Skip to main content
Log in

Overexpression of AtDREB1D transcription factor improves drought tolerance in soybean

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Drought is one of the major abiotic stresses that affect productivity in soybean (Glycine max L.) Several genes induced by drought stress include functional genes and regulatory transcription factors. The Arabidopsis thaliana DREB1D transcription factor driven by the constitutive and ABA-inducible promoters was introduced into soybean through Agrobacterium tumefaciens-mediated gene transfer. Several transgenic lines were generated and molecular analysis was performed to confirm transgene integration. Transgenic plants with an ABA-inducible promoter showed a 1.5- to two-fold increase of transgene expression under severe stress conditions. Under well-watered conditions, transgenic plants with constitutive and ABA-inducible promoters showed reduced total leaf area and shoot biomass compared to non-transgenic plants. No significant differences in root length or root biomass were observed between transgenic and non-transgenic plants under non-stress conditions. When subjected to gradual water deficit, transgenic plants maintained higher relative water content because the transgenic lines used water more slowly as a result of reduced total leaf area. This caused them to wilt slower than non-transgenic plants. Transgenic plants showed differential drought tolerance responses with a significantly higher survival rate compared to non-transgenic plants when subjected to comparable severe water-deficit conditions. Moreover, the transgenic plants also showed improved drought tolerance by maintaining 17–24 % greater leaf cell membrane stability compared to non-transgenic plants. The results demonstrate the feasibility of engineering soybean for enhanced drought tolerance by expressing stress-responsive genes.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  1. Boyer JS (1982) Plant productivity and environment. Science 218(4571):443–448. doi:10.1126/science.218.4571.443

    Article  CAS  PubMed  Google Scholar 

  2. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227. doi:10.1093/jxb/erl164

    Article  CAS  PubMed  Google Scholar 

  3. Tran LS, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM crops 1(1):32–39. doi:10.4161/gmcr.1.1.10569

    Article  PubMed  Google Scholar 

  4. Tran LS, Mochida K (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10(4):447–462. doi:10.1007/s10142-010-0178-z

    Article  CAS  PubMed  Google Scholar 

  5. Hadiarto T, Tran LS (2011) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30(3):297–310. doi:10.1007/s00299-010-0956-z

    Article  CAS  PubMed  Google Scholar 

  6. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63(4):1593–1608

  7. Jogaiah S, Govind SR, Tran LSP (2013) Systems biology-based approaches toward understanding drought tolerance in food crops. Crit Rev Biotechnol 33(1):23–39. doi:10.3109/07388551.2012.659174

    Article  PubMed  Google Scholar 

  8. Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50(7):1260–1276. doi:10.1093/pcp/pcp082

    Article  CAS  PubMed  Google Scholar 

  9. Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol Plant 3(3):469–490. doi:10.1093/mp/ssq016

    Article  CAS  PubMed  Google Scholar 

  10. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):86–96. doi:10.1016/j.bbagrm.2011.08.004

    Article  CAS  PubMed  Google Scholar 

  11. Thao NP, Tran LS (2012) Potentials toward genetic engineering of drought-tolerant soybean. Crit Rev Biotechnol 32(4):349–362. doi:10.3109/07388551.2011.643463

    Article  PubMed  Google Scholar 

  12. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64(2):445–458. doi:10.1093/jxb/ers354

    Article  CAS  PubMed  Google Scholar 

  13. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol. doi:10.1111/nph.12613

    PubMed  Google Scholar 

  14. 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 

  15. Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9(2):189–195. doi:10.1016/j.pbi.2006.01.019

    Article  CAS  PubMed  Google Scholar 

  16. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17(2):113–122. doi:10.1016/j.copbio.2006.02.002

    Article  CAS  PubMed  Google Scholar 

  17. 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(12):1263–1274. doi:10.1007/s00299-006-0204-8

    Article  CAS  PubMed  Google Scholar 

  18. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125. doi:10.1016/j.tibs.2011.11.007

    Article  CAS  PubMed  Google Scholar 

  19. 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(2):639–648. doi:10.1104/Pp.006478

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Siddiqua M, Nassuth A (2011) Vitis CBF1 and Vitis CBF4 differ in their effect on Arabidopsis abiotic stress tolerance, development and gene expression. Plant Cell Environ 34:1345–1359

    Article  CAS  PubMed  Google Scholar 

  21. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17(3):287–291

    Article  CAS  PubMed  Google Scholar 

  22. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45(3):346–350

    Article  CAS  PubMed  Google Scholar 

  23. Fu DL, Huang BR, Xiao YM, Muthukrishnan S, Liang GH (2007) Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Rep 26(4):467–477. doi:10.1007/s00299-006-0258-7

    Article  CAS  PubMed  Google Scholar 

  24. Leung J, Giraudat J (1998) Abscisic Acid Signal Transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222. doi:10.1146/annurev.arplant.49.1.199

    Article  CAS  PubMed  Google Scholar 

  25. Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123(2):553–562

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55(407):2343–2351. doi:10.1093/jxb/erh276

    Article  CAS  PubMed  Google Scholar 

  27. Shen QX, Zhang PN, Ho THD (1996) Aba response complexes: composite promoter units which are necessary and sufficient for ABA induction of gene expression in barley, Hordeum vulgare. Plant Physiol 111(2):563-563

    Google Scholar 

  28. Shen QX, Ho AHD (1997) Promoter switches specific for abscisic acid (ABA)-induced gene expression in cereals. Physiol Plant 101(4):653–664. doi:10.1034/j.1399-3054.1997.1010401.x

