The plant sulfolipid sulfoquinovosyldiacylglycerol accounts for a large fraction of organic sulfur in the biosphere. Aside from sulfur amino acids, sulfolipid represents a considerable sink for sulfate in plants. Plant sulfolipid is found in the photosynthetic membranes of plastids and provides negative charge in the thylakoid membrane where it is thought to stabilize photosynthetic complexes. As the plant sulfolipid is a non-phosphorous glycolipid, its synthesis does not impinge on the supply of phosphate, which is a macronutrient limiting plant growth in many natural environments. Indeed, plants evolved homeostatic mechanisms to balance the amount of sulfolipid with anionic phospholipids maintaining a proper level of anionic charge in the photosynthetic membrane. The strong anionic nature of the sugar sulfonate head group of sulfolipid also makes this lipid an interesting compound for biotechnological applications. As bacterial and plant genes encoding sulfolipid enzymes are now available, biotechnological approaches can be developed to produce the plant sulfolipid in sufficient amounts to pursue the development of practical applications.
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References
Abraham WR, Meyer H, Lindholst S, Vancanneyt M, Smit J (1997) Phospho- and sulfolipids as biomarkers of Caulobacter sensu lato, Brvundimaonas and Hyphomonas. System Appl Microbiol 20: 522–539
Anderson R, Livermore BP, Kates M, Volcani BE (1978) The lipid composition of the non-photosynthetic diatom Nitzschia alba. Biochim Biophys Acta 528: 77–88
Aoki M, Sato N, Meguro A, Tsuzuki M (2004) Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacteria. Eur J Biochem 271: 685–693
Archer SD, McDonald KA, Jackman AP (1997) Effect of light irradiance on the production of sulfolipids from Anabaena 7120 in a fed-batch photobioreactor. Appl Biochem Biotechnol 67: 139–152
Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33: 899–909
Barber GA (1963) The formation of uridine diphosphate L-Rhamnose by enzymes of the tobacco leaf. Arch Biochem Biophys 103: 276–282
Barber J, Gounaris K (1986) What role does sulfolipid play within the thylakoid membrane? Photosynthes Res 9: 239–249
Benning C (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49: 53–75
Benning C, Beatty JT, Prince RC, Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci U S A 90: 1561–1565
Benning C, Somerville CR (1992a) Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J Bacteriol 174: 6479–6487
Benning C, Somerville CR (1992b) Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J Bacteriol 174: 2352–2360
Benson AA (1963) The plant sulfolipid. Adv Lipid Res 1: 387–94
Benson AA (2002) Paving the path. Annu Rev Plant Biol 53: 1–25
Benson AA, Daniel H, Wiser R (1959) A sulfolipid in plants. Proc Natl Acad Sci U S A 45: 1582–1587
Berg S, Edman M, Li L, Wikstrom M, Wieslander A (2001) Sequence properties of the 1, 2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii membranes. Recognition of a large group of lipid glycosyltransferases in eubacteria and archaea. J Biol Chem 276: 22056–22063
Budzikiewicz H, Rullkötter J, Heinz E (1973) Massenspetroskopische Untersuchungen an Glycosylglyceriden. Z Naturforsch [C] 28: 499–504
Cedergren RA, Hollingsworth RI (1994) Occurrence of sulfoquinovosyl diacylglycerol in some members of the family Rhizobiaceae. J Lipid Res 35: 1452–1461
Dembitsky VM, Pechenkina-Shubina EE, Rozentsvet OA (1991) Glycolipids and fatty acids of some seaweeds and marine grasses from the Black Sea. Phytochemistry 30: 2279–2283
Dembitsky VM, Rozentsvet OA, Pechenkina EE (1990) Glycolipids, phospholipids and fatty acids of brown algae species. Phytochemistry 29: 3417–3421
