The Chromodomain Protein MRG-1 Facilitates SC-Independent Homologous Pairing during Meiosis in Caenorhabditis elegans

Abstract

Homologous chromosome pairing is a prerequisite to establish physical linkage between homologs, which is critical for faithful chromosome segregation during meiosis I. The establishment of pairing is genetically separable from subsequent synapsis, defined as stabilization of pairing by the synaptonemal complex (SC). The underlying mechanism of presynaptic pairing is poorly understood. In the nematode Caenorhabditis elegans, a unique cis-acting element, the pairing center (PC), is essential for presynaptic pairing; however, it is not known whether and how the remainder of the chromosome contributes to presynaptic pairing. Here we report direct evidence for presynaptic pairing activity intrinsic to non-PC regions, which is facilitated by a conserved chromodomain protein, MRG-1. In mrg-1 loss-of-function mutants, pairing is compromised specifically in non-PC regions, leading to nonhomologous SC assembly. Our data support a model in which presynaptic alignment in non-PC regions collaborates with initial PC pairing to ensure correct homologous synapsis.

Proteasome regulation of the chromodomain protein MRG-1 controls the balance between proliferative fate and differentiation in theC. elegansgerm line

“…7F). It remains possible that MRG-1 activity is restricted to the PZ through some other mechanism, such as posttranslational modification; however, we consider this unlikely because MRG-1 has been shown to have functions in more proximal regions of the gonad, including maintaining genomic integrity in meiotic cells, silencing X-linked genes and facilitating pairing of homologous chromosomes (Dombecki et al, 2011;Fujita et al, 2002;Olgun et al, 2005;Takasaki et al, 2007;Xu et al, 2012). We propose a model in which MRG-1 sets a Fig.…”

“…We confirm that RFP-1 binds to MRG-1, which is homologous to the mammalian MRG15 (MORF4L1) chromodomain protein. MRG-1 has multiple functions in C. elegans, including facilitating synaptonemal complex-independent pairing of homologous chromosomes (Dombecki et al, 2011), maintaining genomic integrity in germ cells (Xu et al, 2012) and repressing the expression of X-linked genes in the germ line (Takasaki et al, 2007). Additionally, MRG-1 is necessary for proliferation of C. elegans primordial germ cells (Fujita et al, 2002;Takasaki et al, 2007), and loss of MRG15 reduces the proliferation capacity of neural precursor cells in mice (Chen et al, 2009).…”

Meiosis

“…Moreover, pre-synaptic alignment has been demonstrated along the entire length of chromosomes (Nabeshima et al, 2011: PMID 21876678). The chromodomain protein MRG-1, present on the autosomes, plays a role in the non-PC mediated homolog alignment and its absence leads to defects in homolog alignment and synapsis of non-PC regions (Dombecki et al, 2011: PMID 22172672). Mutations in the gene encoding the serine/threonine phosphatase PPH-4.1 cause defective autosomal chromosome pairing and synapsis between non-homologous chromosomes.…”

Arabidopsis MRG domain proteins bridge two histone modifications to elevate expression of flowering genes

“…Due to these dual functions, the deletion of Eaf3 greatly alters the global genomic profile of histone modification, with increased acetylation levels at coding sequences and decreased acetylation levels at the promoter regions (21). MRG-1 , an MRG15 homologue in C. elegans , was recently reported to be involved in homologous chromosome pairing, which is independent of both the pairing centre and meiotic homologous recombination (27). These data suggest that the function of MRG15 family proteins have diversified in different species and participate in varied biological processes.…”