An analytical model of non‐photorespiratory CO₂ release in the light and dark in leaves of C₃ species based on stoichiometric flux balance

Abstract

Leaf respiration continues in the light but at a reduced rate. This inhibition is highly variable, and the mechanisms are poorly known, partly due to the lack of a formal model that can generate testable hypotheses. We derived an analytical model for non-photorespiratory CO2 release by solving steady-state supply/demand equations for ATP, NADH and NADPH, coupled to a widely used photosynthesis model. We used this model to evaluate causes for suppression of respiration by light. The model agrees with many observations, including highly variable suppression at saturating light, greater suppression in mature leaves, reduced assimilatory quotient (ratio of net CO2 and O2 exchange) concurrent with nitrate reduction and a Kok effect (discrete change in quantum yield at low light). The model predicts engagement of non-phosphorylating pathways at moderate to high light, or concurrent with processes that yield ATP and NADH, such as fatty acid or terpenoid synthesis. Suppression of respiration is governed largely by photosynthetic adenylate balance, although photorespiratory NADH may contribute at sub-saturating light. Key questions include the precise diel variation of anabolism and the ATP : 2e -ratio for photophosphorylation. Our model can focus experimental research and is a step towards a fully process-based model of CO2 exchange.Key-words: alternative oxidase; carbon metabolism; Kok effect; photorespiration; photosynthesis; respiration.Abbreviations: A, net CO2 assimilation rate; Ao, net O2 evolution rate; AOX, alternative oxidase; Bn, net anabolic NADH supply; Bp, net anabolic NADPH demand; Bt, net anabolic ATP demand; ci, intercellular CO2 partial pressure; COX, cytochrome oxidase; fm, fraction of photorespiratory NADH that remains in mitochondria; fx, fraction of excess thylakoid reducing potential dissipated as NADPH export; G6PDH, glucose-6-phosphate dehydrogenase; I, incident PPFD; J, potential thylakoid e -transport rate; J′, Vc in RuBP-limiting conditions; Ja, actual thylakoid e -transport rate; Jm, max potential thylakoid e -transport rate; M, maintenance ATP demand; mETC, mitochondrial e -transport chain; O, ambient O2 partial pressure; OPPP, oxidative pentose phosphate pathway; pe, ATP : 2e -ratio, ADP phosphorylated per 2 e -transported to ferredoxin; po, P : O ratio, ratio of ADP phosphorylation to O2 reduction in mitochondria; pom, overall max P : O ratio; pom,ana, max P : O ratio for NADH generated in anabolic C flow; pom,cat, max P : O ratio for NADH derived from catabolic substrate oxidation; pom,cyt, max P : O ratio for cytosol derived NADH; pom,mtx, max P : O ratio for matrix derived NADH; PPFD, photosynthetic photon flux density; QY, quantum yield of CO2 from incident PPFD; Rc, rate of non-photorespiratory CO2 release; Ro, rate of O2 reduction by mitochondria; RuBP, ribulose-1,5-bisphosphate; S, net conversion of TP to sucrose and/or starch; t, net ATP demand resulting from S; TP, triose phosphate; Vana, rate of C flow into C skeletons for biosynthesis; Vby, rate of CO2 release due to ana...

Alternative oxidase: a respiratory electron transport chain pathway essential for maintaining photosynthetic performance during drought stress

“…These studies usually examined photosynthetic performance in response to short‐term or long‐term changes in irradiance, and while they have generally reported only small perturbations in photosynthesis as a result of the change in AOX amount, they are nonetheless a body of work supporting the idea that this unique respiratory pathway may have a specific role in the photosynthesizing cell (Noguchi and Yoshida ). These finding are further supported by recent computational modelling studies of plant metabolism, some of which predict an increased contribution of AOX to respiration with increasing irradiance (Buckley and Adams , Cheung et al , Nikoloski et al ). Interestingly, a role of AOX in optimizing photosynthesis at high irradiance was also recently established for the diatom Phaeodactylum tricornutum , using an AOX knockdown approach (Bailleul et al ), and knockdown of AOX in soybean has also been shown to perturb photosynthesis (Chai et al ).…”

Effects of Elevated CO2 on Levels of Primary Metabolites and Transcripts of Genes Encoding Respiratory Enzymes and Their Diurnal Patterns in Arabidopsis thaliana: Possible Relationships with Respiratory Rates

“…Consistent with this, a higher RQ value was observed in soybean leaves under elevated CO 2 (Leakey et al 2009b). Anabolic processes such as nitrate assimilation were also enhanced under elevated CO 2 ; these would contribute to the high RQ, as suggested by the flux-balanced model (Buckley and Adams 2011). Further research should focus on clarifying which anabolic processes are stimulated in shoots under elevated CO 2 .…”

Evaluating a new method to estimate the rate of leaf respiration in the light by analysis of combined gas exchange and chlorophyll fluorescence measurements

“…3). A new analytical model hypothesizing that the oxidative pentose phosphate pathway is progressively inhibited by the light-driven increase in thylakoid reducing power can reproduce the abrupt transition point of the Kok effect (Buckley and Adams, 2011). Direct measurements of R d (with procedures from, for example, Haupt-Herting et al , 2001; Loreto et al , 2001; Pinelli and Loreto, 2003; Pärnik and Keerberg, 2007), combined with a model analysis, might help to understand fully the inter-entangling of the Kok effect, light inhibition of R d , and photorespiration, and to verify the estimates of R d by the indirect methods evaluated in this study.…”