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Characterization of a male-predominant antisense transcript underexpressed in hybrids of Drosophila pseudoobscura and D. persimilis.

ABSTRACT: Characterizing genes that are misregulated in hybrids may elucidate the genetic basis of hybrid sterility or other hybrid dysfunctions that contribute to speciation. Previously, a small segment of a male-predominant transcript that is underexpressed in adult male hybrids of Drosophila pseudoobscura and D. persimilis relative to pure species was identified in a differential display screen. Here, we obtained the full sequence of this 1330-bp transcript and determined that it is an antisense message with high sequence similarity to the D. melanogaster TRAP100 gene, part of the Mediator protein complex that regulates transcriptional initiation during development. Both the sense and the antisense messages are transcribed in D. pseudoobscura, but only the sense message (TRAP100) is transcribed in D. melanogaster complex species. Unlike the antisense message, the sense message is transcribed similarly in D. pseudoobscura males and females and in hybrids of D. pseudoobscura and D. persimilis. The high sequence similarity between distantly related species suggests that the sense message is functionally constrained within the genus. We speculate that the antisense transcript may have evolved a role in male-specific post-transcriptional regulation of TRAP100 in the D. pseudoobscura lineage and that its underexpression in sterile hybrid males may cause an overproduction of TRAP100 protein, possibly yielding deleterious effects.

SUBMITTER: Noor MA

PROVIDER: S-EPMC1462881 | biostudies-other | 2003 Dec

REPOSITORIES: biostudies-other

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Characterization of a male-predominant antisense transcript underexpressed in hybrids of Drosophila pseudoobscura and D. persimilis.

Noor Mohamed A F MA Michalak Pawel P Donze David D

Genetics 20031201 4

Characterizing genes that are misregulated in hybrids may elucidate the genetic basis of hybrid sterility or other hybrid dysfunctions that contribute to speciation. Previously, a small segment of a male-predominant transcript that is underexpressed in adult male hybrids of Drosophila pseudoobscura and D. persimilis relative to pure species was identified in a differential display screen. Here, we obtained the full sequence of this 1330-bp transcript and determined that it is an antisense messag ...[more]

PMID: 14704168

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Project description:BackgroundThe genetic basis of hybrid incompatibilities is characterized by pervasive cases of gene interactions. Sex chromosomes play a major role in speciation and X-linked hybrid male sterility (HMS) genes have been identified. Interestingly, some of these genes code for proteins with DNA binding domains, suggesting a capability to act as trans-regulatory elements and disturb the expression of a large number of gene targets. To understand how interactions between trans- and cis-regulatory elements contribute to speciation, we aimed to map putative X-linked trans-regulatory elements and to identify gene targets with disrupted gene expression in sterile hybrids between the subspecies Drosophila pseudoobscura pseudoobscura and D. p. bogotana.ResultsWe find six putative trans-regulatory proteins within previously mapped X chromosome HMS loci with sequence changes that differentiate the two subspecies. Among them, the previously characterized HMS gene Overdrive (Ovd) had the largest number of amino acid changes between subspecies, with some substitutions localized within the protein's DNA binding domain. Using an introgression approach, we detected transcriptional responses associated with a sterility/fertility Ovd allele swap. We found a network of 52 targets of Ovd and identified cis-regulatory effects among target genes with disrupted expression in sterile hybrids. However, a combined analysis of polymorphism and divergence in non-coding sequences immediately upstream of target genes found no evidence of changes in candidate regulatory proximal cis-elements. Finally, peptidases were over-represented among target genes.ConclusionsWe provide evidence of divergence between subspecies within the DNA binding domain of the HMS protein Ovd and identify trans effects on the expression of 52 gene targets. Our results identify a network of trans-cis interactions with possible effects on HMS. This network provides molecular evidence of gene × gene incompatibilities as contributors to hybrid dysfunction.

Dataset Information

Characterization of a male-predominant antisense transcript underexpressed in hybrids of Drosophila pseudoobscura and D. persimilis.

Publications

Characterization of a male-predominant antisense transcript underexpressed in hybrids of Drosophila pseudoobscura and D. persimilis.

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