Biopolym. Cell. 2008; 24(6):431-440.
Plant sulfolipid. 1. Functions
1Okanenko A. A., 1Taran N. Yu., 1Kosyk O. I.
  1. Taras Shevchenko National University of Kyiv
    64, Volodymyrska Str., Kyiv, Ukraine, 01601


Plant sulpholipid, sulfoquinovosyl diacylglycerol (SQDG) has been found almost in all photosynthetic organisms. SQDG appears to be concentrated mainly in the chloroplasts of plants, as in envelope so and in lamellar membranes. It is associated with purified chloroplast CF0-CF1 ATPase and supposed does not form lipid matrix but plays a more specific role in the catalytic activity of proteins. SQDG molecules were found in the association of the LHC II-apoproteins and are localised as prosthetic groups at the surface of native D1/D2 heterodimer. Results recent works showed that the physical properties of the PS II complex were altered by the loss of SQDG: for the stable activity PS II needs the presence of SQDG.
Keywords: glycolipid, sulfolipid, sulfoquinovosyldiacylglycerol, SQDG


[1] Kenrick J., Bishop D. The fatty acid composition of phosphatidylglycerol and sulfoquinovosyl diacylglycerol of higher plants in relation to chilling sensitivity. Plant Physiol 1986; 81, N 4:946–948.
[2] Murata N., Siegenthaler P. A. Lipids in photosynthesis: an overview Lipids in photosynthesis: structure, function and genetics. Eds P. A. Siegenthaler, N. Murata Dordrecht: Kluwer Acad. Publ., 1998:3–20.
[3] Benson A. A. A sulfolipid in plants Proc. Nat. Acad. Sci. USA. 1959; 45, N 11:1582–1587.
[4] Barber J., Gounaris K. What role does sulfolipid play within the thylakoid membrane? Photosynth. Res. 1986; 9, N 1–2:239–249.
[5] Benson A. A. The plant sulfolipid Advances in lipid research 1 New York: Acad. press, 1963:387–394.
[6] Harwood J. L. Sulfolipids The Biochemistry of plants. Eds P. K. Stumpf, E. E. Conn New York: Acad. press, 1980 P. 301–320.
[7] Wada H., Murata N. Membrane lipids in Cyanobacteria Lipids in photosynthesis: structure, function and genetics. Eds P. A. Siegenthaler, N. Murata Dordrecht: Kluwer Acad. Publ., 1998:83–101.
[8] Janero D. R., Barrnett R. Cellular and thylakoid-membrane glycolipids of Chlamydomonas reinhardtii 137+. J Lipid Res. 1981;22(7):1119-25.
[9] Harwood J. L. Membrane lipids in algae Lipids in photosynthesis: structure, function and genetics. Eds P. A. Siegenthaler, N. Murata Dordrecht: Kluwer Acad. Publ., 1998:53–64.
[10] Harwood J. L., Jones A. L. Lipid metabolism in algae Adv. Bot. Res 1989; 16:1–53.
[11] Rezanka T., Viden I., Go J. V., Dembitsky V. M. Polar lipids and fatty acids of three wild cyanobacterial strains of the genus Chroococcidiopsis Folia Microbiol 2003–48, N 6 P. 781–786.
[12] Benning C., Beatty J. T., Prince R. C., Somerville C. R. The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation Proc. Nat. Acad. Sci. USA 1993 90, N 4:1561–1565.
[13] Russell N. J., Harwood J. L. Changes in the acyl lipid composition of photosynthetic bacteria grown under photosynthetic and non-photosynthetic conditions Biochem. J 1979; 181, N 2:339–345.
[14] Bychek-Gushchina IA. Study of biochemical aspects of the lichen symbiosis. I. Lipids and fatty acids of cultured lichen symbionts. Biokhimia. 1997; 62(5):571–580.
[15] Guschina I. A., Harwood J. L. Lipid metabolism in the moss Rhytidiadelphus squarrosus (Hedw) Warnst. from lead-contaminated and non-contaminated populations J. Exp. Bot 2002; 53, N 368:455–463.
