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J. Biol. Chem., Vol. 279, Issue 43, 44407-44416, October 22, 2004

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Light and Redox Control of Photosynthesis Gene Expression in Bradyrhizobium

DUAL ROLES OF TWO PpsR^*

Marianne Jaubert, Sébastien Zappa¶, Joël Fardoux, Jean-Marc Adriano¶, Laure Hannibal, Sylvie Elsen||, Jérome Lavergne¶, Andre Verméglio¶, Eric Giraud**, and David Pignol¶**

From the Laboratoire des Symbioses Tropicales et Méditerranéennes (UMR113-IRD-CIRAD-AGRO-M-INRA-UM2), TA 10/J, Campus de Baillarguet, 34398 Montpellier Cedex 5, France, the ^¶CEA/Cadarache DEVM-Laboratoire de Bioénergétique Cellulaire, UMR 6191-CNRS-CEA, Univ-Méditerranée CEA 1000, 13108 Saint Paul lez Durance, Cedex, France, and the ^||Laboratoire de Biochimie et Biophysique des Systèmes Intégrés (UMR 5092 CNRS-CEA-UJF), CEA-Grenoble, 38054 Grenoble cedex 9, France

The two closely related bacteria Bradyrhizobium and Rhodopseudomonas palustris show an unusual mechanism of regulation of photosystem formation by light thanks to a bacteriophytochrome that antirepresses the regulator PpsR. In these two bacteria, we found out, unexpectedly, that two ppsR genes are present. We show that the two Bradyrhizobium PpsR proteins exert antagonistic effects in the regulation of photosystem formation with a classical repressor role for PpsR2 and an unexpected activator role for PpsR1. DNase I footprint analysis show that both PpsR bind to the same DNA TGTN₁₂ACA motif that is present in tandem in the bchC promoter and the crtED intergenic region. Interestingly, the cycA and aerR promoter regions that contain only one conserved palindrome are recognized by PpsR2, but not PpsR1. Further biochemical analyses indicate that PpsR1 only is redox sensitive through the formation of an intermolecular disulfide bond, which changes its oligomerization state from a tetramer to an octamer under oxidizing conditions. Moreover, PpsR1 presents a higher DNA affinity under its reduced form in contrast to what has been previously found for PpsR or its homolog CrtJ from the Rhodobacter species. These results suggest that regulation of photosystem synthesis in Bradyrhizobium involves two PpsR competing for the binding to the same photosynthesis genes and this competition might be modulated by two factors: light via the antagonistic action of a bacteriophytochrome on PpsR2 and redox potential via the switch of PpsR1 oligomerization state.

Received for publication, July 16, 2004

^* 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.

Supported by a French Minister of National Education, Higher Education and Research doctoral grant.

^** Both authors contributed equally and should be considered co-senior authors.

To whom correspondence should be addressed: IRD, LSTM TA 10/J, Campus de Baillarguet, 34398 Montpellier Cedex 5, France. Tel.: 33-467593783; Fax: 33-467593802; E-mail: Giraud{at}mpl.ird.fr.

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