Ukr.Biochem.J. 2025; Volume 97, Issue 3, May-Jun, pp. 13-41
doi: https://doi.org/10.15407/ubj97.03.013
Stress metabolites in wheat: role in adaptation to drought
Yu. E. Kolupaev1,2*, L. I. Relina1, A. I. Oboznyi1, N. I. Ryabchun1,
N. I. Vasko1, V. P. Kolomatska1, O. Yu. Leonov1
1Yuriev Plant Production Institute, National Academy
of Agrarian Sciences of Ukraine, Kharkiv;
2Poltava State Agrarian University, Poltava, Ukraine;
*e-mail: plant_biology@ukr.net
Received: 25 April 2025; Revised: 21 May 2025;
Accepted: 11 June 2025; Available on-line: 07 July 2025
Drought is one of the main factors limiting agricultural production and leading to crop losses. Wheat, being a source of food for over half of the world’s population, is a plant species that is very susceptible to drought. In this regard, research into the species-specific stress metabolites and physiological and biochemical mechanisms of drought tolerance is of particular practical interest. This review comprehensively examines the roles of soluble carbohydrates, proline, polyamines, and GABA, as well as their functional interplay, in adaptation of wheat and other plant species to drought.
Keywords: antioxidants, cellular signaling, drought, gamma-aminobutyric acid, osmoprotectors, polyamines, proline, soluble carbohydrates, stress metabolites, Triticum aestivum
References:
- Razzaq A, Wani SH, Saleem F, Yu M, Zhou M, Shabala S. Rewilding crops for climate resilience: economic analysis and de novo domestication strategies. J Exp Bot. 2021;72(18):6123-6139. PubMed, CrossRef
- IWG Drought. 2020. Regime of access: https://www.unccd.int/sites/default/files/2020-03/IWGDrought-Factsheets_EN-final.pdf.
- Palmgren M, Shabala S. Adapting crops for climate change: regaining lost abiotic stress tolerance in crops. Front Sci. 2024;2:1416023. CrossRef
- Gupta A, Rico-Medina A, Caño-Delgado AI. The physiology of plant responses to drought. Science. 2020;368(6488):266-269. PubMed, CrossRef
- Dietz KJ, Zörb C, Geilfus CM. Drought and crop yield. Plant Biol (Stuttg). 2021;23(6):881-893. PubMed, CrossRef
- Diego N, Spíchal L. Use of plant metabolites to mitigate stress effects in crops. In: Geelen D, Xu L. (eds.). The Chemical Biology of Plant Biostimulants. John Wiley & Sons Ltd, 2020. P. 261-300. CrossRef
- Kirizyi D, Kedruk A, Stasik O. Effects of drought, high temperature and their combinations on the photosynthetic apparatus and plant productivity. In: Yastreb TO, Kolupaev YE, Yemets AI, Blume YB (eds.). Regulation of Adaptive Responses in Plants. New York: Nova Science Publishers, Inc., 2024. P. 1-32.
- Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Handa N, Kapoor D, Bhardwaj R, Zheng B. Phytohormones Regulate Accumulation of Osmolytes Under Abiotic Stress. Biomolecules. 2019;9(7):285. PubMed, PubMed, CrossRef
- Manna M, Thakur T, Chirom O, Mandlik R, Deshmukh R, Salvi P. Transcription factors as key molecular target to strengthen the drought stress tolerance in plants. Physiol Plant. 2021;172(2):847-868. PubMed, CrossRef
- Singh J, Garai S, Das S, Thakur JK, Tripathy BC. Role of C4 photosynthetic enzyme isoforms in C3 plants and their potential applications in improving agronomic traits in crops. Photosynth Res. 2022;154(3):233-258. PubMed, CrossRef
- Kosová K, Vítámvás P, Prášil IT. Wheat and barley dehydrins under cold, drought, and salinity – what can LEA-II proteins tell us about plant stress response? Front Plant Sci. 2014;5:343. PubMed, PubMed, CrossRef
- Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ. The Role of the plant antioxidant system in drought tolerance. Antioxidants (Basel). 2019;8(4):94. PubMed, PubMed, CrossRef
- Smith MA, Graether SP. The Disordered Dehydrin and Its Role in Plant Protection: A Biochemical Perspective. Biomolecules. 2022;12(2):294. PubMed, PubMed, CrossRef
