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First published online November 20, 2003; 10.1104/pp.103.028076

Plant Physiology 133:2010-2020 (2003)
© 2003 American Society of Plant Biologists

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BIOENERGETICS AND PHOTOSYNTHESIS

Photosynthesis and State Transitions in Mitochondrial Mutants of Chlamydomonas reinhardtii Affected in Respiration1

Pierre Cardol, Geoffrey Gloire2, Michel Havaux, Claire Remacle, René Matagne and Fabrice Franck*

Genetics of Microorganisms (P.C., G.C., C.R., R.M.) and Biochemistry and Photobiology (F.F.), Institute of Plant Biology B22, University of Liège, B-4000 Liège, Belgium; and Commissariat à l'Energie Atomique (CEA)/Cadarache, Direction des Sciences du Vivant, Département d'Ecophysiologie Végétale et de Microbiologie, Laboratoire d'Ecophysiologie de la Photosynthèse, Unité Mixte de Recherche 163 CEA Centre National de la Recherche Scientifique, Univ-Méditérranée CEA 1000, F-13108 Saint-Paul-lez-Durance, France (M.H.)

Photosynthetic activities were analyzed in Chlamydomonas reinhardtii mitochondrial mutants affected in different complexes (I, III, IV, I + III, and I + IV) of the respiratory chain. Oxygen evolution curves showed a positive relationship between the apparent yield of photosynthetic linear electron transport and the number of active proton-pumping sites in mitochondria. Although no significant alterations of the quantitative relationships between major photosynthetic complexes were found in the mutants, 77 K fluorescence spectra showed a preferential excitation of photosystem I (PSI) compared with wild type, which was indicative of a shift toward state 2. This effect was correlated with high levels of phosphorylation of light-harvesting complex II polypeptides, indicating the preferential association of light-harvesting complex II with PSI. The transition to state 1 occurred in untreated wild-type cells exposed to PSI light or in 3-(3,4-dichlorophenyl)-1,1-dimethylureatreated cells exposed to white light. In mutants of the cytochrome pathway and in double mutants, this transition was only observed in white light in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. This suggests higher rates of nonphotochemical plastoquinone reduction through the chlororespiratory pathway, which was confirmed by measurements of the complementary area above the fluorescence induction curve in dark-adapted cells. Photo-acoustic measurements of energy storage by PSI showed a stimulation of PSI-driven cyclic electron flow in the most affected mutants. The present results demonstrate that in C. reinhardtii mutants, permanent defects in the mitochondrial electron transport chain stabilize state 2, which favors cyclic over linear electron transport in the chloroplast.


1 This research was supported by Fonds de la Recherche Fondamentale Collective (grant no. 2.4552.01) and by Fonds de la Recherche Fondamentale Collective (grant no. 1.5.145.03 and research fellowship to P.C.). C.R. and F.F. are research associates of the Fonds National de la Recherche Scientifique.

2 Present address: Virology and Immunology, Institute of Pathology B23, University of Liège, B-4000 Liège, Belgium.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.028076.

* Corresponding author; e-mail F.Franck{at}ulg.ac.be; fax 324-3662926.

Received June 10, 2003; returned for revision June 30, 2003; accepted July 21, 2003.




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