Functional & Integrative Genomics

, Volume 15, Issue 1, pp 27–46 | Cite as

The CarERF genes in chickpea (Cicer arietinum L.) and the identification of CarERF116 as abiotic stress responsive transcription factor

  • Amit A. Deokar
  • Vishwajith Kondawar
  • Deshika Kohli
  • Mohammad Aslam
  • Pradeep K. Jain
  • S. Mohan Karuppayil
  • Rajeev K. Varshney
  • Ramamurthy Srinivasan
Original Paper

Abstract

The AP2/ERF family is one of the largest transcription factor gene families that are involved in various plant processes, especially in response to biotic and abiotic stresses. Complete genome sequences of one of the world’s most important pulse crops chickpea (Cicer arietinum L.), has provided an important opportunity to identify and characterize genome-wide ERF genes. In this study, we identified 120 putative ERF genes from chickpea. The genomic organization of the chickpea ERF genes suggested that the gene family might have been expanded through the segmental duplications. The 120 member ERF family was classified into eleven distinct groups (I-X and VI-L). Transcriptional factor CarERF116, which is differentially expressed between drought tolerant and susceptible chickpea cultivar under terminal drought stress has been identified and functionally characterized. The CarERF116 encodes a putative protein of 241 amino acids and classified into group IX of ERF family. An in vitro CarERF116 protein-DNA binding assay demonstrated that CarERF116 protein specifically interacts with GCC box. We demonstrate that CarERF116 is capable of transactivation activity of and show that the functional transcriptional domain lies at the C-terminal region of the CarERF116. In transgenic Arabidopsis plants overexpressing CarERF116, significant up-regulation of several stress related genes were observed. These plants also exhibit resistance to osmotic stress and reduced sensitivity to ABA during seed germination. Based on these findings, we conclude that CarERF116 is an abiotic stress responsive gene, which plays an important role in stress tolerance. In addition, the present study leads to genome-wide identification and evolutionary analyses of chickpea ERF gene family, which will facilitate further research on this important group of genes and provides valuable resources for comparative genomics among the grain legumes.

Keywords

Chickpea (Cicer arietinum L.) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors Genome-wide analysis Abiotic stress response 

