Adenosine Triphosphate/metabolism; Carbon Dioxide/metabolism; Electron Transport/physiology; Electron Transport Complex I/genetics/metabolism; Light; Membrane Potential, Mitochondrial; Mitochondria/metabolism; Photochemistry; Photosynthesis; Plant Leaves/metabolism/radiation effects; Tobacco/radiation effects
Abstract :
[en] The relationship between the development of photoprotective mechanisms (non-photochemical quenching, NPQ), the generation of the electrochemical proton gradient in the chloroplast and the capacity to assimilate CO(2) was studied in tobacco dark-adapted leaves at the onset of illumination with low light. These conditions induce the generation of a transient NPQ, which relaxes in the light in parallel with the activation of the Calvin cycle. Wild-type plants were compared with a CMSII mitochondrial mutant, which lacks the respiratory complex I and shows a delayed activation of photosynthesis. In the mutant, a slower onset of photosynthesis was mirrored by a decreased capacity to develop NPQ. This correlates with a reduced efficiency to reroute electrons at the PSI reducing side towards cyclic electron flow around PSI and/or other alternative acceptor pools, and with a smaller ability to generate a proton motive force in the light. Altogether, these data illustrate the tight relationship existing between the capacity to evacuate excess electrons accumulated in the intersystem carriers and the capacity to dissipate excess photons during a dark to light transition. These data also underline the essential role of respiration in modulating the photoprotective response in dark-adapted leaves, by poising the cellular redox state.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Jensen R.G., and Bassham J.A. Photosynthesis by isolated chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 56 (1966) 1095-1101
Bennoun P. Chlororespiration: sixteen years later. In: Rochaix J.-D., Goldschmidt-Clermont M., and Merchant S. (Eds). The Molecular Biology of Chloroplast and Mitochondria in Chlamydomonas (1998), Kluwer Academic Publishers. Dordrecht, The Netherlands 529-537
Peltier G., and Cournac L. Chlororespiration. Annu. Rev. Plant Biol. 53 (2002) 523-550
Krömer S. Respiration during photosynthesis. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 46 (1995) 45-70
Hoefnagel M.H.N., Atkin O.K., and Wiskich J.T. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta 1366 (1998) 235-255
Gardeström P., Igamberdiev A.U., and Raghavendra A.S. Mitochondrial functions in the light and significance to carbon-nitrogen interactions. In: Foyer C.H., and Noctor G. (Eds). Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in Photosynthesis vol. 12 (2002), Kluwer Academic Press, Dordrecht, the Netherlands 151-172
Fridlyand L.E., Backhausen J.E., and Scheibe R. Flux control of the malate valve in leaf cells. Arch. Biochem. Biophys. 349 (1998) 290-298
Krömer S., Stitt M., and Heldt H.W. Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell. FEBS Lett. 226 (1988) 352-356
Krömer S., Malmberg G., and Gardeström P. Mitochondrial contribution to hotosynthetic metabolism. A study with barley (Hordeum vulgare L.) leaf protoplasts at different light intensities and CO2 concentrations. Plant Physiol. 102 (1993) 947-955
Douce R., and Neuburger M. The uniqueness of plant mitochondria. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40 (1989) 371-414
Gutierres S., Sabar M., Lelandais C., Chétrit P., Diolez P., Degand H., Boutry M., Vedel F., de Kouchkovsky Y., and De Paepe R. Lack of mitochondrial and nuclear encoded subunits of complex I and alteration of respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 3436-3441
Sabar M., De Paepe R., and de Kouchkovsky Y. Complex I impairment, respiratory compensations and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol. 124 (2000) 1239-1250
Noctor G., Dutilleul C., De Paepe R., and Foyer C.H. Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J. Exp. Bot. 55 (2004) 49-57
