Fiziol. rast. genet. 2020, vol. 52, no. 5, 371-387, doi: https://doi.org/10.15407/frg2020.05.371

Influence of drought on the photosynthetic apparatus activity, senescence rate, and productivity in wheat plants

Stasik O.O., Kiriziy D.A., Sokolov­ska-Sergiienko O.G., Bondarenko O.Yu.

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

Effects of soil drought at flowering stage on the functional state of photosynthetic apparatus and chloroplast enzymatic antioxidant defense systems in flag leaf during reproductive period, and the productivity of winter wheat plants of high-protein Natalka variety and drought-tolerant Podolyanka variety were studied in pot experiment. Until flowering and for the control plants during the entire vegetation, the soil moisture content was maintained at a level of 60—70 % of field capacity (FC). Drought treatment (soil moisture 30 % FC) was applied for 7 days covering flowering—early kernel watery ripe period (BBCH 61—71). After that, watering of plants was resumed to a control level which was maintained until the end of the growing season. The estimation of the chlorophyll and Rubisco content, the chloroplast antioxidant enzymes activity, and the net CO2 assimilation and transpiration rates was carried out on flag leaves. The measurements were taken on the third day of watering cessation (the first day the soil moisture reached 30 % FC, BBCH 61), at the end of the drought period (seventh day at 30 % FC, BBCH 71), and after watering resumed at the medium milk (BBCH 75) and late milk (BBCH 77) stages. The components of plant grain productivity were determined by weighing air-dry material at grain full ripeness. It was revealed, that drought stress during flowering inhibited CO2 assimilation and accelerated induction of senescence processes in wheat plants associated with degradation of photosynthetic apparatus and manifested in quicker ontogenetic drop in chlorophyll and Rubisco contents and loss of leaf photosynthetic activity. This exacerbated the drought impact on the plant organism so that after optimal watering return, the physiological and biochemical parameters were not restored to the values of control plants that were all time under optimal moisture supply. Stress-induced premature senescence reduced the supply of plants with assimilates and ultimately led to a decrease in their grain productivity. Impact of drought on flag leaf photosynthetic activity and especially on senescence induction were much more pronounced in the high-protein wheat variety Natalka with a genetically programmed earlier start of the nitrogen-containing compounds remobilization from leaves than in Podolyanka variety. The drought-tolerant variety Podolyanka keep ability to maintain much higher CO2 assimilation activity during drought period and to preserve photosynthetic apparatus from early induction of senescence due to likely more efficient chloroplast antioxidant defense systems, thereby gaining a better assimilates supply for yield formation.

Keywords: Triticum aestivum L., drought, senescence, CO2, assimilation rate, Rubisco, antioxidant enzymes, productivity.

Fiziol. rast. genet.
2020, vol. 52, no. 5, 371-387

Full text and supplemented materials

Free full text: PDF  

References

1. 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].

2. Gregersen, P.L., Culetic, A., Boschian, L. & Krupinska K. (2013). Plant senescence and crop productivity. Plant Mol. Biol., 82, pp. 603-622. https://doi.org/10.1007/s11103-013-0013-8

3. Gepstein, S. & Glick, B.R. (2013). Strategies to ameliorate abiotic stress-induced plant senescence. Plant Molecular Biology, 82, pp. 623-633. https://doi.org/10.1007/s11103-013-0038-z

4. Guo, Y. (2013). Towards systems biological understanding of leaf senescence. Plant Mol. Biol., 82, pp. 519-528. https://doi.org/10.1007/s11103-012-9974-2

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

6. Hortensteiner, S. (2013). Update on the biochemistry of chlorophyll breakdown. Plant Molecular Biology, 82, pp. 505-517. https://doi.org/10.1007/s11103-012-9940-z

7. Avila-Ospina, L., Moison, M., Yoshimoto, K. & Masclaux-Daubresse, C. (2014). Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot., 65, No. 14, pp. 3799-3811. https://doi.org/10.1093/jxb/eru039

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

9. Avin-Wittenberg, T., Baluska, F., Bozhkov, P.V., Elander, P.H., Fernie, A.R., Galili, G., Hassan, A., Hofius, D., Isono, E., Le Bars, R., Masclaux-Daubresse, C., Minina, E.A., Peled-Zehavi, H., Coll, N.S., Sandalio, L.M., Satiat-Jeunemaitre, B., Sirko, A., Testillano, P.S. & Batoko, H. (2018). Autophagy-related approaches for improving nutrient use efficiency and crop yield protection. Journal of Experimental Botany, Vol. 69, No. 6, pp. 1335-1353. https://doi.org/10.1093/jxb/ery069

10. Khanna-Chopra, R. (2012). Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma, 249, pp. 469-481. https://doi.org/10.1007/s00709-011-0308-z

11. De Simone, V., Soccio, M., Borrelli, G.M., Pastore, D. & Trono, D. (2014). Stay-green trait-antioxidant status interrelationship in durum wheat (Triticum durum) flag leaf during post-flowering. J. Plant Res., 127, pp. 159-171. https://doi.org/10.1007/s10265-013-0584-0

12. Krieger-Liszkay, A., Krupinska, K. & Shimakawa, G. (2019). The impact of photosynthesis on initiation of leaf senescence. Physiologia Plantarum, 166, pp. 148-164. https://doi.org/10.1111/ppl.12921

13. Semwal, V.K. & Khanna-Chopra, R. (2018). Reproductive sink enhanced drought induced senescence in wheat fertile line is associated with loss of antioxidant competence compared to its CMS line. Physiology and Molecular Biology of Plants, 24, pp. 591-604. https://doi.org/10.1007/s12298-018-0549-9

14. Jibran, R., Hunter, D.A. & Dijkwel, P.P. (2013). Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol., 82, pp. 547-561. https://doi.org/10.1007/s11103-013-0043-2

15. Yang, J., Zhang, J., Wang, Z., Zhu, Q. & Liu, J. (2003). Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant, Cell Environ., 26, pp. 1621-1631. https://doi.org/10.1046/j.1365-3040.2003.01081.x

16. Lee, S., Seo, P.J., Lee, H.J. & Park, C.M. (2012). A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J., 70, pp. 831-844. https://doi.org/10.1111/j.1365-313X.2012.04932.x

17. 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. Journal of Plant Physiology, 144, pp. 307-313. https://doi.org/10.1016/S0176-1617(11)81192-2

18. Mokronosov, A.T., & Kovalev, A.G. (Eds.). (1989). Photosynthesis and Bioproductivity: Methods of Determination. Agropromizdat, Moskow [in Russian].

19. Aranjuelo, I., Perez, P., Hernandez, L., Irigoyen, J.J., Zita, G., Martinez-Carrasco, R. & Sanchez-Diaz, M. (2005). The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation. Physiol. Plant., 123, No. 3, pp. 348-358. https://doi.org/10.1111/j.1399-3054.2005.00459.x

20. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, No. 5259, pp. 680-685. https://doi.org/10.1038/227680a0

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

22. Chen, G.-X., & Asada, K. (1989). Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their and molecular properties. Plant and Cell Physiology, 30(7), pp. 987-998. https://doi.org/10.1093/oxfordjournals.pcp.a077844

23. Morgun, V.V, Sanin, Y.V. & Schwartau, V.V. (2015). The club 100 centners. Winter wheat varieties of the Institute of Plant Physiology and Genetics of the National Academy of Sciences of Ukraine and the protection system of Syngenta. Kyiv: Logos [in Ukrainian].