[16] Murata N., Hoshi H. Sulfoquinovosyl diacylglycerols in chilling sensitive and chilling resistant plants. Plant Cell Physiol. 1984. 25(7):1241–1245.
[17] Orr G., Raison J. Compositional and thermal properties of thylakoid polar lipids of Nerium oleander L. in relation to chilling sensitivity Plant Physiol 1987 84, N 1:88–92.
[18] Mock T., Kroon B. M. A. Photosynthetic energy conversion under extreme conditions – II: The significance of lipids under light limited growth in Antarctic sea ice diatoms Phytochemistry 2002 61, N 1:53–60.
[19] Sanina N. M., Goncharova S. N., Kostetsky E. Y. Fatty acid composition of individual polar lipid classes from marine macrophytes Phytochemistry 2004 65, N 6:721–730.
[20] Navari-Izzo F., Ricci F., Vazzana C., Quartacci M. F. Unusual composition of thylakoid membranes of the resurrection plant Boea hygroscopica: Changes in lipids upon dehydration and rehydration Physiol. Plant 1995 94, N 1 P. 135–142.
[21] Kylin A., Kuiper P. J. C., Hansson G. Lipids from sugar beet in relation to the preparation and properties of (sodium +potassium)-activated adenosine triphosphotases Physiol. Plant 1972 26, N 2:271–278.
[22] Lopez F., Lobasso S., Colella M., Agostiano A., Corcelli A. Light dependent and biochemical properties of two different bands of bacteriorhodopsin isolated on phenyl-sepharose CL-4B Photochem. and Photobiol 1999 69, N 5:599– 604.
[23] Corcelli A., Colella M., Mascolo G., Fanizzi F. P., Kates M. A novel glycolipid and phospholipid in the purple membrane Biochemistry 2000 39, N 12:3318–3326.
[24] Riekhof W. R., Ruckle M. E., Lydic T. A., Sears B. B., Benning C. The Sulfolipids 2'-O-acyl-sulfoquinovosyl diacylglycerol and sulfoquinovosyl diacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1 Plant Physiol 2003 133, N 2:864–874.
[25] Heinz E. Recent investigation on the biosynthesis of the plant sulfolipid Sulfur nutrition and assimilation in higher plants. Eds L. J. De Kok et al The Hague: SPB Acad. publ., 1993 P. 163–178.
[26] Sundby C., Larsson C. Transbilayer organization of the thylakoid galactolipids Biochim. Biophys. Acta 1985 813, N 1:61–67.
[27] Haines T. H. Anionic lipid headgroups as a protonconducting pathway along the surface of membranes: A hypothesis Proc. Nat. Acad. Sci. USA 1983 80, N 1 P. 160–164.
[28] Schwertner H. A., Biale J. B. Lipid composition of plant mitochondria and of chloroplasts. J Lipid Res. 1973;14(2):235-42.
[29] Kuiper P. J. C., Kahr M., Stuiver C. E. E., Kylin A. Lipid composition of whole roots and Ca2+, Mg2+-activated adenosine triphosphatases from wheat and oat as related to mineral nutrition Physiol. Plant 1974 32, N 1:33–36.
[30] Kuiper P. J. C. Temperature response of adenosine triphosphatase of bean roots as related to growth temperatures and to lipid requirement of the adenosine triphosphatase Physiol. Plant 1972 26, N 2:200–205.
[31] Sakai W. S., Yamamoto H. Y., Miyazaki T., Ross J. W. A model for chloroplast thylakoid membranes involving orderly arrangements of negatively charged lipidic particles containing sulfoquinovosyl diacylglycerol FEBS Lett 1983 158, N 2:203–207.
[32] Quinn P. J. The role of lipids in stability of plant membranes Advances in plant lipid research. Eds J. Sanches, E. Gerda-Olmedo, E. Martinez-Force Seville: Univ. press, 1998:361–366.
[33] Coves J., Joyard J., Douce R. Lipid requirement and kinetic studies of solubilized UDP-galactose:diacylglycerol galactosyltransferase activity from spinach chloroplast envelope membranes Proc. Nat. Acad. Sci. USA 1985 85, N 19:4966–4970.
