Abstract
Drought is one of the major constraints in wheat production and causes a huge loss at grain-filling stage. In this study we highlighted the response of different wheat genotypes under drought stress at the grain-filling stage. Field experiments were conducted to evaluate 72 wheat (Triticum aestivum L.) genotypes under two water regimes: irrigated and drought condition. Four wheat genotypes, two each of drought tolerant (IC36761A, IC128335) and drought-susceptible category (IC335732 and IC138852) were selected on the basis of agronomic traits and drought susceptibility index (DSI), to understand their morphological, biochemical and molecular basis of drought stress tolerance. Among agronomic traits, productive tillers followed by biomass had high percent reduction under drought stress, thus drought stress had a great impact. Antioxidant activity (AO), total phenolic and proline content were found to be significantly higher in IC128335 genotype. Differential expression pattern of transcription factors of ten genes revealed that transcription factor qTaWRKY2 followed by qTaDREB, qTaEXPB23 and qTaAPEX might be utilized for developing wheat varieties resistant to drought stress. Understanding the role of TFs would be helpful to decipher the molecular mechanism involved in drought stress. Identified genotypes (IC128335 and IC36761A) may be useful as parental material for future breeding program to generate new drought-tolerant varieties.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
AbdElgawad H, Zinta G, Beemster GTS et al (2016) Future climate CO2 levels mitigate stress impact on plants: increased defense or decreased challenge? Front Plant Sci 7:556. https://doi.org/10.3389/fpls.2016.00556
Agarwal G, Garg V, Kudapa H et al (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. https://doi.org/10.1111/pbi.12520
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. https://doi.org/10.1007/s11033-010-0504-5
Almer C, Laurent-Lucchetti J, Oechslin M et al (2012) Wheat yield loss attributable to heat waves, drought and water excess at the global, national and subnational scales Wheat yield loss attributable to heat waves, drought and water excess at the global, national and subnational scales. Nat Commun 3:1293. https://doi.org/10.1016/j.jeem.2017.06.002
Appels R, Eversole K, Feuillet C et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):eaar7191
Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Arumuganathan K, Earle ED (1991) Estimation of nuclear DNA content of plants by flow cytometry. Plant Mol Biol Rep 9:229–241. https://doi.org/10.1007/BF02672073
Bakshi M, Oelmüller R (2014) WRKY transcription factors. Plant Signal Behav 9:e27700. https://doi.org/10.4161/psb.27700
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans Biol Sci 334:309–345
Bi H, Luang S, Li Y et al (2016) Identification and characterization of wheat drought-responsive MYB transcription factors involved in the regulation of cuticle biosynthesis. J Exp Bot 67:5363–5380. https://doi.org/10.1093/jxb/erw298
Bohnert HJ (2007) Abiotic stress. Encyclopedia of life sciences. Wiley, Chichester
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
Campbell BM, Vermeulen SJ, Aggarwal PK et al (2016) Reducing risks to food security from climate change. Global Food Secur 11:34–43
Daryanto S, Wang L, Jacinthe P-A (2016) Global Synthesis of drought effects on maize and wheat production. PLoS ONE 11:e0156362. https://doi.org/10.1371/journal.pone.0156362
del Pozo A, Castillo D, Inostroza L et al (2012) Physiological and yield responses of recombinant chromosome substitution lines of barley to terminal drought in a Mediterranean-type environment. Ann Appl Biol 160:157–167. https://doi.org/10.1111/j.1744-7348.2011.00528.x
del Pozo A, Matus I, Serret MD, Araus JL (2014) Agronomic and physiological traits associated with breeding advances of wheat under high-productive Mediterranean conditions. The case of Chile. Environ Exp Bot 103:180–189. https://doi.org/10.1016/J.ENVEXPBOT.2013.09.016
