Can the progressive increase of C4 bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration?

The ability to concentrate CO2 around Rubisco allows C4 crops to suppress photorespiration. However, as phosphoenolpyruvate regeneration requires ATP, the energetic efficiency of the C4 pathway at low photosynthetic flux densities (PFD) becomes a balancing act between primary fixation and concentration of CO2 in mesophyll (M) cells, and CO2 reduction in bundle sheath (BS) cells. At low PFD, retro-diffusion of CO2 from BS cells, relative to the rate of bicarbonate fixation in M cells (termed leakiness φ), is known to increase. This paper investigates whether this increase in ϕ could be explained by incomplete inhibition of photorespiration. The PFD response of φ was measured at various O2 partial pressures in young Zea mays plants grown at 250 (LL) and 750 µmol m⁻² s⁻¹ PFD (HL). φ increased at low PFD and was positively correlated with O2 partial pressure. Low PFD during growth caused BS conductance and interveinal distance to be lower in the LL plants, compared to the HL plants, which correlated with lower φ. Model analysis showed that incomplete inhibition of photorespiration, especially in the HL plants, and an increase in the relative contribution of mitochondrial respiration at low PFD could explain the observed increases in φ.

Bundle sheath leakiness and light limitation during C4 leaf and canopy CO2 uptake.

Perennial species with the C(4) pathway hold promise for biomass-based energy sources. We have explored the extent that CO(2) uptake of such species may be limited by light in a temperate climate. One energetic cost of the C(4) pathway is the leakiness () of bundle sheath tissues, whereby a variable proportion of the CO(2), concentrated in bundle sheath cells, retrodiffuses back to the mesophyll. In this study, we scale from leaf to canopy level of a Miscanthus crop (Miscanthus x giganteus hybrid) under field conditions and model the likely limitations to CO(2) fixation. At the leaf level, measurements of photosynthesis coupled to online carbon isotope discrimination showed that leaves within a 3.3-m canopy (leaf area index = 8.3) show a progressive increase in both carbon isotope discrimination and as light decreases. A similar increase was observed at the ecosystem scale when we used eddy covariance net ecosystem CO(2) fluxes, together with isotopic profiles, to partition photosynthetic and respiratory isotopic flux densities (isofluxes) and derive canopy carbon isotope discrimination as an integrated proxy for at the canopy level. Modeled values of canopy CO(2) fixation using leaf-level measurements of suggest that around 32% of potential photosynthetic carbon gain is lost due to light limitation, whereas using determined independently from isofluxes at the canopy level the reduction in canopy CO(2) uptake is estimated at 14%. Based on these results, we identify as an important limitation to CO(2) uptake of crops with the C(4) pathway.