Skip to main content
SpringerLink
Log in

The Effect of Elevated Temperature on Salt Tolerance Mechanism in C4 Xero-Halophyte Kochia prostrata

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

Abstract

The study of effect of elevated temperature on the mechanisms of salt tolerance in plants are of great interest and perspective under global climate change. This study investigated the individual and combined effects of prolonged heat and four days moderate salinity on morphophysiological and biochemical parameters (biomass, photosystems I and II (Fv/Fm) efficiencies, apparent photosynthesis intensity, transpiration, dark respiration, water-use efficiency, contents of water, free proline, Na+ and K+ in aboveground parts of plants) in the С4 xero-halophyte Кochia prostrata. The physiological processes and biochemical parameters actively involved during acclimation to stress under different treatments (control, heat, salinity, heat + salinity) were identified. A decrease in biomass and change in the K+/Na+ ratio was observed under all treatments. Acclimation to heat resulted in increased dark respiration intensity (Rd) and K+ content. Under salinity conditions, an increase in Na+ content, a decrease in PSI efficiency and transpiration intensity were observed. Combined stress (heat + salinity) resulted in increased proline and Na+ contents in addition to high values of Rd and K+. Principal component analysis showed that under combined stress, dark respiration, K+ and proline are actively involved in acclimation. It was found that acclimation to elevated temperature affects the salt tolerance mechanisms in K. prostrata, since under combined stress, sodium ions accumulated 3-fold less than in plants under normal temperature and salinity. It is assumed that in K. prostrata plants grown at elevated temperature, K+ and proline are more involved in the acclimation to salinity than Na+. Dark respiration is likely the source of additional energy costs. We conclude that acclimation of С4 halophytes to elevated temperature changes the importance of sodium and potassium ions, as well as proline, in the mechanisms of salt tolerance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Dusenge, M.E., Duarte, A.G., and Way, D.A., Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration, New Phytol., 2018, vol. 221, p. 32. https://doi.org/10.1111/nph.15283

    Article  CAS  PubMed  Google Scholar 

  2. Yadav, S., Elansary, H.O., Mattar, M.A., Elhindi, K.M., Alotaibi, M.A., and Mishra, A., Differential accumulation of metabolites in Suaeda species provides new insights into abiotic stress tolerance in C4-halophytic species in elevated CO2 conditions, Agronomy, 2021, vol. 11, p. 131. https://doi.org/10.3390/agronomy11010131

    Article  CAS  Google Scholar 

  3. Quint, M., Delker, C., Franklin, K.A., Wigge, P.A., Halliday, K.J., and van Zanten, M., Molecular and genetic control of plant thermomorphogenesis, Nat. Plants, 2016, vol. 2, p. 15190. https://doi.org/10.1038/nplants.2015.190

    Article  CAS  PubMed  Google Scholar 

  4. Prasad, P.V.V., Pisipati, S.R., Momcilovic, I., and Ristic, Z., Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat, J. Agron. Crop Sci., 2011, vol. 197, p. 430. https://doi.org/10.1111/j.1439-037X.2011.00477.x

    Article  CAS  Google Scholar 

  5. Dias, A.S., Semedo, J., Ramalho, J.C., and Lidon, F.C., Bread and durum wheat under heat stress: a comparative study on the photosynthetic performance, J. Agron. Crop Sci., 2011, vol. 197, p. 50. https://doi.org/10.1111/j.1439-037X.2010.00442.x

    Article  Google Scholar 

  6. Allakhverdiev, S.I., Kreslavski, V.D., Klimov, V.V., Los, D.A., Carpentier, R., and Mohanty, P., Heat stress: an overview of molecular responses in photosynthesis, Photosynth. Res., 2008, vol. 98, p. 541. https://doi.org/10.1007/s11120-008-9331-0

    Article  CAS  PubMed  Google Scholar 

  7. Crafts-Brandner, S.J. and Salvucci, M.E., Sensitivity of photosynthesis in a C4 plant, maize, to heat stress, Plant Physiol., 2002, vol. 129, p. 1773. https://doi.org/10.1104/pp.002170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sage, R.F. and Kubien, D.S., The temperature response of C3 and C4 photosynthesis, Plant, Cell Environ., 2007, vol. 30, p. 1086. https://doi.org/10.1111/j.1365-3040.2007.01682.x

    Article  CAS  PubMed  Google Scholar 

  9. Ullah, A., Bano, A., and Khan, N., Climate change and salinity effects on crops and chemical communication between plants and plant growth-promoting microorganisms under stress, Front. Sustain. Food Syst., 2021. https://doi.org/10.3389/fsufs.2021.618092

    Book  Google Scholar 

  10. Flowers, T.J. and Muscolo, A., Introduction to the special issue: Halophytes in a changing world, AoB Plants, 2015, vol. 7: plv020. https://doi.org/10.1093/aobpla/plv020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yuan, F., Xu, Y., Leng, B., and Wang, B., Beneficial effects of salt on halophyte growth: morphology, cells, and genes, Open Life Sci., 2019, vol. 14, p. 191. https://doi.org/10.1515/biol-2019-0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Panta, S., Flowers, T., Lane, P., Doyle, R., Haros, G., and Shabala, S., Halophyte agriculture: Success stories, Environ. Exp. Bot., 2014, vol. 107, p. 71. https://doi.org/10.1016/j.envexpbot.2014.05.006

    Article  Google Scholar 

  13. Flowers, T.J., Glenn, E.P., and Volkov, V., Could vesicular transport of Na+ and Cl– be a feature of salt tolerance in halophytes? Ann. Bot., 2019, vol. 123, p. 1. https://doi.org/10.1093/aob/mcy164

    Article  CAS  PubMed  Google Scholar 

  14. Cai, Z.Q. and Gao, Q., Comparative physiological and biochemical mechanisms of salt tolerance in five contrasting highland quinoa cultivars, BMC Plant Biol., 2020, vol. 20, p. 70. https://doi.org/10.1186/s12870-020-2279-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Katschnig, D., Jaarsma, R., Almeida, P., Rozema, J., and Schat, H., Differences in proton pumping and Na/H exchange at the leaf cell tonoplast between a halophyte and a glycophyte, AoB Plants, 2014, vol. 6: plu023. https://doi.org/10.1093/aobpla/plu023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Slama, I., Abdelly, C., Bouchereau, A., Flowers, T., and Savouré, A., Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress, Ann. Bot., 2015, vol. 115, p. 433. https://doi.org/10.1093/aob/mcu239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Heuer, B., Role of proline in plant response to drought and salinity, in Handbook of Plant and Crop Stress, Pessarakli, M., Ed., Boca Raton: CRC Press, 2010, p. 213. https://doi.org/10.1201/b10329

    Book  Google Scholar 

  18. Alam, R., Das, D., Islam, M., Murata, Y., and Hoque, M., Exogenous proline enhances nutrient uptake and confers tolerance to salt stress in maize (Zea mays L.), Progr. Agric., 2016, vol. 27, p. 409. https://doi.org/10.3329/pa.v27i4.32120

    Article  Google Scholar 

  19. El Moukhtari, A., Cabassa-Hourton, C., Farissi, M., and Savouré, A., How does proline treatment promote salt stress tolerance during crop plant development? Front. Plant Sci., 2020, vol. 11, p. 1127. https://doi.org/10.3389/fpls.2020.01127

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bromham, L. and Bennett, T.H., Salt tolerance evolves more frequently in C4 grass lineages, J. Evol. Biol., 2014, vol. 27, p. 653. https://doi.org/10.1111/jeb.12320

    Article  CAS  PubMed  Google Scholar 

  21. Kubien, D.S., von Cammerer, S., Furbank, R.T., and Sage, R.F., C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco, Plant Physiol., 2003, vol. 132, p. 1577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sage, R.F. and Zhu, X.-G., Exploiting the engine of C4 photosynthesis, J. Exp. Bot., 2011, vol. 62, p. 2989. https://doi.org/10.1093/jxb/err179

    Article  CAS  PubMed  Google Scholar 

  23. Nakamura, N., Iwano, M., Havaux, M., Yokota, A., and Munekage, Y.N., Promotion of cyclic electron transportaround 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 

  24. Rakhmankulova, Z.F., Shuyskaya, E.V., Voronin, P.Y., Velivetskaya, T.A., Ignatiev, 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. https://doi.org/10.1134/S102144371802005x

    Article  CAS  Google Scholar 

  25. Yamori, W., Hikosaka, K., and Way, D.A., Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation, Photosynth. Res., 2014, vol. 119, p. 101. https://doi.org/10.1007/s11120-013-9874-6

    Article  CAS  PubMed  Google Scholar 

  26. Harris, L.C., Khan, M.A., Zou, J., Smith, B.N., and Hansen, L.D., Effects of salinity and temperature on respiratory metabolism of Salicornia utahensis from a Great Basin playa. In: McArthur, E. Durant; Fairbanks, Daniel J., comps. Shrubland ecosystem genetics and biodiversity: proceedings; Provo, UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, 2001, p. 265.

  27. Wen, X., Qiu, N., Lu, Q., and Lu, C., Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia, Planta, 2005, vol. 220, p. 486. https://doi.org/10.1007/s00425-004-1382-7

    Article  CAS  PubMed  Google Scholar 

  28. Yan, K., Chen, P., Shao, H., Shao, H., Zhao, S.D., Zhang, L., Xu, G., and Sun, J., Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum, J. Agron. Crop Sci., 2012, vol. 198, p. 218. https://doi.org/10.1111/j.1439-037X.2011.00498.x

    Article  CAS  Google Scholar 

  29. Malinovsky, A.V., Voronin, P.Y., and Akanov, E.N., A vegetation climatic unit for studying the impact on higher plants of an increased CO2 concentration in comparison with the atmospheric CO2 concentration, Russ. J. Plant Physiol., 2020, vol. 67, p. 194. . https://doi.org/10.1134/S1021443720010112

    Article  CAS  Google Scholar 

  30. 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. https://doi.org/10.1007/BF00018060

    Article  CAS  Google Scholar 

  31. Voronin, P.Y., Experimental installation for measurements of chlorophyll fluorescence, CO2 exchange, and transpiration of a detached leaf, Russ. J. Plant. Physiol., 2014, vol. 61, p. 269. https://doi.org/10.1134/S1021443714020174

    Article  CAS  Google Scholar 

  32. 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 Academic Publishers, 1998, p. 4357.

