Home LiteratureArticle Details
PMID: 18978071 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional characterization of a higher plant sphingolipid Delta4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis.

Plant physiology ·Vol. 149 ·No. 1 ·2009-01-00 ·Pages 487-98

Michaelson LV, Zäuner S, Markham JE, Haslam RP, Desikan R, Mugford S, Albrecht S, Warnecke D, Sperling P, Heinz E, Napier JA

Abstract

The role of Delta4-unsaturated sphingolipid long-chain bases such as sphingosine was investigated in Arabidopsis (Arabidopsis thaliana). Identification and functional characterization of the sole Arabidopsis ortholog of the sphingolipid Delta4-desaturase was achieved by heterologous expression in Pichia pastoris. A P. pastoris mutant disrupted in the endogenous sphingolipid Delta4-desaturase gene was unable to synthesize glucosylceramides. Synthesis of glucosylceramides was restored by the expression of Arabidopsis gene At4g04930, and these sphingolipids were shown to contain Delta4-unsaturated long-chain bases, confirming that this open reading frame encodes the sphingolipid Delta4-desaturase. At4g04930 has a very restricted expression pattern, transcripts only being detected in pollen and floral tissues. Arabidopsis insertion mutants disrupted in the sphingolipid Delta4-desaturase At4g04930 were isolated and found to be phenotypically normal. Sphingolipidomic profiling of a T-DNA insertion mutant indicated the absence of Delta4-unsaturated sphingolipids in floral tissue, also resulting in the reduced accumulation of glucosylceramides. No difference in the response to drought or water loss was observed between wild-type plants and insertion mutants disrupted in the sphingolipid Delta4-desaturase At4g04930, nor was any difference observed in stomatal closure after treatment with abscisic acid. No differences in pollen viability between wild-type plants and insertion mutants were detected. Based on these observations, it seems unlikely that Delta4-unsaturated sphingolipids and their metabolites such as sphingosine-1-phosphate play a significant role in Arabidopsis growth and development. However, Delta4-unsaturated ceramides may play a previously unrecognized role in the channeling of substrates for the synthesis of glucosylceramides.

