Abstract
We analyzed the distribution of transposable elements (TEs: transposons, LTR retrotransposons, and non-LTR retrotransposons) in the chromosomes of the nematode Caenorhabditis elegans. The density of transposons (DNA-based elements) along the chromosomes was found to be positively correlated with recombination rate, but this relationship was not observed for LTR or non-LTR retrotransposons (RNA-based elements). Gene (coding region) density is higher in regions of low recombination rate. However, the lower TE density in these regions is not due to the counterselection of TE insertions within exons since the same positive correlation between TE density and recombination rate was found in noncoding regions (both in introns and intergenic DNA). These data are not compatible with a global model of selection acting against TE insertions, for which an accumulation of elements in regions of reduced recombination is expected. We also found no evidence for a stronger selection against TE insertions on the X chromosome compared to the autosomes. The difference in distribution of the DNA and RNA-based elements along the chromosomes in relation to recombination rate can be explained by differences in the transposition processes.
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- Acad B. A., Weiss R. Regional myocardial O2 consumption and coronary blood flow responses to acetylcholine in rabbit heart. Arch Int Physiol Biochim. 1989 Apr;97(2):197–204. doi: 10.3109/13813458909104539. [DOI] [PubMed] [Google Scholar]
- Bachtrog D., Weiss S., Zangerl B., Brem G., Schlötterer C. Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome. Mol Biol Evol. 1999 May;16(5):602–610. doi: 10.1093/oxfordjournals.molbev.a026142. [DOI] [PubMed] [Google Scholar]
- Barnes T. M., Kohara Y., Coulson A., Hekimi S. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics. 1995 Sep;141(1):159–179. doi: 10.1093/genetics/141.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benson D. A., Boguski M. S., Lipman D. J., Ostell J., Ouellette B. F., Rapp B. A., Wheeler D. L. GenBank. Nucleic Acids Res. 1999 Jan 1;27(1):12–17. doi: 10.1093/nar/27.1.12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biémont C. Population genetics of transposable DNA elements. A Drosophila point of view. Genetica. 1992;86(1-3):67–84. doi: 10.1007/BF00133712. [DOI] [PubMed] [Google Scholar]
- Biémont C., Tsitrone A., Vieira C., Hoogland C. Transposable element distribution in Drosophila. Genetics. 1997 Dec;147(4):1997–1999. doi: 10.1093/genetics/147.4.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Britten R. J. Active gypsy/Ty3 retrotransposons or retroviruses in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):599–601. doi: 10.1073/pnas.92.2.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 1998 Dec 11;282(5396):2012–2018. doi: 10.1126/science.282.5396.2012. [DOI] [PubMed] [Google Scholar]
- Cao L., Alani E., Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990 Jun 15;61(6):1089–1101. doi: 10.1016/0092-8674(90)90072-m. [DOI] [PubMed] [Google Scholar]
- Charlesworth B., Langley C. H., Sniegowski P. D. Transposable element distributions in Drosophila. Genetics. 1997 Dec;147(4):1993–1995. doi: 10.1093/genetics/147.4.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994 Sep 15;371(6494):215–220. doi: 10.1038/371215a0. [DOI] [PubMed] [Google Scholar]
- Collins J. J., Anderson P. The Tc5 family of transposable elements in Caenorhabditis elegans. Genetics. 1994 Jul;137(3):771–781. doi: 10.1093/genetics/137.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins J., Forbes E., Anderson P. The Tc3 family of transposable genetic elements in Caenorhabditis elegans. Genetics. 1989 Jan;121(1):47–55. doi: 10.1093/genetics/121.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devine S. E., Chissoe S. L., Eby Y., Wilson R. K., Boeke J. D. A transposon-based strategy for sequencing repetitive DNA in eukaryotic genomes. Genome Res. 1997 May;7(5):551–563. doi: 10.1101/gr.7.5.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dib C., Fauré S., Fizames C., Samson D., Drouot N., Vignal A., Millasseau P., Marc S., Hazan J., Seboun E. A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature. 1996 Mar 14;380(6570):152–154. doi: 10.1038/380152a0. [DOI] [PubMed] [Google Scholar]
