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DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes

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Abstract

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We demonstrate the role of DREB1A transcription factor in better root and shoot partitioning and higher transpiration efficiency in transgenic chickpea under drought stress

Abstract

Chickpea (Cicer arietinum L.) is mostly exposed to terminal drought stress which adversely influences its yield. Development of cultivars for suitable drought environments can offer sustainable solutions. We genetically engineered a desi-type chickpea variety to ectopically overexpress AtDREB1A, a transcription factor known to be involved in abiotic stress response, driven by the stress-inducible Atrd29A promoter. From several transgenic events of chickpea developed by Agrobacterium-mediated genetic transformation, four single copy events (RD2, RD7, RD9 and RD10) were characterized for DREB1A gene overexpression and evaluated under water stress in a biosafety greenhouse at T6 generation. Under progressive water stress, all transgenic events showed increased DREB1A gene expression before 50 % of soil moisture was lost (50 % FTSW or fraction of transpirable soil water), with a faster DREB1A transcript accumulation in RD2 at 85 % FTSW. Compared to the untransformed control, RD2 reduced its transpiration in drier soil and higher vapor pressure deficit (VPD) range (2.0–3.4 kPa). The assessment of terminal water stress response using lysimetric system that closely mimics the soil conditions in the field, showed that transgenic events RD7 and RD10 had increased biomass partitioning into shoot, denser rooting in deeper layers of soil profile and higher transpiration efficiency than the untransformed control. Also, RD9 with deeper roots and RD10 with higher root diameter showed that the transgenic events had altered rooting pattern compared to the untransformed control. These results indicate the implicit influence of rd29A::DREB1A on mechanisms underlying water uptake, stomatal response, transpiration efficiency and rooting architecture in water-stressed plants.

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Abbreviations

DAS:

Days after sowing

DREB1A:

Dehydration-responsive element binding factor 1A

FTSW:

Fraction of transpirable soil water

NTR:

Normalized transpiration ratio

nptII:

Neomycin phosphotransferase II

RLD:

Root length density

TE:

Transpiration efficiency

VPD:

Vapor pressure deficit

WW:

Well-watered

WS:

Water-stressed

References

  • Anbazhagan K, Bhatnagar-Mathur P, Sharma KK, Baddam R, Kavi Kishor PB, Vadez V (2014) Changes in water uptake and phenology favors yield gain in terminal water stressed chickpea AtDREB1A transgenics in greenhouse environment. Funct Plant Biol. doi:10.1071/FP14115

    Google Scholar 

  • Behnam B, Kikuchi A, Celebi-Toprak F, Yamanaka S, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2006) The Arabidopsis DREB1A gene driven by the stress-inducible rd29A promoter increases salt-stress tolerance in proportion to its copy number in tetrasomic tetraploid potato (Solanum tuberosum). Plant Biotechnol 23:169–177. doi:10.1007/s00299-007-0360-5

    Article  CAS  Google Scholar 

  • Belko N, Zaman-Allah M, Cisse N, Diop NN, Zombre G, Ehlers JD, Vadez V (2012) Lower soil moisture threshold for transpiration decline under water deficit correlates with lower canopy conductance and higher transpiration efficiency in drought tolerant cowpea. Funct Plant Biol 39:306–322. doi:10.1071/FP11282

    Article  Google Scholar 

  • Bhatnagar-Mathur P, Devi MJ, Reddy DS, Lavanya M, Vadez V, Serraj R, Yamaguchi-Shinozaki K, Sharma KK (2007) Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082. doi:10.1007/s00299-007-0406-8

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Devi JM, Lavanya M, Vani G, Sharma KK (2009) Genetic engineering of chickpea (Cicer arietinum L.) with the P5CSF129A gene for osmoregulation with implications on drought tolerance. Mol Breed 23:591–606. doi:10.1007/s11032-009-9258-y

    Article  CAS  Google Scholar 

  • Bhatnagar-Mathur P, Rao JS, Vadez V, Dumbala SR, Rathore A, Yamaguchi-Shinozaki K, Sharma KK (2014) Transgenic peanut overexpressing the DREB1A transcription factor has higher yields under drought stress. Mol Breed 33:327–340. doi:10.1007/s11032-013-9952-7

