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Effects of varying nitrogen sources on amino acid synthesis costs in Arabidopsis thaliana under different light and carbon-source conditions.

Arnold A, Sajitz-Hermstein M, Nikoloski Z - PLoS ONE (2015)

Bottom Line: Our results identify nitrogen supply as a key determinant of amino acid costs, in agreement with experimental evidence.In addition, the association of the determined costs with experimentally observed growth patterns suggests that metabolite synthesis costs are involved in shaping regulation of plant growth.Finally, we find that simultaneous uptake of both nitrogen sources can lead to efficient utilization of energy source, which may be the result of evolutionary optimization.

View Article: PubMed Central - PubMed

Affiliation: Computational Systems Biology, School of Engineering and Science, Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany; Systems Biology and Mathematical Modeling Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany.

ABSTRACT
Plants as sessile organisms cannot escape their environment and have to adapt to any changes in the availability of sunlight and nutrients. The quantification of synthesis costs of metabolites, in terms of consumed energy, is a prerequisite to understand trade-offs arising from energetic limitations. Here, we examine the energy consumption of amino acid synthesis in Arabidopsis thaliana. To quantify these costs in terms of the energy equivalent ATP, we introduce an improved cost measure based on flux balance analysis and apply it to three state-of-the-art metabolic reconstructions to ensure robust results. We present the first systematic in silico analysis of the effect of nitrogen supply (nitrate/ammonium) on individual amino acid synthesis costs as well as of the effect of photoautotrophic and heterotrophic growth conditions, integrating day/night-specific regulation. Our results identify nitrogen supply as a key determinant of amino acid costs, in agreement with experimental evidence. In addition, the association of the determined costs with experimentally observed growth patterns suggests that metabolite synthesis costs are involved in shaping regulation of plant growth. Finally, we find that simultaneous uptake of both nitrogen sources can lead to efficient utilization of energy source, which may be the result of evolutionary optimization.

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Schematic representation of the dependency of costs on the different investigated scenarios.Shown are the trends of amino acid synthesis costs for autotrophic and heterotrophic day (AD and HD) as well as night (N). The gradient represents the costs trend whereby lighter gray implies lower costs.
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pone.0116536.g004: Schematic representation of the dependency of costs on the different investigated scenarios.Shown are the trends of amino acid synthesis costs for autotrophic and heterotrophic day (AD and HD) as well as night (N). The gradient represents the costs trend whereby lighter gray implies lower costs.

Mentions: The majority of amino acid costs for night conditions are higher than those for heterotrophic day conditions. In addition, the costs for heterotrophic day conditions are distinctly exceeded by the costs for autotrophic conditions. While amino acid synthesis costs were systematically affected by the alternation of day and night, as well as of the trophic level (Fig. 4), positing hypotheses about resource reallocation in plants based on comparison of these costs warrants caution. The impact of metabolite synthesis costs in terms of energy depends on the availability of the respective resources (e.g., light intensity or on the amount of sugar storage): a limitation of resource availability imposes constraints on the energy budget. The effect of metabolite synthesis costs then depends on their ratio to the energy budget. Consequently, an environmental shift accompanied with a change in resource limitation may not only alter the metabolite synthesis costs but also the cellular energy budget and, hence, the effect of costs. The shift of the total energetic budget may then have important implications on resource reallocations.


Effects of varying nitrogen sources on amino acid synthesis costs in Arabidopsis thaliana under different light and carbon-source conditions.

Arnold A, Sajitz-Hermstein M, Nikoloski Z - PLoS ONE (2015)

Schematic representation of the dependency of costs on the different investigated scenarios.Shown are the trends of amino acid synthesis costs for autotrophic and heterotrophic day (AD and HD) as well as night (N). The gradient represents the costs trend whereby lighter gray implies lower costs.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4338252&req=5

pone.0116536.g004: Schematic representation of the dependency of costs on the different investigated scenarios.Shown are the trends of amino acid synthesis costs for autotrophic and heterotrophic day (AD and HD) as well as night (N). The gradient represents the costs trend whereby lighter gray implies lower costs.
Mentions: The majority of amino acid costs for night conditions are higher than those for heterotrophic day conditions. In addition, the costs for heterotrophic day conditions are distinctly exceeded by the costs for autotrophic conditions. While amino acid synthesis costs were systematically affected by the alternation of day and night, as well as of the trophic level (Fig. 4), positing hypotheses about resource reallocation in plants based on comparison of these costs warrants caution. The impact of metabolite synthesis costs in terms of energy depends on the availability of the respective resources (e.g., light intensity or on the amount of sugar storage): a limitation of resource availability imposes constraints on the energy budget. The effect of metabolite synthesis costs then depends on their ratio to the energy budget. Consequently, an environmental shift accompanied with a change in resource limitation may not only alter the metabolite synthesis costs but also the cellular energy budget and, hence, the effect of costs. The shift of the total energetic budget may then have important implications on resource reallocations.

Bottom Line: Our results identify nitrogen supply as a key determinant of amino acid costs, in agreement with experimental evidence.In addition, the association of the determined costs with experimentally observed growth patterns suggests that metabolite synthesis costs are involved in shaping regulation of plant growth.Finally, we find that simultaneous uptake of both nitrogen sources can lead to efficient utilization of energy source, which may be the result of evolutionary optimization.

View Article: PubMed Central - PubMed

Affiliation: Computational Systems Biology, School of Engineering and Science, Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany; Systems Biology and Mathematical Modeling Group, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany.

ABSTRACT
Plants as sessile organisms cannot escape their environment and have to adapt to any changes in the availability of sunlight and nutrients. The quantification of synthesis costs of metabolites, in terms of consumed energy, is a prerequisite to understand trade-offs arising from energetic limitations. Here, we examine the energy consumption of amino acid synthesis in Arabidopsis thaliana. To quantify these costs in terms of the energy equivalent ATP, we introduce an improved cost measure based on flux balance analysis and apply it to three state-of-the-art metabolic reconstructions to ensure robust results. We present the first systematic in silico analysis of the effect of nitrogen supply (nitrate/ammonium) on individual amino acid synthesis costs as well as of the effect of photoautotrophic and heterotrophic growth conditions, integrating day/night-specific regulation. Our results identify nitrogen supply as a key determinant of amino acid costs, in agreement with experimental evidence. In addition, the association of the determined costs with experimentally observed growth patterns suggests that metabolite synthesis costs are involved in shaping regulation of plant growth. Finally, we find that simultaneous uptake of both nitrogen sources can lead to efficient utilization of energy source, which may be the result of evolutionary optimization.

Show MeSH
Related in: MedlinePlus