Open Access Research

Chromatin structural changes around satellite repeats on the female sex chromosome in Schistosoma mansoni and their possible role in sex chromosome emergence

Julie MJ Lepesant1*, Céline Cosseau1, Jérome Boissier1, Michael Freitag2, Julien Portela1, Déborah Climent1, Cécile Perrin1, Adhemar Zerlotini3 and Christoph Grunau1

Author Affiliations

1 Université de Perpignan Via Domitia, CNRS, UMR 5244 Ecologie et Evolution des Interactions (2EI), 52 Avenue Paul Alduy, 66860 Perpignan Cedex, France

2 Department of Biochemistry and Biophysics, ALS 2011, Oregon State University, Corvallis, OR 97331-7305, USA

3 CEBio - Centro de Excelência em Bioinformática, Rua Araguari, 741/301 - Barro Preto - BH/MG - CEP 30190-110, Brazil

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Genome Biology 2012, 13:R14  doi:10.1186/gb-2012-13-2-r14

Published: 29 February 2012

Abstract

Background

In the leuphotrochozoan parasitic platyhelminth Schistosoma mansoni, male individuals are homogametic (ZZ) whereas females are heterogametic (ZW). To elucidate the mechanisms that led to the emergence of sex chromosomes, we compared the genomic sequence and the chromatin structure of male and female individuals. As for many eukaryotes, the lower estimate for the repeat content is 40%, with an unknown proportion of domesticated repeats. We used massive sequencing to de novo assemble all repeats, and identify unambiguously Z-specific, W-specific and pseudoautosomal regions of the S. mansoni sex chromosomes.

Results

We show that 70 to 90% of S. mansoni W and Z are pseudoautosomal. No female-specific gene could be identified. Instead, the W-specific region is composed almost entirely of 36 satellite repeat families, of which 33 were previously unknown. Transcription and chromatin status of female-specific repeats are stage-specific: for those repeats that are transcribed, transcription is restricted to the larval stages lacking sexual dimorphism. In contrast, in the sexually dimorphic adult stage of the life cycle, no transcription occurs. In addition, the euchromatic character of histone modifications around the W-specific repeats decreases during the life cycle. Recombination repression occurs in this region even if homologous sequences are present on both the Z and W chromosomes.

Conclusion

Our study provides for the first time evidence for the hypothesis that, at least in organisms with a ZW type of sex chromosomes, repeat-induced chromatin structure changes could indeed be the initial event in sex chromosome emergence.