Eitsuka T, Nakagawa K, Igarashi M, Miyazawa T (2004) Telomerase inhibition by sulfoquinovosyldiacylglycerol from edible purple laver (Porphyra yezoensis). Cancer Lett 212: 15–20
Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 95: 1950–1955
Essigmann B, Hespenheide BM, Kuhn LA, Benning C (1999) Prediction of the active-site structure and NAD(+) binding in SQD1, a protein essential for sulfolipid biosynthesis in Arabidopsis. Arch Biochem Biophys 369: 30–41
Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270–276
Gage DA, Huang ZH, Benning C (1992) Comparison of sulfoquinovosyl diacylglycerol from spinach and the purple bacterium Rhodobacter spaeroides by fast atom bombardment tandem mass spectrometry. Lipids 27: 632–636
Golik J, Dickey JK, Todderud G, Lee D, Alford J, Huang S, Klohr S, Eustice D, Aruffo A, Agler ML (1997) Isolation and structure determination of sulfonoquinovosyl dipalmitoyl glyceride, a P-selectin receptor inhibitor from the alga Dictyochloris fragrans. J Nat Prod 60: 387–389
Gordon DM, Danishefsky SJ (1992) Synthesis of a cyanobacterial sulfolipid: confirmation of its structure, stereochemistry and anti-HIV-1 activity. J Am Chem Soc 114: 659–663
Gounaris K, Barber J (1985) Isolation and characterisation of a photosystem II reaction center lipoprotein complex. FEBS Lett 188: 68–72
Güler S, Essigmann B, Benning C (2000) A cyanobacterial gene, sqdX, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglycerol. J Bacteriol 182: 543–545
Güler S, Seeliger A, Härtel H, Renger G, Benning C (1996) A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271: 7501–7507
Gustafson KR, Cardellina JH, Fuller RW, Weislow OS, Kiser RF, Snader KM, Patterson GM, Boyd MR (1989) AIDS-antiviral sulfolipids from cyanobacteria (blue-green algae). J Natl Cancer Inst 81: 1254–1258
Haas R, Siebertz HP, Wrage K, Heinz E (1980) Localization of sulfolipid labeling within cells and chloroplasts. Planta 148: 238–244
Hagio M, Sakurai I, Sato S, Kato T, Tabata S, Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43: 1456–1464
Haines TH (1973) Sulfolipids and halosulfolipids. In JA Erwin, ed, Lipids and Biomembranes of Eucryotic Organisms. Academic, New York, pp 197–232
Haines TH (1983) Anionic lipid headgroups as a proton-conducting pathway along the surface of membranes: a hypothesis. Proc Natl Acad Sci U S A 80: 160–164
Hamed LB, Youssef NB, Ranieri A, Zarrouk M, Abdelly C (2005) Changes in content and fatty acid profiles of total lipids and sulfolipids in the halophyte Crithmum maritimum under salt stress. J Plant Physiol 162: 599–602
Hanashima S, Mizushina Y, Ohta K, Yamazaki T, Sugawara F, Sakaguchi K (2000a) Structure–activity relationship of a novel group of mammalian DNA polymerase inhibitors, synthetic sulfoquinovosylacylglycerols. Jpn J Cancer Res 91: 1073–1083
Hanashima S, Mizushina Y, Yamazaki T, Ohta K, Takahashi H, Koshino H, Sahara H, Sakaguchi K, Sugawara F (2000b) Structural determination of sulfoquinovosyldiacylglycerol by chiral syntheses. Tetrahedron Lett 41: 4403–4407
Hanashima S, Mizushina Y, Yamazaki T, Ohta K, Takahashi S, Sahara H, Sakaguchi K, Sugawar F (2001) Synthesis of sulfoquinovosylacylglycerols, inhibitors of eukaryotic DNA polymerase alpha and beta. Bioorg Med Chem 9: 367–376
Härtel H, Essigmann B, Lokstein H, Hoffmann-Benning S, Peters-Kottig M, Benning C (1998) The phospholipid-deficient pho1 mutant of Arabidopsis thaliana is affected in the organization, but not in the light acclimation, of the thylakoid membrane. Biochim Biophys Acta 1415: 205–218
Harwood JL (1980) Sulfolipids. In PK Stumpf, ed, The Biosynthesis of Plants, Vol. 4. Academic, New York, pp 301–320