[34] Li L., Karlsson O. P., Wieslander A. Activating amphiphiles cause a conformational changes of the 1,2-diacylglycerol transferase from Acholeplasma laidlavii membranes according to proteolitic digestion J. Biol. Chem 1997 272, N 47:29602–29606.
[35] Benson A. A. Plant membrane lipids Annu. Rev. Plant Physiol 1964 15, N 2:1–16.
[36] Anderson J. M. The molecular organization of chloroplast thylakoids Biochim. et Biophys. Acta. 1975 416, N 2 P. 191–235.
[37] Leech R. M., Rumsby M. G., Thomson W. W. Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves Plant Physiol 1973 52, N 3:240–245.
[38] Okanenko A. A., Taran N. YU. Action elevated temperatures and lack of moisture on the composition of the lipid complex chloroplasts of leaves of winter wheat environmental factors and organization of primary photosynthetic processes K.: Nauk. dumka, 1989 p 120–126.
[39] Latowski D., Kostecka A., Strzalka K. Effect of monogalactosyldiacylglycerol and other thylakoid lipids on violaxanthin de-epoxidation in liposomes Biochem. Soc. Trans 2000 28, N 6:810–812.
[40] Latowski D., Akerlund H.-E., Strziika K. Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity Biochemistry 2004 43, N 15:4417–20.
[41] Bush D. S. Calcium regulation in plant cells and its role in signaling Annu. Rev. Plant Physiol. Mol. Biol 1995 46 P. 95–122.
[42] Miller D. D., Callaham D. A., Gross D. J., Hepler P. K. Free Ca2+ gradient in growing pollen tubes of Lilium. J. Cell Sci. 1992; 101(1):7–12.
[43] Clark G. B., Roux S. J. Annexins of plant cells Plant Physiol 1995 109, N 4:1133–1139.
[44] Seigneurin-Berny D., Rolland N., Dorne A. J., Joyard J. Sulfolipid is a potential candidate for annexin binding to the outer surface of chloroplast Biochem. Biophys. Res. Communs 2000 272, N 2:519–524.
[45] De Vitry C., Ouyang Y., Finazzi G., Wollman F.-A., Kallas T. The chloroplast rieske iron-sulfur protein at the crossroad of electron transport and signal transduction J. Biol. Chem 2004 279, N 43:44621–44627.
[46] Choquet Y., Zito F., Wostrikoff K., Wollman F.-A. Cytochrome f translation in Chlamydomonas chloroplast is autoregulated by its carboxyl-terminal domain Plant Cell 2003 15, N 6:1443–1454.
[47] Kruk J., Jemioia-Rzeminska M., Strzaika K. Cytochrome c is reduced mainly by plastoquinol and not by superoxide in thylakoid membranes at low and medium light intensities: its specific interaction with thylakoid membrane lipids Biochem. J 2003 375, N 6:215–220.
[48] Gounaris K., Barber J. Isolation and characterization of a photosystem II reaction centre lipoprotein complex FEBS Lett 1985 188, N 1:68–72.
[49] Vijayan P., Routaboul J.-M., Browse J. A genetic approach to investigating membrane lipid structure and photosynthetic function Lipids in photosynthesis: structure, function and genetics. Eds P. A. Siegenthaler, N. Murata Dordrecht: Kluwer Acad. Publ., 1998:263–285.
[50] De Kruijff B., Pilon R., Hof R., van't, Demel R. Lipid-protein interactions in chloroplast protein import Lipids in photosynthesis: structure, function and genetics. Eds P. A. Siegenthaler, N. Murata Dordrecht: Kluwer Acad. Publ., 1998:191–208.
[51] Radunz A., Bader K., Schmid G. Influence of antisera to sulfoquinovosyl diglyceride and to -sitosterol on the photosynthetic electron transport in chloroplasts from higher plants Structure, function and metabolism of plant lipids. Eds P.-A. Sieghenthaler, W. Eichenberger Amsterdam: Elsevier Sci. Publ., 1984:479–484.
[52] Murata N., Higash S.-I., Fugimura Y. Glycerolipids in various preparation of photosystem II from spinach chloroplasts Biochim. et Biophys. Acta 1990 1019, N 3:261–268.
