Фізіологія рослин і генетика 2022, том 54, № 2, 95-122, doi: https://doi.org/10.15407/frg2022.02.095

Вплив посухи і високої температури на фізіолого-біохімічні процеси та продуктивність рослин

Кірізій Д.А., Стасик О.О.

  • Інститут фізіології рослин і генетики Національної академії наук України 03022 Київ, вул. Васильківська, 31/17

Огляд присвячено аналізу і систематизації літературних даних, а також результатів власних робіт авторів щодо впливу комбінованої дії стресових чинників на фізіолого-біохімічні процеси та продуктивність рослин. Актуальність цих досліджень зумовлена тим, що у польових умовах посіви зазвичай піддаються одночасному впливу низки різних абіотичних стресових чинників, серед яких посуха і висока температура є найбільш значущими у зв’язку з глобальними змінами клімату. Дослідження останніх років показали, що реакція рослин на комбінацію різних абіотичних стресорів є унікальною і не може бути безпосередньо екстрапольована з простого вивчення кожного зі стресів, що діють окремо. Було виявлено специфічні фізіологічні реакції, комбінації метаболітів і білків, а також транскрипти, які є унікальними для конкретних комбінацій стресорів. Наголошується на важливості дослідження особливостей функціону­вання фотосинтетичного апарату, метаболізму активних форм кисню (АФК) і реакції продихів при адаптації рослин до комбінації посухи та теплового стресу, розробки методик широкомасштабного фенотипування фізіолого-біохімічних відповідей рослин під час стресу і наступних фаз відновлення для виявлення фізіологічних маркерів стресостійкості та скринінгу перспективних для селекції форм агрономічно значущих культур з підвищеною толерантністю до комбінації посухи та теплового стресу, щоб пом’якшити негативний вплив прогнозованих глобальних кліматичних змін на сільськогосподарське виробництво.

Ключові слова: посуха, висока температура, фотосинтез, водний режим, антиоксидантний захист, продуктивність

Фізіологія рослин і генетика
2022, том 54, № 2, 95-122

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1. www.ipcc.ch

2. https: // ourworldindata.org/owid-grapher

3. www.ncdc.noaa.gov

4. Peters, G.P., Marland, G., Le Quere, C., Boden, T., Canadell, J.G. & Raupach, M.R. (2011). Rapid growth in CO2 emissions after the 2008-2009 global financial crisis. Nat. Clim. Chang., 2, pp. 2-4. https://doi.org/10.1038/nclimate1332

5. Turek-Hankins, L.L., de Perez, E.C., Scarpa, G., Ruiz-Diaz, R., Schwerdtle, P.N., Joe, E.T., Galappaththi, E.K., French, E.M., Austin, S.E., Singh, C., Sina, M., Siders, A.R., van Aalst, M.K., Templeman, S., Nunbogu, A.M., Berrang-Ford, L., Agrawal, T., the Global Adaptation Mapping Initiative team & Mach, K.J. (2021). Climate change adaptation to extreme heat: a global systematic review of implemented action. Oxford Open Climate Change, 1(1). https://doi.org/10.1093/oxfclm/kgab005

6. Fahad, S., Bajwa, A.A., Nazir, U., Anjum, S.A., Farooq, A., Zohaib, A., Sadia, S., Nasim, W., Adkins, S., Saud, S., Ihsan, M.Z., Alharby, H., Wu, C., Wang, D. & Huang, J. (2017). Crop Production under Drought and Heat Stress: Plant Responses and Management Options. Front. Plant Sci., 8, 1147. https://doi.org/10.3389/fpls.2017.01147

7. Yadav, M.R., Choudhary, M., Singh, J., Lal, M.K., Jha, P.K., Udawat, P., Gupta, N.K., Rajput, V.D., Garg, N.K., Maheshwari, C., Hasan, M., Gupta, S., Jatwa, T.K., Kumar, R., Yadav, A.K. & Prasad, P.V.V. (2022). Impacts, Tolerance, Adaptation, and Mitigation of Heat Stress on Wheat under Changing Climates. Int. J. Mol. Sci., 23, 2838. https://doi.org/10.3390/ijms23052838

8. Mittler, R. & Blumwald, E. (2010). Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev. Plant Biol., 61, pp. 443-462. https://doi.org/10.1146/annurev-arplant-042809-112116

9. Zandalinas, S.I., Fritschi, F.B. & Mittler, R. (2021). Global Warming, Climate Change, and Environmental Pollution: Recipe for a Multifactorial Stress Combination Disaster. Trends in Plant Science, 26, No. 6. https://doi.org/10.1016/j.tplants.2021.02.011

10. Carmo-Silva, A.E., Gore, M.A., Andrade-Sanchez, P., French, A.N., Hunsaker, D.J. & Salvucci, M.E. (2012). Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ. Exp. Bot., 83, pp. 1-11. https://doi.org/10.1016/j.envexpbot.2012.04.001

11. 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

12. Matiu, M., Ankerst, D.P. & Menzel, A. (2017). Interactions between temperature and drought in global and regional crop yield variability during 1961-2014. PLoS One, 12(5), e0178339. https://doi.org/10.1371/journal.pone.0178339

13. Gray, S.B., Dermody, O., Klein, S.P., Locke, A.M., McGrath, J.M., Paul, R.E., Rosenthal, D.M., Ruiz-Vera, U.M., Siebers, M.H., Strellner, R., Ainsworth, E.A., Bernacchi, C.J., Long, S.P., Ort, D.R. & Leakey, A.D.B. (2016). Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean. Nat. Plants, 2, 16132. https://doi.org/10.1038/nplants.2016.132

14. Morgun, V.V., Kiriziy, D.A. & Shadchina, T.M. (2010). Ecophysiological and genetic aspects of adaptation of cultivated plants to global climate changes. Physiol. biochem. cult. plants, 42, No. 1, pp. 3-22 [in Russian].

