ZucAt: multi-compartment metabolic model of growing Arabidopsis thaliana

Version 2

The model presents a multi-compartmental (mesophyll, phloem and root) metabolic model of growing Arabidopsis thaliana. The flux balance analysis (FBA) of the model quantifies: sugar metabolism, central carbon and nitrogen metabolism, energy and redox metabolism, proton turnover, sucrose translocation from mesophyll to root and biomass growth under both dark- and light-growth conditions with corresponding growth either on starch (in darkness) or on CO2 (under light). The FBA predicts that photosynthetically active plastid [under fixed ratio of photorespiration / photosynthesis = 0.2] can operate in different energy modes by levering the cyclic electron flow through FQR reaction in light photosynthesis system: (i) when flux through FQR = 0, the plastid is forced to import ATP from cytosol to fulfil the ATP/NADPH requirement for carbon fixation; (ii) when the flux through FQR equals to 0.35 of non-cyclic photosynthesis, the plastid becomes self-sufficient in terms of the ATP balance; (iii) when the flux through FQR is >0.35 of non-cyclic photosynthesis, then the plastid produces ATP surplus, which is exported to cytosol. Thus, the interplay between cyclic photophosphorylation and photorespiration can play regulatory role in adapting of the energy state of plastid to various conditions to hold ATP/NADPH ratio sufficient for the carbon fixation in Calvin cycle. Under all tested “light” scenarios, NADPH is over-produced in light photosynthesis system, and therefore its surplus is exported from plastid through malate/oxaloacetate shuttle into mitochondria, where the reduced equivalents are used for ATP synthesis. From the energetic point of view, mitochondria is the main ATP provider for cytoplasmic processes together with plastid (when it is actual), glycolysis under both light- and dark-growth conditions; also, mitochondria is the main sink for reduced equivalents translocated both from plastid and from cytoplasm. The model described all main metabolic processes participating in the proton metabolism. The translocation of sucrose among plant tissues was associated with an integral balance of protons, which in turn was partially defined by operational modes of the energy metabolism (photosynthesis, respiration). The proton fluxes predicted by FBA generally corresponds to the molecular mechanisms and functional peculiarity of the sucrose transporters SWEET and SUC/STP proton-symporters and net-flux of sucrose from ‘source’ to ‘sink’ tissue. Thus, our multi-compartmental model adequately describes the growth stoichiometry and quantifies sucrose translocation processes of Arabidopsis thaliana in light and dark conditions.