- Kolupaev YuE, Yastreb TO, Ryabchun NI, Kokorev AI, Kolomatska VP, Dmitriev AP. Redox homeostasis of cereals during acclimation to drought. Theor Exp Plant Physiol. 2023;35(2): 133-168. CrossRef
- Singh M, Kumar J, Singh S, Singh VP, Prasad SM. Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol. 2015;14:407-426. CrossRef
- Sun Z, Li S, Chen W, Zhang J, Zhang L, Sun W, Wang Z. Plant Dehydrins: Expression, Regulatory Networks, and Protective Roles in Plants Challenged by Abiotic Stress. Int J Mol Sci. 2021;22(23):12619. PubMed, PubMed, CrossRef
- Riyazuddin R, Nisha N, Singh K, Verma R, Gupta R. Involvement of dehydrin proteins in mitigating the negative effects of drought stress in plants. Plant Cell Rep. 2022;41(3):519-533. PubMed, CrossRef
- Szlachtowska Z, Rurek M. Plant dehydrins and dehydrin-like proteins: characterization and participation in abiotic stress response. Front Plant Sci. 2023;14:1213188. PubMed, PubMed, CrossRef
- Norouzi M, Toorchi M, Hosseina Salekdeh Gh, Mohammadi SA, Neyshabouri MR, Aharizad S. Effect of water deficit on growth, grain yield and osmotic adjustment in rapeseed. J Food Agricult Environ. 2008;6(2):312-318.
- Blum A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ. 2017;40(1):4-10. PubMed, CrossRef
- Mahmood T, Abdullah M, Ahmar S, Yasir M, Iqbal MS, Yasir M, Ur Rehman S, Ahmed S, Rana RM, Ghafoor A, Nawaz Shah MK, Du X, Mora-Poblete F. Incredible Role of Osmotic Adjustment in Grain Yield Sustainability under Water Scarcity Conditions in Wheat (Triticum aestivum L.). Plants (Basel). 2020;9(9):1208. PubMed, PubMed, CrossRef
- Wahab A, Abdi G, Saleem MH, Ali B, Ullah S, Shah W, Mumtaz S, Yasin G, Muresan CC, Marc RA. Plants’ Physio-Biochemical and Phyto-Hormonal Responses to Alleviate the Adverse Effects of Drought Stress: A Comprehensive Review. Plants (Basel). 2022;11(13):1620. PubMed, PubMed, CrossRef
- Gupta N, Thind SK. Foliar application of glycine betaine alters sugar metabolism of wheat leaves under prolonged field drought stress. Proc Natl Acad Sci, India, Sect. B Biol Sci. 2019; 89:877-884. CrossRef
- Akula R, Mukherjee S. New insights on neurotransmitters signaling mechanisms in plants. Plant Signal Behav. 2020;15(6):1737450. PubMed, PubMed, CrossRef
- Suhel M, Husain T, Pandey A, Singh S, Dubey NK, Prasad SM, Singh VP. An appraisal of ancient molecule GABA in abiotic stress tolerance in plants, and its crosstalk with other signaling molecules. J Plant Growth Regul. 2023;42:614-629. CrossRef
- Jurkonienė S, Mockevičiūtė R, Gavelienė V, Šveikauskas V, Zareyan M, Jankovska-Bortkevič E, Jankauskienė J, Žalnierius T, Kozeko L. Proline Enhances Resistance and Recovery of Oilseed Rape after a Simulated Prolonged Drought. Plants (Basel). 2023;12(14):2718. PubMed, PubMed, CrossRef
- Guo X, Xin Z, Yang T, Ma X, Zhang Y, Wang Z, Ren Y, Lin T. Metabolomics Response for Drought Stress Tolerance in Chinese Wheat Genotypes (Triticum aestivum). Plants (Basel). 2020;9(4):520. PubMed, PubMed, CrossRef
- Raza A, Anas M, Bhardwaj S, Mir RA, Charagh S, Elahi M, Zhang X, Mir RR, Weckwerth W, Fernie AR, Siddique KHM, Hu Z, Varshney RK. Harnessing metabolomics for enhanced crop drought tolerance. Crop J. 2025;13(2):311-327. CrossRef
- Hasanuzzaman M, Mahmud JA, Anee TI, Nahar K, Islam MT. Drought stress tolerance in wheat: Omics approaches in understanding and enhancing antioxidant defense. In: Zargar S, Zargar M. (eds.). Abiotic Stress-Mediated Sensing and Signaling in Plants: An Omics Perspective. Springer, Singapore, 2018. P. 267-307. CrossRef
- Munaweera TIK, Jayawardana NU, Rajaratnam R, Dissanayake N. Modern plant biotechnology as a strategy in addressing climate change and attaining food security. Agric Food Secur. 2022;11:26. CrossRef
- Asseng S, Milroy S, Bassu S., Saab MT. Wheat. In: Steduto P, Hsiao TC, Fereres E, Raes D. (eds.). Crop yield response to water. Rome: Food and Agriculture Organization of the United Nations, 2012. P. 92-100.
