Differential Effects of Chromatin and Gcn4 on the 50-Fold Range of Expression among Individual Yeast Ty1 Retrotransposons

Abstract

Approximately 30 copies of the Ty1 retrotransposon are present in the genome of Saccharomyces cerevisiae. Previous studies gave insights into the global regulation of Ty1 transcription but provided no information on the behavior of individual genomic elements. This work shows that the expression of 31 individual Ty1 elements in S288C varies over a 50-fold range. Their transcription is repressed by chromatin structures, which are antagonized by the Swi/Snf and SAGA chromatin-modifying complexes in highly expressed Ty1 elements. These elements carry five potential Gcn4 binding sites in their promoter regions that are mostly absent in weakly expressed Ty1 copies. Consistent with this observation, Gcn4 activates the transcription of highly expressed Ty1 elements only. One of the potential Gcn4 binding sites acts as an upstream activating sequence in vivo and interacts with Gcn4 in vitro. Since Gcn4 has been shown to interact with Swi/Snf and SAGA, we predict that Gcn4 activates Ty1 transcription by targeting these complexes to specific Ty1 promoters.

We are very grateful to P. Stragier for his hospitality to facilitate initiation of the project. We thank F. Winston and M. Proft for technical advice; B. Daignan-Fornier, A. Hinnebusch, S. Gangloff, M. Proft, and F. Winston for plasmids and strains; and F. Allemand for valuable help in the purification of His-tagged Gcn4 protein. Special thanks go to B. Daignan-Fornier, A. Gabriel, C. Condon, and P. Stragier for helpful comments on the manuscript.

This work was supported by a grant from the CNRS (UPR 9073). A.M. was a recipient of a Docteur Ingénieur fellowship from the CNRS and of a fellowship from ARC (Association pour la Recherche contre le Cancer).