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Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow.

ABSTRACT: An understanding of the balance between carbon and nitrogen assimilation in plants is key to future bioengineering for a range of applications. Metabolomic analysis of the model plant, Arabidopsis thaliana, using combined NMR-MS revealed the presence of two hemiterpenoid glycosides that accumulated in leaf tissue, to ~1% dry weight under repeated nitrate-deficient conditions. The formation of these isoprenoids was correlated with leaf nitrate concentrations that could also be assayed in the metabolomic data using a unique flavonoid-nitrate mass spectral adduct. Analysis of leaf and root tissue from plants grown in hydroponics with a variety of root stressors identified the conditions under which the isoprenoid pathway in leaves was diverted to the hemiterpenoids. These compounds were strongly induced by root wounding or oxidative stress and weakly induced by potassium deficiency. Other stresses such as cold, saline, and osmotic stress did not induce the compounds. Replacement of nitrate with ammonia failed to suppress the formation of the hemiterpenoids, indicating that nitrate sensing was a key factor. Feeding of intermediates was used to study aspects of 2-C-methyl-d-erythritol-4-phosphate pathway regulation leading to hemiterpenoid formation. The formation of the hemiterpenoids in leaves was strongly correlated with the induction of the phenylpropanoids scopolin and coniferin in roots of the same plants. These shunts of photosynthetic carbon flow are discussed in terms of overflow mechanisms that have some parallels with isoprene production in tree species.

SUBMITTER: Ward JL

PROVIDER: S-EPMC3127892 | biostudies-literature | 2011 Jun

REPOSITORIES: biostudies-literature

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Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow.

Ward Jane L JL Baker John M JM Llewellyn Aimee M AM Hawkins Nathaniel D ND Beale Michael H MH

Proceedings of the National Academy of Sciences of the United States of America 20110613 26

An understanding of the balance between carbon and nitrogen assimilation in plants is key to future bioengineering for a range of applications. Metabolomic analysis of the model plant, Arabidopsis thaliana, using combined NMR-MS revealed the presence of two hemiterpenoid glycosides that accumulated in leaf tissue, to ~1% dry weight under repeated nitrate-deficient conditions. The formation of these isoprenoids was correlated with leaf nitrate concentrations that could also be assayed in the meta ...[more]

PMID: 21670294

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Project description:BackgroundThe formation of acetate by fast-growing Escherichia coli (E. coli) is a commonly observed phenomenon, often referred to as overflow metabolism. Among various studies that have been carried over decades, a recent work (Basan, M. et al. Nature 528, 99-104, 2015) suggested and validated that it is the differential proteomic efficiencies in energy biogenesis between fermentation and respiration that lead to the production of acetate at rapid growth conditions, as the consequence of optimally allocating the limited proteomic resource. In the current work, we attempt to incorporate this newly developed proteome allocation theory into flux balance analysis (FBA) to capture quantitatively the extent of overflow metabolism in different E. coli strains.ResultsA concise constraint was introduced into a FBA-based model with three proteomic cost parameters to represent constrained allocation of proteome over two energy (respiration and fermentation) pathways and biomass synthesis. Linear relationships were shown to exist between the three proteomic cost parameters. Tests with three different strains revealed that the proteomic cost of fermentation was consistently lower than that of respiration. A slow-growing strain appeared to have a higher proteomic cost for biomass synthesis than fast-growing strains. Different assumed levels of carbon flowing into pentose phosphate pathway affected the absolute value of model parameters, but had no qualitative impact on the comparative proteomic costs. For the prediction of biomass yield, significant errors that occurred for one of the tested strains (ML308) were rectified by adjusting the cellular energy demand according to literature data.ConclusionsWith the aid of a concise proteome allocation constraint, our FBA-based model is able to quantitatively predict the onset and extent of the overflow metabolism in various E. coli strains. Such prediction is enabled by three linearly-correlated (as opposed to uniquely determinable) proteomic cost parameters. The linear relationships between these parameters, when determined using data from cell culturing experiments, render biologically meaningful comparative proteomic costs between fermentation and respiration pathways and between the biomass synthesis sectors of slow- and fast-growing species. Simultaneous prediction of acetate production and biomass yield in the overflow region requires the use of reliable cellular energy demand data.

Dataset Information

Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow.

Publications

Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow.

Similar Datasets

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