Multiple regulatory roles of AP2/ERF transcription factor in angiosperm

Botanical Studies

Volumn 58, Issue 1, 2017, Pages

  Gu, Chao ^a   Guo, Zhi Hua ^a   Hao, Ping Ping ^a   Wang, Guo Ming ^a   Jin, Zi Ming ^a   Zhang, Shao Ling ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

AP2 ERF TF; Fruit ripening; Phytohormones; Plant growth and development; Stress

Indexed keywords

EID: 85008211302     PISSN: 1817406X     EISSN: None     Source Type: Journal    
DOI: 10.1186/s40529-016-0159-1     Document Type: Review

References (98)

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
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 16:2463–2480
3. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
4. Anderson JP, Lichtenzveig J, Gleason C, Oliver RP, Singh KB (2010) The B-3 ethylene response factor MtERF1-1 mediates resistance to a subset of root pathogens in Medicago truncatula without adversely affecting symbiosis with rhizobia. Plant Physiol 154:861–873
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 29:23–32
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 USA 101:4706–4711
7. Chakravarthy S, Tuori RP, D’Ascenzo MD, Fobert PR, Despres C, Martin GB (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050
8. Chen TT, Yang QC, Gruber M, Kang JM, Sun Y, Ding W, Zhang TJ, Zhang XQ (2012) Expression of an alfalfa (Medicago sativa L.) ethylene response factor gene MsERF8 in tobacco plants enhances resistance to salinity. Mol Biol Rep 39:6067–6075
9. 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 66:1053–1065
10. Du DL, Hao RJ, Cheng TR, Pan HT, Yang WR, Wang J, Zhang QX (2013) Genome-wide analysis of the AP2/ERF gene family in Prunus mume. Plant Mol Biol Rep 31:741–750
11. Du HW, Huang M, Zhang ZX, Cheng SY (2014) Genome-wide analysis of the AP2/ERF gene family in maize waterlogging stress response. Euphytica 198:115–126
12. 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
13. Fischer U, Droge-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 17:1162–1171
14. 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
15. Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034
16. 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
17. Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677
18. Guo HW, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49
19. Han YC, Kuang JF, Chen JY, Liu XC, Xiao YY, Fu CC, Wang JN, Wu KQ, Lu WJ (2016) Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol 171:1070–1084
20. Hao DY, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861
21. Hao DY, Yamasaki K, Sarai A, Ohme-Takagi M (2002) Determinants in the sequence specific binding of two plant transcription factors, CBF1 and NtERF2, to the DRE and GCC motifs. Biochem 41:4202–4208
22. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu JZ, 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
23. Hayama H, Shimada T, Fujii H, Ito A, Kashimura Y (2006) Ethylene-regulation of fruit softening and softening-related genes in peach. J Exp Bot 57:4071–4077
24. Jofuku KD, Denboer BGW, Vanmontagu M, Okamuro JK (1994) Control of arabidopsis flower and seed development by the homeotic gene apetala2. Plant Cell 6:1211–1225
25. Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478
26. Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, Inukai Y (2011) The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J 67:472–484
27. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153
28. Koyama T, Nii H, Mitsuda N, Ohta M, Kitajima S, Ohme-Takagi M, Sato F (2013) A regulatory cascade involving class II ETHYLENE RESPONSE FACTOR transcriptional repressors operates in the progression of leaf senescence. Plant Physiol 162:991–1005
29. Krizek B (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916–1929
30. 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
31. Lee JM, Joung JG, McQuinn R, Chung MY, Fei ZJ, Tieman D, Klee H, Giovannoni J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70:191–204
32. Li YC, Zhu BZ, Xu WT, Zhu HL, Chen AJ, Xie YH, Shao Y, Luo YB (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep 26:1999–2008
33. Li ZF, Zhang LX, Yu YW, Quan RD, Zhang ZJ, Zhang HW, Huang RF (2011) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68:88–99
34. Li XP, Zhu XY, Mao J, Zou Y, Fu DW, Chen WX, Lu WJ (2013) Isolation and characterization of ethylene response factor family genes during development, ethylene regulation and stress treatments in papaya fruit. Plant Physiol Bioch 70:81–92
35. Li T, Jiang Z, Zhang L, Tan D, Wei Y, Yuan H, Li T, Wang A (2016) Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J 88:735–748
36. Licausi F, Giorgi FM, Zenoni S, Osti F, Pezzotti M, Perata P (2010a) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genom 11:719
37. Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010b) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62:302–315
38. 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
39. 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
40. Liu M, Pirrello J, Kesari R, Mila I, Roustan JP, Li Z, Latche A, Pech JC, Bouzayen M, Regad F (2013) A dominant repressor version of the tomato Sl-ERF.B3 gene confers ethylene hypersensitivity via feedback regulation of ethylene signaling and response components. Plant J 76:406–419
41. Liu MC, Diretto G, Pirrello J, Roustan JP, Li ZG, Giuliano G, Regad F, Bouzayen M (2014) The chimeric repressor version of an ethylene response factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol 203:206–218
42. 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 15:165–178
43. 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
44. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Bba-Gene Regul Mech 1819:86–96
45. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947
46. 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
47. Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007
