Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Sep;141(1):159–179. doi: 10.1093/genetics/141.1.159

Meiotic Recombination, Noncoding DNA and Genomic Organization in Caenorhabditis Elegans

T M Barnes 1, Y Kohara 1, A Coulson 1, S Hekimi 1
PMCID: PMC1206715  PMID: 8536965

Abstract

The genetic map of each Caenorhabditis elegans chromosome has a central gene cluster (less pronounced on the X chromosome) that contains most of the mutationally defined genes. Many linkage group termini also have clusters, though involving fewer loci. We examine the factors shaping the genetic map by analyzing the rate of recombination and gene density across the genome using the positions of cloned genes and random cDNA clones from the physical map. Each chromosome has a central gene-dense region (more diffuse on the X) with discrete boundaries, flanked by gene-poor regions. Only autosomes have reduced rates of recombination in these gene-dense regions. Cluster boundaries appear discrete also by recombination rate, and the boundaries defined by recombination rate and gene density mostly, but not always, coincide. Terminal clusters have greater gene densities than the adjoining arm but similar recombination rates. Thus, unlike in other species, most exchange in C. elegans occurs in gene-poor regions. The recombination rate across each cluster is constant and similar; and cluster size and gene number per chromosome are independent of the physical size of chromosomes. We propose a model of how this genome organization arose.

