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Plant Biol (Stuttg) 2003; 5(2): 125-136
DOI: 10.1055/s-2003-40726
Review Article

Georg Thieme Verlag Stuttgart · New York

Plant Sphingolipids Today - Are They Still Enigmatic?

S. Spassieva 1 , J. Hille 1
  • 1Department Molecular Biology of Plants, Research School GBB, University of Groningen, The Netherlands
Further Information

Publication History

Publication Date:
21 July 2003 (online)

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Abstract

Sphingolipids are a diverse group of lipids found in all eukaryotes and some bacteria, consisting of a hydrophobic ceramide and a hydrophilic head group. We have summarised the contemporary understanding of the structure of plant sphingolipids with an emphasis on glucosylceramides and inositolphosphorylceramides. Plant glucosylceramides are important structural components of plasma and vacuole membranes. Inositolphosphorylceramides have been identified as moieties of the glycosylphosphorylinositol (GPI) anchors of plant proteins targeted to the plasma membrane. In the last few years, progress has been made in the cloning of plant genes coding for enzymes involved in sphingolipid metabolism. As found in yeast and mammals, the plant sphingolipid pathway is a potential generator of powerful cell signals. The role of plant sphingolipid metabolites in programmed cell death and calcium influx is discussed.

Key words

Plant sphingolipids - ceramide - sphingolipid signalling - membrane lipids - plant GPI-anchored proteins

