Home LiteratureArticle Details
PMID: 12692343 Published · ppublish English Journal Article

The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment.

Plant physiology ·Vol. 131 ·No. 4 ·2003-04-00 ·Pages 1834-42

Rylott EL, Gilday AD, Graham IA

Abstract

Phosphoenolpyruvate carboxykinase (PEPCK) catalyzes the conversion of oxaloacetate to phosphoenolpyruvate in the gluconeogenic production of sugars from storage oil in germinating oilseeds. Here, we present the results of analysis on PEPCK antisense Arabidopsis plants with a range of enzyme activities from 20% to 80% of wild-type levels. There is a direct correlation between enzyme activity and seedling establishment during early post-germinative growth, thus demonstrating the absolute requirement of PEPCK and gluconeogenesis in this process. Soluble sugar levels in the 35S-PCK1 antisense seedlings are reduced and seedling establishment can be rescued with an exogenous supply of sucrose. We observed an increase in the respiration of acetyl coenzyme A units released from fatty acid beta-oxidation and a corresponding decrease in the production of sugars with decreasing enzyme activity in 2-d-old antisense seedlings. The 35S-PCK1 antisense lines have a more extreme phenotype when compared with Arabidopsis mutants disrupted in the glyoxylate cycle. We conclude that the 35S-PCK1 antisense seedlings are compromised in the ability to use both storage lipid and storage protein through gluconeogenesis to produce soluble sugars.

