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Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids

Liénard, Marjorie A. LU ; Araripe, Luciana O. and Hartl, Daniel L. (2016) In Proceedings of the National Academy of Sciences of the United States of America 113(29). p.4200-4207
Abstract

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... (More)

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.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Gene conflict, Hybrid male sterility, Postzygotic reproductive isolation, Transcription factor
in
Proceedings of the National Academy of Sciences of the United States of America
volume
113
issue
29
pages
4200 - 4207
publisher
National Acad Sciences
external identifiers
  • scopus:84978900543
  • wos:000380224500013
ISSN
0027-8424
DOI
10.1073/pnas.1608337113
language
English
LU publication?
yes
id
833612d1-cae6-4d56-b47c-47763d6efd12
date added to LUP
2017-01-10 11:50:37
date last changed
2017-11-19 04:36:33
@article{833612d1-cae6-4d56-b47c-47763d6efd12,
  abstract     = {<p>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.</p>},
  author       = {Liénard, Marjorie A. and Araripe, Luciana O. and Hartl, Daniel L.},
  issn         = {0027-8424},
  keyword      = {Gene conflict,Hybrid male sterility,Postzygotic reproductive isolation,Transcription factor},
  language     = {eng},
  month        = {07},
  number       = {29},
  pages        = {4200--4207},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids},
  url          = {http://dx.doi.org/10.1073/pnas.1608337113},
  volume       = {113},
  year         = {2016},
}