Abstract
The composition of vacuolar membrane phospholipids in the taproot of red beet (Beta vulgaris L.), cv. Modana, was determined at normal conditions and under different types of stress (hypo- and hyperosmotic and oxidative stress). The experiments have shown that, among vacuolar membrane phospholipids in red beet taproot, phosphatidylcholines and phosphatidylethanolamines dominated and accounted for 70% of total phospholipids. It is interesting that the content of phosphatidic acid was high (20% of total phospholipids of the vacuolar membrane). Stress effects brought about changes in the composition of membrane phospholipids, which may be an element of phenotypic adaptation. Under hypoosmotic stress, reliable changes in the content of phosphatidic acid were observed, hyperosmotic stress was associated with changes in the level of phosphatidylcholines and phosphatidylinositols, and oxidative stress was notable for changes in the content of phosphatidylethanolamines and phosphatidylserines. The most significant changes were observed in the classes of phospholipids that may be involved in structural modification of membranes associated with transformation of their bilayer lamellar structure into hexagonal. These phospholipids comprise phosphatidic acid, phosphatidylcholines, and phosphatidylethanolamines. Revealed changes in the content of these phospholipids may alter the ratio between lamellar bilayer and nonbilayer hexagonal lipid structures in the vacuolar membrane and act as an important adaptation mechanism ensuring protection against stress.
Similar content being viewed by others
Abbreviations
- PA:
-
phosphatidic acid
- PC:
-
phosphatidylcholines
- PE:
-
phosphatidylethanolamines
- PI:
-
phosphatidylinositols
- PL:
-
phospholipids
- PS:
-
phosphatidylserines
References
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, J. Biol. Chem., 2002, vol. 277, pp. 31994–32002.
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. Hortic. Sci., 2009, vol. 134, pp. 511–520.
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, pp. 59–69.
Alvarez-Pizarro, J., Gomes-Filho, C., de Lacerda, C., Alencar, N., and Prisco, J., Salt-induced changes on H+-ATPase activity, sterol and phospholipid content and lipid peroxidation of root plasma membrane from dwarf-cashew (Anacardium occidentale L.) seedlings, Plant Growth Regul., 2009, vol. 59, pp. 125–135.
Martinez-Ballesta, M. and Carvajal, M., Mutual interactions between aquaporins and membrane components, Front. Plant Sci., 2016, vol. 7: 1322. doi 10.3389/fpls.2016.01322
Uemura, M. and Steponkus, P.L., A contrast of the plasma membrane lipid composition of oat and rye leaves in relation to freezing tolerance, Plant Physiol., 1994, vol. 104, pp. 479–496.
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., 2016, vol. 39, pp. 787–803.
Zhang, C., Hicks, G.R., and Raikhel, V., Molecular composition of plant vacuoles: important but less understood regulations and roles of tonoplast lipids, Plants, 2015, vol. 4, pp. 320–333.
Lin, Q., Wang, Y.M., Nose, A., Hong, H.T., and Agarie, S., Effects of high night temperature on lipid and protein compositions in tonoplasts isolated from Ananas comosus and Kalanchoe pinnata leaves, Biol. Plant., 2008, vol. 52, pp. 59–64.
Zhou, Y., Pan, X., Qu, H., and Underhill, S.J., Tonoplast lipid composition and proton pump of pineapple fruit during low-temperature storage and blackheart development, J. Membr. Biol., 2014, vol. 247, pp. 429–439.
Salyaev, R.K., Kuzevanov, V.Ya., Khaptagaev, S.B., and Kopytchuk, V.N., Isolation and purification of vacuoles and vacuolar membranes from plant cells, Sov. Plant Physiol., 1981, vol. 28, pp. 1295–1305.
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, pp. 859–871.
Bligh, E.G. and Dyer, W.J., A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol., 1959, vol. 37, pp. 911–917.
Vaskovsky, V.E., Kostetsky, E.Y., and Vasendin, J.M., A universal reagent for phospholipid analysis, J. Chromatogr., 1975, vol. 114, pp. 129–141.
