Abstract
Radiation mutagenesis could provide new drought-tolerant lines for selection purposes in sustainable agriculture. Drought tolerance and yield stability are closely related to co** with oxidative stress, which occurs at severe/prolonged water deprivation. In this study, the response of a newly generated winter wheat mutant line M181/1338K to severe drought stress at seedling stage (3–4th leaf) was compared to that of two established varieties—Guinness (drought tolerant) and Farmer (drought sensitive). Oxidative damage and antioxidant status analyses were performed on second leaves of control, stressed (45–46% leaf water deficit) and recovered plants. Genotypes exhibited similar pattern of stress response, comprising proline accumulation, rise in hydrogen peroxide content and oxidative damage to membrane lipids, increase in total antioxidant and antiradical activities, in phenolic and flavonoid content, in ascorbate and glutathione pools, mobilization of superoxide dismutase (SOD), catalase (CAT) and peroxidase (POX) enzyme isoforms. Farmer responded to severe water stress with the highest levels of oxidative damage to membranes, proline accumulation, and glutathione content, and slower normalization of the studied parameters upon recovery. Guinness presented a better control of oxidative membrane damage and it the highest accumulation of flavonoids under drought. The new mutant line M181/1338K had similarities with Guinness in its response to severe water stress, such as the same proline and glutathione levels. Unlike Guinness, the mutant genotype had more pronounced oxidative damage to membranes, along with higher POX activities, and tended to accumulate less flavonoids under drought, which could be regarded as secondary effects of the induced mutagenesis.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-020-03182-1/MediaObjects/11738_2020_3182_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-020-03182-1/MediaObjects/11738_2020_3182_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-020-03182-1/MediaObjects/11738_2020_3182_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-020-03182-1/MediaObjects/11738_2020_3182_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-020-03182-1/MediaObjects/11738_2020_3182_Fig5_HTML.png)
Similar content being viewed by others
Abbreviations
- AO:
-
Total antioxidant activity
- AR:
-
Antiradical activity
- ASC:
-
Ascorbic acid
- CAT:
-
Catalase
- DPPH:
-
2,2-Diphenyl-1-picrylhydrazyl
- DW:
-
Dry weight
- FRAP:
-
Ferric reducing antioxidant power assay
- FW:
-
Fresh weight
- GSSG:
-
Oxidized glutathione
- GSH:
-
Reduced glutathione
- MDA:
-
Malondialdehyde
- POX:
-
Peroxidase
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SOD:
-
Superoxide dismutase
- TW:
-
Weight at full turgidity
References
Abid M, Ali S, Qi LK, Zahoor R, Tian Z, Jiang D, Snider J, Dai T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Sci Rep 8:4615. https://doi.org/10.1038/s41598-018-21441-7
Ahloowalia BS, Maluszynski M (2001) Induced mutations–a new paradigm in plant breeding. Euphytica 118:167–173. https://doi.org/10.1023/A:1004162323428
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Anjum S, **e X, Wang L, Saleem M, Man C, Lei W (2011) Morphological, physiological andbiochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032. https://doi.org/10.5897/AJAR10.027
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Benzie I, Strain J (1999) Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol. https://doi.org/10.1016/S0076-6879(99)99005-5
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brand-Williams W, Cuvelier M, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Chakraborty U, Pradhan B (2012) Oxidative stress in five wheat varieties (Triticum aestivum L.) exposed to water stress and study of their antioxidant enzyme defense system, water stress responsive metabolites and H2O2 accumulation. Braz J Plant Physiol 24:117–130. https://doi.org/10.1590/S1677-04202012000200005