Supplementary material

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References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78. doi:10.1105/tpc.006130 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Agarwal M, Hao YJ, Kapoor A, Dong CH, Fujii H, Zheng XW, 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. doi:10.1074/jbc.M605895200 PubMedCrossRefGoogle Scholar
  3. Allen MD, 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 17:5484–5496. doi:10.1093/emboj/17.18.5484 PubMedCentralPubMedCrossRefGoogle Scholar
  4. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659. doi:10.1104/pp. 104.052084 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Balaji S, Babu MM, Iyer LM, Aravind L (2005) Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 33:3994–4006. doi:10.1093/nar/gki709 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435. doi:10.1023/a:1006058700720 PubMedCrossRefGoogle Scholar
  7. Campos-Soriano L, Gomez-Ariza J, Bonfante P, Segundo BS (2011) A rice calcium-dependent protein kinase is expressed in cortical root cells during the presymbiotic phase of the arbuscular mycorrhizal symbiosis. BMC Plant Biol 11 doi:10.1186/1471-2229-11-90
  8. Carvalho LC, Santos S, Vilela BJ, Amancio S (2008) Solanum lycopersicon Mill. and Nicotiana benthamiana L. under high light show distinct responses to anti-oxidative stress. J Plant Physiol 165:1300–1312. doi:10.1016/j.jplph.2007.04.009 PubMedCrossRefGoogle Scholar
  9. Chen H, Nelson RS, Sherwood JL (1994) Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotech 16(4):664–668Google Scholar
  10. Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC et al (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972PubMedCentralPubMedCrossRefGoogle Scholar
  11. Cho SK, Kim JE, Park JA, Eom TJ, Kim WT (2006) Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580:3136–3144. doi:10.1016/j.febslet.2006.04.062 PubMedCrossRefGoogle Scholar
  12. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x PubMedCrossRefGoogle Scholar
  13. Dai XY, Xu YY, Ma QB, Xu WY, Wang T, Xue YB, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143:1739–1751. doi:10.1104/pp. 106.094532 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Dalal M, Tayal D, Chinnusamy V, Bansal KC (2009) Abiotic stress and ABA-inducible group 4 LEA from Brassica napus plays a key role in salt and drought tolerance. J Biotechnol 139:137–145. doi:10.1016/j.jbiotec.2008.09.014 PubMedCrossRefGoogle Scholar
  15. Dellaporta S, Wood J, Hicks J (1983) A plant DNA minipreparation: version II plant. Mol Biol Rep 1:19–21. doi:10.1007/BF02712670 CrossRefGoogle Scholar
  16. Deokar AA, Kondawar V, Jain PK, Karuppayil SM, Raju NL, Vadez V, Varshney RK, Srinivasan R (2011) Comparative analysis of expressed sequence tags (ESTs) between drought-tolerant and -susceptible genotypes of chickpea under terminal drought stress. BMC Plant Biol 11 doi:10.1186/1471-2229-11-70
  17. Dong N, Liu X, Lu Y, Du LP, Xu HJ, Liu HX, Xin ZY, Zhang ZY (2010) Overexpression of TaPIEP1, a pathogen-induced ERF gene of wheat, confers host-enhanced resistance to fungal pathogen Bipolaris sorokiniana. Funct Integr Genomic 10:215–226. doi:10.1007/s10142-009-0157-4 CrossRefGoogle Scholar
  18. Elmayan T, Tepfer M (1995) Evaluation in tobacco of the organ specificity and strength of the rold promoter, domain-A of the 35S promoter and the 35S (2) promoter. Transgenic Res 4:388–396. doi:10.1007/bf01973757 PubMedCrossRefGoogle Scholar
  19. FAOSTAT (2012). http://faostat.fao.org/.
  20. Fehlberg V, Vieweg MF, Dohmann EMN, Hohnjec N, Puhler A, Perlick AM, Kuster H (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. J Exp Bot 56:799–806. doi:10.1093/jxb/eri074 PubMedCrossRefGoogle Scholar
  21. 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. doi:10.2307/3870944 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Gu YQ, Yang C, Thara VK, Zhou J, Martin GB (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12:771–785. doi:10.2307/3871000 PubMedCentralPubMedCrossRefGoogle Scholar
  23. Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin GB (2002) Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14:817–831. doi:10.1105/tpc.000794 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Guo YL (2013) Gene family evolution in green plants with emphasis on the origination and evolution of Arabidopsis thaliana genes. Plant J 73:941–951. doi:10.1111/tpj.12089 PubMedCrossRefGoogle Scholar
  25. Haberer G, Kieber JJ (2002) Cytokinins. New insights into a classic phytohormone. Plant Physiol 128:354–362. doi:10.1104/pp. 010773 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21:3029–3038. doi:10.1093/emboj/cdf316 PubMedCentralPubMedCrossRefGoogle Scholar
  27. Horan K, Shelton CR, Girke T (2010) Predicting conserved protein motifs with Sub-HMMs. BMC Bioinforma 11:205. doi:10.1186/1471-2105-11-205 CrossRefGoogle Scholar
  28. Hu YB, Chong K, Wang T (2008) OsRAF is an ethylene responsive and root abundant factor gene of rice. Plant Growth Regul 54:55–61. doi:10.1007/s10725-007-9228-5 CrossRefGoogle Scholar
  29. Huang ZJ, Zhang ZJ, Zhang XL, Zhang HB, Huang DF, Huang RF (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573:110–116. doi:10.1016/j.febslet.2004.07.064 PubMedCrossRefGoogle Scholar