15. Danquah, A., de Zelicourt, A., Colcombet, J. & Hirt, H. (2014). The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv., 32, pp. 40-52. https://doi.org/10.1016/j.biotechadv.2013.09.006

16. Gilroy, S., Suzuki, N., Miller, G., Choi, W.-G., Toyota, M., Devireddy, A.R. & Mittler, R. (2014). A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci., 19, pp. 623-630. https://doi.org/10.1016/j.tplants.2014.06.013

17. Kolupaev, Yu.E., Karpets, Y.V. & Dmitriev, A.P. (2015). Signal mediators in plants in response to abiotic stress: Calcium, reactive oxygen and nitrogen species. Cytol. Genet., 49(5), pp. 338-348. https://doi.org/10.3103/S0095452715050047

18. Baxter, A., Mittler, R. & Suzuki, N. (2014). ROS as key players in plant stress signalling. J. Exp. Bot., 65, pp. 1229-1240. https://doi.org/10.3389/fpls.2016.00187

19. Munoz-Espinoza, V.A., Lopez-Climent, M.F., Casaretto, J.A. & Gomez-Cadenas, A. (2015). Water stress responses of tomato mutants impaired in hormone biosynthesis reveal abscisic acid, jasmonic acid and salicylic acid interactions. Front. Plant Sci., 6, pp. 1-14. https://doi.org/10.3389/fpls.2015.00997

20. Casaretto, J.A., El-kereamy, A., Zeng, B., Stiegelmeyer, S.M., Chen, X., Bi, Y.M. & Rothstein, S.J. (2016). Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics, 17, 312. https://doi.org/10.1186/s12864-016-2659-5

21. Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E. & Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytol., 203, pp. 32-43. https://doi.org/10.1111/nph.12797

22. Ahmed, I.M., Nadira, U.A., Bibi, N., Cao, F., He, X., Zhang, G. & Wu, F. (2014). Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environ. Exp. Bot., 111, pp. 1-12. https://doi.org/10.1016/j.envexpbot.2014.10.003

23. Zandalinas, S.I., Balfagon, D., Arbona, V., Gomez-Cadenas, A., Inupakutika, M.A. & Mittler, R. (2016). ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J. Exp. Bot., 67, pp. 5381-5390. https://doi.org/10.1093/jxb/erw299

24. Zandalinas, S.I., Rivero, R.M., Martinez, V., Gomez-Cadenas, A. & Arbona, V. (2016). Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol., 16, 105. https://doi.org/10.1186/s12870-016-0791-7

25. Zandalinas, S.I., Mittler, R., Balfagon, D., Arbona, V. & Gomez-Cadenas, A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162, pp. 2-12. https://doi.org/10.1111/ppl.12540

26. Rasmussen, S., Barah, P., Suarez-Rodriguez, M.C., Bressendorff, S., Friis, P., Costantino, P., Bones, A.M., Nielsen, H.B. & Mundy, J. (2013). Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol., 161, pp. 1783-1794. https://doi.org/10.1104/pp.112.210773

27. Pandey, P., Ramegowda, V., & Senthil-Kumar, M. (2015). Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front. Plant Sci., 6, pp. 1-14. https://doi.org/10.3389/fpls.2015.00723

28. Zandalinas, S.I., Sengupta, S., Fritschi, F.B., Azad, R.K., Nechushtai, R. & Mittler, R. (2021).The impact of multifactorial stress combination on plant growth and survival. New Phytologist, 230, pp. 1034-1048. https://doi.org/10.1111/nph.17232

29. Keles, Y. & Oncel, I. (2002). Response of antioxidative defence system to temperature and water stress combinations in wheat seedlings. Plant Sci. 163, pp. 783-790. https://doi.org/10.1016/S0168-9452(02)00213-3

30. Ahmed, I.M., Dai, H., Zheng,W., Cao, F., Zhang, G., Sun, D. & Wu, F. (2013). Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol. Biochem., 63, pp. 49-60. https://doi.org/10.1016/j.plaphy.2012.11.004

31. Giraud, E., Ho, L.H.M., Clifton, R., Carroll, A., Estavillo, G., Tan, Y.-F., Howell, K.A., Ivanova, A., Pogson, B.J., Millar, A.H. & Whelan, J. (2008). The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol., 147, pp. 595-610. https://doi.org/10.1104/pp.107.115121

32. Haghjou, M.M., Shariati, M. & Smirnoff, N. (2009). The effect of acute high light and low temperature stresses on the ascorbate-glutathione cycle and superoxide dismutase activity in two Dunaliella salina strains. Physiol. Plant., 135, pp. 272-280. https://doi.org/10.1111/j.1399-3054.2008.01193.x

