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RESEARCH ARTICLE
Contents Vol 34(2)

Contrasting responses by respiration to elevated CO2 in intact tissue and isolated mitochondria

Dan Bruhn A B C , Joseph T. Wiskich D and Owen K. Atkin A E
+ Author Affiliations
- Author Affiliations

A Department of Biology, The University of York, PO Box 373, York YO10 5YW, UK.

B Risø National Laboratory, Plant Research Department, Building 309, PO Box 49, DK-4000, Denmark.

C Present address: Plant and Soil Science Laboratory, Department of Agricultural Sciences, Faculty of Life Science, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark.

D School of Biological Sciences, Flinders University of South Australia, SA 5042, Australia.

E Corresponding author. Email: OKA1@york.ac.uk

Functional Plant Biology 34(2) 112-117 https://doi.org/10.1071/FP06247
Submitted: 3 October 2006  Accepted: 6 December 2006   Published: 12 February 2007

Abstract

The question of whether elevated concentrations of CO2 directly inhibit mitochondrial respiration in plants has received considerable attention. Although there is a growing consensus that elevated [CO2] rarely inhibits respiration of intact tissues, past studies have reported that elevated [CO2] does impact on O2 uptake in isolated mitochondria; what remains unclear, however, is the site(s) where elevated [CO2] impacts on mitochondrial electron transport (ETC). Here we investigated direct effects of [CO2] on respiratory activity of ETC enzymes, intact mitochondria and whole tissues using potato tubers (Solanum tuberosum L. cv. Desiree). Plots of O2 uptake against the redox poise of the ubiquinone (UQ) pool in isolated mitochondria were used to determine whether elevated [CO2] inhibits UQ-reducing and UQ-oxidising pathways differentially. Our results show that mitochondrial respiration was more inhibited via [CO2]/[HCO3–] effects on cytochrome c oxidase (COX) than on succinate dehydrogenase, with [HCO3–] rather than [CO2] inhibiting COX. However, the inhibitory effects at the mitochondrial level did not translate into inhibitory effects at the tissue level. Alternative oxidase (AOX) activity is normally absent in young potato tubers, as was the case in the present study. Thus, the lack of CO2-mediated inhibition at the tissue level was not the result of increases in AOX activity masking the effects of CO2 elsewhere in the respiratory system. We discuss whether the direct impact of elevated [CO2] on respiration is dependent on the rate of metabolic activity and flux control coefficients in individual tissues.


Acknowledgements

DB was supported by the Nordic Academy of Advanced Study, the Danish Research Agency and the Danish Research Training Council. The financial support of a UK Natural Environment Research Council Grant GR8/04360 (to OKA) and an Australian Research Council Grant (to JTW) is acknowledged.


References


Amthor JS (1991) Respiration in a future, higher-CO2 world. Plant, Cell and Environment 14, 13–20.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Amthor JS (1997) Plant respiratory responses to elevated carbon dioxide partial pressure. In ‘Advances in carbon dioxide effects research’. (Eds LH Allen Jr, MB Kirkham, DM Olszyk, CE Whitman) pp. 35–77. (American Society of Agronomy: Madison, WI)

Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornely respiration paradigms: 30 years later. Annals of Botany 86, 1–20.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Atkin OK, Zhang Q, Wiskich JT (2002) Effect of temperature on rates of alternative and cytochrome pathway respiration and their relationship with the redox pose of the quinone pool. Plant Physiology 128, 212–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bendall DS, Ranson SL, Walker DA (1960) Effects of carbon dioxide on the oxidation of succinate and reduced diphosphopyridine nucleotide by Ricinus mitochondria. Biochemical Journal 76, 221–225.
| PubMed |
open url image1

Bruhn D, Mikkelsen TN, Atkin OK (2002) Does the direct effect of atmospheric CO2 concentration on leaf respiration vary with temperature? Responses in two species of Plantago that differ in relative growth rate. Physiologia Plantarum 114, 57–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bunce JA (2004) A comparison of the effects of carbon dioxide concentration and temperature, translocation and nitrate reduction in darkened soybean leaves. Annals of Botany 93, 665–669.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chapman KSR, Hatch MD (1977) Regulation of mitochondrial NAD-malic enzyme involved in C4 pathway photosynthesis. Archives of Biochemistry and Biophysics 184, 298–306.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Covey-Crump EM, Bykova NV, Affourtit C, Hoefnagel MHN, Gardeström P, Atkin OK (2007) Temperature-dependent changes in respiration rates and redox poise of the ubiquinone pool in protoplasts and isolated mitochondria of potato leaves. Physiologia Plantarum 129, 175–184.
| Crossref |
open url image1

Cramer MD, Richards MB (1999) The effect of rhizophere dissolved inorganic carbon on gas exchange characteristic and growth rates of tomato seedling. Journal of Experimental Botany 50, 79–87.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Day DA, Neuberger M, Douce R (1985) Biochemical characterisation of chlorophyll-free mitochondria from pea leaves. Australian Journal of Plant Physiology 12, 219–228. open url image1

Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Drake BG, Azcon-Bieto J, Berry J, Bunce J, Dijkstra P , et al. (1999) Does elevated atmospheric CO2 concentration inhibit mitochondrial respiration in green plants. Plant, Cell and Environment 22, 649–657.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Geiger M, Stitt M, Geigenberger P (1998) Metabolism in slices from growing potato tubers responds differently to addition of sucrose and glucose. Planta 206, 234–244.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Gifford RM (2004) The CO2 fertilising effect – does it occur in the real world? The International Free Air CO2 Enrichment (FACE) workshop: short- and long-term effects of elevated atmospheric CO2 on managed ecosystems, Ascona, Switzerland, March 2004. New Phytologist 163, 221–225.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Gonzàlez-Meler MA, Siedow JN (1999) Direct inhibition of mitochondrial respiratory enzymes by elevated CO2: does it matter at the tissue or whole-plant level. Tree Physiology 19, 253–259.
| PubMed |
open url image1

Gonzàlez-Meler MA, Ribas-Carbó M, Siedow JN, Drake BG (1996) Direct inhibition of plant mitochondrial respiration by elevated CO2. Plant Physiology 112, 1349–1355.
| PubMed |
open url image1

Gonzàlez-Meler MA, Taneva L, Trueman RJ (2004) Plant respiration and elevated atmospheric CO2 concentration: cellular response and global significance. Annals of Botany 94, 647–656.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Grace J (2004) Understanding and managing the global carbon cycle. Journal of Ecology 92, 189–202.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Gunes G, Watkins CB, Hotchkiss JH (2001) Physiological responses of fresh-cut apple slices under high CO2 and low O2 partial pressures. Postharvest Biology and Technology 22, 197–204.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hoefnagel MHN, Miller AH, Wiskich JT, Day DA (1995) Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria. Archives of Biochemistry and Biophysics 318, 394–400.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hole CC (1977) The effect of a reduction in carbon dioxide concentration on the loss of carbon dioxide from pea fruits. Annals of Botany 41, 1367–1370. open url image1

IPCC (2001) ‘Climate change 2001: the scientific basis. Contribution of Working Group I to the third assessment report of the Intergovernmental Panel on Climate Change.’ (Eds JT Houghton, D Ding, DJ Griggs, M Noguer, PJ van der Linden, X Dai, K Maskell, CA Johnson) (Cambridge University Press: Cambridge)

Lambers H , Chapin FS III , Pons TJ (1998) ‘Plant physiological ecology.’ (Springer: New York)

Levy PE, Meir P, Allen SJ, Jarvis PG (1999) The effect of aqueous transport of CO2 in xylem sap on gas exchange in woody plants. Tree Physiology 19, 53–58.
| PubMed |
open url image1

Lowry OH, Rosenbrough HJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.
| PubMed |
open url image1

Moore AL, Dry IB, Wiskich JT (1988) Measurement of the redox state of the ubiquinone pool in plant-mitochondria. FEBS Letters 235, 76–80.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Neuburger M, Douce R (1980) Effect of bicarbonate and oxaloacetate on malate oxidation by spinach leaf mitochondria. Biochimica et Biophysica Acta 589, 176–189.
| PubMed |
open url image1

Neuburger M, Journet E-P, Bligny R, Carde J-P, Douce R (1982) Purification of plant mitochondria by isopycnic centrifugation in density gradients of percoll. Archives of Biochemistry and Biophysics 217, 312–323.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Palet A, Ribas-Carbó M, Argilés JM, Azcón-Bieto J (1991) Short-term effects of carbon dioxide on carnation callus cell respiration. Plant Physiology 96, 467–472.
| PubMed |
open url image1

Ranson SL, Walker DA, Clarke ID (1960) Effects of carbon dioxide on mitochondrial enzymes from Ricinus. Biochemical Journal 76, 216–221.
| PubMed |
open url image1

Sands R, Nugroho PB, Leung DWM, Sun OJ, Clinton PW (2000) Changes in soil CO2 and O2 concentrations when radiata pine is grown in competition with pasture or weeds and possible feedbacks with radiata prine root growth and respiration. Plant and Soil 225, 213–225.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Theologis A, Laties GG (1978) Relative contribution of cytochrome-mediated and cyanide-resistant electron transport in fresh and aged potato slices. Plant Physiology 62, 232–237.
| PubMed |
open url image1

Valentini R, Matteucci G, Dolman AJ, Schulze E-D, Rebmann C , et al. (2000) Respiration as the main determinant of carbon balance in European forests. Nature 404, 861–865.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1