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LARGE-SCALE BIOLOGY ARTICLE
Model-Assisted Analysis of Sugar Metabolism throughout Tomato Fruit Development Reveals Enzyme and Carrier Properties in Relation to Vacuole Expansion W
Bertrand P. Beauvoit,a,b,1 Sophie Colombié,a Antoine Monier,a Marie-Hélène Andrieu,a Benoit Biais,a Camille Bénard,a Catherine Chéniclet,a,b,c,d,e Martine Dieuaide-Noubhani,a,b Christine Nazaret,f Jean-Pierre Mazat,b,g and Yves Gibona a INRA,
UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d’Ornon Cedex, France de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France. c Université de Bordeaux, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France d CNRS, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France e INSERM, Bordeaux Imaging Center, US 004, F-33000 Bordeaux, France f Institut de Mathématiques de Bordeaux, ENSTBB-Institut Polytechnique de Bordeaux, F-33600 Pessac, France g IBGC-CNRS, UMR 5095, 33077 Bordeaux Cedex, France b Université
A kinetic model combining enzyme activity measurements and subcellular compartmentation was parameterized to fit the sucrose, hexose, and glucose-6-P contents of pericarp throughout tomato (Solanum lycopersicum) fruit development. The model was further validated using independent data obtained from domesticated and wild tomato species and on transgenic lines. A hierarchical clustering analysis of the calculated fluxes and enzyme capacities together revealed stage-dependent features. Cell division was characterized by a high sucrolytic activity of the vacuole, whereas sucrose cleavage during expansion was sustained by both sucrose synthase and neutral invertase, associated with minimal futile cycling. Most importantly, a tight correlation between flux rate and enzyme capacity was found for fructokinase and PPi-dependent phosphofructokinase during cell division and for sucrose synthase, UDP-glucopyrophosphorylase, and phosphoglucomutase during expansion, thus suggesting an adaptation of enzyme abundance to metabolic needs. In contrast, for most enzymes, flux rates varied irrespectively of enzyme capacities, and most enzymes functioned at
LARGE-SCALE BIOLOGY ARTICLE
Model-Assisted Analysis of Sugar Metabolism throughout Tomato Fruit Development Reveals Enzyme and Carrier Properties in Relation to Vacuole Expansion W
Bertrand P. Beauvoit,a,b,1 Sophie Colombié,a Antoine Monier,a Marie-Hélène Andrieu,a Benoit Biais,a Camille Bénard,a Catherine Chéniclet,a,b,c,d,e Martine Dieuaide-Noubhani,a,b Christine Nazaret,f Jean-Pierre Mazat,b,g and Yves Gibona a INRA,
UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d’Ornon Cedex, France de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France. c Université de Bordeaux, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France d CNRS, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France e INSERM, Bordeaux Imaging Center, US 004, F-33000 Bordeaux, France f Institut de Mathématiques de Bordeaux, ENSTBB-Institut Polytechnique de Bordeaux, F-33600 Pessac, France g IBGC-CNRS, UMR 5095, 33077 Bordeaux Cedex, France b Université
A kinetic model combining enzyme activity measurements and subcellular compartmentation was parameterized to fit the sucrose, hexose, and glucose-6-P contents of pericarp throughout tomato (Solanum lycopersicum) fruit development. The model was further validated using independent data obtained from domesticated and wild tomato species and on transgenic lines. A hierarchical clustering analysis of the calculated fluxes and enzyme capacities together revealed stage-dependent features. Cell division was characterized by a high sucrolytic activity of the vacuole, whereas sucrose cleavage during expansion was sustained by both sucrose synthase and neutral invertase, associated with minimal futile cycling. Most importantly, a tight correlation between flux rate and enzyme capacity was found for fructokinase and PPi-dependent phosphofructokinase during cell division and for sucrose synthase, UDP-glucopyrophosphorylase, and phosphoglucomutase during expansion, thus suggesting an adaptation of enzyme abundance to metabolic needs. In contrast, for most enzymes, flux rates varied irrespectively of enzyme capacities, and most enzymes functioned at