33. Sales, C.R.G., Ribeiro, R.V., Silveira, J.A.G., Machado, E.C., Martins, M.O. & Lagoa, A.M.M.A. (2013). Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature. Plant Physiol. Biochem., 73, pp. 326-336. https://doi.org/10.1016/j.plaphy.2013.10.012

34. Srivastava, G., Kumar, S., Dubey, G., Mishra, V. & Prasad, S.M. (2012). Nickel and ultraviolet-B stresses induce differential growth and photosynthetic responses in Pisum sativum L. seedlings. Biol. Trace Elem. Res., 149, pp. 86-96. https://doi.org/10.1007/s12011-012-9406-9

35. Wang, X., Li, Y., Lu, H. & Wang, S. (2016). Combined effects of elevated temperature and CO2 concentration on Cd and Zn accumulation dynamics in Triticum aestivum L. J. Environ. Sci., 47, pp. 109-119. https://doi.org/10.1016/j.jes.2015.11.029

36. Cherif, J., Mediouni, C., Ben Ammar, W. & Jemal, F. (2011). Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum). J. Environ. Sci., 23, pp. 837-844. https://doi.org/10.1016/S1001-0742(10)60415-9

37. Alhdad, G.M., Seal, C.E., Al-Azzawi, M.J. & Flowers, T.J. (2013). The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: the role of antioxidants. Environ. Exp. Bot., 87, pp. 120-125. https://doi.org/10.1016/j.envexpbot.2012.10.010

38. Castagna, A., Di Baccio, D., Ranieri, A.M., Sebastiani, L. & Tognetti, R. (2015). Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones. Environ. Sci. Pollut. Res., 22, pp. 2064-2075. https://doi.org/10.1007/s11356-014-3481-8

39. Iyer, N.J., Tang, Y. & Mahalingam, R. (2013). Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ., 36, pp. 706-720. https://doi.org/10.1111/pce.12008

40. Ainsworth, E.A., Rogers, A. & Leakey, A.D.B. (2008). Targets for crop biotechnology in a future high-CO2 and high-O3 world. Plant Physiol., 147, pp. 13-19. https://doi.org/10.1104/pp.108.117101

41. Perez-Lopez, U., Miranda-Apodaca, J., Munoz-Rueda, A. & Mena-Petite, A. (2013). Lettuce production and antioxidant capacity are differentially modified by salt stress and light intensity under ambient and elevated CO2. J. Plant Physiol., 170, pp. 1517-1525. https://doi.org/10.1016/j.jplph.2013.06.004

42. Rivero, R.M., Mestre, T.C., Mittler, R., Rubio, F., Garcia-Sanchez, F. & Martinez, V. (2013). The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ., 37, pp. 1059-1073. https://doi.org/10.1111/pce.12199

43. Nuccio, M.L., Wu, J., Mowers, R., Zhou, H.P., Meghji, M., Primavesi, L.F., Paul, M.J., Xi, C., Gao, Y., Haque, E., Basu, S.S. & Lagrimini, L.M. (2015). Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat. Biotechnol., 33, pp. 862-869. https://doi.org/10.1038/nbt.3277

44. 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, pp. 463-477. https://doi.org/10.2478/intag-2013-0017

45. Posch, B.C., Kariyawasam, B.C., Bramley, H., Coast, O., Richards, R.A., Reynolds, M.P., Trethowan, R. & Atkin, O.K. (2019). Exploring high temperature responses of photosynthesis and respiration to improve heat tolerance in wheat. J. Exp. Bot., 70, No. 19, pp. 5051-5069. https://doi.org/10.1093/jxb/erz257

46. Landi, S., Hausman, J.F., Guerriero, G. & Esposito, S. (2017). Poaceae vs. abiotic stress: focus on drought and salt stress, recent insights and perspectives. Front. Plant Sci., 8, 1214. https://doi.org/10.3389/fpls.2017.01214

47. Aprile, A., Havlickova, L., Panna, R., Mare, C., Borrelli, G.M., Marone, D., Perrotta, C., Rampino, P., De Bellis, L., Curn, V., Mastrangelo, A.M., Rizza, F. & Cattivelli, L. (2013). Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics, 14, pp. 1-18. https://doi.org/10.1186/1471-2164-14-821

48. Niinemets, U. (2015). Uncovering the hidden facets of drought stress: secondary metabolites make the difference. Tree Physiol., 36, pp. 129-132. https://doi.org/10.1093/treephys/tpv128

49. Zandalinas, S.I., Sales, C., Beltran, J., Gomez-Cadenas, A. & Arbona, V. (2017). Activation of secondary metabolism in citrus plants is associated to sensitivity to combined drought and high temperatures. Front. Plant Sci., 7, 1954. https://doi.org/10.3389/fpls.2016.01954

50. Poorter, H., Niinemets, U., Poorter, L., Wright, I.J. & Villar, R. (2009). Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol., 182, pp. 565-588. https://doi.org/10.1111/j.1469-8137.2009.02830.x

51. Shahinnia, F., Le Roy, J., Laborde, B., Sznajder, B., Kalambettu, P., Mahjourimajd, S., Tilbrook, J. & Fleury, D. (2016). Genetic association of stomatal traits and yield in wheat grown in low rainfall environments. BMC Plant Biol., 16, 150. https://doi.org/10.1186/s12870-016-0838-9

52. De Boeck, H.J., Bassin, S., Verlinden, M., Zeiter, M. & Hiltbrunner, E. (2015). Simulated heat waves affected alpine grassland only in combination with drought. New Phytol., 209, pp. 531-541. https://doi.org/10.1111/nph.13601

