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. 1993 Jul;134(3):749–768. doi: 10.1093/genetics/134.3.749

Two Types of Sites Required for Meiotic Chromosome Pairing in Caenorhabditis Elegans

K S McKim 1, K Peters 1, A M Rose 1
PMCID: PMC1205513  PMID: 8349107

Abstract

Previous studies have shown that isolated portions of Caenorhabditis elegans chromosomes are not equally capable of meiotic exchange. These results led to the proposal that a homolog recognition region (HRR), defined as the region containing those sequences enabling homologous chromosomes to pair and recombine, is localized near one end of each chromosome. Using translocations and duplications we have localized the chromosome I HRR to the right end. Whereas the other half of chromosome I did not confer any ability for homologs to pair and recombine, deficiencies in this region dominantly suppressed recombination to the middle of the chromosome. These deletions may have disrupted pairing mechanisms that are secondary to and require an HRR. Thus, the processes of pairing and recombination appear to utilize at least two chromosomal elements, the HRR and other pairing sites. For example, terminal sequences from other chromosomes increase the ability of free duplications to recombine with their normal homologs, suggesting that telomere-associated sequences, homologous or nonhomologous, play a role in facilitating meiotic exchange. Recombination can also initiate at internal sites separated from the HRR by chromosome rearrangement, such as deletions of the unc-54 region of chromosome I. When crossing over was suppressed in a region of chromosome I, compensatory increases were observed in other regions. Thus, the presence of the HRR enabled recombination to occur but did not determine the distribution of the crossover events. It seems most likely that there are multiple initiation sites for recombination once homolog recognition has been achieved.

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Selected References

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  1. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  2. Albertson D. G., Thomson J. N. The kinetochores of Caenorhabditis elegans. Chromosoma. 1982;86(3):409–428. doi: 10.1007/BF00292267. [DOI] [PubMed] [Google Scholar]
  3. Anderson P., Brenner S. A selection for myosin heavy chain mutants in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4470–4474. doi: 10.1073/pnas.81.14.4470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  5. Baker B. S., Carpenter A. T. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics. 1972 Jun;71(2):255–286. doi: 10.1093/genetics/71.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burnham C. R., Stout J. T., Weinheimer W. H., Kowles R. V., Phillips R. L. Chromosome pairing in maize. Genetics. 1972 May;71(1):111–126. doi: 10.1093/genetics/71.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carpenter A. T. Gene conversion, recombination nodules, and the initiation of meiotic synapsis. Bioessays. 1987 May;6(5):232–236. doi: 10.1002/bies.950060510. [DOI] [PubMed] [Google Scholar]
  9. Chandley A. C. A model for effective pairing and recombination at meiosis based on early replicating sites (R-bands) along chromosomes. Hum Genet. 1986 Jan;72(1):50–57. doi: 10.1007/BF00278817. [DOI] [PubMed] [Google Scholar]
  10. Comings D. E., Riggs A. D. Molecular mechanisms of chromosome pairing, folding and function. Nature. 1971 Sep 3;233(5314):48–50. doi: 10.1038/233048a0. [DOI] [PubMed] [Google Scholar]
  11. Engebrecht J., Hirsch J., Roeder G. S. Meiotic gene conversion and crossing over: their relationship to each other and to chromosome synapsis and segregation. Cell. 1990 Sep 7;62(5):927–937. doi: 10.1016/0092-8674(90)90267-i. [DOI] [PubMed] [Google Scholar]
  12. Ferguson E. L., Horvitz H. R. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics. 1985 May;110(1):17–72. doi: 10.1093/genetics/110.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hawley R. S., Arbel T. Yeast genetics and the fall of the classical view of meiosis. Cell. 1993 Feb 12;72(3):301–303. doi: 10.1016/0092-8674(93)90108-3. [DOI] [PubMed] [Google Scholar]
  14. Hawley R. S. Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. Genetics. 1980 Mar;94(3):625–646. doi: 10.1093/genetics/94.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Herman R. K., Albertson D. G., Brenner S. Chromosome rearrangements in Caenorhabditis elegans. Genetics. 1976 May;83(1):91–105. doi: 10.1093/genetics/83.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Herman R. K., Kari C. K., Hartman P. S. Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics. 1982 Nov;102(3):379–400. doi: 10.1093/genetics/102.3.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Herman R. K., Kari C. K. Recombination between small X chromosome duplications and the X chromosome in Caenorhabditis elegans. Genetics. 1989 Apr;121(4):723–737. doi: 10.1093/genetics/121.4.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Herman R. K., Madl J. E., Kari C. K. Duplications in Caenorhabditis elegans. Genetics. 1979 Jun;92(2):419–435. doi: 10.1093/genetics/92.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hodgkin J., Horvitz H. R., Brenner S. Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics. 1979 Jan;91(1):67–94. doi: 10.1093/genetics/91.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Holliday R. Recombination and meiosis. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):359–370. doi: 10.1098/rstb.1977.0024. [DOI] [PubMed] [Google Scholar]
  21. Horvitz H. R., Brenner S., Hodgkin J., Herman R. K. A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol Gen Genet. 1979 Sep;175(2):129–133. doi: 10.1007/BF00425528. [DOI] [PubMed] [Google Scholar]
  22. Jones G. H. The control of chiasma distribution. Symp Soc Exp Biol. 1984;38:293–320. [PubMed] [Google Scholar]
  23. Kim J. S., Rose A. M. The effect of gamma radiation on recombination frequency in Caenorhabditis elegans. Genome. 1987 Jun;29(3):457–462. doi: 10.1139/g87-079. [DOI] [PubMed] [Google Scholar]
  24. Kleckner N., Padmore R., Bishop D. K. Meiotic chromosome metabolism: one view. Cold Spring Harb Symp Quant Biol. 1991;56:729–743. doi: 10.1101/sqb.1991.056.01.082. [DOI] [PubMed] [Google Scholar]
  25. Lambie E. J., Roeder G. S. A yeast centromere acts in cis to inhibit meiotic gene conversion of adjacent sequences. Cell. 1988 Mar 25;52(6):863–873. doi: 10.1016/0092-8674(88)90428-x. [DOI] [PubMed] [Google Scholar]
  26. Lichten M., Borts R. H., Haber J. E. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics. 1987 Feb;115(2):233–246. doi: 10.1093/genetics/115.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Maguire M. P. Evidence on the nature and complexity of the mechanism of chiasma maintenance in maize. Genet Res. 1985 Feb;45(1):37–49. doi: 10.1017/s0016672300021947. [DOI] [PubMed] [Google Scholar]
  28. Maguire M. P. The mechanism of meiotic homologue pairing. J Theor Biol. 1984 Feb 21;106(4):605–615. doi: 10.1016/0022-5193(84)90010-9. [DOI] [PubMed] [Google Scholar]
  29. McKim K. S., Howell A. M., Rose A. M. The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics. 1988 Dec;120(4):987–1001. doi: 10.1093/genetics/120.4.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McKim K. S., Rose A. M. Chromosome I duplications in Caenorhabditis elegans. Genetics. 1990 Jan;124(1):115–132. doi: 10.1093/genetics/124.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meneely P. M., Herman R. K. Suppression and function of X-linked lethal and sterile mutations in Caenorhabditis elegans. Genetics. 1981 Jan;97(1):65–84. doi: 10.1093/genetics/97.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Powers P. A., Smithies O. Short gene conversions in the human fetal globin gene region: a by-product of chromosome pairing during meiosis? Genetics. 1986 Feb;112(2):343–358. doi: 10.1093/genetics/112.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Prasad S. S., Baillie D. L. Evolutionarily conserved coding sequences in the dpy-20-unc-22 region of Caenorhabditis elegans. Genomics. 1989 Aug;5(2):185–198. doi: 10.1016/0888-7543(89)90045-1. [DOI] [PubMed] [Google Scholar]
  34. Rose A. M., Baillie D. L. A mutation in Caenorhabditis elegans that increases recombination frequency more than threefold. Nature. 1979 Oct 18;281(5732):599–600. doi: 10.1038/281599a0. [DOI] [PubMed] [Google Scholar]
  35. Rose A. M., Baillie D. L., Curran J. Meiotic pairing behavior of two free duplications of linkage group I in Caenorhabditis elegans. Mol Gen Genet. 1984;195(1-2):52–56. doi: 10.1007/BF00332723. [DOI] [PubMed] [Google Scholar]
  36. Rose A. M., Baillie D. L. The Effect of Temperature and Parental Age on Recombination and Nondisjunction in CAENORHABDITIS ELEGANS. Genetics. 1979 Jun;92(2):409–418. doi: 10.1093/genetics/92.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rosenbluth R. E., Baillie D. L. The genetic analysis of a reciprocal translocation, eT1(III; V), in Caenorhabditis elegans. Genetics. 1981 Nov-Dec;99(3-4):415–428. doi: 10.1093/genetics/99.3-4.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rosenbluth R. E., Johnsen R. C., Baillie D. L. Pairing for recombination in LGV of Caenorhabditis elegans: a model based on recombination in deficiency heterozygotes. Genetics. 1990 Mar;124(3):615–625. doi: 10.1093/genetics/124.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Smithies O., Powers P. A. Gene conversions and their relation to homologous chromosome pairing. Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):291–302. doi: 10.1098/rstb.1986.0008. [DOI] [PubMed] [Google Scholar]
  40. Starr T., Howell A. M., McDowall J., Peters K., Rose A. M. Isolation and mapping of DNA probes within the linkage group I gene cluster of Caenorhabditis elegans. Genome. 1989 Jun;32(3):365–372. doi: 10.1139/g89-456. [DOI] [PubMed] [Google Scholar]
  41. Surosky R. T., Tye B. K. Meiotic disjunction of homologs in Saccharomyces cerevisiae is directed by pairing and recombination of the chromosome arms but not by pairing of the centromeres. Genetics. 1988 Jun;119(2):273–287. doi: 10.1093/genetics/119.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Szauter P. An analysis of regional constraints on exchange in Drosophila melanogaster using recombination-defective meiotic mutants. Genetics. 1984 Jan;106(1):45–71. doi: 10.1093/genetics/106.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zetka M. C., Rose A. M. Sex-related differences in crossing over in Caenorhabditis elegans. Genetics. 1990 Oct;126(2):355–363. doi: 10.1093/genetics/126.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zetka M. C., Rose A. M. The meiotic behavior of an inversion in Caenorhabditis elegans. Genetics. 1992 Jun;131(2):321–332. doi: 10.1093/genetics/131.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zickler D., Moreau P. J., Huynh A. D., Slezec A. M. Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics. 1992 Sep;132(1):135–148. doi: 10.1093/genetics/132.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]

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