Home LiteratureArticle Details
PMID: 20876112 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants.

James CN, Horn PJ, Case CR, Gidda SK, Zhang D, Mullen RT, Dyer JM, Anderson RG, Chapman KD

Abstract

CGI-58 is the defective gene in the human neutral lipid storage disease called Chanarin-Dorfman syndrome. This disorder causes intracellular lipid droplets to accumulate in nonadipose tissues, such as skin and blood cells. Here, disruption of the homologous CGI-58 gene in Arabidopsis thaliana resulted in the accumulation of neutral lipid droplets in mature leaves. Mass spectroscopy of isolated lipid droplets from cgi-58 loss-of-function mutants showed they contain triacylglycerols with common leaf-specific fatty acids. Leaves of mature cgi-58 plants exhibited a marked increase in absolute triacylglycerol levels, more than 10-fold higher than in wild-type plants. Lipid levels in the oil-storing seeds of cgi-58 loss-of-function plants were unchanged, and unlike mutations in β-oxidation, the cgi-58 seeds germinated and grew normally, requiring no rescue with sucrose. We conclude that the participation of CGI-58 in neutral lipid homeostasis of nonfat-storing tissues is similar, although not identical, between plant and animal species. This unique insight may have implications for designing a new generation of technologies that enhance the neutral lipid content and composition of crop plants.

