Photosynthetica 2025, 63(2):165-181 | DOI: 10.32615/ps.2025.019

Thermal stability changes of photosynthesis during osmotic and salt stress in wheat varieties cultivated in Central Europe and Mediterranean North Africa

A. ALLEM1, 2, R. TARNAI1, S.B. TÓTH1, W.A.E. ABIDO3, S. DULAI1
1 Department of Botany and Plant Physiology, Faculty of Science, Eszterházy Catholic University, H-3301 Eger, P.O. Box 43, Hungary
2 Biological Doctoral School, Hungarian University of Agriculture and Life Sciences, H-2011 Gödöllő, Hungary
3 Agronomy Department, Faculty of Agriculture, Mansoura University, Egypt

The thermal stability of photosynthetic apparatus under osmotic/salt stress was examined in wheat cultivars grown under different climatic conditions. The thermostability of nonstressed plants did not differ significantly from each other and it was not improved by osmotic treatment in the absence of light. In contrast, the salt stress resulted in better thermostability. This was also manifested in the temperature dependence of maximal quantum yield of PSII photochemistry. The temperature dependence of steady-state fluorescence and other photosynthetic parameters indicated a moderate reduction in thermal sensitivity of photosynthesis in well-watered plants which was further enhanced by osmotic, but even more by salt treatment. It seems likely that the osmotic stress-induced thermal stability increase of PSII occurs only in energized thylakoids. The temperature dependence of quantum yield of regulated energy dissipation seems to suggest that the secondary effects of lumen pH might have a role in the protective mechanisms concerning these stresses, but salt stress can also affect thermal stability in other ways as well.

Additional key words: chlorophyll fluorescence; osmotic stress, photosynthesis; salt stress; thermal tolerance; wheat.

Received: March 1, 2025; Revised: May 26, 2025; Accepted: June 2, 2025; Prepublished online: July 8, 2025; Published: July 10, 2025  Show citation

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ALLEM, A., TARNAI, R., TÓTH, S.B., ABIDO, W.A.E., & DULAI, S. (2025). Thermal stability changes of photosynthesis during osmotic and salt stress in wheat varieties cultivated in Central Europe and Mediterranean North Africa. Photosynthetica, 63(2), 165-181. doi: 10.32615/ps.2025.019
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    References

    1. Allakhverdiev S.I., Kreslavski V.D., Klimov V.V. et al.: Heat stress: an overview of molecular responses in photosynthesis. -Photosynth. Res. 98: 541-550, 2008. Go to original source...
    2. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391-396, 2006. Go to original source...
    3. Ashraf M., Harris P.J.C.: Photosynthesis under stressful environments: an overview. - Photosynthetica 51: 163-190, 2013. Go to original source...
    4. Atta K., Mondal S., Gorai S. et al.: Impacts of salinity stress on crop plants: improving salt tolerance through genetic and molecular dissection. - Front. Plant Sci. 14: 1241736, 2023. Go to original source...
    5. Bellasio C.: Quantifying photosynthetic restrictions. - Photosynth. Res. 163: 19, 2025. Go to original source...
    6. Berry J.A., Björkman O.: Photosynthetic response and adaptation to temperature in higher plants. - Annu. Rev. Plant Physiol. 31: 491-543, 1980. Go to original source...
    7. Centritto M., Loreto F., Chartzoulakis K.: The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. - Plant Cell Environ. 26: 585-594, 2003. Go to original source...
    8. Chauhan J., Prathibha M.D., Singh P. et al.: Plant photosynthesis under abiotic stresses: damages, adaptive, and signaling mechanisms. - Plant Stress 10: 100296, 2023. Go to original source...
    9. Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. - Ann. Bot.-London 103: 551-560, 2009. Go to original source...
    10. Chen H.-X., Li W.-J., An S.-Z., Gao X.-Y.: Characterization of PSII photochemistry and thermostability in salt-treated Rumex leaves. - J. Plant Physiol. 161: 257-264, 2004. Go to original source...
    11. Chen T.H.H., Murata N.: Glycinebetaine: an effective protectant against abiotic stress in plants. - Trends Plant Sci. 13: 499-505, 2008. Go to original source...
    12. Clifford S.C., Arndt S.K., Corlett J.E. et al.: The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance in Ziziphus mauritiana (Lamk.). - J. Exp. Bot. 49: 967-977, 1998. Go to original source...