  30. Hwang SH, Lee IA, Yie SW, Hwang DJ (2008) Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227:1141–1150. doi:10.1007/s00425-007-0687-8 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Jacquemin J, Ammiraju JS, Haberer G, Billheimer DD, Yu Y, Liu LC, Rivera LF, Mayer K, Chen M, Wing RA (2014) Fifteen million years of evolution in the oryza genus shows extensive gene family expansion. Mol Plant 7:642–656. doi:10.1093/mp/sst149 PubMedCrossRefGoogle Scholar
  32. Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y, Hwang I, Kim M (2007) The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 225:575–588. doi:10.1007/s00425-006-0373-2 PubMedCrossRefGoogle Scholar
  33. Kagale S, Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6:141–146PubMedCentralPubMedCrossRefGoogle Scholar
  34. Kaur H, Verma P, Petla BP, Rao V, Saxena SC, Majee M (2013) Ectopic expression of the ABA-inducible dehydration-responsive chickpea L-myo-inositol 1-phosphate synthase 2 (CaMIPS2) in Arabidopsis enhances tolerance to salinity and dehydration stress. Planta 237:321–335. doi:10.1007/s00425-012-1781-0 PubMedCrossRefGoogle Scholar
  35. Klinedinst S, Pascuzzi P, Redman J, Desai M, Arias J (2000) A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Mol Biol 42:679–688PubMedCrossRefGoogle Scholar
  36. Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355. doi:10.1111/j.1365-313X.2006.02782.x PubMedCrossRefGoogle Scholar
  37. Lee JH, Hong JP, Oh SK, Lee S, Choi D, Kim WT (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 55:61–81. doi:10.1007/s11103-004-0417-6 PubMedCrossRefGoogle Scholar
  38. 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. doi:10.1186/1471-2164-11-719 PubMedCentralPubMedCrossRefGoogle Scholar
  39. Liu Z, Kong L, Zhang M, Lv Y, Liu Y, Zou M, Lu G, Cao J, Yu X (2013) Genome-wide identification, phylogeny, evolution and expression patterns of AP2/ERF genes and cytokinin response factors in Brassica rapa ssp. pekinensis. PLoS One 8:e83444PubMedCentralPubMedCrossRefGoogle Scholar
  40. Medina J, Ballesteros ML, Salinas J (2007) Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J Exp Bot 58:4333–4346. doi:10.1093/jxb/erm285 PubMedCrossRefGoogle Scholar
  41. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96. doi:10.1016/j.bbagrm.2011.08.004 PubMedCrossRefGoogle Scholar
  42. 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. doi:10.1104/pp. 105.073783 PubMedCentralPubMedCrossRefGoogle Scholar
  43. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379. doi:10.1104/pp. 109.137554 PubMedCentralPubMedCrossRefGoogle Scholar
  44. 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 U S A 94:7076–7081. doi:10.1073/pnas.94.13.7076 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (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 13:1035–1046. doi:10.2307/3871362 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753. doi:10.1023/B:PLAN.0000040903.66496.a4 PubMedCrossRefGoogle Scholar
  47. Qiu YP, Yu DQ (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47. doi:10.1016/j.envexpbot.2008.07.002 CrossRefGoogle Scholar
  48. Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429. doi:10.1111/j.1365-313X.2010.04248.x PubMedCentralPubMedCrossRefGoogle Scholar
  49. Saibo NJM, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Annals Bot 103:609–623. doi:10.1093/aob/mcn227 CrossRefGoogle Scholar
  50. 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 Bioph Res Co 290:998–1009. doi:10.1006/bbrc.2001.6299 CrossRefGoogle Scholar
  51. Sambrook J, Rusell DW (2001) Molecular Cloning: A Laboratory Manual Volume 1. Cold Spring Harbor. CSHL Press, New YorkGoogle Scholar
  52. Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR et al (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131. doi:10.1105/tpc.113.113068 PubMedCentralPubMedCrossRefGoogle Scholar
  53. 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. doi:10.1093/pcp/pcq196 PubMedCrossRefGoogle Scholar
  54. Shimada TL, Shimada T, Takahashi H, Fukao Y, Hara-Nishimura I (2008) A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. Plant J 55:798–809. doi:10.1111/j.1365-313X.2008.03553.x PubMedCrossRefGoogle Scholar
  55. 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. doi:10.1016/s1369-5266(00)80068-0 PubMedCrossRefGoogle Scholar
  56. 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. doi:10.1104/pp. 106.081752 PubMedCentralPubMedCrossRefGoogle Scholar
  57. Stougaard J, Jorgensen JE, Christensen T, Kuhle A, Marcker KA (1990) Interdependence and nodule specificity of cis-acting regulatory elements in the soybean leghemoglobin-lbc3 and n23 gene promoters. Mol Gen Genet 220:353–360. doi:10.1007/bf00391738 PubMedCrossRefGoogle Scholar
  58. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121 PubMedCentralPubMedCrossRefGoogle Scholar
  59. Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic virginia pine (Pinus virginiana mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617. doi:10.1007/s11103-005-0451-z PubMedCrossRefGoogle Scholar
  60. Tapia G, Verdugo I, Yañez M, Ahumada I, Theoduloz C, Cordero C, Poblete F, González E, Ruiz-Lara S (2005) Involvement of ethylene in stress-induced expression of the TLC1.1 retrotransposon from Lycopersicon chilense Dun. Plant Physiol 138:2075–2086. doi:10.1104/pp.105.059766 PubMedCentralPubMedCrossRefGoogle Scholar
