Why an increase in activity of an enzyme in the Calvin-Benson cycle does not always lead to an increased photosynthetic CO2 uptake rate?-a theoretical analysis

Overexpressing Calvin-Benson cycle (CBC) enzyme shown to limit the flow of CO2 through the cycle is a major approach to improve photosynthesis. Though control coefficients of CBC enzymes vary under different environmental and developmental conditions, it is usually implicitly assumed that enzymes in the CBC have a monotonic impact on the CBC fluxes. Here, with a dynamic systems model of the photosynthetic carbon metabolism, we show that, for glycerate-3-phosphate kinase (PGAK), fructose-1,6-bisphosphatase (FBPase), fructose-1,6-bisphosphate aldolase (FBA) and transketolase (TKa), individually increasing activity of these CBC enzymes theoretically leads to an initial increase then decrease in the fluxes through the CBC. Also, the inhibition constants of adenosine diphosphate (ADP) for PGAK and of fructose-6-phosphate (F6P) for FBPase influence the CBC flux in a biphasic manner. These predicted enzymes showing a biphasic manner are always located in different subcycles of the CBC, which consume the shared substrates in the early steps in the CBC and produce intermediates used as substrates for enzymes in the later reactions. We show that the excessive increase in activities of enzymes in one subcycle consuming the shared metabolite could cause low concentrations of metabolites in the other subcycles, which results in low reaction rates of the later reactions and hence lowers overall CBC flux. This study provides a model to explain the underlying reasons that overexpression of enzymes in the CBC sometimes can negatively impact photosynthesis. We find that balanced activities of enzymes in the subcycles of the CBC are required to gain a higher efficiency of the CBC.

Automated summary

The study shows that increasing the activity of certain CBC enzymes can lead to an initial increase followed by a decrease in flux. Factors influencing CBC flux exhibit a biphasic pattern, with affected enzymes always located in different subcycles. Excessive activity of enzymes in one subcycle can lower metabolite concentrations in other subcycles, resulting in decreased overall CBC flux.