Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.

In the male mouse the X and Y chromosomes pair and recombine within the small pseudoautosomal region. Genes located on the unsynapsed segments of the X and Y are transcriptionally silenced at pachytene by Meiotic Sex Chromosome Inactivation (MSCI). The degree to which MSCI is conserved in other vert...

Full description

Bibliographic Details
Main Authors: Silvana Guioli, Robin Lovell-Badge, James M A Turner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3297585?pdf=render
id doaj-29977a50ea8a4d558dee2735fb4dedfb
record_format Article
spelling doaj-29977a50ea8a4d558dee2735fb4dedfb2020-11-25T01:19:26ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0183e100256010.1371/journal.pgen.1002560Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.Silvana GuioliRobin Lovell-BadgeJames M A TurnerIn the male mouse the X and Y chromosomes pair and recombine within the small pseudoautosomal region. Genes located on the unsynapsed segments of the X and Y are transcriptionally silenced at pachytene by Meiotic Sex Chromosome Inactivation (MSCI). The degree to which MSCI is conserved in other vertebrates is currently unclear. In the female chicken the ZW bivalent is thought to undergo a transient phase of full synapsis at pachytene, starting from the homologous ends and spreading through the heterologous regions. It has been proposed that the repair of the ZW DNA double-strand breaks (DSBs) is postponed until diplotene and that the ZW bivalent is subject to MSCI, which is independent of its synaptic status. Here we present a distinct model of meiotic pairing and silencing of the ZW pair during chicken oogenesis. We show that, in most oocytes, DNA DSB foci on the ZW are resolved by the end of pachytene and that the ZW desynapses in broad synchrony with the autosomes. We unexpectedly find that ZW pairing is highly error prone, with many oocytes failing to engage in ZW synapsis and crossover formation. Oocytes with unsynapsed Z and W chromosomes nevertheless progress to the diplotene stage, suggesting that a checkpoint does not operate during pachytene in the chicken germ line. Using a combination of epigenetic profiling and RNA-FISH analysis, we find no evidence for MSCI, associated with neither the asynaptic ZW, as described in mammals, nor the synaptic ZW. The lack of conservation of MSCI in the chicken reopens the debate about the evolution of MSCI and its driving forces.http://europepmc.org/articles/PMC3297585?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Silvana Guioli
Robin Lovell-Badge
James M A Turner
spellingShingle Silvana Guioli
Robin Lovell-Badge
James M A Turner
Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
PLoS Genetics
author_facet Silvana Guioli
Robin Lovell-Badge
James M A Turner
author_sort Silvana Guioli
title Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
title_short Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
title_full Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
title_fullStr Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
title_full_unstemmed Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
title_sort error-prone zw pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-01-01
description In the male mouse the X and Y chromosomes pair and recombine within the small pseudoautosomal region. Genes located on the unsynapsed segments of the X and Y are transcriptionally silenced at pachytene by Meiotic Sex Chromosome Inactivation (MSCI). The degree to which MSCI is conserved in other vertebrates is currently unclear. In the female chicken the ZW bivalent is thought to undergo a transient phase of full synapsis at pachytene, starting from the homologous ends and spreading through the heterologous regions. It has been proposed that the repair of the ZW DNA double-strand breaks (DSBs) is postponed until diplotene and that the ZW bivalent is subject to MSCI, which is independent of its synaptic status. Here we present a distinct model of meiotic pairing and silencing of the ZW pair during chicken oogenesis. We show that, in most oocytes, DNA DSB foci on the ZW are resolved by the end of pachytene and that the ZW desynapses in broad synchrony with the autosomes. We unexpectedly find that ZW pairing is highly error prone, with many oocytes failing to engage in ZW synapsis and crossover formation. Oocytes with unsynapsed Z and W chromosomes nevertheless progress to the diplotene stage, suggesting that a checkpoint does not operate during pachytene in the chicken germ line. Using a combination of epigenetic profiling and RNA-FISH analysis, we find no evidence for MSCI, associated with neither the asynaptic ZW, as described in mammals, nor the synaptic ZW. The lack of conservation of MSCI in the chicken reopens the debate about the evolution of MSCI and its driving forces.
url http://europepmc.org/articles/PMC3297585?pdf=render
work_keys_str_mv AT silvanaguioli errorpronezwpairingandnoevidenceformeioticsexchromosomeinactivationinthechickengermline
AT robinlovellbadge errorpronezwpairingandnoevidenceformeioticsexchromosomeinactivationinthechickengermline
AT jamesmaturner errorpronezwpairingandnoevidenceformeioticsexchromosomeinactivationinthechickengermline
_version_ 1725138331232108544