del Pozo A, Yáñez A, Matus IA et al (2016) Physiological traits associated with wheat yield potential and performance under water-stress in a Mediterranean environment. Front Plant Sci 7:987. https://doi.org/10.3389/fpls.2016.00987
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223. https://doi.org/10.1046/j.1365-313X.1993.04020215.x
Devi R, Kaur N, Gupta AK (2012) Potential of antioxidant enzymes in depicting drought tolerance of wheat (Triticum aestivum L.). Ind J Biochem Biophys 49:257–265
Eshdat Y, Holland D, Faltin Z, Ben-Hayyim G (1997) Plant glutathione peroxidases. Physiol Plant 100:234–240. https://doi.org/10.1111/j.1399-3054.1997.tb04779.x
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206. https://doi.org/10.1016/S1360-1385(00)01600-9
Farooq M, Aziz T, Basra SMA et al (2008) Chilling tolerance in hybrid maize induced by seed priming with salicylic acid. J Agron Crop Sci 194:161–168. https://doi.org/10.1111/j.1439-037X.2008.00300.x
Farooq M, Wahid A, Kobayashi N et al (2009) Plant drought stress: effects, mechanisms and management. Sustainable agriculture. Springer, Netherlands, Dordrecht, pp 153–188
Fleury D, Luo M-C, Dvorak J et al (2010) Physical mapping of a large plant genome using global high-information-content-fingerprinting: the distal region of the wheat ancestor Aegilops tauschii chromosome 3DS. BMC Genomics 11:382. https://doi.org/10.1186/1471-2164-11-382
Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364. https://doi.org/10.1034/j.1399-3054.2003.00223.x
Furbank RT, Tester M (2011) Phenomics: technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16:635–644
Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8:plw055. https://doi.org/10.1093/aobpla/plw055
Giunta F, Motzo R, Deidda M (1993) Effect of drought on yield and yield components of durum wheat and triticale in a Mediterranean environment. F Crop Res 33:399–409. https://doi.org/10.1016/0378-4290(93)90161-F
Greco M, Chiappetta A, Bruno L, Bitonti MB (2012) In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J Exp Bot 63:695–709. https://doi.org/10.1093/jxb/err313
Han Y, Chen Y, Yin S et al (2015) Over-expression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. J Plant Physiol 173:62–71. https://doi.org/10.1016/j.jplph.2014.09.007
Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553. https://doi.org/10.1046/j.1365-3040.1998.00309.x
Hassan NM, El-Bastawisy ZM, El-Sayed AK et al (2015) Roles of dehydrin genes in wheat tolerance to drought stress. J Adv Res 6:179–188. https://doi.org/10.1016/j.jare.2013.11.004
Hatano T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem Pharm Bull (Tokyo) 36:2090–2097. https://doi.org/10.1248/cpb.36.2090
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. https://doi.org/10.1139/b79-163
Hu H, Dai M, Yao J et al (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992. https://doi.org/10.1073/pnas.0604882103
Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science (80-) 330:1820–1824. https://doi.org/10.1126/science.1195487
Jiang Y, Zeng B, Zhao H et al (2012) Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maizeF. J Integr Plant Biol 54:616–630. https://doi.org/10.1111/j.1744-7909.2012.01149.x
Kang Y, Khan S, Ma X (2009) Climate change impacts on crop yield, crop water productivity and food security: a review. Prog Nat Sci 19:1665–1674
Kumar MN, Jane WN, Verslues PE (2013) Role of the putative osmosensor Arabidopsis histidine kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol 161(2):942–953
Kumar S, Beena AS, Awana M, Singh A (2017) Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Front Plant Sci 8:1151. https://doi.org/10.3389/fpls.2017.01151
Larcher W (2003) Physiological plant ecology. In: Ecophysiology and stress physiology of functional groups. Springer, Berlin, Heidelberg
