Functional & Integrative Genomics

, Volume 14, Issue 3, pp 467–477 | Cite as

Identification of ERF genes in peanuts and functional analysis of AhERF008 and AhERF019 in abiotic stress response

  • Liyun Wan
  • Yanshan Wu
  • Jiaquan Huang
  • Xiaofeng Dai
  • Yong Lei
  • Liying Yan
  • Huifang Jiang
  • Juncheng Zhang
  • Rajeev K Varshney
  • Boshou Liao
Original Paper

Abstract

Ethylene-responsive factor (ERF) play an important role in regulating gene expression in plant development and response to stresses. In peanuts (Arachis hypogaea L.), which produce flowers aerially and pods underground, only a few ERF genes have been identified so far. This study identifies 63 ERF unigenes from 247,313 peanut EST sequences available in the NCBI database. The phylogeny, gene structures, and putative conserved motifs in the peanut ERF proteins were analysed. Comparative analysis revealed the absence of two subgroups (A1 and A3) of the ERF family in peanuts; only 10 subgroups were identified in peanuts compared to 12 subgroups in Arabidopsis and soybeans. AP2/ERF domains were found to be conserved among peanuts, Arabidopsis, and soybeans. Outside the AP2/ERF domain, many soybean-specific conserved motifs were also detected in peanuts. The expression analysis of ERF family genes representing each clade revealed differential expression patterns in response to biotic and abiotic stresses. Overexpression of AhERF008 influenced the root gravity of Arabidopsis, whereas overexpression of AhERF019 enhanced tolerance to drought, heat, and salt stresses in Arabidopsis. The information generated in this study will be helpful to further investigate the function of ERFs in plant development and stress response.

Keywords

ERF family Gene function Phylogeny Peanut Stress response Plant development 

Supplementary material

10142_2014_381_MOESM1_ESM.xlsx (18 kb)
ESM Table 1Primer sequences of the peanut ERF genes referenced in this article. (XLSX 18 kb)
10142_2014_381_MOESM2_ESM.xlsx (11 kb)
ESM Table 2Characteristics of the peanut ERF genes. (XLSX 11 kb)
10142_2014_381_MOESM3_ESM.xlsx (2.5 mb)
ESM Table 3ESTs coding the 63 ERF factors identified in peanuts. (XLSX 2592 kb)
10142_2014_381_MOESM4_ESM.xlsx (37 kb)
ESM Table 4Summary of conserved motifs (CMs) within the AhERF family by comparative analysis with soybeans. (XLSX 37 kb)
10142_2014_381_MOESM5_ESM.xlsx (13 kb)
ESM Table 5Expression patterns of the peanut stress responsive ERF genes. (XLSX 12 kb)
10142_2014_381_MOESM6_ESM.xlsx (11 kb)
ESM Table 6Annotated information for the peanut ERFs from the NCBI database. (XLSX 10 kb)
10142_2014_381_Fig5_ESM.gif (199 kb)
ESM Fig. 1

Phylogenetic tree of peanut and soybean ERF proteins. (GIF 198 kb)

10142_2014_381_MOESM7_ESM.tif (763 kb)
High resolution image (TIFF 763 kb)
10142_2014_381_Fig6_ESM.gif (6.1 mb)
ESM Fig. 2

Amino acid sequence alignment of the AP2/ERF DNA-binding domains from the 63 peanut and 98 soybean ERF proteins described by Nakano et al. (2006) using ClustalW. (GIF 6292 kb)

10142_2014_381_MOESM8_ESM.tif (6.1 mb)
High resolution image (TIFF 6292 kb)
10142_2014_381_Fig7_ESM.gif (31 kb)
ESM Fig. 3

Unrooted phylogenetic tree of peanut ERF proteins. (GIF 30 kb)

10142_2014_381_MOESM9_ESM.tif (927 kb)
High resolution image (TIFF 926 kb)
10142_2014_381_Fig8_ESM.gif (24 kb)
ESM Fig. 4

Phylogenetic relationships among peanut CBF/DREB subfamily (group A) unigenes. (GIF 24 kb)

10142_2014_381_MOESM10_ESM.tif (1.8 mb)
High resolution image (TIFF 1846 kb)
10142_2014_381_Fig9_ESM.gif (55 kb)
ESM Fig. 5

Phylogenetic relationships among the peanut ERF subfamily (group B) unigenes. (GIF 54 kb)

10142_2014_381_MOESM11_ESM.tif (1.8 mb)
High resolution image (TIFF 1802 kb)
10142_2014_381_Fig10_ESM.gif (164 kb)
ESM Fig. 6

EAR motif-like sequences conserved in the C-terminal region of subgroups A-5 and B-1 in peanuts and soybeans. (A) Amino acid sequence alignment of the C-terminal region of proteins from subgroup A-5. (B) Amino acid sequence alignment of the C-terminal region of proteins from subgroup B-1 proteins. (GIF 164 kb)