53. Handayani, T. & Watanabe, K. (2020). The combination of drought and heat stress has a greater effect on potato plants than single stresses. Plant, Soil and Environment, 66 (4), pp. 175-182. https://doi.org/10.17221/126/2020-PSE

54. Lamaoui, M., Jemo, M., Datla, R. & Bekkaoui, F. (2018). Heat and Drought Stresses in Crops and Approaches for Their Mitigation. Front. Chem., 6, 26. https://doi.org/10.3389/fchem.2018.00026

55. Dwivedi, R., Prasad, S., Jaiswal, B., Kumar, A., Tiwari, A., Patel, S., Pandey, S. & Pandey, G. (2017). Evaluation of wheat genotypes (Triticum aestivum L.) at grain filling stage for heat tolerance. Int. J. Pure App. Biosci., 5 (2), pp. 971-975. https://doi.org/10.18782/2320-7051.2614

56. Kaushal, N., Awasthi, R., Gupta, K., Gaur, P., Siddique, K. H. & Nayyar, H. (2013). Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Funct. Plant Biol., 40, pp. 1334-1349. https://doi.org/10.1071/FP13082

57. Cairns, J.E., Sonder, K., Zaidi, P.H., Verhulst, N., Mahuku, G., Babu, R., Nair, S.K., Das, B., Govaerts, B., Vinayan, M.T., Rashid, Z., Noor, J.J., Devi P., San Vicente, F. & Prasanna, B.M. (2012). Maize production in a changing climate: impacts, adaptation, and mitigation strategies. Adv. Agron., 114, pp. 1-58. https://doi.org/10.1016/B978-0-12-394275-3.00006-7

58. Singh, V., Nguyen, C.T., Yang, Z., Chapman, C., van Oosterom, E.J. & Hammer, G.L. (2016). Genotypic differences in effects of short episodes of high-temperature stress during reproductive development in sorghum. Crop Sci., 56, pp. 1561-1572. https://doi.org/10.2135/cropsci2015.09.0545

59. Prasad, P.V.V., Pisipati, S.R., Momcilovic, 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, pp. 430-441. https://doi.org/10.1111/j.1439-037X.2011.00477.x

60. Giorno, F., Wolters-Arts, M., Mariani, C. & Rieu, I. (2013). Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants, 2, pp. 489-506. https://doi.org/10.3390/plants2030489

61. Hedhly, A. (2011). Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ. Exp. Bot., 74, pp. 9-16. https://doi.org/10.1016/j.envexpbot.2011.03.016

62. Cohen, I., Zandalinas, S.I., Huck, C.F., Fritschi, B. & Mittler, R. (2021). Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiologia Plantarum, 171, Is. 1, pp. 66-76. https://doi.org/10.1111/ppl.13203

63. Tidy, A.C., Murchie, E.H., Wilson, Z.A. & Ferguson, J.N. (2021). The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress. Plant Cell Environ., 44, pp. 2066-2089. https://doi.org/10.1111/pce.14015

64. Moore, C.E., Meacham-Hensold, K., Lemonnier, P., Slattery, R.A., Benjamin, C., Bernacchi, C.J., Lawson, T. & Cavanagh, A.P. (2021). The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J. Exp. Bot., 72, No. 8, pp. 2822-2844. https://doi.org/10.1093/jxb/erab090

65. Hirayama, T. & Shinozaki, K. (2010). Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J., 61, pp. 1041-1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x

66. Huber, A.E. & Bauerle, T.L. (2016). Long-distance plant signaling pathways in response multiple stressors: the gap in knowledge. J. Exp. Bot., 67, pp. 2063-2079. https://doi.org/10.1093/jxb/erw099

67. Sicher, R.C., Timlin, D. & Bailey, B. (2012). Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J. Plant Physiol., 169, pp. 686-695. https://doi.org/10.1016/j.jplph.2012.01.002

68. Goufo, P., Moutinho-Pereira, J.M., Jorge, T.F., Correia, C.M., Oliveira, M.R., Rosa, E.A.S., Antonio, C. & Trindade, H. (2017). Cowpea (Vigna unguiculata L.Walp.) metabolomics: osmoprotection as a physiological strategy for drought stress resistance and improved yield. Front. Plant Sci., 8, 586. https://doi.org/10.3389/fpls.2017.00586

69. Lee, S.B. & Suh, M.C. (2013). Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol. Plant., 6, pp. 246-249. https://doi.org/10.1093/mp/sss159

70. Blum, A. (2017). Osmotic adjustment is a prime drought stress adaptive engine in support of plant production: osmotic adjustment and plant production. Plant Cell Environ., 40, pp. 4-10. https://doi.org/10.1111/pce.12800

71. Khan, M.S., Kanwal, B. & Nazir, S. (2015). Metabolic engineering of the chloroplast genome reveals that the yeast ArDH gene confers enhanced tolerance to salinity and drought in plants. Front. Plant Sci., 6, 725. https://doi.org/10.3389/fpls.2015.00725

72. Maurel, C., Boursiac, Y., Luu, D.-T., Santoni, V., Shahzad, Z. & Verdoucq, L. (2015). Aquaporins in plants. Physiol Rev., 95, pp. 1321-1358. https://doi.org/10.1152/physrev.00008.2015

