Abstract
When leaves of Helianthus annuus, whose stomates had been opened in the dark in the absence of CO2, were exposed to 25% carbon monoxide (CO), stomatal conductivity for water vapor decreased from about 0.4 to 0.2 cm·s-1. The CO effect on stomatal aperture required a CO/O2 ratio of about 25. As this ratio was decreased the stomata opened, indicating that inhibitio of cytochrome-c oxidase by CO is competitive in respect to O2. Photosynthetically active red light was unable to reverse CO-induced stomatal closure even at high irradiances, when CO2 was absent. When it was present, stomatal opening was occasionally, but not consistently observed. Carbon monoxide did not inhibit photosynthetic carbon reduction in leaves of Helianthus.
In contrast to red light, very weak blue light (405 nm) increased the stomatal aperture in the presence of CO. It also increased leaf ATP/ADP ratios which had been decreased in the presence of CO. The blue-light effect was not related to photosynthesis. Neither could it be explained by photodissociation of the cytochrome a 3-CO complex which has an absorption maximum at 430 nm. The data indicate that ATP derived from mitochondrial oxidative phosphorylation provides energy for stomatal opening in sunflower leaves in the dark as well as in the light. Indirect transfer of ATP from chloroplasts to the cytosol via the triose phosphate/phosphoglycerate exchange which is mediated by the phosphate translocator of the chloroplast envelope can support stomatal opening only if metabolite concentrations are high enough for efficient shuttle transfer of ATP. Blue light causes stomatal opening in the presence of CO by stimulating ATP synthesis.
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Assmann, S.M., Simonici, L., Schroeder, J.I. (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of vicia faba. Nature 318, 285–287
Brooks, A., Farquhar, G.D. (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406
Chance, B. (1953a) The carbon monoxide compounds of the cytochrome oxidases. I. Difference spectra. J. Biol. Chem. 202, 383–396
Chance, B. (1953b) The carbon monoxide compounds of the cytochrome oxidases. II. Photodissociation spectra. J. Biol. Chem. 202, 397–416
Chance, B., Erecinska, M. (1971) Flow flash kinetics of the cytochrome a 3-oxygen reaction in coupled and uncoupled mitochondria using the liquid dye laser. Arch. Biochem. Biophys. 143, 675–687
Dennis, M., Richaud, P. (1985) Cytochrome c oxidase in plant mitochondria. Electron transfer after flash photolysis at low temperature of the CO-bound half reduced complex. Eur. J. Biochem. 147, 533–539
Dietz, K.-J., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim. Biophys. Acta. 767, 432–443
Gardeström, P. (1987) Adenylate ratios in the cytosol, chloroplasts and mitochondria of barley leaf protoplasts during photosynthesis at different carbon dioxide concentrations. FEBS Lett. 212, 114–118
Gerhardt, R., Stitt, M., Heldt, H.W. (1987) Subcellular metabolite levels in spinach leaves. Regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol. 83, 399–407
Hampp, R. (1985) Luminometric methods: ADP, AMP. In: Methods of enzymatic analysis, vol. VII: Metabolites 3, 3rd edn., pp. 370–379, Bergmeyer, H.U., Bergmeyer, J., Grabl, M., eds. VCH-Verlagsgesellschaft Weinheim
Hampp, R., Goller, M., Ziegler, H. (1982) Regulation of the cytosolic adenylate ratio as determined by rapid fractionation of mesophyll protoplasts of oat. Planta 156, 255–263
Heber, U., Heldt, H.W. (1981) The chloroplast envelope: Structure, function and role in leaf metabolism. Annu. Rev. Plant Physiol. 32, 139–168
Heber, U., Neimanis, S., Lange, O.L. (1986) Stomatal aperture, photosynthesis and water fluxes in mesophyll cells as affected by the abscission of leaves. Simultaneous measurements of gas exchange, light scattering and chlorophyll fluorescnece. Planta 167, 554–562
Heber, U., Santarius, K.A. (1970) Direct and indirect transport of ATP and ADP across the chloroplast envelope. Z. Naturforsch. 25b, 718–728
Iino, M., Ogawa, T., Zeiger, E. (1985) Kinetic properties of the blue light response of stomata. Proc. Natl. Acad. Sci. USA 82, 8019–8023
Krömer, S., Stitt, M., Heldt, H.W. (1988) Mitochondrial oxidative phosphorylation participating in photosynthesis metabolism of a leaf cell. FEBS Lett. 226, 352–356
Laisk, A., Oja, V., Kiirats, O., Raschke, K., Heber, U. (1989) The state of the photosynthetic apparatus in leaves as analyzed by rapid gas exchange and optical methods: The pH of the chloroplast stroma and activation of enzymes in vivo. Planta, in press
Mansfield, T.A. (1985) Porosity at a price. The control of stomatal conductance in relation to photosynthesis. In: Topics in photosynthesis, vol. 6: Photosynthetic mechanisms and the environment, pp. 419–452, Barber, J., Bauer, N.R., eds. Elsevier, Amsterdam New York Oxford
Naik, M.S., Nicholas, D.J.D. (1986) Carbon monoxide sensitivity of cytochrome oxidase in wheat leaves in relation to dwarfing genes (Rht) in wheat cultivars. Theor. Appl. Genet. 72, 735–736
Nobel, P.S. (1983) Biophysical plant physiology and ecology. W.H. Freeman, San Francisco
Ogawa, T., Grantz, D., Boyer, J., Govindjee (1982) Effects of cations and abscisic acid on chlorophyll fluorescence. Plant Physiol. 69, 1140–1144
Osmond, C.B., Oja, V., Laisk, A. (1988) Regulation of carboxylation and photosynthetic oscillations during sun-shade acclimation in Helianthus annuus measured with a rapid-response gas exchange system. Aust. J. Plant Physiol. 15, 239–251
Outlaw, W.H., Jr., Manchester, J., Dicamelli, C.A., Randall, D.D., Rapp, B., Veith, G.M. (1979) Photosynthetic carbon reduction pathway is absent in chloroplasts of Vicia faba guard cells. Proc. Natl. Acad. Sci. USA 76, 6371–6375
Outlaw, W.H., Mayne, B.C., Zenger, V.E., Monchester, J. (1981) Presence of both photosystems in guard cells of Vicia faba L. Plant Physiol. 67, 12–16
Peisker, M., Apel, P. (1980) Dark respiration and the effect of oxygen on CO2 compensation concentration in wheat leaves. Z. Pflanzenphysiol. 100, 389–395
Raschke, K. (1979) Movements of stomata. In: Encyclopedia of plant physiology, N.S., vol. 7: Physiology of movements, pp. 383–441, Haupt, W., Feinleib, M.E., eds. Springer, Berlin Heidelberg New York
Ruyters, G. (1980) Blue light-effects on enzymes of the carbohydrate metabolism in Chlorella: 1. Pyruvate kinase. In: The blue light syndrome, pp. 361–367, Senger, H., ed Springer, Berlin Heidelberg New York
Santarius, K.A., Heber, U. (1965) Changes in the intracellular levels of ATP, ADP, AMP and P, and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim. Biophys. Acta. 100, 39–54
Schnabl, H., Michalke, B. (1989) The role of oxidative phosphorylation in stomatal opening. Adenylate pool sizes in light- and dark-treated swelling guard cell protoplasts. Life Sci. Adv.-Plant Physiol, vol. 7, in press
Schwartz, A., Zeiger, E. (1984) Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation. Planta 161, 129–139
Sharpe, R.E., Matthews, M.A., Boyer, J.S. (1984) Kok effect and the quantum yield of photosynthesis: Light partially inhibits dark respiration. Plant Physiol. 75, 95–101
Stitt, M., Lilley, R. McC., Heldt, H.W. (1982) Adenine nucleotide levels in the cytosol, chloroplasts and mitochondria of wheat leaf protoplasts. Plant Physiol. 70, 971–977
Walker, D.A., Sivak, M.N., Prinsley, R.T., Cheesbrough, J.K. (1983) Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol. 73, 542–549
Wulff, K., Döppen, W. (1985) Luminometric methods. ATP. In: Methods of enzymatic analysis, vol. VII: Metabolites 2, 3. Aufl., pp. 340–360, Bergmeyer, H.U., Bergmeyer, J., Grabl, M., eds. VCH-Verlagsgesellschaft, Weinheim
Zeiger, E. (1983) The biology of stomatal guard cells. Annu. Rev. Plant Physiol. 34, 441–475
Zeiger, E., Armond, P., Melis, A. (1981) Fluorescence properties of guard cell chloroplasts. Plant Physiol. 67, 17–20
Zeiger, E., Iino, M., Ogawa, T. (1985) The blue light response of stomata: Pulse kinetics on some mechanistic implications. Photochem. Photobiol. 42, 759–763
Zemel, E., Gepstein, S. (1985) Immunological evidence for the presence of ribulose bisphosphate carboxylase in guard cell chloroplasts. Plant Physiol. 78, 586–590
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Pollok, M., Heber, U. & Naik, M.S. Inhibition of stomatal opening in sunflower leaves by carbon monoxide, and reversal of inhibition by light. Planta 178, 223–230 (1989). https://doi.org/10.1007/BF00393198
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DOI: https://doi.org/10.1007/BF00393198