The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a flexible balance between the cytosolic and plastidic contributions to carbohydrate oxidation in response to phosphate limitation

Shyam Masakapalli, Fiona M. Bryant, Nicholas J. Kruger, R. George Ratcliffe

Research output: Contribution to journalArticlepeer-review

34 Citations (Scopus)

Abstract

Understanding the mechanisms that allow plants to respond to variable and reduced availability of inorganic phosphate is of increasing agricultural importance because of the continuing depletion of the rock phosphate reserves that are used to combat inadequate phosphate levels in the soil. Changes in gene expression, protein levels, enzyme activities and metabolite levels all point to a reconfiguration of the central metabolic network in response to reduced availability of inorganic phosphate, but the metabolic significance of these changes can only be assessed in terms of the fluxes supported by the network. Steady-state metabolic flux analysis was used to define the metabolic phenotype of a heterotrophic Arabidopsis thaliana cell culture grown on a Murashige and Skoog medium containing 0, 1.25 or 5 mm inorganic phosphate. Fluxes through the central metabolic network were deduced from the redistribution of 13C into metabolic intermediates and end products when cells were labelled with [1-13C], [2-13C], or [13C6]glucose, in combination with 14C measurements of the rates of biomass accumulation. Analysis of the flux maps showed that reduced levels of phosphate in the growth medium stimulated flux through phosphoenolpyruvate carboxylase and malic enzyme, altered the balance between cytosolic and plastidic carbohydrate oxidation in favour of the plastid, and increased cell maintenance costs. We argue that plant cells respond to phosphate deprivation by reconfiguring the flux distribution through the pathways of carbohydrate oxidation to take advantage of better phosphate homeostasis in the plastid.

Original languageEnglish
Pages (from-to)964-977
Number of pages14
JournalThe Plant Journal
Volume78
Issue number6
DOIs
Publication statusPublished - 2014

Keywords

  • Arabidopsis thaliana
  • carbon conversion efficiency
  • heterotrophic metabolism
  • metabolic flux analysis
  • phosphate availability
  • phosphate stress
  • Pi homeostasis
  • plastid metabolism
  • pyruvate kinase
  • subcellular compartmentation

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology
  • Genetics
  • Medicine(all)

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