Skip to main content

Sulfolipid Biosynthesis and Function in Plants

  • Chapter
Sulfur Metabolism in Phototrophic Organisms

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 27))

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Barber GA (1963) The formation of uridine diphosphate L-Rhamnose by enzymes of the tobacco leaf. Arch Biochem Biophys 103: 276–282

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Gounaris K (1986) What role does sulfolipid play within the thylakoid membrane? Photosynthes Res 9: 239–249

    Article  CAS  Google Scholar 

  • Benning C (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49: 53–75

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Benning C, Somerville CR (1992a) Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J Bacteriol 174: 6479–6487

    PubMed  CAS  Google Scholar 

  • Benning C, Somerville CR (1992b) Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J Bacteriol 174: 2352–2360

    PubMed  CAS  Google Scholar 

  • Benson AA (1963) The plant sulfolipid. Adv Lipid Res 1: 387–94

    PubMed  CAS  Google Scholar 

  • Benson AA (2002) Paving the path. Annu Rev Plant Biol 53: 1–25

    Article  PubMed  CAS  Google Scholar 

  • Benson AA, Daniel H, Wiser R (1959) A sulfolipid in plants. Proc Natl Acad Sci U S A 45: 1582–1587

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Budzikiewicz H, Rullkötter J, Heinz E (1973) Massenspetroskopische Untersuchungen an Glycosylglyceriden. Z Naturforsch [C] 28: 499–504

    CAS  Google Scholar 

  • Cedergren RA, Hollingsworth RI (1994) Occurrence of sulfoquinovosyl diacylglycerol in some members of the family Rhizobiaceae. J Lipid Res 35: 1452–1461

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dembitsky VM, Rozentsvet OA, Pechenkina EE (1990) Glycolipids, phospholipids and fatty acids of brown algae species. Phytochemistry 29: 3417–3421

    Article  CAS  Google Scholar 

  • Eitsuka T, Nakagawa K, Igarashi M, Miyazawa T (2004) Telomerase inhibition by sulfoquinovosyldiacylglycerol from edible purple laver (Porphyra yezoensis). Cancer Lett 212: 15–20

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270–276

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gounaris K, Barber J (1985) Isolation and characterisation of a photosystem II reaction center lipoprotein complex. FEBS Lett 188: 68–72

    Article  CAS  Google Scholar 

  • Güler S, Essigmann B, Benning C (2000) A cyanobacterial gene, sqdX, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglycerol. J Bacteriol 182: 543–545

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Haas R, Siebertz HP, Wrage K, Heinz E (1980) Localization of sulfolipid labeling within cells and chloroplasts. Planta 148: 238–244

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Haines TH (1973) Sulfolipids and halosulfolipids. In JA Erwin, ed, Lipids and Biomembranes of Eucryotic Organisms. Academic, New York, pp 197–232

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Harwood JL (1980) Sulfolipids. In PK Stumpf, ed, The Biosynthesis of Plants, Vol. 4. Academic, New York, pp 301–320

    Google Scholar 

  • Harwood JL, Nicholls RG (1979) The plant sulpholipid—a major component of the sulphur cycle. Biochem Soc Trans 7: 440–447

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Howard KP, Prestegard JH (1996) Conformation of sulfoquinovosyldiacylglycerol bound to a magnetically oriented membrane system. Biophys J 71: 2573–2582

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kuiper PJC (1970) Lipids in alfalfa leaves in relation to cold hardiness. Plant Physiol 45: 684–686

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lehmann J, Benson AA (1964) The plant sulfolipid. IX. Sulfosugar syntheses from methyl hexoseenides. J Am Chem Soc 86: 4469–4472

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marechal E, Block MA, Dorne A-J, Joyard J (1997) Lipid synthesis and metabolism in the plastid envelope. Physiol Plant 100: 65–77

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Santarius KA (1978) Changes in chloroplast membrane lipids during adaptation of barely to extreme salinity. Plant Physiol 62: 326–329

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • O’Brien JS, Benson AA (1964) Isolation and fatty acid composition of the plant sulfolipid and galactolipids. J Lipid Res 5: 432–434

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Oquist G (1982) Seasonally induced changes in acyl lipids and fatty acids of chloroplast thylakoids of Pinus silvestris. Plant Physiol 69: 869–875

    Article  PubMed  CAS  Google Scholar 

  • Pick U, Gounaris K, Weiss M, Barber J (1985) Tightly bound sulfolipids in chloroplast CF0-CF1. Biochim Biophys Acta 808: 415–420

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pugh CE, Hawkes T, Harwood JL (1995a) Biosynthesis of sulphoquinovosyldiacylglycerol by chloroplast fractions from pea and lettuce. Phytochemistry 39: 1071–1075

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sato N (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117: 495–505

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Sato N, Hagio M, Wada H, Tsuzuki M (2000) Environmental effects on acidic lipids of thylakoid membranes. Biochem Soc Trans 28: 912–914

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Seifert U, Heinz E (1992) Enzymatic characteristics of UDP-sulfoquinovose:diacylglycerol sulfoquinovosyltransferase from chloroplast envelopes. Bot Acta 105: 197–205

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shipley GG, Green JP, Nichols BW (1973) The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim Biophys Acta 311: 531–544

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6) f complex. Nature 426: 413–418

    Article  PubMed  CAS  Google Scholar 

  • Taran N, Okanenko A, Musienko N (2000) Sulpholipid reflects plant resistance to stress-factor action. Biochem Soc Trans 28: 922–924

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tietje C, Heinz E (1998) Uridine-diphospho-sulfoquinovose:diacylglycerol sulfoquinovosyltransferase activity is concentrated in the inner membrane of chloroplast envelopes. Planta 206: 72–78

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Webb MS, Green BR (1991) Biochemical and biophysical properties of thyalkoid acyl lipids. Bichim Biophys Acta 1060: 133–158

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36: 762–770

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science + Business Media B.V

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics