Homologous Chromosome Pairing and Synapsis during Oogenesis

Mlynarczyk-Evans, Susanna; Villeneuve, Anne M.

doi:10.1002/9780470687970.ch5

Cited by 9 publications

(5 citation statements)

References 134 publications

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“…Substantial progress has been made recently in illuminating a conserved mechanism that mediates chromosome movements that likely contribute to the chromosome sorting process in diverse organisms (for reviews, see [1] – [3] ). The common feature of these large-scale spatial reorganization mechanisms involves tethering of one or two specified site(s) on a chromosome to conserved nuclear envelope (NE)- spanning protein complexes, thereby coupling the chromosomes to the cytoskeletal motility apparatus that can transmit forces to drive chromosome movement.…”

Section: Introductionmentioning

confidence: 99%

Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis

2011

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During early meiotic prophase, a nucleus-wide reorganization leads to sorting of chromosomes into homologous pairs and to establishing associations between homologous chromosomes along their entire lengths. Here, we investigate global features of chromosome organization during this process, using a chromosome painting method in whole-mount Caenorhabditis elegans gonads that enables visualization of whole chromosomes along their entire lengths in the context of preserved 3D nuclear architecture. First, we show that neither spatial proximity of premeiotic chromosome territories nor chromosome-specific timing is a major factor driving homolog pairing. Second, we show that synaptonemal complex-independent associations can support full lengthwise juxtaposition of homologous chromosomes. Third, we reveal a prominent elongation of chromosome territories during meiotic prophase that initiates prior to homolog association and alignment. Mutant analysis indicates that chromosome movement mediated by association of chromosome pairing centers (PCs) with mobile patches of the nuclear envelope (NE)–spanning SUN-1/ZYG-12 protein complexes is not the primary driver of territory elongation. Moreover, we identify new roles for the X chromosome PC (X-PC) and X-PC binding protein HIM-8 in promoting elongation of X chromosome territories, separable from their role(s) in mediating local stabilization of pairing and association of X chromosomes with mobile SUN-1/ZYG-12 patches. Further, we present evidence that HIM-8 functions both at and outside of PCs to mediate chromosome territory elongation. These and other data support a model in which synapsis-independent elongation of chromosome territories, driven by PC binding proteins, enables lengthwise juxtaposition of chromosomes, thereby facilitating assessment of their suitability as potential pairing partners.

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Section: Introductionmentioning

confidence: 99%

Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis

2011

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“…Cohesin proteins and other conserved chromosome axis proteins such as HIM-3 (Zetka et al 1999) constitute the axial structure of the SC, whereas coiled-coil proteins such as SYP-1 (MacQueen et al 2002) constitute the central region structure of the SC (reviewed in Mlynarczyk-Evans and Villeneuve 2010; Lui and Colaiacovo 2013). Pairing of homologs and assembly of SC structures are accompanied by a transient clustering of chromosomes within the nucleus and occur in a region of the gonad known as the transition zone (TZ), corresponding to the leptotene and zygotene stages of meiotic prophase.…”

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confidence: 99%

Assembly of the Synaptonemal Complex Is a Highly Temperature-Sensitive Process That Is Supported by PGL-1 DuringCaenorhabditis elegansMeiosis

Bilgir

Dombecki

Chen

et al. 2013

G3 Genes|Genomes|Genetics

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Successful chromosome segregation during meiosis depends on the synaptonemal complex (SC), a structure that stabilizes pairing between aligned homologous chromosomes. Here we show that SC assembly is a temperature-sensitive process during Caenorhabditis elegans meiosis. Temperature sensitivity of SC assembly initially was revealed through identification of the germline-specific P-granule component PGL-1 as a factor promoting stable homolog pairing. Using an assay system that monitors homolog pairing in vivo, we showed that depletion of PGL-1 at 25° disrupts homolog pairing. Analysis of homolog pairing at other chromosomal loci in a pgl-1−null mutant revealed a pairing defect similar to that observed in mutants lacking SC central region components. Furthermore, loss of pgl-1 function at temperatures ≥25° results in severe impairment in loading of SC central region component SYP-1 onto chromosomes, resulting in formation of SYP-1 aggregates. SC assembly is also temperature sensitive in wild-type worms, which exhibit similar SYP-1 loading defects and formation of SYP-1 aggregates at temperatures ≥26.5°. Temperature shift analyses suggest that assembly of the SC is temperature sensitive, but maintenance of the SC is not. We suggest that the temperature sensitive (ts) nature of SC assembly may contribute to fitness and adaptation capacity in C. elegans by enabling meiotic disruption in response to environmental change, thereby increasing the production of male progeny available for outcrossing.

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“…First, the SC serves to stabilize and maintain tight associations along the lengths of aligned homologs (reviewed in Mlynarczyk-Evans and Villeneuve 2010). This is true Supporting information is available online at http:/ /www.genetics.org/ cgi/content/full/genetics.110.115501/DC1.…”

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The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis

2010

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The synaptonemal complex (SC) is a highly ordered proteinaceous structure that assembles at the interface between aligned homologous chromosomes during meiotic prophase. The SC has been demonstrated to function both in stabilization of homolog pairing and in promoting the formation of interhomolog crossovers (COs). How the SC provides these functions and whether it also plays a role in inhibiting CO formation has been a matter of debate. Here we provide new insight into assembly and function of the SC by investigating the consequences of reducing (but not eliminating) SYP-1, a major structural component of the SC central region, during meiosis in Caenorhabditis elegans. First, we find an increased incidence of double CO (DCO) meiotic products following partial depletion of SYP-1 by RNAi, indicating a role for SYP-1 in mechanisms that normally limit crossovers to one per homolog pair per meiosis. Second, syp-1 RNAi worms exhibit both a strong preference for COs to occur on the left half of the X chromosome and a significant bias for SYP-1 protein to be associated with the left half of the chromosome, implying that the SC functions locally in promoting COs. Distribution of SYP-1 on chromosomes in syp-1 RNAi germ cells provides strong corroboration for cooperative assembly of the SC central region and indicates that SYP-1 preferentially associates with X chromosomes when it is present in limiting quantities. Further, the observed biases in the distribution of both COs and SYP-1 protein support models in which synapsis initiates predominantly in the vicinity of pairing centers (PCs). However, discontinuities in SC structure and clear gaps between localized foci of PC-binding protein HIM-8 and X chromosome-associated SYP-1 stretches allow refinement of models for the role of PCs in promoting synapsis. Our data suggest that the CO landscape is shaped by a combination of three attributes of the SC central region: a CO-promoting activity that functions locally at CO sites, a cooperative assembly process that enables CO formation in regions distant from prominent sites of synapsis initiation, and CO-inhibitory role(s) that limit CO number.

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Homologous Chromosome Pairing and Synapsis during Oogenesis

Cited by 9 publications

References 134 publications

Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis

Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of X Chromosome Territories during Caenorhabditis elegans Meiosis

Assembly of the Synaptonemal Complex Is a Highly Temperature-Sensitive Process That Is Supported by PGL-1 DuringCaenorhabditis elegansMeiosis

The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis

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