Abstract
Lipid–protein microdomains (presumably rafts) of the plasmalemma isolated from the beetroots subjected to hyperosmotic stress and hypoosmotic stress were studied. In these microdomains, the variations in the composition of total lipids, sterols, and fatty acids were observed. These variations differed under hypo- and hyperosmotic types of stress. We presumed that such variations were bound up with different strategies, which are probably related to protecting the cell from osmotic stress. One of the protection tendencies might be related, in our opinion, to credible growth of the content of such lipids as sterols and sterol esters, which are considered as raft-forming. Under osmotic stress, these lipids can contribute to the formation of both new raft structures and new membrane contacts of plasmalemma with intracellular organelles. Another protection tendency may be bound up with the redistribution of membrane phospholipids and phosphoglycerolipids possibly to stabilize the membrane’s lamellar structure, which is ensured by credible growth of the content of such lipids as phosphatidylcholines, phosphatidylinositols, and digalactosyldiacylglycerol. The participation of lipid–protein microdomains in the adaptive mechanisms of plant cells may, in our opinion, also be bound up with the redistribution of membrane sterols, which (redistribution) in a number of variants may provoke credible growth in the content of cholesterol or “anti-stress” sterols (campesterol and stigmasterol). So, according to our results, the variations in the content of the plasmalemma lipid–protein microdomains take place under osmotic stress. These variations may influence the functioning of plasmalemma and take part in the adaptive mechanisms of plant cells.
Graphic Abstract
Similar content being viewed by others
Data Availability
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
Abbreviations
- DAG:
-
Diacylglycerol
- DGDG:
-
Digalactosyldiacylglycerol
- DPG:
-
Diphosphatidylglycerol
- FA:
-
Fatty acid
- GC–MS:
-
Gas chromatography–mass spectrometry
- GL:
-
Glycoglycerolipid
- MG:
-
Monoglyceride
- MGDG:
-
Monogalactosyldiacylglycerol
- NL:
-
Neutral lipid
- PA:
-
Phosphatidic acid
- PC:
-
Phosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PG:
-
Phosphatidylglycerol
- PI:
-
Phosphatidylinositol
- PL:
-
Phospholipid
- PS:
-
Phosphatidylserine
- SFA:
-
Saturated fatty acid
- SL:
-
Sphingolipid
- TAG:
-
Triacylglycerol
- TLC:
-
Thin-layer chromatography
- USFA:
-
Unsaturated fatty acid
References
Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE, Travis A (2009) Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J Cell Physiol 218:537–548. https://doi.org/10.1002/jcp.21623
Asano A, Nelson JL, Zhang S, Travis A (2010) Characterization of proteomes associating with three distinct membrane raft sub-types murine sperm. Proteomics 10:3494–3505
Badea C, Basu SK (2009) The effect of low temperature on metabolism of membrane lipids in plants and associated gene expression. Plant Omics 2:78–84
Bligh E, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bretscher MS, Munro S (1998) Cholesterol and the golgi apparatus. Science 261:1280–1281. https://doi.org/10.1126/science.8362242
Brown RE (1998) Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J Cell Sci 111:1–9
Cassim AM, Gouguet P, Gronnier J, Laurent N, Germain V, Grison M, Boutté Y, Gerbeau-Pissot P, Simon-Plas F, Mongrand S (2019) Plant lipids: key players of plasma membrane organization and function. Prog Lipid Res 73:1–27. https://doi.org/10.1016/j.plipres.2018.11.002
Catala A (2012) Lipid peroxidation modifies the picture of membranes from the “Fluid Mosaic Model” to the “Lipid Whisker Model.” Biochemie 94:101–109. https://doi.org/10.1016/j.biochi.2011.09.025
Christie WW (1988) Equivalent chain lengths of methyl ester derivatives of fatty acids on gas chromatography: a reappraisal. J Chromatogr 447:305–314. https://doi.org/10.1016/0021-9673(88)90040-4