MeSH Terms
1-Acylglycerol-3-Phosphate O-Acyltransferase/genetics,metabolism Age Factors Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism DNA Primers/genetics Fatty Acids/analysis Humans Lipids/chemistry Mass Spectrometry Microscopy, Fluorescence Plant Leaves/metabolism Reverse Transcriptase Polymerase Chain Reaction Seeds/chemistry Triglycerides/analysis
Chemicals
Arabidopsis Proteins DNA Primers Fatty Acids Lipids Triglycerides 1-Acylglycerol-3-Phosphate O-Acyltransferase ABHD5 protein, human
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
James Christopher N
Department of Biological Sciences, Center for Plant Lipid Research, University of North Texas, Denton, TX 76203, USA.
Horn Patrick J
Case Charlene R
Gidda Satinder K
Zhang Daiyuan
Mullen Robert T
Dyer John M
Anderson Richard G W
Chapman Kent D
References (46)
46 references, click to expand
  1. The role of alpha-tocopherol in plant stress tolerance.
    J Plant Physiol. 2005 Jul;162(7):743-8 PMID: 16008098
  2. Nile red: a selective fluorescent stain for intracellular lipid droplets.
    J Cell Biol. 1985 Mar;100(3):965-73 PMID: 3972906
  3. Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum.
    Plant Cell. 2006 Sep;18(9):2294-313 PMID: 16920778
  4. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome.
    Cell Metab. 2006 May;3(5):309-19 PMID: 16679289
  5. Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes.
    J Biol Chem. 2004 Oct 1;279(40):42062-71 PMID: 15292255
  6. The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology.
    Proc Natl Acad Sci U S A. 2007 Dec 26;104(52):20890-5 PMID: 18093937
  7. The production of unusual fatty acids in transgenic plants.
    Annu Rev Plant Biol. 2007;58:295-319 PMID: 17472567
  8. Many roads lead to the lipid droplet.
    Cell Metab. 2008 Jun;7(6):472-3 PMID: 18522827
  9. Engineering oilseeds to produce nutritional fatty acids.
    Physiol Plant. 2008 Jan;132(1):1-10 PMID: 18251865
  10. N-Acylethanolamine metabolism interacts with abscisic acid signaling in Arabidopsis thaliana seedlings.
    Plant Cell. 2007 Aug;19(8):2454-69 PMID: 17766402
  11. High-value oils from plants.
    Plant J. 2008 May;54(4):640-55 PMID: 18476869
  12. CGI-58, the causative gene for Chanarin-Dorfman syndrome, mediates acylation of lysophosphatidic acid.
    J Biol Chem. 2008 Sep 5;283(36):24525-33 PMID: 18606822
  13. YLR099C (ICT1) encodes a soluble Acyl-CoA-dependent lysophosphatidic acid acyltransferase responsible for enhanced phospholipid synthesis on organic solvent stress in Saccharomyces cerevisiae.
    J Biol Chem. 2008 Apr 11;283(15):9768-75 PMID: 18252723
  14. Seed storage oil mobilization.
    Annu Rev Plant Biol. 2008;59:115-42 PMID: 18444898
  15. Engineering plant oils as high-value industrial feedstocks for biorefining: the need for underpinning cell biology research.
    Physiol Plant. 2008 Jan;132(1):11-22 PMID: 18251866
  16. Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome.
    Am J Hum Genet. 2001 Nov;69(5):1002-12 PMID: 11590543
  17. The gregarious lipid droplet.
    J Biol Chem. 2008 Oct 17;283(42):28005-9 PMID: 18611863
  18. A rapid method of total lipid extraction and purification.
    Can J Biochem Physiol. 1959 Aug;37(8):911-7 PMID: 13671378
  19. Chanarin-Dorfman syndrome caused by a novel splice site mutation in ABHD5.
    Br J Dermatol. 2008 Jun;158(6):1378-80 PMID: 18410411
  20. N-acylphosphatidylethanolamine synthesis in plants: occurrence, molecular composition, and phospholipid origin.
    Arch Biochem Biophys. 1993 Feb 15;301(1):21-33 PMID: 8442663
  21. An adapter ligation-mediated PCR method for high-throughput mapping of T-DNA inserts in the Arabidopsis genome.
    Nat Protoc. 2007;2(11):2910-7 PMID: 18007627
  22. Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic.
    J Lipid Res. 2007 Apr;48(4):837-47 PMID: 17210984
  23. Analysis of interaction partners for perilipin and ADRP on lipid droplets.
    Mol Cell Biochem. 2006 Mar;284(1-2):167-73 PMID: 16532261
  24. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic.
    J Biol Chem. 2004 Jan 30;279(5):3787-92 PMID: 14597625
  25. Triglyceride containing lipid droplets and lipid droplet-associated proteins.
    Curr Opin Lipidol. 2008 Oct;19(5):441-7 PMID: 18769224
  26. Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12711-6 PMID: 11038591
  27. Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis beta-oxidation mutants.
    Plant Physiol. 2009 Aug;150(4):1981-9 PMID: 19561121
  28. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis.
    Plant J. 2004 Nov;40(4):575-85 PMID: 15500472
  29. Energy. Driving on biomass.
    Science. 2009 May 22;324(5930):1019-20 PMID: 19460990
  30. Rab-regulated membrane traffic between adiposomes and multiple endomembrane systems.
    Methods Enzymol. 2008;439:327-37 PMID: 18374175
  31. Lipid droplets: a classic organelle with new outfits.
    Histochem Cell Biol. 2008 Aug;130(2):263-79 PMID: 18546013
  32. Improved cytochemical method for detecting Jordans' bodies in neutral lipid storage diseases.
    J Clin Pathol. 2007 Aug;60(8):956-8 PMID: 17293389
  33. Chanarin-Dorfman syndrome: deficiency in CGI-58, a lipid droplet-bound coactivator of lipase.
    Biochim Biophys Acta. 2009 Jun;1791(6):519-23 PMID: 19061969
  34. Surface structure and properties of plant seed oil bodies.
    J Cell Biol. 1992 Apr;117(2):327-35 PMID: 1560029
  35. Identification and quantification of glycerolipids in cotton fibers: reconciliation with metabolic pathway predictions from DNA databases.
    Lipids. 2005 Aug;40(8):773-85 PMID: 16296396
  36. Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5.
    Am J Physiol Endocrinol Metab. 2009 Aug;297(2):E289-96 PMID: 19401457
  37. Engineering oilseeds for sustainable production of industrial and nutritional feedstocks: solving bottlenecks in fatty acid flux.
    Curr Opin Plant Biol. 2007 Jun;10(3):236-44 PMID: 17434788
  38. CGI-58 facilitates lipolysis on lipid droplets but is not involved in the vesiculation of lipid droplets caused by hormonal stimulation.
    J Lipid Res. 2007 May;48(5):1078-89 PMID: 17308334
  39. A role for lipid droplets in inter-membrane lipid traffic.
    Proteomics. 2009 Feb;9(4):914-21 PMID: 19160396
  40. At4g24160, a soluble acyl-coenzyme A-dependent lysophosphatidic acid acyltransferase.
    Plant Physiol. 2009 Oct;151(2):869-81 PMID: 19700561
  41. Mechanisms of lipid transport involved in organelle biogenesis in plant cells.
    Annu Rev Cell Dev Biol. 2009;25:71-91 PMID: 19572810
  42. The biogenesis and functions of lipid bodies in animals, plants and microorganisms.
    Prog Lipid Res. 2001 Sep;40(5):325-438 PMID: 11470496
  43. Neutral lipid storage disease: a possible functional defect in phospholipid- linked triacylglycerol metabolism.
    Biochim Biophys Acta. 1991 Feb 22;1096(2):162-9 PMID: 2001430
  44. Location, location: protein trafficking and lipolysis in adipocytes.
    Trends Endocrinol Metab. 2008 Jan;19(1):3-9 PMID: 18155916
  45. Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways.
    Plant Biotechnol J. 2009 Sep;7(7):694-703 PMID: 19702756
  46. CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome.
    J Biol Chem. 2004 Jul 16;279(29):30490-7 PMID: 15136565
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-10-12
Epub
2010-00-27
Pages
17833-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2955100
Subset
IM
Grants
NHLBI NIH HHS · P01 HL020948 · United States
NIGMS NIH HHS · R01 GM052016 · United States
NIGMS NIH HHS · GM-52016 · United States
NHLBI NIH HHS · HL-20948 · United States
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: [email protected]