Modelling central metabolic fluxes by constraint‐based optimization reveals metabolic reprogramming of developing Solanum lycopersicum (tomato) fruit

• Published in: The Plant journal : for cell and molecular biology 2015-01, Vol.81 (1), p.24-39
• Main Authors: Colombié, Sophie, Nazaret, Christine, Bénard, Camille, Biais, Benoît, Mengin, Virginie, Solé, Marion, Fouillen, Laëtitia, Dieuaide‐Noubhani, Martine, Mazat, Jean‐Pierre, Beauvoit, Bertrand, Gibon, Yves
• Format: Article
• Language: English
• Subjects: adenosine triphosphate; Adenosine Triphosphate - metabolism; Behavior; Biomass; carbon; Carbon - metabolism; Carbon dioxide; central metabolism; constraint‐based analysis; energy; Energy Metabolism; flux balance analysis; Fruit - chemistry; Fruit - growth & development; Fruit - metabolism; fruiting; Fruits; Glycolysis; Life Sciences; Lycopersicon esculentum - chemistry; Lycopersicon esculentum - growth & development; Lycopersicon esculentum - metabolism; Mathematics; Metabolic Networks and Pathways; Metabolism; Metabolites; modelling; Models, Biological; nitrogen; Nitrogen - metabolism; Optimization; Original; pentose phosphate cycle; Pentose Phosphate Pathway; pericarp; plant organs; ripening; Solanum lycopersicum; systems biology; Tomatoes
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.12685

Modelling of metabolic networks is a powerful tool to analyse the behaviour of developing plant organs, including fruits. Guided by our current understanding of heterotrophic metabolism of plant cells, a medium‐scale stoichiometric model, including the balance of co–factors and energy, was constructed in order to describe metabolic shifts that occur through the nine sequential stages of Solanum lycopersicum (tomato) fruit development. The measured concentrations of the main biomass components and the accumulated metabolites in the pericarp, determined at each stage, were fitted in order to calculate, by derivation, the corresponding external fluxes. They were used as constraints to solve the model by minimizing the internal fluxes. The distribution of the calculated fluxes of central metabolism were then analysed and compared with known metabolic behaviours. For instance, the partition of the main metabolic pathways (glycolysis, pentose phosphate pathway, etc.) was relevant throughout fruit development. We also predicted a valid import of carbon and nitrogen by the fruit, as well as a consistent CO₂release. Interestingly, the energetic balance indicates that excess ATP is dissipated just before the onset of ripening, supporting the concept of the climacteric crisis. Finally, the apparent contradiction between calculated fluxes with low values compared with measured enzyme capacities suggest a complex reprogramming of the metabolic machinery during fruit development. With a powerful set of experimental data and an accurate definition of the metabolic system, this work provides important insight into the metabolic and physiological requirements of the developing tomato fruits.