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Open Access Research article

Histone modifications in the male germ line of Drosophila a

Wolfgang Hennig123* and Alexandra Weyrich124

Author Affiliations

1 DAAD Laboratory, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

2 CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

3 present address: Institut für Genetik, Johannes Gutenberg-Universität Mainz, Mainz D-55128, Germany

4 present address: Department of Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research (IWZ), Alfred-Kowalke-Str. 17, Berlin D-10315, Germany

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BMC Developmental Biology 2013, 13:7  doi:10.1186/1471-213X-13-7

Published: 22 February 2013

Abstract

Background

In the male germ line of Drosophila chromatin remains decondensed and highly transcribed during meiotic prophase until it is rapidly compacted. A large proportion of the cell cycle-regulated histone H3.1 is replaced by H3.3, a histone variant encoded outside the histone repeat cluster and not subject to cell cycle controlled expression.

Results

We investigated histone modification patterns in testes of D. melanogaster and D. hydei. In somatic cells of the testis envelope and in germ cells these modification patterns differ from those typically seen in eu- and heterochromatin of other somatic cells. During the meiotic prophase some modifications expected in active chromatin are not found or are found at low level. The absence of H4K16ac suggests that dosage compensation does not take place. Certain histone modifications correspond to either the cell cycle-regulated histone H3.1 or to the testis-specific variant H3.3. In spermatogonia we found H3K9 methylation in cytoplasmic histones, most likely corresponding to the H3.3 histone variant. Most histone modifications persist throughout the meiotic divisions. The majority of modifications persist until the early spermatid nuclei, and only a minority further persist until the final chromatin compaction stages before individualization of the spermatozoa.

Conclusion

Histone modification patterns in the male germ line differ from expected patterns. They are consistent with an absence of dosage compensation of the X chromosome during the male meiotic prophase. The cell cycle-regulated histone variant H3.1 and H3.3, expressed throughout the cell cycle, also vary in their modification patterns. Postmeiotically, we observed a highly complex pattern of the histone modifications until late spermatid nuclear elongation stages. This may be in part due to postmeiotic transcription and in part to differential histone replacement during chromatin condensation.