The reactions of the photosynthetic apparatus of the flag leaf of different varieties of winter bread wheat (Triticum aestivum L.) to soil drought, high temperature and their combined effect both under soil moisture deficiency action and at the recovery period after the normal watering resumption were studied, in order to identify the most informative indices of adaptability of wheat varieties to adverse environmental factors. The experiments were performed with plants of the varieties Yednist, Podilska Nyva and Darunok Podillya grown in pot culture under natural light and temperature conditions. The pots (10 kg of soil) were watered daily to maintain the soil moisture level at 70 % of field capacity (FC). Drought treatment was applied to one half of pots by lowering soil moisture content to 30 % FC for seven days during earing-flowering. After that, watering of experimental plants was resumed to the level of control. Measuring of CO2 assimilation and transpiration rate of the flag leaf of the control and treated plants at a temperature of 25 and 42 oC and leaf tissues sampling for physiological and biochemical indices evaluation were performed on the first day of soil moisture reduction to 30 % FC, on the seventh day at this level of soil moisture and a week after the resumption of optimal watering. On the first day of drought at 30 % FC, it was found significant decrease in relative water content (RWC), CO2 assimilation and transpiration rates for all varieties and a tendency to decrease in chlorophyll content for varieties Podilska Nyva and Darunok Podillya. On the seventh day of the drought, the RWC in all varieties declined more, the chlorophyll content decreased significantly, however the degree of inhibition of CO2 assimilation and transpiration reduced for varieties Yednist and Podilska Nyva and remained at the same level in Darunok Podillya. On the seventh day of optimal watering renewal, the CO2 assimilation rate in treated plants of all varieties was restored to the level of control despite the significantly lower chlorophyll content. The increase in temperature to 42 oC severely reduced the CO2 assimilation rate in both control and experimental plants. However, the degree of photosynthesis reduction in treated plants was much greater than in control at the beginning of the drought, but heat resistance of photosynthesis of stressed plants of all varieties did not differ with control after 7 days of water deficit, and was even higher than control on the seventh day of optimal watering renewal, indicating the formation of cross-tolerance of the photosynthetic apparatus to high temperature in plants under drought. The increase in the activity of antioxidant enzymes of chloroplasts superoxide dismutase and ascorbate peroxidase in the leaves of stressed plants was detected. The ratio of the values of photosynthetic apparatus activity and productivity indices of treated plants to control ones was the most informative for the phenotyping of wheat varieties by drought and heat resistance. According to the set of physiological indices defined in our work, the studied varieties can be arranged in the following order of increased drought- and heat-tolerance: Darunok Podillya < Podilska Nyva < Yednist.
Keywords: Triticum aestivum L., drought, high temperature stress, photosynthesis, transpiration, cross-adaptation, antioxidant enzymes, productivity
Full text and supplemented materials
Free full text: PDFReferences
1. 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].
2. Lesk, C., Rowhani, P. & Ramankutty, N. (2016). Influence of extreme weather disasters on global crop production. Nature, 529, No. 7584, pp. 84-87. https://doi.org/10.1038/nature16467
3. Pequeno, D.N.L., Hernandez-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
4. Morgun, V.V. (2017). Contribution of plant physiology and genetics to food security of our country. In: Plant Physiology: Achievements and new directions of development, Vol. 1 (pp. 9-13), Logos, Kyiv [in Ukrainian].
