Advertisement

Russian Journal of Plant Physiology

, Volume 65, Issue 6, pp 784–800 | Cite as

Very Long-Chain Fatty Acids in Composition of Plant Membrane Lipids

  • A. V. Zhukov
Reviews
  • 1 Downloads

Abstract

Literary data on very long-chain fatty acids (VLCFAs) that are present in polar lipids of the plant cell membranes are discussed. Large amounts of VLCFA are found in polar lipids of some cellular organelles as well as in nonextractable lipids from diverse plant objects, where the influence of surface lipids on the relative content of these FAs is excluded. In some plants, the VLCFA fraction in membrane lipids increases under several kinds of stress. Amounts and diversity of VLCFAs are lower in flowering plants as compared with the representatives of more ancient taxons—gymnosperms, ferns, and marine algae. Presence of VLCFAs in the composition of annular lipids of the cell membranes is assumed. Biosynthesis of VLCFAs, enzymes involved in the process, and encoding genes are discussed.

Keywords

plants very long-chain fatty acids cell membranes polar lipids fatty acid biosynthesis stress 

Abbreviations

ACC

acetyl–CoA carboxylase

ACP

acyl-carrying protein

DGDG and MGDG

di- and monogalactosyldi-acylglicerol

ECR

trans-2,3-enoyl–ACP reductase

ER

endoplsmic reticulum

HCD

3-hydroxyacyl–ACP dehydratase

KCR

3-ketoacyl–ACP reductase

KCS

3-ketoacyl–CoA-synthase

LACS

LACS—long-chain acyl–CoA-synthetase

PG, PI, PS, PC, and PE

phosphatidyl glycerol, -inositol, -serine, -choline, and -ethanolamine

PL

phospholipid

SQDG

sulfoquinovosyl diacylglycerol

TAG

triacylglycerol

VLCFA

very long-chain fatty acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Denic, V. and Weissman, J.S., A molecular caliper mechanism for determining very long-chain fatty acid length, Cell, 2007, vol. 130, pp. 663–677.CrossRefPubMedGoogle Scholar
  2. 2.
    Shepherd, T., Robertson, G.W., Griffiths, D.W., and Birch, A.N.E., Epicuticular wax composition in relation to aphid infestation and resistance in red raspberry (Rubus idaeus L.), Phytochemistry, 1999, vol. 52, pp. 1239–1254.CrossRefGoogle Scholar
  3. 3.
    Zhukov, A.V. and Vereshchagin, A.G., Composition features of individual fractions of polar lipids from soybean seeds, Sov. Plant Physiol., 1980, vol. 27, pp. 390–398.Google Scholar
  4. 4.
    Lü, S., Song, T., Kosma, D.K., Parsons, E.P., Rowland, O., and Jenks, M.A., Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis, Plant J., 2009, vol. 59, pp. 553–564.CrossRefPubMedGoogle Scholar
  5. 5.
    Denisova, E.V. and Mazyarkina, T.V., Geneticheskie osnovy selektsii rapsa (Brassica napus L.) na uluchshenie biokhimicheskikh kachestv semyan (Genetic Basis of Brassica napus L. Selection for Improving the Biochemical Quality of Seeds), Novosibirsk: Inst. Cytol. Genet., Sib. Otd., Russ. Acad. Sci., 2010.Google Scholar
  6. 6.
    Wu, G., Truksa, M., Datla, N., Vrinten, P., Bauer, J., Zank, T., Cirpus, P., Heinz, E., and Qiu, X., Stepwise engineering to produce high yields of very long-chain polyunsaturated fatty acids in plants, Nat. Biotech., 2005, vol. 23, pp. 1013–1017.CrossRefGoogle Scholar
  7. 7.
    Bigogno, C., Khozin-Goldberg, I., Boussiba, S., Vonshak, A., and Cohen, Z., Lipid and fatty acid composition of the green oleagineous alga Parietochloris incise, the richest plant source of arachidonic acid, Phytochemistry, 2002, vol. 60, pp. 497–503.CrossRefPubMedGoogle Scholar
