Mathematical modeling of the central carbohydrate metabolism in Arabidopsis reveals a substantial regulatory influence of vacuolar invertase on whole plant carbon metabolism.

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  • Additional Information
    • Source:
      Publisher: American Society of Plant Biologists Country of Publication: United States NLM ID: 0401224 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1532-2548 (Electronic) Linking ISSN: 00320889 NLM ISO Abbreviation: Plant Physiol Subsets: MEDLINE
    • Publication Information:
      Publication: : [Rockville, MD] : American Society of Plant Biologists
      Original Publication: Lancaster, Pa., American Society of Plant Physiologists.
    • Subject Terms:
    • Abstract:
      A mathematical model representing metabolite interconversions in the central carbohydrate metabolism of Arabidopsis (Arabidopsis thaliana) was developed to simulate the diurnal dynamics of primary carbon metabolism in a photosynthetically active plant leaf. The model groups enzymatic steps of central carbohydrate metabolism into blocks of interconverting reactions that link easily measurable quantities like CO(2) exchange and quasi-steady-state levels of soluble sugars and starch. When metabolite levels that fluctuate over diurnal cycles are used as a basic condition for simulation, turnover rates for the interconverting reactions can be calculated that approximate measured metabolite dynamics and yield kinetic parameters of interconverting reactions. We used experimental data for Arabidopsis wild-type plants, accession Columbia, and a mutant defective in vacuolar invertase, AtbetaFruct4, as input data. Reducing invertase activity to mutant levels in the wild-type model led to a correct prediction of increased sucrose levels. However, additional changes were needed to correctly simulate levels of hexoses and sugar phosphates, indicating that invertase knockout causes subsequent changes in other enzymatic parameters. Reduction of invertase activity caused a decline in photosynthesis and export of reduced carbon to associated metabolic pathways and sink organs (e.g. roots), which is in agreement with the reported contribution of vacuolar invertase to sink strength. According to model parameters, there is a role for invertase in leaves, where futile cycling of sucrose appears to have a buffering effect on the pools of sucrose, hexoses, and sugar phosphates. Our data demonstrate that modeling complex metabolic pathways is a useful tool to study the significance of single enzyme activities in complex, nonintuitive networks.
    • References:
      Phytochemistry. 2007 Aug-Sep;68(16-18):2375-92. (PMID: 17555779)
      Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540. (PMID: 15012299)
      Planta. 1996;198(1):17-23. (PMID: 8580769)
      Plant Physiol. 1985 Sep;79(1):11-7. (PMID: 16664354)
      Bioinformatics. 2006 Feb 15;22(4):514-5. (PMID: 16317076)
      Mol Syst Biol. 2006;2:59. (PMID: 17102804)
      Phytochemistry. 2007 Mar;68(6):709-31. (PMID: 17234224)
      Plant Physiol. 1999 Sep;121(1):1-8. (PMID: 10482654)
      Curr Opin Microbiol. 2004 Oct;7(5):513-8. (PMID: 15451507)
      Eur J Biochem. 1988 Aug 15;175(3):661-72. (PMID: 3137030)
      J Exp Bot. 2004 May;55(400):1177-86. (PMID: 15073223)
      Plant Physiol. 1989 Oct;91(2):656-62. (PMID: 16667083)
      Plant J. 2004 Sep;39(6):847-62. (PMID: 15341628)
      Plant J. 1997 Sep;12(3):605-14. (PMID: 9351245)
      Plant Cell. 2004 Dec;16(12):3304-25. (PMID: 15548738)
      Plant Physiol. 1994 Oct;106(2):679-687. (PMID: 12232360)
      Trends Plant Sci. 2008 Apr;13(4):165-71. (PMID: 18329321)
      J Exp Bot. 2008;59(11):2969-77. (PMID: 18641398)
      Photosynth Res. 2006 Oct;90(1):45-66. (PMID: 17131095)
      Plant Physiol. 1999 Jan;119(1):267-76. (PMID: 9880369)
      FEBS Lett. 1999 Nov 12;461(1-2):13-8. (PMID: 10561488)
      Biotechnol Bioeng. 1997 Aug 20;55(4):592-608. (PMID: 18636570)
      Trends Plant Sci. 2004 Dec;9(12):606-13. (PMID: 15564128)
      Arch Biochem Biophys. 1989 May 1;270(2):681-90. (PMID: 2523212)
      Plant Physiol. 1983 Dec;73(4):989-94. (PMID: 16663357)
      Planta. 2005 Oct;222(2):386-95. (PMID: 16052318)
      Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:49-81. (PMID: 15012186)
      J Theor Biol. 2005 Jun 7;234(3):383-93. (PMID: 15784272)
      Photosynth Res. 2002;72(1):27-37. (PMID: 16228532)
      Biotechnol Bioeng. 1997 Jul 20;55(2):305-16. (PMID: 18636489)
      Funct Plant Biol. 2007 Jun;34(6):508-516. (PMID: 32689380)
      Arch Biochem Biophys. 1981 Nov;212(1):237-46. (PMID: 6272652)
      Plant Physiol. 1992 Aug;99(4):1275-8. (PMID: 16669032)
      EMBO J. 1994 Jan 1;13(1):1-7. (PMID: 8306952)
      Plant Cell. 1995 Mar;7(3):259-70. (PMID: 7734961)
      Science. 2003 Apr 11;300(5617):332-6. (PMID: 12690200)
      J Exp Bot. 2000 Feb;51 Spec No:319-28. (PMID: 10938839)
      Plant J. 2002 Apr;30(2):221-35. (PMID: 12000458)
      J Plant Physiol. 2008 Nov 28;165(17):1817-29. (PMID: 18430487)
      Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2994-9. (PMID: 16481625)
      Plant Physiol. 1992 Aug;99(4):1443-8. (PMID: 16669056)
    • Accession Number:
      0 (Arabidopsis Proteins)
      57-50-1 (Sucrose)
      7440-44-0 (Carbon)
      9005-25-8 (Starch)
      EC 3.2.1.26 (beta-Fructofuranosidase)
    • Publication Date:
      Date Created: 20100309 Date Completed: 20100825 Latest Revision: 20240317
    • Publication Date:
      20240317
    • Accession Number:
      PMC2862412
    • Accession Number:
      10.1104/pp.110.154443
    • Accession Number:
      20207708