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Dosage Compensation via Transposable Element Mediated Rewiring of a Regulatory Network

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Science  15 Nov 2013:
Vol. 342, Issue 6160, pp. 846-850
DOI: 10.1126/science.1239552

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Getting the Dosage Right

As sex chromosomes evolve, they must compensate for differential gene dosage, especially in non-sex-specific genes. However, owing to the relative rarity of chromosomes that are in the process of becoming sex chromosomes, the ongoing evolutionary processes resulting in dosage compensation are unclear. Ellison and Bachtrog (p. 846; see the Perspective by Chuong and Feschotte) identified a specific transposable element involved in dosage compensation in males on the evolutionarily new neo-X chromosome of Drosophila miranda. A particular copy of this transposable element has been inserted at chromatin entry sites on the neo-X chromosome that favorably binds to the male-specific lethal complex, which in turn facilitates the spreading of chromatin silencing on a single chromosome to provide dosage compensation.

Abstract

Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use cis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.

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