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PLoS Genet. 2014 Feb 13;10(2):e1004159. doi: 10.1371/journal.pgen.1004159. eCollection 2014.

Sex-specific embryonic gene expression in species with newly evolved sex chromosomes.

Author information

  • 1Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, United States of America.
  • 2Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, California, United States of America.
  • 3Department of Integrative Biology, University of California, Berkeley, Berkeley, California, United States of America.
  • 4Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, United States of America ; Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, California, United States of America ; Department of Integrative Biology, University of California, Berkeley, Berkeley, California, United States of America.

Abstract

Sex chromosome dosage differences between females and males are a significant form of natural genetic variation in many species. Like many species with chromosomal sex determination, Drosophila females have two X chromosomes, while males have one X and one Y. Fusions of sex chromosomes with autosomes have occurred along the lineage leading to D. pseudoobscura and D. miranda. The resulting neo-sex chromosomes are gradually evolving the properties of sex chromosomes, and neo-X chromosomes are becoming targets for the molecular mechanisms that compensate for differences in X chromosome dose between sexes. We have previously shown that D. melanogaster possess at least two dosage compensation mechanisms: the well- characterized MSL-mediated dosage compensation active in most somatic tissues, and another system active during early embryogenesis prior to the onset of MSL-mediated dosage compensation. To better understand the developmental constraints on sex chromosome gene expression and evolution, we sequenced mRNA from individual male and female embryos of D. pseudoobscura and D. miranda, from ∼0.5 to 8 hours of development. Autosomal expression levels are highly conserved between these species. But, unlike D. melanogaster, we observe a general lack of dosage compensation in D. pseudoobscura and D. miranda prior to the onset of MSL-mediated dosage compensation. Thus, either there has been a lineage-specific gain or loss in early dosage compensation mechanism(s) or increasing X chromosome dose may strain dosage compensation systems and make them less effective. The extent of female bias on the X chromosomes decreases through developmental time with the establishment of MSL-mediated dosage compensation, but may do so more slowly in D. miranda than D. pseudoobscura. These results also prompt a number of questions about whether species with more sex-linked genes have more sex-specific phenotypes, and how much transcript level variance is tolerable during critical stages of development.

PMID:
24550743
PMCID:
PMC3923672
DOI:
10.1371/journal.pgen.1004159
[PubMed - indexed for MEDLINE]
Free PMC Article
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