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J. Biol. Chem., Vol. 279, Issue 34, 35273-35280, August 20, 2004

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Low Affinity Orthophosphate Carriers Regulate PHO Gene Expression Independently of Internal Orthophosphate Concentration in Saccharomyces cerevisiae^*

Benoît Pinson, Michel Merle¶, Jean-Michel Franconi¶, and Bertrand Daignan-Fornier

From the Institut de Biochimie et Génétique Cellulaires, UMR 5095 CNRS-Université Victor Segalen Bordeaux 2, 33077 Bordeaux Cedex and the ^¶Unité de Résonance Magnétique des Systèmes Biologiques, UMR 5536, CNRS-Université Victor Segalen Bordeaux 2, Case 93, 146 Rue Leo-Saignat, 33076 Bordeaux, France

Phosphate is an essential nutrient that must be taken up from the growth medium through specific transporters. In Saccharomyces cerevisiae, both high and low affinity orthophosphate carriers allow this micro-organism to cope with environmental variations. Intriguingly, in this study we found a tight correlation between selenite resistance and expression of the high affinity orthophosphate carrier Pho84p. Our work further revealed that mutations in the low affinity orthophosphate carrier genes (PHO87, PHO90, and PHO91) cause deregulation of phosphate-repressed genes. Strikingly, the deregulation due to pho87, pho90, or pho91 mutations was neither correlated to impaired orthophosphate uptake capacity nor to a decrease of the intracellular orthophosphate or polyphosphate pools, as shown by ³¹P NMR spectroscopy. Thus, our data clearly establish that the low affinity orthophosphate carriers affect phosphate regulation independently of intracellular orthophosphate concentration through a new signaling pathway that was found to strictly require the cyclin-dependent kinase inhibitor Pho81p. We propose that phosphate-regulated gene expression is under the control of two different regulatory signals as follows: the sensing of internal orthophosphate by a yet unidentified protein and the sensing of external orthophosphate by low affinity orthophosphate transporters; the former would be required to maintain phosphate homeostasis, and the latter would keep the cell informed on the medium phosphate richness.

Received for publication, May 14, 2004 , and in revised form, June 11, 2004.

^* This work was supported by CNRS UMR 5095/University Bordeaux 2 and by Grant 5843 from the Association pour la Recherche contre le Cancer. 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.

To whom correspondence should be addressed: Institut de Biochimie et Génétique Cellulaires, CNRS UMR 5095, 1 Rue Camille Saint-Saëns, 33077 Bordeaux Cedex, France. Tel.: 33-5-56-99-90-19; Fax: 33-5-56-99-90-59; E-mail: benoit.pinson{at}ibgc.u-bordeaux2.fr.

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