  8. 8.
    Cassagne, C., Lessire, R., Bessoule, J.J., Moreau, P., Creach, A., Schneider, F., and Sturbois, B., Biosynthesis of very long chain fatty acids in higher plants, Prog. Lipid Res., 1994, vol. 33, pp. 55–69.CrossRefPubMedGoogle Scholar
  9. 9.
    Bach, L. and Faure, J.-D., Role of very-long-chain fatty acids in plant development, when chain length does matter, C. R. Biol., 2010, vol. 333, pp. 361–370.CrossRefPubMedGoogle Scholar
  10. 10.
    Haslam, T.M. and Kunst, L., Extending the story of very-long-chain fatty acids elongation, Plant Sci., 2013, vol. 210, pp. 93–107.CrossRefPubMedGoogle Scholar
  11. 11.
    Millar, A.A., Wrischer, M., and Kunst, L., Accumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology, Plant Cell, 1998, vol. 10, pp. 1889–1902.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Lessire, R., Hartmann-Bouillon, M.-A., and Cassagne, C., Very-long-chain fatty acids: occurrence and biosynthesis in membrane fractions from etiolated maize coleoptiles, Phytochemistry, 1982, vol. 21, pp. 55–59.CrossRefGoogle Scholar
  13. 13.
    Bohn, M., Heinz, E., and Lüthje, S., Lipid composition of plasma membranes isolated from corn (Zea mays L.) roots, Arch. Biochem. Biophys., 2001, vol. 387, pp. 35–40.CrossRefPubMedGoogle Scholar
  14. 14.
    Kuiper, P.J. and Stuiver, B., Cyclopropane fatty acids in relation to earliness in spring and drought tolerance in plants, Plant Physiol., 1972, vol. 49, pp. 307–309.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Murata, N., Sato, N., and Takahashi, N., Very-longchain saturated fatty acids in phosphatidylserine from higher plant tissues, Biochim. Biophys. Acta, 1984, vol. 795, pp. 147–150.CrossRefGoogle Scholar
  16. 16.
    Zhukov, A.V., Stefanov, K.L., and Vereshchagin, A.G., The qualitative composition of individual classes of polar lipids from soybean seeds, Sov. Plant Physiol., 1987, vol. 34, pp. 518–527.Google Scholar
  17. 17.
    Mckillican, M. and Sims, R.P.A., Lipid changes in maturing oil bearing plants. III. Changes in lipid classes in flax and sunflower oils, J. Am. Oil Chem. Soc., 1963, vol. 40, pp. 108–113.CrossRefGoogle Scholar
  18. 18.
    Khor, H.-T., Lipids and fatty acid composition of developing winged bean seeds, Phytochemistry, 1985, vol. 24, pp. 856–857.CrossRefGoogle Scholar
  19. 19.
    Furt, F., Simon-Plas, F., and Mongrand, S., Lipids of the plant plasma membrane, in The Plant Plasma Membrane. Plant Cell Monographs, Murphy, A.S., Eds., Berlin, Heidelberg: Springer-Verlag, 2011, vol. 19, pp. 3–30.CrossRefGoogle Scholar
  20. 20.
    Zhigacheva, I.V., Burlakova, E.B., Misharina, T.A., Terenina, M.B., Krikunova, N.I., Generozova, I.P., Shugaev, A.G., and Fattokhov, S.G., Fatty acid composition of membrane lipids and energy metabolism in mitochondria of pea seedlings under water deficit, Russ. J. Plant Physiol., 2013, vol. 60, pp. 212–220.CrossRefGoogle Scholar
  21. 21.
    Sen Gupta, A.K., Fatty acids of soyabean phosphatides and glycerides with special reference to the oxydised fatty acids, Fett. Lipid, 1974, vol. 77, pp. 440–442. https://doi.org/10.1002/lipi.19740761004 Google Scholar
  22. 22.