Harwood JL, Nicholls RG (1979) The plant sulpholipid—a major component of the sulphur cycle. Biochem Soc Trans 7: 440–447
Heinz E (1993) Recent investigations on the biosynthesis of the plant sulfolipid. In LJ De Kok, ed, Sulfur Nutrition and Assimilation in Higher Plants. SPB Academic, The Hague, The Netherlands, pp 163–178
Heinz E, Schmidt H, Hoch M, Jung KH, Binder H, Schmidt RR (1989) Synthesis of different nucleoside 5′-diphospho-sulfoquinovoses and their use for studies on sulfolipid biosynthesis in chloroplasts. Eur J Biochem 184: 445–453
Hossain Z, Kurihara H, Hosokawa M, Takahashi K (2005) Growth inhibition and induction of differentiation and apoptosis mediated by sodium butyrate in Caco-2 cells with algal glycolipids. In Vitro Cell Dev Biol Anim 41: 154–159
Howard KP, Prestegard JH (1996) Conformation of sulfoquinovosyldiacylglycerol bound to a magnetically oriented membrane system. Biophys J 71: 2573–2582
Inoue K, Demel R, de Kruijff B, Keegstra K (2001) The N-terminal portion of the preToc75 transit peptide interacts with membrane lipids and inhibits binding and import of precursor proteins into isolated chloroplasts. Eur J Biochem 268: 4036–4043
Jordan P, Fromme P, Witt H, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411: 909–917
Joyard J, Blee E, Douce R (1986) Sulfolipid synthesis from 35SO4 and [1–14C]acetate in isolated intact spinach chloroplasts. Bichim Biophys Acta 879: 78–87
Kim YH, Yoo JS, Kim MS (1997) Structural characterization of sulfoquinvosyl, monogalactosyl and digalactosyl diacylglcyerols by FAB-CID-MS/MS. J Mass Spec 32: 968–977
Kleppinger-Sparace KF, Mudd JB (1987) Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants: the incorporation of 35SO4 by intact chloroplasts in darkness. Plant Physiol 84: 682–687
Kleppinger-Sparace KF, Mudd JB (1990) Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants: use of adenosine-5′-phosphosulfate and adenosine-3′-phosphate 5′-phosphosulfate as precursors. Plant Physiol 93: 256–263
Kleppinger-Sparace KF, Mudd JB, Bishop DG (1985) Biosynthesis of sulfoquinovosyldiacylglycerol in higher plants: the incorporation of 35SO4 by intact chloroplasts. Arch Biochem Biophys 240: 859–865
Kleppinger-Sparace KF, Sparace SA, Mudd JB (1990) Plant Sulfolipids. In H Rennenberg, C Brunold, LJ De Kok, I Stulen, eds, Sulfur Nutrition and Sulfur Assimilation in Higher Plants. SPB Academic, The Hague, pp 77–88
Kuiper PJC (1970) Lipids in alfalfa leaves in relation to cold hardiness. Plant Physiol 45: 684–686
Kuiper PJC, Kähr M, Stuiver CEE, Kylin A (1974) Lipid composition of whole roots and of Ca2+ and Mg2+-activated adenosine triphosphatases from wheat and oat as related to mineral nutrition. Physiol Plant 32: 33–36
Kuriyama I, Musumi K, Yonezawa Y, Takemura M, Maeda N, Iijima H, Hada T, Yoshida H, Mizushina Y (2005) Inhibitory effects of glycolipids fraction from spinach on mammalian DNA polymerase activity and human cancer cell proliferation. J Nutr Biochem 16: 594–601
Langworthy TA, Mayberry WR, Smith PF (1976) A sulfonolipid and novel glucosamidyl glycolipids from the extreme thermoacidophile Bacillus acidocaldarius. Biochim Biophys Acta 431: 550–569
Leech RM, Rumsby MG, Thomson WW (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiol 52: 240–245
Lehmann J, Benson AA (1964) The plant sulfolipid. IX. Sulfosugar syntheses from methyl hexoseenides. J Am Chem Soc 86: 4469–4472
Loya S, Reshef V, Mizrachi E, Silberstein C, Rachamim Y, Carmeli S, Hizi A (1998) 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 61: 891–895
