Proline is considered one of the most important osmolytes accumulated by plants in response to stress factors that cause cell dehydration. A significant body of data has been accumulated on changes in the proline content of cultivated plants of different genotypes under osmotic stress. This fully applies to one of the most important cultivated cereals — durum wheat (Triticum aestivum). However, these data lack objective evaluation and systematization. The aim of this study was to conduct a meta-analysis of data on changes in proline content in wheat plants of various genotypes at early phases of development under drought. Only experimental data obtained under controlled growth conditions were selected for processing. Another key criterion for selecting studies for inclusion in the meta-analysis was the availability of objective data on the level of drought tolerance of the studied genotypes. As a result, the ratios of the mean proline content in plants under stress conditions to the mean content in control conditions — ln(R/R) — were determined based on 112 studies presented in 21 journal articles. It was concluded that the proline content in the vegetative organs of T. aestivum under drought increases significantly. At the same time, there was no significant difference in the degree of increase of this indicator in drought-resistant and sensitive genotypes. In other words, the increase in proline content in wheat is a universal response to osmotic stress. The study also separately discusses the interpretation of data related to the enhanced drought tolerance of transformants with modified proline synthesis or catabolism.

Supplementary Material. Supplementary Material (Table S1) is available on this website: ukrbotj82-04-277-S1.pdf (50 KB)

Keywords: drought, meta-analysis, proline, resistance, Triticum aestivum

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1. Alia, Saradhi P.P., Mohanty P. 1997. Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. Journal of Photochemistry and Photobiology, 38: 253–257. https://doi.org/10.1016/S1011-1344(96)07470-2
2. Alvarez M.E., Savouré A., Szabados L. 2022. Proline metabolism as regulatory hub. Trends in Plant Science, 27(1): 39–55. https://doi.org/10.1016/j.tplants.2021.07.009
3. Amoah J.N., Ko C.S., Yoon J.S., Weon S.Y. 2019. Effect of drought acclimation on oxidative stress and transcript expression in wheat (Triticum aestivum L.). Journal of Plant Interactions, 14(1): 492–505. https://doi.org/10.1080/17429145.2019.1662098
4. Ben Rejeb K., Lefebvre-De Vos D., Le Disquet I., Leprince A.S., Bordenave M., Maldiney R., Jdey A., Abdelly C., Savouré A. 2015. Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. The New Phytologist, 208(4): 1138–1148. https://doi.org/10.1111/nph.13550
5. Burda B.U., O'Connor E.A., Webber E.M., Redmond N., Perdue L.A. 2017. Estimating data from figures with a Web-based program: Considerations for a systematic review. Research Synthesis Methods, 8: 258–262. https://doi.org/10.1002/jrsm.1232
6. Chakraborty U., Pradhan B. 2012. Drought stress-induced oxidative stress and antioxidative responses in four wheat (Triticum aestivum L.) varieties. Archives of Agronomy and Soil Science, 58(6): 617–630. https://doi.org/10.1080/03650340.2010.533660
7. Cha-Um S., Rai V., Takabe T. 2019. Proline, glycinebetaine, and trehalose uptake and inter-organ transport in plants under stress. In: Osmoprotectant-mediated abiotic stress tolerance in plants: Recent advances and future perspectives. Eds M.A. Hossain, V. Kumar, D.J Burritt., M. Fujita, P.S.A. Mäkelä. Switzerland AG Cham: Springer Nature, pp. 201–223. https://doi.org/10.1007/978-3-030-27423-8_9
8. Cheng L., Wang Y., He Q., Li H., Zhang X., Zhang F. 2016. Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration. BMC Plant Biology, 16(1): 188. https://doi.org/10.1186/s12870-016-0871-8