    Sriti, J., Wannes, W.A., Talou, T., Mhamdi, B., Hamdaoui, G., and Marzouk, B., Lipids, fatty acid and tocol distribution of coriander fruit’s different parts, Ind. Crops Prod., 2010, vol. 31, pp. 294–300.CrossRefGoogle Scholar
  23. 23.
    Xue, C., Hu, Y., Saito, H., Zhang, Z., Li, Z., Cai, Y., Ou, C., Lin, H., and Imbs, A.B., Molecular species composition of glycolipids from Spirulina platensis, Food Chem., 2002, vol. 77, pp. 9–13.CrossRefGoogle Scholar
  24. 24.
    Sanina, N.M., Goncharova, S.N., and Kostetsky, E.Y., Fatty acid composition of individual polar lipid classes from marine macrophytes, Phytochemistry, 2004, vol. 65, pp. 721–730.CrossRefPubMedGoogle Scholar
  25. 25.
    Kylin, A., Kuiper, P.J.C., and Hansson, G., Lipids from sugar beet in relation to the preparation and properties of (sodium + potassium)-activated adenosine triphosphatases, Physiol. Plant., 1972, vol. 26, pp. 271–278.CrossRefGoogle Scholar
  26. 26.
    Ivanova, T.I., Myasoedov, N.A., Pchelkin, V.P., Tsydendambaev, V.D., and Vereshchagin, A.G., Increased content of very-long-chain fatty acids in the lipids of halophyte vegetative organs, Russ. J. Plant Physiol., 2009, vol. 56, pp. 787–794.CrossRefGoogle Scholar
  27. 27.
    Rozentsvet, O.A., Nesterov, V.N., and Bogdanova, E.S., Membrane-forming lipids of wild halophytes growing under the conditions of Prieltonie of South Russia. http://dx.doi.org/10.1016/j.phytochem.2014.05.00710.1016/j.phytochem.2014.05.007.
  28. 28.
    Makarenko, S.P., Konstantinov, Yu.M., Khotimchenko, S.V., Konenkina, T.A., and Arziev, A.Sh., Fatty acid composition of mitochondrial membrane lipids in cultivated (Zea mays) and wild (Elymus sibiricus) grasses, Russ. J. Plant Physiol., 2003, vol. 50, pp. 487–491.CrossRefGoogle Scholar
  29. 29.
    Belenko, E.L., Datunashvili, E.N., Tsydendambaev, V.D., and Vereshchagin, A.G., Absolute content and fatty acid composition of lipids from ripening grape berries, Sov. Plant Physiol., 1984, vol. 31, pp. 482–488.Google Scholar
  30. 30.
    Tsydendambaev, V.D. and Vereshchagin, A.G., Study of sugar beet root lipids in connection with the function of sugar accumulation. 1. Fatty acid composition of lipids from the resting root parenchyma, Sov. Plant Physiol., 1980, vol. 27, pp. 619–625.Google Scholar
  31. 31.
    Shayakhmetova, I.Sh., Trunova, T.I., Tsydendambaev, V.D., and Vereshchagin, A.G., Role of cell membrane lipids in frost hardening of winter wheat leaves and tillering nodes, Sov. Plant Physiol., 1990, vol. 37, pp. 1186–1195.Google Scholar
  32. 32.
    Zhukov, A.V. and Vereshchagin, A.G., Device for quantitative extraction of lipids from plant material, Sov. Plant Physiol., 1974, vol. 21, pp. 659–663.Google Scholar
  33. 33.
    Bach, L., Michaelson, L.V., Haslam, R., Bellec, Y., Gissot, L., Marion, J., Da Costa, M., Boutin, J.-P., Miquel, M., Teller, F., Domergue, F., Markham, J.E., Beaudoin, F., Napier, J.A., and Faure, J.-D., The plant very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 14727–14731.CrossRefPubMedGoogle Scholar
  34. 34.
