Measurements of the Engagement of Cyanide-Resistant Respiration in the Crassulacean Acid Metabolism Plant <i>Kalanchoë daigremontiana</i> with the Use of On-Line Oxygen Isotope Discrimination

Robinson, Sharon A.; Yakir, Dan; Ribas‐Carbó, Miquel; Giles, Larry; Osmond, C. B.; Siedow, James N.

doi:10.1104/pp.100.3.1087

Cited by 99 publications

(67 citation statements)

References 18 publications

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“…Engagement of the alternative pathway has been observed in response to increased anabolic demand resulting from salinity and drought (Wagner & Krab 1995), temperature (Gonzàlez-Meler et al 1999), illumination (Ribas-Carbo et al 2000b), wounding (Kinraide & Marek 1980) and during the de-acidi cation phase of Crassulacean acid metabolism (Robinson et al 1992), as well as in response to decreased phosphorylation via the cytochrome-c pathway resulting from cold stress (Ordentlich et al 1991;Gonzàlez-Meler et al 1999;Ribas-Carbo et al 2000a) and phosphorus de ciency (Parsons et al 1999). Other than in thermogenic tissues the function of the alternative oxidase is uncertain.…”

Section: Discussionmentioning

confidence: 99%

Application of an enthalpy balance model of the relation between growth and respiration to temperature acclimation ofEucalyptus globulusseedlings

Macfarlane

Adams

Hansen

2002

Proc. R. Soc. Lond. B

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The enthalpy balance model of growth uses measurements of the rates of heat and CO 2 production to quantify rates of decarboxylation, oxidative phosphorylation and net anabolism. Enthalpy conversion ef ciency (h H ) and the net rate of conservation of enthalpy in reduced biosynthetic products (R S G DH B ) can be calculated from metabolic heat rate (q) and CO 2 rate (R C O 2 ). h H is closely related to carbon conversion ef ciency and the ef ciency of conservation of available electrons in biosynthetic products. R S G DH B and h H can be used, together with biomass composition, to describe the rate and ef ciency of growth of plant tissues. q is directly related to the rate of O 2 consumption and the ratio q:R C O 2 is inversely related to the respiratory quotient.We grew seedlings of Eucalyptus globulus at 16 and 28°C for four to six weeks, then measured q and R C O 2 using isothermal calorimetry. Respiratory rate at a given temperature was increased by a lower growth temperature but h H was unaffected. Enthalpy conversion ef ciency-and, therefore, carbon conversion ef ciency-decreased with increasing temperature from 15 to 35°C. The ratio of oxidative phosphorylation to oxygen consumption (P/O ratio) was inferred in vivo from h H and by assuming a constant ratio of growth to maintenance respiration with changing temperature. The P/O ratio decreased from 2.1 at 10-15°C to less than 0.3 at 35°C, suggesting that decreased ef ciency was not only due to activity of the alternative oxidase pathway. In agreement with predictions from non-equilibrium thermodynamics, growth rate was maximal near 25°C, where the calculated P/O ratio was about half maximum. We propose that less ef cient pathways, such as the alternative oxidase pathway, are necessary to satisfy the condition of conductance matching whilst maintaining a near constant phosphorylation potential. These conditions minimize entropy production and maximize the ef ciency of mitochondrial energy conversions as growing conditions change, while maintaining adequate nite rates of energy processing.

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Section: Discussionmentioning

confidence: 99%

Application of an enthalpy balance model of the relation between growth and respiration to temperature acclimation ofEucalyptus globulusseedlings

Macfarlane

Adams

Hansen

2002

Proc. R. Soc. Lond. B

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“…The discrimination against 18 O associated with the cytochrome oxidase pathway is ϳ18‰ (Guy et al 1992), but with the cyanide-resistant alternative oxidase pathway (AOX) it is much greater: ϳ31‰ in green tissues and ϳ26‰ in nongreen tissues (Robinson et al 1992). The discrimination in the Mehler reaction is ϳ15‰ and in photorespiration ϳ21‰ (Berry 1992;Guy et al 1993).…”

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Evaluation of community respiratory mechanisms with oxygen isotopes: A case study in Lake Kinneret