Lata C, Muthamilarasan M, Prasad M (2015) Drought stress responses and signal transduction in plants. Elucidation of abiotic stress signaling in plants. Springer New York, New York, pp 195–225
Lee TG, Jang CS, Kim JY et al (2007) A Myb transcription factor (TaMyb1) from wheat roots is expressed during hypoxia: roles in response to the oxygen concentration in root environment and abiotic stresses. Physiol Plant 129:375–385. https://doi.org/10.1111/j.1399-3054.2006.00828.x
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87. https://doi.org/10.1038/nature16467
Li F, Zhang L, Ji H et al (2020) The specific W-boxes of GAPC5 promoter bound by TaWRKY are involved in drought stress response in wheat. Plant Sci 26:110460
Lindemose S, O’Shea C, Jensen M et al (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878. https://doi.org/10.3390/ijms14035842
Lipiec J, Doussan C, Nosalewicz A, Kondracka K (2013) Effect of drought and heat stresses on plant growth and yield: a review. Int Agrophys 27:463–477. https://doi.org/10.2478/intag-2013-0017
Madani A, Rad AS, Pazoki A et al (2010) Wheat (Triticum aestivum L.) grain filling and dry matter partitioning responses to source: sink modifications under postanthesis water and nitrogen deficiency. Acta Sci Agron 32:145–151. https://doi.org/10.4025/actasciagron.v32i1.6273
Mahrookashani A, Siebert S, Hüging H, Ewert F (2017) Independent and combined effects of high temperature and drought stress around anthesis on wheat. J Agron Crop Sci 203:453–463. https://doi.org/10.1111/jac.12218
Mao X, Jia D, Li A et al (2011) Transgenic expression of TaMYB2A confers enhanced tolerance to multiple abiotic stresses in Arabidopsis. Funct Integr Genomics 11:445–465. https://doi.org/10.1007/s10142-011-0218-3
Mao X, Zhang H, Qian X et al (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946. https://doi.org/10.1093/jxb/err462
Matiu M, Ankerst DP, Menzel A (2017) Interactions between temperature and drought in global and regional crop yield variability during 1961–2014. PLoS ONE 12:e0178339. https://doi.org/10.1371/journal.pone.0178339
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Nezhadahmadi A, Prodhan ZH, Faruq G (2013) Drought tolerance in wheat. Sci World J 2013:12. https://doi.org/10.1155/2013/610721
Pereira S, Guimarães F, Carvalho J et al (2011) Transcription factors expressed in soybean roots under drought stress. Genet Mol Res 10:3689–3701. https://doi.org/10.4238/2011.October.21.5
Pradhan GP, Prasad PVV, Fritz AK et al (2012) Effects of drought and high temperature stress on synthetic hexaploid wheat. Funct Plant Biol 39:190. https://doi.org/10.1071/FP11245
Prasad PVV, Pisipati SR, Momčilović I, Ristic Z (2011) Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF–Tu expression in spring wheat. J Agron Crop Sci 197:430–441. https://doi.org/10.1111/j.1439-037X.2011.00477.x
Qin Y, Wang M, Tian Y et al (2012) Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol Biol Rep 39:7183–7192. https://doi.org/10.1007/s11033-012-1550-y
Ravikumar G, Manimaran P, Voleti SR et al (2014) Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice. Transgenic Res 23:421–439. https://doi.org/10.1007/s11248-013-9776-6
Reczek CR, Chandel NS (2015) ROS-dependent signal transduction. Curr Opin Cell Biol 33:8–13. https://doi.org/10.1016/j.ceb.2014.09.010
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258. https://doi.org/10.1016/J.TPLANTS.2010.02.006
Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 10:407–21
Samota MK, Sasi M, Awana M et al (2017) Elicitor-induced biochemical and molecular manifestations to improve drought tolerance in rice (Oryza sativa L.) through seed-priming. Front Plant Sci 8:934. https://doi.org/10.3389/fpls.2017.00934
Sangster TA, Queitsch C, Dolan L, Freeling M (2005) The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. This review comes from a themed issue on growth and development edited. Curr Opin Plant Biol 8:86–92. https://doi.org/10.1016/j.pbi.2004.11.012
