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J. Biol. Chem., Vol. 281, Issue 39, 29155-29164, September 29, 2006

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Nucleosome Depletion Activates Poised RNA Polymerase III at Unconventional Transcription Sites in Saccharomyces cerevisiae^*

Elisa Guffanti¹, Riccardo Percudani, Olivier Harismendy, Julie Soutourina, Michel Werner, Maria Giuseppina Iacovella^¶, Rodolfo Negri^¶, and Giorgio Dieci²

From the Dipartimento di Biochimica e Biologia Molecolare, Università degli Studi di Parma, 43100 Parma, Italy, the Service de Biochimie et Génétique Moléculaire, Commissariat à l'Energie Atomique (CEA)/Saclay, 91191 Gif-sur-Yvette, France, and the ^¶Istituto Pasteur - Fondazione Cenci Bolognetti, Dipartimento di Biologia Cellulare, Università di Roma La Sapienza, 00185 Roma, Italy

RNA polymerase (pol) III, assisted by the transcription factors TFIIIC and TFIIIB, transcribes small untranslated RNAs, such as tRNAs. In addition to known pol III-transcribed genes, the Saccharomyces cerevisiae genome contains loci (ZOD1, ETC1-8) associated to incomplete pol III transcription complexes (Moqtaderi, Z., and Struhl, K. (2004) Mol. Cell. Biol. 24, 4118-4127). We show that a short segment of the ZOD1 locus, containing box A and box B promoter elements and a termination signal between them, directs the pol III-dependent production of a small RNA both in vitro and in vivo. In yeast cells, the levels of both ZOD1- and ETC5-specific transcripts were dramatically enhanced upon nucleosome depletion. Remarkably, transcription factor and pol III occupancy at the corresponding loci did not change significantly upon derepression, thus suggesting that chromatin opening activates poised pol III to transcription. Comparative genomic analysis revealed that the ZOD1 promoter is the only surviving portion of a tDNA^Ile ancestor, whose transcription capacity has been preserved throughout evolution independently from the encoded RNA product. Similarly, another TFIIIC/TFIIIB-associated locus, close to the YGR033c open reading frame, was found to be the strictly conserved remnant of an ancient tDNA^Arg. The maintenance, by eukaryotic genomes, of chromatin-repressed, non-coding transcription units has implications for both genome expression and organization.

Received for publication, January 13, 2006 , and in revised form, June 9, 2006.

^* This work was supported by the Human Frontier Science Program Grant RGY0011/2002-C (to G. D.) and by a grant from the Italian Ministry of Education, University and Research (PRIN and FIRB programs). 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.

¹ Recipient of an EMBO Short-term Fellowship.

² To whom correspondence should be addressed: Dipartimento di Biochimica e Biologia Molecolare, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43100 Parma, Italy. Tel.: 39-0521-905649; Fax: 39-0521-905151; E-mail: giorgio.dieci{at}unipr.it.

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