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.

Critical Roles of Vacuolar Invertase in Floral Organ Development and Male and Female Fertilities Are Revealed through Characterization of GhVIN1-RNAi Cotton Plants

“…Biochemically, VIN activity may regulate reproductive development by modulating cytoplasmic hexose levels and sugar signaling. Flux analysis and modeling of sugar metabolism in tomato pericarp indicate that VIN-catalyzed sucrolytic activity in the vacuole induces hexose efflux from the vacuole into cytoplasm, coupled with Suc influx during cell division of fruit development (Beauvoit et al, 2014). Thus, VINs are able to regulate not only vacuolar sugar homeostasis but also cytosolic hexose levels through coupling with the activities of tonoplast sugar transporters.…”

“…9). Pertinently, VIN is the major enzyme hydrolyzing Suc in tomato pericarp at the cell division stage (Beauvoit et al, 2014), when unloading occurs symplasmically (Palmer et al, 2015).…”

Metabolic model of central carbon and energy metabolisms of growing Arabidopsis thaliana in relation to sucrose translocation

“…Kinetic modelling of plant metabolism was used to unravel local and global system features, such as flux and concentration control coefficients and regulation patterns [44] in relation to different external or internal states, stimuli and conditions [31]. A kinetic model of sugar metabolism throughout tomato Solanum lycopersicum fruit development revealed importance of different enzymes on different development stages, as well as importance of sugar accumulation in vacuole together with organic acids to enable osmotic-driven vacuole expansion during the cell division [45]. Also, different regulatory scenarios of starch turnover by the circadian clock through dynamic adjustment of starch turnover to changing environmental conditions were suggested based on mathematical modelling [4].…”

Modeling Sugar Metabolism in Tomato Fruit

“…Just like summer's best tomatoes in August (with all Model of carbohydrate metabolism in developing tomato fruit. For abbreviations, chemical reactions, rate equations, and kinetic parameters, see Beauvoit et al (2014). (Reprinted from Beauvoit et al [2014], Figure 2. …”

“…Such modeling has examined the effects of increasing atmospheric CO 2 and the fluxes of carbohydrate metabolism in sugarcane (Saccharum officinarum) stem parenchyma and potato (Solanum tuberosum) tubers. In a new study, Beauvoit et al (2014) applied kinetic mathematical models to examine tomato (Solanum lycopersicum) fruit development.…”