9. Dbira S., Al Hassan M., Gramazio P., Ferchichi A., Vicente O., Prohens J., Boscaiu M. 2018. Variable levels of tolerance to water stress (drought) and associated biochemical markers in Tunisian barley landraces. Molecules, 23: 613. https://doi.org/10.3390/molecules23030613
10. De Carvalho K., de Campos M.K.F., Domingues D.S., Pereira L.F.P., Vieira L.G.E. 2013. The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Molecular Biology Reports, 40(4): 3269–3279. https://doi.org/10.1007/s11033-012-2402-5
11. Dubrovna O.V., Priadkina G.O., Mykhalska S.I., Komisarenko A.G. 2022. Drought-tolerance of transgenic winter wheat with partial suppression of the proline dehydrogenase gene. Regulatory Mechanisms in Biosystems, 13(4): 385–392. https://doi.org/10.15421/022251
12. Dubrovna O.V., Stasik O.O., Priadkina G.O., Zborivska O.V., Sokolovska-Sergiienko O.G. 2020. Resistance of genetically modified wheat plants, containing a doublestranded RNA suppressor of the proline dehydrogenase gene, to soil moisture deficiency. Agricultural Science and Practice, 7(2): 24–34. https://doi.org/10.15407/agrisp7.02.024
13. El-Beltagi H.S., Mohamed H.I., Sofy M.R. 2020. Role of ascorbic acid, glutathione and proline applied as singly or in sequence combination in improving chickpea plant through physiological change and antioxidant defense under different levels of irrigation intervals. Molecules, 25: 1702. https://doi.org/10.3390/molecules25071702
14. Fabro G., Rizzi Y.S., Alvarez M.E. 2016. Arabidopsis proline dehydrogenase contributes to flagellin-mediated PAMP-triggered immunity by affecting RBOHD. Molecular Plant-Microbe Interactions, 29(8): 620–628. https://doi.org/10.1094/MPMI-01-16-0003-R
15. Faisal S., Mujtaba S.M., Asma, Mahboob W. 2019. Polyethylene glycol mediated osmotic stress impacts on growth and biochemical aspects of wheat (Triticum aestivum L.). Journal of Crop Science and Biotechnology, 22: 213–223. https://doi.org/10.1007/s12892-018-0166-0
16. Forlani G., Trovato M., Funck D., Signorelli S. 2019. Regulation of proline accumulation and its molecular and physiological functions in stress defence. In: Osmoprotectant-mediated abiotic stress tolerance in plants: recent advances and future perspectives. Eds M.A. Hossain, V. Kumar, D.J. Burritt, M. Fujita, P.S.A. Mäkelä. Switzerland AG Cham: Springer Nature, pp. 73–97. https://doi.org/10.1007/978-3-030-27423-8_3
17. Ghosh U.K., Islam M.N., Siddiqui M.N., Cao X., Khan M.A.R. 2022. Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biology, 24(2): 227–239. https://doi.org/10.1111/plb.13363
18. Guo R., Shi L., Jiao Y., Li M., Zhong X., Gu F., Liu Q., Xia X. 2018. Metabolic responses to drought stress in the tissues of drought-tolerant and drought-sensitive wheat genotype seedlings. AoB Plants, 10(2): ply016. https://doi.org/10.1093/aobpla/ply016
19. Gupta A., Rico-Medina A., Caño-Delgado A.I. 2020. The physiology of plant responses to drought. Science, 368(6488): 266–269. https://doi.org/10.1126/science.aaz7614
20. Hasanuzzaman M., Mahmud J.A., Anee T.I., Nahar K.M., Islam T. 2018. Drought stress tolerance in wheat: Omics approaches in understanding and enhancing antioxidant defense abiotic stress-mediated sensing and signaling in plants: an omics perspective. In: Abiotic Stress-Mediated Sensing and Signaling in Plants: An Omics Perspective. Eds S.M. Zargar, M.Y. Zargar. Singapore: Springer Nature, pp. 267–307. https://doi.org/10.1007/978-981-10-7479-0_10
21. Karpets Yu.V., Taraban D.A., Kokorev A.I., Yastreb T.O., Kobyzeva L.N., Kolupaev Yu.E. 2023. Response of wheat seedlings with different drought tolerance to melatonin action under osmotic stress. Agriculture and Forestry, 69(5): 53–69. https://doi.org/10.17707/AgricultForest.69.4.05
22. Kaur G., Asthir B. 2015. Proline: a key player in plant abiotic stress tolerance. Biologia Plantarum, 59: 609–619. https://doi.org/10.1007/s10535-015-0549-3
23. Kaur G., Asthir B., Bains N.S. 2018. Modulation of proline metabolism under drought and salt stress conditions in wheat seedlings. Indian Journal of Biochemistry & Biophysics, 55: 114–124.
