Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell

Krömer, Silke; Stitt, Mark; Heldt, Hans W.

doi:10.1016/0014-5793(88)81453-4

Cited by 128 publications

(79 citation statements)

References 11 publications

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“…If the average rate of assimilate export from a leaf is 10 to 15 mg.dm-2 h-', then sucrose hydrolysis within the vacuole could account for 17 to 30% of the next flux. Recently, Kromer et al (20) showed that mitochondrial oxidative phosphorylation was essential for supplying the cytosol with ATP during photosynthesis. The sucrose formation pathway requires the equivalent of one ATP per sucrose molecule synthesized, and if futile cycling occurs (Fig.…”

Section: Changes In Acid Invertase During Leaf Developmentmentioning

confidence: 99%

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

Huber

1989

Plant Physiol.

176

136

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It is not known why some species accumulate high concentrations of sucrose in leaves during photosynthesis while others do not. To determine the possible basis, we have studied 10 species, known to differ in the accumulation of sucrose, in terms of activities of sucrose hydrolyzing enzymes. In general, acid invertase activity decreased as leaves expanded; however, activities remaining in mature, fully expanded leaves ranged from low (<10 micromoles per gram fresh weight per hour) to very high (>100 micromoles per gram fresh weight per hour). In contrast, sucrose synthase activities were low and relatively similar among the species (4-10 micromoles per gram fresh weight per hour). Importantly, leaf sucrose concentration, measured at midaftemoon, was negatively correlated with acid invertase activity. We propose that sucrose accumulation in vacuoles of species such as soybean and tobacco is prevented by acid invertase-mediated hydrolysis. Initial attempts were made to characterize the relatively high activity of acid invertase from mature soybean leaves. Two apparent forms of the enzyme were resolved by Mono Q chromatography. The two forms had similar affinity for substrate (apparent Km [sucrose] = 3 millimolar) and did not interconvert upon rechromatography. It appeared that the loss of whole leaf invertase activity during expansion was largely the result of changes in one of the enzyme forms. Overall, the results provide a mechanism to explain why some species do not accumulate sucrose in their leaves. Some futile cycling between sucrose and hexose sugars is postulated to occur in these species, and thus, the energy cost of sucrose production may be higher than is generally thought.In many common higher plants, the principal end products of leaf photosynthesis are the carbohydrates starch and sucrose. However, species differ in the partitioning of photosynthetically fixed carbon between starch and sucrose and the extent to which sucrose normally accumulates in leaves during the photoperiod (9, 13). Accumulation of carbohydrates in leaves is critical, as they are mobilized in darkness to support continued translocation (albeit at a reduced rate) and thereby maintain heterotrophic plant parts.Plant species such as soybean that accumulate starch typically do not accumulate soluble sugars; conversely, species ' Cooperative investigations ofthe U.S. Department ofAgriculture,

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Section: Changes In Acid Invertase During Leaf Developmentmentioning

confidence: 99%

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

Huber

1989

Plant Physiol.

176

136

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“…Several explanations for reduced Rc in the light have been proposed, most of which involve photosynthesis to some degree:(1) ExcessATP or redox equivalents generated by the light reactions of photosynthesis can help satisfy cellular ATP demand, permitting a reduced rate of respiratory substrate oxidation. In full sunlight, chloroplasts may rely on the mitochondrial electron transport chain (mETC) as an electron sink to oxidize photoreductant, limiting photoinhibition (Krömer, Stitt & Heldt 1988;Krömer & Heldt, 1991a;Saradadevi & Raghavendra 1992;Hurry et al 1996); (2) Biosynthesis of fatty acids, amino acids, phenolics and many other metabolites and compounds, requires NADPH, which in darkness is supplied by the chloroplastic oxidative pentose phosphate pathway (OPPP). Photosynthetically derived NADPH could satisfy these anabolic demands, permitting reduced CO2 release in the OPPP; (3) Photorespiration drives NADH production via Gly decarboxylation in mitochondria; subsequent reduction of hydroxypyruvate in peroxisomes also requires NADH, yet mitochondria seemingly meet less than half of that demand (Krömer & Heldt 1991b).…”