Maeda N, Hada T, Murakami-Nakai C, Kuriyama I, Ichikawa H, Fukumori Y, Hiratsuka J, Yoshida H, Sakaguchi K, Mizushina Y (2005) Effects of DNA polymerase inhibitory and antitumor activities of lipase-hydrolyzed glycolipid fractions from spinach. J Nutr Biochem 16: 121–128
Marechal E, Block MA, Dorne A-J, Joyard J (1997) Lipid synthesis and metabolism in the plastid envelope. Physiol Plant 100: 65–77
Matsubara K, Matsumoto H, Mizushina Y, Mori M, Nakajima N, Fuchigami M, Yoshida H, Hada T (2005) Inhibitory effect of glycolipids from spinach on in vitro and ex vivo angiogenesis. Oncol Rep 14: 157–160
Matsumoto K, Sakai H, Ohta K, Kameda H, Sugawara F, Abe M, Sakaguchi K (2005a) Monolayer membranes and bilayer vesicles characterized by alpha- and beta-anomer of sulfoquinovosyldiacylglycerol (SQDG). Chem Phys Lipids 133: 203–214
Matsumoto K, Sakai H, Takeuchi R, Tsuchiya K, Ohta K, Sugawara F, Abe M, Sakaguchi K (2005b) Effective form of sulfoquinovosyldiacylglycerol (SQDG) vesicles for DNA polymerase inhibition. Colloids Surf B Biointerfaces 46: 175–181
Matsumoto K, Takenouchi M, Ohta K, Ohta Y, Imura T, Oshige M, Yamamoto Y, Sahara H, Sakai H, Abe M, Sugawara F, Sato N, Sakaguchi K (2004) Design of vesicles of 1, 2-di-O-acyl-3-O-(beta-D-sulfoquinovosyl)-glyceride bearing two stearic acids (beta-SQDG-C18), a novel immunosuppressive drug. Biochem Pharmacol 68: 2379–2386
Matsumoto Y, Sahara H, Fujita T, Hanashima S, Yamazaki T, Takahashi S, Sugawara F, Mizushina Y, Ohta K, Takahashi N, Jimbow K, Sakaguchi K, Sato N (2000) A novel immunosuppressive agent, SQDG, derived from sea urchin. Transplant Proc 32: 2051–2053
Menke W, Radunz A, Schmid GH, Koenig F, Hirtz RD (1976) Intermolecular interactions of polypeptides and lipids in the thylakoid membrane. Z Naturforsch [C] 31: 436–444
Minoda A, Sato N, Nozaki H, Okada K, Takahashi H, Sonoike K, Tsuzuki M (2002) Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269: 2353–2358
Minoda A, Sonoike K, Okada K, Sato N, Tsuzuki M (2003) Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. FEBS Lett 553: 109–112
Mizushina Y, Maeda N, Kawasaki M, Ichikawa H, Murakami C, Takemura M, Xu X, Sugawara F, Fukumori Y, Yoshida H, Sakaguchi K (2003a) Inhibitory action of emulsified sulfoquinovosyl acylglycerol on mammalian DNA polymerases. Lipids 38: 1065–1074
Mizushina Y, Watanabe I, Ohta K, Takemura M, Sahara H, Takahashi N, Gasa S, Sugawara F, Matsukage A, Yoshida S, Sakaguchi K (1998) Studies on inhibitors of mammalian DNA polymerase alpha and beta: sulfolipids from a pteridophyte, Athyrium niponicum. Biochem Pharmacol 55: 537–541
Mizushina Y, Xu X, Asahara H, Takeuchi R, Oshige M, Shimazaki N, Takemura M, Yamaguchi T, Kuroda K, Linn S, Yoshida H, Koiwai O, Saneyoshi M, Sugawara F, Sakaguchi K (2003b) A sulphoquinovosyl diacylglycerol is a DNA polymerase epsilon inhibitor. Biochem J 370: 299–305
Mudd JB, Kleppinger-Sparace KF (1987) Sulfolipids. In PK Stumpf, ed, The Biochemistry of Plants, Vol. 9. Lipids: Structure and Function. Academic, New York, pp 275–288
Mulichak AM, Theisen MJ, Essigmann B, Benning C, Garavito RM (1999) Crystal structure of SQD1, an enzyme involved in the biosynthesis of the plant sulfolipid headgroup donor UDP-sulfoquinovose. Proc Natl Acad Sci U S A 96: 13097–13102
Müller M, Santarius KA (1978) Changes in chloroplast membrane lipids during adaptation of barely to extreme salinity. Plant Physiol 62: 326–329
Murakami C, Miuzno T, Hanaoka F, Yoshida H, Sakaguchi K, Mizushina Y (2004) Mechanism of cell cycle arrest by sulfoquinovosyl monoacylglycerol with a C18-saturated fatty acid (C18-SQMG). Biochem Pharmacol 67: 1373–1380
Murakami C, Takemura M, Yoshida H, Sugawara F, Sakaguchi K, Mizushina Y (2003a) Analysis of cell cycle regulation by 1-mono-O-acyl-3-O-(alpha-D-sulfoquinovosyl)-glyceride (SQMG), an inhibitor of eukaryotic DNA polymerases. Biochem Pharmacol 66: 541–550