10142_2014_381_MOESM12_ESM.tif (2 mb)
High resolution image (TIFF 2029 kb)
10142_2014_381_Fig11_ESM.gif (129 kb)
ESM Fig. 7

Soybean-specific sequence motifs conserved in subgroups A-6, B-1, and B-2 of the ERF family are also exist in peanuts. (A) Amino acid sequence alignment of proteins from subgroup A-6. (B) Amino acid sequence alignment of proteins from subgroup B-1. (C) Amino acid sequence alignment of proteins from subgroup B-2. (GIF 128 kb)

10142_2014_381_MOESM13_ESM.tif (3.4 mb)
High resolution image (TIFF 3518 kb)

References

  1. 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(12):1263–1274PubMedCrossRefGoogle Scholar
  2. 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):2463–2480PubMedCentralPubMedCrossRefGoogle Scholar
  3. An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 53(6):412–428PubMedCrossRefGoogle Scholar
  4. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 1(34 (Web Server issue)):W369–W373CrossRefGoogle Scholar
  5. 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(1):23–32PubMedCrossRefGoogle Scholar
  6. Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci U S A 101(13):4706–4711PubMedCentralPubMedCrossRefGoogle Scholar
  7. Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140(4):1384–1396PubMedCentralPubMedCrossRefGoogle Scholar
  8. 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 163:1167–1178PubMedCrossRefGoogle Scholar
  9. Chen N, Yang Q, Su M, Pan L, Chi X, Chen M, He Y, Yang Z, Wang T, Wang M, Yu S (2012) Cloning of six ERF family transcription factor genes from peanut and analysis of their expression during abiotic stress. Plant Mol Biol Report 30(6):1415–1425CrossRefGoogle Scholar
  10. Chen X, Zhu W, Azam S, Li H, Zhu F, Li H, Hong Y, Liu H, Zhang E, Wu H, Yu S, Zhou G, Li S, Zhong N, Wen S, Li X, Knapp SJ, Ozias-Akins P, Varshney RK, Liang X (2013) Deep sequencing analysis of the transcriptomes of peanut aerial and subterranean young pods identifies candidate genes related to early embryo abortion. Plant. Biotechnol J 11(1):115–127Google Scholar
  11. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55(395):225–236Google Scholar
  12. Chuck G, Muszynski M, Kellogg E, Hake S, Schmidt RJ (2002) The control of spikelet meristem identity by the branched silkless1 gene in maize. Science 298(5596):1238–1241PubMedCrossRefGoogle Scholar
  13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743PubMedCrossRefGoogle Scholar
  14. FAOSTAT (2010) FAO Statistical Database. From Food and Agricultural Organization, Rome, Italy, www.faostat.fao.org/site/339/default.aspx
  15. 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 Interact 17(10):1162–1171PubMedCrossRefGoogle Scholar
  16. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9(4):436–442Google Scholar
  17. Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23:412–427PubMedCentralPubMedCrossRefGoogle Scholar
  18. 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(5):771–786PubMedCentralPubMedCrossRefGoogle Scholar
  19. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7(4):465–471PubMedCrossRefGoogle Scholar
  20. 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 plants. J Biol Chem 273:26857–26861PubMedCrossRefGoogle Scholar
  21. 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 460:1026–1030PubMedCrossRefGoogle Scholar
  22. Hu L, Liu S (2011) Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genet Mol Biol 34(4):624–633PubMedCentralPubMedCrossRefGoogle Scholar
  23. 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—Life Sci 50:7–14Google Scholar
  24. 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 46:46–53PubMedGoogle Scholar
  25. 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 17:287–291PubMedCrossRefGoogle Scholar
  26. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331PubMedCrossRefGoogle Scholar
  27. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SC, Ritsema T, Pieterse CM (2010a) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232(6):1423–1432PubMedCentralPubMedCrossRefGoogle Scholar
  28. Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CM, Ritsema T (2010b) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant-Microbe Interact 23(2):187–197PubMedCrossRefGoogle Scholar
  29. 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 11:719PubMedCentralPubMedCrossRefGoogle Scholar
  30. 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(3):639–649PubMedCrossRefGoogle Scholar
  31. 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 10:1391–1406PubMedCentralPubMedCrossRefGoogle Scholar
  32. Liu L, White MJ, MacRae TH (1999) Transcription factors and their genes in higher plants functional domains, evolution and regulation. Eur J Biochem 262:247–257PubMedCrossRefGoogle Scholar
  33. Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15(1):165–178PubMedCentralPubMedCrossRefGoogle Scholar
  34. Mehrnia M, Balazadeh S, Zanor MI, Mueller-Roeber B (2013) EBE, an AP2/ERF transcription factor highly expressed in proliferating cells, affects shoot architecture in Arabidopsis. Plant Physiol 162(2):842–857PubMedCentralPubMedCrossRefGoogle Scholar
  35. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):86–96PubMedCrossRefGoogle Scholar
  36. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genomewide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432PubMedCentralPubMedCrossRefGoogle Scholar