24. Kirova E., Pecheva D., Simova-Stoilova L. 2021. Drought response in winter wheat: protection from oxidative stress and mutagenesis effect. Acta Physiologiae Plantarum, 43: 8. https://doi.org/10.1007/s11738-020-03182-1
25. Khomenko S.O., Kochmarskyi V.S., Fedorenko I.V., Fedorenko M.V. 2017. Drought tolerance and yield components of bread spring wheat collection samples in environments of the Forest-Steppe of Ukraine. Myronivka Bulletin, 4: 79–87. https://doi.org/10.31073/mvis201704-07
26. Klümper W., Qaim M. 2014. A meta-analysis of the impacts of genetically modified crops. PloS ONE, 9(11): e111629. https://doi.org/10.1371/journal.pone.0111629
27. Kolupaev Yu.E., Blume Ya.B. 2022. Plant adaptation to changing environment and its enhancement. The Open Agriculture Journal, 16 (Suppl-1, M1): e187433152208251. https://doi.org/10.2174/18743315-v16-e2208251
28. Kolupaev Yu.E., Yastreb T.O., Salii A.M., Kokorev A.I., Ryabchun N.I., Zmiievska O.A., Shkliarevskyi M.A. 2022. State of antioxidant and osmoprotective systems in etiolated winter wheat seedlings of different cultivars due to their drought tolerance. Zemdirbyste-Agriculture, 109(4): 313–322. https://doi.org/10.13080/z-a.2022.109.040
29. Kolupaev Yu.E., Yastreb T.O., Ryabchun N.I., Kokorev A.I., Kolomatska V.P., Dmitriev A.P. 2023. Redox homeostasis of cereals during acclimation to drought. Theoretical and Experimental Plant Physiology, 35(2): 133–168. https://doi.org/10.1007/s40626-023-00271-7
30. Kolupaev Yu.E., Ryabchun N.I., Leonov O.Yu., Kokorev A.I., Taraban D.A., Shakhov I.V., Shkliarevskyi M.A., Yastreb T.O. 2024. Functioning of the antioxidant and osmoprotective systems of Triticum aestivum cultivars growing under soil drought conditions. Botanica, 30(3): 102–116. https://doi.org/10.35513/Botlit.2024.3.1
31. Kosakivska I.V., Vasyuk V.A., Voytenko L.V., Shcherbatiuk M.M., Babenko L.M., Romanenko K.O. 2022a. Effects of exogenous bacterial quorum-sensing signal molecule/messenger N-hexanoyl-L-homoserine lactone (C6-HSL) on acorn germination and plant growth of Quercus robur and Q. rubra (Fagaceae). Ukrainian Botanical Journal, 79(5): 329–338. https://doi.org/10.15407/ukrbotj79.05.329
32. Kosakivska I.V., Vedenicheva N.P., Babenko L.M., Voytenko L.V., Romanenko K.O., Vasyuk V.A. 2022b. Exogenous phytohormones in the regulation of growth and development of cereals under abiotic stresses. Molecular Biology Reports, 49(1): 617–628. https://doi.org/10.1007/s11033-021-06802-2
33. Lau S.-E., Lim L.W.T., Hamdan M.F., Chan C., Saidi N.B., Ong-Abdullah J., Tan B.C. 2025. Enhancing plant resilience to abiotic stress: The power of biostimulants. Phyton — International Journal of Experimental Botany, 94(1). https://doi.org/10.32604/phyton.2025.059930
34. Maghsoudi K., Emam Y., Niazi A., Pessarakli M., Arvin M.J. 2018. P5CS expression level and proline accumulation in the sensitive and tolerant wheat cultivars under control and drought stress conditions in the presence/absence of silicon and salicylic acid. Journal of Plant Interactions, 13(1): 461–471. https://doi.org/10.1080/17429145.2018.1506516
35. Mansour M.M.F., Salama K.H.A. 2020. Proline and abiotic stresses: responses and adaptation. In: Plant ecophysiology and adaptation under climate change: mechanisms and perspectives. II: mechanisms of adaptation and stress amelioration. Ed. M. Hasanuzzaman. Singapore: Springer Nature, pp. 357–397. https://doi.org/10.1007/978-981-15-2172-0_12
36. Marcińska I., Czyczyło-Mysza I., Skrzypek E., Filek M., Grzesiak S., Grzesiak M.T., Janowiak F., Hura T., Dziurka M., Dziurka K., Nowakowska A., Quarrie S.A. 2013. Impact of osmotic stress on physiological and biochemical characteristics in drought-susceptible and drought-resistant wheat genotypes. Acta Physiologiae Plantarum, 35: 451–461. https://doi.org/10.1007/s11738-012-1088-6
37. Meena M., Divyanshu K., Kumar S., Swapnil P., Zehra A., Shukla V., Yadav M., Upadhyay R.S. 2019. Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon, 5(12): e02952. https://doi.org/10.1016/j.heliyon.2019.e02952