References

  • 1 Abbas H., Tanaka T., Duke S., Porter J., Wray E., Hodges L., Sessions A., Wang E., Merrill A. H., Riley R.. Fumonisin- and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases.  Plant Physiol.. (1994);  106 1085-1093
    PubMedGoogle Scholar
  • 2 Asai T., Stone J. M., Heard J. E., Kovtun Y., Yorgey P., Sheen J., Ausubel F. M.. Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways.  Plant Cell. (2000);  12 1823-1836
    CrossrefPubMedGoogle Scholar
  • 3 Boggs J. M.. Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function.  Biochim. Biophys. Acta. (1987);  906 353-404
    PubMedGoogle Scholar
  • 4 Bohn M., Heinz E., Luthje S.. Lipid composition and fluidity of plasma membranes isolated from corn (Zea mays L.) roots.  Arch. Biochem. Biophys.. (2001);  387 35-40
    CrossrefPubMedGoogle Scholar
  • 5 Borner G. H. H., Sherrier D. J., Stevens T. J., Arkin I. T., Dupree P.. Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A Genomic Analysis.  Plant Physiol.. (2002);  129 486-499
    CrossrefPubMedGoogle Scholar
  • 6 Brandwagt B. F., Mesbah L. A., Takken F. L., Laurent P. L., Kneppers T. J., Hille J., Nijkamp H. J.. 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
  • 7 Brodersen P., Petersen M., Pike H. M., Olszak B., Skov S., Odum N., Jorgensen L. B., Brown R. E., Mundy J.. 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
  • 8 Cahoon E. B., Lynch D. V.. Analysis of glucocerebrosides of rye (Secale cereale L. cv Puma) leaf and plasma membrane.  Plant Physiol.. (1991);  95 58-68
    PubMedGoogle Scholar
  • 9 Cantatore J. L., Murphy S. M., Lynch D. V.. Compartmentation and topology of glucosylceramide synthesis.  Biochem. Soc. Trans.. (2000);  28 748-750
    CrossrefPubMedGoogle Scholar
  • 10 Carter H. E., Hendry R. A., Nojima S., Stanacev N. Z., Ohno K.. Biochemistry of the sphingolipids XIII. Determination of the structure of cerebrosides from wheat flour.  J. Biol. Chem.. (1961);  236 1912-1916
    PubMedGoogle Scholar
  • 11 Carter H. E., Jonson P., Weber E. J.. Glycolipids.  Ann. Rev. Biochem.. (1965);  34 109-142
    PubMedGoogle Scholar
  • 12 Carter H. E., Koob J. L.. Sphingolipids in bean leaves (Phaseolus vulgaris). .  J. Lipid Res.. (1969);  10 363-369
    PubMedGoogle Scholar
  • 13 Crowther G. J., Lynch D. V.. Characterization of sphinganine kinase activity in corn shoot microsomes.  Arch. Biochem. Biophys.. (1997);  337 284-290
    CrossrefPubMedGoogle Scholar
  • 14 Darjania L., Ichise N., Ichikawa S., Okamoto T., Okuyama H., Thompson Jr G. A.. Dynamic turnover of arabinogalactan proteins in cultured Arabidopsis cells.  Plant Physiol. Biochem.. (2002);  40 69-79
    CrossrefPubMedGoogle Scholar
  • 15 de Nobel H., van Den E. H., Klis F. M.. Cell wall maintenance in fungi.  Trends Microbiol.. (2000);  8 344-345
    CrossrefPubMedGoogle Scholar
  • 16 Fujino Y., Ito S.. Existance of ceramide in alfalfa leaves.  Biochem. Biophys. Acta. (1971);  231 242-243
    PubMedGoogle Scholar
  • 17 Fujino Y., Ohnishi M.. Sphingolipids in wheat grain.  J. Cereal Sci.. (1983);  1 159-168
    PubMedGoogle Scholar
  • 18 Fujino Y., Ohnishi M., Ito S.. Further studies on sphingolipids in wheat grain.  Lipids. (1985);  20 337-342
    PubMedGoogle Scholar
  • 19 Gilchrist D., Wang H., Bostock R.. Sphingosine-related mycotoxins in plant and animal diseases.  Can. J. Bot.. (1995);  73 (Suppl. 1) S459-S467
    PubMedGoogle Scholar
  • 20 Guillas I., Kirchman P. A., Chuard R., Pfefferli M., Jiang J. C., Jazwinski S. M., Conzelmann A.. C26-CoA-dependent ceramide synthesis of Saccharomyces cerevisiae is operated by Lag1 p and Lac1 p.  EMBO J.. (2001);  20 2655-2665
    CrossrefPubMedGoogle Scholar
  • 21 Hakomori S.. Chemistry of glycosphingolipids. Hanahan, D. J., ed. Handbook of lipid research. New York; Plemun Press (1983): 1-165
    Google Scholar
  • 22 Hanada K., Hara T., Nishijima M.. Purification of the serine palmitoyltransferase complex responsible for sphingoid base synthesis by using affinity peptide chromatography techniques.  J. Biol. Chem.. (2000);  275 8409-8415
    CrossrefPubMedGoogle Scholar
