Ethylene response factors gene regulation and expression profiles under different stresses in rice

Pegoraro, Camila; Farias, Daniel da Rosa; Mertz, Liliane Marcia; Santos, Railson Schreinert dos; Maia, Luciano Carlos da; Rombaldi, Cesar Valmor; Oliveira, Antonio Costa de

Abstract

Stresses can cause large yield reductions in cultivated plants. The response to these stresses occurs via a plethora of signalling pathways, where a large number of genes is induced or repressed. Among the environmental stress responsive genes, there are the members of the ethylene response factors (ERF) gene family. The mRNA levels of different ERF are regulated by many hormones and molecules produced under different stress conditions. In this study, with the goal of identifying the response of rice ERF genes to environmental stress, it was analysed the transcriptional expression profile of 114 of these genes under stress by anoxia, salt and Magnaporthe grisea. Also, aiming to characterize how the regulation of ERF genes occurs, the amount of known cis regulatory elements in the promoter region of these genes and their association with the expression profiles under the tested conditions were also assessed. The results indicate that some ERF members present the same specific expression profiles under different environmental stresses, while others do not. Within the ERF family, the regulation of gene expression is complex for some genes which have many cis elements in their promoters, but simple for others, demonstrating high levels of divergence among them. The findings demonstrate the importance of the study of each ERF separately, since it is not possible to establish general rules for regulation and probably for the function of these genes.

Oryza sativa; transcription; cis elements; environmental stresses

Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signaling & Behavior 5:369-374.
Brivanlou A, Darnell J (2002) Signal transduction and the control of gene expression. Science 295:813-818.
Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, Lammeren AAM, Miki BLA, Custers JBM, Campagne MML (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. The Plant Cell 14:1737-1749.
Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiology 162:1566-1582.
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology 11:163.
Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiology and Biochemistry 42:273-282.
Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology 10:151.
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 Journal 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. The Plant Cell 8:155-168.
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. The Plant Cell 12:393-404.
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. Current Opinion in Plant Biology 9:436-442.
Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. The Plant Cell 23:412-427.
Gallego-Bartolome J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabad D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Molecular Biology and Evolution 27:1247-1256.
Grennan AK (2008) Ethylene response factors in jasmonate signaling and defense response. Plant Physiology 146:1457-1458.
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology 124:1854-1865.
Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology 54:767-781.
Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel RAM, Westhoff P (2004) Cis-Regulatory elements for mesophyll-specific gene expression in the C₄ plant Flaveria trinervia, the promoter of the C₄ phosphoenolpyruvate carboxylase gene. The Plant Cell 16:1077-1090.
Higo K,Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Research 27:297-300.
Jung KI-H, SeoY-S, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiology 152:1674-1692.
Lasanthi-Kudahettige R,Magneschi L,LOreti E, Gonzali S, Licausi F, Novi G, Beretta O,Vitulli F, Alpi A, Perata P. (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiology 144:218-231.
Li X, Zhu X, Mao J, Zou Y, Fu D, Chen W, Lu W (2013) Isolation and characterization of ethylene response factor family genes during development, ethylene regulation and stress treatments in papaya fruit. Plant Physiology and Biochemistry 70:81-92.
Licausi F, Dongen JT, GiuntoliB, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana The Plant Journal 62: 302-315.
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. The Plant Cell 10:1391-1406.
Liu L, White MJ, Macrae TH (1999) Transcription factors and their genes in higher plants functional domains, evolution and regulation. European Journal of Biochemistry 262:247-257.
Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K (2009) An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to AW-box sequence conserved among proximal upstream regions of genes Involved in fatty acid synthesis. The Plant Journal 60:476-487.
Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiology and Biochemistry 47:785-795.
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiology 140:411-432.
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell 7:173-182.
Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29:2001-2007.
Ribot C, Hirsch J, Balzergue S, Tharreau D, Nottéghem JL, Lebrum MH, Morel JB (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea Journal of Plant Physiology 165:114-124.
Rombauts S, Florquin K,Lescot M, Marchal K,Rouze P, Van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiology 132:1162-1176.
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 dehydrationand cold-inducible gene expression. Biochemical and Biophysical Research Communications 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. The Plant Cell 18:1292-1309.
Santos RS dos, Krüger MM, Pegoraro C, Madabula F, Da Maia LC, Rombaldi CV, Oliveira AC de (2013) Transcriptional regulation of seven ERFs in rice under oxygen depletion and iron overload stress. Tropical Plant Biology 6:16-25.
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. The Plant Journal 50:1079-1092.
Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki k (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. The Plant Journal 33:259-270.
Solano R, Stepanova A, Chao QM, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSEFACTOR1. Genes & Development 12:3703-3714.
Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Current Opinion in Plant Biology 12:548-555.
Stockinger EJ, Gilmour SJ,Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences 94:1035-1040.
Vahala J, Felten J, Love J, Gorzsás A, Gerber L, Lamminmäki A, Kangasjärvi J, Sundberg B (2013) A genome-wide screen for ethylene-induced ethylene response factors (ERFs) in hybrid aspen stem identifies ERF genes that modify stem growth and wood properties. New Phytologist 200:511-522.
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.
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. The Plant Cell 6:251-264.
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57:781-803.
Yamamoto S, Suzuki K, Shinshi H (1999) Elicitor-responsive ethylene independent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. The Plant Journal 20:571-579.
Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. The Journal of Biological Chemistry 277:45049-45058.
Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2008) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology 58:585-596.
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiology 139:822-835.
Walley JW, Coughlan S, Hudson ME, Covington MF, Kaspi R, Banu G, Harmer SL, Dehesh K (2007) Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genetics 3:e172.
Welsch R, Maass D, Voegel T, Della-Penna D, Beyer P (2007) Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiology 145:1073-1085.
Wu L, ZhangZ, Zhang H, Wang X-C, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiology 148:1953-1963.
Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research 97:111-119.
Zimmermann P, Laule O, Schmitz J, Hruz T, Bleuler S, Gruissem W (2008) Genevestigator transcriptome meta-analysis and biomarker search using rice and barley gene expression databases. Molecular Plant 1:851-857.
Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu S-H (2011) Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana Proceedings of the National Academy of Sciences 108:14992-14997.