38. Mei Y., Qiu D., Xiao S., Chen D. 2018. Evaluation of high temperature tolerance and physiological responses of different Anoectochilus germplasm resources. Applied Ecology and Environmental Research, 16(5): 7017–7031. https://doi.org/10.15666/aeer/1605_70177031
39. Michaletti A., Naghavi M.R., Toorchi M., Toorchi M., Zolla L., Rinalducci S. 2018. Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Scientific Reports, 8: 5710. https://doi.org/10.1038/s41598-018-24012-y
40. Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V.B., Vandepoele K., Gollery M., Shulaev V., Van Breusegem F. 2011. ROS signaling: the new wave? Trends in Plant Science, 16(6): 300–309. https://doi.org/10.1016/j.tplants.2011.03.007
41. Mockevičiūtė R., Jurkonienė S., Šveikauskas V., Zareyan M., Jankovska-Bortkevič E., Jankauskienė J., Kozeko L., Gavelienė V. 2023. Probiotics, proline and calcium induced protective responses of triticum aestivum under drought stress. Plants, 12(6): 1301. https://doi.org/10.3390/plants12061301
42. Munaweera T.I.K., Jayawardana N.U., Rajaratnam R., Dissanayake N. 2022. Modern plant biotechnology as a strategy in addressing climate change and attaining food security. Agriculture & Food Security, 11: 26. https://doi.org/10.1186/s40066-022-00369-2
43. Nasirzadeh L., Sorkhilaleloo B., Majidi Hervan E., Fatehi F. 2021. Changes in antioxidant enzyme activities and gene expression profiles under drought stress in tolerant, intermediate, and susceptible wheat genotypes. Cereal Research Communications, 49: 83–89. https://doi.org/10.1007/s42976-020-00085-2
44. Noor S., Ali S., Rehman H., Ullah F., Ali G.M. 2018. Comparative study of transgenic (DREB1A) and non-transgenic wheat lines on relative water content, sugar, proline and chlorophyll under drought and salt stresses. Sarhad Journal of Agriculture, 34(4): 986–993. https://doi.org/10.17582/journal.sja/2018/34.4.986.993
45. Oboznyi A.I., Kolupaev Yu.E., Yastreb T.O. 2013. Superoxide dismutase activity and the contents of low-molecular-weight protective compounds at the formation of cross-resistance of wheat seedlings to heat and osmotic stresses. Agrokhimiya, 8: 59–61.
46. Ozturk M., Turkyilmaz Unal B., García-Caparrós P., Khursheed A., Gul A., Hasanuzzaman M. 2021. Osmoregulation and its actions during the drought stress in plants. Physiologia Plantarum, 172(2): 1321–1335. https://doi.org/10.1111/ppl.13297
47. Poustini K., Siosemardeh A., Ranjbar M. 2007. Proline accumulation as a response to salt stress in 30 wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Genetic Resources and Crop Evolution, 54: 925–934. https://doi.org/10.1007/s10722-006-9165-6
48. Pykalo S., Demydov O., Yurchenko T., Khomenko S., Humeniuk O., Kharchenko M., Prokopik N. 2020. Methods for evaluation of wheat breeding material for drought tolerance. Visnyk of the Lviv University. Series Biology, 82: 63–79. https://doi.org/10.30970/vlubs.2020.82.05
49. Qayyum A., Al Ayoubi S., Sher A., Bibi Y., Ahmad S., Shen Z., Jenks M. A. 2021. Improvement in drought tolerance in bread wheat is related to an improvement in osmolyte production, antioxidant enzyme activities, and gaseous exchange. Saudi Journal of Biological Sciences, 28(9): 5238–5249. https://doi.org/10.1016/j.sjbs.2021.05.040
50. Raza A., Charagh S., Abbas S., Hassan M.U., Saeed F., Haider S., Sharif R., Anand A., Corpas F.J., Jin W., Varshney R.K. 2023. Assessment of proline function in higher plants under extreme temperatures. Plant Biology, 25(3): 379–395. https://doi.org/10.1111/plb.13510
51. Rehman A.U., Bashir F., Ayaydin F., Kóta Z., Páli T., Vass I. 2021. Proline is a quencher of singlet oxygen and superoxide both in in vitro systems and isolated thylakoids. Physiologia Plantarum, 172(1): 7–18. https://doi.org/10.1111/ppl.13265
52. Ren Y., Miao M., Meng Y., Cao J., Fan T., Yue J., Xiao F., Liu Y., Cao S. 2018. DFR1-mediated inhibition of proline degradation pathway regulates drought and freezing tolerance in Arabidopsis. Cell Reports, 23(13): 3960–3974. https://doi.org/10.1016/j.celrep.2018.04.011
