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A transcriptional repressor of the ERF family confers drought tolerance to rice and regulates genes preferentially located on chromosome 11

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Abstract

Plant-specific ethylene response factors (ERFs) play important roles in abiotic and biotic stress responses in plants. Using a transgenic approach, we identified two rice ERF genes, OsERF4a and OsERF10a, which conferred drought stress tolerance. In particular, OsERF4a contains a conserved ERF-associated amphiphilic repression (EAR) motif in its C-terminal region that has been shown to function as a transcriptional repression domain. Expression profiling of transgenic rice plants over-expressing OsERF4a using either a constitutively active or an ABA-inducible promoter identified 45 down-regulated and 79 up-regulated genes in common. The increased stress tolerance by over-expression of the EAR domain-containing protein OsERF4a could result from suppression of a repressor of the defense response. Expression of the putative silent information regulator 2 (Sir2) repressor protein was repressed, and expression of several stress-response genes were induced by OsERF4a over-expression. The Sir2 and 7 out of 9 genes that were down-regulated by OsERF4a over-expression were induced by high salinity and drought treatments in non-transgenic control plants. Genes that were down- and up-regulated by OsERF4a over-expression were highly biased toward chromosome 11. Rice chromosome 11 has several large clusters of disease-resistance and defense-response genes. Taken together, our results suggest that OsERF4a is a positive regulator of shoot growth and water-stress tolerance in rice during early growth stages. We propose that OsERF4a could work by suppressing a repressor of the defense responses and/or by controlling the expression of a large number of genes located on chromosome 11.

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Abbreviations

ERF:

Ethylene response factor

EAR:

ERF-associated amphiphilic repression

TF:

Transcription factors

DRE:

Dehydration-responsive elements

Sir2:

Silent information regulator 2

qRT-PCR:

Quantitative real-time PCR

References

  • Alonso JM, Stepanova AN (2004) The ethylene signaling pathway. Science 306:1513–1515

    Article  PubMed  CAS  Google Scholar 

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404–13409

    Article  PubMed  CAS  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    Article  PubMed  CAS  Google Scholar 

  • Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417–435

    Article  PubMed  CAS  Google Scholar 

  • Bourdenx B, Bernard A, Domergue F, Pascal S, Leger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubes J (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156:29–45

    Article  PubMed  CAS  Google Scholar 

  • Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198

    Article  PubMed  Google Scholar 

  • Chuck G, Meeley RB, Hake S (1998) The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev 12:1145–1154

    Article  PubMed  CAS  Google Scholar 

  • Consortia TRCaS (2005) The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20

    Google Scholar 

  • 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. Plant J 33:751–763

    Article  PubMed  CAS  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

    PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hao D, 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

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Sun Q, Qin F, Li C, Zhao Y, Zhou DX (2007) Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144:1508–1519

    Article  PubMed  CAS  Google Scholar 

  • Islam MA, Du H, Ning J, Ye H, Xiong L (2009) Characterization of Glossy1-homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Mol Biol 70:443–456

    Article  PubMed  CAS  Google Scholar 

  • Jang IC, Choi WB, Lee KH, Song SI, Nahm BH, Kim JK (2002) High-level and ubiquitous expression of the rice cytochrome c gene OsCc1 and its promoter activity in transgenic plants provides a useful promoter for transgenesis of monocots. Plant Physiol 129:1473–1481

    Article  PubMed  CAS  Google Scholar 

  • Jang IC, Pahk YM, Song SI, Kwon HJ, Nahm BH, Kim JK (2003) Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J 33:531–541

    Article  PubMed  CAS  Google Scholar 

  • Kagale S, Links MG, Rozwadowski K (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152:1109–1134

    Article  PubMed  CAS  Google Scholar 

  • Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11:109–112

    Article  PubMed  CAS  Google Scholar 

  • Kurata N, Yamazaki Y (2006) Oryzabase. An integrated biological and genome information database for rice. Plant Physiol 140:12–17

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Lu J, Ju H, Zhou G, Zhu C, Erb M, Wang X, Wang P, Lou Y (2011) An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. Plant J 68:583–596

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351

    Article  PubMed  CAS  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  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • 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 13:1959–1968

