A Component of C. elegans Meiotic Chromosome Axes at the Interface of Homolog Alignment, Synapsis, Nuclear Reorganization, and Recombination

Abstract

A universal feature of meiotic prophase is the pairing of homologous chromosomes, a fundamental prerequisite for the successful completion of all subsequent meiotic events. HIM-3 is a Caenorhabditis elegans meiosis-specific non-cohesin component of chromosome axes that is required for synapsis. Our characterization of new him-3 alleles reveals previously unknown functions for the protein. HIM-3 is required for the establishment of initial contacts between homologs, for the nuclear reorganization characteristic of early meiotic prophase, and for the coordination of these events with synaptonemal complex (SC) assembly. Despite the absence of homolog alignment, we find that recombination is initiated efficiently, indicating that initial pairing is not a prerequisite for early steps of the recombination pathway. Surprisingly, RAD-51-marked recombination intermediates disappear with apparent wild-type kinetics in him-3 null mutants in which homologs are spatially unavailable for recombination, raising the possibility that HIM-3's presence at chromosome axes inhibits the use of sister chromatids as templates for repair. We propose that HIM-3 is a molecular link between multiple landmark events of meiotic prophase; it is critical for establishing chromosome identity by configuring homologs to facilitate their recognition while simultaneously imposing structural constraints that later promote the formation of the crossover essential for proper segregation.

Molecular Assembly of Meiotic Proteins Asy1 and Zyp1 and Pairing Promiscuity in Rye (Secale cereale L.) and Its Synaptic Mutant sy10

“…The protein Zyp1 of A. thaliana is a component of the transverse filaments of the SC (Higgins et al 2005) and has been shown to have equivalent proteins in yeast (Sym et al 1993), mammals (Heyting 1996), Caenorhabditis elegans (Couteau et al 2004), and D. melanogaster (Page and Hawley 2004). Antibodies raised against these two proteins of A. thaliana were used in this study to monitor and compare the assembly of bivalents in wild type and its synaptic mutant sy10.…”

ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis

“…Studies indicate that a protein complex comprising Hop1, Red1, and Mek1 is instrumental in establishing interhomolog bias by virtue of its capacity to actively prevent Rad51-mediated intersister chromatid repair (Hollingsworth and Ponte 1997;Woltering et al 2000;Niu et al 2005). It has also been proposed that HIM-3, a protein that is related to Hop1 on the basis that it contains a HORMA domain and is a component of chromosome axes, may also prevent the use of sister chromatids for repair during meiosis in Caenorhabditis elegans (Zetka et al 1999;Couteau et al 2004).…”

Multiple Barriers to Nonhomologous DNA End Joining During Meiosis inDrosophila

“…In addition, for a crossover to generate a chiasma, the crossover must occur between homologs and not between sisters. Thus, there appears to be a barrier (or semipermeable barrier) between the sister chromatids that promotes homolog exchange, possibly involving the activity of chromosome axis proteins (Couteau et al 2004;Webber et al 2004;Niu et al 2005;Kim et al 2010;Li et al 2011). Finally, homologous repair must be promoted while more error-prone mechanisms that could introduce de novo mutations in the germline such as nonhomologous end joining (NHEJ) are inhibited.…”