- Khan N, Ali S, Zandi P, Mehmood A, Ullah S, Ismail MI, Shahid MA, Babar MA. Role of sugars, amino acids and organic acids in improving plant abiotic stress tolerance. Pak J Bot. 2020;52(2):355-363. CrossRef
- Kaur H, Manna M, Thakur T, Gautam V, Salvi P. Imperative role of sugar signaling and transport during drought stress responses in plants. Physiol Plant. 2021;171(4):833-848. PubMed, CrossRef
- Bilyavska NO, Fediuk OM, Zolotareva EK. Chloroplasts of cold-tolerant plants. Plant Sci Today. 2019;6(4):407-411. CrossRef
- Dutta T, Neelapu NR, Wani SH, Surekha C. Role and Regulation of Osmolytes as Signaling Molecules to Abiotic Stress Tolerance. In: Khan MIR, Ferrante A, Reddy PS, Khan NA. Plant Signaling Molecules. Role and Regulation Under Stressful Environments. Elsevier Inc., 2019. P. 459-477. CrossRef
- Salam U, Ullah S, Tang ZH, Elateeq AA, Khan Y, Khan J, Khan A, Ali S. Plant metabolomics: an overview of the role of primary and secondary metabolites against different environmental stress factors. Life (Basel). 2023;13(3):706. PubMed, PubMed, CrossRef
- Gurrieri L, Merico M, Trost P, Forlani G, Sparla F. Impact of drought on soluble sugars and free proline content in selected Arabidopsis mutants. Biology (Basel). 2020;29;9(11):367. PubMed, PubMed, CrossRef
- Caffrey M, Fonseca V, Leopold AC. Lipid-sugar interactions : relevance to anhydrous biology. Plant Physiol. 1988;86(3):754-758. PubMed, PubMed, CrossRef
- Strauss G, Hauser H. Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc Natl Acad Sci USA. 1986;83(8):2422-2426. PubMed, PubMed, CrossRef
- Van den Ende W, El-Esawe SK. Sucrose signaling pathways leading to fructan and anthocyanin accumulation: a dual function in abiotic and biotic stress responses? Environ Exp Botany. 2014;108:4-13. CrossRef
- Coello P, Hey SJ, Halford NG. The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J Exp Bot. 2011;62(3):883-893. PubMed, CrossRef
- Kolupaev YE, Yastreb TO, Dmitriev AP. Gasotransmitters as key members of the signaling network regulating stomatal response: interaction with other molecules. Phyton-Int J Exp Bot. 2024;93(12):3151-3195. CrossRef
- Morelli R, Russo-Volpe S, Bruno N, Lo Scalzo R. Fenton-dependent damage to carbohydrates: free radical scavenging activity of some simple sugars. J Agric Food Chem. 2003;51(25):7418-7425. PubMed, CrossRef
- Ende WV, Peshev D. Sugars as antioxidants in plants. In: Tuteja N, Gill S (eds.). Crop Improvement Under Adverse Conditions. Springer, New York, 2013. P. 285-307. CrossRef
- Gangola MP, Ramadoss BR. Sugars play a critical role in abiotic stress tolerance in plants. In: Wani SH. (ed.). Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance Plants. Academic Press, 2018. P. 17-38. CrossRef
- Hu M, Shi Z, Zhang Z, Zhang Y, Li H. Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regul. 2012;68:177-188. CrossRef
- Sami F, Yusuf M, Faizan M, Faraz A, Hayat S. Role of sugars under abiotic stress. Plant Physiol Biochem. 2016;109:54-61. PubMed, CrossRef
- Kosar F, Akram NA, Sadiq M, Al-Qurainy F, Ashraf M. Trehalose: A key organic osmolyte effectively involved in plant abiotic stress tolerance. J Plant Growth Regul. 2019;38:606-618. CrossRef
- Teramoto N, Sachinvala ND, Shibata M. Trehalose and trehalose-based polymers for environmentally benign, biocompatible and bioactive materials. Molecules. 2008;13(8):1773-1816. PubMed, PubMed, CrossRef
- Rasheed Y, Khalid F, Ashraf H, Asif K, Maqsood MF, Naz N, Shahbaz M, Zulfiqar U, Ali Q, Rana S. Enhancing plant stress resilience with osmolytes and nanoparticles. J Soil Sci Plant Nutr. 2024;24:1871-1906. CrossRef
- Luo Y, Li WM, Wang W. Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot. 2008;63(1-3):378-384. CrossRef
- John R, Raja V, Ahmad M, Jan N, Majeed U, Ahmad S, Yaqoob U, Kaul T. Trehalose: metabolism and role in stress signalling in plants. In: Sarwat M, Ahmad A, Abdin M, Ibrahim M. (eds.). Stress Signaling in Plants: Genomics and Proteomics Perspective. Springer, Cham., 2017. Vol. 2. P. 261-275. CrossRef
- Yeo ET, Kwon HB, Han SE, Lee JT, Ryu JC, Byu MO. Genetic engineering of drought resistant potato plants by introduction of the trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells. 2000;10(3):263-268. PubMed, CrossRef
- Cortina C, Culiáñez-Macià FA. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 2005;169(1):75-82. CrossRef
- Sah SK, Kaur G, Wani SH. Metabolic engineering of compatible solute trehalose for abiotic stress tolerance in plants. In: Iqbal N, Nazar R, Khan NA. Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. Springer, New Delhi. 2016. P. 83–96. CrossRef
- Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA. 2002;99(25):15898-15903. PubMed, PubMed, CrossRef
- Yan S, Liu Q, Li W, Yan J, Fernie AR. Raffinose family oligosaccharides: crucial regulators of plant development stress responses. Crit Rev Plant Sci. 2022;41(4):286-303. CrossRef
- Cacela C, Hincha DK. Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes. Biophys J. 2006;90(8):2831-2842. PubMed, PubMed, CrossRef
- Knaupp M, Mishra KB, Nedbal L, Heyer AG. Evidence for a role of raffinose in stabilizing photosystem II during freeze-thaw cycles. Planta. 2011;234(3):477-486. PubMed, CrossRef
- Liu Y, Li T, Zhang C, Zhang W, Deng N, Dirk LMA, Downie AB, Zhao T. Raffinose positively regulates maize drought tolerance by reducing leaf transpiration. Plant J. 2023;114(1):55-67. PubMed, CrossRef
- Vinson CC, Mota APZ, Porto BN, Oliveira TN, Sampaio I, Lacerda AL, Danchin EGJ, Guimaraes PM, Williams TCR, Brasileiro ACM. Characterization of raffinose metabolism genes uncovers a wild Arachis galactinol synthase conferring tolerance to abiotic stresses. Sci Rep. 2020;10(1):15258. PubMed, PubMed, CrossRef
- Szablińska-Piernik J, Lahuta LB. Polar Metabolites Profiling of Wheat Shoots (Triticum aestivum L.) under Repeated Short-Term Soil Drought and Rewatering. Int J Mol Sci. 2023;24(9):8429. PubMed, PubMed, CrossRef
- Xue GP, McIntyre CL, Glassop D, Shorter R. Use of expression analysis to dissect alterations in carbohydrate metabolism in wheat leaves during drought stress. Plant Mol Biol. 2008;67(3):197-214. PubMed, CrossRef
- Seki M, Umezawa T, Urano K, Shinozaki K. Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol. 2007;10(3):296-302. PubMed, CrossRef
- Bazargani MM, Hajirezaei MR, Salekdeh GH, Bushehri AAS, Falahati-Anbaran M, Moradi F, Naghavi MR, Ehdaie B. A view on the role of metabolites in enhanced stem reserves remobilization in wheat under drought during grain filling. Austr J Crop Sci. 2012;6(12):1613-1623.
