Article (Scientific journals)
Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids.
Lienard, Marjorie; Araripe, Luciana O; Hartl, Daniel L
2016In Proceedings of the National Academy of Sciences of the United States of America, 113 (29), p. 4200 - E4207
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Keywords :
gene conflict; hybrid male sterility; postzygotic reproductive isolation; transcription factor; DNA-Binding Proteins; Drosophila Proteins; Animals; DNA-Binding Proteins/genetics; Drosophila/genetics; Drosophila/physiology; Drosophila Proteins/genetics; Female; Infertility, Male/genetics; Male; Sperm Motility; Transgenes; Drosophila; Infertility, Male; Multidisciplinary
Abstract :
[en] Crosses between closely related animal species often result in male hybrids that are sterile, and the molecular and functional basis of genetic factors for hybrid male sterility is of great interest. Here, we report a molecular and functional analysis of HMS1, a region of 9.2 kb in chromosome 3 of Drosophila mauritiana, which results in virtually complete hybrid male sterility when homozygous in the genetic background of sibling species Drosophila simulans. The HMS1 region contains two strong candidate genes for the genetic incompatibility, agt and Taf1 Both encode unrelated DNA-binding proteins, agt for an alkyl-cysteine-S-alkyltransferase and Taf1 for a subunit of transcription factor TFIID that serves as a multifunctional transcriptional regulator. The contribution of each gene to hybrid male sterility was assessed by means of germ-line transformation, with constructs containing complete agt and Taf1 genomic sequences as well as various chimeric constructs. Both agt and Taf1 contribute about equally to HMS1 hybrid male sterility. Transgenes containing either locus rescue sterility in about one-half of the males, and among fertile males the number of offspring is in the normal range. This finding suggests compensatory proliferation of the rescued, nondysfunctional germ cells. Results with chimeric transgenes imply that the hybrid incompatibilities result from interactions among nucleotide differences residing along both agt and Taf1 Our results challenge a number of preliminary generalizations about the molecular and functional basis of hybrid male sterility, and strongly reinforce the role of DNA-binding proteins as a class of genes contributing to the maintenance of postzygotic reproductive isolation.
Disciplines :
Genetics & genetic processes
Author, co-author :
Lienard, Marjorie  ;  Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, Department of Biology, Lund University, 22362 Lund, Sweden mlienard@fas.harvard.edu dhartl@oeb.harvard.edu
Araripe, Luciana O;  Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138
Hartl, Daniel L;  Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, mlienard@fas.harvard.edu dhartl@oeb.harvard.edu
Language :
English
Title :
Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids.
Publication date :
19 July 2016
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
ISSN :
0027-8424
eISSN :
1091-6490
Publisher :
National Academy of Sciences, United States
Volume :
113
Issue :
29
Pages :
E4200 - E4207
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH - National Institutes of Health
Sverige Vetenskapsrådet
EMBO - European Molecular Biology Organization
Funding text :
We thank BestGene, Inc., for carrying embryo microinjections; Dr. Norbert Perrimon's laboratory for discussion on quantitative PCR normalization; Dr. Russ Corbett-Detig and Dr. Jean-Marc Lassance for valuable discussions; Kalsang Namgyal for technical assistance; and the reviewers and coreviewer Katharine Korunes for their constructive comments on the manuscript. This work was supported by National Institutes of Health Grant AI106734 (to D.L.H.), and postdoctoral fellowships from the Swedish Research Council and the European Molecular Biology Organization (to M.A.L.).
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