    Zheng, H., Rowland, O., and Kunst, L., Disruptions of the Arabidopsis Enoil-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis, Plant Cell, 2005, vol. 17, pp. 1467–1481.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Roudier, F., Gissot, L., Beaudoin, F., Haslam, R., Michaelson, L., Marion, J., Molino, D., Lima, A., Bach, L., Morin, H., Tellier, F., Palauqui, J.-C., Bellec, Y., Renne, C., Miquel, M., et al., Very-long-chain fatty acids involved in polar auxin transport and developmental patterning in Arabidopsis, Plant Cell, 2010, vol. 22, pp. 364–375.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Kajiwara, N., Furutani, M., Hibara, K., and Tasaka, M., The GURKE gene encoding an acetyl-CoA carboxylase is required for partitioning the embrio apex into three subregions in Arabidopsis, Plant Cell Physiol., 2004, vol. 45, pp. 1122–1128.CrossRefPubMedGoogle Scholar
  37. 37.
    Millar, A. and Kunst, L., Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme, Plant J., 1997, vol. 12, pp. 121–131.CrossRefPubMedGoogle Scholar
  38. 38.
    Baud, S., Guyon, V., Kronenberger, J., Wuilleme, S., Miquel, M., Caboche, M., Lepiniec, L., and Rochat, C., Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embrio development in Arabidopsis, Plant J., 2003, vol. 33, pp. 75–86.CrossRefPubMedGoogle Scholar
  39. 39.
    Schneiter, R., Hitomi, M., Ivessa, A.S., Fasch, E.-V., Kohlwein, S.D., and Tartakoff, A.M., A yeast acetyl coenzyme A carboxylase mutant links very-long-chain fatty acid synthesis to the structure and function of the nuclear membrane-pore complex, Mol. Cell Biol., 1996, vol. 16, pp. 7161–7172.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Schneiter, R., Brugger, B., Amman, C.M., Prestwich, G.D., Epand, R.F., Zelling, G., Wieland, F.T., and Epand, R.M., Identification and biophysical characterization of a very-long-chainfatty-acid-substituted phosphatidylinositol in yeast subcellular membranes, Biochem. J., 2004, vol. 381, pp. 941–949.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Marelli, M., Lusk, C.P., Chan, H., Aitchison, J.D., and Wozniak, R.W., A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope, J. Cell Biol., 2001, vol. 153, pp. 709–724.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Mongrand, S., Bados, A., Patouille, B., Lacomblez, C., Chavent, M., Cassagne, C., and Bessoule, J.-J., Taxonomy of Gymnospermae: multivariate analyses of leaf fatty acids composition, Phytochemistry, 2001, vol. 58, pp. 101–115.CrossRefPubMedGoogle Scholar
  43. 43.
    Zhukov, A.V., Kuznetsova, E.I., Sidorov, R.A., Pchelkin, V.P., and Tsydendambaev, V.D., Fatty acid composition of lipids from leaves and strobila of Cycas revoluta, Russ. J. Plant Physiol., 2018, vol. 65, pp. 23–29.CrossRefGoogle Scholar
  44. 44.
    Jamieson, G.R. and Reid, E.H., The fatty acids composition of fern lipids, Phytochemistry, 1975, vol. 14, pp. 2229–2232.CrossRefGoogle Scholar
  45. 45.
    Robinson, P.M., Smith, D.L., Safford, R., and Nichols, B.W., Lipid metabolism in the fern Polipodium vulgare, Phytochemistry, 1973, vol. 12, pp. 1377–1381.CrossRefGoogle Scholar
  46. 46.
    Dembitsky, V.M. and Rezanka, T., Distribution of diacylglycerylhomoserines, phospholipids and fatty acids in thirteen moss species from Southwestern Siberia, Biochem. Syst. Ecol., 1995, vol. 23, pp. 71–78.CrossRefGoogle Scholar
  47. 47.
    Los', D.A., Desaturazy zhirnykh kislot (Fatty Acids Desaturases), Moscow: Nauchnyi Mir, 2014.Google Scholar
  48. 48.
    Leonard, A.E., Pereira, S.L., Sprecher, H., and Huang, Y.S., Elongation of long-chain fatty acids, Prog. Lipid Res., 2004, vol. 43, pp. 36–54.CrossRefPubMedGoogle Scholar
