Fiziol. rast. genet. 2024, vol. 56, no. 3, 230-253, doi: https://doi.org/10.15407/frg2024.03.230

Features of light induction of gas exchange in wheat leaves under drought of different duration and during the recovery period

Kiriziy D.A., Kedruk A.S., Sokolov­ska-Sergiienko О.G., Makharynska N.M., Stasik O.O.

  • Institute of Plant Physiology and Genetics, National Academy of Sciences of Ukraine 31/17 Vasylkivska St., Kyiv, 03022, Ukraine

In order to find ways to further improve the functioning of photosynthetic and stomatal apparatus under changing environmental conditions, the peculiarities of induction processes dynamics of CO2 and H2O gas exchange parameters in flag leaves of wheat plants of two genotypes contrasting in drought resistance were investigated at changes in lighting both under drought conditions and during the recovery period. Plants of winter bread wheat varieties Chygyrynka and Sofia Kyivska were grown under the conditions of pot experiment. Temperature and lighting were natural. The plants were subjected to a 7-day drought (30 % FC) during the flowering period. After that, the soil moisture in the pots with experimental plants was restored to the control level (70 % FC), which was maintained until the end of the growing season. Induction curves of flag leaves photosynthesis and transpiration were recorded after keeping them in the dark for 30 minutes. At the end of this period, the dark respiration rate was recorded and the light was turned on. CO2 and H2O gas exchange indices were recorded at 10-minute intervals. The total lighting time was 60 minutes. Genotypic differences in the dynamics of CO2 assimilation and transpiration induction in winter wheat leaves during the transition from darkness to light were revealed. Drought had a significant effect on the induction dynamics, in particular, it reduced the increase in gas exchange rate and its final value under light saturation, while genotypic differences were more contrasted. The photosynthetic apparatus of wheat leaves of the drought-tolerant variety (Sofia Kyivska) was able to adapt to short-term moderate drought and recover almost completely after its termination. In the sensitive variety (Chygyrynka), this ability was expressed less, which led to a significant decrease in grain productivity of plants. It was found that suppression of CO2 assimilation rate in wheat leaves under drought conditions was more due to its negative effect on the photosynthetic apparatus of the mesophyll cells than on the functioning of the stomata. The water use efficiency during photosynthesis decreases in plants exposed to stressor. In the drought-tolerant variety, this index quickly recovered to the control level, and in the sensitive variety, it remained significantly lower even a week after the end of the drought.

Keywords: Triticum aestivum L., winter bread wheat, drought, photosynthesis, transpiration, light induction, productivity

Fiziol. rast. genet.
2024, vol. 56, no. 3, 230-253

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References

1. Ray, D.K., Ramankutty, N., Mueller, N.D., West, P.C. & Foley, J.A. (2012). Recent patterns of crop yield growth and stagnation. Nature Comm., 3, 1293. https://doi.org/10.1038/ncomms2296

2. Ray, D.K., Mueller, N.D., West, P.C. & Foley, J.A. (2013). Yield trends are insufficient to double global crop production by 2050. PLoS One, 8, e66428. https://doi.org/10.1371/journal.pone.0066428

3. Long, S.P., Marshall-Colon, A. & Zhu, X.G. (2015). Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 161, pp. 56-66. https://doi.org/10.1016/j.cell.2015.03.019

4. Carmo-Silva, E., Andralojc, P.J., Scales, J.C., Driever, S.M., Mead, A., Lawson, T., Raines, C.A. & Parry, M.A.J. (2017). Phenotyping of field-grown wheat in the UK highlights contribution of light response of photosynthesis and flag leaf longevity to grain yield. J. Exp. Bot., 68, pp. 3473-3486. https://doi.org/10.1093/jxb/erx169

5. Sanchez-Bragado, R., Elazab, A., Zhou, B.W., Serret, M.D., Bort, J., Nieto-Taladriz, M.T. & Araus, J.L. (2014). Contribution of the ear and the flag leaf to grain filling in durum wheat inferred from the carbon isotope signature: genotypic and growing conditions effects. J. Int. Plant Biol., 56, pp. 444-454. https://doi.org/10.1111/jipb.12106

