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Biosynthesis of Sphingolipids in Plants (and Some of Their Functions)

  • Simone Zäuner
  • Philipp Ternes
  • Dirk Warnecke
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 688)

Abstract

Our knowledge of plant sphingolipid metabolism and function has significantly increased over the past years. This applies mainly to the identification and the functional characterization of genes and enzymes involved in sphingolipid biosynthesis. In addition a number of plant mutants have provided new insights into sphingolipid functions. Very little is still known about intracellular transport, spatial distribution, degradation and signaling functions of sphingolipids. However, combination of Arabidopsis genetics with lipidomics and cell biology will soon bring our understanding of these issues to a new level.

Keywords

Chain Base Serine Palmitoyltransferase Ulatory Molecule Plant Sphingolipid Confer Aluminum Tolerance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Sperling P, Heinz E. Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim Biophys Acta 2003; 1632:1–15.PubMedGoogle Scholar
  2. 2.
    Sperling P, Warnecke D, Heinz E. Plant sphingolipids. In: Daum G, ed. Lipid metabolism and membrane biogenesis. Berlin, Heidelberg: Springer-Verlag, 2004; 6:337–381.Google Scholar
  3. 3.
    Dunn TM, Lynch DV, Michaelson LV et al. A postgenomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann Bot (Lond) 2004; 93:483–497.CrossRefGoogle Scholar
  4. 4.
    Lynch DV, Dunn TM. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytologist 2004; 161:677.CrossRefGoogle Scholar
  5. 5.
    Hofius D, Tsitsigiannis DI, Jones JD et al. Inducible cell death in plant immunity. Semin Cancer Biol 2007; 17:166–187.CrossRefPubMedGoogle Scholar
  6. 6.
    Gadjev I, Stone JM, Gechev TS. Programmed cell death in plants new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 2008; 270:87–144.CrossRefPubMedGoogle Scholar
  7. 7.
    Peskan T, Westermann M, Oelmuller R. Identification of low-density Triton X-100-insoluble plasma membrane microdomains in higher plants. Eur J Biochem 2000; 267:6989–6995.CrossRefPubMedGoogle Scholar
  8. 8.
    Mongrand S, Morel J, Laroche J et al. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 2004; 279:36277–36286.CrossRefPubMedGoogle Scholar
  9. 9.
    Lefebvre B, Furt F, Hartmann MA et al. Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 2007; 144:402–418.CrossRefPubMedGoogle Scholar
  10. 10.
    Roche Y, Gerbeau-Pissot P, Buhot B et al. Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts. FASEB J 2008; 22:3980–3991.CrossRefPubMedGoogle Scholar
  11. 11.
    Borner GH, Sherrier DJ, Weimar T et al. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 2005; 137:104–116.CrossRefPubMedGoogle Scholar
  12. 12.
    Laloi M, Perret AM, Chatre L et al. Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 2007; 143:461–472.CrossRefPubMedGoogle Scholar
  13. 13.
    Brodersen P, Petersen M, Pike HM et al. Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 2002; 16:490–502.CrossRefPubMedGoogle Scholar
  14. 14.
    Petersen NH, McKinney LV, Pike H et al. Human GLTP and mutant forms of ACD11 suppress cell death in the Arabidopsis acd11 mutant. FEBS J 2008; 275:4378–4388.CrossRefPubMedGoogle Scholar
  15. 15.
    Petersen NH, Joensen J, McKinney LV et al. Identification of proteins interacting with Arabidopsis ACD11. J Plant Physiol 2008.Google Scholar
  16. 16.
    West G, Viitanen L, Alm C et al. Identification of a glycosphingolipid transfer protein GLTP1 in Arabidopsis thaliana. FEBS J 2008; 275:3421–3437.CrossRefPubMedGoogle Scholar
  17. 17.
    Brodersen P, Malinovsky FG, Hematy K et al. The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol 2005; 138:1037–1045.CrossRefPubMedGoogle Scholar
  18. 18.
    Pruett ST, Bushnev A, Hagedorn K et al. Biodiversity of sphingoid bases (“sphingosines”) and related amino alcohols. J Lipid Res 2008; 49:1621–1639.CrossRefPubMedGoogle Scholar
  19. 19.
    Sperling P, Zähringer U, Heinz E. A sphingolipid desaturase from higher plants. Identification of a new cytochrome b5 fusion protein. J Biol Chem 1998; 273:28590–28596.CrossRefPubMedGoogle Scholar
  20. 20.
    Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 2008; 9:139–150.CrossRefPubMedGoogle Scholar
  21. 21.
    Markham JE, Jaworski JG. Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 2007; 21:1304–1314.CrossRefPubMedGoogle Scholar
  22. 22.
    Michaelson LV, Zäuner S, Markham JE et al. Functional characterization of a higher plant sphingolipid ?4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis. Plant Physiol 2009; 149:487–498.CrossRefPubMedGoogle Scholar
  23. 23.
    Sperling P, Franke S, Lüthje S et al. Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiol Biochem 2005; 43:1031–1038.CrossRefPubMedGoogle Scholar
  24. 24.
    Chen M, Han G, Dietrich CR et al. The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 2006; 18:3576–3593.CrossRefPubMedGoogle Scholar
  25. 25.
    Tamura K, Mitsuhashi N, Hara-Nishimura I et al. Characterization of an Arabidopsis cDNA encoding a subunit of serine palmitoyltransferase, the initial enzyme in sphingolipid biosynthesis. Plant Cell Physiol 2001; 42:1274–1281.CrossRefPubMedGoogle Scholar
  26. 26.
    Teng C, Dong H, Shi L et al. Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol 2008; 146:1322–1332.CrossRefPubMedGoogle Scholar
  27. 27.
    Shi L, Bielawski J, Mu J et al. Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 2007; 17:1030–1040.CrossRefPubMedGoogle Scholar
  28. 28.
    Dietrich CR, Han G, Chen M et al. Loss-of-function mutations and inducible RNAi suppression of Arabidopsis LCB2 genes reveal the critical role of sphingolipids in gametophytic and sporophytic cell viability. Plant J 2008; 54:284–298.CrossRefPubMedGoogle Scholar
  29. 29.
    Takahashi Y, Berberich T, Kanzaki H et al. Serine palmitoyltransferase, the first step enzyme in sphingolipid biosynthesis, is involved in nonhost resistance. Mol Plant Microbe Interact 2009; 22:31–38.CrossRefPubMedGoogle Scholar
  30. 30.
    Sperling P, Ternes P, Moll H et al. Functional characterization of sphingolipid C4-hydroxylase genes from Arabidopsis thaliana. FEBS Lett 2001; 494:90–94.CrossRefPubMedGoogle Scholar
  31. 31.
    Chen M, Markham JE, Dietrich CR et al. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 2008; 20:1862–1878.CrossRefPubMedGoogle Scholar
  32. 32.
    Marion J, Bach L, Bellec Y et al. Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J 2008; 56:169–179.CrossRefPubMedGoogle Scholar
  33. 33.
    Brandwagt BF, Mesbah LA, Takken FL et al. A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 2000; 97:4961–4966.CrossRefPubMedGoogle Scholar
  34. 34.
    Brandwagt BF, Kneppers TJ, Nijkamp HJ et al. Overexpression of the tomato Asc-1 gene mediates high insensitivity to AAL toxins and fumonisin B1 in tomato hairy roots and confers resistance to Alternaria alternata f. sp. lycopersici in Nicotiana umbratica plants. Mol Plant Microbe Interact 2002; 15:35–42.CrossRefPubMedGoogle Scholar
  35. 35.
    Pata MO, Wu BX, Bielawski J et al. Molecular cloning and characterization of OsCDase, a ceramidase enzyme from rice. Plant J 2008; 55:1000–1009.CrossRefPubMedGoogle Scholar
  36. 36.
    Nagano M, Ihara-Ohori Y, Imai H et al. Functional association of cell death suppressor, Arabidopsis Bax inhibitor-1, with fatty acid 2-hydroxylation through cytochrome b. Plant J 2009.Google Scholar
  37. 37.
    Leipelt M, Warnecke D, Zähringer U et al. Glucosylceramide synthases, a gene family responsible for the biosynthesis of glucosphingolipids in animals, plants and fungi. J Biol Chem 2001; 276:33621–33629.CrossRefPubMedGoogle Scholar
  38. 38.
    Tamura K, Nishiura H, Mori J et al. Cloning and characterization of a cDNA encoding serine palmitoyltransferase in Arabidopsis thaliana. Biochem Soc Trans 2000; 28:745–747.CrossRefPubMedGoogle Scholar
  39. 39.
    Imai H, Nishiura H. Phosphorylation of sphingoid long-chain bases in Arabidopsis: functional characterization and expression of the first sphingoid long-chain base Kinase gene in plants. Plant Cell Physiol 2005; 46:375–380.CrossRefPubMedGoogle Scholar
  40. 40.
    Worrall D, Liang YK, Alvarez S et al. Involvement of sphingosine kinase in plant cell signalling. Plant J 2008; 56:64–72.CrossRefPubMedGoogle Scholar
  41. 41.
    Tsegaye Y, Richardson CG, Bravo JE et al. Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J Biol Chem 2007; 282:28195–28206.CrossRefPubMedGoogle Scholar
  42. 42.
    Nishikawa M, Hosokawa K, Ishiguro M et al. Degradation of sphingoid long-chain base 1-phosphates (LCB-1Ps): functional characterization and expression of AtDPL1 encoding LCB-1P lyase involved in the dehydration stress response in Arabidopsis. Plant Cell Physiol 2008; 49:1758–1763.CrossRefPubMedGoogle Scholar
  43. 43.
    Liang H, Yao N, Song JT et al. Ceramides modulate programmed cell death in plants. Genes Dev 2003; 17:2636–2641.CrossRefPubMedGoogle Scholar