  • 23 Hanada K., Hara T., Nishijima M., Kuge O., Dickson R. C., Nagiec M. M.. A mammalian homolog of the yeast LCB1 encodes a component of serine palmitoyltransferase, the enzyme catalyzing the first step in sphingolipid synthesis.  J. Biol. Chem.. (1997);  272 32108-32114
    CrossrefPubMedGoogle Scholar
  • 24 Hannun Y. A., Luberto C., Argraves K. M.. Enzymes of sphingolipid metabolism: from modular to integrative signaling.  Biochemistry. (2001);  40 4893-4903
    CrossrefPubMedGoogle Scholar
  • 25 Hannun Y. A., Obeid L. M.. The Ceramide-centric universe of lipid-mediated cell regulation: Stress encounters of the lipid kind.  J. Biol. Chem.. (2002);  277 25847-25850
    CrossrefPubMedGoogle Scholar
  • 26 Hsieh T. C., Kaul K., Laine R. A., Lester R. L.. Structure of a major glycophosphoceramide from tobacco leaves, PSL-I: 2- deoxy-2-acetamido-D-glucopyranosyl(alpha1 leads to 4)-D- glucuronopyranosyl(alpha1 leads to 2)myoinositol-1-O-phosphoceramide.  Biochemistry. (1978);  17 3575-3581
    CrossrefPubMedGoogle Scholar
  • 27 Hsieh T. C., Lester R. L., Laine R. A.. Glycophosphoceramides from plants. Purification and characterization of a novel tetrasaccharide derived from tobacco leaf glycolipids.  J. Biol. Chem.. (1981);  256 7747-7755
    PubMedGoogle Scholar
  • 28 Imai H., Ohnishi M., Hotsubo K., Kojima M., Ito S.. Sphingoid base composition of cerebrosides from plant leaves.  Biosci. Biotechnol. Biochem.. (1997);  61 351-353
    PubMedGoogle Scholar
  • 29 Imai H., Yamamoto K., Shibahara A., Miyatani S., Nakayama T.. Determining double-bond positions in monoenoic 2-hydroxy fatty acids of glucosylceramides by gas chromatography-mass spectrometry.  Lipids. (2000);  35 233-236
    PubMedGoogle Scholar
  • 30 Jenkins G. M., Richards A., Wahl T., Mao C., Obeid L., Hannun Y.. Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. .  J. Biol. Chem.. (1997);  272 32566-32572
    CrossrefPubMedGoogle Scholar
  • 31 Kaul K., Lester R. L.. Characterization of inositol-containing phosphosphingolipids from tobacco leaves.  Plant Physiol.. (1975);  55 120-129
    PubMedGoogle Scholar
  • 32 Kawaguchi M., Imai H., Naoe M., Yasui Y., Ohnishi M.. Cerebrosides in grapevine leaves: distinct composition of sphingoid bases among the grapevine species having different tolerances to freezing temperature.  Biosci. Biotechnol. Biochem.. (2000);  64 1271-1273
    CrossrefPubMedGoogle Scholar
  • 33 Leipelt M., Warnecke D., Zahringer U., Ott C., Muller F., Hube B., Heinz E.. 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
  • 34 Lester R. L., Dickson R. C.. Sphingolipids with inositolphosphate-containing head groups.  Adv. Lipid Res.. (1993);  26 253-274
    PubMedGoogle Scholar
  • 35 Lynch D. V.. Sphingolipids. Moore, T. S., ed. Lipid Metabolism in Plants. Boca Raton; CRC Press (1993 a): 285-308
    Google Scholar
  • 36 Lynch D. V.. Enzymes of sphingolipid metabolism in plants. Merrill, A. H., Jr. and Hannun, Y., eds. Sphingolipid Metabolism. San Diego; Academic Press (2000): 130-149
    Google Scholar
  • 37 Lynch D. V., Caffrey M., Hogan J. L., Steponkus P. L.. Calorimetric and x-ray diffraction studies of rye glucocerebroside mesomorphism.  Biophys. J.. (1992);  61 1289-1300
    PubMedGoogle Scholar
  • 38 Lynch D. V., Cahoon E. B., Fairfield S. R., Tannishtha. Glycosphingolipids of plant membranes. Quinn, P. J. and Harwood, J. L., eds. Physical Properties of Membrane Lipids. London; Portland Press (1990): 47-52
    Google Scholar
  • 39 Lynch D. V., Fairfield S. R.. Sphingolipid long-chain base synthesis in plants.  Plant Physiol.. (1993);  103 1421-1429
    PubMedGoogle Scholar
  • 40 Lynch D. V., Phinney A. J.. The transbilayer distribution of glucosylceramide in plant plasma membrane. Kader, J. C. and Mazliak, P., eds. Plant Lipid Metabolism. Dordrecht; Kluwer Academic Publishers (1995): 239-241
    Google Scholar
  • 41 Lynch D. V., Spence R. A., Theiling K. M., Thomas K. W., Lee M. T.. Enzymatic reactions involved in ceramide metabolism. Murata, N. and Somerville, C. R., eds. Biochemistry and Molecular Biology of Membrane and Storage Lipids in Plants. Rockville; ASPP (1993 b): 183-190
    Google Scholar