  49. 49.
    Kheldt, G.V., Biokhimiya rastenii (Plant Biochemistry), Moscow: BINOM, Lab. Znanii, 2011.Google Scholar
  50. 50.
    Kihara, A., Very long-chain fatty acids: elongation, physiology and related disorders, J. Biochem., 2012, vol. 152, pp. 387–395.CrossRefPubMedGoogle Scholar
  51. 51.
    Neess, D., Bek, S., Engelsby, H., Gallego, S.F., and Faergeman, N.J., Long-chain acyl-CoA esters in metabolism and signaling: role of acyl-CoA binding proteins, Prog. Lipid Res., 2015, vol. 59, pp. 1–25.CrossRefPubMedGoogle Scholar
  52. 52.
    Fehling, E. and Mukherjee, K.D., Acyl-CoA elongase from a higher plant (Lunaria annua): metabolic intermediates of very-long-chain acyl-CoA products and substrate specificity, Biochim. Biophys. Acta, 1991, vol. 1082, pp. 239–246.CrossRefPubMedGoogle Scholar
  53. 53.
    Fulda, M., Shockey, J., Werber, M., Wolter, F.P., and Heinz, E., Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid ß-oxidation, Plant J., 2002, vol. 32, pp. 93–103.CrossRefPubMedGoogle Scholar
  54. 54.
    Siegenthaler, P.A., Molecular organization of acyl lipids in photosynthetic membranes of higher plants, in Lipids in Photosynthesis: Structure, Function and Genetics, Siegenthaler, P.A. and Murata, N., Eds., Dordrecht: Springer, 1998, vol. 6, pp. 71–77.Google Scholar
  55. 55.
    Tai, H. and Jaworski, J.G., 3-Ketoacyl-acyl carrier protein synthase III from spinach (Spinacia oleracea) is not similar to other condensing enzymes of fatty acids synthase, Plant Physiol., 1993, vol. 103, pp. 1361–1367.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Abbadi, A., Brummel, M., and Spener, F., Knockout of the regulatory site of 3-ketoacyl-ACP synthase III enhances short- and medium-chain acyl-ACP synthesis, Plant J., 2000, vol. 24, pp. 1–9.CrossRefPubMedGoogle Scholar
  57. 57.
    Jessen, D., Roth, C., Wiermer, M., and Fulda, M., Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis, Plant Physiol., 2015, vol. 167, pp. 351–366.CrossRefPubMedGoogle Scholar
  58. 58.
    Von Wettstein-Knowles, P., Biosynthesis and genetics of waxes. Waxes: Chemistry, in Molecular Biology and Functions, Hamilton R.J., Ed., Ayr: Oily Press, 1995, pp. 91–129.Google Scholar
  59. 59.
    Hitchcock, C. and Nichols, B.W., Plant Lipid Biochemistry, New York: Academic, 1971.Google Scholar
  60. 60.
    Todd, J., Post-Beitenmiller, D., and Jaworski, J.G., KCS1 encodes a fatty acids elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana, Plant J., 1999, vol. 17, pp. 119–130.CrossRefPubMedGoogle Scholar
  61. 61.
    Kim, M.J., Shin, J.S., Kim, J.K., and Suh, M.C., Genomic structures and characterization of the 5'-flanking regions of acyl carrier protein and ?4-palmitoil- ACP desaturase genes from Coriandrum sativum, Biochim. Biophys. Acta, 2005, vol. 1730, pp. 235–244.CrossRefPubMedGoogle Scholar
  62. 62.
    Sperling, P., Schmidt, H., and Heinz, E., A cytochrome-b5-containing fusion protein similar to plant acyl lipid desaturases, Eur. J. Biochem., 1995, vol. 232, pp. 798–805.CrossRefPubMedGoogle Scholar
  63. 63.
    Schwartzbeck, J.L., Jung, S., Abbott, A.G., Mosley, E., Lewis, S., Pries, G.L., and Powell, G.L., Endoplasmic oleoyl-PC desaturase references the second double bond, Phytochemistry, 2001, vol. 57, pp. 643–652.CrossRefPubMedGoogle Scholar
