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J. Biol. Chem., Vol. 279, Issue 2, 1060-1069, January 9, 2004

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Inactivation of the Chloroplast ATP Synthase Subunit Results in High Non-photochemical Fluorescence Quenching and Altered Nuclear Gene Expression in Arabidopsis thaliana^*

Cristina Dal Bosco, Lina Lezhneva, Alexander Biehl, Dario Leister, Heinrich Strotmann¶, Gerd Wanner, and Jörg Meurer||

From the Ludwig-Maximilians-Universität, Department Biologie I, Botanik, Menzingerstrasse 67, 80638 München, Abteilung für Ertragsphysiologie und Pflanzenzüchtung, Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné Weg 10, 50829 Köln, and ^¶Heinrich-Heine-Universität, Biochemie der Pflanzen, Universitätsstrasse 1, 40225 Düsseldorf, Germany

The nuclear atpC1 gene encoding the subunit of the plastid ATP synthase has been inactivated by T-DNA insertion mutagenesis in Arabidopsis thaliana. In the seedling-lethal dpa1 (deficiency of plastid ATP synthase 1) mutant, the absence of detectable amounts of the subunit destabilizes the entire ATP synthase complex. The expression of a second gene copy, atpC2, is unaltered in dpa1 and is not sufficient to compensate for the lack of atpC1 expression. However, in vivo protein labeling analysis suggests that assembly of the ATP synthase and subunits into the thylakoid membrane still occurs in dpa1. As a consequence of the destabilized ATP synthase complex, photophosphorylation is abolished even under reducing conditions. Further effects of the mutation include an increased light sensitivity of the plant and an altered photosystem II activity. At low light intensity, chlorophyll fluorescence induction kinetics is close to those found in wild type, but non-photochemical quenching strongly increases with increasing actinic light intensity resulting in steady state fluorescence levels of about 60% of the minimal dark fluorescence. Most fluorescence quenching relaxed within 3 min after dark incubation. Spectroscopic and biochemical studies have shown that a high proton gradient is responsible for most quenching. Thylakoids of illuminated dpa1 plants were swollen due to an increased proton accumulation in the lumen. Expression profiling of 3292 nuclear genes encoding mainly chloroplast proteins demonstrates that most organelle functions are down-regulated. On the contrary, the mRNA expression of some photosynthesis genes is significantly up-regulated, probably to compensate for the defect in dpa1.

Received for publication, August 1, 2003 , and in revised form, October 22, 2003.

^* This work was supported by German Science Foundation Grant ME1794-2,1 (to J. M.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Sheet 1.

^|| To whom correspondence should be addressed: Ludwig-Maximilians-Universität, Department Biologie I, Botanik, Menzingerstr. 67, 80638 München, Germany. Tel.: 49-89-17861288; Fax: 49-89-1782274; E-mail: meurer{at}botanik.biologie.uni-muenchen.de.

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