5. Senapati, N., Stratonovitch, P., Paul, M.J. & Semenov, M.A. (2019). Drought tolerance during reproductive development is important for increasing wheat yield potential under climate change in Europe. J. Exp. Bot., 70, No. 9, pp. 2549-2560. https://doi.org/10.1093/jxb/ery226
6. Lopes, M.S., Rebetzke, G.J. & Reynolds, M. (2014). Integration of phenotyping and genetic platforms for a better understanding of wheat performance under drought. J. Exp. Bot., 65, No. 21, pp. 6167-6177. https://doi.org/10.1093/jxb/eru384
7. Ghodke, P.H., Ramakrishnan, S., Shirsat, D.V., Vani, G.K. & Arora, A. (2019). Morphological characterization of wheat genotypes for stay green and physiological traits by multivariate analysis under drought stress. Plant Physiol. Rep., 24, No. 3, pp. 305-315. https://doi.org/10.1007/s40502-019-00458-8
8. Ahanger, M.A., Siddique, K.H.M. & Ahmad, P. (2021). Understanding drought tolerance in plants. Physiol. Plant., 172, No. 2, pp. 286-288. https://doi.org/10.1111/ppl.13442
9. Feller, U. (2016). Drought stress and carbon assimilation in a warming climate: Reversible and irreversible impacts. J. Plant Physiol., 203, pp. 84-94. https://doi.org/10.1016/j.jplph.2016.04.002
10. Kiriziy, D.A., Stasik, O.O., Pryadkina, G.A. & Shadchina, T.M. (2014). Photosynthesis, Vol. 2, Assimilation of CO2 and the mechanisms of its regulation. Logos, Kyiv [in Russian].
11. Abid, M., Ali, S., Qi, L.K., Zahoor, R., Tian, Z., Jiang, D., Snider, J.L. & Dai, T. (2018). Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Sci. Rep., 8, pp. 1-15. https://doi.org/10.1038/s41598-018-21441-7
12. 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
13. Morales, F., Ancin, M., Fakhet, D., Gonzalez-Torralba, J., Gamez, A.L., Seminario, A., Soba, D., Mariem, S.B., Garriga, M. & Aranjuelo, I. (2020). Photosynthetic metabolism under stressful growth conditions as a bases for crop breeding and yield improvement. Plants, 9, No. 1, p. 88. https://doi.org/10.3390/plants9010088
14. Krieger-Liszkay, A., Krupinska, K. & Shimakawa, G. (2019). The impact of photosynthesis on initiation of leaf senescence. Physiol. Plant., 166, pp. 148-164. https://doi.org/10.1111/ppl.12921
15. 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
16. Riaz, M.W., Yang, L., Yousaf, M.I., Sami, A., Mei, X.D., Shah, L., Rehman, S., Xue, L., Si, H. & Ma, C. (2021). Effects of heat stress on growth, physiology of plants, yield and grain quality of different spring wheat (Triticum aestivum L.) genotypes. Sustainability, 13, p. 2972. https://doi.org/10.3390/su13052972
17. Busch, F.A. & Sage, R.F. (2017). The sensitivity of photosynthesis to O2 and CO2 concentration identifies strong Rubisco control above the thermal optimum. New Phytologist, 213, No. 3, pp. 1036-1051. https://doi.org/10.1111/nph.14258
18. Cohen, I., Zandalinas, S.I., Huck, C., Fritschi, F.B. & Mittler, R. (2021). Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiol. Plant., 171, No. 1, pp. 66-76. https://doi.org/10.1111/ppl.13203
19. Zandalinas, S.I., Mittler, R., Balfagon, D., Arbona, V. & Gomez-Cadenas, A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiol. Plant., 162, pp. 2-12. https://doi.org/10.1111/ppl.12540
20. 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
21. 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, p. 364. https://doi.org/10.3390/agronomy11020364
22. Zhang, X. & Huang, B. (2020). Drought priming-induced heat tolerance: Metabolic pathways and molecular mechanisms. In: Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants (pp. 149-160), Elsevier Inc. https://doi.org/10.1016/B978-0-12-817892-8.00009-X
23. Wang, X., Liu, F. & Jiang, D. (2017) Priming: a promising strategy for crop production in response to future climate. J. Integr. Agric., 16, No. 12, pp. 2709-2716. https://doi.org/10.1016/S2095-3119(17)61786-6
24. Mokronosov, A.T. & Kovalev, A.G. (Eds.). (1989). Photosynthesis and Bioproductivity: Methods of Determination. Agropromizdat, Moskow [in Russian].