53. Renzetti M., Bertolini E., Trovato M. 2024. Proline metabolism genes in transgenic plants: Meta-analysis under drought and salt stress. Plants, 13: 1913. https://doi.org/10.3390/plants13141913
54. Romanenko O., Kushch I., Zayets S., Solodushko M. 2018. Viability of seeds and sprouts of winter crop varieties under drought conditions of Steppe. Ahroekolohichnyy Zhurnal, 1: 87–95. https://doi.org/10.33730/2077-4893.1.2018.160584
55. Sánchez-Reinoso A.D., Garcés-Varón G., Restrepo-Díaz H. 2014. Biochemical and physiological characterization of three rice cultivars under different daytime temperature conditions. Chilean Journal of Agricultural Research, 74(4): 373–379. https://doi.org/10.4067/S0718-58392014000400001
56. Schneider J.R., Wurlitzer W.B., Ferla N.J., Huzar-Novakowiski J., Chavarria G. 2025. A metanalytic study: does water deficit always increase soybean proline concentration? Theoretical and Experimental Plant Physiology, 37: article 4. https://doi.org/10.1007/s40626-024-00346-z
57. Sharma V., Kumar A., Chaudhary A., Mishra A., Rawat S., Basavaraj B.Y., Shami V., Kaushik P. 2022. Response of wheat genotypes to drought stress stimulated by PEG. Stresses, 2(1): 26–51. https://doi.org/10.3390/stresses2010003
58. Sun Y., Wang C., Chen H.Y.H., Ruan H. 2020. Response of plants to water stress: A meta-analysis. Frontiers in Plant Science, 11: 978. https://doi.org/10.3389/fpls.2020.00978
59. Szabados L., Savouré A. 2010. Proline: a multifunctional amino acid. Trends in Plant Science, 15(2): 89–97. https://doi.org/10.1016/j.tplants.2009.11.009
60. Tuteja N., Sopory S.K. 2008. Chemical signaling under abiotic stress environment in plants. Plant Signaling & Behavior, 3(8): 525–536. https://doi.org/10.4161/psb.3.8.6186
61. Valifard M., Moradshahi A., Kholdebarin B. 2012. Biochemical and physiological responses of two wheat (Triticum aestivum L.) cultivars to drought stress applied at seedling stage. Journal of Agricultural Science and Technology, 14: 1567–1578.
62. Vayner A.O., Kolupaev Yu.E., Yastreb T.O. 2013. Participation of hydrogen peroxide in induction of proline accumulation in millet plants under action of NaCl. Bulletin of Kharkiv National University. Series Biology, 2(29): 32–38.
63. Vendruscolo E.C.G., Schuster I., Pileggi M., Scapim C.A., Molinari H.B.C., Marur C.J., Vieira L.G.E. 2007. Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology, 164(10): 1367–1376. https://doi.org/10.1016/j.jplph.2007.05.001
64. Viechtbauer W. 2010. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3): 1–48. https://doi.org/10.18637/jss.v036.i03
65. Voetberg G.S., Sharp R.E. 1991. Growth of the maize primary root at low water potentials III. Role of increased proline deposition in osmotic adjustment. Plant Physiology, 96(4): 1125–1130. https://doi.org/10.1104/pp.96.4.1125
66. Wu H., Yang Z. 2024. Effects of drought stress and postdrought rewatering on winter wheat: A meta-analysis. Agronomy, 14(2): 298. https://doi.org/10.3390/agronomy14020298
67. Yastreb T.O., Kokorev A.I., Makaova B.E., Ryabchun N.I., Sakhno T. V., Dmitriev A.P., Kolupaev Yu.E. 2023. Response of the antioxidant system of wheat seedlings with different genotypes to exogenous prooxidants: the relationship with resistance to abiotic stressors. Ukrainian Biochemical Journal, 95(6): 81–96. https://doi.org/10.15407/ubj95.06.081
68. Yerlikaya B.A., Mostafa K., Aydin A., Yerlikaya S., Mehmood M., Yilmaz N.N., Yildirim K., Kavas M. 2024. Innovations in plant genome editing and biotechnology: addressing global agricultural challenges. Turkish Journal of Botany, 48(7): 351–375. https://doi.org/10.55730/1300-008X.2823
69. Zarse K., Schmeisser S., Groth M., Priebe S., Beuster G., Kuhlow D., Guthke R., Platzer M., Kahn C.R., Ristow M. 2012. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metabolism, 15(4): 451–465. https://doi.org/10.1016/j.cmet.2012.02.013