Skip to main content
Log in

Comparative Contribution of СО22О Exchange Components to the Process of Adaptation to Drought in Xero-Halophytes from the Family Chenopodiaceae with Different Types of Photosynthesis

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Components of СО22О exchange (rates of apparent photosynthesis, transpiration, and dark respiration), as well as efficiency of photosystem I, growth rate, and proline content, were investigated in plants of the С3 species (Atriplex verrucifera M. Bieb), two populations of the С4 species (A. tatarica L.), and two populations of the intermediate С3–С4 species (Sedobassia sedoides (Pall.) Freitag & G. Kadereit), family Chenopodiaceae, in the course of adaptation to PEG-induced moderate osmotic stress (–0.4…–0.5 MPa). Two taken СО2 concentrations (400 and 200 ppm) enabled the examination of stomatal and metabolic contribution to the formation of the mechanisms of drought tolerance and estimate sensitivity of stomata. Under moderate water deficit, the С3 species showed drought tolerance and succulence and was notable for insensitive stomata. Examination of growth characteristics made it possible to reveal differences in productivity and tolerance between populations of the С4 and С3–С4 species. In spite of a different nature of carbon-concentrating mechanism (aspartate in С4 and photorespiratory in С3–С4), populations tolerant to water deficiency shared common features: less sensitive stomata and operation of the mechanism stabilizing water balance of the leaf cells probably due to proline and cyclic transport of electrons. Realization of such a strategy maintains coordination among parameters of СО22О exchange, which ensures a lower variability of dark respiration and a greater tolerance of plants to moderate osmotic stress. In nontolerant populations, adaptation mainly depends on stomatal closure, which probably results in upsetting the balance among parameters of СО22О exchange.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

REFERENCES

  1. Ashraf, M. and Harris, P.J.C., Photosynthesis under stressful environments: an overview, Photosynthetica, 2013, vol. 51, p. 163. https://doi.org/10.1007/s11099-013-0021-6

    Article  CAS  Google Scholar 

  2. Rakhmankulova, Z.F., The relationship between photosynthesis and respiration of the whole plant in normal and adverse environmental conditions, Zh. Obshch. Biol., 2002, vol. 63, no. 3, p. 44.

    Google Scholar 

  3. Frole, K. and Gilbert, M., Differences in drought sensitivities and photosynthetic limitations between co-occurring C3 and C4 (NADP-ME) Panicoid grasses, Ann. Bot., 2010, vol. 105, p. 493. https://doi.org/10.1093/aob/mcp307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Way, D.A., Katul, G.G., Manzoni, S., and Vico, G., Increasing water use efficiency along the C3-to-C4 evolutionary pathway: a stomatal optimization perspective, J. Exp. Bot., 2014, vol. 65, p. 3683. https://doi.org/10.1093/jxb/eru205

    Article  PubMed  PubMed Central  Google Scholar 

  5. 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. Cycles, 1996, vol. 10, p. 693.

    Article  CAS  Google Scholar 

  6. 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 

  7. 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 

  8. 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. London B., 2012, vol. 367, p. 583. https://doi.org/10.1098/rstb.2011.0261

    Article  CAS  Google Scholar 

  9. Shabala, S., Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops, Ann. Bot., 2013, vol. 112, p. 1209. https://doi.org/10.1093/aob/mct205

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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: Kluwer, 1998, vol. 5, p. 4357.

  11. Sage, R.F., Sage, T.L., and Kocacinar, F., Photorespiration and the evolution of C4 photosynthesis, Annu. Rev. Plant Biol., 2012, vol. 63, p. 19. https://doi.ogr/10.1146/annurev-arplant-042811-105511

    Article  CAS  Google Scholar 

  12. Khoshravesh, R., Stinson, C.R., Stata, M., Busch, F.A., Sage, R.F., Ludwig, M., and Sage, T.L., C3–C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis, J. Exp. Bot., 2016, vol. 67, p. 3065. https://doi.org/10.1093/jxb/erw150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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 

  14. 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 

  15. Shuyskaya, E.V., Rakhmankulova, Z.F., Biktimerova, G.Ya., Shcherbakov, A.V., Fedyaev, V.V., Suyundukov, Ya.T., and Usmanov, I.Yu., Ecological and physiological analysis of representatives from Chenopodiaceae family on saline soils of the South Urals, Rastit. Resur., 2014, vol. 50, p. 614.