  33. Schreiber, U., Chlorophyll fluorescence and photosynthetic energy conversion: Simple introductory experiments with the TEACHING-PAM chlorophyll fluorometer, Effeltrich: Heinz Walz GmbH, 1997.

  34. Sagers, J.K., Waldron, B.L., Creech, J.E., Mott, I.W., and Bugbee, B., Salinity tolerance of three competing rangeland plant species: Studies in hydroponic culture, Ecol. Evol., 2017, vol. 7, p. 10916. https://doi.org/10.1002/ece3.3607

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rakhmankulova, Z., Shuyskaya, E., Toderich, K., and Voronin, P., Elevated atmospheric CO2 concentration improved C4 xero-halophyte Kochia prostrata physiological performance under saline conditions, Plants, 2021, vol. 10, p. 491. https://doi.org/10.3390/plants10030491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rakhmankulova, Z.F., Physiological aspects of photosynthesis–respiration interrelations, Russ. J. Plant Physiol., 2019, vol. 66, p. 365. https://doi.org/10.1134/S1021443719030117

    Article  CAS  Google Scholar 

  37. Azedo-Silva, J., Osorio, J., Fonseca, F., and Correia, M.J., Effects of soil drying and subsequent re-watering on the activity of nitrate reductase in roots and leaves of Helianthus annuus, Funct. Plant Biol., 2004, vol. 31, p. 611. https://doi.org/10.1071/fp04018

    Article  CAS  PubMed  Google Scholar 

  38. Hasanuzzaman, M., Bhuyan, M.H.M.B., Nahar, K., Hossain, M.S., Mahmud, J.A., Hossen, M.S., Masud, A.A.C., Moumita, and Fujita, M., Potassium: A vital regulator of plant responses and tolerance to abiotic stresses, Agronomy, 2018, vol. 8, p. 31. https://doi.org/10.3390/agronomy8030031

    Article  CAS  Google Scholar 

  39. Bhowmick, A.C., Salma, U., and Siddiquee, T.A., Effect of temperature on the uptake of Na+, K+, Ca2+ and Mg2+ By the various anatomical parts of the vegetable Amaranth gangeticus, IOSR J. Environ. Sci., Toxicol. Food Technol., 2013, vol. 3, p. 20. https://doi.org/10.9790/2402-0362031

    Article  CAS  Google Scholar 

  40. Munns, R. and Tester, M., Mechanisms of salinity tolerance, Ann. Rev. Plant Biol., 2008, vol. 59, p. 651. https://doi.org/10.1146/annurev.arplant.59.032607.092911

    Article  CAS  Google Scholar 

Download references

Funding

The results of CO2/H2O gas exchange were obtained within the state assignment of Ministry of Science and Higher Education of the Russian Federation (theme no. 122042700044-6). Other results were obtained within joint RFBR and JPSSBP grant (No. 21-54-50006; 120214809).

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127276, Moscow, Russia

    Z. F. Rakhmankulova, E. V. Shuyskaya, M. Yu. Prokofieva & P. Yu. Voronin

  2. International Platform for Dryland Research and Education (IPDRE), Tottori University, 680-0001, 1390 Hamasaka Tottori, Japan

    K. N. Toderich

  3. International Center for Biosaline Agriculture for Central Asia and Caucasus, 100000, Tashkent, Uzbekistan

    K. N. Toderich

  4. Arid Land Research Center (ALRC), Tottori University, 680-0001, 1390 Hamasaka Tottori, Japan

    N. Yamanaka

Authors
  1. Z. F. Rakhmankulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. V. Shuyskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Yu. Prokofieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. N. Toderich
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. Yamanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Yu. Voronin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Authors ZFR and EVS designed the experiments. ZFR, EVS, MYuP, KNT, NYa, and PYuV collected samples and performed the experiments. ZFR drafted the manuscript and all authors revised it.

Corresponding author

Correspondence to Z. F. Rakhmankulova.

Ethics declarations

Conflict of interest. The authors declare that they have no conflicts of interest.

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

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. The Effect of Elevated Temperature on Salt Tolerance Mechanism in C4 Xero-Halophyte Kochia prostrata. Russ J Plant Physiol 69, 137 (2022). https://doi.org/10.1134/S1021443722060322

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S1021443722060322

Keywords:

Search

Navigation