Resolving leaf level metabolism of C4Setaria viridis acclimated to low light through a biochemical model

Abstract

AbstractWhen C4 plants are exposed to low light, CO2 concentration in the bundle sheath (BS) decreases, causing an increase in photorespiration, leakiness (the ratio of CO2 leak rate out of the BS over the rate of supply via C4 acid decarboxylation), and a consequent reduction in biochemical efficiency. This can to some extent be mitigated by complex acclimation syndromes, which are of primary importance for crop productivity, but not well studied. We unveil a strategy of leaf-level low light acclimation involving regulation of electron transport processes. Firstly, we characterise anatomy, gas-exchange and electron transport of Setaria viridis grown under low light. Through a newly developed biochemical model we resolve the photon fluxes, and reaction rates to explain how these concerted acclimation strategies sustain photosynthetic efficiency. Smaller BS in low light-grown plants limited leakiness but sacrificed light harvesting and ATP production. To counter ATP shortage and maintain high assimilation rates, plants facilitated light penetration through mesophyll and upregulated cyclic electron flow in the BS. This novel shade tolerance mechanism based on optimisation of light reactions is more efficient than the known mechanisms involving the rearrangement of dark reactions and can potentially lead to innovative strategies for crop improvement.SignificanceWe mechanistically link the optical cross section with the rate of electron transport, the engagement of cyclic electron flow, the relative rate of ATP and NADPH generation, and ultimately the apportioning of dark reactions between mesophyll and bundle sheath cells. The striking capacity of S. viridis to acclimate light reactions presents a novel and perhaps the most efficient shade tolerance strategy, potentially leading to novel possibilities for crop improvement.