Noctor G., De Paepe R., and Foyer C.H. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12 (2007) 125-134
Dutilleul C., Garmier M., Noctor G., Mathieu C., Chétrit P., Foyer C.H., and de Paepe R. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15 (2003) 1212-1226
Dutilleul C., Lelarge C., Prioul J.L., De Paepe R., Foyer C.H., and Noctor G. Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol. 139 (2005) 64-78
Priault P., Fresneau C., Noctor G., De Paepe R., Cornic G., and Streb P. The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance. J. Exp. Bot. 57 (2006) 2075-2085
Dutilleul C., Driscoll S., Cornic G., De Paepe R., Foyer C.H., Noctor G., and Functional mitochondrial complex I. is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol. 131 (2003) 264-275
Ort D.R., and Baker N.R. A photoprotective role for O2 as an alternative electron sink in photosynthesis?. Curr. Opin. Plant Biol. 5 (2002) 193-198
Johnson G.N. Cyclic electron transport in C3 plants: fact or artefact?. J. Exp. Bot. 56 (2005) 407-416
Joliot P., and Joliot A. Cyclic electron flow in C3 plants. Biochim. Biophys. Acta 1757 (2006) 362-368
Mehler A.M. Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33 (1951) 65-77
Noguchi K., and Yoshida K. Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8 (2008) 87-99
Horton P., Ruban A.V., and Walters R.G. Regulation of light harvesting in green plants. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 47 (1996) 655-684
Demmig-Adams B., Gilmore A.M., and Adams W.W. Carotenoids 3: in vivo function of carotenoids in higher plants. Faseb J. 10 (1996) 403-412
Aro E.M., Virgin I., and Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143 (1993) 113-134
Dall'Osto L., Caffarri S., and Bassi R. A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17 (2005) 1217-1232
Allen J.F. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098 (1992) 275-335
Wraight C.A., and Crofts A.R. Energy-dependent quenching of chlorophyll alpha fluorescence in isolated chloroplasts. Eur. J. Biochem. 17 (1970) 319-327
Baroli I., and Niyogi K.K. Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 (2000) 1385-1394
Holt N.E., Fleming G.R., and Niyogi K.K. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43 (2004) 8281-8289
Demmig-Adams B., Adams W.W., Heber U., Neimanis S., Winter K., Krüger A., Czygan F.C., Bilger W., and Björkman O. Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol. 92 (1990) 293-301
Yamamoto H.Y., Nakayama T.O., and Chichester C.O. Studies on the light and dark interconversions of leaf xanthophylls. Arch. Biochem. Biophys. 97 (1962) 168-173
Li X.P., Björkman O., Shih C., Grossman A.R., Rosenquist M., Jansson M.S., and Niyogi K.K. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 (2000) 391-395
Li X.P., Gilmore A.M., Caffarri S., Bassi R., Golan T., Kramer D., and Niyogi K.K. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279 (2004) 22866-22874
Finazzi G., Johnson G.N., Dall'Osto L., Joliot P., Wollman F.A., and Bassi R. A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc. Natl. Acad. Sci U. S. A. 101 (2004) 12375-12380
Crouchman S., Ruban A.V., and Horton P. PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett. 580 (2006) 2053-2058
Kalituho L., Beran K.C., and Jahns P. The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol. 143 (2007) 1861-1870
Munekage Y., Hojo M., Meurer J., Endo T., Tasaka M., and Shikanai T. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110 (2002) 361-371
Golding A.J., and Johnson G.N. Down regulation of linear and activation of cyclic electron transport during drought. Planta 218 (2003) 107-114
Miyake C., Miyata M., Shinzaki Y., and Tomizawa K. CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves. Relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol. 46 (2005) 629-637
Melkonian J., Wolfe D.W., and Owens T.G. Effects of elevated carbon dioxide on gas exchange and photochemical and nonphotochemical quenching at low temperature in tobacco plants varying in Rubisco activity. Photosynth. Res. 83 (2005) 63-74