Murakami C, Yamazaki T, Hanashima S, Takahashi S, Ohta K, Yoshida H, Sugawara F, Sakaguchi K, Mizushina Y (2002) Structure-function relationship of synthetic sulfoquinovosyl-acylglycerols as mammalian DNA polymerase inhibitors. Arch Biochem Biophys 403: 229–236
Murakami C, Yamazaki T, Hanashima S, Takahashi S, Takemura M, Yoshida S, Ohta K, Yoshida H, Sugawara F, Sakaguchi K, Mizushina Y (2003b) A novel DNA polymerase inhibitor and a potent apoptosis inducer: 2-mono-O-acyl-3-O-(alpha-D-sulfoquinovosyl)-glyceride with stearic acid. Biochim Biophys Acta 1645: 72–80
Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M, Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 137–145
Norman HA, Mischke CF, Allen B, Vincent JS (1996) Semi-preparative isolation of plant sulfoquinovosyldiacylglycerols by solid phase extraction and HPLC procedures. J Lipid Res 37: 1372–1376
O’Brien JS, Benson AA (1964) Isolation and fatty acid composition of the plant sulfolipid and galactolipids. J Lipid Res 5: 432–434
Ohta K, Hanashima S, Mizushina Y, Yamazaki T, Saneyoshi M, Sugawara F, Sakaguchi K (2000) Studies on a novel DNA polymerase inhibitor group, synthetic sulfoquinovosylacylglycerols: inhibitory action on cell proliferation. Mutat Res 467: 139–152
Ohta K, Mizushina Y, Hirata N, Takemura M, Sugawara F, Matsukage A, Yoshida S, Sakaguchi K (1998) Sulfoquinovosyldiacylglycerol, KM043, a new potent inhibitor of eukaryotic DNA polymerases and HIV-reverse transcriptase type 1 from a marine red alga, Gigartina tenella. Chem Pharm Bull (Tokyo) 46: 684–686
Ohta K, Mizushina Y, Hirata N, Takemura M, Sugawara F, Matsukage A, Yoshida S, Sakaguchi K (1999) Action of a new mammalian DNA polymerase inhibitor, sulfoquinovosyldiacylglycerol. Biol Pharm Bull 22: 111–116
Ohta K, Mizushina Y, Yamazaki T, Hanashima S, Sugawara F, Sakaguchi K (2001) Specific interaction between an oligosaccharide on the tumor cell surface and the novel antitumor agents, sulfoquinovosylacylglycerols. Biochem Biophys Res Commun 288: 893–900
Okanenko A (2000) Sulfoquinovosyldiacylglycerol in higher plants: Biosynthesis and physiological function. In C Brunold, ed, Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Paul Haupt, Bern, CH, pp 203–216
Oquist G (1982) Seasonally induced changes in acyl lipids and fatty acids of chloroplast thylakoids of Pinus silvestris. Plant Physiol 69: 869–875
Pick U, Gounaris K, Weiss M, Barber J (1985) Tightly bound sulfolipids in chloroplast CF0-CF1. Biochim Biophys Acta 808: 415–420
Pick U, Weiss M, Gounaris K, Barber J (1987) The role of different thylakoid glycolipids in the function of reconstituted chloroplast ATP synthase. Biochim Biophys Acta 891: 28–39
Pugh CE, Hawkes T, Harwood JL (1995a) Biosynthesis of sulphoquinovosyldiacylglycerol by chloroplast fractions from pea and lettuce. Phytochemistry 39: 1071–1075
Pugh CE, Roy AB, Hawkes T, Harwood JL (1995b) A new pathway for the synthesis of the plant sulpholipid, sulphoquinovosyldiacylglycerol. Biochem J 309 (Pt 2): 513–519
Quartacci MF, Pinzino C, Sgherri C, Navari-Izzo F (1995) Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought. Plant Physiol 108: 191–197
Quasney ME, Carter LC, Oxford C, Watkins SM, Gershwin ME, German JB (2001) Inhibition of proliferation and induction of apoptosis in SNU-1 human gastric cancer cells by the plant sulfolipid, sulfoquinovosyldiacylglycerol. J Nutr Biochem 12: 310–315
Radunz A, Schmid GH (1992) Binding of lipids onto polypeptides of the thylakoid membrane I. Galactolipids and sulpholipid as prosthetic groups of core peptides of the photosystem II complex. Z Naturforsch [C] 47: 406–415