MeSH Terms
Arabidopsis/enzymology,genetics,growth & development Arabidopsis Proteins/genetics,metabolism Cloning, Molecular DNA, Bacterial/genetics Gene Expression Regulation, Plant Glucosylceramides/biosynthesis Lysophospholipids/metabolism Mutagenesis, Insertional Open Reading Frames Oxidoreductases/genetics,metabolism Phylogeny Pichia/genetics Sequence Deletion Sphingosine/analogs & derivatives,metabolism
Chemicals
Arabidopsis Proteins DNA, Bacterial Glucosylceramides Lysophospholipids T-DNA sphingosine 1-phosphate Oxidoreductases sphingolipid desaturase Sphingosine
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Michaelson Louise V
Biological Chemistry Department, Rothamsted Research, Harpenden, Hertshire AL5 2JQ, United Kingdom.
Zäuner Simone
Markham Jonathan E
Haslam Richard P
Desikan Radhika
Mugford Sarah
Albrecht Sandra
Warnecke Dirk
Sperling Petra
Heinz E
Napier Johnathan A
References (46)
46 references, click to expand
  1. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts.
    Plant Physiol. 2005 Jan;137(1):104-16 PMID: 15618420
  2. Fatty acid desaturases from the microalga Thalassiosira pseudonana.
    FEBS J. 2005 Jul;272(13):3401-12 PMID: 15978045
  3. A trial of phenome analysis using 4000 Ds-insertional mutants in gene-coding regions of Arabidopsis.
    Plant J. 2006 Aug;47(4):640-51 PMID: 16813574
  4. Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis.
    Cell Res. 2007 Dec;17(12):1030-40 PMID: 18059378
  5. Identification and characterization of a sphingolipid delta 4-desaturase family.
    J Biol Chem. 2002 Jul 12;277(28):25512-8 PMID: 11937514
  6. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis.
    Plant Cell. 2008 Jul;20(7):1862-78 PMID: 18612100
  7. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets.
    PLoS One. 2007;2(8):e718 PMID: 17684564
  8. Degenerative spermatocyte, a novel gene encoding a transmembrane protein required for the initiation of meiosis in Drosophila spermatogenesis.
    Mol Gen Genet. 1996 Nov 27;253(1-2):157-65 PMID: 9003299
  9. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  10. 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(7):1304-14 PMID: 17340572
  11. 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 Apr;54(2):284-98 PMID: 18208516
  12. The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development.
    Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14727-31 PMID: 18799749
  13. 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 Dec;18(12):3576-93 PMID: 17194770
  14. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  15. The Critical Requirement for Linolenic Acid Is Pollen Development, Not Photosynthesis, in an Arabidopsis Mutant.
    Plant Cell. 1996 Mar;8(3):403-416 PMID: 12239389
  16. Separation and identification of major plant sphingolipid classes from leaves.
    J Biol Chem. 2006 Aug 11;281(32):22684-94 PMID: 16772288
  17. A higher plant delta8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants.
    Plant Physiol. 2007 Aug;144(4):1968-77 PMID: 17600137
  18. Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis.
    Dev Cell. 2001 Dec;1(6):771-81 PMID: 11740939
  19. Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins.
    Nature. 2003 Jun 5;423(6940):651-4 PMID: 12789341
  20. Plant sphingolipids: structural diversity, biosynthesis, first genes and functions.
    Biochim Biophys Acta. 2003 Jun 10;1632(1-3):1-15 PMID: 12782146
  21. Sphingosine 1-phosphate signalling in mammalian cells.
    Biochem J. 2000 Jul 15;349(Pt 2):385-402 PMID: 10880336
  22. Intracellular signalling: sphingosine-1-phosphate branches out.
    Curr Biol. 2001 Jul 10;11(13):R535-8 PMID: 11470429
  23. Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1.
    Plant J. 2004 Jun;38(5):810-22 PMID: 15144382
  24. Ceramides modulate programmed cell death in plants.
    Genes Dev. 2003 Nov 1;17(21):2636-41 PMID: 14563678
  25. The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes.
    J Lipid Res. 2008 Jan;49(1):183-91 PMID: 17921532
  26. Sphingosine-1-phosphate: an enigmatic signalling lipid.
    Nat Rev Mol Cell Biol. 2003 May;4(5):397-407 PMID: 12728273
  27. The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis.
    Plant Physiol. 2007 Jul;144(3):1467-80 PMID: 17468211
  28. Characterization of ceramide synthesis. A dihydroceramide desaturase introduces the 4,5-trans-double bond of sphingosine at the level of dihydroceramide.
    J Biol Chem. 1997 Sep 5;272(36):22432-7 PMID: 9312549
  29. Characterization of two GL8 paralogs reveals that the 3-ketoacyl reductase component of fatty acid elongase is essential for maize (Zea mays L.) development.
    Plant J. 2005 Jun;42(6):844-61 PMID: 15941398
  30. Structure determination of soybean and wheat glucosylceramides by tandem mass spectrometry.
    J Mass Spectrom. 2000 Mar;35(3):347-53 PMID: 10767763
  31. The dihydroceramide desaturase is not essential for cell viability in Schizosaccharomyces pombe.
    FEBS Lett. 2003 Mar 13;538(1-3):192-6 PMID: 12633877
  32. Point-counterpoint of sphingosine 1-phosphate metabolism.
    Circ Res. 2004 Apr 2;94(6):724-34 PMID: 15059942
  33. Death and taxis: what non-mammalian models tell us about sphingosine-1-phosphate.
    Semin Cell Dev Biol. 2004 Oct;15(5):529-40 PMID: 15271298
  34. Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis.
    Plant Physiol. 2008 Mar;146(3):1322-32 PMID: 18218968
  35. Functional characterization of sphingolipid C4-hydroxylase genes from Arabidopsis thaliana.
    FEBS Lett. 2001 Apr 6;494(1-2):90-4 PMID: 11297741
  36. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling.
    Nature. 2008 Mar 27;452(7186):487-91 PMID: 18305484
  37. Identification of fungal sphingolipid C9-methyltransferases by phylogenetic profiling.
    J Biol Chem. 2006 Mar 3;281(9):5582-92 PMID: 16339149
  38. Involvement of sphingosine kinase in plant cell signalling.
    Plant J. 2008 Oct;56(1):64-72 PMID: 18557834
  39. Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture.
    Plant Physiol. 2005 Feb;137(2):724-37 PMID: 15665242
  40. Sphingolipids, new players in plant signaling.
    Trends Plant Sci. 2003 Jul;8(7):317-20 PMID: 12878015
  41. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate.
    Nature. 2001 Mar 29;410(6828):596-9 PMID: 11279499
  42. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci.
    Plant J. 1996 Oct;10(4):655-61 PMID: 8893542
  43. Disruptions of the Arabidopsis Enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis.
    Plant Cell. 2005 May;17(5):1467-81 PMID: 15829606
  44. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis.
    Plant Physiol. 2005 Sep;139(1):5-17 PMID: 16166256
  45. A new class of lipid desaturase central to sphingolipid biosynthesis and signalling.
    Trends Plant Sci. 2002 Nov;7(11):475-8 PMID: 12417141
  46. A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana.
    Ann Bot. 2004 May;93(5):483-97 PMID: 15037448
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2009-01-00
Epub
2008-00-31
Pages
487-98
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2613699
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/C/00004949 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com