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TOR Regulates the Subcellular Localization of Ime1, a Transcriptional Activator of Meiotic Development in Budding Yeast

Departament de Ciències Mèdiques Bàsiques, Facultat de Medicina, Universitat de Lleida, 25198 Lleida, Catalunya, Spain

Received 21 April 2003/ Returned for modification 27 May 2003/ Accepted 14 July 2003

The transcriptional activator Ime1 is a key regulator of meiosis and sporulation in budding yeast. Ime1 is controlled at different levels by nutrients and cell-type signals. Previously, we have proposed that G₁ cyclins would transmit nutritional signals to the Ime1 pathway by preventing the accumulation of Ime1 within the nucleus. We show here that nutritional signals regulate the subcellular localization of Ime1 through the TOR pathway. The inactivation of TOR with rapamycin promotes the nuclear accumulation and stabilization of Ime1, with consequent induction of early meiotic genes. On the contrary, the activation of TOR by glutamine induces the relocalization of Ime1 to the cytoplasm. Thus, TOR may sense optimal nitrogen- and carbon-limiting conditions to modulate Ime1 function. Besides TOR, ammonia induces an independent mechanism that prevents the accumulation of Ime1 in the nucleus. Both TOR and ammonia regulate Ime1 localization in the absence of Cdk1 activity and therefore use mechanisms different from those exerted by G₁ cyclins. Integration of independent mechanisms into a single early controlling step, such as the nuclear accumulation of Ime1, may help explain why yeast cells execute the meiotic program only when the appropriate internal and external conditions are met together.

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