Transvection regulates the sex-biased expression of a fly X-linked gene
Enhancer-gene interactions drive split
In many species across the animal kingdom, male and female phenotypes differ. One such example is the wing spot seen in male Drosophila biarmipes flies but not the female flies. Galouzis and Prud'homme investigate the X-linked yellow gene and its enhancer. Investigating the genetics of the trait, they found evidence that the male-specific phenotype is caused by a trans interaction between the enhancer and gene that silences the gene when it is present in only one copy in the male (which only has a single X chromosome) versus the two copies found in the female. This gene thus appears to be regulated by differing genomic interactions in male and female flies and is an example of the phenomenon known as transvection.
Science, this issue p. 396
Abstract
Sexual dimorphism in animals results from sex-biased gene expression patterns. These patterns are controlled by genetic sex determination hierarchies that establish the sex of an individual. Here we show that the male-biased wing expression pattern of the Drosophila biarmipes gene yellow, located on the X chromosome, is independent of the fly sex determination hierarchy. Instead, we find that a regulatory interaction between yellow alleles on homologous chromosomes (a process known as transvection) silences the activity of a yellow enhancer functioning in the wing. Therefore, this enhancer can be active in males (XY) but not in females (XX). This transvection-dependent enhancer silencing requires the yellow intron and the chromatin architecture protein Mod(mdg4). Our results suggest that transvection can contribute more generally to the sex-biased expression of X-linked genes.
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Supplementary Material
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Information & Authors
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Published In
Science
Volume 371 | Issue 6527
22 January 2021
22 January 2021
Copyright
Copyright © 2021, American Association for the Advancement of Science.
This is an article distributed under the terms of the Science Journals Default License.
Submission history
Received: 15 April 2020
Accepted: 17 December 2020
Published in print: 22 January 2021
Acknowledgments
We are grateful to the Bloomington Drosophila Stock Center for fly stocks; Flybase for information support; N. Gompel for the anti-Yellow antibody; A. Sultanova for assistance in the collection of abdomens; and M. Paris, N. Gompel, J. Ewbank, and all laboratory members for helpful comments on the manuscript. Funding: This work was funded by the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC grant agreement 615789 (B.P.). C.C.G. acknowledges funding from the Fondation pour la Recherche Médicale (FRM FDT201904008114). Author contributions: B.P. conceived the project. B.P. and C.C.G. designed the experiments. C.C.G. performed all experiments and statistical analyses. C.C.G. and B.P. analyzed the results and wrote the manuscript. Competing interests: The authors declare no competing interests. Data and materials availability: The authors declare that the data supporting the findings of this study are available in the manuscript or supplementary materials, and raw image data are deposited in the figshare digital repository (31).
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Funding Information
European Research Council: 615789
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