Regulation of the Different Chromatin States of Autosomes and X Chromosomes in the Germ Line of C. elegans

Abstract

The Maternal-Effect Sterile (MES) proteins are essential for germline viability in Caenorhabditis elegans. Here, we report that MES-4, a SET-domain protein, binds to the autosomes but not to the X chromosomes. MES-2, MES-3, and MES-6 are required to exclude MES-4 and markers of active chromatin from the X chromosomes. These findings strengthen the emerging view that in the C. elegans germ line, the X chromosomes differ in chromatin state from the autosomes and are generally silenced. We propose that all four MES proteins participate in X-chromosome silencing, and that the role of MES-4 is to exclude repressors from the autosomes, thus enabling efficient repression of the Xs.

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

“…Our analysis might be identifying those genes. Second, the X chromosomes of Drosophila and other animals become precociously condensed and inactivated in spermatocytes (11)(12)(13)(14). If X-chromosome inactivation occurs early enough to alter steady-state transcript levels in spermatocytes, then this effect could explain the underrepresentation we observe.…”

“…Indeed, in the only full-genome study of chromosomal bias to date, it was shown that C. elegans has essentially no X-chromosome genes showing male-biased germ line-restricted expression (15). This correlates with an altered chromatin state in those germ cells (11,12).…”

“…However, this may be because of compensation, in advance, for the precocious inactivation of those X chromosomes in preparation for meiosis (20). It certainly seems clear that the X chromosome is a poor location for male-biased gene expression in C. elegans, and in late spermatocytes of Drosophila and humans, where X-chromosome inactivation has been implicated (11,12,15,20). However, X inactivation does not explain the paucity of Xchromosome genes showing male-biased expression in the Drosophila soma, or indeed in the bulk of spermatogenesis.…”

‘Escaping’ the X chromosome leads to increased gene expression in the male germline of Drosophila melanogaster

“…More recent studies have provided empirical support for MSCI in a variety of species, including mammals (Richler et al, 1992;Handel et al, 1994;Turner, 2007), Caenorhabditis elegans (Fong et al, 2002;Kelly et al, 2002) and D. melanogaster (Hense et al, 2007;Vibranovski et al, 2009a). However, there is currently debate regarding the extent of X-linked germline expression silencing in Drosophila and whether it occurs through the same mechanism described as MSCI in other taxa.…”

Trouble in transitioning: activation of zygotic transcription can lead to DNA breakage and genome instability

“…To do so, we took advantage of the fact that the X chromosome in the germ cells of C. elegans is mostly transcriptionally silent. [14][15][16] If ZGA was triggering damage, we reasoned, then we would expect RAD-51 foci to form on the transcriptionally active autosomes, but rarely on the transcriptionally silenced X chromosomes. Using antibodies to differentiate between the autosomes and the X chromosomes, we found that in 98% of the nuclei scored, RAD-51 foci exclusively formed on the autosomes and not on the X chromosomes.…”