    Article  CAS  Google Scholar 

  • Celebi-Toprak F, Behnam B, Serrano G, Kasuga M, Yamaguchi-Shinozaki K, Naka H, Watanabe JA, Yamanaka S, Watanabe KN (2005) Tolerance to salt stress of the transgenic tetrasomic tetraploid potato, Solanum tuberosum cv Desiree appears to be induced by the DREB1A gene and rd29A promoter of Arabidopsis thaliana. Breed Sci 55:311–319. doi:10.1270/jsbbs.55.311

    Article  CAS  Google Scholar 

  • Cong L, Zheng H-C, Zhang Y-X, Chai T-Y (2008) Arabidopsis DREB1A confers high salinity tolerance and regulates the expression of GA dioxygenases in tobacco. Plant Sci 174:156–164. doi:10.1016/j.plantsci.2007.11.002

    Article  CAS  Google Scholar 

  • Datta K, Baisakh N, Ganguly M, Krishnan S, Yamaguchi Shinozaki K, Datta SK (2012) Overexpression of Arabidopsis and rice stress genes’ inducible transcription factor confers drought and salinity tolerance to rice. Plant Biotechnol J 10:579–586. doi:10.1111/j.1467-7652.2012.00688.x

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta S, Wood J, Hicks J (1983) A plant DNA mini preparation: version II. Plant Mol Biol Report 1:19–21. doi:10.1007/BF02712670

    Article  CAS  Google Scholar 

  • Devi MJ, Bhatnagar-Mathur P, Sharma KK, Serraj R, Anwar SY, Vadez V (2011) Relationships between transpiration efficiency and its surrogate traits in the rd29A:DREB1A transgenic lines of groundnut. J Agron Crop Sci 197:272–283. doi:10.1111/j.1439-037X.2011.00464.x

    Article  CAS  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865. doi:10.1104/pp.124.4.1854

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hong B, Tong Z, Ma N, Li J, Kasuga M, Yamaguchi-Shinozaki K, Gao J (2006) Heterologous expression of the AtDREB1A gene in chrysanthemum increases drought and salt stress tolerance. Sci China Ser C Life Sci 49:436–445. doi:10.1007/s11427-006-2014-1

    Article  CAS  Google Scholar 

  • Hsieh T-H, J-t Lee, Y-y Charng, Chan M-T (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626. doi:10.1104/pp.006783

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106. doi:10.1126/science.280.5360.104

    Article  CAS  PubMed  Google Scholar 

  • 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. Nature 17:287–291. doi:10.1038/7036

    CAS  Google Scholar 

  • 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 45:346–350. doi:10.1093/pcp/pch037

    Article  CAS  PubMed  Google Scholar 

  • Kholová J, Hash CT, Kakkera A, Kocová M, Vadez V (2010) Constitutive water-conserving mechanisms are correlated with the terminal drought tolerance of pearl millet [Pennisetum glaucum (L.) R. Br.]. J Exp Bot 61:369–377. doi:10.1093/jxb/erp314

    Article  PubMed Central  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. doi:10.1105/tpc.10.8.1391

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2005) Molecular studies on stress-responsive gene expression in Arabidopsis and improvement of stress tolerance in crop plants by regulon biotechnology. JARQ 39:221–229

    Article  CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71. doi:10.1111/j.1399-3054.2005.00592.x

    Article  CAS  Google Scholar 

  • Oh S-J, Song SI, Kim Y-S, Jang H-J, Kim SY, Kim M, Kim Y-K, Nahm BH, Kim J-K (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351. doi:10.1104/pp.104.059147.1

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 47:493–500. doi:10.1139/G03-140

    Article  CAS  PubMed  Google Scholar 

  • Polizel AM, Medri ME, Nakashima K, Yamanaka N, Farias JRB, de Oliveira MCN et al (2011) Molecular, anatomical and physiological properties of a genetically modified soybean line transformed with rd29A:AtDREB1A for the improvement of drought tolerance. Genet Mol Res 10:3641–3656. doi:10.4238/2011.October.21.4

