Faster than expected Rubisco deactivation in shade reduces cowpea photosynthetic potential in variable light conditions

Abstract

Cowpea is the major source of vegetable protein for rural populations in sub-Saharan Africa and average yields are not keeping pace with population growth. Each day, crop leaves experience many shade events and the speed of photosynthetic adjustment to this dynamic environment strongly affects daily carbon gain. Rubisco activity is particularly important because it depends on the speed and extent of deactivation in shade and recovers slowly on return to sun. Here, direct biochemical measurements showed a much faster rate of Rubisco deactivation in cowpea than prior estimates inferred from dynamics of leaf gas exchange in other species1–3. Shade-induced deactivation was driven by decarbamylation, and half-times for both deactivation in shade and activation in saturating light were shorter than estimates from gas exchange (≤53% and 79%, respectively). Incorporating these half-times into a model of diurnal canopy photosynthesis predicted a 21% diurnal loss of productivity and suggests slowing Rubisco deactivation during shade is an unexploited opportunity for improving crop productivity.

Variation of Photosynthetic Induction in Major Horticultural Crops Is Mostly Driven by Differences in Stomatal Traits

“…By applying the FvCB model on dynamic A vs. C i , it was assumed that the slow A induction changes are mainly caused by Rubisco activation. Although the role of Rubisco activation during A induction has been verified experimentally ( Taylor et al, 2022 ), other processes, such as changes in mesophyll conductance could also play a role during A induction ( Liu et al, 2021 ; Sakoda et al, 2021 ). However, mesophyll conductance changes have been suggested to be far more rapid than the observed V cmax kinetics presented here, and the relative importance of mesophyll conductance for A induction is still under debate ( De Souza et al, 2020 ; Liu et al, 2021 ; Sakoda et al, 2021 ).…”

Sunflecks in the upper canopy: dynamics of light‐use efficiency in sun and shade leaves of Fagus sylvatica

“…It should be emphasized that photosynthetic recovery is not only due to NPQ relaxation, but the product of many processes including: chloroplast relocation (Sztatelman et al ., 2016), state transitions (Mullineaux & Emlyn‐Jones, 2005), and respiration rates (Atkin et al ., 2000). The relative contribution of each to photosynthetic recovery currently remains unexplored, yet understanding these processes may hold the key to improve productivity (Kromdijk et al ., 2016; Taylor et al ., 2022).…”

“…Thus, differences of activation levels under low irradiance, and/or of deactivation speed during this 30 min period, may partly contribute to the differences in photosynthesis induction between canopy depths. The speed of Rubisco deactivation has been found to vary between species (Pearcy et al ., 1996), and is increasingly considered as a potential target for productivity improvements under fluctuating light (Taylor et al ., 2022).…”

“…This is followed by the first phase of the induction response, which lasts 1–2 min, consisting of rapid light‐activation of enzymes involved in the ribulose‐1,5‐biphosphate (RuBP) regeneration pathway (Kirschbaum & Pearcy, 1988; Sassenrath‐Cole & Pearcy, 1992). For leaves experiencing longer periods of shade, activation of Rubisco is also needed, involving Rubisco activase (Taylor et al ., 2022), itself requiring electron transport through photosystem I (PSI) and adenosine 5′‐triphosphate (ATP) production (Campbell & Ogren, 1992). This process can take > 10 min (Woodrow & Mott, 1989).…”

A Year at the Forefront of Engineering Photosynthesis

“…In addition, Rubisco reactivation on shade–sun transitions is known to be slow ( Sassenrath-Cole et al, 1994 ; Tanaka et al, 2019 ), providing an opportunity for engineering. Notably, a recent paper that determined in vitro and in vivo Rubisco deactivation half-times in cowpea found faster Rubisco deactivation than previously predicted from wheat values ( Taylor et al, 2022 ). Furthermore, the speed of Rubisco response to sun–shade transitions differed more than Rubisco induction on shade–sun transitions, leading the authors to hypothesise that Rubisco deactivation could be a new target for engineering ( Taylor et al, 2022 ).…”