Skip to main content
SpringerLink
Log in

The gene family of dehydration responsive element-binding transcription factors in grape (Vitis vinifera): genome-wide identification and analysis, expression profiles, and involvement in abiotic stress resistance

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The dehydration responsive element-binding (DREB) proteins play a critical role in plant development and abiotic stress-mediated gene expression. Therefore, they represent one of the most attractive regulons for breeding programs. However, no comprehensive summary of grapevine DREB family genes is available. During this study, 38 VvDREB members were identified from the entire grapevine genome and its expression sequence tag assembly. These were organized into the same subgroups, A1 through A6, as for Arabidopsis DREBs. The VvDREB genes were distributed in 15 out of 19 chromosomes in grapevine. Multiple sequence alignments were performed and a three-dimensional structure was created to demonstrate sequence conservation. Microarray analysis showed potential regulatory roles for VvDREBs in responses to various abiotic stresses, hormone treatments, berry ripening, exposure to light, and bud development. Cis-acting regulatory elements, such as W-box, MYB-binding site, and light-responsive elements, were the most frequently found in the putative promoter regions. Furthermore, microarray transcriptional profiling of grapevine plants that over-expressed VvDREB23 revealed 248 up-regulated and 229 down-regulated genes, with fold-changes of >1.5 when compared with the empty vector control. Gene ontology classifications showed that different genes function in cellular glucan metabolism, lipid transport, the endomembrane system, cell wall structure, and other important metabolic and developmental processes, as well as in the regulation of molecular functions. Our report provides an overview and constitutes a foundation for further study of this VvDREB gene family. All the microarray data and transcription profiling of transgenic versus empty-vector control transformant grapevines were retrieved from the online resources.

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

AP2/ERF:

APETALA 2/ethylene responsive element-binding factor

CBF:

C-repeat binding factor

CRT:

C-repeat

DRE:

Dehydration responsive element

DREB:

Dehydration responsive element-binding protein

VvDREB :

Vitis vinifera dehydration responsive element-binding protein

TF:

Transcription factor

References

  1. 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. Plant Cell 6(2):251–264. doi:10.1105/tpc.6.2.251

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24(5):701–713

    Article  CAS  PubMed  Google Scholar 

  3. 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. doi:10.1146/annurev.arplant.57.032905.105444

    Article  CAS  PubMed  Google Scholar 

  4. 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(3):998–1009. doi:10.1006/bbrc 2001.6299

    Article  CAS  PubMed  Google Scholar 

  5. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16(4):433–442. doi:10.1046/j.1365-313x.1998.00310.x

    Article  CAS  PubMed  Google Scholar 

  6. 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(8):1391–1406

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42(4):657–665

    Article  CAS  PubMed  Google Scholar 

  8. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103(49):18822–18827. doi:10.1073/pnas.0605639103

    Article  CAS  PubMed  Google Scholar 

  9. Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14(10):2565–2575

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko KR, Marsch-Martinez N, Krishnan A, Nataraja KN, 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(39):15270–15275. doi:10.1073/pnas.0707294104

    Article  CAS  PubMed  Google Scholar 

  11. Tsutsui T, Kato W, Asada Y, Sako K, Sato T, Sonoda Y, Kidokoro S, Yamaguchi-Shinozaki K, Tamaoki M, Arakawa K, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Ikeda A, Yamaguchi J (2009) DEAR1, a transcriptional repressor of DREB protein that mediates plant defense and freezing stress responses in Arabidopsis. J Plant Res 122(6):633–643. doi:10.1007/s10265-009-0252-6

    Article  CAS  PubMed  Google Scholar 

  12. Rae L, Lao NT, Kavanagh TA (2011) Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234(3):429–444. doi:10.1007/s00425-011-1414-z

    Article  CAS  PubMed  Google Scholar 

  13. Chen H, Je J, Song C, Hwang JE, Lim CO (2012) A proximal promoter region of Arabidopsis DREB2C confers tissue-specific expression under heat stress. J Integr Plant Biol 54(9):640–651. doi:10.1111/j.1744-7909.2012.01137.x