Chipilski R, Kocheva K, Nenova V, Georgiev G (2012) Physiological responses of two wheat cultivars to soil drought. Zeitschr Naturforsch Sect C Biosci 67C:181–186. https://doi.org/10.1515/znc-2012-3-410
Dalmia A, Sawhney V (2004) Antioxidant defense mechanism under drought stress in wheat seedlings. Physiol Mol Biol Plants 10:109–114
Daryanto S, Wang L, Jacinthe P (2016) Global synthesis of drought effects on maize and wheat production. PLoS ONE 11:1–15. https://doi.org/10.1371/journal.pone.0156362
Fontaine M, Steinemann A, Hayes M (2014) State droughtprograms and plans: survey of the Western United States. Nat Hazards Rev 15:95–99. https://doi.org/10.1061/(ASCE)NH.1527-6996.0000094
Foyer C, Harbinson J (1994) Oxygen metabolism and regulation of photosynthetic electron transport. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC Press, Boca Raton, pp 1–41
Fu L, Xu B, Xu X, Gan R, Zhang Y, **a E, Li H (2011) Antioxidant capacities and total phenolic contents of 62 fruits. Food Chem 129:345–350. https://doi.org/10.1016/j.foodchem.2011.04.079
Gregorová Z, Kováčik J, Klejdus B, Maglovski M, Kuna R, Hauptvogel P, Matušíková B (2015) Drought-induced responses of physiology, metabolites, and PR proteins in Triticum aestivum. J Agric Food Chem 63:8125–8133. https://doi.org/10.1021/acs.jafc.5b02951
Hameed A, Bibi N, Akhter J, Iqbal N (2011) Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Plant Physiol Biochem 49:178–185. https://doi.org/10.1016/j.plaphy.2010.11.009
Hasanuzzaman M, Mahmud J, Anee T, Islam M, Nahar K (2018) Drought stress tolerance in wheat: omics approaches in understanding and enhancing antioxidant defense. In: Zargar SM, Zargar MY (eds) Abiotic stress-mediated sensing and signaling in plants: an omics perspective. Springer Nature, Singapore, pp 267–307. https://doi.org/10.1007/978-981-10-7479-0_10
Hasanuzzaman M, Bhuyan M, Anee T, Parvin K, Nahar K, Mahmud J, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8:384. https://doi.org/10.3390/antiox8090384
Katerova Z, Miteva L (2010) Glutathione and herbicide resistance in plants. In: Chan MT, Umar S, Anjum NA (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 191–207
Kocheva K, Nenova V, Karceva T, Petrov P, Georgiev G, Landjeva S, Börner A (2014) Changes in water status, membrane stability and antioxidant capacity of wheat seedlings carrying different Rht-B1 dwarfing alleles under drought stress. J Agron Crop Sci 200:83–91. https://doi.org/10.1111/jac.12047
Kramer G, Norman H, Krizek D, Mirecki R (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochem 30:2101–2108. https://doi.org/10.1016/0031-9422(91)83595-C
Larson R (1988) The antioxidants of higher plants. Phytochemistry 27:969–978. https://doi.org/10.1016/0031-9422(88)80254-1
Lascano H, Antonicelli G, Luna C, Melchiorre M, Gómez L, Racca R, Trippi V, Casano L (2001) Antioxidant system response of different wheat cultivars under drought: field and in vitro studies. Funct Plant Biol 28:1095–1102. https://doi.org/10.1071/PP01061
Ma D, Sun D, Wang C, Li Y, Guo T (2014) Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol Biochem 80:60–66. https://doi.org/10.1016/j.plaphy.2014.03.024
Mhamdi A, Noctor G, Baker A (2012) Plant catalases: peroxisomal redox guardians. Arch Biochem Biophys 525:181–194. https://doi.org/10.1016/j.abb.2012.04.015
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Mohammadkhani N, Sharifi P (2016) Anti-oxidative response of different wheat genotypes to drought during anthesis. Iran J Plant Physiol 6:1845–1855. https://doi.org/10.22034/IJPP.2016.532655
Nemati M, Piro A, Norouzi M, Moghaddam Vahed M, Nisticò DM, Mazzuca S (2019) Comparative physiological and leaf proteomic analyses revealed the tolerant and sensitive traits to drought stress in two wheat parental lines and their F6 progenies. Environ Exp Bot 158:223–237. https://doi.org/10.1016/j.envexpbot.2018.10.024
Noctor G, Foyer C (1998) Ascorbate and glutathione: kee** active oxygen under control. Annu Rev Plant Biol 49:249–279. https://doi.org/10.1146/annurev.arplant.49.1.249
Ornstein L (1964) Enzyme bulletin. Canalco Industrial Corporation, Rockvill, Maryland, p 12