  61. Tian Y, Zhang HW, Pan XW, Chen XL, Zhang ZJ, Lu XY, Huang RF (2011) Overexpression of ethylene response factor TERF2 confers cold tolerance in rice seedlings. Transgenic Res 20:857–866. doi:10.1007/s11248-010-9463-9 PubMedCrossRefGoogle Scholar
  62. Tiwari SB, Belachew A, Ma SF, Young M, Ade J, Shen Y, Marion CM, Holtan HE, Bailey A, Stone JK, Edwards L, Wallace AD, Canales RD, Adam L, Ratcliffe OJ, Repetti PP (2012) The EDLL motif: a potent plant transcriptional activation domain from AP2/ERF transcription factors. Plant J 70:855–865. doi:10.1111/j.1365-313X.2012.04935.x PubMedCrossRefGoogle Scholar
  63. Varshney RK, Hiremath PJ, Lekha P, Kashiwagi J, Balaji J, Deokar AA, Vadez V, Xiao Y, Srinivasan R, Gaur PM, Siddique KHM, Town CD, Hoisington DA (2009) A comprehensive resource of drought- and salinity-responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC Genomics 10 doi:10.1186/1471-2164-10-523
  64. Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar’an B et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246PubMedCrossRefGoogle Scholar
  65. Varshney RK, Thudi M, Nayak SN, Gaur PM, Kashiwagi J, Krishnamurthy L, Jaganathan D, Koppolu J, Bohra A, Tripathi S, Rathore A et al (2014) Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.) TAG Theoretical and applied genetics. Theor Appl Genet 127:445–462. doi:10.1007/s00122-013-2230-6 PubMedCentralPubMedCrossRefGoogle Scholar
  66. Wang H, Huang Z, Chen Q, Zhang Z, Zhang H, Wu Y, Huang D, Huang R (2004) Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol Biol 55:183–192. doi:10.1007/s11103-004-0113-6 PubMedCrossRefGoogle Scholar
  67. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and colinearity. Nucleic Acids Res 40:e49. doi:10.1093/nar/gkr1293 PubMedCentralPubMedCrossRefGoogle Scholar
  68. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217. doi:10.1093/mp/ssm022 PubMedCrossRefGoogle Scholar
  69. Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476. doi:10.1093/dnares/dss026 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Xiang Y, Tang N, Du H, Ye HY, Xiong LZ (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952. doi:10.1104/pp. 108.128199 PubMedCentralPubMedCrossRefGoogle Scholar
  71. 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. doi:10.1007/s11103-007-9237-9 PubMedCrossRefGoogle Scholar
  72. Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, Choi D (2004) The pepper transcription factor CaPF1 confers pathogen and freezing Tolerance in Arabidopsis. Plant Physiol 136:2862–2874. doi:10.1104/pp. 104.042903 PubMedCentralPubMedCrossRefGoogle Scholar
  73. Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y, Hu Y (2013) The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biol 13:148. doi:10.1186/1471-2229-13-148 PubMedCentralPubMedCrossRefGoogle Scholar
  74. Youm JW, Jeon JH, Choi D, Yi SY, Joung H, Kim HS (2008) Ectopic expression of pepper CaPF1 in potato enhances multiple stresses tolerance and delays initiation of in vitro tuberization. Planta 228:701–708. doi:10.1007/s00425-008-0782-5 PubMedCrossRefGoogle Scholar
  75. 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. doi:10.1007/s11103-010-9728-y PubMedCentralPubMedCrossRefGoogle Scholar
  76. 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. doi:10.1093/jxb/ern248 PubMedCentralPubMedCrossRefGoogle Scholar
  77. Zhang GY, Chen M, Li LC, Xu ZS, Chen XP, Guo JM, Ma YZ (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. doi:10.1093/jxb/erp214 PubMedCentralPubMedCrossRefGoogle Scholar
  78. Zhang H, Liu W, Wan L, Li F, Dai L, Li D, Zhang Z, Huang R (2010) 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. doi:10.1007/s11248-009-9357-x PubMedCrossRefGoogle Scholar
  79. Zhu Q, Dabi T, Lamb C (1995) TATA box and initiator functions in the accurate transcription of a plant minimal promoter in-vitro. Plant Cell 7:1681–1689. doi:10.2307/3870029 PubMedCentralPubMedCrossRefGoogle Scholar
  80. Zhu X, Qi L, Liu X, Cai S, Xu H, Huang R, Li J, Wei X, Zhang Z (2014) The wheat ethylene response factor transcription factor pathogen-induced ERF1 mediates host responses to both the necrotrophic pathogen Rhizoctonia cerealis and freezing stresses. Plant Physiol 164:1499–1514. doi:10.1104/pp. 113.229575 PubMedCentralPubMedCrossRefGoogle Scholar
  81. 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 Biophy Res Comm 371:468–474. doi:10.1016/j.bbrc.2008.04.087 CrossRefGoogle Scholar
  82. Zwack PJ, Robinson BR, Risley MG, Rashotte AM (2013) Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant Cell Physiol 54:971–981. doi:10.1093/pcp/pct049 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Amit A. Deokar
    • 1
    • 2
  • Vishwajith Kondawar
    • 1
    • 2
  • Deshika Kohli
    • 1
  • Mohammad Aslam
    • 1
  • Pradeep K. Jain
    • 1
  • S. Mohan Karuppayil
    • 2
  • Rajeev K. Varshney
    • 3
  • Ramamurthy Srinivasan
    • 1
  1. 1.National Research Centre on Plant BiotechnologyIARI, Pusa CampusNew DelhiIndia
  2. 2.School of Life SciencesSwami Ramanand Teerth Marathwada UniversityNandedIndia
  3. 3.International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)PatancheruIndia

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