    13. Coast O., Posch B.C., Rognoni B.G.: Wheat photosystem II heat tolerance: evidence for genotype-by-environment interactions. - Plant J. 111: 1368-1382, 2022. Go to original source...
    14. Darkó É., Janda T., Majláth I. et al.: Salt stress response of wheat-barley addition lines carrying chromosomes from the winter barley "Manas". - Euphytica 203: 491-504, 2015. Go to original source...
    15. Dau H.: New trends in photobiology: Short-term adaptation of plants to changing light intensities and its relation to Photosystem II photochemistry and fluorescence emission. - J. Photoch. Photobio. B 26: 3-27, 1994. Go to original source...
    16. Demmig B., Winter K., Krüger A., Czygan F.C.: Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. - Plant Physiol. 87: 17-24, 1988. Go to original source...
    17. Demmig-Adams B.: Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. - BBA-Bioenergetics 1020: 1-24, 1990. Go to original source...
    18. Demmig-Adams B., Stewart J.J., López-Pozo M. et al.: Zeaxanthin, a molecule for photoprotection in many different environments. - Molecules 25: 5825, 2020. Go to original source...
    19. dos Santos T.B., Ribas A.F., de Souza S.G.H. et al.: Physiological responses to drought, salinity, and heat stress in plants: a review. - Stresses 2: 113-135, 2022.
    20. Dulai S., Molnár I., Lehoczki E.: Effects of growth temperatures of 5 and 25°C on long-term responses of photosystem II to heat stress in atrazine-resistant and susceptible biotypes of Erigeron canadensis. - Aust. J. Plant Physiol. 25: 145-153, 1998. Go to original source...
    21. Dulai S., Molnár I., Szopkó D. et al.: Wheat-Aegilops biuncialis amphiploids have efficient photosynthesis and biomass production during osmotic stress. - J. Plant Physiol. 171: 509-517, 2014. Go to original source...
    22. Dulai S., Molnár I., Prónay J. et al.: Effects of drought on thermal stability of photosynthetic apparatus in bread wheat and Aegilops species originating from various habitats. - Acta Biol. Szeged. 49: 215-217, 2005.
    23. Dulai S., Molnár I., Prónay J. et al.: Effects of drought on photosynthetic parameters and heat stability of PSII in wheat and in Aegilops species originating from dry habitats. - Acta Biol. Szeged. 50: 11-17, 2006.
    24. El Sabagh A., Islam M.S., Skalicky M. et al.: Salinity stress in wheat (Triticum aestivum L.) in the changing climate: adaptation and management strategies. - Front. Agron. 3: 661932, 2021. Go to original source...
    25. Guo Q., Liu L., Barkla B.J.: Membrane lipid remodeling in response to salinity. - Int. J. Mol. Sci. 20: 4264, 2019. Go to original source...
    26. Flexas J., Bota J., Galmés J. et al.: Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. - Physiol. Plantarum 127: 343-352, 2006. Go to original source...
    27. Flexas J., Bota J., Loreto F. et al.: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. - Plant Biol. 6: 269-279, 2004. Go to original source...
    28. Havaux M.: Stress tolerance of photosystem II in vivo: antagonistic effects of water, heat, and photoinhibition stresses. - Plant Physiol. 100: 424-432, 1992. Go to original source...
    29. Havaux M., Tardy F.: Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. - Planta 198: 324-333, 1996. Go to original source...
    30. Havaux M., Tardy F., Ravenel J. et al.: Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. - Plant Cell Environ. 19: 1359-1368, 1996. Go to original source...
    31. Hemker F., Zielasek F., Jahns P.: Combined high light and salt stress enhances accumulation of PsbS and zeaxanthin in Chlamydomonas reinhardtii. - Physiol. Plantarum 176: e14233, 2024. Go to original source...
    32. Hill R., Ulstrup K.E., Ralph P.J.: Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. - B. Mar. Sci. 85: 223-244, 2009.
    33. Horton P., Ruban A.V., Rees D. et al.: Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. - FEBS Lett. 292: 1-4, 1991. Go to original source...
    34. Jahns P., Holzwarth A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. - BBA-Bioenergetics 1817: 182-193, 2012. Go to original source...