Ramani B, Zorn H, Papenbrock J (2004) Quantification and fatty acid profiles of sulfolipids in two halophytes and a glycophyte grown under different salt concentrations. Z Naturforsch [C] 59: 835–842
Reshef V, Mizrachi E, Maretzki T, Silberstein C, Loya S, Hizi A, Carmeli S (1997) New acylated sulfoglycolipids and digalactolipids and related known glycolipids from cyanobacteria with a potential to inhibit the reverse transcriptase of HIV-1. J Nat Prod 60: 1251–1260
Riekhof WR, Ruckle ME, Lydic TA, Sears BB, Benning C (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldiacylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133: 864–874
Rossak M, Schäfer A, Xu N, Gage DA, Benning C (1997) Accumulation of sulfoquinovosyl-1-O-dihydroxyacetone in a sulfolipid-deficient mutant of Rhodobacter sphaeroides inactivated in sqdC. Arch Biochem Biophys 340: 219–230
Rossak M, Tietje C, Heinz E, Benning C (1995) Accumulation of UDP-sulfoquinovose in a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J Biol Chem 270: 25792–25797
Roy AB, Harwood JL (1999) Re-evaluation of plant sulpholipid labelling from UDP-[14C]glucose in pea chloroplasts. Biochem J 344 Pt 1: 185–187
Roy AB, Hewlins MJ, Ellis AJ, Harwood JL, White GF (2003) Glycolytic breakdown of sulfoquinovose in bacteria: a missing link in the sulfur cycle. Appl Environ Microbiol 69: 6434–6441
Sahara H, Hanashima S, Yamazaki T, Takahashi S, Sugawara F, Ohtani S, Ishikawa M, Mizushina Y, Ohta K, Shimozawa K, Gasa S, Jimbow K, Sakaguchi K, Sato N, Takahashi N (2002) Anti-tumor effect of chemically synthesized sulfolipids based on sea urchin’s natural sulfonoquinovosylmonoacylglycerols. Jpn J Cancer Res 93: 85–92
Sahara H, Ishikawa M, Takahashi N, Ohtani S, Sato N, Gasa S, Akino T, Kikuchi K (1997) In vivo anti-tumour effect of 3′-sulphonoquinovosyl 1′-monoacylglyceride isolated from sea urchin (Strongylocentrotus intermedius) intestine. Br J Cancer 75: 324–332
Sanda S, Leustek T, Theisen MJ, Garavito RM, Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276: 3941–3946
Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117: 495–505
Sato N, Aoki M, Maru Y, Sonoike K, Minoda A, Tsuzuki M (2003a) Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 217: 245–251
Sato N, Hagio M, Wada H, Tsuzuki M (2000) Environmental effects on acidic lipids of thylakoid membranes. Biochem Soc Trans 28: 912–914
Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1995) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234: 16–23
Sato N, Sugimoto K, Meguro A, Tsuzuki M (2003b) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phylogeny. DNA Res 10: 229–237
Seifert U, Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose:diacylglycerol sulfoquinovosyltransferase from chloroplast envelopes. Bot Acta 105: 197–205
Seigneurin-Berny D, Rolland N, Dorne AJ, Joyard J (2000) Sulfolipid is a potential candidate for annexin binding to the outer surface of chloroplast. Biochem Biophys Res Commun 272: 519–524
Selstam E, Campbell D (1996) Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus sp. PCC7421, which lacks sulfoquinovosyl diacylglycerol. Arch Microbiol 166: 132–135
Shibuya I, Hase E (1965) Degradation and formation of sulfolipid occurring concurrently with de- and re-generation of chloroplasts in the cells of Chlorella protothecoides. Plant Cell Phyisol 6: 267–283
Shibuya I, Yagi T, Benson AA (1963) Sulfonic acids in algae. Microalgae and Photosynthetic bacteria, Jpn. Soc. Plant Physiol., Tokyo University Press, Tokyo, pp 627–636
Shima H, Tsuruma T, Sahara H, Takenouchi M, Takahashi N, Iwayama Y, Yagihashi A, Watanabe N, Sato N, Hirata K (2005) Treatment with beta-SQAG9 prevents rat hepatic ischemia-reperfusion injury. Transplant Proc 37: 417–421
