Leaf C4 Photosynthesis in silico: The CO2 Concentrating Mechanism

Abstract

A computer model comprised of light reactions in PS II and PS I, electron—proton transport reactions in mesophyll and bundle sheath (BS) chloroplasts, all enzymatic reactions, and most of the known regulatory functions of NADP-malic enzyme type C4 photosynthesis, has been developed as a system of differential budget equations for intermediate compounds. Rate-equations were designed on principles of multisubstrate-multiproduct enzyme kinetics. The model provided good simulations for rates of photosynthesis and pool sizes of intermediates under varying light, CO2 and O2. A principle novelty of the model for NADP-ME type species is the hypothesis that electrons transported into the BS chloro-plasts via the malate shuttle enter the electron transport chain with the help of NAD(P)H-plastoquinone oxyreductase (NDH, or an enzyme of similar function). In the model, the electrons from reduced plastoquinone pass through the Q-cycle and photosystem I (PS I) only once, without cycling around PS I, as commonly assumed. With this the ratio of 2 ATP/NADPH, satisfying the energy requirements process, is fixed, provided that 2 H+/e− are transported by the Q-cycle and 2 H+/e− by NDH, and 4 H+are utilized per ATP generated. The hypothesis is based on modeling results showing that there must be fine control of the ATP/NADPH ratio in BS chloroplasts for optimum function of C4 photosynthesis. The CO2 concentrating function of NADP-ME type C4 photosynthesis, which occurs as the rate of the C4 cycle exceeds the rate of CO2 assimilation in BS cells (overcycling), can be explained on the basis of two processes. First, alternative consumption of some ATP in BS chloroplasts to support other processes (e.g. starch and protein synthesis) reduces the ATP/NADPH ratio available in BS. As a result, some CO2 imported into BS remains unassimilated and accumulates, resulting in overcycling back to the mesophyll. Second, the residual photorespiratory activity alternatively consumes some ribulose 1,5-bisphosphate for oxygenation; as with the alternative consumption of ATP, some CO2 imported into BS remains unassimilated and accumulates, causing overcycling. The CO2 evolved from photorespiration in BS also contributes to the CO2 pump in C4 plants.