    Article  CAS  PubMed  Google Scholar 

  14. Omidvar V, Abdullah SN, Ho CL, Mahmood M, Al-Shanfari AB (2012) Isolation and characterization of two ABRE-binding proteins: EABF and EABF1 from the oil palm. Mol Biol Rep 39(9):8907–8918. doi:10.1007/s11033-012-1758-x

    Article  CAS  PubMed  Google Scholar 

  15. Zhou ML, Ma JT, Zhao YM, Wei YH, Tang YX, Wu YM (2012) Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica. Gene 506(1):10–17. doi:10.1016/j.gene.2012.06.089

    Article  CAS  PubMed  Google Scholar 

  16. Cortes AJ, This D, Chavarro C, Madrinan S, Blair MW (2012) Nucleotide diversity patterns at the drought-related DREB2 encoding genes in wild and cultivated common bean (Phaseolus vulgaris L.). Theor Appl Genet 125(5):1069–1085. doi:10.1007/s00122-012-1896-5

    Article  CAS  PubMed  Google Scholar 

  17. Li J, Sima W, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y, Feng Y, Hao Y, Ye Z (2012) Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. J Exp Bot 63(18):6407–6420. doi:10.1093/jxb/ers295

    Article  CAS  PubMed  Google Scholar 

  18. Jin X, Xue Y, Wang R, Xu R, Bian L, Zhu B, Han H, Peng R, Yao Q (2012) Transcription factor OsAP21 gene increases salt/drought tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep. doi:10.1007/s11033-012-2228-1

    Google Scholar 

  19. Mao D, Chen C (2012) Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS One 7(10):e47275. doi:10.1371/journal.pone.0047275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Tillett RL, Wheatley MD, Tattersall EA, Schlauch KA, Cramer GR, Cushman JC (2012) The Vitis vinifera C-repeat binding protein 4 (VvCBF4) transcriptional factor enhances freezing tolerance in wine grape. Plant Biotechnol J 10(1):105–124. doi:10.1111/j.1467-7652.2011.00648.x

    Article  CAS  PubMed  Google Scholar 

  21. Zhuang J, Peng R-H, Cheng Z-M, Zhang J, Cai B, Zhang Z, Gao F, Zhu B, Fu X-Y, Jin X-F (2009) Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci Hortic 123(1):73–81. doi:10.1016/j.scienta.2009.08.002

    Article  CAS  Google Scholar 

  22. Licausi F, Giorgi FM, Zenoni S, Osti F, Pezzotti M, Perata P (2010) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics 11:719. doi:10.1186/1471-2164-11-719

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467. doi:10.1038/nature06148

    Article  CAS  PubMed  Google Scholar 

  24. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36

    CAS  PubMed  Google Scholar 

  25. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  Google Scholar 

  26. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. doi:10.1002/jcc.20084

    Article  CAS  PubMed  Google Scholar 

  27. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17(18):5484–5496. doi:10.1093/emboj/17.18.5484

    Article  CAS  PubMed  Google Scholar 

  28. Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, Cox T, Cuff J, Curwen V, Down T (2002) The Ensembl genome database project. Nucleic Acids Res 30:38–41

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193. doi:10.1016/S0076-6879(06)11009-5

    Article  CAS  PubMed  Google Scholar 

  30. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3. doi:10.2202/1544-6115.1027

  32. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(Web Server issue):W64–70. doi:10.1093/nar/gkq310

  33. Cramer GR, Ergul A, Grimplet J, Tillett RL, Tattersall EA, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7(2):111–134. doi:10.1007/s10142-006-0039-y

    Article  CAS  PubMed  Google Scholar 

  34. Grimplet J, Deluc LG, Tillett RL, Wheatley MD, Schlauch KA, Cramer GR, Cushman JC (2007) Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics 8:187. doi:10.1186/1471-2164-8-187

