title: Model-assisted analysis of sugar metabolism throughout tomato fruit development reveals enzyme and carrier properties in relation to vacuole expansion.
abstract: 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 <5% of their maximal catalytic capacity. One of the major findings with the model was the high accumulation of soluble sugars within the vacuole together with organic acids, thus enabling the osmotic-driven vacuole expansion that was found during cell division.
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France Université de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France. bbeauvoi@bordeaux.inra.fr.
authors.forename: Bertrand P
authors.initials: BP
authors.lastname: Beauvoit
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Sophie
authors.initials: S
authors.lastname: Colombié
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Antoine
authors.initials: A
authors.lastname: Monier
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Marie-Hélène
authors.initials: MH
authors.lastname: Andrieu
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Benoit
authors.initials: B
authors.lastname: Biais
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Camille
authors.initials: C
authors.lastname: Bénard
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France Université de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France. Université de Bordeaux, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France CNRS, Bordeaux Imaging Center, UMS 3420, F-33000 Bordeaux, France INSERM, Bordeaux Imaging Center, US 004, F-33000 Bordeaux, France.
authors.forename: Catherine
authors.initials: C
authors.lastname: Chéniclet
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France Université de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France.
authors.forename: Martine
authors.initials: M
authors.lastname: Dieuaide-Noubhani
authors.affiliation: Institut de Mathématiques de Bordeaux, ENSTBB-Institut Polytechnique de Bordeaux, F-33600 Pessac, France.
authors.forename: Christine
authors.initials: C
authors.lastname: Nazaret
authors.affiliation: Université de Bordeaux, 146 rue Léo-Saignat, F-33076 Bordeaux Cedex, France. IBGC-CNRS, UMR 5095, 33077 Bordeaux Cedex, France.
authors.forename: Jean-Pierre
authors.initials: JP
authors.lastname: Mazat
authors.affiliation: INRA, UMR 1332 Biologie du Fruit et Pathology, F33883 Villenave d'Ornon Cedex, France.
authors.forename: Yves
authors.initials: Y
authors.lastname: Gibon
mesh_terms: D001692:Biological Transport; D050260:Carbohydrate Metabolism; D002352:Carrier Proteins / Q000378:metabolism; D002455:Cell Division; D005638:Fruit / Q000201:enzymology / Q000254:growth & development / Q000378:metabolism; D005941:Glucokinase / Q000037:antagonists & inhibitors / Q000378:metabolism; D005964:Glucosyltransferases / Q000378:metabolism / Q000502:physiology; D007700:Kinetics; D018551:Solanum lycopersicum / Q000201:enzymology / Q000254:growth & development / Q000378:metabolism*; D008954:Models, Biological; D009997:Osmotic Pressure; D010940:Plant Proteins / Q000037:antagonists & inhibitors / Q000378:metabolism; D030821:Plants, Genetically Modified / Q000378:metabolism; D013395:Sucrose / Q000378:metabolism; D014617:Vacuoles / Q000378:metabolism / Q000502:physiology; D043324:beta-Fructofuranosidase / Q000037:antagonists & inhibitors / Q000378:metabolism
chemical_list: D002352:Carrier Proteins; D010940:Plant Proteins; D013395:Sucrose; D005964:Glucosyltransferases; C022699:sucrose synthase; D005941:Glucokinase; D043324:beta-Fructofuranosidase