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Proc Natl Acad Sci U S A. 2016 Apr 12;113(15):E2114-23. doi: 10.1073/pnas.1525164113. Epub 2016 Mar 29.

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes.

Author information

1
The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
2
Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy; Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
3
Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
4
Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556;
5
Department of Entomology, Riverside Center for Disease Vector Research, Institute for Integrative Genome Biology, University of California, Riverside, CA 92521;
6
Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
7
National Biodefense Analysis and Countermeasures Center, Frederick, MD 21702;
8
Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy;
9
Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
10
Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892;
11
Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Laboratory of Evolutionary Cytogenetics, Tomsk State University, Tomsk 634050, Russia;
12
School of Informatics and Computing, Indiana University, Bloomington, IN 47405;
13
School of Informatics and Computing, Indiana University, Bloomington, IN 47405; Department of Biology, Indiana University, Bloomington, IN 47405;
14
Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
15
The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Laboratory of Evolutionary Cytogenetics, Tomsk State University, Tomsk 634050, Russia; igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.
16
The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.
17
Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556; igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.

Abstract

Y chromosomes control essential male functions in many species, including sex determination and fertility. However, because of obstacles posed by repeat-rich heterochromatin, knowledge of Y chromosome sequences is limited to a handful of model organisms, constraining our understanding of Y biology across the tree of life. Here, we leverage long single-molecule sequencing to determine the content and structure of the nonrecombining Y chromosome of the primary African malaria mosquito, Anopheles gambiae We find that the An. gambiae Y consists almost entirely of a few massively amplified, tandemly arrayed repeats, some of which can recombine with similar repeats on the X chromosome. Sex-specific genome resequencing in a recent species radiation, the An. gambiae complex, revealed rapid sequence turnover within An. gambiae and among species. Exploiting 52 sex-specific An. gambiae RNA-Seq datasets representing all developmental stages, we identified a small repertoire of Y-linked genes that lack X gametologs and are not Y-linked in any other species except An. gambiae, with the notable exception of YG2, a candidate male-determining gene. YG2 is the only gene conserved and exclusive to the Y in all species examined, yet sequence similarity to YG2 is not detectable in the genome of a more distant mosquito relative, suggesting rapid evolution of Y chromosome genes in this highly dynamic genus of malaria vectors. The extensive characterization of the An. gambiae Y provides a long-awaited foundation for studying male mosquito biology, and will inform novel mosquito control strategies based on the manipulation of Y chromosomes.

KEYWORDS:

Anopheles gambiae; PacBio; RNA-Seq; Y-chromosome; tandem repetitive DNA

PMID:
27035980
PMCID:
PMC4839409
DOI:
10.1073/pnas.1525164113
[Indexed for MEDLINE]
Free PMC Article

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