- Bagherikia S, Pahlevani M, Yamchi A, Zaynalinezhad K, Mostafaie A. Transcript profiling of genes encoding fructan and sucrose metabolism in wheat under terminal drought stress. J Plant Growth Regul. 2019;38:148-163. CrossRef
- Faisal S, Mujtaba SM, Asma, Mahboob W. Polyethylene glycol mediated osmotic stress impacts on growth and biochemical aspects of wheat (Triticum aestivum L.). J Crop Sci Biotechnol. 2019;22:213-223. CrossRef
- Marcińska I, Czyczyło-Mysza I, Skrzypek E, Filek M, Grzesiak S, Grzesiak MT, Janowiak F, Hura T, Dziurka M, Dziurka K, Nowakowska A, Quarrie SA. Impact of osmotic stress on physiological and biochemical characteristics in drought-susceptible and drought-resistant wheat genotypes. Acta Physiol Plant. 2013;35(2):451-461. CrossRef
- Kaur K, Gupta AK, Kaur N. Effect of water deficit on carbohydrate status and enzymes of carbohydrate metabolism in seedlings of wheat cultivars. Indian J Biochem Biophys. 2007;44(4):223-230. PubMed
- Ghaffar A, Hussain N, Ajaj R, Shahin SM, Bano H, Javed M, Khalid A, Yasmin M, Shah KH, Zaheer M, Iqbal M, Zafar ZU, Athar HU. Photosynthetic activity and metabolic profiling of bread wheat cultivars contrasting in drought tolerance. Front Plant Sci. 2023;14:1123080. PubMed, PubMed, CrossRef
- Guo R, Shi L, Jiao Y, Li M, Zhong X, Gu F, Liu Q, Xia X, Li H. Metabolic responses to drought stress in the tissues of drought-tolerant and drought-sensitive wheat genotype seedlings. AoB Plants. 2018;10(2):ply016. PubMed, PubMed, CrossRef
- Kolupaev YuE, Yastreb TO, Salii AM, Kokorev AI, Ryabchun NI, Zmiievska OA, Shkliarevskyi MA. State of antioxidant and osmoprotective systems in etiolated winter wheat seedlings of different cultivars due to their drought tolerance. Zemdirbyste-Agriculture. 2022;109(4):313-322. CrossRef
- Kolupaev YuE, Ryabchun NI, Leonov OYu, Kokorev AI, Taraban DA, Shakhov IV, Shkliarevskyi MA, Yastreb TO. Functioning of the antioxidant and osmoprotective systems of Triticum aestivum cultivars growing under soil drought conditions. Botanica. 2024;30(3):102-116. CrossRef
- Alvarez ME, Savouré A, Szabados L. Proline metabolism as regulatory hub. Trends Plant Sci. 2022;27(1):39-55. PubMed, CrossRef
- Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010;15(2):89-97. PubMed, CrossRef
- Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN. Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev Camb Philos Soc. 2015;90(4):1065-1099. PubMed, CrossRef
- Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan MAR. Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biol (Stuttg). 2022;24(2):227-239. PubMed, CrossRef
- Funck D, Stadelhofer B, Koch W. Ornithine-delta-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biol. 2008;8:40. PubMed, PubMed, CrossRef
- Meena M, Divyanshu K, Kumar S, Swapnil P, Zehra A, Shukla V, Yadav M, Upadhyay RS. Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon. 2019;5(12):e02952. PubMed, PubMed, CrossRef
- El Moukhtari A, Cabassa-Hourton C, Farissi M, Savouré A. How does proline treatment promote salt stress tolerance during crop plant development? Front Plant Sci. 2020;11:1127. PubMed, PubMed, CrossRef
- Forlani G, Trovato M, Funck D, Signorelli S. Regulation of proline accumulation and its molecular and physiological functions in stress defence. In: Hossain MA, Kumar V, Burritt DJ, Fujita M, Mäkelä PSA. (eds.). Osmoprotectant-mediated abiotic stress tolerance in plants: recent advances and future perspectives. Switzerland AG Cham, Springer Nature, 2019. P. 73-97. CrossRef
- Liang X, Zhang L, Natarajan SK, Becker DF. Proline mechanisms of stress survival. Antioxid Redox Signal. 2013;19(9):998-1011. PubMed, PubMed, CrossRef
- Kaur G, Asthir B. Proline: a key player in plant abiotic stress tolerance. Biol Plant. 2015;59:609-619. CrossRef