[53] Gasser A., Raddatz S., Radunz A., Schmid G. H. Comparative immunological and chemical analysis of lipids and carotenoids of the D1-Peptide and of the lightharvestingcomplex of photosystem II of Nicotiana tabacum. Z Naturforsch C. 1999;54(3-4):199-208.
[54] Krupa Z., Huner N. P. A., Williams J. P., Maissan E., James D. R. Development at cold-hardening temperatures Plant Physiol 1987 84, N 1:19–24.
[55] Sigrist M., Zwellenberg C., Giroud C. H., Eichenberger W., Boschetti A. Sulfolipid associated with light-harvesting complex associated with photosystem II apoproteins of Chlamydomonas reinhardii Plant Sci 1988 58, N 1 P. 15–23.
[56] Remy R., Tremolieres A., Duval J. C., Ambard-Bretteville F., Dubacq J. P. Study of the supramolecular organization of light-harvesting chlorophyll protein (LHCP) FEBS Lett 1982 137, N 2:271–275.
[57] Rawyler A., Siegenthaler P. A. Role of lipids in functions of photosynthetic membranes revealed by treatment with lipolytic acyl hydrolase Eur. J. Biochem 1980 110, N 1 P. 179–187.
[58] Larsson U. K., Andersson B. Different degrees of phosphorylation and lateral mobility of two polypeptides belonging to the light-harvesting complex of photosystem II Biochim. et Biophys. Acta 1985 809, N 3:396–402.
[59] Kruse O., Hankamer B., Konczak C., Gerle C., Morris E., Radunz A., Schmid G. H., Barber J. Phosphatidylglycerol is involved in the dimerization of photosystem II J. Biol. Chem 2000 275, N 9:6509–6514.
[60] Michel H., Hunt D. F., Shabanowitz J., Bennett J. Tandem mass spectrometry reveals that three photosystem II proteins of spinach chloroplasts contain N-acetyl-O-phosphothreonine at their NH2 termini. J Biol Chem. 1988;263(3):1123-30.
[61] Hagio M., Gombos Z., Varkonyi Z., Masamoto K., Sato N., Tsuzuki M., Wada H. Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis Plant Physiol 2000 124, N 2:795–804
[62] Sato N., Hagio M., Wada H., Tsuzuki M. Environmental effects on acidic lipids of thylakoid membranes Biochem. Soc. Trans 2000 28, N 6:912–914.
[63] Pick U., Gounaris K., Weiss M., Barber J. Tightly bound sulfolipids in chloroplast CF0-CF1 Biochim. et Biophys. Acta 1985 808, N 3:415–420.
[64] Livn A., Racker E. Partial resolution of the enzymes catalyzing photophosphorylation. V. Interaction of coupling factor I from chloroplasts with ribonucleic acid and lipids. J. Biol. Chem. 1969; 244(5):1332–1338.
[65] Balasubramanian R., Zorn H., Papenbrock J. Quantification and fatty acid profiles of sulfolipids in two halophytes and a glycophyte grown under different salt concentrations. Z Naturforsch C. 2004;59(11-12):835-42.
[66] Debez A., Saadaoui D., Balasubramanian R., Ouerghi Z., Koyro H.-W., Huchzermeyer B., Abdelly C. Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity Environ. Exp. Bot 2006 57, N 3 P. 285–295.
[67] Vishwanath B. S., Eichenberger W., Frey F. J., Frey B. M. Interaction of plant lipids with 14 kDa phospholipase A2 enzymes. Biochem J. 1996;320 ( Pt 1):93-9.
[68] Lambers J. W., Terpstra W. Inactivation of chlorophyllase by negatively charged plant membrane lipids Biochim. et Biophys. Acta 1985 831, N 2:225–235.
[69] Di Baccio D., Quartacci M. F., Dalla Vecctila F., La Rocca N., Rascto N., Navari-lzzo F. Bleaching herbicide effects on plastids of dark-grown plants: lipid composition of etioplasts in amitrole and norfIurazon-treated barley leaves J. Exp. Bot 2002 53, N 376:1857–1865.