  • 42 Lynch D. V., Steponkus P. L.. Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma).  Plant Physiol.. (1987 a);  83 761-767
    PubMedGoogle Scholar
  • 43 Lynch D. V., Steponkus P. L.. Thermotropic phase behavior of glucocerebrosides from rye leaves.  Cryobiology. (1987 b);  24 555-556
    PubMedGoogle Scholar
  • 44 Mao C., Xu R., Bielawska A., Obeid L. M.. Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity.  J. Biol. Chem.. (2000 a);  275 6876-6884
    CrossrefPubMedGoogle Scholar
  • 45 Mao C., Xu R., Bielawska A., Szulc Z. M., Obeid L. M.. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide.  J. Biol. Chem.. (2000 b);  275 31369-31378
    CrossrefPubMedGoogle Scholar
  • 46 Mao C., Xu R., Szulc Z. M., Bielawska A., Galadari S. H., Obeid L. M.. Cloning and characterization of a novel human alkaline ceramidase. A mammalian enzyme that hydrolyzes phytoceramide.  J. Biol. Chem.. (2001);  276 26577-26588
    CrossrefPubMedGoogle Scholar
  • 47 Merrill Jr. A. H.. De novo sphingolipid biosynthesis: a necessary, but dangerous pathway.  J. Biol. Chem.. (2002);  277 25843-25846
    CrossrefPubMedGoogle Scholar
  • 48 Merrill A. H., Jr., Schmelz E. M., Wang E., Dillehay D. L., Rice L. G., Meredith F., Riley R. T.. Importance of sphingolipids and inhibitors of sphingolipid metabolism as components of animal diets.  J. Nutr.. (1997);  127 830-833
    PubMedGoogle Scholar
  • 49 Merrill A. H., Jr., van Echten G., Wang E., Sandhoff K.. Fumonisin B1 inhibits sphingosine (sphinganine) N-acyltransferase and de novo sphingolipid biosynthesis in cultured neurons in situ.  J. Biol. Chem.. (1993);  268 27299-27306
    PubMedGoogle Scholar
  • 50 Morita N., Nakazato H., Okuyama H., Kim Y., Thompson Jr. G. A.. Evidence for a glycosylinositolphospholipid-anchored alkaline phosphatase in the aquatic plant Spirodela oligorrhiza. .  Biochim. Biophys. Acta. (1996);  1290 53-62
    PubMedGoogle Scholar
  • 51 Muniz M., Riezman H.. Intracellular transport of GPI-anchored proteins.  EMBO J.. (2000);  19 10-15
    CrossrefPubMedGoogle Scholar
  • 52 Nagiec M. M., Baltisberger J. A., Wells G. B., Lester R. L., Dickson R. C.. The LCB2 gene of Saccharomyces and the related LCB1 gene encode subunits of serine palmitoyltransferase, the initial enzyme in sphingolipid synthesis.  Proc. Natl. Acad. Sci. USA. (1994);  91 7899-7902
    PubMedGoogle Scholar
  • 53 Ng C. K., Carr K., McAinsh M. R., Powell B., Hetherington A. M.. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate.  Nature. (2001);  410 596-599
    CrossrefPubMedGoogle Scholar
  • 54 Ng C. K. Y., Hetherington A. M.. Sphingolipid-mediated signalling in Plants.  Ann. Bot.. (2001);  88 957-965
    CrossrefPubMedGoogle Scholar
  • 55 Nishiura H., Tamura K., Morimoto Y., Imai H.. Characterization of sphingolipid long-chain base kinase in Arabidopsis thaliana. .  Biochem. Soc. Trans.. (2000);  28 747-748
    CrossrefPubMedGoogle Scholar
  • 56 Norberg P., Mansson J. E., Liljenberg C.. Characterization of glucosylceramide from plasma membranes of plant root cells.  Biochim. Biophys. Acta. (1991);  1066 257-260
    PubMedGoogle Scholar
  • 57 Norberg P., Nilsson R., Nyiredy S., Liljenberg C.. Glucosylceramides of oat root plasma membranes - physicochemical behaviour in natural and in model systems.  Biochim. Biophys. Acta. (1996);  1299 80-86
    PubMedGoogle Scholar
  • 58 Ohnishi M., Fujino Y.. Chemical composition of ceramide and cerebroside in Azuki bean seeds.  Agric. Biol. Chem.. (1981);  45 1283-1284
    PubMedGoogle Scholar
  • 59 Ohnishi M., Fujino Y.. Sphingolipids in immature and mature soybeans.  Lipids. (1982);  17 803-810
    PubMedGoogle Scholar
  • 60 Ohnishi M., Imai H., Kojima M., Yoshida S., Murata N., Fujino Y., Ito S.. Separation of cerebroside species in plants by reversed-phase HPLC and their phase transition temperature.  Proc. ISF-JOCS World Congress II. (1988): 930-935
    Google Scholar
  • 61 Ohnishi M., Ito S., Fujino Y.. Characterization of sphingolipids in spinach leaves.  Biochem. Biophys. Acta. (1983);  752 416-422
    PubMedGoogle Scholar
