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The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco

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Abstract

Ethylene responsive factors (ERFs) are important plant-specific transcription factors, some of which have been demonstrated to interact with the ethylene-responsive GCC box and the dehydration-responsive element (DRE); however, data on the roles of ERF proteins in connection with various signaling pathways are limited. In this research, we used the GCC box, an essential cis-acting element responsive to ethylene and methyl jasmonate (MeJA), as bait in a yeast one-hybrid system to isolate transcription factors from tomato (Lycopersicon esculentum Mill.). One of the cDNAs, which was designated Jasmonate and Ethylene Response Factor 1 (JERF1), encodes an ERF protein, containing a conserved ERF DNA-binding motif and functioning as a transcriptional activator in yeast through targeting to the nucleus in onion (Allium cepa L.) epidermal cells. Biochemical analysis revealed that JERF1 bound not only to the GCC box but also to the DRE sequence. Expression of the JERF1 gene in tomato was induced by ethylene, MeJA, abscisic acid (ABA) and salt treatment, indicating that JERF1 might act as a connector among different signal transduction pathways. Further research with transgenic JERF1 tobacco (Nicotiana tabacum L.) plants indicated that overexpressing JERF1 activated expression of GCC box-containing genes such as osmotin, GLA, Prb-1b and CHN50 under normal growth conditions, and subsequently resulted in enhanced tolerance to salt stress, suggesting that JERF1 modulates osmotic tolerance by activation of downstream gene expression through interaction with the GCC box or DRE.

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Abbreviations

ABA :

Abscisic acid

CaMV :

Cauliflower mosaic virus

DRE :

Dehydration-responsive element

ERF :

Ethylene-responsive factor

GFP :

Green fluorescent protein

JA :

Jasmonate

JERF1 :

Jasmonate and ethylene responsive factor 1

MeJA :

Methyl jasmonic acid

NLS :

Nuclear localization signal

OE :

Overexpression of JERF1 in tobacco

PR :

Pathogenesis-related

WT :

Wild type

References

  • Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrar S, Ausubel FM, Ecker JR (2003) Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA 100:2992–2997

    Article  CAS  PubMed  Google Scholar 

  • Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol 34:129–136

    CAS  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115

    Article  CAS  PubMed  Google Scholar 

  • Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032

    Article  CAS  PubMed  Google Scholar 

  • Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  CAS  PubMed  Google Scholar 

  • Eyal Y, Meller Y, Lev-Yadum S, Fluhr R (1993) A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J 4:225–234

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Almeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378

    Article  CAS  PubMed  Google Scholar 

  • Fukuda Y, Ohme M, Shinshi H (1991) Gene structure and expression of a tobacco endochitinase gene in suspension-cultured tobacco cells. Plant Mol Biol 16:1–10

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    Article  CAS  PubMed  Google Scholar 

  • Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94:2122–2127

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  CAS  PubMed  Google Scholar 

  • Jia Y, Martin GB (1999) Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. Plant Mol Biol 40:455–465

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant. Plant Cell 15:165–178

    Article  CAS  PubMed  Google Scholar 

  • Menke FLH, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible ERF domain transcription factor ORCA2. EMBO J 18:4455–4463

    Article  CAS  PubMed  Google Scholar 

  • Norman-Setterblad C, Vidal S, Palva ET (2000) Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol Plant Microbe Interact 13:430–438

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2114

    Article  CAS  PubMed  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679–689

    Article  CAS  PubMed  Google Scholar 

  • Quesada V, Ponce MR, Micol L (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154:421–436

    CAS  PubMed  Google Scholar 

  • Raghothama KG, Kononowicz AK, Maggio A, Narasimhan ML, Wang G, Hasegawa PM, Bressan RA (1997) Tissue specific activation of the osmotin gene by ABA, ethylene and NaCl involves the same promoter region. Plant Mol Biol 34:393–402

    Article  CAS  PubMed  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    Article  CAS  PubMed  Google Scholar 

  • Rouster J, Leah R, Cameron-Kills V (1997) Identification of a methyl jasmonate-responsive region in promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Somssich IE (1998) Transcriptional control of plant genes responsive to pathogens. Curr Opin Plant Biol 1:311–315