73. Vandeleur, R.K., Sullivan, W., Athman, A., Jordans, C., Gilliham, M., Kaiser, B.N. & Tyerman, S.D. (2014). Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant Cell Environ., 37, pp. 520-538. https://doi.org/10.1111/pce.12175

74. Arbona, V., Manzi, M., de Ollas, C. & Gomez-Cadenas, A. (2013). Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int. J. Mol. Sci., 14, pp. 4885-4811. https://doi.org/10.3390/ijms14034885

75. Saibo, N.J., Lourenco, T. & Oliveira, M.M. (2009). Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann. Bot., 103, pp. 609-623. https://doi.org/10.1093/aob/mcn227

76. Rahnama, A., Poustini, K., Tavakkol-Afshari, R. & Tavakoli, A. (2010). Growth and stomatal responses of bread wheat genotypes in tolerance to salt stress. Int. J. Biol. Life Sci., 6, pp. 216-221. https://doi.org/10.5281/zenodo.1078158

77. Nishiyama, Y. & Murata, N. (2014). Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl. Microbiol. Biotechnol., 98, pp. 8777-8796. https://doi.org/10.1007/s00253-014-6020-0

78. Abdelhakim, L.O.A., Rosenqvist, E., Wollenweber, B., Spyroglou, I., Ottosen, C.-O. & Panzarova, K. (2021). Investigating Combined Drought and Heat Stress Effects in Wheat under Controlled Conditions by Dynamic Image-Based Phenotyping. Agronomy, 11, 364. https://doi.org/10.3390/agronomy11020364

79. Kedruk, A.C., Kiriziy, D.A., Sokolovska-Sergienko, O.G. & Stasik, O.O. (2021). Response of the photosynthetic apparatus of winter wheat varieties to the combined action of drought and high temperature. Fiziol. rast. genet., 53, No. 5, pp. 387-405 [in Ukrainian]. https://doi.org/10.15407/frg2021.05.387

80. Tricker, P.J., ElHabti, A., Schmidt, J. & Fleury, D. (2018). The physiological and gene­tic basis of combined drought and heat tolerance in wheat. J. Exp. Bot., 69, No. 13, pp. 3195-3210. https://doi.org/10.1093/jxb/ery081

81. Omae, H., Kumar, A. & Shono, M. (2012). Adaptation to High Temperature and Water Deficit in the Common Bean (Phaseolus vulgaris L.) during the Reproductive Period. Journal of Botany, 2012, article ID 803413. https://doi.org/10.1155/2012/803413

82. Caverzan, A., Casassola, A. & Brammer, S.P. (2016). Antioxidant responses of wheat plants under stress. Genet. Mol. Biol., 39, No. 1, pp. 1-6. https://doi.org/10.1590/1678-4685-GMB-2015-0109

83. Kolupaev, Yu.E. & Kokorev, A.I. (2019). Antioxidant system and plant resistance to water deficit. Fiziol. rast. genet., 51, No. 1, pp. 28-54 [in Russian]. https://doi.org/10.15407/frg2019.01.028

84. Morgun, V.V., Stasik, O.O., Kiriziy, D.A. & Sokolovska-Sergiienko, O.G. (2019). Effect of drought on photosynthetic apparatus, activity of antioxidant enzymes, and productivity of modern winter wheat varieties. Regulatory Mechanisms in Biosystems, 10, No. 1, pp. 16-25. https://doi.org/10.15421/021903

85. Kumar, D., Kushwaha, S., Delvento, C., Liatukas, Z., Vivekanand, V., Svensson, J.T., Henriksson, T., Brazauskas, G. & Chawade, A. (2020). Affordable Phenotyping of Winter Wheat under Field and Controlled Conditions for Drought Tolerance. Agronomy, 10, 882. https://doi.org/10.3390/agronomy10060882

86. Degen, G.E., Orr, D.J. & Carmo-Silva, E. (2021). Heat-induced changes in the abundance of wheat Rubisco activase isoforms. New Phytologist, 229, pp. 1298-1311. https://doi.org/10.1111/nph.16937

87. Ruggiero, A., Punzo, P., Landi, S., Costa, A., VanOoosten, M. & Grillo, S. (2017). Improving plant water use efficiency through molecular genetics. Horticulturae, 3, 31. https://doi.org/10.3390/horticulturae3020031

88. Sikuku, P.A., Netondo, G.W., Onyango, J.C. & Musyimi, D.M. (2010). Chlorophyll fluorescence, protein and chlorophyll content of three NERICA rainfed rice varieties under varying irrigation regimes. ARPN J. Agr. Biol. Sci., 5, pp. 19-25. http://www.arpnjournals.com/jabs/research_papers/rp_2010/jabs_0310_179.pdf

89. Ellsworth, P.Z. & Cousins, A.B. (2016). Carbon isotopes and water use efficiency in C4 plants. Curr. Opin. Plant Biol., 31, pp. 155-161. https://doi.org/10.1016/j.pbi.2016.04.006

90. Correia, B., Hancock, R.D., Amaral, J., Gomez-Cadenas, A., Valledor, L. & Pinto, G. (2018). Combined Drought and Heat Activates Protective Responses in Eucalyptus globulus That Are Not Activated When Subjected to Drought or Heat Stress Alone. Front. Plant Sci., 9, 819. https://doi.org/10.3389/fpls.2018.00819

