Skip to main content

Advertisement

Log in

Overexpression of the transcription factor HvSNAC1 improves drought tolerance in barley (Hordeum vulgare L.)

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

NAC proteins constitute a family of plant-specific transcription factors that are involved in many plant cellular processes including responses to abiotic stress. In this study, a cDNA clone encoding the HvSNAC1 transcription factor was isolated from drought-stressed barley using a bioinformatics approach based on amino acid sequence data of the stress-related SNAC1 protein from rice. Phylogenetic analysis of the deduced amino acid sequence of HvSNAC1 showed that this protein belongs to the stress clade of NAC proteins that include SNAC1 and TaNAC2. Expression analysis indicated that the HvSNAC1 gene is strongly induced by different abiotic stresses including drought. Overexpression of HvSNAC1 in barley under the control of a constitutive promoter produced plants that grew normally under well-watered conditions when compared with wild-type plants. Transgenic barley plants overexpressing HvSNAC1 showed higher drought tolerance at different growth stages when compared with wild-type plants. In addition, the constitutive overexpression of HvSNAC1 resulted in improved water status, photosynthetic activity and reduced water loss rate when compared with wild-type plants under drought conditions. Furthermore, the transgenic plants also showed significantly improved productivity, as reflected by the increase in biological yield over the wild-type plants under severe field drought conditions. In conclusion, the HvSNAC1 gene could be a useful tool for improving barley productivity under field drought conditions without impairment in growth under normal field conditions.

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

Similar content being viewed by others

References

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Bartels D, Sunkars R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Bartlett JG, Alves SC, Smedley M, Snape JW, Harwood WA (2008) High-throughput Agrobacterium-mediated barley transformation. Plant Methods 22:1–12

    Google Scholar 

  • Bhargava S, Sawant K (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32

    Article  CAS  Google Scholar 

  • Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Christiansen M, Holm P, Gregersen P (2011) Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggest conserved functions compared to both monocots and dicots. BMC Res Notes 4:302

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol l46:521–526

    Article  Google Scholar 

  • Delessert C, Kazan K, Wilson I, Straeten D, Manners J, Dennis E, Dolferus R (2005) The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J 43:745–757

    Article  CAS  PubMed  Google Scholar 

  • Fang Y, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563

    Article  CAS  PubMed  Google Scholar 

  • Habash DZ, Kehel Z, Nachit M (2009) Genomic approaches for designing durum wheat ready for climate change with a focus on drought. J Exp Bot 60:2805–2815

    Article  CAS  PubMed  Google Scholar 

  • Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383–397

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu H, Dai J, Yao B, Xiao X, Li Q, Zhang XL (2006) Over-expressing a NAM, ATAF and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  CAS  PubMed  Google Scholar 

  • Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

    Article  CAS  PubMed  Google Scholar 

  • Jensen M, Rung J, Gregersen P, Gjetting T, Fuglsang A, Hansen M, Joehnk N, Lyngkjaer M, Collinge D (2007) The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol Biol 65:137–150

    Article  CAS  PubMed  Google Scholar 

  • Jeong J, Kim Y, Baek K, Jung H, Ha S, Choi Y, Kim M, Reuzeau C, Kim J (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer Y, Rouzé 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 30:325–327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu P, Chen N, An R, Su Z, Qi B, Ren F, Chen J, Wang X (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson G (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Mir RR, Zaman-Allah M, Sreenivasulu N, Trethowan R, Varshney RK (2012) Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops. Theor Appl Genet 125:625–645

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249

    Article  CAS  PubMed  Google Scholar 

  • Mysore K, Crasta R, Tuori P, Folkerts O, Swirsky B, Martin B (2002) Comprehensive transcript profiling of Pto and Prf-mediated host defense responses to infection by Pseudomonas syringae pv tomato. Plant J 32:299–315

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signalling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103

    Article  CAS  PubMed  Google Scholar 

  • Olsen A, Ernst H, Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  CAS  PubMed  Google Scholar 

  • Puranik S, Sahu P, Srivastava P, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

    Article  CAS  PubMed  Google Scholar 

  • Ren T, Qu F, Morris TJ (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917–1926

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saad AS, Li X, Li H, Huang T, Gao C, Guo M, Cheng W, Zhao G, Liao Y (2013) A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Sci 203–204:33–40

    Article  PubMed  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses using full-length cDNA microarray. Plant Cell 13:61–72

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca M, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes unlock the future. Curr Opin Biotechnol 17:113–122

    Article  CAS  PubMed  Google Scholar 

  • Vandesompele J, Preter KD, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.1–research0034.11

    Article  Google Scholar 

  • Wang M, Waterhouse PM (1997) A Rapid and simple method of assaying plants transformed with hygromycin or PPT resistance genes. Plant Mol Biol Rep 15:209–215

    Article  CAS  Google Scholar 

  • Xia N, Zhang G, Liu X, Deng L, Cai G, Zhang Y, Wang X, Zhao J, Huang L, Kang Z (2010) Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37:3703–3712

    Article  CAS  PubMed  Google Scholar 

  • Xue G, Waya H, Richardsonb T, Drentha J, Joycec P, McIntyrea L (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Bio l57:781–803

    Article  Google Scholar 

  • Youens-Clark K, Buckler E, Casstevens T, Chen C, DeClerck G, Derwent P, Dharmawardhana P, Jaiswal P, Kersey P, Karthikeyan A, Lu J, McCouch S, Ren L, Spooner W, Stein J, Thomason J, Wei S, Ware D (2010) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39:D1085–D1094

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu J (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmermann P, Laule O, Schmitz J, Hruz T, Bleuler S, Gruissem W (2008) GeneVestigator transcriptome meta-analysis and biomarker search using rice and barley gene expression databases. Mol Plant 1:851–857

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Mrs. Samar Misbeh, Miss Shireen Qasrawi and Mr. Mohammad Sheik Omar for technical assistance. This work was supported in part by a Grant from the Scientific Research Fund, Ministry of Higher Education, in part by a Grant from the Deanship of Scientific Research, University of Jordan and in part by a Grant from the International Foundation of Science/Sweden.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. M. Al Abdallat.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1224 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Al Abdallat, A.M., Ayad, J.Y., Abu Elenein, J.M. et al. Overexpression of the transcription factor HvSNAC1 improves drought tolerance in barley (Hordeum vulgare L.). Mol Breeding 33, 401–414 (2014). https://doi.org/10.1007/s11032-013-9958-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-013-9958-1

Keywords

Navigation