Ozolina, N.V., Gurina, V.V., Nesterkina, I.S., Dudareva, L.V., Katyshev, A.I., and Nurminskii, V.N., Fatty acid composition of total lipids in vacuolar membrane under abiotic stress, Biochemistry (Moscow), Suppl. Ser. A: Membr. Cell Biol., 2017, vol. 34, pp. 63–69.
Wu, J., 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, pp. 852–858.
Campos, P.S., Quartin, V., Ramalho, J.C., and Nunes, M.A., Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants, J. Plant Physiol., 2003, vol. 160, pp. 283–292.
Bohn, M., Lüthje, S., Sperling, P., Heinz, E., and Dörffling, K., Plasma membrane lipid alterations induced by cold acclimation and abscisic acid treatment of winter wheat seedlings differing in frost resistance, J. Plant Physiol., 2007, vol. 164, pp. 146–156.
Tavernier, E. and Pugin, A., Phospholipase activities associated with the tonoplast from Acer pseudoplatanus cells: identification of a phospholipase A1 activity, Biochem. Biophys. Acta, 1995, vol. 1233, pp. 118–122.
Behzadipour, M., Ratajczak, R., Faist, K., Pawlitschek, P., Trémolières, A., and Kluge, M., Phenotypic adaptation of tonoplast fluidity to growth temperature in the CAM plant Kalanchoe daigremontiana Ham. et Per. is accompanied by changes in the membrane phospholipid and protein composition, J. Membr. Biol., 1998, vol. 166, pp. 61–70.
Norberg, P. and Lijenberg, C., Lipids of membranes prepared from oat root cells, Plant Physiol., 1991, vol. 96, pp. 1136–1141.
Su, K., Bremer, D.J., Jeannotte, R., Welti, R., and Yang, C., Membrane lipid composition and heat tolerance in cool-season turfgrasses, including a hybrid bluegrass, J. Am. Soc. Hortic. Sci., 2009, vol. 134, pp. 511–520.
Sankhagowit, S., Lee, E.Y., Wong, C.L., and Malmstadt, N., Oxidation of membrane curvature-regulating phosphatidylethanolamine lipid results in formation of bilayer and cubic structures, Langmuir, 2016, vol. 32, pp. 2450–2457.
Berglund, A.H., Quaetacci, M.F., Calucci, L., Navari-Izzo, F., Pinzino, C., and Liljenberg, C., Alterations of wheat root plasma lipid composition induced by copper stress result in changed physicochemical properties of plasma membrane lipid vesicles, Biochem. Biophys. Acta, 2002, vol. 1564, pp. 466–472.
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., 2013, vol. 4: 1. doi 10.3389/tpls.2013.00001
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, pp. 573–581.
Okazaki, Y. and Saito, K., Roles of lipids as signaling molecules and mitigators during stress response in plants, Plant J., 2014, vol. 79, pp. 584–596.
Almsherqi, Z.A., Kohlwein, S.D., and Deng, Y., Cubic membranes: a legend beyond the Flatland* of cell membrane organization, J. Cell Biol., 2006, vol. 173, pp. 839–844.
De Kruijff, B., Lipid polimorfism and biomembrane function, Curr. Opin. Chem. Biol., 1997, vol. 1, pp. 564–569.
Xue, H.W., Chen, X., and Me, Y., Function and regulation of phospholipid signaling in plants, Biochem. J., 2009, vol. 421, pp. 145–156.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N.V. Ozolina, V.V. Gurina, I.S. Nesterkina, V.N. Nurminskii, 2018, published in Fiziologiya Rastenii, 2018, Vol. 65, No. 5, pp. 358–365.
Rights and permissions
About this article
Cite this article
Ozolina, N.V., Gurina, V.V., Nesterkina, I.S. et al. Dynamics of Phospholipid Content in the Vacuolar Membrane of Red Beet Taproots Exposed to Abiotic Stress. Russ J Plant Physiol 65, 702–708 (2018). https://doi.org/10.1134/S1021443718040088
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443718040088