Sex chromosome silencing in the marsupial male germ line

doi:10.1073/pnas.0700323104

Sex chromosome silencing in the marsupial male germ line

*Howard Hughes Medical Institute and Department of Molecular Biology, Massachusetts General Hospital, and Department of Genetics, Harvard Medical School, Boston, MA 02114;
^†Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio, TX 78245; and
^‡Department of Biology, University of Texas, San Antonio, TX 78249

Edited by Arthur D. Riggs, Beckman Research Institute of the City of Hope, Duarte, CA, and approved April 20, 2007 (received for review January 12, 2007)

Abstract

In marsupials, dosage compensation involves silencing of the father's X-chromosome. Because no XIST orthologue has been found, how imprinted X-inactivation occurs is unknown. In eutherians, the X is subject to meiotic sex chromosome inactivation (MSCI) in the paternal germ line and persists thereafter as postmeiotic sex chromatin (PMSC). One hypothesis proposes that the paternal X is inherited by the eutherian zygote as a preinactive X and raises the possibility of a similar process in the marsupial germ line. Here we demonstrate that MSCI and PMSC occur in the opossum. Surprisingly, silencing occurs before X–Y association. After MSCI, the X and Y fuse through a dense plate without obvious synapsis. Significantly, sex chromosome silencing continues after meiosis, with the opossum PMSC sharing features of eutherian PMSC. These results reveal a common gametogenic program in two diverse clades of mammals and support the idea that male germ-line silencing may have provided an ancestral form of mammalian dosage compensation.

Footnotes

^§To whom correspondence should be addressed. E-mail: lee{at}molbio.mgh.harvard.edu
Author contributions: J.R.M. and J.T.L. contributed equally to this work; S.H.N., J.R.M., and J.T.L. designed research; S.H.N. performed research; J.L.V. and J.R.M. contributed new reagents/analytic tools; S.H.N. and J.T.L. analyzed data; and S.H.N. and J.T.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0700323104/DC1.
Abbreviations:

XCI,

X-chromosome inactivation;

MSCI,

meiotic sex chromosome inactivation;

PMSC,

postmeiotic sex chromatin;

DP,

dense plate;

XIC,

X-inactivation center;

Pol-II,

polymerase II.