24. Gaju, O., Allard, V., Martre, P., Le Gouis, J., Moreau, D., Bogard, M., Hubbart, S. & Foulkes, M.J. (2014). Nitrogen partitioning and remobilization in relation to leaf senescence, grain yield and grain nitrogen concentration in wheat cultivars. Field Crop Research, 155, pp. 213-223. https://doi.org/10.1016/j.fcr.2013.09.003

25. Distelfeld, A., Avni, R. & Fischer, A. (2014). Senescence, nutrient remobilization, and yield in wheat and barley. J. Exp. Bot., 65, pp. 3783-3798. https://doi.org/10.1093/jxb/ert477

26. Zhang, H. & Zhou, C. (2013). Signal transduction in leaf senescence. Plant Mol. Biol., 82, pp. 539-545. https://doi.org/10.1007/s11103-012-9980-4

27. Christopher, J.T., Christopher, M.J., Borrell, A.K., Fletcher, S. & Chenu, K. (2016). Stay-green traits to improve wheat adaptation in well-watered and water-limited environments. Journal of Experimental Botany, Vol. 67, No. 17, pp. 5159-5172. https://doi.org/10.1093/jxb/erw276

28. 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 Physiology Reports, 24(3), pp. 305-315. https://doi.org/10.1007/s40502-019-00458-8

29. Bogard, M., Jourdan, M., Allard, V., Martre, P., Perretant, M.R., Ravel, C., Heumez, E., Orford, S., Snape, J., Griffiths, S., Gaju, O., Foulkes, J. & Le Gouis, J. (2011). Anthesis date mainly explained correlations between post-anthesis leaf senescence, grain yield, and grain protein concentration in a winter wheat population segregating for flowering time QTLs. J. Exp. Bot., 62(10), pp. 3621-36. https://doi.org/10.1093/jxb/err061

30. Gong, Y.H., Zhang, J., Gao, J.F., Lu, J.Y. & Wang, J.R. (2005). Slow export of photoassimilate from stay-green leaves during late grain-filling stage in hybrid winter wheat (Triticum aestivum L.). J. Agron. Crop Sci., 191, No. 4, pp. 292-299. https://doi.org/10.1111/j.1439-037X.2005.00173.x

31. Chauhan, S., Srivalli, S., Nautiyal, A.R. & Khanna-Chopra, R. (2009). Wheat cultivars differing in heat tolerance show a differential response to monocarpic senescence under high-temperature stress and the involvement of serine proteases. Photosynthetica, 47(4), pp. 536-547. https://doi.org/10.1007/s11099-009-0079-3

32. 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

33. 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].

34. Feller, U., Anders, I. & Mae, T. (2008). Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot., 59, No. 7, pp. 1615-1624 https://doi.org/10.1093/jxb/erm242

35. Galmes, J., Aranjuelo, I., Medrano, H. & Flexas, J. (2013). Variation in Rubisco content and activity under variable climatic factors. Photosynth. Res., 117, pp.73-90. https://doi.org/10.1007/s11120-013-9861-y

36. Wang, P., Mugume, Y., & Bassham, D. C. (2018). New advances in autophagy in plants: Regulation, selectivity and function. Seminars in Cell & Developmental Biology, 80, pp. 113-122. https://doi.org/10.1016/j.semcdb.2017.07.018

37. Kolupaev, Yu.E., & Kokorev, A.I. (2019). Antioxidant system and plant resistance to water deficit. Fiziol. rast. genet., 51(1), pp. 28-54 [in Russian]. https://doi.org/10.15407/frg2019.01.028

38. Cui, M.H., Ok, S.H., Yoo, K.S., Jung, K.W., Yoo, S.D. & Shin, J.S. (2013). An Arabidopsis cell growth defect factor-related protein, CRS, promotes plant senescence by increasing the production of hydrogen peroxide. Plant Cell Physiol., 54, pp. 155-167. https://doi.org/10.1093/pcp/pcs161

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(1), pp. 16-25. https://doi.org/10.15421/021903

40. 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. Regulatory Mechanisms in Biosystems, 10(4), pp. 406-414. https://doi.org/10.15421/021961

41. Abid, M., Tian, Z., Ata-Ul-Karim, S.T., Wang, F., Liu, Y., Zahoor, R., Jiang, D. & Dai, T. (2016). Adaptation to and recovery from drought stress at vegetative stages in wheat (Triticum aestivum) cultivars. Functional Plant Biology, 43, pp. 1159-1169.