Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation

Raghavendra, Agepati S.; Padmasree, Kollipara

doi:10.1016/j.tplants.2003.09.015

Cited by 427 publications

(352 citation statements)

References 65 publications

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“…Potential coupling mechanisms have been discussed by numerous recent reviews on mitochondriachloroplast interactions (Krömer 1995;Hoefnagel et al 1998;Raghavendra & Padmasree 2003). Here, we discuss…”

Section: Mechanisms For Subcellular Adenylate and Reductant Couplingmentioning

confidence: 91%

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

Buckley

Adams

2010

Plant Cell & Environment

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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...

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Section: Mechanisms For Subcellular Adenylate and Reductant Couplingmentioning

confidence: 91%

“…Thirdly, the available evidence suggests that the many kinetic constraints on metabolic carbon flow are exquisitely coordinated (Raghavendra & Padmasree 2003;Noctor, De Paepe & Foyer 2006;Rasmusson & Escobar 2007). Any effective model of respiration should at least attempt to capture this coordination.…”

Section: Some Thoughts On the Nature Of Our Modelmentioning

confidence: 99%

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

Buckley

Adams

2010

Plant Cell & Environment

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“…Mitochondrial 2-oxoglutarate has been also associated with biochemical and retrograde signalling in plants (Hodges, 2002) (not shown). Nitric oxide and ascorbate have been proposed to act as mitochondrion-to-plastid signals (reviewed in: Raghavendra and Padmasree, 2003). Numbers of chloroplast (¨3000) and mitochondrial (¨2000) proteins encoded in the nucleus are according to Richly and Leister (2004c).…”

Section: Signalling Involving Sugars or Reactive Oxygen Speciesmentioning

confidence: 99%

“…The complex metabolic interdependence of chloroplasts and mitochondria is well documented (Raghavendra and Padmasree, 2003). For instance, photosynthesis provides substrates for mitochondrial respiration, but depends itself on a range of compounds synthesized by mitochondria, including ATP in the dark.…”

Section: Cross-talk Between Chloroplast and Mitochondrionmentioning

confidence: 99%

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Leister¹

2005

Gene

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Post-endosymbiotic evolution of chloroplasts was characterized by a massive transfer of cyanobacterial genes to the nucleus, followed by re-routing of many of their encoded proteins. In consequence, most plastid proteins are nucleus-encoded, enabling an anterograde (nucleusto-plastid) control of the organelle. The regulation of chloroplast functions includes also cross-talk between chloroplasts and mitochondria, as well as retrograde (plastid-to-nucleus) signalling. Genetic analyses reveal that redox state, flux through the chlorophyll biosynthetic pathway, sugar sensing and reactive oxygen species contribute to retrograde signalling. However, the identity of the messenger molecule(s) remains largely unknown. Novel facets of the chloroplast -mitochondrion cross-talk have been revealed by the characterization of mitochondrial mutants affected in chloroplast properties. Studies of the nuclear chloroplast transcriptome imply the existence of at least three distinct types of transcriptional regulation: a master switch, acting in a binary mode by either inducing or repressing the same large set of genes; a ''mixed response'' with about equal numbers of up-and down-regulated genes; and mechanisms supporting the specific co-regulation of nuclear genes for photosynthesis and for plastid gene expression. The recent discovery of the latter mode of control highlights a possibly ancient route to co-ordinate chloroplast and nuclear genome expression. D

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“…2000;Gardestrom & Igamberdiev 2002;Noctor et al . 2003;Raghavendra & Padmasree 2003). For instance, photorespiration initiates in the chloroplasts with the oxidation of ribulose-1:5-bisphosphate; mitochondria in subsequent steps of this pathway oxidize glycine to serine, releasing ammonia (NH 3 ) and CO 2 .…”

Section: Introductionmentioning

confidence: 99%

Oxygen consumption during leaf nitrate assimilation in a C₃ and C₄ plant: the role of mitochondrial respiration

Bloom

2004

Plant Cell & Environment

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Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation

Cited by 427 publications

References 65 publications

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

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

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Oxygen consumption during leaf nitrate assimilation in a C₃ and C₄ plant: the role of mitochondrial respiration

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Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation

Cited by 427 publications

References 65 publications

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

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

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

Oxygen consumption during leaf nitrate assimilation in a C3 and C4 plant: the role of mitochondrial respiration

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

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

Oxygen consumption during leaf nitrate assimilation in a C₃ and C₄ plant: the role of mitochondrial respiration