Increased bundle-sheath leakiness of CO2 during photosynthetic induction shows a lack of co-ordination between the C4 and C3 cycles

Authors: WANG, YU - University Of Illinois; STUTZ, SAMANTHA - University Of Illinois; Bernacchi, Carl; BOYD, RYAN - University Of Illinois; ORT, DONALD - University Of Illinois; LONG, STEPHEN - University Of Illinois

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/25/2022
Publication Date: 11/3/2022
Citation: Wang, Y., Stutz, S., Bernacchi, C.J., Boyd, R., Ort, D.R., Long, S. 2022. Increased bundle-sheath leakiness of CO2 during photosynthetic induction shows a lack of co-ordination between the C4 and C3 cycles. New Phytologist. 236(5):1661-1675. https://doi.org/10.1111/nph.18485.
DOI: https://doi.org/10.1111/nph.18485

Interpretive Summary: Certain crops use a photosynthetic pathway that uses energy to concentrate carbon dioxide in leaves, which results in a much more efficient photosynthesis and growth rate at higher temperatures. Some of the carbon dioxide that is concentrated the leaves leaks out, which can, at times, lower the efficiency of photosynthesis and growth. Historically, measurements were made at steady-state, meaning that the conditions around the leaves were very uniform for a long period of time. In this study we made similar measurements but which changing conditions around the leaf. Our results show that the leakiness is much greater when the leaves are not at steady-state. This suggests that major crops that use this concentrating mechanisms have lower efficiency than previously thought, and that there may be opportunity to improve this feature.

Technical Abstract: • Use of a complete dynamic model of NADP-ME C4 photosynthesis indicated that during dark or shade to high-light transitions induction of the C4 pathway was more rapid than that of the C3, resulting in a predicted transient increase in bundle-sheath CO2 leakiness (f) • Previously, f was measured at steady-state, here we developed a new method, coupling a tunable diode laser absorption spectroscope (TDL) with a gas exchange system, to track in sorghum and maize through the non-steady-state condition of photosynthetic induction. • In both species, f showed a transient increase to >0.35 before declining to a steady-state of 0.2 by 1500 s after illumination. Average ' was 60% higher than at steady-state over the first 600 s of induction and 30% higher over the first 1500 s. • The transient increase in f, which was consistent with the model prediction, indicated that capacity to assimilate CO2 into the C3 cycle in the bundle-sheath failed to keep pace with the rate of dicarboxylate delivery by the C4 cycle. Because non-steady-state light conditions are the norm in field canopies, the results suggest that f in these major crops in the field is significantly higher and energy conversion efficiency lower than previous measured values under steady-state conditions.