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Published Online January 2, 2003
Science DOI: 10.1126/science.1079190

Reports

Submitted on October 8, 2002
Accepted on December 13, 2002

Paucity of Genes on the Drosophila X-Chromosome Showing Male-Biased Expression

Michael Parisi 1, Rachel Nuttall 2, Daniel Naiman 3, Gerard Bouffard 4, James Malley 5, Justen Andrews 6, Scott Eastman 2, Brian Oliver 1*

1 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda, MD 20892-8028, USA.
2 Incyte Genomics, Palo Alto, CA 94304, USA.
3 Department of Mathematical Sciences, John Hopkins University, Baltimore, MD 21218, USA.
4 National Institutes of Health Intramural Sequencing Center, National Human Genome Research Institute, National Institutes of Health, Department of Health and Human Services, Gaithersburg, MD 20877, USA.
5 Center for Information Technology, National Institutes of Health, Department of Health and Human Services, Bethesda, MD 20892-5620, USA.
6 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda, MD 20892-8028, USA; Present address: Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN 47405-3700, USA.

* To whom correspondence should be addressed. E-mail: oliver{at}helix.nih.gov.

Sex chromosomes are primary determinants of sexual dimorphism in many organisms. These chromosomes are thought to arise via the divergence of an ancestral autosome pair, and are almost certainly influenced by differing selection in males and females. Exploring how sex chromosomes differ from autosomes is highly amenable to genomic analysis. We examined global gene expression in Drosophila melanogaster and report a dramatic underrepresentation of X-chromosome genes showing high relative expression in males. Using comparative genomics, we find that these same X-chromosome genes are exceptionally poorly conserved in the mosquito Anopheles gambiae. These data indicate that the X-chromosome is a disfavored location for genes selectively expressed in males.


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »


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