[70] Kurihara H., Mitani T., Kawabata J., Hatano M. Inhibitory effect on the -glucosidase reaction by the aggregated state of sulfoquinovosyl-diacylglycerol Bios. Biotechnol. Biochem 1997 61, N 3:536–538.
[71] Kurihara H., Tada S., Takahashi K., Hatano M. Digalactosyldiacylglycerol suppression of inhibition by sulfoquinovosyl-diacylglycerol of -glucosidase Bios. Biotechnol. Biochem 1996 60, N 5:932–934.
[72] Gustafson K. R., Cardelina J. H., Fuller R. W., Weislow O. S., Kiser R. F., Snader K. M., Patterson G. M. L., Boyd M. R. AIDS-antiviral SL from cyanobacteria (blue-green algae) J. Nat. Cancer Inst 1989 81, N 16:1254–1258.
[73] Hanashima S., Mizushina Y., Yamazaki T., Ohta K., Takahashi S., Sakaguchi K., Sugawara F. Synthesis of sulfoquinovosyl acylglycerols, inhibitors of eukaryotic DNA polymerase and. Bioorg. and Med. Chem. 2001; 9(2)367–376.
[74] Ohta K., Mizushina Y., Hirata N., Takemura M., Sugawara F., Matsukage A., Yoshida S., Sakaguchi K. Sulfoquinovosyldiacylglycerol, KM043, a new potent inhibitor of eukaryotic DNA polymerases and HIV-reverse transcriptase type 1 from a marine red alga, Gigartina tenella Chem. and Pharm. Bull. (Tokyo) 1998 46, N 4:684–686.
[75] Loya S., Reshef V., Mizrachi E., Silberstein C., Rachamin Y., Carmeli S., Hizi A. The inhibition of the reverse transcriptase of HIV-1 by the natural sulfoglycolipids from cyanobacteria: contribution of different moieties to their high potency J. Nat. Prod 1998 61, N 7:891–895.
[76] Ogawa A., Murate T., Izuta S., Takemura M., Furuta K., Kobayashi J., Kamikawa T., Nimura Y., Yoshida S. Sulfated glycoglycerolipid from an archaebacterium inhibits eukaryotic DNA polymerase, and retroviral reverse transcriptase and affects methyl methanesulfonate cytotoxicity Int. J. Cancer 1998 76, N 4:512–518.
[77] Keegstra K., Cline K. Protein import and routing systems of chloroplasts The Plant Cell 1999 11, N 4:557–570.
[78] Van't Hof R., Demel R. A., Keegstra K., de Kruijff B. Lipid-peptide interactions between fragments of the transit peptide of ribulose-1,5-bisphosphate carboxylase/oxygenase and chloroplast membrane lipids FEBS Lett 1991 291, N 2:350–354.
[79] Van't Hof R., van Klompenburg W., Pilon M., Kozubek A., de Korte-Kool G., Demel R. A., Weisbeek P. J., de Kruijff B. The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids J. Biol. Chem 1993 268, N 6:4037–4042.
[80] Pilon M., Wienk H., Sips W., de Swaaf M., Talboom I., van't Hof R., de Korte-Kool G., Demel R., Weisbeek P., de Kruijff B. Functional domains of the ferredoxin transit sequence involved in chloroplast import J. Biol. Chem 1995 270, N 8:3882–3893.
[81] Horniak L., Pilon M., Van't Hof R., De Kruijff B. The secondary structure of the ferredoxin transit sequence is modulated by its interaction with negatively charged lipids FEBS Lett 1993 334, N 2:241–246.
[82] Lancelin J.-M., Bally I., Arland G. J., Blackedge M., Gans P., Stein M., Jacquot J.-P. NMR structure of ferredoxin chloroplastic transit peptide from Chlamydomonas reinhardtii promoted by trifluoroethanol in aqueous solution FEBS Lett 1994 343, N 3:261–266.
[83] Pain D., Blobel G. Protein import into chloroplasts requires a chloroplast ATPase Proc. Nat. Acad. Sci. USA 1987 84, N 10:3288–3292.