    35. Jat M., Ray M., Ahmad M.A., Prakash P.: Unravelling the photosynthetic dynamics and fluorescence parameters under ameliorative effects of 24-epibrassinolide in wheat (Triticum aestivum L.) grown under heat stress regime. - Sci. Rep.-UK 14: 30745, 2024. Go to original source...
    36. Jiang Z., van Zanten M., Sasidharan R.: Mechanisms of plant acclimation to multiple abiotic stresses. - Commun. Biol. 8: 655, 2025. Go to original source...
    37. Kalaji H.M., Govindjee, Bosa K. et al.: Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. - Environ. Exp. Bot. 73: 64-72, 2011. Go to original source...
    38. Kaur G., Sanwal S.K., Kumar A. et al.: Role of osmolytes dynamics in plant metabolism to cope with salinity induced osmotic stress. - Discov. Agric. 2: 59, 2024. Go to original source...
    39. Khristin M.S., Smolova T.N., Kreslavski V.D.: Thermal stress, aggregation of chlorophyll-protein complexes, and light-dependent recovery of PSII activity in wheat seedlings. - Russ. J. Plant Physiol. 68: 867-872, 2021. Go to original source...
    40. Kiss A.Z., Ruban A.V., Horton P.: The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. - J. Biol. Chem. 283: 3972-3978, 2008. Go to original source...
    41. Klughammer C., Schreiber U.: Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. - PAM Appl. Notes 1: 27-35, 2008.
    42. Kouřil R., Lazár D., Ilík P. et al.: High-temperature induced chlorophyll fluorescence rise in plants at 40-50°C: experimental and theoretical approach. - Photosynth. Res. 81: 49-66, 2004. Go to original source...
    43. Ladjal M., Epron D., Ducrey M.: Effects of drought preconditioning on thermotolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings. -Tree Physiol. 20: 1235-1241, 2000. Go to original source...
    44. Lavaud J., Kroth P.: In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. - Plant Cell Physiol. 47: 1010-1016, 2006. Go to original source...
    45. Lawlor D.W., Cornic G.: Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. - Plant Cell Environ. 25: 275-294, 2002. Go to original source...
    46. Lazár D., Ilík P.: High-temperature induced chlorophyll fluorescence changes in barley leaves: comparison of the critical temperatures determined from fluorescence induction and from fluorescence temperature curve. - Plant Sci. 124: 159-164, 1997. Go to original source...
    47. Lazár D., Ilík P., Nauą J.: An appearance of K-peak in fluorescence induction depends on the acclimation of barley leaves to higher temperatures. - J. Lumin. 72-74: 595-596, 1997. Go to original source...
    48. Lu C., Li L., Liu X. et al.: Salt stress inhibits photosynthesis and destroys chloroplast structure by downregulating chloroplast development-related genes in Robinia pseudoacacia seedlings. - Plants-Basel 12: 1283, 2023. Go to original source...
    49. Lu C., Zhang J.: Effects of water stress on PSII photochemistry and its thermostability in wheat plants. - J. Exp. Bot. 50: 1199-1206, 1999. Go to original source...
    50. Mathur S., Mehta P., Jajoo A.: Effects of dual stress (high salt and high temperature) on the photochemical efficiency of wheat leaves (Triticum aestivum). - Physiol. Mol. Biol. Pla. 19: 179-188, 2013. Go to original source...
    51. Medrano H., Escalona J.M., Cifre J. et al.: A ten-year study on physiology of two Spanish grapevine cultivars under field conditions: effects of water availability from leaf photosynthesis to grape yield and quality. - Funct. Plant Biol. 30: 607-619, 2003. Go to original source...
    52. Mitchell D., Schönbeck L., Shah S., Santiago L.S.: Leaf drought and heat tolerance are integrated across three temperate biome types. - Sci. Rep.-UK 15: 12201, 2025. Go to original source...
    53. Molnár I., Gáspár L., Sárvári É. et al.: Physiological and morphological responses to water stress in Aegilops biuncialis and Triticum aestivum genotypes with differing tolerance to drought. - Funct. Plant. Biol. 31: 1149-1159, 2004. Go to original source...
    54. Molnár I., Csízi K., Dulai S. et al.: Light dependence of thermostability of photosynthetic apparatus. - In: Garab G. (ed.): Photosynthesis: Mechanisms and Effects. Pp. 2241-2244. Springer, Dordrecht 1998. Go to original source...
    55. Moloi M.J., Tóth C., Hafeez A., Tóth B.: Insights into the photosynthetic efficiency and chloroplast ultrastructure of heat-stressed edamame cultivars during the reproductive stages. - Agronomy 15: 301, 2025. Go to original source...
    56. Mondal S., Singh R.P., Crossa J. et al.: Earliness in wheat: a key to adaptation under terminal and continual high temperature stress in South Asia. - Field Crop. Res. 151: 19-26, 2013. Go to original source...
    57. Munns R.: Comparative physiology of salt and water stress. - Plant Cell Environ. 25: 239-250, 2002. Go to original source...
    58. Munns R., Tester M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
    59. Murata N., Mohanty P.S., Hayashi H., Papageorgiou G.C.: Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. - FEBS Lett. 296: 187-189, 1992. Go to original source...
    60. Müller P., Li X.-P., Niyogi K.K.: Non-photochemical quenching: a response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
    61. Nagy Z., Galiba G.: Drought and salt tolerance are not necessarily linked: a study on wheat varieties differing in drought resistance under consecutive water and salinity stresses. - J. Plant Physiol. 145: 168-174, 1995. Go to original source...
    62. Nash D., Miyao M., Murata N.: Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. - BBA-Bioenergetics 807: 127-133, 1985. Go to original source...
    63. Nauą J., Kuropatwa R., Klinkovský T. et al.: Heat injury of barley leaves detected by the chlorophyll fluorescence temperature curve. - BBA-Bioenergetics 1101: 359-362, 1992. Go to original source...
    64. Ozturk M., Unal B.T., García-Caparrós P. et al.: Osmoregulation and its actions during the drought stress in plants. - Physiol. Plantarum 172: 1321-1335, 2021. Go to original source...
    65. Pshybytko N.L., Kruk J., Kabashnikova L.F., Strzalka K. et al.: Function of plastoquinone in heat stress reactions of plants. - BBA-Bioenergetics 1777: 1393-1399, 2008. Go to original source...
    66. Raison J.K., Roberts J.K.M., Berry J.A.: Correlation between the thermal stability of chloroplast (thylakoid) membranes and the composition and fluidity of their polar lipids upon acclimation of the higher plant, Nerium oleander, to growth temperature. - BBA-Biomembranes 688: 218-228, 1982. Go to original source...
    67. Ramakers L.A.I., Harbinson J., Wientjes E., van Amerongen H.: Unravelling the different components of nonphotochemical quenching using a novel analytical pipeline. - New Phytol. 245: 625-636, 2025. Go to original source...
    68. Rehman S., Yang J., Zhang J. et al.: Salt stress in wheat: a physiological and genetic perspective. - Plant Stress 16: 100832, 2025. Go to original source...
    69. Ribeiro R.V., Santos M.G., Machado E.C., Oliveira R.F.: Photochemical heat-shock response in common bean leaves as affected by previous water deficit. - Russ. J. Plant Physiol. 55: 350-358, 2008. Go to original source...
    70. Schreiber U., Berry J.A.: Heat-induced changes of chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. - Planta 136: 233-238, 1977. Go to original source...
    71. Schreiber U., Bilger W.: Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. - In: Tenhunen J.D., Cararino F.M., Lange O.L., Oechel W.D. (ed.): Plant Response to Stress. NATO ASI Series. Vol. 15. Pp. 27-53. Springer, Berlin-Heidelberg 1987. Go to original source...
    72. Shanker A.K., Amirineni S., Bhanu D. et al.: High-resolution dissection of photosystem II electron transport reveals differential response to water deficit and heat stress in isolation and combination in pearl millet [Pennisetum glaucum (L.) R. Br.]. - Front. Plant Sci. 13: 892676, 2022. Go to original source...
    73. Sharkey T.D.: Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. - Plant Cell Environ. 28: 269-277, 2005. Go to original source...
    74. Shu S., Yuan Y., Chen J. et al.: The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress. - Sci. Rep.-UK 5: 14390, 2015. Go to original source...
    75. Smirnoff N.: The role of active oxygen in response of plants to water deficit and desiccation. - New Phytol. 125: 27-58, 1993. Go to original source...
