Increased bundle‐sheath leakiness of CO₂ during photosynthetic induction shows a lack of coordination between the C₄ and C₃ cycles

Abstract

Summary Use of a complete dynamic model of NADP‐malic enzyme C4 photosynthesis indicated that, during transitions from dark or shade to high light, induction of the C4 pathway was more rapid than that of C3, resulting in a predicted transient increase in bundle‐sheath CO2 leakiness (ϕ). Previously, ϕ has been measured at steady state; here we developed a new method, coupling a tunable diode laser absorption spectroscope with a gas‐exchange system to track ϕ in sorghum and maize through the nonsteady‐state condition of photosynthetic induction. In both species, ϕ showed a transient increase to > 0.35 before declining to a steady state of 0.2 by 1500 s after illumination. Average ϕ 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 ϕ, which was consistent with 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 nonsteady‐state light conditions are the norm in field canopies, the results suggest that ϕ in these major crops in the field is significantly higher and energy conversion efficiency lower than previous measured values under steady‐state conditions.

Lessons from relatives: C4 photosynthesis enhances CO2assimilation during the low-light phase of fluctuations

“…Alternatively, if the CCM is faster to activate during light induction than the C3 cycle there could be transient over-pumping of CO2 and an increase in BS leakiness -where CO2 diffuses out of BS cells back into M cells, raising the energetic cost of carbon fixation due to the futile cycling of PEP. Greater BS leakiness during induction relative to steady state has been previously observed in maize and sorghum (Wang et al, 2022). Lags in CCM deactivation during transitions to lower light could also increase leakiness and reduce quantum yields if Mal/Asp accumulated in the BS is decarboxylated despite insufficient C3 cycle activity.…”

Faster induction of photosynthesis increases biomass and grain yield in glasshouse‐grown transgenic Sorghum bicolor overexpressing Rieske FeS

“…Photosynthetic induction in C 4 plants is slower than in closely related C 3 species and, in NADP-ME dicot Flaveria bidentis, the inefficiency was attributed to an incomplete suppression of photorespiration caused by a slow build-up of the C 4 cycle intermediates (Arce Cubas et al, 2023;Sage and McKown, 2006). Alternatively, Rubisco activation was proposed as a primary cause of lost efficiency based on the increased leakiness of CO 2 detected during the photosynthetic induction in NADP-ME monocots, maize and sorghum, and metabolic modelling of NADP-ME C 4 photosynthesis (Wang et al, 2021(Wang et al, , 2022. In this work, similar levels of PhiPSII between control and transgenic plants in the beginning of induction suggested unaltered linear electron flow rate (Figure 6), whilst the faster establishing of NPQ in plants with increased Rieske content indicated that more pmf was generated, likely, via cyclic electron flow.…”

Greater leaf photosynthesis in the field by increasing mesophyll conductance via modified cell wall porosity and thickness in tobacco

“…The LI-COR 6800 gas exchange system (LI-COR Environmental) was coupled to a tunable-diode laser absorption spectroscope (TDLAS model TGA 200A; Campbell Scientific) to measure online carbon isotope discrimination 65,66 . The TDL was connected to the LI-6800 reference and sample air streams using the ports on the back of the sensor head.…”