Mechanism of C₄ Photosynthesis

Abstract

A theoretical model of the composition of the inorganic carbon pool generated in C4 leaves during steady-state photosynthesis was derived. This model gives the concentrations of CO2 and 02 in the bundle sheath cells for any given net photosynthesis rate and inorganic carbon pool size. The model predicts a bundle sheath CO2 concentration of 70 micromolar during steady state photosynthesis in a typical C4 plant, and that about 13% of the inorganic carbon generated in bundle sheath cells would leak back to the mesophyll cells, predominantly as CO2. Under these circumstances the flux of carbon through the C4 acid cycle would have to exceed the net rate of CO2 assimilation by 15.5%. With the calculated 02 concentration of 0.44 millimolar, the potential photorespiratory CO2 loss in bundle sheath cells would be about 3% of CO2 assimilation. Among the factors having a critical influence on the above values are the permeability of bundle sheath chloroplasts to HCO3-, the activity of carbonic anhydrase within these chloroplasts, the assumed stromal volume, and the permeability coefficients for CO2 and 02 diffusion across the interface between bundle sheath and mesophyll cells. The model suggests that as the net photosynthesis rate changes in C4 plants, the level and distribution of the components of the inorganic carbon pool change in such a way that C4 acid overcycling is maintained in an approximately constant ratio with respect to the net photosynthesis rate.The generally accepted function of the C4 pathway is to concentrate CO2 in the bundle sheath cells where Rubisco and the PCR cycle are specifically located (4, 13). During photosynthesis in C4 leaves, a pool of inorganic carbon develops to a substantially higher concentration than would be expected from equilibration with CO2 in air (8,12 on the observed net fixation rate and pool size, which indicated the likelihood of a large CO2 component (8). However, in this simple model the concentrations of CO2 and HCO3-, and the fluxes of carbon were determined empirically and it was not possible to take detailed account of the intracellular distribution of inorganic carbon. The size and composition of such inorganic carbon pools would be affected by the pH of the various subcompartments and their permeabilities to bicarbonate. Uncertainty about the level and location of carbonic anhydrase is another complicating factor (2).To operate effectively, the bundle sheath cells must restrict the diffusion of inorganic carbon back to the mesophyll, while still allowing the influx of C4 acids and efflux of photosynthetically produced 02 (13). The extent to which inorganic carbon leaks back to the mesophyll will depend not only on the permeability of the interface between bundle sheath and mesophyll cells to CO2 and HCO3-, but also on the cytosolic concentrations of these components in bundle sheath cells during photosynthesis. Similarly, the flux of 02 will be determined by the concentration in bundle sheath cells and its permeability. The factors that affect these steady-st...

Carbonic anhydrases in plants and algae

“…Results of recent experiments support the view of Jenkins et al (1989). Ludwig et al (1998) transformed the NADP-ME-type C4 dicot Flaveria bidentis with a construct encoding the tobacco chloroplast CA lacking a transit sequence.…”

“…Furthermore, it was postulated that CA must be excluded from the bundle sheath cells to avoid loss of accumulated CO 2 due to its conversion to HCO 3 -and leakage of the latter back to mesophyll cells through plasmodesmata (Burnell & Hatch 1988). However, results of later modelling studies indicated that effects of CA in the bundle sheath would be less severe (Jenkins, Furbank & Hatch 1989).…”

Loss of the Transit Peptide and an Increase in Gene Expression of an Ancestral Chloroplastic Carbonic Anhydrase Were Instrumental in the Evolution of the Cytosolic C4 Carbonic Anhydrase in Flaveria

“…Rubisco and the other enzymes of the photosynthetic carbon reduction cycle, located in the bundle sheath cell chloroplasts, reduce the released CO 2 and the remaining three-carbon compound diffuses back into the mesophyll cells, where it can undergo another round of the C 4 acid cycle. This combination of anatomical and biochemical characteristics, including the cell-specific expression of enzymes, results in an efficient CO 2 concentrating mechanism whereby the CO 2 level in the C 4 bundle sheath cells is up to 20 times that of the surrounding mesophyll cells and photorespiration is essentially eliminated (Jenkins et al, 1989).…”

Carbonic Anhydrase Activity in Leaves and Its Role in the First Step of C4 Photosynthesis

“…After measuring the rate of 180 loss due to the nonenzymic reaction, the enzyme-catalyzed rate was determined by adding a sample of extract containing CA. CA activity in the CO2 hybridration direction was deduced from the increase in rate of 180 loss over that observed without enzyme by applying this factor to the nonenzymic first order rate constant for the CO2 hydration reaction (25°C and an ionic strength of 0.1 [7] …”