Külheim C., Agren J., and Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 297 (2002) 91-93
Kramer D.M., Cruz J.A., and Kanazawa A. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8 (2003) 27-32
Takizawa K., Cruz J.A., Kanazawa A., and Kramer D.M. The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim. Biophys. Acta 1767 (2007) 1233-1244
Joliot P., Béal D., and Joliot A. Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim. Biophys. Acta 1656 (2004) 166-176
Breyton C., Nandha B., Johnson G.N., Joliot P., and Finazzi G. Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45 (2006) 13465-13475
Siefermann D., and Yamamoto H.Y. Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts: a transmembrane model for the violaxanthin cycle. Arch. Biochem. Biophys. 171 (1975) 70-77
Heber U. Conformational changes of chloroplasts induced by illumination of leaves in vivo. Biochim. Biophys. Acta 180 (1969) 302-319
Avenson T.J., Cruz J.A., and Kramer D.M. Modulation of energy-dependent quenching of excitons in antennae of higher plants. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 5530-5535
Cardol P., Gloire G., Havaux M., Remacle C., Matagne R., and Franck F. Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol. 133 (2003) 2010-2020
Von Jagow G., and Link T.A. Use of specific inhibitors on mitochondrial bc1 complex. Methods Enzymol. 126 (1986) 253-271
Genty B., Harbinson J., Briantais J.-M., and Baker N.R. The relationship between non-photochemical quenching of chlorophyll fluorescence and the rate of photosystem 2 photochemistry in leaves. Photosynth. Res. 25 (1990) 249-257
Briantais J.M., Vernotte C., Picaud M., and Krause G.H. A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim. Biophys. Acta 548 (1979) 128-138
Witt H.T. Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochim. Biophys. Acta 505 (1979) 355-427
Cruz J.A., Sacksteder C.A., Kanazawa A., and Kramer D.M. Contribution of electric field (ΔΨ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into ΔΨ and ΔpH by ionic strength. Biochemistry 40 (2001) 1226-1237
Joliot P., and Joliot A. Cyclic electron transfer in plant leaf. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10209-10214
Allen J.F. Photosynthesis of ATP-electrons, proton pumps, rotors, and poise,. Cell 110 (2002) 273-276
Heber U., and Walker D. Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol. 100 (1992) 1621-1626
Liu Y.J., Norberg F.E., Szilágyi A., De Paepe R., Akerlund H.E., and Rasmusson A.G. The mitochondrial external NADPH dehydrogenase modulates the leaf NADPH/NADP+ ratio in transgenic Nicotiana sylvestris. Plant Cell Physiol. 49 (2008) 251-263
Joliot P., and Joliot A. Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4913-4918
Nandha B., Finazzi G., Joliot P., Hald S., and Johnson G.N. The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim. Biophys. Acta 1767 (2007) 1252-1259
DalCorso G., Pesaresi P., Masiero S., Aseeva E., Schünemann D., Finazzi G., Joliot P., Barbato R., and Leister D. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132 (2008) 273-285
Siebke K., Laisk A., Neimanis S., and Heber U. Evidence that NADP-dependent glyceraldehydephosphate dehydrogenase, but not ferredoxin-NADP reductase, controls electron flow to phosphoglycerate in the dark-light transition. Planta 185 (1991) 337-343
Joët T., Genty B., Josse E.M., Kuntz M., Cournac L., and Peltier G. Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem. 277 (2002) 31623-31630
Avenson T.J., Cruz J.A., Kanazawa A., and Kramer D.M. Regulating the proton budget of higher plant photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 9709-9713
Laisk A., Eichelmann H., Oja V., Talts E., and Scheibe R. Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol. 48 (2007) 1575-1588
Scheibe R. R, NADP-malate dehydrogenase in C3 plants: regulation and role of a light-activated enzyme. Physiol. Plant. 71 (1987) 393-400
Schansker G., Tóth S.Z., and Strasser R.J. Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim. Biophys. Acta 1706 (2005) 250-261