- Natarajan SK, Zhu W, Liang X, Zhang L, Demers AJ, Zimmerman MC, Simpson MA, Becker DF. Proline dehydrogenase is essential for proline protection against hydrogen peroxide-induced cell death. Free Radic Biol Med. 2012;53(5):1181-1191. PubMed, PubMed, CrossRef
- Signorelli S, Coitiño EL, Borsani O, Monza J. Molecular mechanisms for the reaction between (˙)OH radicals and proline: insights on the role as reactive oxygen species scavenger in plant stress. J Phys Chem B. 2014;118(1):37-47. PubMed, CrossRef
- Signorelli S, Dans PD, Coitiño EL, Borsani O, Monza J. Connecting proline and γ-aminobutyric acid in stressed plants through non-enzymatic reactions. PLoS One. 2015;10(3):e0115349. PubMed, PubMed, CrossRef
- Mansour MMF, Salama KHA. Proline and abiotic stresses: Responses and adaptation. In: Hasanuzzaman M. (ed.). Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives II. Springer, Singapore, 2020. P. 357-397. CrossRef
- de Carvalho K, de Campos MK, Domingues DS, Pereira LF, Vieira LG. The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol Biol Rep. 2013;40(4):3269-3279. PubMed, CrossRef
- Dubrovna OV, Stasik OO, Priadkina GO, Zborivska OV, Sokolovska-Sergiienko OG. Resistance of genetically modified wheat plants, containing a doublestranded RNA suppressor of the proline dehydrogenase gene, to soil moisture deficiency. Agricult Sci Pract. 2020;7(2):24-34. CrossRef
- Dubrovna OV, Priadkina GO, Mykhalska SI, Komisarenko AG. Drought-tolerance of transgenic winter wheat with partial suppression of the proline dehydrogenase gene. Regul Mech Biosyst. 2022;13(4):385-392. CrossRef
- Bekka S, Abrous-Belbachir O, Djebbar R. Effects of exogenous proline on the physiological characteristics of Triticum aestivum L. and Lens culinaris Medik. under drought stress. Acta Agricult Slovenica. 2018;111(2):477-491. CrossRef
- Kolupaev YE, Yastreb TO, Ryabchun NI, Kuzmyshyna NV, Shkliarevskyi MA, Barabolia O, Pysarenko VM. Response of Triticum aestivum seedlings of different ecological and geographical origin to heat and drought: relationship with resistance to oxidative stress and osmolyte accumulation. Agricult Forest. 2023;69(2):83-99. CrossRef
- Yastreb TO, Kokorev AI, Makaova BE, Ryabchun NI, Sakhno TV, Dmitriev AP, Kolupaev YuE. Response of the antioxidant system of wheat seedlings with different genotypes to exogenous prooxidants: the relationship with resistance to abiotic stressors. Ukr Biochem J. 2023;95(6):81-96. CrossRef
- Vayner AO, Kolupaev YuE, Yastreb TO. Participation of hydrogen peroxide in induction of proline accumulation in millet plants under action of NaCl. Bull Kharkiv Natl Agrar Univ. Ser Biology. 2013;2(29): 32-38.
- Ben Rejeb K, Lefebvre-De Vos D, Le Disquet I, Leprince AS, Bordenave M, Maldiney R, Jdey A, Abdelly C, Savouré A. Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol. 2015;208(4):1138-1148. PubMed, CrossRef
- Signorelli S, Tarkowski ŁP, O’leary B, Tabares-da Rosa S, Borsani O, Monza J. GABA and Proline Metabolism in Response to Stress. In: Gupta DK, Corpas FJ. (eds.). Hormones and Plant Response, vol. 2. Springer International Publishing, 2021. P. 291-314. CrossRef
- Rajendrakumar CS, Reddy BV, Reddy AR. Proline-protein interactions: protection of structural and functional integrity of M4 lactate dehydrogenase. Biochem Biophys Res Commun. 1994;201(2):957-963. PubMed, CrossRef
- Sharma P, Dubey RS. Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol. 2005;162(8):854-864. PubMed, CrossRef
- Mishra S, Dubey RS. Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol. 2006;163(9):927-936. PubMed, CrossRef
- Valifard M, Moradshahi A, Kholdebarin B. Biochemical and physiological responses of two wheat (Triticum aestivum L.) cultivars to drought stress applied at seedling stage. J Agr Sci Tech. 2012;14:1567-1578.