Conrard L, Stommen A, Cloos A-S, Steinkuhler J, Dimova R, Pollet H, Tyteca D (2018) Spatial relationship and functional relevance of three lipid domain populations at the erythrocyte surface. Cell Physiol Biochem 51:1554–1565. https://doi.org/10.1159/000495645
Fujimoto M, Hayashi T, Su TP (2012) The role of cholesterol in the association of endoplasmic reticulum membranes with mitochondria. Biochem Biophys Res Commun 417:635–639. https://doi.org/10.1016/j.bbrc.2011.12.022
Gronnier J, Gerbeau-Pessot P, Germain V, Mongrand S, Simon-Plas F (2018) Divide and rule: plant plasma membrane organization. Trends Plant Sci 23:899–917. https://doi.org/10.1016/jtplants.2018.07.007
Grunwald C (1971) Effects of free sterols, steryl ester, and steryl glycoside on membrane permeability. Plant Physiol 48:653–655. https://doi.org/10.1104/pp.48.5.653
Guo Q, Liu L, Barkla BJ (2019) Membrane lipid remodeling in response to salinity. Int J Mol Sci 20:4264. https://doi.org/10.3390/ijms20174264
Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4:494. https://doi.org/10.3389/fpls.2013.00494
Kates M (1972) Techniques of Lipidology: Isolation, Analysis and Identification of Lipids. Elsevier, Amsterdam
Konig S, Ischebeck T, Lerche J, Stenzel I, Heilmann I (2008) Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem J 415:387–399. https://doi.org/10.1042/BJ20081306
Kumar MS, Mawlog I, Ali K, Tyagi A (2018) Regulation of phytosterol biosynthetic pathway during drought stress in rice. Plant Physiol Biochem 129:11–20. https://doi.org/10.1016/j.plaphy.2018.05.019
Laloi M, Perret A, Chatre L, Melser S, Cantrel C, Vaultier M-N, Zachowski A, Bathany K, Schmitter J-M, Vallet M, Lessire R, Hartmann M-A, Moreau P (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472. https://doi.org/10.1104/pp.106.091496
Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148:558–568. https://doi.org/10.1016/0076-6879(87)48054-3
Lefebvre B, Furt F, Hartmann M-A, Michaelson L, Carde J-P, Sargueil-Boiron F, Rossignol M, Napier J, Cullimore J, Bessoule J-J, Mongrand S (2007) Sharacterization of lipid rafts from Medicago truncatula roots plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144:402–418. https://doi.org/10.1104/pp.106.094102
Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50. https://doi.org/10.1126/science.1174621
Marsh D (2011) Pivotal surfaces in inverse hexagonal and cubic phases of phospholipids and glycolipids. Chem Phys Lipids 164:177–183. https://doi.org/10.1016/j.chemphyslip.2010.12.010
Mongrand S, Morel J, Laroche J, Claverol S, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells. J Biol Chem 279:36277–36286. https://doi.org/10.1074/jbc.M403440200
Narayanan S, Tamura PJ, Roth MR, Prasad PV, Welti R (2016) Wheat leaf lipid composition during heat stress: I. High day and night temperatures result in major lipid alteration. Plant Cell Environ 39:787–803. https://doi.org/10.1111/pce.12649
Nesterov VN, Nesterkina IS, Rozentsve OA, Ozolina NV, Salyaev RK (2017) Detection of lipid-protein microdomains (rafts) and investigation of their functional role in the chloroplast membranes of halophytes. Dokl Biochem Biophys 476:303–305. https://doi.org/10.1134/S1607672917050040
Nikulina GN (1965) Review of methods for colorimetric determination of phosphorus by “molybdenum blue.” Nauka, Leningrad
Nurminsky VN, Ozolina NV, Nesterkina IS, Kolesnikova EV, Korzun AM, Chernyshov MYu, Tikhonov NV, Tarkov MS, Salyaev RK (2011) Stability of plant vacuolar membranes under the conditions of osmotic stress and influence of redox agents. Biochem (mosc) Suppl Ser A Membr Cell Biol 5:185–190. https://doi.org/10.1134/S1990747811020048
Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584–596. https://doi.org/10.1111/tpj.12556
Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794. https://doi.org/10.1046/j.1365-313x.2000.00845.x
Ozolina NV, Nesterkina IS, Kolesnikova EV, Salyaev RK, Nurminsky VN, Rakevich AL, Martynovich EF, Yu CV (2013) Tonoplast of Beta vulgaris L. contains detergent-resistant membrane microdomains. Planta 237:859–871. https://doi.org/10.1007/s00425-012-1800-1
