Modeling sugar metabolism in tomato fruit.

Plant metabolism changes during development and involves many enzymes acting in different subcellular compartments. Although difficult for our brains to grasp, this complexity lends itself to mathematical modeling (reviewed in Schallau and Junker, 2010; Rohwer, 2012). Such modeling has examined the effects of increasing atmospheric CO2 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. Tomato fruit development includes a stage of rapid cell division, followed by fruit expansion and then maturation (reviewed in Pesaresi et al., 2014). To establish the model parameters, the authors first examined the growth-associated increase in vacuole size and estimated the water flow across the tonoplast, since the vacuole expands dramatically during fruit development. The authors next modeled sugar metabolism during fruit development, beginning with the sugarcane model and adding vacuolar enzymes and transporters, and plastids (see figure). The authors input measured values for enzyme capacities (Vmax) and the contents of glucose, fructose, sucrose, and glucose-6-phosphate into the model and optimized the parameters (such as sugar carrier capacities) for 10 phases of development, from cell division to fruit expansion. Finally, they validated the model on previously published data for different tomato varieties, including transgenic lines with altered levels of acid invertase, and a wild tomato species, Lycopersicon chmielewskii. Examination of the model over time showed that the capacities of tonoplast carriers, and sucrose import, changed over the course of fruit development, with Vmax that was high during cell division and lower at maturation, indicating that the vacuoles of cells during the division phase have an unexpectedly high capacity for sugar transport. The flux of sugars through different enzymes also changed during development; for example, acid invertase cleavage of sucrose in the vacuole showed high flux during the cell division phase. The model also showed that the sugars and organic acids (malate and citrate) stored in the vacuole increased the osmotic strength of the vacuole, likely driving osmotic expansion of the vacuole, but this effect decreased during development. Also, sucrose import into cells and transport into the vacuole controlled sugar concentration in the vacuole. Finally, the authors used hierarchical clustering of flux and Vmax to identify enzymes that have different effects during development. For example, hexose carriers, sugar kinases, and other enzymes showed maximal activity at the cell division phase. Intriguingly, the model indicated that the metabolic changes that occur during fruit growth show hallmarks of conservation of energy during both the cell division and expansion phases. This modeling revealed unexpected characteristics of sugar transport and metabolic fluxes in tomato development. Further research may incorporate energy metabolism in mitochondria and other aspects of development and perhaps link metabolism to sugar’s well-known role in signaling. Don’t look for good tomatoes in the dead of winter yet; nevertheless, although metabolic engineering by altering one or a few enzymes has generally proven difficult, metabolic engineering informed by well-constructed models may prove successful. 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.)