  64. 64.
    Yadav, N.S., Wierzbicki, A., Aegerter, M., Caster, C.S., Pérez-Grau, L., Kinney, A.J., Hitz, W.D., Booth, J.R., Jr., Schweiger, B., and Stecca, K.L., Cloning of higher plant-3 fatty acid desaturases, Plant Physiol., 1993, vol. 103, pp. 467–476.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Iskandarov, U., Khozin-Goldberg, I., and Cohen, Z., Identification and characterization of D12, D6, and D5 desaturases from the green microalga Parietochloris incisa, Lipids, 2010, vol. 45, pp. 519–530.CrossRefPubMedGoogle Scholar
  66. 66.
    Dyer, J.M. and Millen, R.T., Immunocytological localization of two plant fatty acid desaturases in the endoplasmic reticulum, FEBS Lett., 2001, vol. 494, pp. 44–47.CrossRefPubMedGoogle Scholar
  67. 67.
    Goodwin, T.V. and Mercer, E.I., Introduction to Plant Biochemistry, London: Pergamon, 1983.Google Scholar
  68. 68.
    Chen, J.I. and Beversdorf, W.D., Fatty acid inheritance in microspore-derived populations of spring rapeseed (Brassica napus L.), Theor. Appl. Genet., 1990, vol. 80, pp. 465–469.PubMedGoogle Scholar
  69. 69.
    Mazliak, P., Desaturation processes in fatty acid and acyl lipid biosynthesis, J. Plant Physiol., 1994, vol. 143, pp. 399–406.CrossRefGoogle Scholar
  70. 70.
    Sprecher, H., Luthria, D.L., Mohammed, B.S., and Baykousheva, S.P., Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids, J. Lipid Res., 1995, vol. 36, pp. 2471–2477.PubMedGoogle Scholar
  71. 71.
    Wallis, J.G. and Browse, J., The 8-desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids, Arch. Biochem. Biophys., 1999, vol. 365, pp. 307–316.CrossRefPubMedGoogle Scholar
  72. 72.
    Agrawal, V.P., Lessire, R., and Stumpf, P.K., Biosynthesis of very long chain fatty acids in microsomes from epidermal cells of Allium porrum L., Arch. Biochem. Biophys., 1984, vol. 230, pp. 580–589.CrossRefPubMedGoogle Scholar
  73. 73.
    Popov, V.N., Antipina, O.V., Pchelkin, V.P., and Tsydendambaev, V.D., Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening, Russ. J. Plant Physiol., 2012, vol. 59, pp. 177–182.CrossRefGoogle Scholar
  74. 74.
    Sanina, N.M., Goncharova, S.N., and Kostesky, E.Y., Seasonal changes in thermotropic behavior of phospho- and glycolipids from Laminaria japonica, in Advanced Research on Plant Lipids, Murata, N., Eds., Dordrecht: Kluwer, 2003, pp. 385–388.CrossRefGoogle Scholar
  75. 75.
    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.CrossRefPubMedGoogle Scholar
  76. 76.
    Kuiper, P.J.C., Lipids in grape roots in relation to chloride transport, Plant Physiol., 1968, vol. 43, pp. 1367–1371.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Tsydendambaev, V.D., Ivanova, T.I., Khalilova, L.A., Kurkova, E.B., Myasoedov, N.A., and Balnokin, Yu.V., Fatty acid composition of lipids in vegetative organs of the halophyte Suaeda altissima under different levels of salinity, Russ. J. Plant Physiol., 2013, vol. 60, pp. 661–671.CrossRefGoogle Scholar
  78. 78.
    Azachi, M., Sadka, A., Fishtr, M., Goldshlag, P., Gokhman, I., and Zamir, A., Salt induction of fatty acid elongase and membrane lipid modifications in the extreme halotolerant alga Dunaliella salina, Plant Physiol., 2002, vol. 129, pp. 1320–1329.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations