DOI: 10.1101/gad.1011602. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in <i>C. elegans</i>

Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans

10.1101/gad.1011602

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

Analysis of Caenorhabditis elegans syp-1 mutants reveals that both synapsis-dependent and -independent mechanisms contribute to stable, productive alignment of homologous chromosomes during meiotic prophase. Early prophase nuclei undergo normal reorganization insyp-1 mutants, and chromosomes initially pair. However, the polarized nuclear organization characteristic of early prophase persists for a prolonged period, and homologs dissociate prematurely; furthermore, the synaptonemal complex (SC) is absent. The predicted structure of SYP-1, its localization at the interface between intimately paired, lengthwise-aligned pachytene homologs, and its kinetics of localization with chromosomes indicate that SYP-1 is an SC structural component. A severe reduction in crossing over together with evidence for accumulated recombination intermediates in syp-1mutants indicate that initial pairing is not sufficient for completion of exchange and implicates the SC in promoting crossover recombination. Persistence of polarized nuclear organization in syp-1 mutants suggests that SC polymerization may provide a motive force or signal that drives redispersal of chromosomes. Whereas our analysis suggests that the SC is required to stabilize pairing along the entire lengths of chromosomes, striking differences in peak pairing levels for opposite ends of chromosomes in syp-1 mutants reveal the existence of an additional mechanism that can promote local stabilization of pairing, independent of synapsis.

Bibliography

MacQueen, A. J., ColaiÃ¡covo, M. P., McDonald, K., & Villeneuve, A. M. (2002). Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes & Development, 16(18), 2428â2442.

Authors 4

Amy J. MacQueen (first)
Mónica P. Colaiácovo (additional)
Kent McDonald (additional)
Anne M. Villeneuve (additional)

References 49 Referenced 351

Albertson D.G. Rose A.M. Villeneuve A.M. (1997) Chromosome organization, mitosis, and meiosis. in C. elegans II, ed Riddle D.L. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 47–78.
10.1073/pnas.92.18.8259
10.1016/0092-8674(92)90446-J
10.1051/medsci/20031967725
10.1101/gad.864101
10.1093/genetics/162.1.113 / Genetics / A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the C. elegans germ line. by Colaiácovo (2002)
10.1016/S0092-8674(00)81481-6
10.1083/jcb.148.3.417
10.1016/S1097-2765(00)80438-4
10.1007/BF00292857
10.1093/genetics/94.3.625 / Genetics / Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. by Hawley (1980)
10.1093/genetics/91.1.67 / Genetics / Nondisjunction mutants of the nematode Caenorhabditis elegans. by Hodgkin (1979)
10.1093/genetics/156.2.617 / Genetics / Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. by Kelly (2000)
10.1016/S0092-8674(00)81480-4
10.1016/S0959-440X(97)80056-5
10.1101/gad.902601
10.1007/BF00294052
10.1007/BF00293532
10.1385/1-59259-201-5:77
10.1093/genetics/120.4.987 / Genetics / The effects of translocations on recombination frequency in Caenorhabditis elegans. by McKim (1988)
10.1093/genetics/134.3.749 / Genetics / Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. by McKim (1993)
10.1002/j.1460-2075.1992.tb05616.x / EMBO J. / A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. by Meuwissen (1992)
{'key': '2021111508094628000_16.18.2428.23', 'first-page': '41', 'article-title': 'Structure and function of the synaptonemal complex.', 'volume': '61 Suppl.', 'author': 'Moses', 'year': '1969', 'journal-title': 'Genetics'} / Genetics / Structure and function of the synaptonemal complex. by Moses (1969)
10.1093/genetics/141.1.75 / Genetics / Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. by Nag (1995)
10.1093/genetics/158.3.1013 / Genetics / The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. by Novak (2001)
10.1101/gad.935001
10.1016/S1097-2765(00)00059-9
.
10.1101/gad.9.21.2684
10.1101/gad.11.20.2600
10.1139/g92-162 / Genome / Meiotic chromosome structure: Relationship between the synaptonemal complex and the chromatid cores. by Rufas (1992)
Schedl T. (1997) Developmental genetics of the germ line. in C. elegans II, ed Riddle D.L. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 241–269.
10.1038/35085086
10.1016/0092-8674(92)90447-K
10.1073/pnas.93.17.9043
10.1016/0092-8674(94)90197-X
10.1016/0092-8674(93)90114-6
10.1128/MCB.22.9.3078-3088.2002
10.1093/genetics/149.2.817 / Genetics / Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. by Tung (1998)
10.1093/genetics/136.3.887 / Genetics / A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. by Villeneuve (1994)
10.1016/S0092-8674(01)00500-1
10.1146/annurev.ge.18.120184.001555
10.1038/88878
10.1093/genetics/131.3.609 / Genetics / A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. by Williams (1992)
10.1002/pro.5560060606
10.1093/genetics/153.3.1271 / Genetics / Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. by Zalevsky (1999)
10.1101/gad.13.17.2258
10.1146/annurev.genet.32.1.619
10.1146/annurev.genet.33.1.603

Dates

Type	When
Created	22 years, 11 months ago (Sept. 16, 2002, 12:40 p.m.)
Deposited	3 years, 9 months ago (Nov. 15, 2021, 11:15 a.m.)
Indexed	4 weeks, 2 days ago (July 23, 2025, 8:49 a.m.)
Issued	22 years, 11 months ago (Sept. 15, 2002)
Published	22 years, 11 months ago (Sept. 15, 2002)
Published Online	22 years, 11 months ago (Sept. 15, 2002)
Published Print	22 years, 11 months ago (Sept. 15, 2002)

Funders 0

None

BibTeX

@article{MacQueen_2002, title={Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans}, volume={16}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.1011602}, DOI={10.1101/gad.1011602}, number={18}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={MacQueen, Amy J. and Colaiácovo, Mónica P. and McDonald, Kent and Villeneuve, Anne M.}, year={2002}, month=sep, pages={2428–2442} }

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  "ISSN": [
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    "1549-5477"
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  "subject": [],
  "container-title-short": "Genes Dev.",
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