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Different Ways of Maintaining Water Balance in Leaves in Two Populations of C4 Atriplex tatarica Differing in Productivity and Drought Tolerance

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Abstract

The effects of water deficiency (–0.3 MPa) on plant growth, the water and proline content, fluorescence parameters chlorophyll PSI and II, and CO2/H2O gas exchange in plant leaves were studied in two populations of xero-halophyte Atriplex tatarica L. (C4 NAD-ME) with contrasting productivity. Based on growth parameter analysis, a less-productive population (P1) was more tolerant of osmotic stress, and a more-productive population (P2) was less tolerant. The studied populations demonstrated different ways of maintaining the water balance in leaves. P1 was characterised by an insensitivity of its stomatal apparatus, a significant decrease in water potential of mesophyll cells’ apoplast in substomatal cavity, an increase in proline content, and activation of PSI cyclic electron transport in leaves. In P2, maintaining the water content in leaves under stress conditions was achieved by stomatal closure. The impact of stress was manifested by decreased intensity of photosynthesis, transpiration, PSII efficiency and more intensified of dark respiration in P2. Thus, various ways by which to maintain the water balance in plant leaves in two populations were revealed under weak osmotic stress.

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REFERENCES

  1. Ghannoum, O., C4 photosynthesis and water stress, Ann. Bot., 2009, vol. 103, p. 635. https://doi.org/10.1093/aob/mcn093

    Article  CAS  PubMed  Google Scholar 

  2. Haxeltine, A. and Prentice, I.C., BIOME3: An equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability, and competition among plant functional types, Global Biogeochem. Cycle, 1996, vol. 10, p. 693. https://doi.org/10.1029/96GB02344

    Article  CAS  Google Scholar 

  3. Taylor, S.H., Ripley, B.S., Woodward, F.I., and Osborne, C.P., Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment, Plant Cell Environ., 2011, vol. 34, p. 65. https://doi.org/10.1111/j.1365-3040.2010.02226.x

    Article  CAS  PubMed  Google Scholar 

  4. Osborne, C.P. and Sack, L., Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics, Philos. Trans. R. Soc., B, 2012, vol. 367, p. 583. https://doi.org/10.1098/rstb.2011.0261

  5. Sage, R.F. and McKown, A.D., Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J. Exp. Bot., 2006, vol. 57, p. 303. https://doi.org/10.1093/jxb/erj040

    Article  CAS  PubMed  Google Scholar 

  6. Taylor, S.H., Aspinwall, M.J., Blackman, C.J., Choat, B., Tissue, D.T., and Ghannoum, O., CO2 availability influences hydraulic function of C3 and C4 grass leaves. J. Exp. Bot., 2018, vol. 69, p. 2731. https://doi.org/10.1093/jxb/ery095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lawson, T. and Blatt, M.R., Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency, Plant Physiol., 2014, vol. 164, p. 1556. https://doi.org/10.1104/pp.114.237107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bellasio, C., Quirk, J., Buckley, T.N., and Beerling, D.J., A dynamic hydro-mechanical and biochemical model of stomatal conductance for C4 photosynthesis, Plant Physiol., 2017, vol. 175, p. 104. https://doi.org/10.1104/pp.17.00666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Domec, J.C., Smith, D.D., and McCulloh, K.A., A synthesis of the effects of atmospheric carbon dioxide enrichment on plant hydraulics: implications for whole-plant water use efficiency and resistance to drought, Plant Cell Environ., 2017, vol. 40, p. 921. https://doi.org/10.1111/pce.12843

    Article  CAS  PubMed  Google Scholar 

  10. Kocacinar, F., McKown, A.D., Sage, T.L., and Sage, R.F., Photosynthetic pathway influences xylem structure and function in Flaveria (Asteraceae), Plant Cell Environ., 2008, vol. 31, p. 1363. https://doi.org/10.1111/j.1365-3040.2008.01847.x

    Article  CAS  PubMed  Google Scholar 

  11. Le Houérou, H.N., The role of saltbushes (Atriplex spp.) in arid land rehabilitation in the Mediterranean Basin: a review, Agrofor. Syst., 1992, vol. 18, p. 107. https://doi.org/10.1007/BF00115408

    Article  Google Scholar 

  12. Rakhmankulova, Z.F., Shuyskaya, E.V., Voronin, P.Yu., and Usmanov, I.Yu., Comparative study on resistance of C3 and C4 xero-halophytes of the genus Atriplex to water deficit and salinity, Russ. J. Plant Physiol., 2019, vol. 66, p. 250. https://doi.org/10.1134/S1021443719020109