48. Oñate-Sánchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143:400–409
49. Pacifici E, Polverari L, Sabatini S (2015) Plant hormone cross-talk: the pivot of root growth. J Exp Bot 66:1113–1121
50. Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31:349–360
51. Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad Q, Regad F, Latche A, Pech JC, Bouzayen M (2006) Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol 47:1195–1205
52. Pirrello J, Prasad BC, 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
53. Pré 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 147:1347–1357
54. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
55. Qi WW, Sun F, Wang QJ, Chen ML, Huang YQ, Feng YQ, Luo XJ, Yang JS (2011) Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a Gibberellin biosynthetic gene. Plant Physiol 157:216–228
56. Rao GD, Sui JK, Zeng YF, He CY, Zhang JG (2015) Genome-wide analysis of the AP2/ERF gene family in Salix arbutifolia. Febs Open Bio 5:132–137
57. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103:11081–11085
58. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
59. 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
60. 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
61. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcriptionfactor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827
62. Sasaki K, Mitsuhara I, Seo S, Ito H, Matsui H, Ohashi Y (2007) Two novel AP2/ERF domain proteins interact with cis-element VWRE for wound-induced expression of the Tobacco tpoxN1 gene. Plant J 50:1079–1092
63. Shaikhali J, Heiber I, Seidel T, Stroher E, Hiltscher H, Birkmann S, Dietz K-J, Baier M (2008) The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol 8:48
64. Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
65. Solano R, Stepanova A, Chao QM, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Gene Dev 12:3703–3714
66. Swaminathan K, Peterson K, Jack T (2008) The plant B3 superfamily. Trends Plant Sci 13:647–655
67. 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
68. Tang YH, Qin SS, Guo YL, Chen YB, Wu PZ, Chen YP, Li MR, Jiang HW, Wu GJ (2016) Genome-wide analysis of the AP2/ERF gene family in physic nut and overexpression of the JcERF011 gene in rice increased its sensitivity to salinity stress. PLoS ONE 11:e0150879
69. 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
70. Trujillo LE, Sotolongo M, Menendez C, Ochogavia ME, Coll Y, Hernandez 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 49:512–525
71. Urbanova T, Leubner-Metzger G (2016) Gibberellins and seed germination. Annu Plant Rev 49:253–284
72. van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297
73. Wang A, Tan D, Takahashi A, Li TZ, Harada T (2007) MdERFs, two ethylene-response factors involved in apple fruit ripening. J Exp Bot 58:3743–3748
74. Wang YH, Wan LY, Zhang LX, Zhang ZJ, Zhang HW, Quan RD, Zhou SR, Huang RF (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 78:275–288
75. Welsch R, Maass D, Voegel T, DellaPenna D, Beyer P (2007) Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol 145:1073–1085
76. Werner T, Motyka V, Strnad M, Schmulling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492
77. Wilson K, Long D, Swinburne J, Coupland G (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an arabidopsis gene related to APETALA2. Plant Cell 8:659–671
78. Wu LJ, Chen XL, Ren HY, Zhang ZJ, Zhang HW, Wang JY, Wang XC, Huang RF (2007) ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta 226:815–825
79. Wu LJ, Zhang ZJ, Zhang HW, Wang XC, Huang RF (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
80. Xiao YY, Chen JY, Kuang JF, Shan W, Xie H, Jiang YM, Lu WJ (2013) Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot 64:2499–2510
81. 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 442:705–708
82. 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: 585–596
83. Yang CY, Hsu FC, Li JP, Wang NN, Shih MC (2011) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol 156:202–212
84. Yin XR, Chen KS, Allan AC, Wu RM, Zhang B, Lallu N, Ferguson IB (2008) Ethylene-induced modulation of genes associated with the ethylene signalling pathway in ripening kiwifruit. J Exp Bot 59:2097–2108
85. Yin XR, Xie XL, Xia XJ, Yu JQ, Ferguson IB, Giovannoni JJ, Chen KS (2016) Involvement of an ethylene response factor in chlorophyll degradation during citrus fruit degreening. Plant J 86:403–412
86. 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
87. 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
88. Zhang HW, Huang ZJ, Xie BY, Chen Q, Tian X, Zhang XL, Zhang HB, Lu XY, Huang DF, Huang RF (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 220:262–270
89. 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
90. Zhang HB, Yang YH, Zhang ZJ, Chen J, Wang XC, Huang RF (2008) Expression of the ethylene response factor gene TSRF1 enhances abscisic acid responses during seedling development in tobacco. Planta 228:777–787
91. Zhang ZJ, Zhang HW, Quan RD, Wang XC, Huang RF (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 150:365–377
92. Zhang Z, Li F, Li D, Zhang H, Huang R (2010a) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232:765–774
93. 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
94. Zhang Z, Liu X, Wang X, Zhou M, Zhou X, Ye X, Wei X (2012a) An R2R3 MYB transcription factor in wheat, TaPIMP1, mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense- and stress-related genes. New Phytol 196:1155–1170
95. Zhang ZJ, Wang J, Zhang RX, Huang RF (2012b) The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J 71:273–287
96. Zhao Y, Wei T, Yin KQ, Chen Z, Gu H, Qu LJ, Qin G (2012) Arabidopsis RAP2.2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytol 195:450–460
97. Zhu XL, Qi L, Liu X, Cai SB, Xu HJ, Huang RF, Li JR, Wei XN, Zhang ZY (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
98. 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 Bioph Res Co 371:468–474