    Article  CAS  PubMed  Google Scholar 

  • Ray JD, Sinclair TR (1998) The effect of pot size on growth and transpiration of maize and soybean during water deficit stress. J Exp Bot 49:1381–1386. doi:10.1093/jxb/49.325.1381

    Article  CAS  Google Scholar 

  • Saibo NJM, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623. doi:10.1093/aob/mcn227

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sambrook J, Fritsh EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sharma KK, Bhatnagar-Mathur P, Vani G (2006) Genetic engineering of chickpea for tolerance to drought stress. In: Annual workshop of Indo-Swiss collaboration in Biotechnology and Pulse Network, ICRISAT, Patancheru, India

  • Suo H, Ma Q, Ye K, Yang C, Tang Y, Hao J, Zhang Z-J, Chen M, Feng Y, Nian H (2012) Overexpression of AtDREB1A causes a severe dwarf phenotype by decreasing endogenous gibberellin levels in soybean [Glycine max (L.) Merr]. PLoS One 7:e45568. doi:10.1371/journal.pone.0045568

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trewavas A (2009) What is plant behaviour? Plant, Cell Environ 32:606–616. doi:10.1111/j.1365-3040.2009.01929.x

    Article  Google Scholar 

  • Trewavas AJ, Malhó R (1997) Signal perception and transduction: the origin of the phenotype. Plant Cell 9:1181–1195. doi:10.1105/tpc.9.7.1181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Turner, NC (2003) Adaptation to drought: lessons from studies with chickpea. Indian J Plant Physiol (special issue) 11–17

  • Vadez V, Rao S, Sharma KK, Devi MJ (2007) DREB1A allows for more water uptake in groundnut by a large modification in the root/shoot ratio under water deficit. SAT eJournal 5:1–5

    Google Scholar 

  • Vadez V, Rao JS, Bhatnagar-Mathur P, Sharma KK (2013) DREB1A promotes root development in deep soil layers and increases water extraction under water stress in groundnut. Plant Biol 15:45–52. doi:10.1111/j.1438-8677.2012.00588.x

    Article  CAS  PubMed  Google Scholar 

  • Vadez V, Kholova J, Medina S, Aparna K, Anderberg H (2014) Transpiration efficiency: new insights into an old story. J Exp Bot. doi:10.1093/jxb/eru040

    PubMed  Google Scholar 

  • Zaman-Allah M, Jenkinson DM, Vadez V (2011) Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use. Funct Plant Biol 38:270–281. doi:10.1071/FP10244

    Article  Google Scholar 

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Acknowledgments

This work was supported by funds from the Indo-Swiss Collaboration for Biotechnology (ISCB) that was jointly funded by the Swiss Agency for Development and Cooperation (SDC), Switzerland and the Department of Biotechnology (DBT), Government of India. We are grateful to Dr. K. Yamaguchi-Shinozaki, Japan International Research Center for Agricultural Sciences (JIRCAS), Japan, for providing the gene construct used for developing transgenic events. KA would like to acknowledge financial support from the Council for Scientific and Industrial Research (CSIR), Government of India, for her Ph.D. Program. This work was undertaken as part of the CGIAR Research Program on Grain Legumes.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Telangana, 502324, India

    Krithika Anbazhagan, Pooja Bhatnagar-Mathur, Vincent Vadez, Srinivas Reddy Dumbala & Kiran K. Sharma

  2. Department of Genetics, Osmania University, Hyderabad, Telangana, 500007, India

    Krithika Anbazhagan & P. B. Kavi Kishor

Authors
  1. Krithika Anbazhagan
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  2. Pooja Bhatnagar-Mathur
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  3. Vincent Vadez
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  4. Srinivas Reddy Dumbala
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  5. P. B. Kavi Kishor
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  6. Kiran K. Sharma
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Corresponding author

Correspondence to Kiran K. Sharma.

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Communicated by Prakash Lakshmanan.

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Anbazhagan, K., Bhatnagar-Mathur, P., Vadez, V. et al. DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes. Plant Cell Rep 34, 199–210 (2015). https://doi.org/10.1007/s00299-014-1699-z

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  • DOI: https://doi.org/10.1007/s00299-014-1699-z

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