Heterochromatin Protein 1 Is Involved in Control of Telomere Elongation in Drosophila melanogaster

Abstract

Telomeres of Drosophila melanogaster contain arrays of the retrotransposon-like elements HeT-A and TART. Their transposition to broken chromosome ends has been implicated in chromosome healing and telomere elongation. We have developed a genetic system which enables the determination of the frequency of telomere elongation events and their mechanism. The frequency differs among lines with different genotypes, suggesting that several genes are in control. Here we show that the Su(var)2-5 gene encoding heterochromatin protein 1 (HP1) is involved in regulation of telomere length. Different Su(var)2-5 mutations in the heterozygous state increase the frequency of HeT-A and TART attachment to the broken chromosome end by more than a hundred times. The attachment occurs through either HeT-A/TART transposition or recombination with other telomeres. Terminal DNA elongation by gene conversion is greatly enhanced by Su(var)2-5 mutations only if the template for DNA synthesis is on the same chromosome but not on the homologous chromosome. The Drosophila lines bearing the Su(var)2-5 mutations maintain extremely long telomeres consisting of HeT-A and TART for many generations. Thus, HP1 plays an important role in the control of telomere elongation in D. melanogaster.

We are sincerely grateful to Y. B. Schwartz for helpful suggestions and discussions during this work. We thank J. Eissenberg for critical comments on the manuscript. We also thank J. Eissenberg, M. L. Pardue, K. L. Traverse, C.-T. Wu, J. Modolell, M. Gatti, and the Umeå Stock Center for Drosophila stocks and plasmids.

This work was supported by the Russian state program Frontiers in Genetics, the Russian Foundation for Basic Research, and by an International Research Scholar award from the Howard Hughes Medical Institute to P.G.