    76. Stefanov M.A., Rashkov G.D., Borisova P.B., Apostolova E.L.: Changes in photosystem II complex and physiological activities in pea and maize plants in response to salt stress. - Plants-Basel 13: 1025, 2024. Go to original source...
    77. Sun Y., Wang Q., Xiao H., Cheng J.: Low light facilitates cyclic electron flows around PSI to assist PSII against high temperature stress. - Plants-Basel 11: 3537, 2022. Go to original source...
    78. Suzuki N., Rivero R.M., Shulaev V. et al.: Abiotic and biotic stress combinations. - New Phytol. 203: 32-43, 2014. Go to original source...
    79. Szopkó D., Darkó É., Molnár I. et al.: Photosynthetic responses of a wheat (Asakaze)-barley (Manas) 7H addition line to salt stress. - Photosynthetica 55: 317-328, 2017. Go to original source...
    80. Szopkó D., Dulai S.: Environmental factors affecting the heat stability of the photosynthetic apparatus. - Acta Biol. Plant. Agr. 6: 90-107, 2018. Go to original source...
    81. Tang Y., Wen X., Lu Q. et al.: Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. - Plant Physiol. 143: 629-638, 2007. Go to original source...
    82. Tardy F., Havaux M.: Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. - BBA-Biomembranes 1330: 179-193, 1997. Go to original source...
    83. Tóth S., Puthur J.T., Nagy V., Garab G.: Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygen-evolving complexes. - Plant Physiol. 149: 1568-1578, 2009. Go to original source...
    84. Tóth S., Schansker G., Garab G., Strasser R.J.: Photosynthetic electron transport activity in heat-treated barley leaves: the role of internal alternative electron donors to photosystem II. -BBA-Bioenergetics 1767: 295-305, 2007. Go to original source...
    85. Touchette B.W., Schmitt S.R., Moody J.W.G.: Enhanced thermotolerance of photosystem II by elevated pore-water salinity in the coastal marsh graminoid Sporobolus pumilus. -Aquat. Biol. 29: 111-122, 2020. Go to original source...
    86. Urban L., Aarrouf J., Bidel L.P.R.: Assessing the effects of water deficit on photosynthesis using parameters derived from measurements of leaf gas exchange and of chlorophyll a fluorescence. - Front. Plant Sci. 8: 2068, 2017. Go to original source...
    87. Vani B., Saradhi P., Mohanty P.: Alteration in chloroplast structure and thylakoid membrane composition due to in vivo heat treatment of rice seedlings: correlation with the functional changes. - J. Plant Physiol. 158: 583-592, 2001. Go to original source...
    88. Vineeth T.V., Krishna G.K., Pandesha P.H. et al.: Photosynthetic machinery under salinity stress: trepidations and adaptive mechanisms. - Photosynthetica 61: 73-93, 2023. Go to original source...
    89. Wang G.P., Li F., Zhang J. et al.: Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. - Photosynthetica 48: 30-41, 2010. Go to original source...
    90. Wang Q.-L., Chen J.-H., He N.-Y., Guo F.-Q.: Metabolic reprogramming in chloroplasts under heat stress in plants. - Int. J. Mol. Sci. 19: 849, 2018. Go to original source...
    91. Wang X., Chen Z., Sui N.: Sensitivity and responses of chloroplasts to salt stress in plants. - Front. Plant Sci. 15: 1374086, 2024. Go to original source...
    92. Wen X., Qiu N., Lu Q., Lu C.: Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. - Planta 220: 486-497, 2005. Go to original source...
    93. Yamane Y., Kashino Y., Koike H., Satoh K.: Increases in the fluorescence F0 level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants. - Photosynth. Res. 52: 57-64, 1997. Go to original source...
    94. Yan K., Chen P., Shao H. et al.: Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum. - J. Agron. Crop Sci. 198: 218-225, 2012. Go to original source...
    95. Yang X., Lu M., Wang Y. et al.: Response mechanism of plants to drought stress. - Horticulturae 7: 50, 2021. Go to original source...
    96. Yang Z., Li J.-L., Liu L.-N. et al.: Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum. - Front. Plant Sci. 10: 1722, 2020. Go to original source...
    97. Zahra N., Hafeez M.B., Ghaffar A. et al.: Plant photosynthesis under heat stress: effects and management. - Environ. Exp. Bot. 206: 105178, 2023. Go to original source...

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