6. Murchie, E.H., Reynolds, M., Slafer, G.A., Foulkes, M.J., Acevedo-Siaca, L., McAusland, L., Sharwood, R., Griffiths, S., Flavell, R.B., Gwyn, J., Sawkins, M. & Carmo-Silva, E.A. (2023). Wiring diagram for source strength traits impacting wheat yield potential. J. Exp. Bot., 74 (1), pp. 72-90. https://doi.org/10.1093/jxb/erac415

7. Slattery, R.A., Walker, B.J., Weber, A.P. & Ort, D.R. (2018). The impacts of fluctuating light on crop performance. Plant Physiol., 176, pp. 990-1003. https://doi.org/10.1104/pp.17.01234

8. Tanaka, Y., Adachi, S. & Yamori, W. (2019). Natural genetic variation of the photosynthetic induction response to fluctuating light environment. Curr. Opinion Plant Biol., 49, pp. 52-59. https://doi.org/10.1016/j.pbi.2019.04.010

9. Taylor, S.H. & Long, S.P. (2017). Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21 % of productivity. Philosoph. Transact. Royal Society B, Biol. Sci., 372 (1730), 20160543. https://doi.org/10.1098/rstb.2016.0543

10. Wang, Y., Burgess, S.J., de Becker, E.M. & Long, S.P. (2020). Photosynthesis in the fleeting shadows: an overlooked opportunity for increasing crop productivity? Plant J., 101 (4), pp. 874-884. https://doi.org/10.1111/tpj.14663

11. Deans, R.M., Farquhar, G.D. & Busch, F.A. (2019). Estimating stomatal and biochemical limitations during photosynthetic induction. Plant, Cell Env., 42, pp. 3227-3240. https://doi.org/10.1111/pce.13622

12. Acevedo-Siaca, L., Coe, R., Quick, W.P. & Long, S.P. (2021). Variation between rice accessions in photosynthetic induction in flag leaves and underlying mechanisms. J. Exp. Bot., 72 (4), pp. 1282-1294. https://doi.org/10.1093/jxb/eraa520

13. Taylor, S.H., Gonzalez-Escobar, E., Page, R., Parry, M.A.J., Long, S.P. & Carmo-Silva, E. (2022). Faster than expected Rubisco deactivation in shade reduces cowpea photosynthetic potential in variable light conditions. Nature Plants, 8, pp. 118-124. https://doi.org/10.1038/s41477-021-01068-9

14. Salter, W.T., Merchant, A.M., Richards, R.A., Trethowan, R. & Buckley, T.N. (2019). Rate of photosynthetic induction in fluctuating light varies widely among genotypes of wheat. J. Exp. Bot., 70(10), pp. 2787-2796. https://doi.org/10.1093/jxb/erz100

15. Soleh, M.A., Tanaka, Y., Nomoto, Y., Iwahashi, Y., Nakashima, K., Fukuda, Y., Long, S.P. & Shiraiwa, T. (2016). Factors underlying genotypic differences in the induction of photosynthesis in soybean Glycine max (L.) Merr. Plant, Cell and Env., 39, pp. 685-693. https://doi.org/10.1111/pce.12674

16. Deans, R.M., Brodribb, T.J., Busch, F.A. & Farquhar, G.D. (2019). Plant water use strategy mediates stomatal effects on the light induction of photosynthesis. New Phytol., 222, pp. 382-395. https://doi.org/10.1111/nph.15572

17. McAusland, L., Vialet-Chabrand, S., Davey, P., Baker, N.R., Brendel, O. & Lawson, T. (2016). Effects of kinetics of light-induced stomatal responses on photosynthesis and water use efficiency. New Phytol., 211, pp. 1209-1220. https://doi.org/10.1111/nph.14000

18. Zhang, Q., Peng, S. & Li, Y. (2019). Increase rate of light-induced stomatal conductance is related to stomatal size in the genus Oryza. J. Exp. Bot., 70 (19), pp. 5259-5269. https://doi.org/10.1093/jxb/erz267

19. Sakoda, K., Yamori, W., Groszmann, M. & Evans, J.R. (2021). Stomatal, mesophyll conductance, and biochemical limitations to photosynthesis during induction. Plant Physiol., 185 (1), pp. 146-160. https://doi.org/10.1093/plphys/kiaa011

