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Modulation of Yeast Genome Expression in Response to Defective RNA Polymerase III-Dependent Transcription

Christine Conesa,^1,* Roberta Ruotolo,^2, Pascal Soularue,³ Tiffany A. Simms,⁴ David Donze,⁴ André Sentenac,¹ and Giorgio Dieci^2*

Service de Biochimie et Génétique Moléculaire, Bâtiment 144, CEA/Saclay, 91191 Gif-sur-Yvette Cedex, France,¹ Dipartimento di Biochimica e Biologia Molecolare, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43100 Parma, Italy,² Service de Génomique Fonctionnelle, CEA/Evry, 2 rue Gaston Crémieux, CP22, 91057 Evry Cedex, France,³ Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803⁴

Received 10 February 2005/ Returned for modification 21 March 2005/ Accepted 6 July 2005

We used genome-wide expression analysis in Saccharomyces cerevisiae to explore whether and how the expression of protein-coding, RNA polymerase (Pol) II-transcribed genes is influenced by a decrease in RNA Pol III-dependent transcription. The Pol II transcriptome was characterized in four thermosensitive, slow-growth mutants affected in different components of the RNA Pol III transcription machinery. Unexpectedly, we found only a modest correlation between altered expression of Pol II-transcribed genes and their proximity to class III genes, a result also confirmed by the analysis of single tRNA gene deletants. Instead, the transcriptome of all of the four mutants was characterized by increased expression of genes known to be under the control of the Gcn4p transcriptional activator. Indeed, GCN4 was found to be translationally induced in the mutants, and deleting the GCN4 gene eliminated the response. The Gcn4p-dependent expression changes did not require the Gcn2 protein kinase and could be specifically counteracted by an increased gene dosage of initiator tRNA^Met. Initiator tRNA^Met depletion thus triggers a GCN4-dependent reprogramming of genome expression in response to decreased Pol III transcription. Such an effect might represent a key element in the coordinated transcriptional response of yeast cells to environmental changes.

Supplemental material for this article may be found at http://mcb.asm.org/.

C.C. and R.R. contributed equally to this study.

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