    Article  CAS  Google Scholar 

  29. Su J, Shen QX, Ho THD, Wu R (1998) Dehydration-stress-regulated transgene expression in stably transformed rice plants. Plant Physiol 117(3):913–922. doi:10.1104/Pp.117.3.913

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Garg AK, Kim JK, Owens TG, Ranwala AP, Do Choi Y, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99(25):15898–15903. doi:10.1073/pnas.252637799

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Lee JT, Prasad V, Yang PT, Wu JF, Ho THD, Charng YY, Chan MT (2003) Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ 26(7):1181–1190. doi:10.1046/j.1365-3040.2003.01048.x

    Article  CAS  Google Scholar 

  32. 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(12):2191–2198. doi:10.1007/s10529-008-9811-5

    Article  PubMed  Google Scholar 

  33. Bhatnagar-Mathur P, Devi MJ, Vadez V, Sharma KK (2009) Differential antioxidative responses in transgenic peanut bear no relationship to their superior transpiration efficiency under drought stress. J Plant Physiol 166(11):1207–1217. doi:10.1016/j.jplph.2009.01.001

    Article  CAS  PubMed  Google Scholar 

  34. Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47(3):493–500. doi:10.1139/g03-140

    Article  CAS  PubMed  Google Scholar 

  35. Westgate ME, Peterson CM (1993) Flower and pod development in water-deficient soybeans (Glycine-Max L Merr). J Exp Bot 44(258):109–117. doi:10.1093/Jxb/44.1.109

    Article  Google Scholar 

  36. Zeng P, Vadnais DA, Zhang Z, Polacco JC (2004) Refined glufosinate selection in Agrobacterium-mediated transformation of soybean [Glycine max (L.) Merrill]. Plant Cell Rep 22(7):478–482. doi:10.1007/s00299-003-0712-8

    Article  CAS  PubMed  Google Scholar 

  37. Neelakandan AK, Chamala S, Valliyodan B, Nes WD, Nguyen HT (2012) Metabolic engineering of soybean affords improved phytosterol seed traits. Plant Biotechnol J 10(1):12–19. doi:10.1111/j.1467-7652.2011.00623.x

    Article  CAS  PubMed  Google Scholar 

  38. Yamaguchi M, Sharp RE (2010) Complexity and coordination of root growth at low water potentials: recent advances from transcriptomic and proteomic analyses. Plant Cell Environ 33(4):590–603. doi:10.1111/j.1365-3040.2009.02064.x

    Article  CAS  PubMed  Google Scholar 

  39. Tripathy JN, Zhang J, Robin S, Nguyen TT, Nguyen HT (2000) QTLs for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. Theor Appl Genet 100(8):1197–1202. doi:10.1007/s001220051424

    Article  CAS  Google Scholar 

  40. Babu RC, Zhang JX, Blum A, Ho THD, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166(4):855–862. doi:10.1016/j.plantsci.2003.11.023

    Article  CAS  Google Scholar 

  41. Le DT, Aldrich DL, Valliyodan B, Watanabe Y, Van Ha C, Nishiyama R, Guttikonda SK, Quach TN, Gutierrez-Gonzalez JJ, Tran LSP, Nguyen HT (2012) Evaluation of candidate reference genes for normalization of quantitative rt-pcr in soybean tissues under various abiotic stress conditions. Plos One 7(9):ARTN e46487. doi:10.1371/journal.pone.0046487

    Article  Google Scholar 

  42. 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. doi:10.2307/3870648

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Chow B, McCourt P (2004) Hormone signalling from a developmental context. J Exp Bot 55(395):247–251. doi:10.1093/jxb/erh032

    Article  CAS  PubMed  Google Scholar 

  44. Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7(3):295–307

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Al-Abed D, Madasamy P, Talla R, Goldman S, Rudrabhatla S (2007) Genetic engineering of maize with the Arabidopsis DREB1A/CBF3 gene using split-seed explants. Crop Sci 47:2390–2402

    Article  CAS  Google Scholar 

  46. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21(6):535–553. doi:10.1046/j.1365-3040.1998.00309.x

    Article  CAS  Google Scholar 

  47. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41(4):758–769

  48. de Paiva Rolla AA, de Fatima Correa Carvalho J, Fuganti-Pagliarini R, Engels C, Do Rio A, Marin SR, de Oliveira MC, Beneventi MA, Marcelino-Guimaraes FC, Farias JR, Neumaier N, Nakashima K, Yamaguchi-Shinozaki K, Nepomuceno AL (2014) Phenotyping soybean plants transformed with rd29A:AtDREB1A for drought tolerance in the greenhouse and field. Transgenic Res 23:75–87. doi:10.1007/s11248-013-9723-6

    Article  PubMed  Google Scholar 

  49. Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5(3):250–257. doi:10.1016/S1369-5266(02)00255-8

    Article  CAS  PubMed  Google Scholar 

  50. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6(9):431–438. doi:10.1016/S1360-1385(01)02052-0

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Zhanyuan Zhang, Plant Transformation Core Facility, University of Missouri for the soybean transformation and Dr. Thomas Clemente, University of Nebraska for providing sub-cloning vectors. This work was supported by the United Soybean Board and the Missouri Soybean Merchandising Council funding to HTN.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Henry T. Nguyen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guttikonda, S.K., Valliyodan, B., Neelakandan, A.K. et al. Overexpression of AtDREB1D transcription factor improves drought tolerance in soybean. Mol Biol Rep 41, 7995–8008 (2014). https://doi.org/10.1007/s11033-014-3695-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3695-3

Keywords

Navigation