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Plant Cell Advance Online Publication
Published on March 3, 2006; 10.1105/tpc.105.039073

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Received October 27, 2005
Returned for revision January 23, 2006
Accepted February 14, 2006

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

Paolo Pesaresi 1, Simona Masiero 2, Holger Eubel 3, Hans-Peter Braun 3, Shashi Bhushan 4, Elzbieta Glaser 4, Francesco Salamini 5, and Dario Leister 6*

1 Abteilung für Pflanzenzüchtung und Genetik, Max-Planck-Institut für Züchtungsforschung, D-50829 Cologne, Germany; Fondazione Parco Tecnologico Padano, I-26900 Lodi, Italy
2 Dipartimento di Biologia, Università degli Studi di Milano, I-20133 Milan, Italy
3 Institut für Angewandte Genetik, Universität Hannover, D-30419 Hannover, Germany
4 Department of Biochemistry and Biophysics, Arrhenius Laboratories for Natural Sciences, Stockholm University, SE-10691 Stockholm, Sweden
5 Fondazione Parco Tecnologico Padano, I-26900 Lodi, Italy
6 Abteilung für Pflanzenzüchtung und Genetik, Max-Planck-Institut für Züchtungsforschung, D-50829 Cologne, Germany; Botanisches Institut, Ludwig-Maximilians-Universität, D-80638 Munich, Germany

* To whom correspondence should be addressed. E-mail: leister{at}lrz.uni-muenchen.de.

Arabidopsis thaliana mutants prors1-1 and -2 were identified on the basis of a decrease in effective photosystem II quantum yield. Mutations were localized to the 5'-untranslated region of the nuclear gene PROLYL-tRNA SYNTHETASE1 (PRORS1), which acts in both plastids and mitochondria. In prors1-1 and -2, PRORS1 expression is reduced, along with protein synthesis in both organelles. PRORS1 null alleles (prors1-3 and -4) result in embryo sac and embryo development arrest. In mutants with the leaky prors1-1 and -2 alleles, transcription of nuclear genes for proteins involved in photosynthetic light reactions is downregulated, whereas genes for other chloroplast proteins are upregulated. Downregulation of nuclear photosynthetic genes is not associated with a marked increase in the level of reactive oxygen species in leaves and persists in the dark, suggesting that the transcriptional response is light and photooxidative stress independent. The mrpl11 and prpl11 mutants are impaired in the mitochondrial and plastid ribosomal L11 proteins, respectively. The prpl11 mrpl11 double mutant, but neither of the single mutants, resulted in strong downregulation of nuclear photosynthetic genes, like that seen in leaky mutants for PRORS1, implying that, when organellar translation is perturbed, signals derived from both types of organelles cooperate in the regulation of nuclear photosynthetic gene expression.






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