Abstract
The ATP synthase is a ubiquitous enzyme which is found in bacteria and eukaryotic organelles. It is essential in the photosynthetic and respiratory processes, by transforming the electrochemical proton gradient into ATP energy via proton transport across the membranes. In Escherichia coli, the atp genes coding for the subunits of the ATP synthase enzyme are grouped in the same transcriptional unit, while in higher plants the plastid atp genes are organized into a large (atpI/H/F/A) and a small (atpB/E) atp operon. By using the model plant Arabidopsis thaliana, we have investigated the strategy evolved in chloroplasts to overcome the physical separation of the atp gene clusters and to coordinate their transcription. We show that all the identified promoters in the two atp operons are PEP dependent and require sigma factors for specific recognition. Our results indicate that transcription of the two atp operons is initiated by at least one common factor, the essential SIG2 factor. Our data show that SIG3 and SIG6 also participate in transcription initiation of the large and the small atp operon, respectively. We propose that SIG2 might be the factor responsible for coordinating the basal transcription of the plastid atp genes and that SIG3 and SIG6 might serve to modulate plastid atp expression with respect to physiological and environmental conditions. However, we observe that in the sigma mutants (sig2, sig3 and sig6) the deficiency in the recognition of specific atp promoters is largely balanced by mRNA stabilization and/or by activation of otherwise silent promoters, indicating that the rate-limiting step for expression of the atp operons is mostly post-transcriptional.
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Acknowledgments
We thank F. Courtois and G. Finazzi for critical reading of the manuscript. We are grateful to D. Downey for English editing of the manuscript. We are grateful to M. Hanaoka from K. Tanaka laboratory for providing sig5 seeds and to R. Sharwood from D. Stern laboratory for providing unselected sig6 seeds. M. M.G. was financed by the “Higher Education Commission of Pakistan (HEC)”; O.Z.-A. was financed by the “Institut Français de Coopération à Tunis”. We thank The Centre National de la Recherche Scientifique and the French Ministry of Education for funding.
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Malik Ghulam, M., Zghidi-Abouzid, O., Lambert, E. et al. Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/A and atpB/E, in Arabidopsis thaliana chloroplasts. Plant Mol Biol 79, 259–272 (2012). https://doi.org/10.1007/s11103-012-9910-5
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DOI: https://doi.org/10.1007/s11103-012-9910-5