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Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.)

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Abstract

Transcriptional repressors are emerging as central regulators of development and stress responses in different organisms. The ERF-associated amphiphilic repression (EAR) motif was identified as essential for transcriptional repression. To gain a better understanding of this type of protein, we reported here a novel GmERF4 protein from soybean. Sequence alignment showed that GmERF4 contains one AP2/ERF domain, two putative nuclear localization signal regions and one EAR motif. The GmERF4 protein was preferentially localized to the nucleus of onion epidermis cells and bound specifically to the GCC box and DRE/CRT element in vitro. Furthermore, the expression of GmERF4 was induced by ethylene, JA, SA, cold, salt, drought, and soybean mosaic virus, and repressed by ABA. Constitutive expression of GmERF4 in transgenic tobacco plants increased tolerance to salt and drought stresses compared with wild-type plants, but did not exhibit detectable resistance against bacterial infection.

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Abbreviations

ABA:

Abscisic acid

EAR:

ERF-associated amphiphilic repression

ERF:

Ethylene responsive factor

ET:

Ethylene

ORF:

Open reading frame

RT-PCR:

Reverse transcription polymerase chain reaction

References

  1. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  2. 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 

  3. 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 

  4. Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, Choi D (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol 136:2862–2874

    Article  CAS  PubMed  Google Scholar 

  5. 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 

  6. Fischer U, Dröge-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

    Article  CAS  PubMed  Google Scholar 

  7. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  8. 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 

  9. Oñate-Sánchez L, Singh KB (2002) Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol 128:1313–1322

    Article  PubMed  Google Scholar 

  10. Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latché 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 

  11. 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 

  12. Menke FL, 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 AP2-domain transcription factor, ORCA2. EMBO J 16:4455–4463

    Article  Google Scholar 

  13. 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 

  14. Ohta M, Ohme-Takagi M, Shinshi H (2000) Three ethylene responsive transcription factors in tobacco with distinct transactivation functions. Plant J 22:29–38

    Article  CAS  PubMed  Google Scholar 

  15. 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 

  16. 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 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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  CAS  PubMed  Google Scholar 

  19. 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 

  20. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268

    Article  CAS  PubMed  Google Scholar 

  21. Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305

    Article  CAS  PubMed  Google Scholar 

  22. 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 

  23. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107

    Article  CAS  PubMed  Google Scholar 

  24. Choi MS, Kim MC, Yoo JH, Moon BC, Koo SC, Park BO, Lee JH, Koo YD, Han HJ, Lee SY, Chung WS, Lim CO, Cho MJ (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J Biol Chem 280:40820–40831

    Article  CAS  PubMed  Google Scholar 

  25. Hoekema A, Hirsch P, Hooykaas PJJ, Schilperoort R (1983) A binary plant vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180

    Article  CAS  Google Scholar 

  26. Thilmony RL, Chen Z, Bressan RA, Martin GB (1995) Expression of the tomato Pto gene in tobacco enhances resistance to Pseudomonas syringae pv tabaci expressing avrPto. Plant Cell 7:1529–1536

    Article  CAS  PubMed  Google Scholar 

  27. 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 

  28. Hao D, 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. Biochemistry 41:4202–4208

    Article  CAS  PubMed  Google Scholar 

  29. Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  PubMed  Google Scholar 

  30. Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11(3):109–112

    Article  CAS  PubMed  Google Scholar 

  31. Igarashi D, Ishida S, Fukazawa J, Takahashi Y (2001) 14–3-3 proteins regulate intracellular localization of the bZIP transcriptional activator RSG. Plant Cell 13:2483–2497

    Article  CAS  PubMed  Google Scholar 

  32. Gu Y, Wildermuth M, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin G (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 

  33. Dingwall C, Laskey RA (1991) Nuclear targeting sequences—a consensus? Trends in Biochem Sci 16:478–481

    Article  CAS  Google Scholar 

  34. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a b-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17:5485–5496

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to Dr. R.A. McIntosh (Plant Breeding Institute, University of Sydney, Australia) for reviewing this manuscript. This work was funded by National HITECH Research and Development Program of China (“863” program, #2008AA10Z124 and #2006AA10A111), the National Natural Science Foundation of China (#30700508), National Key Project for Researches on Transgenic Plant (#2008ZX08002-002). We thank Dr. Lijuan Qiu (Soybean Molecular Breeding Group, Institute of Crop Sciences, CAAS) for seed of the soybean cultivars.

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Authors and Affiliations

  1. Department of Chemistry, University of Science and Technology of China, 230026, Hefei, China

    Gaiyun Zhang, Xueping Chen & Jiaming Guo

  2. The National Key Facility for Crop Genetic Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, 100081, Beijing, China

    Ming Chen, Zhaoshi Xu, Liancheng Li & Youzhi Ma

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  1. Gaiyun Zhang
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  2. Ming Chen
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  3. Xueping Chen
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Correspondence to Xueping Chen or Youzhi Ma.

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The authors Gaiyun Zhang and Ming Chen contributed equally to this work.

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Zhang, G., Chen, M., Chen, X. et al. Isolation and characterization of a novel EAR-motif-containing gene GmERF4 from soybean (Glycine max L.). Mol Biol Rep 37, 809–818 (2010). https://doi.org/10.1007/s11033-009-9616-1

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