Bennoun P. Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 4352-4356
Gilmore A.M., and Yamamoto H.Y. Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1899-1903
Diner B., and Joliot P. Effect of the transmembrane electric field on the photochemical and quenching properties of photosystem II in vivo. Biochim. Biophys. Acta 423 (1976) 479-498
Joliot P., and Joliot A. Quantification of the electrochemical proton gradient and activation of ATP synthase in leaves. Biochim. Biophys. Acta 1777 (2008) 676-683
Pfundel E.E., Renganathan M., Gilmore A.M., Yamamoto H.Y., and Dilley R.A. Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin deepoxidation. Plant. Physiol. 106 (1994) 1647-1658
Bulté L., Gans P., Rebeillé F., and Wollman F.A. ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020 (1990) 72-80
Forti G., Furia A., Bombelli P., and Finazzi G. In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii. Plant Physiol. 132 (2003) 1464-1474
Finazzi G., and Rappaport F. In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetics effects on the cytochrome b6f turnover. Biochemistry 37 (1998) 9999-10005
Szal B., Dabrowska Z., Malmberg G., Gardeström P., and Rychter A.M. Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement. Planta 227 (2008) 697-706
Priault P., Vidal G., De Paepe R., and Ribas-Carbo M. Leaf age-related changes in respiratory pathways are dependent on Complex I activity in Nicotiana sylvestris. Physiol. Plant 139 (2007) 64-78
Vidal G., Ribas-Carbo M., Garmier M., Dubertret G., Rasmusson A.G., Mathieu C., Foyer C.H., and De Paepe R. Lack of respiratory chain Complex I impairs AOX engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 19 (2007) 640-655
Stitt M., Lilley R.M., and Heldt H.W. Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol. 70 (1982) 971-977
Krömer S., and Heldt H.W. On the role of mitochondrial oxidative phosphorylation in photosynthesis metabolism as studied by the effect of oligomycin on photosynthesis in protoplasts and leaves of barley (Hordeum vulgare). Plant. Physiol. 95 (1991) 1270-1276
Gardeström P., and Wigge B. Influence of photorespiration on ATP/ADP ratios in the chloroplasts, mitochondria, and cytosol, studied by rapid fractionation of Barley (Hordeum vulgare) protoplasts. Plant Physiol. 88 (1988) 69-76
Junge W., Rumberg B., and Schröder H. the necessity of an electric potential difference and its use for photophosphorylation in short flash groups. Eur. J. Biochem. 14 (1970) 575-581
Weis E., and Berry J. Quantum efficiency of photosystem II in relation to energy-dependent quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 894 (1987) 198-208
Palatnik J.F., Tognetti V.B., Poli H.O., Rodríguez R.E., Blanco N., Gattuso M., Hajirezaei M.R., Sonnewald U., Valle E.M., and Carrillo N. Transgenic tobacco plants expressing antisense ferredoxin-NADP(H) reductase transcripts display increased susceptibility to photo-oxidative damage. Plant J. 35 (2003) 332-341
Horton P., Ruban A.V., and Wentworth M. Allosteric regulation of the light-harvesting system of photosystem II. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 (2000) 1361-1370
Kalituho L., Rech J., and Jahns P. The roles of specific xanthophylls in light utilization. Planta 225 (2007) 423-439
Kanazawa A., and Kramer D.M. In vivo modulation of non photochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 12789-12794
Cruz J.A., Avenson T.J., Kanazawa A., Takizawa K., Edwards G.E., and Kramer D.M. Plasticity in light reactions of photosynthesis for energy production and photoprotection. J. Exp. Bot. 56 (2005) 395-406
Foyer C.H., Lelandais M., and Harbinson J. Control of the quantum efficiencies of photosystems I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves. Plant Physiol. 99 (1992) 979-986
Butler W.L. Energy distribution in the photochemical apparatus of photosynthesis. Annu. Rev. Plant Physiol. 29 (1978) 345-378
Bilger W., and Björkman O. Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 25 (1990) 173-186
