Reduction of bundle sheath size boosts cyclic electron flow in C4 Setaria viridis acclimated to low light

When C-4 leaves are exposed to low light, the CO2 concentration in the bundle sheath (BS) cells decreases, causing an increase in photorespiration relative to assimilation, and a consequent reduction in biochemical efficiency. These effects can be mitigated by complex acclimation syndromes, which are of primary importance for crop productivity but are not well studied. We unveil an acclimation strategy involving the coordination of electron transport processes. First, we characterize the anatomy, gas exchange and electron transport of C-4 Setaria viridis grown under low light. Through a purposely developed biochemical model, we resolve the photon fluxes and reaction rates to explain how the concerted acclimation strategies sustain photosynthetic efficiency. Our results show that a smaller BS in low-light-grown plants limited leakiness (the ratio of CO2 leak rate out of the BS over the rate of supply via C-4 acid decarboxylation) but sacrificed light harvesting and ATP production. To counter ATP shortage and maintain high assimilation rates, plants facilitated light penetration through the mesophyll and upregulated cyclic electron flow in the BS. This shade tolerance mechanism, based on the optimization of light reactions, is possibly more efficient than the known mechanisms involving the rearrangement of carbon metabolism, and could potentially lead to innovative strategies for crop improvement.