Skip to main content
SpringerLink
Log in

Expression of ethylene response factor JERF1 in rice improves tolerance to drought

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Ethylene response factor (ERF) proteins regulate a variety of stress responses in plant. JERF1, a tomato ERF protein, can be induced by abscisic acid (ABA). Overexpression of JERF1 enhanced the tolerance of transgenic tobacco to high salt concentration, osmotic stress, and low temperature by regulating the expression of stress-responsive genes by binding to DRE/CRT and GCC-box cis-elements. In this research, we further report that overexpression of JERF1 significantly enhanced drought tolerance of transgenic rice. The overexpression activated the expression of stress-responsive genes and increased the synthesis of the osmolyte proline by regulating the expression of OsP5CS, encoding the proline biosynthesis key enzyme deltal-pyrroline-5-carboxylate synthetase. JERF1 also activated the expression of two ABA biosynthesis key enzyme genes, OsABA2 and Os03g0810800, and increased the synthesis of ABA in rice. Analysis of cis-elements of JERF1-targeted genes pointed to the existence of DRE/CRT and/or GCC box in their promoters, indicating that JERF1 could activate the expression of related genes in rice by binding to these cis-elements. Unlike some other ERF proteins, constructive overexpression of JERF1 did not change the growth and development of transgenic rice, which makes JEFR1 a potentially useful source in breeding for greater tolerance to abiotic stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ERF:

Ethylene response factor

WT:

Wild-type rice

DRE/CRT:

Dehydration-responsive element/C-repeat

h:

Hour

References

  • Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced in response to cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541–552

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Agrawal G, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon tos17 insertion tagging of a zeaxanthin epoxidase gene and a novel ostatc gene. Plant Physiol 125:1248–1257

    Article  CAS  PubMed  Google Scholar 

  • Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI (1999) Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell 11:1785–1798

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chandler PM, Robertson M (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45:113–141

    Article  CAS  Google Scholar 

  • De Smet I, Zhang H, Inze′ D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  CAS  PubMed  Google Scholar 

  • Fukao T, Xu KN, 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

    Article  CAS  PubMed  Google Scholar 

  • González-Guzmán M, Apostolova N, Bellés JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodríguez PL (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14:1833–1846

    Article  PubMed  Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1910

    Article  CAS  PubMed  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  CAS  PubMed  Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    Article  CAS  PubMed  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  CAS  PubMed  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    Article  CAS  PubMed  Google Scholar 

  • Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for deltal-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857–865

    Article  CAS  PubMed  Google Scholar 

  • Imai R, Ali A, Pramanik HR, Nakaminami K, Sentoku N, Kato H (2004) A distinctive class of spermidine synthase is involved in chilling response in rice. J Plant Physiol 161:883–886

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  CAS  PubMed  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  CAS  PubMed  Google Scholar 

  • Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko K, Marsch-Martinez N, Krishnan A, Nataraja K, Udayakumar M, Pereira A (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104:15270–15275

    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 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176

    Article  CAS  PubMed  Google Scholar 

  • Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575

    Article  CAS  PubMed  Google Scholar 

  • Oh S, Song S, Kim Y, Jang H, Kim S, Kim M, Kim Y, Nahm B, Kim J (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Park HY, Seok HY, Park BK, Kim SH, Goh CH, Lee BH, Lee CH, Moon YH (2008) Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochem Biophys Res Commun 375:80–85

    Article  CAS  PubMed  Google Scholar 

  • Richardt S, Timmerhaus G, Lang D, Qudeimat E, Corrêa LG, Reski R, Rensing SA, Frank W (2010) Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol 72:27–45

    Article  CAS  PubMed  Google Scholar 

  • Saibo NJ, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot (Lond) 103:609–623

    Article  CAS  Google Scholar 

  • Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Márquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–588

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  CAS  PubMed  Google Scholar 

  • Shan DP, Huang JG, Yang YT, Guo YH, Wu CA, Yang GD, Gao Z, Zheng CC (2007) Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytol 176:70–81

    Article  CAS  PubMed  Google Scholar 

  • Shulaev V, Cortes D, Miller G, Mittler R (2008) Metabolomics for plant stress response. Physiol Plant 132:199–208

    CAS  PubMed  Google Scholar 

  • Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Valliyodan B, Nguyen H (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:1–7

    Article  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  CAS  PubMed  Google Scholar 

  • Verslues P, Zhu J (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379

    Article  CAS  PubMed  Google Scholar 

  • Wan XR, Li L (2006) Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochem Biophys Res Commun 347:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • Whitmore AP, Whalley WR (2009) Physical effects of soil drying on roots and crop growth. J Exp Bot 60:2845–2857

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Chen X, Ren H, Zhang Z, Zhang H, Wang J, Wang XC, Huang R (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

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Zhang Z, Zhang H, Wang XC, 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 Physiol 148:1953–1963

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail A, Bailey-Serres J, Ronald P, Mackill D (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708

    Article  CAS  PubMed  Google Scholar 

  • Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102

    CAS  PubMed  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2009) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685

    Article  PubMed  Google Scholar 

  • 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 220:262–270

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (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

    Article  CAS  PubMed  Google Scholar 

  • Zhu J (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Zhang H (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12

    Article  CAS  PubMed  Google Scholar 

  • Zuo KJ, Qin J, Zhao JY, Ling H, Zhang LD, Cao YF, Tang KX (2007) Over-expression GbERF2 transcription factor in tobacco enhances brown spots disease resistance by activating expression of downstream genes. Gene 391:80–90

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation of China (Grant No. 30730060) and Grant Special Foundation of Transgenic Plants in China (2008ZX08001-002, 2008ZX08001-003 and 2009ZX08009-020B).

Author information

Authors and Affiliations

  1. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Zhijin Zhang, Fang Li, Haiwen Zhang & Rongfeng Huang

  2. Hunan Agricultural University, Changsha, 410128, Hunan, China

    Fang Li & Dingjun Li

  3. National Key Facility of Crop Gene Resources and Genetic Improvement, Beijing, 100081, China

    Zhijin Zhang, Haiwen Zhang & Rongfeng Huang

  4. National Center for Plant Gene Research (Beijing), Beijing, 100081, China

    Zhijin Zhang, Haiwen Zhang & Rongfeng Huang

Authors
  1. Zhijin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dingjun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haiwen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rongfeng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rongfeng Huang.

Additional information

Z. Zhang and F. Li contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Z., Li, F., Li, D. et al. Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232, 765–774 (2010). https://doi.org/10.1007/s00425-010-1208-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1208-8

Keywords

Search

Navigation