91. Kromdijk, J., Glowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K. & Long, S.P. (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354, pp. 857-861. https://doi.org/10.1126/science.aai8878

92. Ort, D.R., Merchant, S.S., Alric, J., Barkan, A., Blankenship, R.E., Bock, R., Croce, R., Hanson, M.R., Hibberd, J.M., Long, S.P., Moore, T.A., Moroney, J., Niyogi, K.K., Parry, M.A. J., Peralta-Yahya, P.P., Prince, R.C., Redding, K.E., Spalding, M.H., van Wijk, K.J., Vermaas, W.F. J., von Caemmerer, S., Weber, A.P. M., Yeates, T.O., Yuan, J.S. & Zhu, X.G. (2015). Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA, 112, pp. 8529-8536. https://doi.org/10.1073/pnas.1424031112

93. Balfagon, D., Zandalinas, S.I., Mittler, R. & Gomez-Cadenas, A. (2020). High temperatures modify plant responses to abiotic stress conditions. Physiol. Plant., 170 (3), pp. 335-344. https://doi.org/10.1111/ppl.13151

94. Zandalinas, S.I., Fichman, Y., Devireddy, A.R., Sengupta, S., Azad, R.K. & Mittler, R. (2020). Systemic signaling during abiotic stress combination in plants. Proc. Natl. Acad. Sci., 117, No. 24, pp. 13810-13820. https://doi.org/10.1073/pnas.2005077117

95. He, Z.H., Fujiki, M. & Kohorn, B.D. (1996). A cell wall-associated, receptor-like protein kinase. J. Biol. Chem., 271, pp. 19789-19793. https://doi.org/10.1074/jbc.271.33.19789

96. Walker, J.C. & Zhang, R. (1990). Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature, 345, pp. 743-746. https://doi.org/10.1038/345743a0

97. Shulaev, V., Cortes, D., Miller, G. & Mittler, R. (2008). Metabolomics for plant stress response. Physiol. Plant., 132, pp. 199-208. https://doi.org/10.1111/j.1399-3054.2007.01025.x

98. Lawson, T. & Matthews, J. (2020). Guard cell metabolism and stomatal function. Annu. Rev. Plant Biol., 71, pp. 273-302. https://doi.org/10.1146/annurev-arplant-050718-100251

99. Wani, S.H., Kumar, V., Shriram, V. & Sah, S.K. (2016). Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J., 4, No. 3, pp. 162-176. https://doi.org/10.1016/j.cj.2016.01.010

100. Bauer, H., Ache, P., Lautner, S., Fromm, J., Hartung, W., Al-Rasheid Khaled, K., Sonnewald, A.S., Sonnewald, U., Kneitz, S., Lachmann, Ni., Mendel, R.R., Bittner, F., Hetherington, A.M. & Hedrich, R. (2013). The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr. Biol., 23, pp. 53-57. https://doi.org/10.1016/j.cub.2012.11.022

101. Suzuki, N., Basil, E., Hamilton, J.S., Inupakutika, M.A., Zandalinas, S.I., Tripathy, D., Yuting, L., Dion, E., Fukui, G., Kumazaki, A., Nakano, R., Rivero, R.M., Verbeck, G.F., Azad, R.K., Blumwald, E. & Mittler, R. (2016). ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One, 11, e0147625. https://doi.org/10.1371/journal.pone.0147625

102. Suzuki, N., Miller, G., Salazar, C., Mondal, H.A., Shulaev, E., Cortes, D.F., Shuman, J.L., Luo, X., Shah, J., Schlauch, K., Shulaev, V. & Mittler, R. (2013). Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell, 25, pp. 3553-3569. https://doi.org/10.1105/tpc.113.114595

103. Mittler, R. & Blumwald, E. (2015). The roles of ROS and ABA in systemic acquired acclimation. Plant Cell, 27, pp. 64-70. https://doi.org/10.1105/tpc.114.133090

104. Verma, V., Ravindran, P. & Kumar, P. P. (2016). Plant hormone mediated regulation of stress responses. BMC Plant Biol., 16, 86. https://doi.org/10.1186/s12870-016-0771-y

105. Pornsiriwong, W., Estavillo, G.M., Chan, K.X., Tee, E.E., Ganguly, D., Crisp, P.A., Phua, S.Y., Zhao, C., Qiu, J., Park, J., Yong, M.T., Nisar, N., Yadav, A.K., Schwessinger, B., Rathjen, J., Cazzonelli, C.I., Wilson, P.B., Gilliham, M., Chen, Z.-H. & Pogson, B.J. (2017). A chloroplast retrograde signal, 3'-phosphoadenosine-5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. elife, 6, e23361. https://doi.org/10.7554/eLife.23361

106. Zlatev, Z. & Lidon, F. C. (2012). An overview on drought induced changes in plant growth, water relations and photosynthesis. Emir. J. Food Agric. 24, pp. 57-72. https://doi.org/10.9755/ejfa.v24i1.10599

107. Gill, S.S. & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem., 48, pp. 909-930. https://doi.org/10.1016/j.plaphy.2010.08.016

108. Kolupaev, Yu.E. (2016). Plant cell antioxidants and their role in ROS signaling and plant resistance. Uspekhi Sovrem. Biologii, 136 (2), pp. 181-198 [in Russian].