Sharma P, Shanker Dubey R (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864. https://doi.org/10.1016/j.jplph.2004.09.011
Simova-Stoilova L, Vaseva I, Grigorova B et al (2010) Proteolytic activity and cysteine protease expression in wheat leaves under severe soil drought and recovery. Plant Physiol Biochem 48:200–206. https://doi.org/10.1016/j.plaphy.2009.11.003
Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00895
Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299:152–178. https://doi.org/10.1016/S0076-6879(99)99017-1
Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100:11777–11782. https://doi.org/10.1073/pnas.2033934100
Tang Y, Liu M, Gao S et al (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144:210–224. https://doi.org/10.1111/j.1399-3054.2011.01539.x
Tripathi P, Rabara RC, Rushton PJ (2014) A systems biology perspective on the role of WRKY transcription factors in drought responses in plants. Planta 239:255–266. https://doi.org/10.1007/s00425-013-1985-y
Valifard M, Mohsenzadeh S, Kholdebarin B, Rowshan V (2014) Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South Afr J Bot 93:92–97. https://doi.org/10.1016/J.SAJB.2014.04.002
Vishwakarma H, Junaid A, Manjhi J et al (2018) Heat stress transcripts, differential expression, and profiling of heat stress tolerant gene TaHsp90 in Indian wheat (Triticum aestivum L.) cv C306. PLoS ONE. https://doi.org/10.1371/journal.pone.0198293
Wei TM, Chang XP, Min DH, Jing RL (2010) Analysis of genetic diversity and trapping elite alleles for plant height in drought-tolerant wheat cultivars. Acta Agron Sin 36:895–904. https://doi.org/10.1016/S1875-2780(09)60053-5
Wu K-L, Guo Z-J, Wang H-H, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26. https://doi.org/10.1093/dnares/12.1.9
Xia N, Zhang G, Sun Y-F et al (2010) TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol 74:394–402. https://doi.org/10.1016/J.PMPP.2010.06.005
Xu ZS, Li ZY, Chen Y et al (2012) Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int J Mol Sci 13:15706–15723
Zhang L, Liu G, Zhao G et al (2014) Characterization of a wheat R2R3-MYB transcription factor gene, TaMYB19, involved in enhanced abiotic stresses in Arabidopsis. Plant Cell Physiol 55:1802–1812. https://doi.org/10.1093/pcp/pcu109
Zhao Y, Tian X, Wang F et al (2017) Characterization of wheat MYB genes responsive to high temperatures. BMC Plant Biol. https://doi.org/10.1186/s12870-017-1158-4
Zhu X, Liu S, Meng C et al (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol Biol Rep 31:1053–1067. https://doi.org/10.1007/s11105-013-0565-4
Acknowledgements
The authors acknowledge Director, ICAR-National Bureau of Plant Genetic Resources (ICAR-NBPGR) New Delhi, for the facilities and support provided to carry out the research work. Sincerely acknowledge the ICAR-Indian Institute of Wheat and Barley Research (ICAR-IIWBR) Karnal-Haryana, for providing wheat germplasm, and Dr. J.C.P for providing Laboratory space to carryout gene expression analysis, NIPB-New Delhi.
Author information
Authors and Affiliations
Contributions
SK, DU and NC conceived and designed the research. DU has performed all the experiments and wrote the manuscript. SK, SS, DU, AKS, RB and JK contributed in data analysis. NB and DU has contributed in bioinformatics analysis. JCP contributed in gene expression analysis. SK, JCP, SS, NB and JK contributed in manuscript proofreading. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Upadhyay, D., Budhlakoti, N., Singh, A.K. et al. Drought tolerance in Triticum aestivum L. genotypes associated with enhanced antioxidative protection and declined lipid peroxidation. 3 Biotech 10, 281 (2020). https://doi.org/10.1007/s13205-020-02264-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-020-02264-8