  • 62 Ohnishi M., Ito S., Fujino Y.. Structural characterization of sphingolipids in leafy stems of rice.  Agric. Biol. Chem.. (1985);  49 3327-3329
    PubMedGoogle Scholar
  • 63 Oxley D., Bacic A.. Structure of the glycosylphosphatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells.  Proc. Natl. Acad. Sci. USA. (1999);  96 14246-14251
    CrossrefPubMedGoogle Scholar
  • 64 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
  • 65 Poincelot R. P.. Isolation and lipid composition of spinach chloroplast envelop membranes.  Arch. Biochem. Biophys.. (1973);  159 134-142
    CrossrefPubMedGoogle Scholar
  • 66 Reggiori F., Canivenc-Gansel E., Conzelmann A.. Lipid remodelling leads to the introduction and exchange of defined ceramides on GPI proteins in the ER and Golgi of Saccharomyces cerevisiae. .  EMBO J.. (1997);  16 3506-3518
    CrossrefPubMedGoogle Scholar
  • 67 Reggiori F., Conzelmann A.. Biosynthesis of inositol phosphoceramides and remodelling of glycosylphosphatidylinositol anchors in Saccharomyces cerevisiae are mediated by different enzymes.  J. Biol. Chem.. (1998);  273 30550-30559
    CrossrefPubMedGoogle Scholar
  • 68 Rochester C. P., Kjellbom P., Andersson B., Larsson C.. Lipid composition of plasma membranes isolated from light-grown barley (Hordeum vulgare) leaves: identification of cerebroside as a major component.  Arch. Biochem. Biophys.. (1987);  255 385-391
    CrossrefPubMedGoogle Scholar
  • 69 Sandstrom R. P., Cleland R. E.. Comparison of the lipid composition of oat root and coleoptile plasma membranes: lack of short-term change in response to auxin.  Plant Physiol.. (1989);  90 1207-1213
    PubMedGoogle Scholar
  • 70 Schmelz E. M., Roberts P. C., Kustin E. M., Lemonnier L. A., Sullards M. C., Dillehay D. L., Merrill Jr. A. H.. Modulation of intracellular β-catenin localization and intestinal tumorigenesis in vivo and in vitro by sphingolipids.  Cancer Res.. (2001);  61 6723-6729
    PubMedGoogle Scholar
  • 71 Schorling S., Vallee B., Barz W. P., Riezman H., Oesterhelt D.. Lag1 p and Lac1 p are essential for the Acyl-CoA-dependent ceramide synthase reaction in Saccharomyces cerevisae. .  Mol. Biol. Cell. (2001);  12 3417-3427
    PubMedGoogle Scholar
  • 72 Simons K., Ikonen E.. Functional rafts in cell membranes.  Nature. (1997);  387 569-572
    CrossrefPubMedGoogle Scholar
  • 73 Spassieva S. D., Markham J. E., Hille J.. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin induced programmed cell death.  Plant J.. (2002);  32 561-572
    CrossrefPubMedGoogle Scholar
  • 74 Sperling P., Blume A., Zahringer U., Heinz E.. Further characterization of Delta(8)-sphingolipid desaturases from higher plants.  Biochem. Soc. Trans.. (2000);  28 638-641
    CrossrefPubMedGoogle Scholar
  • 75 Sperling P., Libisch B., Zahringer U., Napier J. A., Heinz E.. Functional identification of a delta8-sphingolipid desaturase from Borago officinalis. .  Arch. Biochem. Biophys.. (2001 a);  388 293-298
    CrossrefPubMedGoogle Scholar
  • 76 Sperling P., Ternes P., Moll H., Franke S., Zahringer U., Heinz E.. Functional characterization of sphingolipid C4-hydroxylase genes from Arabidopsis thaliana. .  FEBS Lett.. (2001 b);  494 90-94
    CrossrefPubMedGoogle Scholar
  • 77 Sperling P., Zahringer 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
  • 78 Spiegel S., Milstien S.. Sphingosine 1-phosphate, a key cell signaling molecule.  J. Biol. Chem.. (2002);  277 25851-25854
    CrossrefPubMedGoogle Scholar
  • 79 Steponkus P. L., Lynch D. V.. Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation.  J. Bioenerg. Biomembr.. (1989);  21 21-41
    PubMedGoogle Scholar
  • 80 Sugawara T., Miyazawa T.. Separation and determination of glycolipids from edible plant sources by high-performance liquid chromatography and evaporative light-scattering detection.  Lipids. (1999);  34 1231-1237
    PubMedGoogle Scholar
  • 81 Sullards M. C., Lynch D. V., Merrill Jr. A. H., Adams J.. Structure determination of soybean and wheat glucosylceramides by tandem mass spectrometry.  J. Mass Spectrom.. (2000);  35 347-353
    CrossrefPubMedGoogle Scholar
  • 82 Takos A. M., Dry I. B., Soole K. L.. Detection of glycosyl-phosphatidylinositol-anchored proteins on the surface of Nicotiana tabacum protoplasts.  FEBS Lett.. (1997);  405 1-4
