TY - JOUR

T1 - A hybrid kinetic and constraint-based model of leaf metabolism allows predictions of metabolic fluxes in different environments

AU - Shameer, S.

AU - Wang, Y.

AU - Bota, P.

AU - Ratcliffe, R.G.

AU - Long, S.P.

AU - Sweetlove, L.J.

PY - 2022/1/31

Y1 - 2022/1/31

N2 - While flux balance analysis (FBA) provides a framework for predicting steady-state leaf metabolic network fluxes, it does not readily capture the response to environmental variables without being coupled to other modelling formulations. To address this, we coupled an FBA model of 903 reactions of soybean (Glycine max) leaf metabolism with e-photosynthesis, a dynamic model that captures the kinetics of 126 reactions of photosynthesis and associated chloroplast carbon metabolism. Successful coupling was achieved in an iterative formulation in which fluxes from e-photosynthesis were used to constrain the FBA model and then, in turn, fluxes computed from the FBA model used to update parameters in e-photosynthesis. This process was repeated until common fluxes in the two models converged. Coupling did not hamper the ability of the kinetic module to accurately predict the carbon assimilation rate, photosystem II electron flux, and starch accumulation of field-grown soybean at two CO2 concentrations. The coupled model also allowed accurate predictions of additional parameters such as nocturnal respiration, as well as analysis of the effect of light intensity and elevated CO2 on leaf metabolism. Predictions included an unexpected decrease in the rate of export of sucrose from the leaf at high light, due to altered starch–sucrose partitioning, and altered daytime flux modes in the tricarboxylic acid cycle at elevated CO2. Mitochondrial fluxes were notably different between growing and mature leaves, with greater anaplerotic, tricarboxylic acid cycle and mitochondrial ATP synthase fluxes predicted in the former, primarily to provide carbon skeletons and energy for protein synthesis.  

AB - While flux balance analysis (FBA) provides a framework for predicting steady-state leaf metabolic network fluxes, it does not readily capture the response to environmental variables without being coupled to other modelling formulations. To address this, we coupled an FBA model of 903 reactions of soybean (Glycine max) leaf metabolism with e-photosynthesis, a dynamic model that captures the kinetics of 126 reactions of photosynthesis and associated chloroplast carbon metabolism. Successful coupling was achieved in an iterative formulation in which fluxes from e-photosynthesis were used to constrain the FBA model and then, in turn, fluxes computed from the FBA model used to update parameters in e-photosynthesis. This process was repeated until common fluxes in the two models converged. Coupling did not hamper the ability of the kinetic module to accurately predict the carbon assimilation rate, photosystem II electron flux, and starch accumulation of field-grown soybean at two CO2 concentrations. The coupled model also allowed accurate predictions of additional parameters such as nocturnal respiration, as well as analysis of the effect of light intensity and elevated CO2 on leaf metabolism. Predictions included an unexpected decrease in the rate of export of sucrose from the leaf at high light, due to altered starch–sucrose partitioning, and altered daytime flux modes in the tricarboxylic acid cycle at elevated CO2. Mitochondrial fluxes were notably different between growing and mature leaves, with greater anaplerotic, tricarboxylic acid cycle and mitochondrial ATP synthase fluxes predicted in the former, primarily to provide carbon skeletons and energy for protein synthesis.  

KW - central carbon metabolism

KW - flux balance analysis

KW - Glycine max

KW - kinetic modelling

KW - metabolic modelling

KW - technical advance

KW - Amino acids

KW - Biosynthesis

KW - Carbon

KW - Carbon dioxide

KW - Forecasting

KW - Kinetics

KW - Metabolism

KW - Starch

KW - Sugar (sucrose)

KW - Analysis models

KW - Central carbon metabolisms

KW - Elevated CO 2

KW - Flux balance analysis

KW - Kinetic models

KW - Kinetics-based model

KW - Metabolic modelling

KW - Technical advances

KW - Tricarboxylic acid cycle

KW - Photosynthesis

U2 - 10.1111/tpj.15551

DO - 10.1111/tpj.15551

M3 - Journal article

VL - 109

SP - 295

EP - 313

JO - The Plant Journal

JF - The Plant Journal

SN - 0960-7412

IS - 1

ER -