20. Kaiser, E., Morales, A., Harbinson, J., Heuvelink, E., Prinzenberg, A.E. & Marcelis, L.F.M. (2016). Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana. Sci. Rep., 6, 31252. https://doi.org/10.1038/srep31252

21. Faralli, M., Cockram, J., Ober, E., Wall, S., Galle, A., Van Rie, J., Raines, C. & Lawson, T. (2019). Genotypic, developmental and environmental effects on the rapidity of gs in wheat: Impacts on carbon gain and water-use efficiency. Front. Plant Sci., 10, 492. https://doi.org/10.3389/fpls.2019.00492

22. Taylor, S.H., Orr, D.J., Carmo-Silva, E. & Long, S.P. (2020). During photosynthetic induction, biochemical and stomatal limitations differ between Brassica crops. Plant, Cell Env., 43, pp. 2623-2636. https://doi.org/10.1111/pce.13862

23. Murchie, E.H., Kefauver, S., Araus, J.L., Muller, O., Rascher, U., Flood, P.J. & Lawson, T. (2018). Measuring the dynamic photosynthome. Ann. Bot., 122 (2), pp. 207-220. https://doi.org/10.1093/aob/mcy087

24. Kaiser, E., Morales, A. & Harbinson, J. (2018). Fluctuating light takes crop photosynthesis on a rollercoaster ride. Plant Physiol., 176, pp. 977-989. https://doi.org/10.1104/pp.17.01250

25. Lawson, T. & Vialet-Chabrand, S. (2019). Speedy stomata, photosynthesis and plant water use efficiency. New Phytol., 221 (1), pp. 93-98. https://doi.org/10.1111/nph.15330

26. Kromdijk, J., GYowacka, 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. Sci., 354, pp. 857-861. https://doi.org/10.1126/science.aai8878

27. Faralli, M., Matthews, J. & Lawson, T. (2019). Exploiting natural variation and genetic manipulation of stomatal conductance for crop improvement. Curr. Opinion Plant Biol., 49, pp. 1-7. https://doi.org/10.1016/j.pbi.2019.01.003

28. Long, S.P., Taylor, S.H., Burgess, S.J., Carmo-Silva, E., Lawson, T., De Souza, A.P., Leonelli, L. & Wang, Y. (2022). Into the shadows and back into sunlight: Photosynthesis in fluctuating light. Ann. Rev. Plant Biol., 73, pp. 617-648. https://doi.org/10.1146/annurev-arplant-070221-024745

29. Eyland, D., van Wesemael, J., Lawson, T. & Carpentier, S. (2021). The impact of slow stomatal kinetics on photosynthesis and water use efficiency under fluctuating light. Plant Physiol., 186 (2), pp. 998-1012. https://doi.org/10.1093/plphys/kiab114

30. Vialet-Chabrand, S., Matthews, J.S.A., Simkin, A.J., Raines, C.A. & Lawson, T. (2017). Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol., 173 (4), pp. 2163-2179. https://doi.org/10.1104/pp.16.01767

31. Yamori, W., Kusumi, K., Iba, K. & Terashima, I. (2020). Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice. Plant Cell Env., 43, pp. 1230-1240. https://doi.org/10.1111/pce.13725

32. 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. Regul. Mechan. Bio., 10 (1), pp. 12-21. https://doi.org/10.15421/021903

33. 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].

34. 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. Plant Physiol., 144, pp. 307-313. https://doi.org/10.1016/S0176-1617(11)81192-2

35. Laisk, A. & Oja, V. (1998). Dynamics of leaf photosynthesis: rapid response measurements and their interpretations. Collingwood, CSIRO Publishing. https://doi.org/10.1071/9780643105294

36. Giannopolitis, C.N. & Ries, S.K. (1977). Superoxide dismutase. Occurrence in higher plants. Plant Physiol., 59 (2), pp. 309-314. https://doi.org/10.1104/pp.59.2.309

37. 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 and Cell Physiol., 30, pp. 987-998. https://doi.org/10.1093/oxfordjournals.pcp.a077844

38. Yan, Y., Ryu, Y., Dechant, B., Li, B. & Kim, J. (2023) Dark respiration explains nocturnal stomatal conductance in rice regardless of drought and nutrient stress. Plant, Cell & Env., 46, pp. 3748-3759. https://doi.org/10.1111/pce.14710

