and promoter analysis of a novel ethylene responsive transcription factor gene GhERF4 from cotton. Plant Physiol Biochem 46:46–53

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 Organ Cult 100:219–227

Kizis D, Pages 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 30:679–689

Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189

Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

Lata C, Yadav A, Prasad M (2011) Role of plant transcription factors in abiotic stress tolerance. In: Shanker A (ed) Abiotic stress/Book2. INTECH Open Access Publishers, Rijeka. ISBN 979-953-307-195-3

Lata C, Mishra AK, Muthamilarasan M, Bonthala VS, Khan Y, Prasad M (2014) Genome-wide investigation and expression profiling of AP2/ERF transcription factor superfamily in foxtail millet (Setaria italica L.). PLoS One 9:e113092

Le DT, Nishiyama R, Watanabe Y, Vankova R, Tanaka M et al (2012) Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels. PLoS One 7(8):e42411

Lee HE, Shin D, Park SR, Han SE, Jeong MJ, Kwon TR, Lee SK, Park SC, Yi BY, Kwon HB, Byun MO (2007) Ethylene responsive element binding protein 1 (StEREBP1) from Solanum tuberosum increases tolerance to abiotic stress in transgenic potato plants. Biochem Biophys Res Commun 353:863–868

Lee SC, Choi DS, Hwang IS, Hwang BK (2010) The pepper oxidoreductase CaOXR1 interacts with the transcription factor CaRAV1 and is required for salt and osmotic stress tolerance. Plant Mol Biol 73:409–424

Li CW, Su RC, Cheng CP, Sanjaya You SJ, Hsieh TH, Chao TC, Chan MT (2011) Tomato RAV transcription factor is a pivotal modulator involved in the AP2/EREBP-mediated defense pathway. Plant Physiol 156:213–227

Li JW, Wang B, Song XM, Wang RR, Chen L, Zhang H et al (2013) Potato leafroll virus (PLRV) and potato virus Y (PVY) influence vegetative growth, physiological metabolism, and microtuber production of in vitro grown shoots of potato (Solanum tuberosum L.). Plant Cell Tissue Organ Cult 114:313–324

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 Genomics 11:719

Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

Lin RC, Park HJ, Wang HY (2008) Role of Arabidopsis RAP2.4 in regulating light and ethylene-mediated developmental processes and drought stress tolerance. Mol Plant 1:42–57

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 10:1391–1406

Liu Y, Zhao TJ, Liu JM, Liu WQ, Liu Q, Yan YB et al (2006) The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett 580:1303–1308

Massa AN, Childs KL, Lin H, Bryan GJ, Giuliano G, Buell CR (2011) The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44. PLoS One 6:e26801

McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15:473–497

Nadarajah K, Omar NS, Thing TY (2014) Molecular characterization of a WRKY gene from Oryza sativa indica cultivar UKMRC9. POJ 7:63–71

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

Nakano T, Suzuki K, Ohtsuki N, Tsujimoto Y, Fujimura T, Shinshi H (2006b) Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana. J Plant Res 119:407–413

Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575

Nouri-Ellouz O, Gargouri-Bouzid R, Sihachakr D, Triki MA, Ducreux G, Drira N, Lakhoua L (2006) Production of potato intraspecific somatic hybrids with improved tolerance to PVY and Pythium aphanidermatum. J Plant Physiol 163:1321–1332

Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351

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

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

Okamuro JK, Caster B, Villarroel R, Montagu MV, 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

Omidvar V, Abdullah SNA, Ho CL, Mahmood M (2013) Isolation and characterization of an ethylene-responsive element binding protein (EgEREBP) from oil palm (Elaeis guineensis). Aust J Crop Sci 7(2):219–226

Oñate Sánchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a non redundant role in plant defence. Plant Physiol 143:400–409

Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Over-expression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

Peng X, Zhang L, Zhang L, Liu Z, Cheng L, Yang Y, Shen S, Chen S, Liu G (2012) The transcriptional factor LcDREB2 cooperates with LcSAMDC2 to contribute to salt tolerance in Leymus chinensis. Plant Cell Tissue Organ Cult 113:245–256