    Article  CAS  Google Scholar 

  13. Rakhmankulova, Z.F., Shuyskaya, E.V., Shcherbakov, A.V., Fedyaev, V.V., Biktimerova, G.Ya., Khafisova, R.R., and Usmanov, I.Yu., Content of proline and flavonoids in the shoots of halophytes inhabiting the South Urals, Russ. J. Plant Physiol., 2015, vol. 62, p. 71. https://doi.org/10.1134/S1021443715010112

    Article  CAS  Google Scholar 

  14. Shavrukov, Y., Salt stress or salt shock: which genes are we studying? J. Exp. Bot., 2013, vol. 64, p. 119. https://doi.org/10.1093/jxb/ers316

    Article  CAS  PubMed  Google Scholar 

  15. Muona, O. and Szmidt, A., A multilocus study of natural populations of Pinus sylvestris, Population Genetics in Forestry, Lecture Notes Biomath. Ser. vol. 60, Berlin: Springer-Verlag, 1985, p. 226.

    Google Scholar 

  16. Isozymes in Plant Biology, Soltis, D.E. and Solis, P.S., Eds., Portland, OR: Dioscorides, 1989.

    Google Scholar 

  17. Nei, M., Molecular Evolutionary Genetics, New York: Columbia Univ. Press, 1987.

    Book  Google Scholar 

  18. Yeh, F.C., Yang, R.C., and Boyle, T. PopGene, Version 1.32. Microsoft Windows-Based Freeware for Population Genetic Analysis, Edmonton: Univ. of Alberta, 1999.

    Google Scholar 

  19. Bates, S., Waldren, R.P., and Tear, I.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, p. 205.

    Article  CAS  Google Scholar 

  20. Voronin, P.Yu., Rakhmankulova, Z.F., Shuyskaya, E.V., Maevskaya, S.N., Nikolaeva, M.K., Maksimov, A.P., Maximov, T.Chr., Myasoedov, N.A., Balnokin, Yu.V., Rymar, V.P., Valdayskih, V.V., and Kuznetsov, Vl.V., New method for quantitative determination of water potential of mesophyll cell’ apoplast in substomatal cavity of the leaf, Russ. J. Plant Physiol., 2017, vol. 64, p. 452. https://doi.org/10.1134/S1021443717020133

    Article  CAS  Google Scholar 

  21. Voronin, P.Yu., Maevskaya, S.N., and Nikolaeva, M.K., Physiological and molecular responses of maize (Zea mays L.) plants to drought and rehydration, Photosynthetica, 2019, vol. 57, p. 850. https://doi.org/10.32615/ps.2019.101

    Article  CAS  Google Scholar 

  22. Klughammer, C. and Schreiber, U., Measuring P700 absorbance changes in the near infrared spectral region with a dual wavelength pulse modulation system, in Photosynthesis: Mechanisms and Effects, Garab G., Ed., Dordrecht: Springer-Verlag, 1998, p. 4357.

  23. Nakamura, N., Iwano, M., Havaux, M., Yokota, A., and Munekage, Y.N., Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C4 photosynthesis in the genus Flaveria, New Phytol., 2013, vol. 199, p. 832. https://doi.org/10.1111/nph.12296

    Article  CAS  PubMed  Google Scholar 

  24. Schreiber, U., Chlorophyll Fluorescence and Photosynthetic Energy Conversion: Simple Introductory Experiments with the TEACHING-PAM Chlorophyll Fluorometer, Effeltrich: Heinz Walz, 1997.

  25. Ben Hassine, A., Bouzid, S., and Lutts, S., Does habitat of Atriplex halimus L. affect plant strategy for osmotic adjustment? Acta Physiol. Plant, 2010, vol. 32, p. 325. https://doi.org/10.1007/s11738-009-0410-4

    Article  Google Scholar 

  26. Kanai, R. and Edwards, G.E., The biochemistry of C4 photosynthesis, in C 4 Plant Biology, Sage, R.F. and Monson, R.K., Eds., San Diego: Academic, 1999, p. 215.

    Google Scholar 

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Funding

This work was supported by Ministry of Science and Higher Education of the Russian Federation (theme FFES-2021-0010).

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Z.F. Rakhmankulova, E.V. Shuyskaya contributed equally to this work.

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Correspondence to Z. F. Rakhmankulova or E. V. Shuyskaya.

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Rakhmankulova, Z.F., Shuyskaya, E.V. & Voronin, P.Y. Different Ways of Maintaining Water Balance in Leaves in Two Populations of C4 Atriplex tatarica Differing in Productivity and Drought Tolerance. Russ J Plant Physiol 68, 1143–1151 (2021). https://doi.org/10.1134/S1021443721060170

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