- Selim DAH, Nassar RMA, Boghdady MS, Bonfill M. Physiological and anatomical studies of two wheat cultivars irrigated with magnetic water under drought stress conditions. Plant Physiol Biochem. 2019;135:480-488. PubMed, CrossRef
- Wang J, Zhang X, Han Z, Feng H, Wang Y, Kang J, Han X, Wang L, Wang C, Li H, Ma G. Analysis of physiological indicators associated with drought tolerance in wheat under drought and re-watering conditions. Antioxidants (Basel). 2022;11(11):2266. PubMed, PubMed, CrossRef
- Romanenko KO, Babenko LM, Smirnov OE, Kosakivska IV. Impact of moderate soil drought on the dynamics and distribution of low molecular weight protectors in Triticum aestivum and Triticum spelta. J Crop Health. 2025;77:32. CrossRef
- Muhammad H, Chachar NA, Chachar Q, Sheikh Muhammad M, Chachar S, Chachar Z. Physiological characterization of six wheat genotypes for drought tolerance. Int J Res – Granthaalayah. 2016;4(2):184-196. CrossRef
- Hassan N, Ebeed H, Aljaarany A. Exogenous application of spermine and putrescine mitigate adversities of drought stress in wheat by protecting membranes and chloroplast ultra-structure. Physiol Mol Biol Plants. 2020;26(2):233-245. PubMed, PubMed, CrossRef
- Sharma V, Kumar A, Chaudhary A, Mishra A, Rawat S, B. BY, Shami V, Kaushik P. Response of wheat genotypes to drought stress stimulated by PEG. Stresses. 2022;2(1):26-51. CrossRef
- Kang Z, Babar MA, Khan N, Guo J, Khan J, Islam S, Shrestha S, Shahi D. Comparative metabolomic profiling in the roots and leaves in contrasting genotypes reveals complex mechanisms involved in post-anthesis drought tolerance in wheat. PLoS One. 2019;14(3):e0213502. PubMed, PubMed, CrossRef
- Saeedipour S, Moradi F. Stress-induced changes in the free amino acid composition of two wheat cultivars with difference in drought resistance. Afr J Biotechnol. 2012;11(40):9559-9565. CrossRef
- Wang X, Mao Z, Zhang J, Hemat M, Huang M, Cai J, Zhou Q, Dai T, Jiang, D. Osmolyte accumulation plays important roles in the drought priming induced tolerance to post-anthesis drought stress in winter wheat (Triticum aestivum L.). Environ Exp Bot. 2019;166:103804. CrossRef
- Griffiths CA, Reynolds MP, Paul MJ. Combining yield potential and drought resilience in a spring wheat diversity panel. Food Energy Secur. 2020;9(4):e241. PubMed, PubMed, CrossRef
- Tuteja N, Sopory SK. Chemical signaling under abiotic stress environment in plants. Plant Signal Behav. 2008;3(8):525-536. PubMed, PubMed, CrossRef
- Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. ROS signaling: the new wave? Trends Plant Sci. 2011;16(6):300-309. PubMed, CrossRef
- Singh P, Basu S, Kumar G. Polyamines metabolism: A way ahead for abiotic stress tolerance in crop plants. In: Wani SH. (ed.). Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants. Academic Press, 2018. P. 39-55. CrossRef
- Pál M, Szalai G, Janda T. Speculation: Polyamines are important in abiotic stress signaling. Plant Sci. 2015;237:16-23. PubMed, PubMed, CrossRef
- Liu Y, Liang H, Lv X, Liu D, Wen X, Liao Y. Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol Biochem. 2016;100:113-129. PubMed, CrossRef
- Chen D, Shao Q, Yin L, Younis A, Zheng B. Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci. 2019;9:1945. PubMed, PubMed, CrossRef
- Kolupaev YuE, Kokorev AI, Dmitriev AP. Polyamines: involvement in cellular signaling and plant adaptation to the effect of abiotic stressors. Cytol Genet. 2022;56(2):148-163. CrossRef
- Minocha R, Majumdar R, Minocha SC. Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci. 2014;5:175. PubMed, PubMed, CrossRef
- Wen X, Moriguchi T. Role of polyamines in stress response in horticultural crops. In: Kanayama Y, Kochetov A. (eds.). Abiotic Stress Biology in Horticultural Plants. Springer, Tokyo, 2015. P. 35-45. CrossRef
- Abbasi NA, Ali I, Hafiz IA, Khan AS. Application of polyamines in horticulture: A review. Int J Biosci. 2017;10(5):319-342. CrossRef
