Skip to main content
SpringerLink
Log in

Questions remaining in sulfolipid biosynthesis: a historical perspective

  • Original Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The plant sulfolipid sulfoquinovosyldiacylglycerol was discovered by A.A. Benson in the late 1950s. The increasing availability of radioisotope-containing biological substrates such as 35S-sulfate provided the means to discover novel biological compounds and to sketch out their biosynthetic pathways. During this time the structure of sulfolipid with its 6-deoxy-6-sulfo-α-d-glucose (sulfoquinovose) headgroup was determined. Immediately, the origin of this unusual biological sulfonic acid mystified the scientific community and several proposals for its biosynthesis were developed and tested. Strong supportive evidence for the nucleotide pathway of sulfolipid biosynthesis became available with the discovery of the bacterial and plant genes encoding the enzymes of sulfolipid biosynthesis during the 1990s. This latter work was based on the foundations laid by A.A. Benson and confirmed one initial hypothesis on sulfolipid biosynthesis. An abbreviated summary of the turning points in defining the mechanism for sulfolipid biosynthesis and remaining issues in sulfolipid biochemistry are provided.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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? Photosynth 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 USA 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

    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

    CAS  Google Scholar 

  • Benson AA (1963) The plant sulfolipid. Adv Lipid Res 1:387–394

    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 USA 45:1582–1587

    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 USA 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 sphaeroides by fast atom bombardment tandem mass spectrometry. Lipids 27:632–636

    Article  PubMed  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 

  • 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 

  • Haines TH (1973) Sulfolipids and halosulfolipids. In: Erwin JA (ed) Lipids and biomembranes of eukaryotic organisms. Academic Press, New York, pp 197–232

    Google Scholar 

  • Harwood JL (1980) Sulfolipids. In: Stumpf PK (ed) The biosynthesis of plants, vol 4. Academic Press, New York, pp 301–320

    Google Scholar 

  • Heinz E (1993) Recent investigations on the biosynthesis of the plant sulfolipid. In: De Kok LJ (ed) Sulfur nutrition and assimilation in higher plants. SPB Academic Publishing, 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 

  • Hoppe W, Schwenn JD (1981) In vitro biosynthesis of the plant sulpholipid: on the origin of the sulphonate group. Z Naturforsch [C ] 36:820–826

    Google Scholar 

  • Joyard J, Blee E, Douce R (1986) Sulfolipid synthesis from 35SO4 and [1–14C]acetate in isolated intact spinach chloroplasts. Biochim Biophys Acta 879:78–87

    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

    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

    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: Rennenberg H, Brunold C, De Kok LJ, Stulen I (eds) sulfur nutrition and sulfur assimilation in higher plants. SPB Academic Publishers, The Hague, pp 77–88

    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 

  • 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 

  • Mudd JB, Kleppinger-Sparace KF (1987) Sulfolipids. In: Stumpf PK (ed) The biochemistry of plants vol. 9. Lipids: structure and function. Academic Press, 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 USA 96:13097–13102

    Article  PubMed  CAS  Google Scholar 

  • Okanenko A (2000) Sulfoquinovosyldiacylglycerol in higher plants: biosynthesis and physiological function. In: Brunold C (ed) Sulfur nutrition and sulfur assimilation in higher plants. Paul Haupt, Bern, CH, pp 203–216

    Google Scholar 

  • Pugh CE, Hawkes T, Harwood JL (1995a) Biosynthesis of sulphoquinovosyldiacylglycerol by chloroplast fractions from pea and lettuce. Phytochem 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

    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 

  • 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 

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

    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

  • 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 

  • Spreitzer RJ, Mets L (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardii with associated light-sensitive phenotypes. Plant Physiol 67:565–569

    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 USA 99:5732–5737

    Article  PubMed  CAS  Google Scholar 

  • Zill LP, Cheniae GM (1962) Lipid metabolism. Ann Rev Plant Physiol 13:225–264

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I am greatly indebted to Chris Somerville, who set me on the trail of sulfolipid, guided me along the way, and one late night in 1987 made the critical suggestion to use R. sphaeroides as the genetic model. He instilled the confidence in me needed to address this classic problem of plant biochemistry at a time when sulfolipid research had come to a near stop. I am also grateful to the students and postdoctoral researchers in my group that ultimately carried the research on sulfolipid biosynthesis and function to fruition.

Work on plant lipids in the Benning lab is currently supported in parts by grants from the US-National Science Foundation, the US-Department of Energy, BASF-Plant Sciences, the MSU Center of Excellence for the Structural Biology Membrane Proteins, and the Michigan Agricultural Experiment Station.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824, USA

    Christoph Benning

Authors
  1. Christoph Benning
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christoph Benning.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benning, C. Questions remaining in sulfolipid biosynthesis: a historical perspective. Photosynth Res 92, 199–203 (2007). https://doi.org/10.1007/s11120-007-9144-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9144-6

Keywords

Search

Navigation