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PMID: 17449810 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis.

The Plant cell ·Vol. 19 ·No. 4 ·2007-04-00 ·Pages 1376-87

Eastmond PJ

Abstract

Hydrogen peroxide is a major by-product of peroxisomal metabolism and has the potential to cause critical oxidative damage. In all eukaryotes, catalase is thought to be instrumental in removing this H(2)O(2). However, plants also contain a peroxisomal membrane-associated ascorbate-dependent electron transfer system, using ascorbate peroxidase and monodehydroascorbate reductase (MDAR). Here, I report that the conditional seedling-lethal sugar-dependent2 mutant of Arabidopsis thaliana is deficient in the peroxisomal membrane isoform of MDAR (MDAR4). Following germination, Arabidopsis seeds rely on storage oil breakdown to supply carbon skeletons and energy for early seedling growth, and massive amounts of H(2)O(2) are generated within the peroxisome as a by-product of fatty acid beta-oxidation. My data suggest that the membrane-bound MDAR4 component of the ascorbate-dependent electron transfer system is necessary to detoxify H(2)O(2), which escapes the peroxisome. This function appears to be critical to protect oil bodies that are in close proximity to peroxisomes from incurring oxidative damage, which otherwise inactivates the triacylglycerol lipase SUGAR-DEPENDENT1 and cuts off the supply of carbon for seedling establishment.

MeSH Terms
Arabidopsis/growth & development,ultrastructure Arabidopsis Proteins/metabolism Germination Hydrolysis Molecular Sequence Data NADH, NADPH Oxidoreductases/metabolism Organelles/enzymology,ultrastructure Plant Oils/metabolism Seeds/physiology
Chemicals
Arabidopsis Proteins Plant Oils NADH, NADPH Oxidoreductases monodehydroascorbate reductase 4, Arabidopsis monodehydroascorbate reductase (NADH)
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Eastmond Peter J
Warwick HRI, University of Warwick, Wellesbourne, Warwickshire, CV35 9EF, UK. [email protected]
References (59)
59 references, click to expand
  1. Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination.
    Plant Cell. 2004 Jun;16(6):1419-32 PMID: 15155886
  2. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 PMID: 10737809
  3. Metal-catalyzed oxidation induces carbonylation of peroxisomal proteins and loss of enzymatic activities.
    Arch Biochem Biophys. 2005 Jul 1;439(1):25-31 PMID: 15922287
  4. Heterologous expression of cDNAs encoding monodehydroascorbate reductases from the moss, Physcomitrella patens and characterization of the expressed enzymes.
    Planta. 2007 Mar;225(4):945-54 PMID: 16983536
  5. Cloning and characterization of the acid lipase from castor beans.
    J Biol Chem. 2004 Oct 29;279(44):45540-5 PMID: 15322116
  6. An intimate collaboration between peroxisomes and lipid bodies.
    J Cell Biol. 2006 Jun 5;173(5):719-31 PMID: 16735577
  7. Mutants of Arabidopsis with alterations in seed lipid fatty acid composition.
    Theor Appl Genet. 1990 Aug;80(2):234-40 PMID: 24220901
  8. Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue.
    Anal Biochem. 1986 Jan;152(1):141-5 PMID: 3954036
  9. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  10. 2,4-Dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid beta-oxidation.
    Plant Cell. 1998 Feb;10(2):183-95 PMID: 9490742
  11. Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5669-74 PMID: 10805817
  12. The Arabidopsis thaliana multifunctional protein gene (MFP2) of peroxisomal beta-oxidation is essential for seedling establishment.
    Plant J. 2006 Mar;45(6):930-41 PMID: 16507084
  13. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta-oxidation.
    Plant Physiol. 2001 Nov;127(3):1266-78 PMID: 11706205
  14. Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana.
    Plant Cell. 2004 Feb;16(2):394-405 PMID: 14742880
  15. Acquisition of membrane lipids by differentiating glyoxysomes: role of lipid bodies.
    J Cell Biol. 1991 Nov;115(4):995-1007 PMID: 1955468
  16. A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin.
    Plant Cell Physiol. 1995 Sep;36(6):1157-62 PMID: 8528608
  17. Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes.
    Plant Physiol. 1996 Feb;110(2):589-98 PMID: 8742335
  18. The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions.
    EMBO J. 1995 Jul 17;14(14):3480-6 PMID: 7628449
  19. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  20. Novel peroxisome clustering mutants and peroxisome biogenesis mutants of Saccharomyces cerevisiae.
    J Cell Biol. 1993 Dec;123(5):1133-47 PMID: 7902359
  21. The isolation and characterisation of a catalase-deficient mutant of barley (Hordeum vulgare L.).
    Planta. 1983 Dec;159(6):505-11 PMID: 24258326
  22. Direct interaction between glyoxysomes and lipid bodies in cotyledons of the Arabidopsis thaliana ped1 mutant.
    Protoplasma. 2001;218(1-2):83-94 PMID: 11732324
  23. Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant.
    J Exp Bot. 2005 Dec;56(422):3041-9 PMID: 16263910
  24. Biochemistry of peroxisomes.
    Annu Rev Biochem. 1992;61:157-97 PMID: 1353950
  25. Membranous appendices of spherosomes (oleosomes) : Possible role in fat utilization in germinating oil seeds.
    Planta. 1978 Jan;140(2):163-9 PMID: 24414473
  26. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana.
    Plant J. 2004 Jul;39(1):45-58 PMID: 15200641
  27. Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells.
    Plant Physiol. 2003 Jun;132(2):870-82 PMID: 12805617
  28. Sensitive and real-time determination of H2O2 release from intact peroxisomes.
    Biochem J. 2002 May 1;363(Pt 3):483-91 PMID: 11964148
  29. Arabidopsis map-based cloning in the post-genome era.
    Plant Physiol. 2002 Jun;129(2):440-50 PMID: 12068090
  30. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis.
    Genomics. 1994 Jan 1;19(1):137-44 PMID: 8188214
  31. The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development.
    J Exp Bot. 2006;57(12):3033-42 PMID: 16873450
  32. Determination of carbonyl content in oxidatively modified proteins.
    Methods Enzymol. 1990;186:464-78 PMID: 1978225
  33. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels.
    Plant J. 1997 May;11(5):993-1005 PMID: 9193071
  34. A protective association between catalase and isocitrate lyase in peroxisomes.
    Arch Biochem Biophys. 2005 Mar 15;435(2):243-52 PMID: 15708367
  35. Chewing the fat: beta-oxidation in signalling and development.
    Trends Plant Sci. 2006 Mar;11(3):124-32 PMID: 16490379
  36. Reduction of phenoxyl radicals mediated by monodehydroascorbate reductase.
    Biochem Biophys Res Commun. 2000 Dec 29;279(3):949-54 PMID: 11162455
  37. Lipid hydroperoxide levels in plant tissues.
    J Exp Bot. 2000 Aug;51(349):1363-70 PMID: 10944149
  38. Evidence for the Presence of the Ascorbate-Glutathione Cycle in Mitochondria and Peroxisomes of Pea Leaves.
    Plant Physiol. 1997 May;114(1):275-284 PMID: 12223704
  39. Patterns of protein oxidation in Arabidopsis seeds and during germination.
    Plant Physiol. 2005 Jun;138(2):790-802 PMID: 15908592
  40. Ascorbate free-radical reduction by glyoxysomal membranes.
    Plant Physiol. 1990 Oct;94(2):531-7 PMID: 16667745
  41. Biochemistry of peroxisomes in health and disease.
    Mol Cell Biochem. 1997 Feb;167(1-2):1-29 PMID: 9059978
  42. The role of metabolism in the antioxidant function of vitamin E.
    Crit Rev Toxicol. 1993;23(2):147-69 PMID: 8329114
  43. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers.
    Plant J. 1993 Aug;4(2):403-10 PMID: 8106085
  44. Oxidation of NADH in Glyoxysomes by a Malate-Aspartate Shuttle.
    Plant Physiol. 1980 Oct;66(4):555-60 PMID: 16661476
  45. Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle.
    Plant J. 2007 May;50(3):381-90 PMID: 17376163
  46. SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds.
    Plant Cell. 2006 Mar;18(3):665-75 PMID: 16473965
  47. A simple procedure for the analysis of single nucleotide polymorphisms facilitates map-based cloning in Arabidopsis.
    Plant Physiol. 2000 Dec;124(4):1483-92 PMID: 11115864
  48. Abnormality in catalase import into peroxisomes leads to severe neurological disorder.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2961-6 PMID: 9501198
  49. Peroxisomal catalase in the methylotrophic yeast Candida boidinii: transport efficiency and metabolic significance.
    J Bacteriol. 2001 Nov;183(21):6372-83 PMID: 11591682
  50. Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation.
    J Cell Sci. 2006 May 1;119(Pt 9):1961-72 PMID: 16636080
  51. Pathways of straight and branched chain fatty acid catabolism in higher plants.
    Prog Lipid Res. 2002 Mar;41(2):156-81 PMID: 11755682
  52. The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts.
    Plant Cell Physiol. 2002 Jul;43(7):697-705 PMID: 12154132
  53. Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress.
    Plant Cell Physiol. 1999 Jul;40(7):725-32 PMID: 10501032
  54. Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase.
    Plant J. 2005 Sep;43(6):900-14 PMID: 16146528
  55. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  56. Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis.
    Plant Physiol Biochem. 2005 Sep;43(9):828-35 PMID: 16289945
  57. Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes.
    Arch Biochem Biophys. 2005 Feb 15;434(2):248-57 PMID: 15639224
  58. Promoter trapping of a novel medium-chain acyl-CoA oxidase, which is induced transcriptionally during Arabidopsis seed germination.
    J Biol Chem. 2000 Nov 3;275(44):34375-81 PMID: 10918060
  59. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants.
    EMBO J. 1997 Aug 15;16(16):4806-16 PMID: 9305623
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2007-04-00
Epub
2007-00-20
Pages
1376-87
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1913749
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/H/00PE0274 · United Kingdom
Biotechnology and Biological Sciences Research Council · JF16985 · United Kingdom
Databases
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AY039980
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