109. Kudla, J., Batistic, O. & Hashimoto, K. (2010). Calcium signals: the lead currency of plant information processing. Plant Cell, 22, pp. 541-563. https://doi.org/10.1105/tpc.109.072686

110. Reddy, A.S., Ali, G.S., Celesnik, H. & Day, I.S. (2011). Coping with stresses: roles of calciumand calcium/calmodulin-regulated gene expression. Plant Cell, 23, pp. 2010-2032. https://doi.org/10.1105/tpc.111.084988

111. Ashraf, M. & Harris, P.J.C. (2013). Photosynthesis under stressful environments: an overview. Photosynthetica, 51, pp. 163-190. https://doi.org/10.1007/s11099-013-0021-6

112. Wahid, A., Gelani, S., Ashraf, M. & Foolad, M.R. (2007). Heat tolerance in plants: an overview. Environ. Exp. Bot., 61, pp. 199-223. https://doi.org/10.1016/j.envexpbot.2007.05.011

113. Wahid, A. & Close, T.J. (2007). Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plantarum, 51, pp. 104-109. https://doi.org/10.1007/s10535-007-0021-0

114. Camejo, D., Rodriguez, P., Morales, M.A., Dell'Amico, J.M., Torrecillas, A. & Alarcon, J.J. (2005). High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J. Plant Physiol., 162, pp. 281-289. https://doi.org/10.1016/j.jplph.2004.07.014

115. Ahn, Y. J. & Zimmerman, J. (2006). Introduction of the carrot HSP17. 7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant Cell Environ., 29, pp. 95-104. https://doi.org/10.1111/j.1365-3040.2005.01403.x

116. Obata, T., Witt, S., Lisec, J., Palacios-Rojas, N., Florez-Sarasa, I., Araus, J.L., Cairns, J.E., Yousfi, S. & Fernie, A.R. (2015). Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol., 169, pp. 2665-2683. https://doi.org/10.1104/pp.15.01164

117. Morales, C.G., Pino, M.T. & del Pozo, A. (2013). Phenological and physiological responses to drought stress and subsequent rehydration cycles in two raspberry cultivars. Sci. Hortic., 162, pp. 234-241. https://doi.org/10.1016/j.scienta.2013.07.025

118. Huang, J.-Z., Xu, S.-L., Ma, T.-C., Li, Y.-F., Fu, H.-W., Li, Z.-F. & Shu, Qi.-Y. (2021). Analysis of proline accumulation, antioxidant capacity and HSP expression in mutant rice lines with different heat tolerance. Australian Journal of Crop Science, Southern Cross Publishing, 15 No. 8, pp. 22-27. https://doi.org/10.21475/ajcs.21.15.09.sp-2

119. Kolupaev, Yu. E., Vainer, A.A. & Yastreb, T.O. (2014). Proline: physiological functions and regulation of the content in plants under stress conditions. Visn. Hark. nac. agrar. univ., Ser. Biol., Iss. 2, pp. 6-22 [in Russian].

120. Szabados, L. & Savoure, A. (2010). Proline: a multifunctional amino acid. Trends in Plant Sci., 15, No. 2, pp. 89-97. https://doi.org/10.1016/j.tplants.2009.11.009

121. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. & Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol., 134, pp. 1683-1696. https://doi.org/10.1104/pp.103.033431

122. Jin, R., Wang, Y., Liu, R., Gou, J. & Chan, Z. (2016). Physiological and metabolic changes of Purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front. Plant Sci., 6, pp. 1-11. https://doi.org/10.3389/fpls.2015.01123

123. Wang, G.-P., Hui, Z., Li, F., Zhao, M.-R., Zhang, J. & Wang, W. (2010). Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycinebetaine. Plant Biotechnol. Rep., 4, pp. 213-222. https://doi.org/10.1007/s11816-010-0139-y

124. Quan, R., Shang, M., Zhang, H., Zhao, Y. & Zhang, J. (2004). Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol. J., 2, pp. 477-486. https://doi.org/10.1111/j.1467-7652.2004.00093.x

125. Su, J., Hirji, R., Zhang, L., He, C., Selvaraj, G. & Wu, R. (2006). Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J. Exp. Bot., 57, pp. 1129-1135. https://doi.org/10.1093/jxb/erj133

126. Koussevitzky, S., Suzuki, N., Huntington, S., Armijo, L., Sha, W., Cortes, D., Shulaev, V. & Mittler, R. (2008). Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem., 283, pp. 34197-34203. https://doi.org/10.1074/jbc.M806337200

127. Fraser, C.M. & Chapple, C. (2011). The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book, 9, e0152. https://doi.org/10.1199/tab.0152

128. Alsamman, A.M., Bousba, R., Baum, M., Hamwieh, A. & Fouad, N. (2021). Comprehensive analysis of the gene expression profile of wheat at the crossroads of heat, drought and combined stress. Highlights in BioScience, 20, 4. https://doi.org/10.36462/H.BioSci.202104

129. Rizhsky, L., Liang, H. & Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol., 130, pp. 1143-1151. https://doi.org/10.1104/pp.006858

130. Rampino, P., Mita, G., Fasano, P., Borrelli, G.M., Aprile, A., Dalessandro, G., De Bellis, L. & Perrotta, C. (2012). Novel durum wheat genes up-regulated in response to a combination of heat and drought stress. Plant Physiol. Biochem., 56, pp. 72-78. https://doi.org/10.1016/j.plaphy.2012.04.006