MeSH Terms
Acetates/metabolism Arabidopsis/enzymology,genetics,growth & development,metabolism Carbohydrate Metabolism Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Phenotype Phosphoenolpyruvate Carboxykinase (ATP)/genetics,metabolism RNA, Messenger/genetics,metabolism Seedlings/enzymology,genetics,growth & development,metabolism
Chemicals
Acetates RNA, Messenger Phosphoenolpyruvate Carboxykinase (ATP)
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Rylott Elizabeth L
Centre for Novel Agricultural Products, Department of Biology (Area 7), University of York, P.O. Box 373, United Kingdom.
Gilday Alison D
Graham Ian A
References (38)
38 references, click to expand
  1. Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon:nitrogen availability.
    Plant Physiol. 2002 Feb;128(2):472-81 PMID: 11842151
  2. Molecular cloning of cucumber phosphoenolpyruvate carboxykinase and developmental regulation of gene expression.
    Plant Mol Biol. 1994 Oct;26(1):423-34 PMID: 7948888
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Mutants of Arabidopsis with alterations in seed lipid fatty acid composition.
    Theor Appl Genet. 1990 Aug;80(2):234-40 PMID: 24220901
  5. 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
  6. 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
  7. 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
  8. Germination and storage reserve mobilization are regulated independently in Arabidopsis.
    Plant J. 2002 Sep;31(5):639-47 PMID: 12207653
  9. The carboxylation of phosphoenolpyruvate and pyruvate. I. The active species of "CO2" utilized by phosphoenolpyruvate carboxykinase, carboxytransphosphorylase, and pyruvate carboxylase.
    J Biol Chem. 1968 Jul 25;243(14):3857-63 PMID: 5661712
  10. Distinct cis-acting elements direct the germination and sugar responses of the cucumber malate synthase gene.
    Mol Gen Genet. 1996 Feb 5;250(2):153-61 PMID: 8628214
  11. Carbon Dioxide Fixation into Oxalacetate in Higher Plants.
    Plant Physiol. 1957 Nov;32(6):591-600 PMID: 16655053
  12. Co-ordinate regulation of genes involved in storage lipid mobilization in Arabidopsis thaliana.
    Biochem Soc Trans. 2001 May;29(Pt 2):283-7 PMID: 11356168
  13. Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L.
    Plant Cell. 1989 Mar;1(3):293-300 PMID: 2535504
  14. Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds.
    Biochem J. 1996 Aug 1;317 ( Pt 3):653-8 PMID: 8760346
  15. Gluconeogenesis from amino acids in germinating castor bean endosperm and its role in transport to the embryo.
    Plant Physiol. 1967 Nov;42(11):1587-95 PMID: 16656694
  16. Re-examining the role of the glyoxylate cycle in oilseeds.
    Trends Plant Sci. 2001 Feb;6(2):72-8 PMID: 11173291
  17. Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development
    Planta. 1999 Nov;210(1):9-18 PMID: 10592027
  18. Identification of the regulatory steps in gluconeogenesis in cotyledons of Cucurbita pepo.
    Biochim Biophys Acta. 1978 Aug 3;542(1):1-11 PMID: 208645
  19. Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana.
    Plant J. 2000 Sep;23(6):759-70 PMID: 10998187
  20. Binary Agrobacterium vectors for plant transformation.
    Nucleic Acids Res. 1984 Nov 26;12(22):8711-21 PMID: 6095209
  21. A mechanism of conversion of fat to carbohydrate in castor beans.
    Nature. 1957 Jul 6;180(4575):35-6 PMID: 13451633
  22. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration.
    Methods Mol Biol. 1998;82:259-66 PMID: 9664431
  23. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants.
    Nature. 2002 Jan 24;415(6870):451-4 PMID: 11807559
  24. Phosphoenolpyruvate carboxykinase activity in grape berries.
    Plant Physiol. 1975 Jul;56(1):67-71 PMID: 16659259
  25. Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid beta-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings.
    Plant J. 2001 Oct;28(1):1-12 PMID: 11696182
  26. Apparent induction of key enzymes of the glyoxylic acid cycle in senescent barley leaves.
    Planta. 1988 Dec;176(4):548-50 PMID: 24220952
  27. PEP carboxykinase exchange reaction in photosynthetic bacteria.
    Plant Physiol. 1968 May;43(5):788-92 PMID: 5661493
  28. Ripening-related occurrence of phosphoenolpyruvate carboxykinase in tomato fruit.
    Plant Mol Biol. 2001 Nov;47(4):499-506 PMID: 11669575
  29. Phosphoenolpyruvate carboxykinase and gluconeogenesis in cotyledons of Cucurbita pepo.
    Biochim Biophys Acta. 1978 May 11;524(1):207-18 PMID: 656445
  30. ACX3, a novel medium-chain acyl-coenzyme A oxidase from Arabidopsis.
    Plant Physiol. 2000 Jun;123(2):733-42 PMID: 10859203
  31. Sucrose synthesis from acetate in the germinating castor bean: kinetics and pathway.
    J Biol Chem. 1961 Apr;236:988-95 PMID: 13690532
  32. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize
    Plant Physiol. 1999 Jun;120(2):539-46 PMID: 10364405
  33. Developmental regulation of expression of the malate synthase gene in transgenic plants.
    Plant Mol Biol. 1990 Oct;15(4):539-49 PMID: 2102373
  34. Using immunohistochemistry to study plant metabolism: the examples of its use in the localization of amino acids in plant tissues, and of phosphoenolpyruvate carboxykinase and its possible role in pH regulation.
    J Exp Bot. 2001 Apr;52(356):565-76 PMID: 11373305
  35. A rapeseed cold-inducible transcript encodes a phosphoenolpyruvate carboxykinase.
    Plant Physiol. 1995 Oct;109(2):611-8 PMID: 7480349
  36. Characterization of the 12S globulin complex of Brassica napus. Evolutionary relationship to other 11-12S storage globulins.
    Eur J Biochem. 1991 Mar 28;196(3):617-21 PMID: 2013284
  37. Does phosphoenolpyruvate carboxykinase have a role in both amino acid and carbohydrate metabolism?
    Amino Acids. 2001;20(3):225-41 PMID: 11354601
  38. Control of gluconeogenesis by isocitrate lyase in endosperm of germinating castor bean seedlings
    Plant J. 1999 Aug;19(4):423-31 PMID: 10504564
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2003-04-00
Pages
1834-42
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC166940
Subset
IM
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]