Skip to main content
SpringerLink
Log in

Differential Gene Expression Pattern of Drought Responsive Transcription Factors in Chickpea: An Expressional Analysis

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Chickpea (Cicer arietinum L.) is an important grain crop mainly grown in arid and semi-arid regions of the world. Drought is the major factor limiting chickpea growth and productivity. Transcription factors (TFs) genes have been reported as key regulators of drought tolerance in plants. In this study, we determined the relative gene expression of transcription factors of WRKY, DREB2A, and CarNAC3 in three weeks seedlings of tolerant (MCC537) and susceptible (MCC674) genotypes under progressive water deficit through semi-quantitative reverse transcriptase PCR (SqRT-PCR) method. Furthermore, results of SqRT-PCR were more confirmed by quantitative PCR (qPCR). Relative gene expression analysis of the selected genes using qPCR revealed different dehydration-responsive expression patterns. The expression of WRKY gene was significantly induced in both tolerant and sensitive genotypes under severe drought stress (at the last time point). Also, in tolerant genotype, DREB2A gene was approximately expressed three, five and fourfold higher than control plants at three times points, respectively. Moreover, the expression level of CarNAC3 gene in this genotype increased four and twofold higher compared to the relative control at 2 and 4 days after stress, respectively. However, the expression of these genes in the susceptible genotype was constant or decreased relative to the control. Furthermore, the CarNAC3 and DREB2A genes showed higher and more effective expression than the WRKY gene. Overall, the results demonstrated that these TFs may play an important role to improve drought tolerance and have a potential to facilitate molecular breeding and development of drought-tolerant chickpea varieties.

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

Similar content being viewed by others

References

  • Abid G, Muhovski Y, Mingeot D, Watillon B, Toussaint A, Mergeai G, M’hamdi M, Sassi K, Jebara M (2015) Identification and characterization of drought stress responsive genes in faba bean (Vicia faba L.) by suppression subtractive hybridization. Plant Cell Tissue Org Cult 121:367–379

    CAS  Google Scholar 

  • Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38:3883–3896

    CAS  PubMed  Google Scholar 

  • Agarwal G, Garg V, Kudapa H, Doddamani D, Pazhamala LT, Khan AW, Thudi M, Lee SH, Varshney RK (2016) Genome-wide dissection of AP2/ERF and HSP90 gene families in five legumes and expression profiles in chickpea and pigeonpea. Plant Biotechnol J 14:1563–1577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad F, Gaur P, Croser J (2005) Chickpea (Cicer arietinum L.). In: Singh R, Jauhar P (eds) Genetic resources, chromosome engineering and crop improvement—grain legumes. CRC Press, Boca Raton, pp 185–214

    Google Scholar 

  • Anbazhagan K, Bhatnagar-Mathur P, Vadez V, Dumbala S, Kishor PBK, Sharma K (2015) DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes. Plant Cell Rep 34:199–210

    CAS  PubMed  Google Scholar 

  • Badhan S, Kole P, Ball A, Mantri N (2018) RNA sequencing of leaf tissues from two contrasting chickpea genotypes reveals mechanisms for drought tolerance. Plant Physiol Biochem 129:295–304

    CAS  PubMed  Google Scholar 

  • Basu S, Rabara R (2017) Abscisic acid—an enigma in the abiotic stress tolerance of crop plants. Plant Gene 11:90–98

    CAS  Google Scholar 

  • Çevik S, Akpinar G, Yildizli A, Kasap M, Karaosmanoğlu K, Ünyayar S (2019) Comparative physiological and leaf proteome analysis between drought-tolerant chickpea Cicer reticulatum and drought-sensitive chickpea C. arietinum. J Biosci 44:20

    PubMed  Google Scholar 

  • Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochem Biophys Acta 1819:120–128

    CAS  PubMed  Google Scholar 

  • Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

    CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    CAS  PubMed  Google Scholar 

  • FAOSTAT (2017) Food and Agriculture Organization of the United Nations Statistics Division. FAO, Rome

    Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF Cold Response Pathway. Plant Cell 14:1675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ganjeali A, Porsa H, Bagheri A (2011) Assessment of Iranian chickpea (Cicer arietinum L.) germplasms for drought tolerance. Agric Water Manag 98:1477–1484

