Academic journal article Genetics

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes in Caenorhabditis Species

Academic journal article Genetics

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes in Caenorhabditis Species

Article excerpt

SEXUAL reproduction relies on the specialized cell division program of meiosis for the generation of haploid gametes. During meiosis, an elaborate chromosome dance occurs where chromosomes pair side by side, synapse via the elaboration of the synaptonemal complex (SC), a tripartite proteinaceous structure, and undergo crossover recombination to connect homologous chromosomes, thus ensuring that homologs segregate from each other at the first meiotic division (reviewed in Zickler and Kleckner 2015). Defects in chromosome pairing, synapsis, or recombination can lead to infertility or aneuploid progeny, and thus it is critical that germ cells monitor these events and ensure they occur properly. However, sex chromosomes of the heterogametic sex are either partially (e.g., XY in mammalian and Drosophila males) or completely hemizygous (e.g., X0 in a number of insects and worms). Consequently, sex chromosomes, or the underlying meiotic program, must be modified to promote sex chromosome segregation during meiosis.

Meiotic sex chromosome inactivation (MSCI) is the process whereby sex chromosomes accumulate repressive chromatin marks and are transcriptionally silenced (Handel 2004) and has been proposed to be important for sex chromosome transmission during meiosis (reviewed in Checchi and Engebrecht 2011b and Turner 2015). MSCI has been reported to occur in diverse species, including Caenorhabditis elegans (Kelly et al. 2002) and Homo sapiens (de Vries et al. 2012). In C. elegans, MSCI is important for shielding the hemizygous X from checkpoint machinery (Checchi and Engebrecht 2011a). On the other hand, elegant work by Turner and colleagues has demonstrated that MSCI is essential for preventing the expression of a small number of Y-linked genes during male meiosis in mice (Royo et al. 2010). Further, the conservation of MSCI has recently been brought into question, as chickens do not appear to undergo MSCI even though they have differentiated sex chromosomes (Guioli et al. 2012), and in Drosophila, the topic has been highly debated (Vibranovski et al. 2009; Meiklejohn et al. 2011; Mikhaylova and Nurminsky 2011; Vibranovski 2014). Thus, the universality and precise role of MSCI is not currently known.

MSCI has been proposedtobe relatedto, andevolved from, the more general silencing that occurs when any unpaired chromatin is present, termed meiotic silencing of unpaired or unsynapsed chromatin (MSUC) (Maine et al. 2005; Schimenti 2005). However, at least in worms, evidence exists that these processes are not identical and may involve different molecular machinery (Checchi and Engebrecht 2011a). In mice, the tumor suppressor, BRCA1 has been shown to be required for both MSCI and MSUC through recruitment of the checkpoint kinase ATR (Turner et al. 2004, 2005); however, the precise molecular pathway(s) for acquisition of either MSUC or MSCI has not been elucidated.

While reproductive strategies, and sex chromosomes, have evolved independently in many different lineages, the process of meiosis is well conserved. This is illustrated by the robust conservation of the meiotic recombination machinery (Villeneuve and Hillers 2001; Cole et al. 2010). On the other hand, components of the SC are less conserved; however, analyses in the basal metazoan hydra suggests that there is a higher level of conservation of SC components than previously thought (Fraune et al. 2012). Information about the conservation of the molecular machinery that mediates MSCI or MSUC is more limited.

Here we examined meiotic silencing in the elegans group of nematodes, which includes both female/male and independently evolved hermaphroditic/male species (reviewed in Ellis and Lin 2014). These worms are morphologically very similar, yet recent studies indicate that the genetic networks underlying these similarities have diverged substantially (Verster et al. 2014). We found that while MSCI and MSUC are conserved among this group of worms, the repressive chromatin marks that mediate these processes and their regulatory gene networks are distinct, suggesting significant plasticity in the sex chromosome epigenetic landscape. …

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