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Villa, Raffaella ; Jagtap, Pravin Kumar Ankush ; Thomae, Andreas W. ; Campos Sparr, Aline ; Forné, Ignasi ; Hennig, Janosch ; Straub, Tobias ; Becker, Peter B.:
Divergent evolution toward sex chromosome-specific gene regulation in Drosophila.
In: Genes & Development.
Bd. 35
(2021)
Heft 13-14
.
- S. 1055-1070.
ISSN 1549-5477
DOI: https://doi.org/10.1101/gad.348411.121
Abstract
The dosage compensation complex (DCC) of Drosophila identifies its X-chromosomal binding sites with exquisite selectivity. The principles that assure this vital targeting are known from the D. melanogaster model: DCC-intrinsic specificity of DNA binding, cooperativity with the CLAMP protein, and noncoding roX2 RNA transcribed from the X chromosome. We found that in D. virilis, a species separated from melanogaster by 40 million years of evolution, all principles are active but contribute differently to X specificity. In melanogaster, the DCC subunit MSL2 evolved intrinsic DNA-binding selectivity for rare PionX sites, which mark the X chromosome. In virilis, PionX motifs are abundant and not X-enriched. Accordingly, MSL2 lacks specific recognition. Here, roX2 RNA plays a more instructive role, counteracting a nonproductive interaction of CLAMP and modulating DCC binding selectivity. Remarkably, roX2 triggers a stable chromatin binding mode characteristic of DCC. Evidently, X-specific regulation is achieved by divergent evolution of protein, DNA, and RNA components.