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Molecular and Cellular Biology, September 2004, p. 8210-8220, Vol. 24, No. 18
0270-7306/04/$08.00+0     DOI: 10.1128/MCB.24.18.8210-8220.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

cis-Acting Determinants of Heterochromatin Formation on Drosophila melanogaster Chromosome Four

Fang-Lin Sun,1,{dagger} Karmella Haynes,2,{dagger} Cory L. Simpson,2 Susan D. Lee,2 Lynne Collins,2 Jo Wuller,2 Joel C. Eissenberg,3 and S. C. R. Elgin2*

Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland,1 Department of Biology, Washington University,2 Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, Missouri3

Received 15 April 2004/ Returned for modification 18 May 2004/ Accepted 18 June 2004

The heterochromatic domains of Drosophila melanogaster (pericentric heterochromatin, telomeres, and the fourth chromosome) are characterized by histone hypoacetylation, high levels of histone H3 methylated on lysine 9 (H3-mK9), and association with heterochromatin protein 1 (HP1). While the specific interaction of HP1 with both H3-mK9 and histone methyltransferases suggests a mechanism for the maintenance of heterochromatin, it leaves open the question of how heterochromatin formation is targeted to specific domains. Expression characteristics of reporter transgenes inserted at different sites in the fourth chromosome define a minimum of three euchromatic and three heterochromatic domains, interspersed. Here we searched for cis-acting DNA sequence determinants that specify heterochromatic domains. Genetic screens for a switch in phenotype demonstrate that local deletions or duplications of 5 to 80 kb of DNA flanking a transposon reporter can lead to the loss or acquisition of variegation, pointing to short-range cis-acting determinants for silencing. This silencing is dependent on HP1. A switch in transgene expression correlates with a switch in chromatin structure, judged by nuclease accessibility. Mapping data implicate the 1360 transposon as a target for heterochromatin formation. We propose that heterochromatin formation is initiated at dispersed repetitive elements along the fourth chromosome and spreads for ~10 kb or until encountering competition from a euchromatic determinant.

* Corresponding author. Mailing address: Department of Biology, CB-1229, Washington University, One Brookings Dr., St. Louis, MO 63130. Phone: (314) 935-5348. Fax: (314) 935-5125. E-mail: selgin{at}biology.wustl.edu.

{dagger} F.-L.S. and K.H. contributed equally to this work.

Molecular and Cellular Biology, September 2004, p. 8210-8220, Vol. 24, No. 18
0022-538X/04/$08.00+0     DOI: 10.1128/MCB.24.18.8210-8220.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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