  37. Nelson SC, Simpson CE, Starr JL (1989) Resistance to Meloidogyne arenaria in Arachis spp.. Germplasm J Nematol 21(4S):654–660Google Scholar
  38. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7(2):173–182PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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 13:1959–1968PubMedCentralPubMedCrossRefGoogle Scholar
  40. Oliva M, Dunand C (2007) Waving and skewing: how gravity and the surface of growth media affect root development in Arabidopsis. New Phytol 176(1):37–43PubMedCrossRefGoogle Scholar
  41. Oñate-Sánchez L, Singh KB (2002) Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol 128(4):1313–1322Google Scholar
  42. 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(5):1035–1046PubMedCentralPubMedCrossRefGoogle Scholar
  43. Philosoph-Hadas S, Friedman H, Meir S (2005) Gravitropic bending and plant hormones. Vitam Horm 72:31–78PubMedCrossRefGoogle Scholar
  44. Pirrello J, Prasad BC, Zhang W, Chen K, Mila I, Zouine M, Latché 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(1):190PubMedCentralPubMedCrossRefGoogle Scholar
  45. Pre M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147(3):1347–1357PubMedCentralPubMedCrossRefGoogle Scholar
  46. 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(8):1042–1052PubMedGoogle Scholar
  47. 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 290:998–1009PubMedCrossRefGoogle Scholar
  48. Seo YJ, Park JB, Cho YJ, Jung C, Seo HS, Park SK, Nahm BH, Song JT (2010) Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol Cells 30(3):271–277PubMedCrossRefGoogle Scholar
  49. Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Gen Genomics 284(6):455–475CrossRefGoogle Scholar
  50. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12(23):3703–3714PubMedCentralPubMedCrossRefGoogle Scholar
  51. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanism. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedGoogle Scholar
  52. Upadhyay RK, Soni DK, Singh R, Dwivedi UN, Pathre UV, Nath P, Sane AP (2013) SlERF36, an EAR-motif-containing ERF gene from tomato, alters stomatal density and modulates photosynthesis and growth. J Exp Bot. doi:10.1093/jxb/ert162 PubMedCentralPubMedGoogle Scholar
  53. Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS One 6(9):e25216PubMedCentralPubMedCrossRefGoogle Scholar
  54. 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(2):183–192PubMedCrossRefGoogle Scholar
  55. 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 67:589–602PubMedCrossRefGoogle Scholar
  56. Wang Y, Wan L, Zhang L, Zhang Z, Zhang H, Quan R, Zhou S, Huang R (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78(3):275–288PubMedCrossRefGoogle Scholar
  57. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708PubMedCrossRefGoogle Scholar
  58. 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 J53(7):570–585CrossRefGoogle Scholar
  59. 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):251–264PubMedCentralPubMedCrossRefGoogle Scholar
  60. Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58:585–596PubMedCrossRefGoogle Scholar
  61. 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(1):2862–2874PubMedCentralPubMedCrossRefGoogle Scholar
  62. 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(4):701–708PubMedCrossRefGoogle Scholar
  63. 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(4–5):321–331PubMedCentralPubMedCrossRefGoogle Scholar
  64. Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220(2):262–270Google Scholar
  65. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (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):689–707PubMedCrossRefGoogle Scholar
  66. Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64(3):265–278PubMedCrossRefGoogle Scholar
  67. 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(15):4095–4107PubMedCentralPubMedCrossRefGoogle Scholar
  68. Zhang Z, Zhang H, Quan R, Wang XC, Huang R (2009) Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol 150(1):365–377Google Scholar
  69. Zhu Z, Shi J, Xu W, Li H, He M, Xu Y, Xu T, Yang Y, Cao J, Wang Y (2013) Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J Plant Physiol 170(10):923–933PubMedCrossRefGoogle Scholar
  70. 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 populous trichocarpa. Biochem Biophys Res Commun 371(3):468–474PubMedCrossRefGoogle Scholar
  71. Zhuang J, Chen JM, Yao QH, Xiong F, Sun CC, Zhou XR, Zhang J, Xiong AS (2011) Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum. Mol Biol Rep 38(2):745–753PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Liyun Wan
    • 1
  • Yanshan Wu
    • 1
  • Jiaquan Huang
    • 1
  • Xiaofeng Dai
    • 2
  • Yong Lei
    • 1
  • Liying Yan
    • 1
  • Huifang Jiang
    • 1
  • Juncheng Zhang
    • 3
  • Rajeev K Varshney
    • 4
  • Boshou Liao
    • 1
  1. 1.Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of AgricultureOil Crops Research Institute of Chinese Academy of Agricultural SciencesWuhanChina
  2. 2.Institute of Agro-products Processing Science and TechnologyChinese Academy of Agricultural SciencesBeijingChina
  3. 3.The State Key Laboratory of Plant Cell and Chromosome EngineeringInstitute of Genetics and Developmental Biology, Chinese Academy of SciencesBeijingChina
  4. 4.International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)HyderabadIndia

Personalised recommendations