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Does Elevated Atmospheric CO2 Concentration Inhibit Mitochondrial Respiration in Green Plants?

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Does Elevated Atmospheric CO2 Concentration Inhibit Mitochondrial Respiration in Green Plants? Plant, Cell and Environment (1999) 22, 649–657 ORIGINAL ARTICLE OA 220 EN Does elevated atmospheric CO2 concentration inhibit mitochondrial respiration in green plants? B. G. DRAKE1, J. AZCON-BIETO2, J. BERRY3, J. BUNCE4, P. DIJKSTRA1, J. FARRAR5, R. M. GIFFORD6, M. A. GONZALEZ-MELER7, G. KOCH8, H. LAMBERS9, J. SIEDOW10 & S. WULLSCHLEGER11 1Smithsonian Environmental Research Center, PO Box 28, Edgewater, MD 21037, USA; 2Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, Spain; 3Department of Plant Biology Carnegie Institution of Washington, 260 Panama Street, Stanford, CA 94305, USA; 4USDA/ARS, Climate Stress Laboratory, 10300 Baltimore Avenue, Beltsville, MD 20705, USA; 5School of Biological Sciences, University College of North Wales, Bangor, Gwynedd LL57 2UW, UK; 6CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia; 7Developmental, Cell and Molecular Biology Group/Botany Department, Duke University, PO Box 91000, Durham, NC 27708, USA; 8Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA; 9Department of Plant Ecology and Evolutionary Biology Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands; 10Dean of Faculty Development, 104 Allen Building, Duke University, Durham, NC, USA; 11Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA ABSTRACT respiration per unit DW [µmol g DW–1], Rubisco, ribulose- 1,5-bisphosphate carboxylase/oxygenase; Vc,max, maximum There is abundant evidence that a reduction in mitochon- –2 –1 in vivo rate of carboxylation at Rubisco (µmol m s ). drial respiration of plants occurs when atmospheric CO2 (Ca) is increased. Recent reviews suggest that doubling the present Ca will reduce the respiration rate [per unit INTRODUCTION dry weight (DW)] by 15 to 18%. The effect has two com- There have been indications in the literature of a direct ponents: an immediate, reversible effect observed in effect of elevated atmospheric CO2 concentration (Ca) par- leaves, stems, and roots of plants as well as soil microbes, tially suppressing higher plant respiration since the late and an irreversible effect which occurs as a consequence nineteenth century (Kidd 1916; Mangin 1896 quoted in of growth in elevated Ca and appears to be specific to C3 Murray 1995). Over the last 15 years such an effect has species. The direct effect has been correlated with inhibi- been frequently reported both as rapid reversible responses tion of certain respiratory enzymes, namely cytochrome- to elevated C , and as longer term responses measured on c-oxidase and succinate dehydrogenase, and the indirect a plants grown continuously at elevated Ca (reviewed in or acclimation effect may be related to changes in tissue Amthor 1997; Drake et al. 1997b; Curtis & Wang 1998). composition. Although no satisfactory mechanisms to Inhibition of respiration by elevated Ca has also been explain these effects have been demonstrated, plausible reported for microbial respiration (Drake et al. 1997b). mechanisms have been proposed and await experimental Mechanisms for this inhibition have not yet been demon- testing. These are carbamylation of proteins and direct strated unequivocally, the fast acting reversible response inhibition of enzymes of respiration. A reduction of foliar being particularly mystifying. If there is a significant effect respiration of 15% by doubling present ambient Ca of the globally rising Ca on higher plant or microbial respi- would represent 3 Gt of carbon per annum in the global ration rates then there are likely to be substantial implica- carbon budget. tions for the global carbon cycle and agricultural systems. To quantify the implications and understand them suffi- Key-words: acclimation to rising CO2; dark respiration; global ciently to allow a predictive capability, requires knowledge carbon cycle; rising CO2. not only of respiration and the exact character of the sup- Abbreviations: ATP, adenosine triphosphate; Km, Michaelis- pression, but also of the role of autotrophic and het- Menton coefficient; Ca, concentration of CO2 in the air erotrophic respiration in ecosystem processes. –1 (µmol mol–1); NAD, oxidized nicotin adenine dinucleotide; We use the term respiration (R, µmol g DW ) to mean NADH, reduced nicotin adenine dinucleotide; NADP, oxi- the consumption of O2 or the efflux of CO2 per unit dry dized nicotin adenine phosphate dinucleotide; NADPH, matter and we concentrate on effects observed when Ca is –1 reduced nicotine adenine phosphate dinucleotide; R, rate of in the range of 0–1000 µmol mol . Two kinds of effects of elevated Ca on apparent dark respiration in intact plants or Correspondence: B. G. Drake. tissues have been reported (Amthor 1991; Gonzàlez- This paper was prepared by the participants in a workshop held 8–9 Meler, Drake & Azcon-Bieto 1996a; Drake et al. 1997b): a January 1998 at the Smithsonian Environmental Research Center, direct, immediate effect in which respiration is reversibly Edgewater, Maryland, 21037 USA. reduced by exposure to elevated Ca, and an indirect effect © 1999 Blackwell Science Ltd 649 650 B. G. Drake et al. in which respiration of plants grown in elevated Ca differs expressed on a dry-mass basis. In an expanded meta-anal- from the respiration of plants grown in normal ambient Ca ysis, Curtis & Wang (1998) reported that leaf respiration when measured at a common value of Ca. expressed on a dry-mass basis was reduced by 18% in In this paper, we review the data available on the effect woody plants grown at elevated Ca concentrations. of elevated Ca on respiration, discuss the potential bio- The analyses of Poorter et al. (1992), Curtis (1996), and chemical candidates for a mechanism whereby changes in Curtis & Wang (1998) did not attempt to separate the direct ambient Ca could bring about changes in the rate of respira- effects per se from the indirect effects which probably occur tion, and consider the potential effect of elevated Ca on as a result of acclimation of the plant to elevated Ca. Drake changes in construction, maintenance and transport costs. et al. (1997b) indicated an average 18% direct inhibition for With the aid of a model for the global carbon cycle, we foliage while Amthor’s (1997) analysis of 36 species in 45 evaluate the significance for the global carbon budget of studies reported 15% direct inhibition in shoots, leaves and reduced dark respiration in foliage. We also suggest roots due to a doubling of the Ca. Both Amthor (1997) and research goals for determining the mechanistic basis for Drake et al. (1997b) reported that the indirect effect was the impact of rising Ca on dark respiration of plants. smaller than the direct effect. The acclimation effect gener- ally results in reduced respiration (Baker et al. 1992; Azcón- Bieto et al. 1994), although in some experiments acclimation EVIDENCE FOR THE EFFECT OF ELEVATED led to increased respiration (Thomas et al. 1993). C ON RESPIRATION a Mechanisms suspected to be involved in the direct and An increasing number of studies have reported direct indirect effects (discussed below) include changes in car- and/or acclimation responses of higher plant respiration to bohydrate availability, growth rate and biomass allocation, Ca enrichment (Table 1). These responses have been altered chemical composition of tissues, interactions observed in leaves, whole-plants, roots and in the stems of between Ca and key respiratory enzymes, and dark CO2 woody plants (Gonzàlez-Meler et al. 1996a; Ryan et al. fixation (Amthor 1991). Other aspects of the responses that 1996; Wullschleger, Norby & Hanson 1995). have been explored include the effects of Ca on growth and Poorter et al. (1992), who produced the first quantita- maintenance respiration, the apparent paradox of increased tive analysis of data on the tissue-specific response of res- growth rate and reduced respiration (Bunce 1994) the piration to elevated Ca, reported both increases and potential interaction of nutrients and temperature in the decreases in leaf, root and whole-plant respiration as a responses to Ca (Wullschleger, Ziska & Bunce 1994) and result of exposure to elevated Ca. Estimated changes in the biochemical mechanisms involved in a direct effect of respiration due to elevated Ca averaged across 41 C3 and Ca on mitochondrial respiration (Gonzàlez-Meler, Drake & six C4 species ranged from a 16% stimulation of respira- Azcon-Bieto 1996a). tion when expressed on a leaf-area basis to a 14% inhibi- Is the effect of elevated Ca on respiration an artifact of sys- tion when expressed on a dry-mass basis. By contrast, tematic measurement errors? Two candidates for producing Curtis (1996) conducted a statistical meta-analysis of pub- systematic artifacts in gas exchange systems are dilution of lished data on leaf respiration for trees grown at elevated the air by transpired water vapour and leaks between the Ca and reported a significant reduction in respiration chamber and the surrounding air. Although each of these regardless of whether the data were expressed on a mass could, under certain conditions, produce an apparent reduc- or area basis. This analysis did support the basic conclu- tion in CO2 efflux, in most available studies, insufficient sion of Poorter et al. (1992) that the magnitude of the data are given to conclude whether or to what extent these effect was dependent on how the data were expressed, errors were necessarily a part of the experiment. Moreover, with the apparent elevated Ca-induced effects on area- no one has produced a convincing set of experiments based rates of respiration being only about half those accompanying measurements of respiration to permit us to conclude that these potential sources of artifacts are capable of causing the sort of errors needed to produce the effects Table 1. Estimates of the direct effect (E, %) of elevated Ca on R observed (only the direct effect is involved here since the in leaves of plants. E is expressed as the ratio of Re, the rate of indirect effect could only result from changes in the tissue as respiration measured in tissues grown and measured at elevated Ca, a result of growth in elevated Ca).
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