Full Text

The Full Text of this article is available as a PDF (5.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Bernardi G. The isochore organization of the human genome and its evolutionary history--a review. Gene. 1993 Dec 15;135(1-2):57–66. doi: 10.1016/0378-1119(93)90049-9. [DOI] [PubMed] [Google Scholar]
  3. Cangiano G., La Volpe A. Repetitive DNA sequences located in the terminal portion of the Caenorhabditis elegans chromosomes. Nucleic Acids Res. 1993 Mar 11;21(5):1133–1139. doi: 10.1093/nar/21.5.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chakravarti A. A graphical representation of genetic and physical maps: the Marey map. Genomics. 1991 Sep;11(1):219–222. doi: 10.1016/0888-7543(91)90123-v. [DOI] [PubMed] [Google Scholar]
  5. Charlesworth B., Langley C. H., Stephan W. The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics. 1986 Apr;112(4):947–962. doi: 10.1093/genetics/112.4.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chuang P. T., Albertson D. G., Meyer B. J. DPY-27:a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell. 1994 Nov 4;79(3):459–474. doi: 10.1016/0092-8674(94)90255-0. [DOI] [PubMed] [Google Scholar]
  8. Civardi L., Xia Y., Edwards K. J., Schnable P. S., Nikolau B. J. The relationship between genetic and physical distances in the cloned a1-sh2 interval of the Zea mays L. genome. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8268–8272. doi: 10.1073/pnas.91.17.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Coulson A., Sulston J., Brenner S., Karn J. Toward a physical map of the genome of the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7821–7825. doi: 10.1073/pnas.83.20.7821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dujon B., Alexandraki D., André B., Ansorge W., Baladron V., Ballesta J. P., Banrevi A., Bolle P. A., Bolotin-Fukuhara M., Bossier P. Complete DNA sequence of yeast chromosome XI. Nature. 1994 Jun 2;369(6479):371–378. doi: 10.1038/369371a0. [DOI] [PubMed] [Google Scholar]
  11. Emmons S. W., Rosenzweig B., Hirsh D. Arrangement of repeated sequences in the DNA of the nematode Caenorhabditis elegans. J Mol Biol. 1980 Dec 25;144(4):481–500. doi: 10.1016/0022-2836(80)90333-2. [DOI] [PubMed] [Google Scholar]
  12. Felsenstein K. M., Emmons S. W. Nematode repetitive DNA with ARS and segregation function in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Feb;8(2):875–883. doi: 10.1128/mcb.8.2.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gibson T. J., Rosenthal A., Waterston R. H. Lorist6, a cosmid vector with BamHI, NotI, ScaI and HindIII cloning sites and altered neomycin phosphotransferase gene expression. Gene. 1987;53(2-3):283–286. doi: 10.1016/0378-1119(87)90017-5. [DOI] [PubMed] [Google Scholar]
  14. Greenwald I., Coulson A., Sulston J., Priess J. Correlation of the physical and genetic maps in the lin-12 region of Caenorhabditis elegans. Nucleic Acids Res. 1987 Mar 11;15(5):2295–2307. doi: 10.1093/nar/15.5.2295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Ikemura T., Wada K. Evident diversity of codon usage patterns of human genes with respect to chromosome banding patterns and chromosome numbers; relation between nucleotide sequence data and cytogenetic data. Nucleic Acids Res. 1991 Aug 25;19(16):4333–4339. doi: 10.1093/nar/19.16.4333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johnston M., Andrews S., Brinkman R., Cooper J., Ding H., Dover J., Du Z., Favello A., Fulton L., Gattung S. Complete nucleotide sequence of Saccharomyces cerevisiae chromosome VIII. Science. 1994 Sep 30;265(5181):2077–2082. doi: 10.1126/science.8091229. [DOI] [PubMed] [Google Scholar]
  20. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kennedy B. P., Aamodt E. J., Allen F. L., Chung M. A., Heschl M. F., McGhee J. D. The gut esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Mol Biol. 1993 Feb 20;229(4):890–908. doi: 10.1006/jmbi.1993.1094. [DOI] [PubMed] [Google Scholar]
  22. La Volpe A., Ciaramella M., Bazzicalupo P. Structure, evolution and properties of a novel repetitive DNA family in Caenorhabditis elegans. Nucleic Acids Res. 1988 Sep 12;16(17):8213–8231. doi: 10.1093/nar/16.17.8213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Madl J. E., Herman R. K. Polyploids and sex determination in Caenorhabditis elegans. Genetics. 1979 Oct;93(2):393–402. doi: 10.1093/genetics/93.2.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. McKim K. S., Peters K., Rose A. M. Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics. 1993 Jul;134(3):749–768. doi: 10.1093/genetics/134.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Meyer B. J., Casson L. P. Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell. 1986 Dec 26;47(6):871–881. doi: 10.1016/0092-8674(86)90802-0. [DOI] [PubMed] [Google Scholar]
  27. Mouchiroud D., D'Onofrio G., Aïssani B., Macaya G., Gautier C., Bernardi G. The distribution of genes in the human genome. Gene. 1991 Apr;100:181–187. doi: 10.1016/0378-1119(91)90364-h. [DOI] [PubMed] [Google Scholar]
  28. Oliver S. G., van der Aart Q. J., Agostoni-Carbone M. L., Aigle M., Alberghina L., Alexandraki D., Antoine G., Anwar R., Ballesta J. P., Benit P. The complete DNA sequence of yeast chromosome III. Nature. 1992 May 7;357(6373):38–46. doi: 10.1038/357038a0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Sigurdson D. C., Herman R. K., Horton C. A., Kari C. K., Pratt S. E. An X-autosome fusion chromosome of Caenorhabditis elegans. Mol Gen Genet. 1986 Feb;202(2):212–218. doi: 10.1007/BF00331639. [DOI] [PubMed] [Google Scholar]
  32. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  33. 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]
  34. Stephan W. Recombination and the evolution of satellite DNA. Genet Res. 1986 Jun;47(3):167–174. doi: 10.1017/s0016672300023089. [DOI] [PubMed] [Google Scholar]
  35. Sulston J., Du Z., Thomas K., Wilson R., Hillier L., Staden R., Halloran N., Green P., Thierry-Mieg J., Qiu L. The C. elegans genome sequencing project: a beginning. Nature. 1992 Mar 5;356(6364):37–41. doi: 10.1038/356037a0. [DOI] [PubMed] [Google Scholar]
  36. Waterston R., Martin C., Craxton M., Huynh C., Coulson A., Hillier L., Durbin R., Green P., Shownkeen R., Halloran N. A survey of expressed genes in Caenorhabditis elegans. Nat Genet. 1992 May;1(2):114–123. doi: 10.1038/ng0592-114. [DOI] [PubMed] [Google Scholar]
  37. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]
  38. Wu T. C., Lichten M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science. 1994 Jan 28;263(5146):515–518. doi: 10.1126/science.8290959. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. de Lange T. Human telomeres are attached to the nuclear matrix. EMBO J. 1992 Feb;11(2):717–724. doi: 10.1002/j.1460-2075.1992.tb05104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES