Skip to main content
SpringerLink
Log in

Influence of Oxidative Stress upon the Lipid Composition of Raft Structures of the Vacuolar Membrane

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

Abstract

The influence of oxidative stress on the lipid composition of raft structures of vacuolar membranes isolated from Beta vulgaris L. beet roots was studied in order to clarify the role of these membrane structures in the adaptation mechanisms of the plant cell. Changes in the qualitative and quantitative composition of major lipids, sterols, and fatty acids resulting from stress were analyzed and compared with changes in lipids, the role of which has been reliably established in protecting cells from stress. Previously, the presence of three types of raft structures was shown in the vacuolar membrane. Under oxidative stress, variations took place in the composition of the lipids of these structures. The most significant of them, capable of influencing the protective mechanisms of the plant cell, were identified in raft microdomains of zone four of the sucrose gradient (35% sucrose). They consisted of an increase in the content of sphingolipids, phosphatidylserine, β-sitosterol, and digalactosyl diglyceride and a decrease in phosphatidic acid. Less pronounced differences were found in the lipid composition of microdomains of zone two of the sucrose gradient (15% sucrose): the amount of cholesterol and sphingolipids increased and the content of phosphatidic acid and monogalactosyldiglyceride decreased. Among the variations in lipid composition that can affect the protective mechanisms of the plant cell, an increase in the content of phosphatadylcholine, campesterol and β-sitosterol was noted in microdomains of zone six (60% sucrose). The complex of identified variations in the lipid composition in the studied raft microdomains of the vacuolar membrane may be the result of a stress response and participate in the formation of adaptation mechanisms of the plant cell.

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

REFERENCES

  1. Menshikova, E.E. and Zenkov, N.A., Antioxidants and inhibitors of radical processes, Usp. Sovr. Biol., 1993, vol. 113 (4), p. 442.

    Google Scholar 

  2. Okazaki, Y. and Saito, K., Roles of lipids as signaling molecules and mitigators during stress response in plants, Plant J., 2014, vol. 79, p. 584. https://doi.org/10.1111/tpj.12556

    Article  CAS  PubMed  Google Scholar 

  3. Gronnier, J., Gerbeau-Pessot, P., Germain, V., Mongrand, S., and Simon-Plas, F., Divide and rule: Plant plasma membrane organization, Trends Plant Sci., 2018, vol. 23, p. 899. https://doi.org/10.1016/jtplants.2018.07.007

    Article  CAS  PubMed  Google Scholar 

  4. Cassim, A.M., Gouguet, P., Gronnier, J., Laurent, N., Germain, V., Grison, M., Boutté, Y., Gerbeau-Pissot, P., Simon-Plas, F., and Mongrand, S., Plant lipids: Key players of plasma membrane organization and function, Prog. Lipid Res., 2019, vol. 73, p. 1. https://doi.org/10.1016/j.plipres.2018.11.002

    Article  CAS  Google Scholar 

  5. Peskan, T., Westermann, M., and Oelmüller, R., Identification of low-density Triton X-100 insoluble plasma membrane microdomains in higher plants, Eur. J. Biochem., 2000, vol. 267, p. 6989. https://doi.org/10.1046/j.1432-1327.2000.01776.x

    Article  CAS  PubMed  Google Scholar 

  6. Lingwood, D. and Simons, K., Lipid rafts as a membrane-organizing principle, Science, 2010, vol. 327, p. 46. https://doi.org/10.1126/science.1174621

    Article  CAS  PubMed  Google Scholar 

  7. Pike, L.J., Growth factor receptors, lipid rafts and caveolae: An evolving story, Biochim. Biophys. Acta, 2005, vol. 1746, p. 260. https://doi.org/10.1006/jbbamcr.200.05.005

    Article  CAS  PubMed  Google Scholar 

  8. Ozolina, N.V., Nesterkina, I.S., Kolesnikova, E.V., Salyaev, R.K., Nurminsky, V.N., Rakevich, A.L., Martynovich, E.F., and Chernyshov, M.Yu., Tonoplast of Beta vulgaris L. contains detergent-resistant membrane microdomains, Planta, 2013, vol. 237, p. 859. https://doi.org/10.1007/s00425-012-1800-1

    Article  CAS  PubMed  Google Scholar 

  9. Ozolina, N.V., Nesterkina, I.S., Gurina, V.V., and Nurminsky, V.N., Non-detergent isolation of membrane structures from beet plasmalemma and tonoplast having lipid composition characteristic of rafts, J. Membr. Biol., 2020, vol. 253, p. 479. https://doi.org/10.1007/s00232-020-00137-y

    Article  CAS  PubMed  Google Scholar 

  10. Narayanan, S., Tamura, P.J., Roth, M.R., Vara Prasad, P.V., and Welti, R., Wheat leaf lipid composition during heat stress: I. High day and night temperatures result in major lipid alterations, Plant Cell Environ., 2015, vol. 39, p. 787. https://doi.org/10.1111/pce.12649

    Article  CAS  Google Scholar 

  11. Ozolina, N.V., Gurina, V.V., Nesterkina, I.S., and Nurminsky, V.N., Variations in the content of tonoplast lipids under abiotic stress, Planta, 2020, vol. 251, p. 107. https://doi.org/10.1007/s00425-020-03399-x

    Article  CAS  PubMed  Google Scholar 

  12. Salyaev, R.K., Kuzevanov, V.Ya., Khaptagaev, S.B., and Kopytchuk, V.N., Isolation and purification of vacuoles and vacuolar membranes from plant cells, Russ. J. Plant Physiol., 1981, vol. 28, p. 1295.

    Google Scholar 

  13. Nikulina, G.N., Obzor metodov kolichestvennogo opredeleniia fosfora po obrazovaniiu molibdenovoi sini (Review of Methods for the Quantitative Determination of Phosphorus by the Formation of Molybdenum Blue), Leningrad: Nauka, 1965.

  14. Bradford, M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, p. 248. https://doi.org/10.1006/abio.1976.9999

    Article  CAS  PubMed  Google Scholar 

  15. Ozolina, N.V., Kapustina, I.S., Gurina, V.V., and Nurminsky, V.N., Role of tonoplast microdomains in plant cell protection against osmotic stress, Planta, 2022, vol. 255, p. 65. https://doi.org/10.1007/s00425-021-03800-3

    Article  CAS  PubMed  Google Scholar 

  16. Ristic, Z. and Ashworth, E.N., Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation, Protoplasma, 1993, vol. 172, p. 111. https://doi.org/10.1007/BF01379368

    Article  Google Scholar 

  17. Vladimirov, Yu.A., Archakov, A.I., and Frank, G.M., Perekisnoe okislenie lipidov v biologicheskikh membranakh (Lipid Peroxidation in Biological Membranes), Moscow: Nauka, 1972.

  18. Nurminsky, V.N., Korzun, A.M., Rozinov, S.V., and Salyaev, R.K., Computer time-lapse video recording of a fraction of isolated vacuoles, Biomed. Khim., 2004, vol. 50, p. 180.

    Google Scholar 

  19. Folch, J., Lees, M., and Sloan Stanley, G.H., A simple method for the isolation and purification of total lipides from animal tissues, J. Biol. Chem., 1957, vol. 226, p. 497. https://doi.org/10.1016/S0021-9258(18)64849-5

    Article  CAS  PubMed  Google Scholar 

  20. Christie, W.W., Equivalent chain lengths of methyl ester derivatives of fatty acids on gas chromatography, J. Chromatogr. A., 1988, vol. 447, p. 305. https://lipidlibrary.aocs.org/lipid-analysis/selected-topics-in-the-analysis-of-lipids/preparation-of-ester-derivatives-of-fatty-acids-for-chromatographic-analysis.

    Article  CAS  Google Scholar 

  21. Zhou, Y., Pan, X., Qu, H., and Underhill, S.J., Low temperature alters plasma membrane lipid composition and ATPase activity of pineapple fruit during blackheart development, J. Bioenerg. Biomembr., 2014, vol. 46, p. 59. https://doi.org/10.1007/s10863-013-9538-4

    Article  CAS  PubMed  Google Scholar 

  22. Boldyrev, A.A., Biologicheskie membrany i transport ionov (Biological Membranes and Ion Transport), Moscow: MSU, 1985.

  23. Valitova, Yu.N., Sulkarnaeva, F.G., and Minibaeva, F.V., Plant sterols: Diversity, biosynthesis, physiological functions, Biochemistry (Moscow), 2016, vol. 81, p. 1050. https://doi.org/10.1134/S0006297916080046

    Article  CAS  Google Scholar 

  24. Shuler, I., Milon, A., Nakatani, Y., Ourisson, G., Albrecht, A.M., Benveniste, P., and Hartman, M.A., Differential effects of plant sterols on water permeability and on acyl chain phosphatidylcholine bilayers, Proc. Natl. Acad. Sci. USA, 1991, vol. 88, p. 6926. https://doi.org/10.1073/pnas.88.16.6926

    Article  Google Scholar 

  25. Wang, T., Hicks, K.B., and Moreau, R., Antioxidant activity of photosterols, oryzanol, and other phytosterols conjugates, J. Am. Oil Chem. Soc., 2002, vol. 79, p. 1201. https://doi.org/10.1007/s11746-002-0628-x

    Article  CAS  Google Scholar 

  26. Hartmann, M.A., Plant sterols and the membrane environment, Trends Plant Sci., 1998, vol. 3, p. 170. https://doi.org/10.1016/S1360-1385(98)01233-3

    Article  Google Scholar 

  27. Wegener, A., Gimbel, W., Werner, T., Hani, J., Ernst, D., and Sandermann, H., Molecular cloning of ozone-inducible protein from Pinus sylvestris L. with high sequence similarity to vertebrate 3-hydroxy-3-methylglutaryl-CoA-syntas, Biochim. Biophys. Acta, 1997, vol. 1350, p. 247.

    Article  CAS  PubMed  Google Scholar 

  28. Gennis, R., Biomembranes: Molecular Structure and Function, New York: Springer, 1989.

    Book  Google Scholar 

  29. Wu, J.L., Seliskar, D.M., and Gallagher, J.L., The response of plasma membrane lipid composition in callus of the halophyte Spartina patens (Poaceae) to salinity stress, Am. J. Bot., 2005, vol. 92, p. 852. https://doi.org/10.3732/ajb.92.5.852

    Article  CAS  PubMed  Google Scholar 

  30. Makarenko, S.P., Konenkina, T.A., and Salyaev, R.K., Chemical composition and structure of vacuolar membranes, Biol. Membrany, 1992, vol. 9, p. 290.

    CAS  Google Scholar 

  31. Zhou, Y., Pan, X., Qu, H., and Underhill, S.J., Low temperature alters plasma membrane lipid composition and ATPase activity of pineapple fruit during blackheart development, J. Bioenerg. Biomembr., 2014, vol. 46, p. 59. https://doi.org/10.1007/s10863-013-9538-4

    Article  CAS  PubMed  Google Scholar 

  32. Arisz, S.A., van Wijk, R., Roels, W., Zhu, J.K., Haring, M.A., and Munnik, T., Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase, Front. Plant Sci., vol. 4. https://doi.org/10.3389/tpls.2013.00001

  33. McLeoughlin, F., Arzis, S.A., Dekker, H.L., Kramer, G., de Koster, C.G., Haring, M.A., Munnik, T., and Testerink, C., Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots, Biochem. J., 2013, vol. 450, p. 573. https://doi.org/10.1042/BJ20121639