  44. 44.
    Wang W, Yang X, Tangchaiburana S et al. An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 2008; 20:3163–3179.CrossRefPubMedGoogle Scholar
  45. 45.
    Wright BS, Snow JW, O’Brien TC et al. Synthesis of 4-hydroxysphinganine and characterization of sphinganine hydroxylase activity in corn. Arch Biochem Biophys 2003; 415:184–192.CrossRefPubMedGoogle Scholar
  46. 46.
    Markham JE, Li J, Cahoon EB et al. Separation and identification of major plant sphingolipid classes from leaves. J Biol Chem 2006; 281:22684–22694.CrossRefPubMedGoogle Scholar
  47. 47.
    Uemura M, Joseph RA, Steponkus PL. Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 1995; 109:15–30.PubMedGoogle Scholar
  48. 48.
    Uemura M, Steponkus PL. A contrast of the plasma membrane lipid composition of oat and rye leaves in relation to freezing tolerance. Plant Physiol 1994; 104:479–496.PubMedGoogle Scholar
  49. 49.
    Cahoon EB, Lynch DV. Analysis of glucocerebrosides of rye (Secale cereale L. cv Puma) leaf and plasma membrane. Plant Physiol 1991; 95:58–68.CrossRefPubMedGoogle Scholar
  50. 50.
    Townley HE, McDonald K, Jenkins GI et al. Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner. Biol Chem 2005; 386:161–166.CrossRefPubMedGoogle Scholar
  51. 51.
    Ternes P, Franke S, Zähringer U et al. Identification and characterization of a sphingolipid ? 4-desaturase family. J Biol Chem 2002; 277:25512–25518.CrossRefPubMedGoogle Scholar
  52. 52.
    Bach L, Michaelson LV, Haslam R et al. The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proc Natl Acad Sci USA 2008; 105:14727–14731.CrossRefPubMedGoogle Scholar
  53. 53.
    da Silva AL, Sperling P, Horst W et al. A possible role of sphingolipids in the aluminium resistance of yeast and maize. J Plant Physiol 2006; 163:26–38.CrossRefPubMedGoogle Scholar
  54. 54.
    Ryan PR, Liu Q, Sperling P et al. A higher plant delta8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiol 2007; 144:1968–1977.CrossRefPubMedGoogle Scholar
  55. 55.
    Denny PW, Shams-Eldin H, Price HP et al. The protozoan inositol phosphorylceramide synthase: a novel drug target that defines a new class of sphingolipid synthase. J Biol Chem 2006; 281:28200–28209.CrossRefPubMedGoogle Scholar
  56. 56.
    Abbas HK, Tanaka T, Duke SO et al. Fumonisin-and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol 1994; 106:1085–1093.PubMedGoogle Scholar
  57. 57.
    Crowther GJ, Lynch DV. Characterization of sphinganine kinase activity in corn shoot microsomes. Arch Biochem Biophys 1997; 337:284–290.CrossRefPubMedGoogle Scholar
  58. 58.
    Nishiura H, Tamura K, Morimoto Y et al. Characterization of sphingolipid long-chain base kinase in Arabidopsis thaliana. Biochem Soc Trans 2000; 28:747–748.CrossRefPubMedGoogle Scholar
  59. 59.
    Chalfant CE, Spiegel S. Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J Cell Sci 2005; 118:4605–4612.CrossRefPubMedGoogle Scholar
  60. 60.
    Coursol S, Fan LM, Le Stunff H et al. Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 2003; 423:651–654.CrossRefPubMedGoogle Scholar
  61. 61.
    Coursol S, Le Stunff H, Lynch DV et al. Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture. Plant Physiol 2005; 137:724–737.CrossRefPubMedGoogle Scholar
  62. 62.
    Pandey S, Assmann SM. The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 2004; 16:1616–1632.CrossRefPubMedGoogle Scholar
  63. 63.
    Ng CK, Carr K, McAinsh MR et al. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 2001; 410:596–599.CrossRefPubMedGoogle Scholar
  64. 64.
    Le Stunff H, Galve-Roperh I, Peterson C et al. Sphingosine-1-phosphate phosphohydrolase in regulation of sphingolipid metabolism and apoptosis. J Cell Biol 2002; 158:1039–1049.CrossRefPubMedGoogle Scholar
  65. 65.
    Haynes CA, Allegood JC, Park H et al. Sphingolipidomics: Methods for the comprehensive analysis of sphingolipids. J Chromatogr B Analyt Technol Biomed Life Sci 2008.Google Scholar
  66. 66.
    Welti R, Shah J, Li W et al. Plant lipidomics: discerning biological function by profiling plant complex lipids using mass spectrometry. Front Biosci 2007; 12:2494–2506.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.Departments of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA
  2. 2.Albrecht-von-Haller-Institute for Plant Sciences Department for Plant BiochemistryUniversity of GoettingenGoettingenGermany
  3. 3.Biocenter Klein FlottbekUniversity of HamburgHamburgGermany

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