    Google Scholar 

  • Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Commun 396:283–288

    CAS  PubMed  Google Scholar 

  • Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, Jain M (2016) Transcriptome analyses reveal genotype- and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci Rep 6:19228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ha CV, Nasr Esfahani M, Watanabe Y, Tran UT, Sulieman S, Mochida K, Van Nguyen D, Tran LSP (2014) Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS ONE 9:e114107

    PubMed  PubMed Central  Google Scholar 

  • Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193

    CAS  PubMed  Google Scholar 

  • Hassan NM, El-Bastawisy ZM, El-Sayed AK, Ebeed HT, Nemat Alla MM (2015) Roles of dehydrin genes in wheat tolerance to drought stress. J Adv Res 6:179–188

    CAS  PubMed  Google Scholar 

  • Heid CA, Stevens J, Livak KJ, Williams PM (1996) Real time quantitative PCR. Genome Res 6:986–994

    CAS  PubMed  Google Scholar 

  • Hiremath PJ, Farmer A, Cannon SB, Woodward J, Kudapa H, Tuteja R, Kumar A, Bhanuprakash A, Mulaosmanovic B, Gujaria N, Krishnamurthy L, Gaur PM, Kavikishor PB, Shah T, Srinivasan R, Lohse M, Xiao Y, Town CD, Cook DR, May GD, Varshney RK (2011) Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol J 9:922–931

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Yadav M, Kant C, Sharma P, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729

    CAS  PubMed  Google Scholar 

  • Konda AK, Farmer R, Soren KR, Ps S, Setti A (2018) Structural modelling and molecular dynamics of a multi-stress responsive WRKY TF-DNA complex towards elucidating its role in stress signalling mechanisms in chickpea. J Biomol Struct Dyn 36:2279–2291

    CAS  PubMed  Google Scholar 

  • Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semiarid environments. In: Spaks DLED (ed) Advances in agronomy. Academic Press, New York, pp 107–138

    Google Scholar 

  • Kumar M, Chauhan AS, Kumar M, Yusuf MA, Sanyal I, Chauhan PS (2019) Transcriptome sequencing of chickpea (Cicer arietinum l.) genotypes for identification of drought-responsive genes under drought stress condition. Plant Mol Biol Rep 37:186–203

    CAS  Google Scholar 

  • Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinform 6(1):62

    Google Scholar 

  • Lata C, Muthamilarasan M, Prasad M (2015) Drought Stress responses and signal transduction in plants. In: Pandey GK (ed) Elucidation of abiotic stress signaling in plants: functional genomics perspectives. Springer, New York, pp 195–225

    Google Scholar 

  • Li MJ, Qiao Y, Li YQ, Shi ZL, Zhang N, Bi CL, Guo JK (2016) A R2R3-MYB transcription factor gene in common wheat (namely TaMYBsm1) involved in enhancement of drought tolerance in transgenic arabidopsis. J Plant Res 129:1097–1107

    CAS  PubMed  Google Scholar 

  • Mahdavi Mashaki K, Garg V, Nasrollahnezhad Ghomi AA, Kudapa H, Chitikineni A, Zaynali K, Nezhad K, Yamchi A, Soltanloo H, Varshney RK, Thudi M (2018) RNA-Seq analysis revealed genes associated with drought stress response in kabuli chickpea (Cicer arietinum L.). PLoS ONE 13:e0199774

    PubMed  PubMed Central  Google Scholar 

  • Marè C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L (2004) Hv-WRKY38: a new transcription factor involved in cold and drought-response in barley. Plant Mol Biol 55:399–416

    PubMed  Google Scholar 

  • Meena MK, Ghawana S, Sardar A, Dwivedi V, Khandal H, Roy R, Chattopadhyay D (2015) Investigation of genes encoding calcineurin B-like protein family in legumes and their expression analyses in chickpea (Cicer arietinum L). PLoS ONE 10:e0123640

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nguyen KH, Ha CV, Watanabe Y, Tran UT, Nasr Esfahani M, Nguyen DV, Tran LSP (2015) Correlation between differential drought tolerability of two contrasting drought-responsive chickpea cultivars and differential expression of a subset of CaNAC genes under normal and dehydration conditions. Front Plant Sci 6:449

    PubMed  PubMed Central  Google Scholar 

  • Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248

    PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran LS (2014) Response of plants to water stress. Front Plant Sci 5:86

    PubMed  PubMed Central  Google Scholar 

  • Peng H, Cheng HY, Chen C, Yu XW, Yang JN, Gao WR, Shi QH, Zhang H, Li JG, Ma H (2009) A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. J Plant Physiol 166:1934–1945

    CAS  PubMed  Google Scholar 

  • Ramalingam A, Kudapa H, Pazhamala LT, Garg V, Varshney RK (2015) Gene expression and yeast two-hybrid studies of 1R-MYB transcription factor mediating drought stress response in chickpea (Cicer arietinum L.). Front Plant Sci 6:1117

    PubMed  PubMed Central  Google Scholar 

  • Roorkiwal M, Nayak SN, Thudi M, Upadhyaya HD, Brunel D, Mournet P, This D, Sharma PC, Varshney RK (2014) Allele diversity for abiotic stress responsive candidate genes in chickpea reference set using gene based SNP markers. Front Plant Sci 5:248

    PubMed  PubMed Central  Google Scholar 

  • Roorkiwal M, Rathore A, Das RR, Singh MK, Jain A, Srinivasan S, Gaur PM, Chellapilla B, Tripathi S, Li Y, Hickey JM, Lorenz A, Sutton T, Crossa J, Jannink JL, Varshney RK (2016) Genome-enabled prediction models for yield related traits in chickpea. Front Plant Sci 7:1666

    PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Google Scholar 

  • Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla RK, Tripathi V, Jain D, Yadav RK, Chattopadhyay D (2009) CAP2 enhances germination of transgenic tobacco seeds at high temperature and promotes heat stress tolerance in yeast. FEBS J 276:5252–5262

    CAS  PubMed  Google Scholar 

  • Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C, Zhang F, Chen X (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144:210–224

    CAS  PubMed  Google Scholar 

  • 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 1:32–39

    PubMed  Google Scholar 

  • Varshney R, Pazhamala L, Kashiwagi J, Gaur P, Krishnamurthy L, Hoisington D (2011) Genomics and physiological approaches for root trait breeding to improve drought tolerance in chickpea (Cicer arietinum L.). In: Costa De Oliveira A, Varshney RK (eds.) Root genomics. Springer, Berlin, pp 233–250.

  • Varshney RK, Mohan SM, Gaur PM, Gangarao NVPR, Pandey MK, Bohra A, Sawargaonkar SL, Chitikineni A, Kimurto PK, Janila P, Saxena KB, Fikre A, Sharma M, Rathore A, Pratap A, Tripathi S, Datta S, Chaturvedi SK, Mallikarjuna N, Anuradha G, Babbar A, Choudhary AK, Mhase MB, Bharadwaj C, Mannur DM, Harer PN, Guo B, Liang X, Nadarajan N, Gowda CLL (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31:1120–1134

    PubMed  Google Scholar 

  • Waqas M, Azhar MT, Rana IA, Azeem F, Ali MA, Nawaz MA, Chung G, Atif RM (2019) Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea (Cicer arietinum L.) reveal their role in abiotic stress-responses. Genes Genomics 41:467–481

    CAS  PubMed  Google Scholar 

  • Yu X, Liu Y, Wang S, Tao Y, Wang Z, Shu Y, Peng H, Mijiti A, Wang Z, Zhang H, Ma H (2016) CarNAC4, a NAC-type chickpea transcription factor conferring enhanced drought and salt stress tolerances in arabidopsis. Plant Cell Rep 35:613–627

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Research Center for Plant Sciences, Ferdowsi University of Mashhad.

Author information

Authors and Affiliations

  1. Biotechnology and Plant Breeding Dept., College of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Sara Borhani & Abdolreza Bagheri

  2. Research Center for Plant Sciences, Ferdowsi University of Mashhad, Mashhad, Iran

    Saeedreza Vessal & Farhad Shokouhifar

Authors
  1. Sara Borhani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saeedreza Vessal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdolreza Bagheri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Farhad Shokouhifar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saeedreza Vessal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Borhani, S., Vessal, S., Bagheri, A. et al. Differential Gene Expression Pattern of Drought Responsive Transcription Factors in Chickpea: An Expressional Analysis. J Plant Growth Regul 39, 1211–1220 (2020). https://doi.org/10.1007/s00344-019-10056-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-019-10056-5

Keywords

Search

Navigation