Pino MT, Skinner JS, Jeknic Z, Park EJ, Hayes PM, Chen THH (2007) Ectopic overexpression of AtCBF1 in potato enhances freezing tolerance in: cold hardiness in plants: molecular genetics. Plant Biotechnol J 5:676

Pirrello J, Prasad BN, Zhang W, Chen K, Mila I, Zouine M, Latche A, Pech JC, Ohme-Takagi M, Regad F, Bouzayen M (2012) Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol 12:190

Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

Roosens NH, Al Bitar F, Loenders K, Angenon G, Jacobs M (2002) Overexpression of ornithine-delta-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Mol Breed 9:73–80

Saeed AI, Hagabati NK, Braisted JC, Liang W, Sharov V, Howe EA et al (2006) TM4 microarray software suite. Methods Enzymol 411:134–193

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. Biochem Biophys Res Commun 290:998–1009

Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

Schenk PM, Kazan K, Wilson I et al (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

Sherraf I, Tizroutine S, Chaput MH, Allot M, Mussio I, Sihachaker D, Rossignol L, Ducreux G (1994) Production and characterization of intergeneric somatic hybrids through protoplast electrofusion between potato (Solanum tuberosum L.) and Lycopersicon pennelli. Plant Cell Tissue Organ Cult 37:137–144

Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

Song X, Li Y, Hou X (2013) Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genomics 14:573

Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12:557–569

Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ et al (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

Taji T, Oshumi C, Luchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular revolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latche A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550:149–154

Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Correa Molinari HB, Marur CJ, Esteves Vieira LG (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376

Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

Wang X, Dong J, Liu Y, Gao H (2010) A novel dehydration-responsive element-binding protein from Caragana korshinskiiis involved in the response to multiple abiotic stresses and enhances stress tolerance in transgenic tobacco. Plant Mol Biol Rep 28:664–675

Watanabe KN, Kikuchi A, Shimazaki T, Asahina M (2011) Salt and drought stress tolerances in transgenic potatoes and wild species. Potato Res 54:319–324

Wei G, Pan Y, Lei J, Zhu YX (2005) Molecular cloning, phylogenetic analysis, expressional profiling and in vitro studies of TINY2 from Arabidopsis thaliana. J Biochem Mol Biol 38:440–446

Weisz R, Kaminski J, Smilowitz Z (1994) Water deficit effects on potato leaf growth and transpiration: utilizing fraction extractable soil water for comparison with other crops. Am Potato J 71:829–840

Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

Xu ZS, Chen M, Li LC, Ma YZ (2008) Functions of the ERF transcription factor family in plants. Botany 86:969–977

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

Xu W, Li F, Ling L, Liu A (2013) Genome-wide survey and expression profiles of the AP2/ERF family in castor bean (Ricinus communis L.). BMC Genomics 14:785

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

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

Zhang GY, Chen M, Chen XP, Xu ZS, Guan S, Li LC, Li AL, Guo JM, Mao L, Ma YZ (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107

Zhao MG, Tian QT, Zhang WH (2007) Nitric oxide synthase dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217

Zhou D, Kalaitzis P, Mattoo AK, Tucker ML (1996) The mRNA for an ETR1 homologue in tomato is constitutively expressed in vegetative and reproductive tissues. Plant Mol Biol 30:1331–1338

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

Zhuang J, Xiong AS, Peng RH, Gao F, Zhu B, Zhang J, Fu XY, Jin XF, Chen JM, Zhang Z et al (2010) Analysis of Brassica rapa ESTs: gene discovery and expression patterns of AP2/ERF family genes. Mol Biol Rep 37(5):2485–2492

Zhuang J, Chen JM, Yao QH, Xiong F, Sun CC, Zhou XR, Zhang J, Xiong AS (2011a) Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum. Mol Biol Rep 38:745–753

Zhuang J, Yao Q-H, Xiong A-S, Zhang J (2011b) Isolation, phylogeny and expression patterns of AP2-like genes in apple (Malus × domestica Borkh). Plant Mol Biol Rep 29:209–216