Section: Introductionmentioning

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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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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“…The controversy of whether or not mitochondrial respiration is occurring during photosynthesis has been long standing (16), and recent reports by Kromer and colleagues (20,21) working with barley (Hordeum vulgare) leaf protoplasts provide convincing evidence that mitochondrial ATP production is required for optimal photosynthesis. However, Budde and Randall (7,8) recently reported that the pea leaf mtPDC is primarily in an inactivated form in illuminated leaves and that photosynthesis was required for this inactivation to occur.…”

mentioning

confidence: 99%

“…Inactivation of the mtPDC, which is the primary point of entry for carbon into the Krebs cycle, could call into question whether the Krebs cycle is providing the reducing equivalents to drive mitochondrial ATP formation. Kromer and colleagues (20,21) did not establish the source of the reducing equivalents for oxidative phosphorylation in their experiments. Photorespiratory glycine to serine conversion in the mitochondria could easily provide sufficient NADH for oxidative phosphorylation, and, in fact, glycine has been shown to be the preferred substrate for leaf mitochondria (13).…”

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confidence: 99%

Light Regulation of Leaf Mitochondrial Pyruvate Dehydrogenase Complex

Gemel¹,

Randall²

1992

Plant Physiol.

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Light-dependent inactivation of mitochondrial pyruvate dehydrogenase complex (mtPDC) in pea (Pisum sativum L.) leaves was further characterized, and this phenomenon was extended to several monocot and dicot species. The light-dependent inactivation of mtPDC in vivo was rapidly reversed in the dark, even after prolonged illumination. The mtPDC can be efficiently cycled through the inactivated-reactivated status by rapid light-dark cycling. Light-dependent inactivation of mtPDC was shown to be suppressed by inhibitors of photorespiratory carbon metabolism, including 2-pyridylhydroxymethane sulfonate, isonicotinic acid hydrazide, and aminoacetonitrile, and by an inhibitor of photosynthesis, 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Glycine fed to pea leaf strips in the dark yielded partially inactivated leaf mtPDC, and this inactivation was blocked by inhibitors of glycine oxidation. It is concluded that the photorespiratory glycine to serine conversion that occurs in C3 leaf mitochondria can provide the NADH to drive oxidative phosphorylation and subsequent inactivation of mtPDC. Glycine oxidation also produces ammonium ion, which has been shown to enhance the inactivation of mtPDC in vitro by stimulating the pyruvate dehydrogenase kinase that catalyzes the phosphorylation (inactivation) of the mtPDC. Thus, light-dependent, photorespiration-stimulated inactivation of the mtPDC can regulate carbon entry into the Krebs cycle during C3 photosynthesis.The mtPDC2 links glycolytic carbon metabolism with the Krebs cycle by catalyzing the oxidative decarboxylation of pyruvate to acetyl-CoA. Pyruvate provides the primary substrate for the Krebs cycle, which, in turn, provides the reducing equivalents for ATP production by oxidative phosphorylation. for regulation of the mitochondrial complex through product feedback by NADH and acetyl-CoA (23) and inactivationreactivation by reversible phosphorylation (26,27). Plants are unique in having an additional isoform of PDC in their plastids (10, 11) that is also quite sensitive to product feedback regulation but does not undergo regulation by reversible phosphorylation (10,27). In vitro studies of the PDC kinase have also shown that the phosphorylation-inactivation reaction is stimulated by micromolar NH4+ (29) and is inhibited by pyruvate, the substrate for the PDC (26,30). In situ studies with purified pea leaf mitochondria have shown that the PDC phosphorylation status is increased when the mitochondria are oxidizing substrates other than pyruvate (6), in particular, glycine, an intermediate of the photorespiratory carbon oxidation pathway.The controversy of whether or not mitochondrial respiration is occurring during photosynthesis has been long standing (16), and recent reports by Kromer and colleagues (20, 21) working with barley (Hordeum vulgare) leaf protoplasts provide convincing evidence that mitochondrial ATP production is required for optimal photosynthesis. However, Budde and Randall (7,8) recently reported that the pea leaf mtPDC is primarily in an inactivate...

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Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell

Cited by 128 publications

References 11 publications

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

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

Light Regulation of Leaf Mitochondrial Pyruvate Dehydrogenase Complex

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Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell

Cited by 128 publications

References 11 publications

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis

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

Light Regulation of Leaf Mitochondrial Pyruvate Dehydrogenase Complex

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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