    CrossrefPubMedGoogle Scholar
  • 83 Takos A. M., Dry I. B., Soole K. L.. Glycosyl-phosphatidylinositol-anchor addition signals are processed in Nicotiana tabacum. .  Plant J.. (2000);  21 43-52
    CrossrefPubMedGoogle Scholar
  • 84 Tamura K., Mitsuhashi N., Hara-Nishimura I., Imai H.. 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
  • 85 Tamura K., Nishiura H., Mori J., Imai H.. Cloning and characterization of a cDNA encoding serine palmitoyltransferase in Arabidopsis thaliana. .  Biochem. Soc. Trans.. (2000);  28 745-747
    CrossrefPubMedGoogle Scholar
  • 86 Tavernier E., Le Quoc D., Le Quoc K.. Lipid composition of the vacuolar membrane of Acer pseudoplatanus cultured cells.  Biochim. Biophys. Acta. (1993);  1167 242-247
    PubMedGoogle Scholar
  • 87 Ternes P., Franke S., Zahringer U., Sperling P., Heinz E.. Identification and characterization of a sphingolipid delta4-desaturase family.  J. Biol. Chem.. (2002);  227 25512-25518
    PubMedGoogle Scholar
  • 88 Thudichum J. L. W.. Reports of the medical officer of privy council and local government board. N. Ser. III. (1874): 113
    Google Scholar
  • 89 Tolleson W. H., Couch L. H., Melchior W. B., Jr., Jenkins G. R., Muskhelishvili M., Muskhelishvili L., McGarrity L. J., Domon O., Morris S. M., Howard P. C.. Fumonisin B1 induces apoptosis in cultured human keratinocytes through sphinganine accumulation and ceramide depletion.  Int. J. Oncol.. (1999);  14 833-843
    PubMedGoogle Scholar
  • 90 Uemura M., Steponkus P. L.. 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
  • 91 Venkataraman K., Riebeling C., Bodennec J., Riezman H., Allegood J. C., Sullards M. C., Merrill A. H., Jr., Futerman A. H.. Upstream of growth and differentiation factor 1 (uog1), a mammalian homolog of the yeast longevity assurance gene 1 (LAG1), regulates N-Stearoyl-sphinganine (C18-(Dihydro)ceramide) synthesis in a Fumonisin B1-independent manner in mammalian cells.  J. Biol. Chem.. (2002);  277 35642-35649
    CrossrefPubMedGoogle Scholar
  • 92 Vesper H., Schmelz E. M., Nikolova-Karakashian M. N., Dillehay D. L., Lynch D. V., Merrill Jr. A. H.. Sphingolipids in food and the emerging importance of sphingolipids to nutrition.  J. Nutr.. (1999);  129 1239-1250
    PubMedGoogle Scholar
  • 93 Wang E., Li J., Bostock R., Gilchrist D.. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development.  Plant Cell. (1996);  8 375-391
    CrossrefPubMedGoogle Scholar
  • 94 Wang E., Norred W. P., Bacon C. W., Riley R. T., Merrill Jr. A. H.. Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. .  J. Biol. Chem.. (1991);  266 14486-14490
    PubMedGoogle Scholar
  • 95 Weiss B., Stoffel W.. Human and murine serine-palmitoyl-CoA transferase - cloning, expression and characterization of the key enzyme in sphingolipid synthesis.  Eur. J. Biochem.. (1997);  249 239-247
    CrossrefPubMedGoogle Scholar
  • 96 Witsenboer H., Schaik C. E., Bino R. J., Loffler H. J. M., Nijkamp H. J., Hille J.. Effects of Alternaria alternata f.sp. lycopersici toxins at different levels of tomato plant cell development.  Plant Science. (1988);  56 253-260
    CrossrefPubMedGoogle Scholar
  • 97 Xu X., Bittman R., Duportail G., Heissler D., Vilcheze C., London E.. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide.  J. Biol. Chem.. (2001);  276 33540-33546
    CrossrefPubMedGoogle Scholar
  • 98 Yoshida S., Uemura M.. Lipid composition of plasma membranes and tonoplasts isolated from etiolated seedlings of mung bean (Vigna radiata L.).  Plant Physiol.. (1986);  82 807-812
    PubMedGoogle Scholar
  • 99 Yoshida S., Washio K., Kenrick J., Orr G.. Thermotropic properties of lipids extracted from plasma membrane and tonoplast isolated from chilling-sensitive mung bean (Vigna radiata [L.] Wilczek).  Plant Cell Physiol.. (1988);  29 1411-1416
    PubMedGoogle Scholar

S. Spassieva

Dept. Molecular Biology of Plants
Research School GBB
University of Groningen

Kerklaan 30

9751 NN Haren

The Netherlands

Email: s.d.spassieva@biol.rug.nl

Section Editor: L. A. C. J. Voesenek