Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm

Abstract

The distribution of resources between enzymes of photosynthetic carbon metabolism might be assumed to have been optimized by natural selection. However, natural selection for survival and fecundity does not necessarily select for maximal photosynthetic productivity. Further, the concentration of a key substrate, atmospheric CO 2 , has changed more over the past 100 years than the past 25 million years, with the likelihood that natural selection has had inadequate time to reoptimize resource partitioning for this change. Could photosynthetic rate be increased by altered partitioning of resources among the enzymes of carbon metabolism? This question is addressed using an ''evolutionary'' algorithm to progressively search for multiple alterations in partitioning that increase photosynthetic rate. To do this, we extended existing metabolic models of C 3 photosynthesis by including the photorespiratory pathway (PCOP) and metabolism to starch and sucrose to develop a complete dynamic model of photosynthetic carbon metabolism. The model consists of linked differential equations, each representing the change of concentration of one metabolite. Initial concentrations of metabolites and maximal activities of enzymes were extracted from the literature. The dynamics of CO 2 fixation and metabolite concentrations were realistically simulated by numerical integration, such that the model could mimic well-established physiological phenomena. For example, a realistic steady-state rate of CO 2 uptake was attained and then reattained after perturbing O 2 concentration. Using an evolutionary algorithm, partitioning of a fixed total amount of protein-nitrogen between enzymes was allowed to vary. The individual with the higher light-saturated photosynthetic rate was selected and used to seed the next generation. After 1,500 generations, photosynthesis was increased substantially. This suggests that the ''typical'' partitioning in C 3 leaves might be suboptimal for maximizing the light-saturated rate of photosynthesis. An overinvestment in PCOP enzymes and underinvestment in Rubisco, sedoheptulose-1,7-bisphosphatase, and fructose-1,6-bisphosphate aldolase were indicated. Increase in sink capacity, such as increase in ADP-glucose pyrophosphorylase, was also indicated to lead to increased CO 2 uptake rate. These results suggest that manipulation of partitioning could greatly increase carbon gain without any increase in the total protein-nitrogen investment in the apparatus for photosynthetic carbon metabolism.

Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency

“…Those studies highlighted the effects g s can have on crop yield, not only through reduced CO 2 diffusion but also through the impact on water loss and evaporative cooling of the leaf. Indeed, enhancing photosynthesis yields by only 2% to 3% is sufficient to substantially increase plant growth and biomass over the course of a growing season (Lefebvre et al, 2005;Zhu et al, 2007). …”

Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis

“…Equations for the three exceptions were as given by Zhu et al (2007). Otherwise, a general reversible reaction of the form A + B , → C + D was assumed, following the standard kinetic equation of a reversible reaction with two substrates and two products (Cleland, 1963), as in Zhu et al (2007).…”

“…The carbon metabolism part of photosynthetic C3 carbon assimilation and photorespiratory C2 metabolism (Zhu et al, 2007) was used as a basis of the kinetic model of C4 metabolism, upon which MC-BSC metabolite transfer reactions were added. The four major components required for developing this C4 model are described below.…”

“…The total concentration of the adenylate nucleotide ([CA]) chloroplast was assumed constant (Pettersson and Ryde-Pettersson, 1988;Poolman et al, 2000;Zhu et al, 2007Zhu et al, , 2012. Similarly, the sum of [NADPH] and [NADP] in chloroplast stroma ([CN]) was assumed constant in both the MCs and BSCs.…”

“…In recent years, in silico experiments based on systems modeling have emerged as an effective way to understand control properties of the C3 photosynthetic system and focus practical engineering on key targets (Fell, 1997;Poolman et al, 2000;Zhu et al, 2007Zhu et al, , 2012. Steady-state models of C4 photosynthesis were first developed over 30 years ago (Berry and Farquhar, 1978;Collatz et al, 1992;von Caemmerer, 2000), and the metabolite transport processes of C4 photosynthesis were simply described (Hatch and Osmond, 1976).…”