39. Zhang, J., Chen, X., Song, Y. & Gong, Z. (2024). Integrative regulatory mechanisms of stomatal movements under changing climate. J. Integr. Plant Biol., 66, No. 3, pp. 368-393. https://doi.org/10.1111/jipb.13611

40. Amaral, J., Lobo, A.K.M. & Carmo-Silva, E. (2024). Regulation of Rubisco activity in crops. New Phytol., 241, pp. 35-51. https://doi.org/10.1111/nph.19369

41. Zahra, N., Hafeez, M.B., Kausar, A., Al Zeidi, M., Asekova, S., Siddique, K. H. & Farooq, M. (2023). Plant photosynthetic responses under drought stress: Effects and management. J. Agr. Crop Sci., 209 (5), pp. 651-672. https://doi.org/10.1111/jac.12652

42. 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

43. Sade, N., del Mar Rubio-Wilhelmi, M., Umnajkitikorn, K. & Blumwald, E. (2018). Stress-induced senescence and plant tolerance to abiotic stress. J. Exp. Bot., 69, No. 4, pp. 845-853. https://doi.org/10.1093/jxb/erx235

44. 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

45. Have, M., Marmagne, A., Chardon, F. & Masclaux-Daubresse, C. (2017). Nitrogen remobilization during leaf senescence: lessons from Arabidopsis to crops. J. Exp. Bot., 68, No. 10, pp. 2513-2529. https://doi.org/10.1093/jxb/erw365

46. Nunes, T.D.G., Zhang, D. & Raissig, M.T. (2020). Form, development and function of grass stomata. Plant J., 101, pp. 780-799. https://doi.org/10.1111/tpj.14552

47. Ehonen, S., Yarmolinsky, D., Kollist, H. & Kangasj¬rvi, J. (2019). Reactive oxygen species, photosynthesis, and environment in the regulation of stomata. Antioxidants & Redox Sign., 30, No. 9, pp. 1220-1237. https://doi.org/10.1089/ars.2017.7455

48. Henry, C., John, G.P., Pan, R., Bartlett, M.K., Fletcher, L.R., Scoffoni, C. & Sack, L. (2019). A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Comm., 10, 3398. https://doi.org/10.1038/s41467-019-11006-1

49. Walker, B.J., Kramer, D.M., Fisher, N. & Fu, X. (2020). Flexibility in the energy balancing network of photosynthesis enables safe operation under changing environmental conditions. Plants, 9, 301. https://doi.org/10.3390/plants9030301

50. Foyer, C. H. & Shigeoka, S. (2011). Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol., 155 (1), pp. 93-100. https://doi.org/10.1104/pp.110.166181

51. Endo, T. & Asada, K. (2008). Photosystem I and photoprotection: cyclic electron flow and water-water cycle. In: Demmig-Adams, B., Adams, W.W. & Mattoo, A.K. (Eds.). Photoprotection, Photoinhibition, Gene Reg. Env. (pp. 205-221), Dordrecht: Springer Sci., Business Media B.V. https://doi.org/10.1007/1-4020-3579-9_14

52. Sun, H., Yang, Y.-J. & Huang, W. (2020). The water-water cycle is more effective in regulating redox state of photosystem I under fluctuating light than cyclic electron transport. Biochim. Biophys. Acta. Bio., 1861, 148235. https://doi.org/10.1016/j.bbabio.2020.148235

53. Endres, L., Silva, J.V., Ferreira, V.M. & de Souza Barbosa, G. (2010). Photosynthesis and water relations in brazilian sugarcane. Open Agricult. J., 4 (1), pp. 31-37. https://doi.org/10.2174/1874331501004010031

54. Morgun, V.V., Stasik, O.O., Kiriziy, D.A., Sokolovska-Sergiienko, O.G. & Makharynska, N.M. (2019). Effects of drought at different periods of wheat development on the leaf photosynthetic apparatus and productivity. Reg. Mech. Biosyst., 10 (4), pp. 406-414. https://doi.org/10.15421/021961

55. Wu, H. & Yang, Z. (2024). Effects of drought stress and postdrought rewatering on winter wheat: A meta-analysis. Agronom., 14, 298. https://doi.org/10.3390/agronomy14020298