Publication Dates

Publication in this collection
10 Feb 2014
Date of issue
Dec 2013

History

Received
24 Aug 2013
Accepted
11 Dec 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signaling & Behavior 5:369-374.

[2] Brivanlou A, Darnell J (2002) Signal transduction and the control of gene expression. Science 295:813-818.

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

[4] Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiology 162:1566-1582.

[5] Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology 11:163.

[6] Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiology and Biochemistry 42:273-282.

[7] Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology 10:151.

[8] 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 Journal 33:751-763.

[9] 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. The Plant Cell 8:155-168.

[10] 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. The Plant Cell 12:393-404.

[11] 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. Current Opinion in Plant Biology 9:436-442.

[12] Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. The Plant Cell 23:412-427.

[13] Gallego-Bartolome J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabad D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Molecular Biology and Evolution 27:1247-1256.

[14] Grennan AK (2008) Ethylene response factors in jasmonate signaling and defense response. Plant Physiology 146:1457-1458.

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

[16] Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology 54:767-781.

[17] Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel RAM, Westhoff P (2004) Cis-Regulatory elements for mesophyll-specific gene expression in the C₄ plant Flaveria trinervia, the promoter of the C₄ phosphoenolpyruvate carboxylase gene. The Plant Cell 16:1077-1090.

[18] Higo K,Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Research 27:297-300.

[19] Jung KI-H, SeoY-S, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiology 152:1674-1692.

[20] Lasanthi-Kudahettige R,Magneschi L,LOreti E, Gonzali S, Licausi F, Novi G, Beretta O,Vitulli F, Alpi A, Perata P. (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiology 144:218-231.