    Article  PubMed Central  PubMed  Google Scholar 

  35. Carvalho LC, Vilela BJ, Mullineaux PM, Amancio S (2011) Comparative transcriptomic profiling of Vitis vinifera under high light using a custom-made array and the Affymetrix GeneChip. Mol Plant 4(6):1038–1051. doi:10.1093/mp/ssr027

    Article  CAS  PubMed  Google Scholar 

  36. Coito JL, Rocheta M, Carvalho L, Amancio S (2012) Microarray-based uncovering reference genes for quantitative real time PCR in grapevine under abiotic stress. BMC Res Notes 5(1):220. doi:10.1186/1756-0500-5-220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Koyama K, Sadamatsu K, Goto-Yamamoto N (2010) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics 10(3):367–381. doi:10.1007/s10142-009-0145-8

    Article  CAS  PubMed  Google Scholar 

  38. Sreekantan L, Mathiason K, Grimplet J, Schlauch K, Dickerson JA, Fennell AY (2010) Differential floral development and gene expression in grapevines during long and short photoperiods suggests a role for floral genes in dormancy transitioning. Plant Mol Biol 73(1–2):191–205. doi:10.1007/s11103-010-9611-x

    Article  CAS  PubMed  Google Scholar 

  39. Pilati S, Perazzolli M, Malossini A, Cestaro A, Dematte L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C (2007) Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at veraison. BMC Genomics 8:428. doi:10.1186/1471-2164-8-428

    Article  PubMed Central  PubMed  Google Scholar 

  40. Lund ST, Peng FY, Nayar T, Reid KE, Schlosser J (2008) Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster. Plant Mol Biol 68(3):301–315. doi:10.1007/s11103-008-9371-z

    Article  CAS  PubMed  Google Scholar 

  41. Lijavetzky D, Carbonell-Bejerano P, Grimplet J, Bravo G, Flores P, Fenoll J, Hellin P, Oliveros JC, Martinez-Zapater JM (2012) Berry flesh and skin ripening features in Vitis vinifera as assessed by transcriptional profiling. PLoS One 7(6):e39547. doi:10.1371/journal.pone.0039547

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Ali MB, Howard S, Chen S, Wang Y, Yu O, Kovacs LG, Qiu W (2011) Berry skin development in Norton grape: distinct patterns of transcriptional regulation and flavonoid biosynthesis. BMC Plant Biol 11:7. doi:10.1186/1471-2229-11-7

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Diaz-Riquelme J, Grimplet J, Martinez-Zapater JM, Carmona MJ (2012) Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol 12:181. doi:10.1186/1471-2229-12-181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. 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(2):344–360. doi:10.1093/pcp/pcq196

    Article  CAS  PubMed  Google Scholar 

  45. Wang N, Zheng Y, Xin H, Fang L, Li S (2012) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep. doi:10.1007/s00299-012-1340-y

    Google Scholar 

  46. Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11(3):109–112. doi:10.1016/j.tplants.2006.01.004

    Article  CAS  PubMed  Google Scholar 

  47. Dong CJ, Liu JY (2010) The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biol 10:47. doi:10.1186/1471-2229-10-47

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the earmarked fund for the China Agriculture Research System. The authors are grateful to the persons who shared their microarray data online and to Priscilla Licht for help in revising our English composition.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Tao Zhao, Jingying Liu & Fengwang Ma

  2. Institute of Pomology and Olericulture, Sichuan Agricultural University, Chengdu, 611130, People’s Republic of China

    Hui Xia

Authors
  1. Tao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jingying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fengwang Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengwang Ma.

Additional information

Tao Zhao and Hui Xia contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, T., Xia, H., Liu, J. et al. The gene family of dehydration responsive element-binding transcription factors in grape (Vitis vinifera): genome-wide identification and analysis, expression profiles, and involvement in abiotic stress resistance. Mol Biol Rep 41, 1577–1590 (2014). https://doi.org/10.1007/s11033-013-3004-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-013-3004-6

Keywords

Search

Navigation