25. Shmatko, I. G., Grigoryuk, I. A., Shvedova, O. E. & Petrenko, N. I. (1985). Determination of the physiological reaction of cereals to deterioration of water availability and temperature increase. IPPG, Kiev [in Russian].
26. Wellburn, A.R. (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol., 144, pp. 307-313. https://doi.org/10.1016/S0176-1617(11)81192-2
27. Giannopolitis, C.N. & Ries, S.K. (1977). Superoxide dismutase. Occurrence in higher plants. Plant Physiol., 59, No. 2, pp. 309-314. https://doi.org/10.1104/pp.59.2.309
28. Chen, G.-X. & Asada, K. (1989). Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol., 30, No. 7, pp. 987-998. https://doi.org/10.1093/oxfordjournals.pcp.a077844
29. Arnon, D.I. (1949). Copper enzyme in isolated chloroplasts. Polyphenolooxidase in Beta vulgaris. Plant. Physiol., 24, No. 1, pp. 1-5. https://doi.org/10.1104/pp.24.1.1
30. Stasik, O.O., Kiriziy, D.A., Sokolovska-Sergiienko, O.G. & Bondarenko, O.Yu. (2020). Influence of drought on the photosynthetic apparatus activity, senescence rate, and productivity in wheat plants. Fiziol. rast. genet., 52, No. 5, pp. 371-387. https://doi.org/10.15407/frg2020.05.371
31. 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
32. Wang, X., Vignjevic, M., Liu, F., Jacobsen, S., Jiang, D. & Wollenweber, B. (2015). Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul., 75, pp. 677-687. https://doi.org/10.1007/s10725-014-9969-x
33. Llorens, E., Gonzalez-Hernandez, A.I., Scalschi, L., Fernandez-Crespo, E., Camanes, G., Vicedo, B. & Garcia-Agustin, P. (2020). Priming mediated stress and cross-stress tolerance in plants: concepts and opportunities. In: Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants (pp. 1-20), New York: Acad. Press. https://doi.org/10.1016/B978-0-12-817892-8.00001-5
34. 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
35. Kolupaev, Yu.E. & Oboznyi, A.I. (2013). Reactive oxygen species and antioxidative system at cross adaptation of plants to activity of abiotic stressors. Visn. Hark. nac. agrar. univ., Ser. Biol., Iss. 3, pp. 18-31.
36. Perez, I.B. & Brown, P.J. (2014). The role of ROS signaling in cross-tolerance: from model to crop. Frontiers in Plant Science, 5, p. 754. https://doi.org/10.3389/fpls.2014.00754
37. Taran, N.Yu., Okanenko, O.A., Batsmanova, L.M. & Musienko, M.M. (2004). Secondary oxidative stress as an element of the general adaptive response to unfavourable environment action. Physiol. biochem. cult. plants, 36, No. 1, pp. 3-14 [in Ukrainian].
38. 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
39. 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
40. Sun, M., Jiang, F., Cen, B., Wen, J., Zhou, Y. & Wu, Z. (2018). Respiratory burst oxidase homologue-dependent H2O2 and chloroplast H2O2 are essential for the maintenance of acquired thermotolerance during recovery after acclimation. Plant, Cell & Envion., 41, No. 10, pp. 2373-2389. https://doi.org/10.1111/pce.13351
41. Snider, J.L., Oosterhuis, D.M. & Kawakami, E.M. (2010). Genotypic differences in thermotolerance are dependent upon prestress capacity for antioxidant protection of the photosynthetic apparatus in Gossypium hirsutum. Physiol. Plant., 138, No. 3, pp. 268-277. https://doi.org/10.1111/j.1399-3054.2009.01325.x
42. Radchenko, M., Sychuk, A. & Morderer, Ye. (2014). Decrease of the herbicide fenoxaprop phytotoxicity in the drought condition: the role of antioxidant enzymatic system. Journal of Plant Protection Research, 54, No. 4, pp. 390-394. https://doi.org/10.2478/jppr-2014-0058