Shimojima M, Benning C (2003) Native uridine 5′-diphosphate-sulfoquinovose synthase, SQD1, from spinach purifies as a 250-kDa complex. Arch Biochem Biophys 413: 123–130
Shimojima M, Hoffmann-Benning S, Garavito RM, Benning C (2005) Ferredoxin-dependent glutamate synthase moonlights in plant sulfolipid biosynthesis by forming a complex with SQD1. Arch Biochem Biophys 436: 206–214
Shipley GG, Green JP, Nichols BW (1973) The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim Biophys Acta 311: 531–544
Shirahashi H, Murakami N, Watanabe M, Nagatsu A, Sakakibara J, Tokuda H, Nishino H, Iwashima A (1993) Isolation and identification of anti-tumor-promoting principles from the fresh-water cyanobacterium Phormidium tenue. Chem Pharm Bull (Tokyo) 41: 1664–1666
Sigrist M, Zwillenberg C, Giroud CH, Eichenberger W, Boschetti A (1988) Sulfolipid associated with the light harvesting complex associated with photosystem II apoproteins of Chlamydomonas reinhardtii. Plant Sci 58: 15–23
Sprott GD, Bakouche L, Rajagopal K (2006) Identification of sulfoquinovosyl diacylglycerol as a major polar lipid in Marinococcus halophilus and Salinicoccus hispanicus and substitution with phosphatidylglycerol. Can J Microbiol 52: 209–219
Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6) f complex. Nature 426: 413–418
Taran N, Okanenko A, Musienko N (2000) Sulpholipid reflects plant resistance to stress-factor action. Biochem Soc Trans 28: 922–924
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680
Tietje C, Heinz E (1998) Uridine-diphospho-sulfoquinovose:diacylglycerol sulfoquinovosyltransferase activity is concentrated in the inner membrane of chloroplast envelopes. Planta 206: 72–78
van’t Hof R, van Klompenburg W, Pilon M, Kozubek A, Korte-Kool G, Demel RA, Weisbeek PJ, de Kruijff B (1993) The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids. J Biol Chem 268: 4037–4042
Vasange M, Rolfsen W, Bohlin L (1997) A sulphonoglycolipid from the fern Polypodium decumanum and its effect on the platelet activating-factor receptor in human neutrophils. J Pharm Pharmacol 49: 562–566
Vishwanath BS, Eichenberger W, Frey FJ, Frey BM (1996) Interaction of plant lipids with 14 kDa phospholipase A2 enzymes. Biochem J 320 (Pt 1): 93–99
Webb MS, Green BR (1991) Biochemical and biophysical properties of thyalkoid acyl lipids. Bichim Biophys Acta 1060: 133–158
Weissenmayer B, Geiger O, Benning C (2000) Disruption of a gene essential for sulfoquinovosyldiacylglycerol biosynthesis in Sinorhizobium meliloti has no detectable effect on root nodule symbiosis. Mol Plant Microbe Interact 13: 666–672
Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002) The pgp1 locus of Arabidopsis encodes a phosphatidylglycerol synthase with impaired activity. Plant Physiol 129: 594–604
Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36: 762–770
Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci U S A 99: 5732–5737
Zähringer U, Moll H, Hettmann T, Knirel YA, Schäfer G (2000) Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius has a unique Asn-linked highly branched hexasaccharide chain containing 6-sulfoquinovose. Eur J Biochem 267: 4144–4149
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Benning, C., Garavito, R.M., Shimojima, M. (2008). Sulfolipid Biosynthesis and Function in Plants. In: Hell, R., Dahl, C., Knaff, D., Leustek, T. (eds) Sulfur Metabolism in Phototrophic Organisms. Advances in Photosynthesis and Respiration, vol 27. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6863-8_10
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