4.7 Article

A male-specific doublesex isoform reveals an evolutionary pathway of sexual development via distinct alternative splicing mechanisms

Journal

COMMUNICATIONS BIOLOGY
Volume 5, Issue 1, Pages -

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s42003-022-03664-7

Keywords

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Funding

  1. National Key R&D Program of China [2019YFA0802400]
  2. National Natural Science Foundation of China [31970943, 31700905]
  3. Jiangsu Innovation and Entrepreneurship Team Program

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A new ancestral male-specific doublesex isoform, dsxM2, was identified and the splicing-based mechanism underlying sex-specific Dmrt function was explored. The study reveals the evolutionary pathway from sexually monomorphic to sex-specific doublesex.
An ancestral male-specific doublesex isoform, dsxM2, is identified via intron retention, with a masculinizing function weaker than the modern dsxM The doublesex/mab-3 related transcription factor (Dmrt) genes regulate sexual development in metazoans. Studies of the doublesex (dsx) gene in insects, in particular Drosophila melanogaster, reveal that alternative splicing of dsx generates sex-specific Dsx isoforms underlying sexual differentiation. Such a splicing-based mechanism underlying sex-specific Dmrt function is thought to be evolved from a transcription-based mechanism used in non-insect species, but how such transition occurs during evolution is not known. Here we identified a male-specific dsx transcript (dsx(M2)) through intron retention (IR), in addition to previously identified dsx(M) and dsx(F) transcripts through alternative polyadenylation (APA) with mutually exclusive exons. We found that Dsx(M2) had similarly masculinizing function as Dsx(M). We also found that the IR-based mechanism generating sex-specific dsx transcripts was conserved from flies to cockroaches. Further analysis of these dsx transcripts suggested an evolutionary pathway from sexually monomorphic to sex-specific dsx via the sequential use of IR-based and APA-based alternative splicing.

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