[21] Li X, Zhu X, Mao J, Zou Y, Fu D, Chen W, Lu W (2013) Isolation and characterization of ethylene response factor family genes during development, ethylene regulation and stress treatments in papaya fruit. Plant Physiology and Biochemistry 70:81-92.

[22] Licausi F, Dongen JT, GiuntoliB, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana The Plant Journal 62: 302-315.

[23] 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. The Plant Cell 10:1391-1406.

[24] Liu L, White MJ, Macrae TH (1999) Transcription factors and their genes in higher plants functional domains, evolution and regulation. European Journal of Biochemistry 262:247-257.

[25] Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K (2009) An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to AW-box sequence conserved among proximal upstream regions of genes Involved in fatty acid synthesis. The Plant Journal 60:476-487.

[26] Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiology and Biochemistry 47:785-795.

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

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

[29] Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html

[30] Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29:2001-2007.

[31] Ribot C, Hirsch J, Balzergue S, Tharreau D, Nottéghem JL, Lebrum MH, Morel JB (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea Journal of Plant Physiology 165:114-124.

[32] Rombauts S, Florquin K,Lescot M, Marchal K,Rouze P, Van de Peer Y (2003) Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant Physiology 132:1162-1176.

[33] 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 dehydrationand cold-inducible gene expression. Biochemical and Biophysical Research Communications 290:998-1009.

[34] 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. The Plant Cell 18:1292-1309.

[35] Santos RS dos, Krüger MM, Pegoraro C, Madabula F, Da Maia LC, Rombaldi CV, Oliveira AC de (2013) Transcriptional regulation of seven ERFs in rice under oxygen depletion and iron overload stress. Tropical Plant Biology 6:16-25.

[36] 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. The Plant Journal 50:1079-1092.

[37] Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki k (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. The Plant Journal 33:259-270.

[38] Solano R, Stepanova A, Chao QM, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSEFACTOR1. Genes & Development 12:3703-3714.

[39] Stepanova AN, Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Current Opinion in Plant Biology 12:548-555.

[40] Stockinger EJ, Gilmour SJ,Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences 94:1035-1040.

[41] Vahala J, Felten J, Love J, Gorzsás A, Gerber L, Lamminmäki A, Kangasjärvi J, Sundberg B (2013) A genome-wide screen for ethylene-induced ethylene response factors (ERFs) in hybrid aspen stem identifies ERF genes that modify stem growth and wood properties. New Phytologist 200:511-522.

[42] 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.

[43] 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. The Plant Cell 6:251-264.

[44] Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57:781-803.

[45] Yamamoto S, Suzuki K, Shinshi H (1999) Elicitor-responsive ethylene independent activation of GCC box-mediated transcription that is regulated by both protein phosphorylation and dephosphorylation in cultured tobacco cells. The Plant Journal 20:571-579.

[46] Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. The Journal of Biological Chemistry 277:45049-45058.

[47] Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2008) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology 58:585-596.

[48] Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiology 139:822-835.

[49] Walley JW, Coughlan S, Hudson ME, Covington MF, Kaspi R, Banu G, Harmer SL, Dehesh K (2007) Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genetics 3:e172.

[50] Welsch R, Maass D, Voegel T, Della-Penna D, Beyer P (2007) Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiology 145:1073-1085.

[51] Wu L, ZhangZ, Zhang H, Wang X-C, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiology 148:1953-1963.

[52] Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research 97:111-119.

[53] Zimmermann P, Laule O, Schmitz J, Hruz T, Bleuler S, Gruissem W (2008) Genevestigator transcriptome meta-analysis and biomarker search using rice and barley gene expression databases. Molecular Plant 1:851-857.

[54] Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu S-H (2011) Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana Proceedings of the National Academy of Sciences 108:14992-14997.

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Ethylene response factors gene regulation and expression profiles under different stresses in rice

Abstract

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History