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Phi-Van L, Stratling WH (1996) Dissection of the ability of the chicken lysozyme gene 5′ matrix attachment region to stimulate transgene expression and to dampen position effects. Biochemistry 35:10735–10742

    Article  PubMed  CAS  Google Scholar 

  • Robyr D, Suka Y, Xenarios I, Kurdistani SK, Wang A, Suka N, Grunstein M (2002) Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109:437–446

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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 30:271–277

    Article  PubMed  CAS  Google Scholar 

  • Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Tran LS, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2007) Plant gene networks in osmotic stress response: from genes to regulatory networks. Methods Enzymol 428:109–128

    Article  PubMed  CAS  Google Scholar 

  • 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:e25216

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Gao F, Wu J, Dai J, Wei C, Li Y (2010) Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression. Plant Cell Physiol 51:1291–1299

    Article  PubMed  CAS  Google Scholar 

  • Witzel K, Weidner A, Surabhi GK, Varshney RK, Kunze G, Buck-Sorlin GH, Borner A, Mock HP (2010) Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant Cell Environ 33:211–222

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Yang S, Wang S, Liu X, Yu Y, Yue L, Wang X, Hao D (2009) Four divergent Arabidopsis ethylene-responsive element-binding factor domains bind to a target DNA motif with a universal CG step core recognition and different flanking bases preference. FEBS J 276:7177–7186

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Chen M, Chen X, Xu Z, Li L, Guo J, Ma Y (2010) Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Mol Biol Rep 37:809–818

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta. doi:10.1007/s00425-013-1852-x

    Google Scholar 

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Acknowledgments

This work was supported by the Technology Development Program for Life Industry through the Korea Institute of Planning and Evaluation for Technology of Food, Agriculture, Forestry and Fisheries (Grant number 111076-5).

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Authors and Affiliations

  1. Division of Bioscience and Bioinformatics, Myongji University, Yongin, 449-728, Korea

    Joungsu Joo, Hae Jong Choi, Youn Hab Lee & Sang Ik Song

  2. Genomics Genetics Institute, GreenGene BioTech, Inc., Yongin, Kyonggido, 449–728, Korea

    Yeon-Ki Kim

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  1. Joungsu Joo
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Correspondence to Sang Ik Song.

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425_2013_1880_MOESM1_ESM.ppt

Supplementary material 1. Fig. S1 Stress tolerance of transgenic plants over-expressing OsERFs during the vegetative stage. T1 transgenic plants and NT controls were grown in a greenhouse for four weeks. The plants were subjected to 7 days of drought stress followed by rehydration in a greenhouse. a Drought stress tolerance test of T1 transgenic plants. b Drought stress tolerance of T1 OsERF4a and OsERF10a over-expressing transgenic plants. W, well-watered; D, drought-stressed and rehydrated. Photographs were taken on the indicated days. Fig. S2 Genomic Southern blotting analyses of 101ERF4a (a), 105ERF4a (b) and 101ERF10a (c) plants. Ten micrograms of genomic DNA were double-digested with EcoRI and XhoI restriction enzymes, separated on a 0.8 % agarose gel, blotted onto a membrane, and hybridized with a 32P-labeled MAR probe. (PPT 1,409 kb) (PPT 1,409 kb)

425_2013_1880_MOESM2_ESM.xlsx

Supplementary material 2. Table S1 A list of the rice ERF transcription factor genes used for rice transformation. Table S2 Down- and up-regulated genes in 101ERF4a and 105ERF4a plants compared with NT controls. Table S3 Commonly up-regulated genes in 101ERF4a and 105ERF4a plants compared with NT controls. Table S4 The chromosomal distribution of down- and up-regulated genes in rice plants over-expressing OsERF4a. Table S5 Gene-specific primers used for RT-PCR and quantitative RT-PCR. (XLSX 50 kb) (XLSX 50 kb)

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Joo, J., Choi, H.J., Lee, Y.H. et al. A transcriptional repressor of the ERF family confers drought tolerance to rice and regulates genes preferentially located on chromosome 11. Planta 238, 155–170 (2013). https://doi.org/10.1007/s00425-013-1880-6

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