    Google Scholar 

  16. 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 

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

    Article  CAS  Google Scholar 

  18. Blatt, M.R., Cellular signaling and volume control in stomatal movements in plants, Annu. Rev. Cell. Dev. Biol., 2000, vol. 16, p. 221. https://doi.org/10.1146/annurev.cellbio.16.1.221

    Article  CAS  PubMed  Google Scholar 

  19. Lawson, T., Guard cell photosynthesis and stomatal function, New Phytol., 2009, vol. 181, p. 13. https://doi.org/10.1111/j.1469-8137.2008.02685.x

    Article  CAS  PubMed  Google Scholar 

  20. Outlaw, W.H., Integration of cellular and physiological functions of guard cells, Crit. Rev. Plant Sci., 2003, vol. 22, p. 503. https://doi.org/10.1080/713608316

    Article  Google Scholar 

  21. 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 c photosynthesis in the genus Flaveria,New Phytol., 2013, vol. 199, p. 832. https://doi.org/10.1111/nph.12296

    Article  CAS  PubMed  Google Scholar 

  22. Vogan, P.J. and Sage, R.F., Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis, Oecologia, 2012, vol. 169, p. 341. https://doi.org/10.1007/s00442-011-2201-z

    Article  PubMed  Google Scholar 

  23. Sage, R.F., Khoshravesh, R., and Sage, T.L., From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis, J. Exp. Bot., 2014, vol. 65, p. 3341. https://doi.org/10.1093/jxb/eru180

    Article  PubMed  Google Scholar 

  24. Kadereit, G. and Freitag, H., Molecular phylogeny of Camphorosmeae (Camphorosmoideae, Chenopodiaceae): implications for biogeography, evolution of C4 photosynthesis and taxonomy, Taxon, 2011, vol. 60, p. 51. https://doi.org/10.1002/tax.601006

    Article  Google Scholar 

  25. Voznesenskaya, E.V., Koteyeva, N.K., Akhani, H., Roalson, E.H., and Edwards, G.E., Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis, J. Exp. Bot., 2013, vol. 64, p. 3583. https://doi.org/10.1093/jxb/ert191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shuyskaya, E., Rakhmankulova, Z., Voronin, P., Kuznetsova, N., Biktimerova, G., and Usmanov, I., Salt and osmotic stress tolerance of the C3–C4 xero-halophyte Bassia sedoides from two populations differ in productivity and genetic polymorphism, Acta Physiol. Plant., 2015, vol. 37, p. 236.

    Article  Google Scholar 

  27. Rakhmankulova, Z.F., Shuyskaya, E.V., Suyundukov, Ya.T., Usmanov, I.Yu., and Voronin, P.Yu., Different responses of two ecotypes of C3–C4 xero-halophyte Bassia sedoides to osmotic and ionic factors of salt stress, Russ. J. Plant Physiol., 2016, vol. 63, p. 349.

    Article  CAS  Google Scholar 

  28. Rakhmankulova, Z.F., Shuyskaya, E.V., Voronin, P.Yu., Velivetskaya, T.A., Ignat’ev, A.V., and Usmanov, I.Yu., Role of photorespiration and cyclic electron transport in C4 photosynthesis evolution in the C3–C4 intermediate species Sedobassia sedoides,Russ. J. Plant Physiol., 2018, vol. 65, p. 455.

    Article  CAS  Google Scholar 

  29. Rakhmankulova, Z.F., Shuyskaya, E.V., Voronin, P.Yu., and Usmanov, I.Yu., Comparative study on resistance of C3 and C4 xerohalophytes of the genus Atriplex to water deficit and salinity, Russ. J. Plant Physiol., 2019, vol. 66, p. 250.

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research, project no. 17-04-00853-а.

Author information

Authors and Affiliations

Authors

Corresponding authors

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

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies involving animals or human participants performed by any of the authors.

CONFLICT OF INTERESTS

The authors declare that they have no conflict of interests.

Additional information

Translated by N. Balakshina

Abbreviations: CCM—carbon concentrating mechanism.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rakhmankulova, Z.F., Shuyskaya, E.V., Prokofieva, M.Y. et al. Comparative Contribution of СО22О Exchange Components to the Process of Adaptation to Drought in Xero-Halophytes from the Family Chenopodiaceae with Different Types of Photosynthesis. Russ J Plant Physiol 67, 494–506 (2020). https://doi.org/10.1134/S102144372003019X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S102144372003019X

Keywords:

Navigation