    Article  CAS  Google Scholar 

  34. Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H-E., Rajashekar, C.B., Williams, T.D., and Wang, X., Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis, J. Biol. Chem., 2002, vol. 277, p. 3199. https://doi.org/10.1074/jbc.M205375200

    Article  CAS  Google Scholar 

  35. Shishova, M.F. and Emelyanov, V.V., Changes in the proteome and lipidome of plant cell membranes during development, Russ. J. Plant Physiol., 2021, vol. 68, p. 800. https://doi.org/10.31857/S001533032105016X

    Article  CAS  Google Scholar 

  36. Su, K., Bremer, D.J., Jeannotte, R., Welti, R., and Yang, C., Membrane lipid composition and heat tolerance in cool-season turgrasses, including a hybrid bluegrass, J. Am. Soc. Hortic. Sci., 2009, vol. 134, p. 511. https://doi.org/10.21273/JASHS.134.5.511

    Article  Google Scholar 

  37. Zhigacheva, I.V., Burlakova, E.B., Misharina, T.A., Terenina, M.B., Krikunova, N.I., Generozova, I.P., Shugaev, A.G., and Fattakhov, S.G., Fatty acid composition of membrane lipids and energetics of mitochondria of pea seedlings under conditions of water deficiency, Russ. J. Plant Physiol., 2013, vol. 60, p. 205. https://doi.org/10.1134/S1607672911020104

    Article  CAS  Google Scholar 

  38. Los, D.A., Mironov, K.S., and Allakhverdiev, S.I., Regulatory role of membrane fluidity in gene expression and physiological functions, Photosynth. Res., 2013, vol. 116, p. 489. https://doi.org/10.1007/s11120-013-9823-4

    Article  CAS  PubMed  Google Scholar 

  39. Badea, C. and Basu, S.K., The effect of low temperature on metabolism of membrane lipids in plants and associated gene expression, Plant OMICS, 2009, vol. 2, p. 78. https://www.pomics.com/Saikat_2_2_2009_78_84.pdf.

    CAS  Google Scholar 

  40. Demin, I.N., Naraikina, N.V., Tsydendambaev, V.D., Moshkov, I.E., and Trunova, T.I., Introduction of the desA-12-acyl-lipid desaturase gene of cyanobacteria increases resistance of potato plants to oxidative stress caused by hypothermia, Russ. J. Plant Physiol., 2008, vol. 55, p. 710.

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

The work was carried out using the equipment of the Bioanalytics Central Analytical Center of Siberian Institute of Plant Physiology and Biochemistry (Siberian Branch, Russian Academy of Sciences, Irkutsk).

Funding

This work was carried out within the framework of a project financed by the state budget (no. 122041100052-0).

Author information

Authors and Affiliations

  1. Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences, Irkutsk, Russia

    N. V. Ozolina, I. S. Kapustina, V. V. Gurina, E. V. Spiridonova & V. N. Nurminsky

Authors
  1. N. V. Ozolina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. S. Kapustina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. V. Gurina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. V. Spiridonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. N. Nurminsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. V. Ozolina.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Abbreviations: FA—fatty acids; SFA—saturated fatty acids; UFA—unsaturated fatty acids; SP—sphingolipids; DGDG—digalactosyldiacylglycerides; MGDG—monogalactosyldiacylglycerides; PA—phosphatidic acid; PC—phosphatidylcholines; PE—phosphatidylethanolamines; PG—phosphatidylglycerols; PI—phosphatidylinositols; PS—phosphatidylserines.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozolina, N.V., Kapustina, I.S., Gurina, V.V. et al. Influence of Oxidative Stress upon the Lipid Composition of Raft Structures of the Vacuolar Membrane. Russ J Plant Physiol 71, 29 (2024). https://doi.org/10.1134/S102144372460449X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S102144372460449X

Keywords:

Search

Navigation