Rachovska G, Uhr Zl (2010) Inheritance of quantitative characteristics associated with productivity of F1 hybrids winter common wheat. Field Crops Stud 6:361–367
Scandalios J (1993) Oxygen stress and superoxide dismutase. Plant Physiol 101:7–12. https://doi.org/10.1104/pp.101.1.7
Scandalios J (1994) Regulation and properties of plant catalases. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, Florida, pp 275–315
Sen A, Ozturk I, Yaycili O, Alikamanoglu S (2017) Drought tolerance in irradiated wheat mutants studied by genetic and biochemical markers. J Plant Growth Regul 36:669–679. https://doi.org/10.1007/s00344-017-9668-8
Shah Z, Rehman H, Akhtar T, Daur I, Nawaz M, Ahmad M, Rana I, Atif R, Yang S, Chung G (2017) Redox and ionic homeostasis regulations against oxidative, salinity and drought stress in wheat. Front Genet 8:141. https://doi.org/10.3389/fgene.2017.00141
Simova-Stoilova L, Demirevska K, Petrova T, Tsenov N, Feller U (2008) Antioxidative protection in wheat varieties under severe recoverable drought at seedling stage. Plant Soil Environ 54:529–536
Simova-Stoilova L, Demirevska K, Petrova T, Tsenov N, Feller U (2009) Antioxidative protection and proteolytic activity in tolerant and sensitive wheat (Triticum aestivum L.) varieties subjected to long-term field drought. Plant growth Regul 58:107–117. https://doi.org/10.1007/s10725-008-9356-6
Singh S, Gupta A, Kaur N (2012) Differential Responses of antioxidative defence system to long-term field drought in wheat (Triticum aestivum L.) genotypes differing in drought tolerance. J Agron Crop Sci 198:185–195. https://doi.org/10.1111/j.1439-037X.2011.00497.x
Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. Philos Trans R Soc Lond B Biol Sci 355:1455–1464. https://doi.org/10.1098/rstb.2000.0706
Spiridon I, Bodirlau R, Teaca C (2011) Total phenolic content and antioxidant activity of plants used in traditional Romanian herbal medicine. Cent Eur J Biol 6:388–396. https://doi.org/10.2478/s11535-011-0028-6
Swain T, Goldstein JL (1964) The quantitative analyses of phenolic compounds. In: Pridham JB (ed) Methods in polyphenol chemistry. Pergamon Press, Oxford, pp 131–146
Tyagi S, Sharma S, Taneja M, Shumayla KR, Sembi J, Upadhyay S (2017) Superoxide dismutases in bread wheat (Triticum aestivum L.): comprehensive characterization and expression analysis during development and biotic and abiotic stresses. Agri Gene 6:1–13. https://doi.org/10.1016/j.aggene.2017.08.003
Varela M, Arslan I, Reginato M, Cenzano A, Luna M (2016) Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina). Plant Physiol Biochem 104:81–91. https://doi.org/10.1016/j.plaphy.2016.03.014
Vassileva V, Vaseva I, Dimitrova A (2019) Expression profiling of DNA methyltransferase genes in wheat genotypes with contrasting drought tolerance. Bulg J Agric Sci 25(5):845–851
Verbrugge N, Hermans C (2008) Proline accumulation in plants. Amino Acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6
Woodbury W, Spencer A, Stahmann M (1971) An improved procedure using ferricyanide for detecting catalase isoenzymes. Anal Biochem 44:301–305. https://doi.org/10.1016/0003-2697(71)90375-7
Zaharieva T, Abadía J (2003) Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221:269–275. https://doi.org/10.1007/s00709-002-0051-6
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559. https://doi.org/10.1016/S0308-8146(98)00102-2
Acknowledgements
This work was supported in part by project BUL 5014, IAEA—Vienna, and by project BG05M2OP001-2.002-0001 (D.P.) of the Ministry of Science and Education, Bulgaria. The authors are grateful to their colleague assoc. prof. Irina Vaseva, who helped for substantial improvement of the English expression.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Kuzniak-Gebarowska.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kirova, E., Pecheva, D. & Simova-Stoilova, L. Drought response in winter wheat: protection from oxidative stress and mutagenesis effect. Acta Physiol Plant 43, 8 (2021). https://doi.org/10.1007/s11738-020-03182-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-020-03182-1