Luz

Barkan

Sagi

et al. 2002

Limnology & Oceanography

125

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Gross and net O 2 production between May 1996 and February 1999 was determined in bottle incubation experiments with H 2 18 O spike and from the change in O 2 concentration. Carbon fixation rates were obtained from 14 C incubations. In general, production rates determined using the H 2 18 O-spike were about twice the primary production determined by the 14 C method, where the latter was close to net oxygen evolution. These relationships are similar to results for the open ocean. During the spring bloom, when the dinoflagellate Peridinium was abundant, the ratio of gross O 2 production to carbon fixation was about 7.5, and net O 2 production was greater than carbon fixation. The difference between O 2 gross production and carbon fixation results, at least in part, from uptake by Mehler reaction and from recycling of the 14 C tracer by dark respiration and the alternative oxidase (AOX). We used the difference in isotopic discrimination against 18 O, occurring during O 2 consumption by various biological pathways, to place constraints on the relative engagement of these pathways. We estimated the overall discrimination against 18 O in the lake from O 2 isotopic mass balance as 20.5-29‰. The only mechanism that can explain the strong overall fractionation in the lake is AOX, which strongly discriminates against 18 O (ϳ31‰). Our results show, for the first time, that uptake by AOX is widespread and quantitatively important to oxygen consumption in aquatic systems.Oxygen exchange by photosynthesis and respiration is the largest biogeochemical cycle in aquatic systems. In order to understand this cycle, it is necessary to know the gross rates of the major processes involved in oxygen production and uptake. Production of O 2 is known to occur in one process in photosystem II, but O 2 consumption in aquatic organisms is possible by several reactions. These include ordinary respiration through the cytochrome oxidase pathway, respiration by the alternative oxidase pathway, Mehler reaction, and photorespiration. The first two processes take place in light as well as in dark conditions, whereas the latter two occur only under illumination. Although the presence of the above mechanisms has been established in different studies, their quantitative importance in the overall O 2 uptake in aquatic systems is not well known, and it is necessary to assess their role in natural environments. In this respect, ordinary O 2 incubation methods, which are very useful for the assessment of photosynthetic production from light-and dark-incubation experiments (e.g., Williams and Purdie 1991), do not provide the necessary information. The main drawback of these methods is their inability to measure the rate of O 2 AcknowledgmentsWe thank Y. Geiffman and the Mekorot Watershed Unit for provision of wind data and extend special thanks to the Kinneret Limnological Laboratory skipper M. Hatab. We are grateful

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“…Currently, the only available method to measure the partitioning of electrons between the alternative and Cyt pathways in the absence of inhibitors is that of O,-isotope fractionation, which can be performed on intact tissue (Robinson et al, 1992 and on isolated mitochondria (Guy et al, 1989;Ribas-Carbo et al, 1995.…”

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The Effects of Salicylic Acid and Tobacco Mosaic Virus Infection on the Alternative Oxidase of Tobacco

et al. 1997

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Salicylic acid (SA) is a signal in systemic acquired resistance and an inducer of the alternative oxidase protein in tobacco (Nicofiana tabacum cv Xanthi nc) cell suspensions and during thermogenesis i n aroid spadices. The effects of SA on the levels of alternative oxidase protein and the pathogenesis-related l a mRNA (a marker for systemic acquired resistance), and on the partitioning of electrons between the Cyt and alternative pathways were investigated in tobacco. Leaves were treated with 1.0 mM SA and mitochondria isolated at times between 1 h and 3 d after treatment. Alternative oxidase protein increased 2.5-fold within 5 h, reached a maximum (9-fold) after 12 h, and remained at twice the level of control plants after 3 d. Measurements of isotope fractionation of '*O by intact leaf tissue gave a value of 23% at all times, identical to that of control plants, indicating a constant 27 to 30% of electron-flow partitioning to the alternative oxidase independent of treatment with SA. Transgenic NahC tobacco p!ants that express bacterial salicylate hydroxylase and possess very low levels of SA gave a fractionation of 23% and showed control levels of alternative oxidase protein, suggesting that steady-state alternative oxidase accumulates i n an SA-independent manner. lnfection of plants with tobacco mosaic virus resulted in an increase in alternative oxidase protein in both infected and systemic leaves, but no increase was observed in comparably infected NahC plants. Total respiration rate and partitioning of electrons to the alternative pathway in virus-infected plants was comparable to that in uninfected controls.

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Measurements of the Engagement of Cyanide-Resistant Respiration in the Crassulacean Acid Metabolism Plant Kalanchoë daigremontiana with the Use of On-Line Oxygen Isotope Discrimination

Cited by 99 publications

References 18 publications

Application of an enthalpy balance model of the relation between growth and respiration to temperature acclimation ofEucalyptus globulusseedlings

Application of an enthalpy balance model of the relation between growth and respiration to temperature acclimation ofEucalyptus globulusseedlings

Evaluation of community respiratory mechanisms with oxygen isotopes: A case study in Lake Kinneret

The Effects of Salicylic Acid and Tobacco Mosaic Virus Infection on the Alternative Oxidase of Tobacco

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