Ozolina NV, Gurina VV, Nesterkina IS, Nurminsky VN (2020a) Variations in the content of tonoplast lipids under abiotic stress. Planta 251:107. https://doi.org/10.1007/s00425-020-03399-x
Ozolina NV, Nesterkina IS, Gurina VV, Nurminsky VN (2020b) Non-detergent isolation of membrane structures from beet plasmalemma and tonoplast having lipid composition characteristic of rafts. J Membr Biol 253:479–489. https://doi.org/10.1007/s00232-020-00137-y
Peskan T, Westermann M, Oelmuller R (2000) Identification of low-density Triton X 100 insoluble plasma membrane microdomains in higher plants. Eur J Biochem 267:6989–6995. https://doi.org/10.1046/j.1432-1327.2000.01776.x
Piironen V, Toivo J, Lampi AM (2002) Plant sterols in cereals and cereal products. Cereal Chem 79:148–154. https://doi.org/10.1094/CCHEM.2002.79.1.148
Pike LJ (2004) Lipid rafts: Heterogeneity on the high seas. J Biochem 378:281–292. https://doi.org/10.1042/BJ20031672
Pike LJ (2005) Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim Biophys Acta 1746:260–273
Poston CN, Duong E, Cao Y, Bazemore-Walker CR (2011) Proteomic analysis of lipid raft-enriched membranes isolated from internal organelles. Biochem Biophys Res Commun 415:355–360. https://doi.org/10.1016/j.bbrc.2011.10.072
Ristic Z, Ashworth EN (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during Rapid Cold Acclimation. Protoplasma 172:111–123. https://doi.org/10.1007/BF01379368
Schuler I, Milon A, Nakatani Y, Ourisson G, Albrecht AM, Benveniste P, Hartman M-A (1991) Differential effects of plant sterols on water permeability and on acyl chain orderingof soybean phosphatidylcholine bilayers. Proc Natl Acad Sci USA 88:6926–6930. https://doi.org/10.1073/pnas.88.16.6926
Sengupta P, Baird B, Holowka D (2007) Lipid rafts, fluid/fluid phase separation, and their relevance to plasma membrane structure and function. Semin Cell Dev Biol 18:583–590. https://doi.org/10.1016/j.semcdb.2007.07.010
Senthil-Kumar M, Wang K, Mysore KS (2013) AtCYP710A1 gene-mediated stigmasterol production plays a role in imparting temperature stress tolerance in Arabidopsis thaliana. Plant Signal Behav. https://doi.org/10.4161/psb.23142
Shuler I, Durtail G, Glasser N, Benveniste P, Hartmann M-A (1990) Soybean phosphatidylcholine vesicles containing plant sterols: a fluorescence anisotropy study. Biochim Biophys Acta Biomembr 1028:82–88. https://doi.org/10.1016/0005-2736(90)90268-s
Valitova JN, Sulkarnayeva AG, Minibaeva FV (2016) Plant sterols: diversity, biosynthesis and physiological functions. Biochemistry 81:819–834. https://doi.org/10.1134/S0006297916080046
Vaskovsky VE, Latyshev NA (1975) Modified Jungnickel’s reagent for detecting phospholipids and other phosphorus compounds on thin-layer chromatograms. J Chromatogr 115:246–249. https://doi.org/10.1016/s0021-9673(00)89042-1
Vladimirov YA, Archakov AI (1972). In: Frank GM (ed) Lipid Peroxidation in Biological Membranes. Springer, Dordrecht, NL
Wu J-L, Seliskar DM, Gallagher JL (1998) Stress tolerance in the marsh plant Spartina patens: impact of NaCl on growth and root plasma membrane lipid composition. Physiol Plant 102:307–317. https://doi.org/10.1034/j.1399-3054.1998.1020219.x
Acknowledgements
This work was carried out using the equipment of Central Analytical Center “Bioanalytics” of Siberian Institute of Plant Physiology and Biochemistry (Siberian Branch of Russian Academy of Sciences, Irkutsk). This work was conducted with partial use of the Russian Foundation for Basic Research, grant No. 19-04-00013.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflict of interest regarding the publication of this article.
Ethical Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ozolina, N.V., Kapustina, I.S., Gurina, V.V. et al. Role of Plasmalemma Microdomains (Rafts) in Protection of the Plant Cell Under Osmotic Stress. J Membrane Biol 254, 429–439 (2021). https://doi.org/10.1007/s00232-021-00194-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00232-021-00194-x