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1061

    Article  CAS  PubMed  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    Article  CAS  PubMed  Google Scholar 

  • Sessa G, Meller Y, Fluhr R (1995) A GCC element and a G-box motif participate in ethylene-induced expression of the PRB-1b gene. Plant Mol Biol 28:145–153

    CAS  PubMed  Google Scholar 

  • Shinshi H, Usami S, Ohme-Takagi M (1995) Identification of an ethylene-responsive region in the promoter of a tobacco class I chitinase gene. Plant Mol Biol 27:923–932

    CAS  PubMed  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSIVE FACTOR1. Genes Dev 12:3703–3714

    CAS  PubMed  Google Scholar 

  • Sperisen C, Ryals J, Meins F (1991) Comparison of cloned genes provides evidence for intergenomic exchange of DNA in the evolution of a tobacco glucan endo-1,3-beta glucosidase gene family. Proc Natl Acad Sci USA 88:1820–1824

    CAS  PubMed  Google Scholar 

  • Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci USA 94:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Thara VK, Tang X, Gu Y, Martin GB, Zhou JM (1999) Pseudomonas syringae pv. tomato induces the expression of tomato EREBP-like genes Pti4 and Pti5 independent of ethylene, salicylate and jasmonate. Plant J 20:475–483

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

    Article  PubMed  Google Scholar 

  • van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43–53

    Article  PubMed  Google Scholar 

  • Veena, Reddy VS, Sopory SK (1999) Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. Plant J 17:385–395

    Article  CAS  PubMed  Google Scholar 

  • Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95:7209–7214

    Article  CAS  PubMed  Google Scholar 

  • Werner J, Finkelstein RR (1995) Arabidopsis mutants with reduced response to NaCl and osmotic stress. Physiol Plant 93:659–666

    Article  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell [Suppl] 14:165–183

  • Xu Y, Chang PLC, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085

    Article  CAS  PubMed  Google Scholar 

  • Yang YN, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16:3207–3218

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Droge-Laser W, Dixon RA, Lamb C (1996) Transcriptional activation of plant defense genes. Curr Opin Genet Dev 6:624–630

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Dr. Daoxin Xie and Dr. Qiang Liu for their help with construction of the GCC box bait and tomato cDNA library. This work was supported by the Major State Basic Research program of China (G1999011704), Special Foundation of Transgenic Plants in China (JY03A23-02), the National Science Foundation of China (to R.F.H. and Q.C) and the National Grand Scientific Engineering Program of China. Haiwen Zhang and Zejun Huang contributed equally to this work.

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Authors and Affiliations

  1. The National Plant Gene Research Center (Beijing), Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, 100081, Beijing, China

    Haiwen Zhang, Zejun Huang, Qi Chen, Xiulin Zhang, Hongbo Zhang, Dafang Huang & Rongfeng Huang

  2. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 100081, Beijing, China

    Haiwen Zhang, Bingyan Xie & Xin Tian

  3. Hunan Agricultural University, 410128, Changsha, China

    Haiwen Zhang & Xiangyang Lu

Authors
  1. Haiwen Zhang
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  2. Zejun Huang
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  3. Bingyan Xie
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  4. Qi Chen
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  5. Xin Tian
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  6. Xiulin Zhang
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  8. Xiangyang Lu
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  9. Dafang Huang
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  10. Rongfeng Huang
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Corresponding author

Correspondence to Rongfeng Huang.

Additional information

The gene bank accession numbers for the sequences mentioned in this article are AY044235 (JERF1), X66942 (prb-1b), M60402 (GLA), X51599 (CHN50), X95308 (osmotin), AF093743 (NP24), AF076277 (ERF1), AB008104 (AtERF2), AB008105 (AtERF3), D38123 (EREBP1), D38126 (EREBP2), U89255 (Pti4), U89256 (Pti5), AF058827 (Tsi1)

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Zhang, H., Huang, Z., Xie, B. et al. 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 (2004). https://doi.org/10.1007/s00425-004-1347-x

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