131. Johnson, S.M., Lim, F.-L., Finkler, A., Fromm, H., Slabas, A.R. & Knight, M.R. (2014). Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics, 15, 456. https://doi.org/10.1186/1471-2164-15-456

132. Bi, A., Fan, J., Hu, Z., Wang, G., Amombo, E., Fu, J. & Hu, T. (2016). Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. Front. Plant Sci., 7, 453. https://doi.org/10.3389/fpls.2016.00453

133. Morgun, V.V., Dubrovna, O.V. & Morgun, B.V. (2016). The modern biotechnologies of producing wheat plants resistant to stresses. Fiziol. rast. genet., 48, No. 3, pp. 196-213 [in Ukrainian]. https://doi.org/10.15407/frg2016.03.196

134. Corrales, A.R., Carrillo, L., Lasierra, P., Nebauer, S.G., Dominguez-Figueroa, J., Renau-Morata, B., Pollmann, S., Granell, A., Molina, R.-V., Vicente-Carbajosa, J. & Medina, J. (2017). Multifaceted role of cycling Dof Factor 3 (CDF3) in the regulation of flowering time and abiotic stress responses in Arabidopsis. Plant Cell Environ., 40, pp. 748-764. https://doi.org/10.1111/pce.12894

135. Kulkarni, M., Soolanayakanahally, R., Ogawa, S., Uga, Y., Selvaraj, M.G. & Kagale, S. (2017). Drought response in wheat: key genes and regulatory mechanisms controlling root system architecture and transpiration efficiency. Front. Chem., 5, 106. https://doi.org/10.3389/fchem.2017.00106

136. He, G.H., Xu, Y.J., Wang, X.Y., Liu, M.J., Li, S.P., Chen, M., Ma, Y.-Z. & Xu, Z.-S. (2016). Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biol., 16, 116. https://doi.org/10.1186/s12870-016-0806-4

137. Hasanuzzaman, M., Nahar, K., Hossain, M.S., Mahmud, J.A., Rahman, A., Inafuku, M., Oku, H. & Fujita, M. (2017). Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int. J. Mol. Sci., 18, 200. https://doi.org/10.3390/ijms18010200

138. Kiriziy, D.A., Kedruk, A.S., Sokolovska-Sergiienko, O.G., Dubrovna, O.V. & Stasik, O.O. (2021). Responses of photosynthetic apparatus of genetically modified wheat plants containing a double-stranded RNA suppressor of the proline dehydrogenase gene to drought and high temperature. Fisiol. rast. genet., 53, No. 6, pp. 532-549. https://doi.org/10.15407/frg2021.06.532

139. Kishchenko, O., Stepanenko, A. & Borisjuk, M. (2021). Induced mutagenesis in wheat: from ionizing radiation to site-specific gene editing. Fiziol. rast. genet., 53, No. 1, pp. 29-54 [in Ukrainian]. https://doi.org/10.15407/frg2021.01.029

140. da Costa, M.V.J., Ramegowda, Y., Ramegowda, V., Karaba, N.N., Sreeman, S.M. & Udayakumar, M. (2021). Combined Drought and Heat Stress in Rice: Responses, Phenotyping and Strategies to Improve Tolerance. Rice Science, 28 (3), pp. 233-242. https://doi.org/10.1016/j.rsci.2021.04.003

141. Pequeno, D.N.L., Hernґandez-Ochoa, I.M., Reynolds, M., Sonder, K., MoleroMilan, A., Robertson, R.D., Lopes, M.S., Xiong, W., Kropff, M. & Asseng, S. (2021). Climate impact and adaptation to heat and drought stress of regional and global wheat production. Environ. Res. Lett., 16, 054070. https://doi.org/10.1088/1748-9326/abd970

142. Waraich, E.A., Ahmad, R., Halim, A. & Aziz, T. (2012). Alleviation of temperature stress by nutrient management in crop plants: a review. J. Soil Sci. Plant Nut., 12, pp. 221-244. https://doi.org/10.4067/S0718-95162012000200003

143. Gautam, P., Lal, B., Tripathi, R., Shahid, M., Baig, M.J., Raja, R., Maharana, S. & Nayak, A. (2016). Role of silica and nitrogen interaction in submergence tolerance of rice. Environ. Exp. Bot., 125, pp. 98-109. https://doi.org/10.1016/j.envexpbot.2016.02.008

144. Ma, D., Sun, D., Wang, C., Qin, H., Ding, H., Li, Y. & Guo, T. (2016). Silicon application alleviates drought stress in wheat through transcriptional regulation of multiple antioxidant defense pathways. J. Plant Growth Regul., 35, pp. 1-10. https://doi.org/10.1007/s00344-015-9500-2

145. Kosakivska, I.V., Vasyuk, V.A. & Voytenko, L.V. (2019). Effect of exogenous abscisic acid on morphological characteristics of winter wheat and spelt under hyperthermia. Fiziol. rast. genet., 51, No. 4, pp. 324-337 [in Ukrainian]. https://doi.org/10.15407/frg2019.04.324

146. Vedenicheva, N.P. & Kosakivska, I.V. (2020). Cytokinins in cereals ontogenesis and adaptation. Fiziol. rast. genet., 52. No. 1, pp. 3-30 [in Ukrainian]. https://doi.org/10.15407/frg2020.01.003