- Dooner H. K., Martínez-Férez I. M. Germinal excisions of the maize transposon activator do not stimulate meiotic recombination or homology-dependent repair at the bz locus. Genetics. 1997 Dec;147(4):1923–1932. doi: 10.1093/genetics/147.4.1923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dreyfus D. H., Emmons S. W. A transposon-related palindromic repetitive sequence from C. elegans. Nucleic Acids Res. 1991 Apr 25;19(8):1871–1877. doi: 10.1093/nar/19.8.1871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Goldman A. S., Lichten M. The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics. 1996 Sep;144(1):43–55. doi: 10.1093/genetics/144.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill W. G., Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed] [Google Scholar]
- 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]
- Kazazian H. H., Jr, Moran J. V. The impact of L1 retrotransposons on the human genome. Nat Genet. 1998 May;19(1):19–24. doi: 10.1038/ng0598-19. [DOI] [PubMed] [Google Scholar]
- Ketting R. F., Haverkamp T. H., van Luenen H. G., Plasterk R. H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 1999 Oct 15;99(2):133–141. doi: 10.1016/s0092-8674(00)81645-1. [DOI] [PubMed] [Google Scholar]
- Kliman R. M., Hey J. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol. 1993 Nov;10(6):1239–1258. doi: 10.1093/oxfordjournals.molbev.a040074. [DOI] [PubMed] [Google Scholar]
- LaMunyon C. W., Ward S. Increased competitiveness of nematode sperm bearing the male X chromosome. Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):185–189. doi: 10.1073/pnas.94.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Langley C. H., Montgomery E., Hudson R., Kaplan N., Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988 Dec;52(3):223–235. doi: 10.1017/s0016672300027695. [DOI] [PubMed] [Google Scholar]
- Li W., Shaw J. E. A variant Tc4 transposable element in the nematode C. elegans could encode a novel protein. Nucleic Acids Res. 1993 Jan 11;21(1):59–67. doi: 10.1093/nar/21.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marín I., Plata-Rengifo P., Labrador M., Fontdevila A. Evolutionary relationships among the members of an ancient class of non-LTR retrotransposons found in the nematode Caenorhabditis elegans. Mol Biol Evol. 1998 Nov;15(11):1390–1402. doi: 10.1093/oxfordjournals.molbev.a025867. [DOI] [PubMed] [Google Scholar]
- McCarron M., Duttaroy A., Doughty G., Chovnick A. Drosophila P element transposase induces male recombination additively and without a requirement for P element excision or insertion. Genetics. 1994 Mar;136(3):1013–1023. doi: 10.1093/genetics/136.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore J. K., Haber J. E. Capture of retrotransposon DNA at the sites of chromosomal double-strand breaks. Nature. 1996 Oct 17;383(6601):644–646. doi: 10.1038/383644a0. [DOI] [PubMed] [Google Scholar]
- Naclerio G., Cangiano G., Coulson A., Levitt A., Ruvolo V., La Volpe A. Molecular and genomic organization of clusters of repetitive DNA sequences in Caenorhabditis elegans. J Mol Biol. 1992 Jul 5;226(1):159–168. doi: 10.1016/0022-2836(92)90131-3. [DOI] [PubMed] [Google Scholar]
- Pasyukova E., Nuzhdin S., Li W., Flavell A. J. Germ line transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol Gen Genet. 1997 Jun;255(1):115–124. doi: 10.1007/s004380050479. [DOI] [PubMed] [Google Scholar]
- Plasterk R. H. Molecular mechanisms of transposition and its control. Cell. 1993 Sep 10;74(5):781–786. doi: 10.1016/0092-8674(93)90458-3. [DOI] [PubMed] [Google Scholar]
- Rezsohazy R., van Luenen H. G., Durbin R. M., Plasterk R. H. Tc7, a Tc1-hitch hiking transposon in Caenorhabditis elegans. Nucleic Acids Res. 1997 Oct 15;25(20):4048–4054. doi: 10.1093/nar/25.20.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosenzweig B., Liao L. W., Hirsh D. Sequence of the C. elegans transposable element Tc1. Nucleic Acids Res. 1983 Jun 25;11(12):4201–4209. doi: 10.1093/nar/11.12.4201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruvolo V., Hill J. E., Levitt A. The Tc2 transposon of Caenorhabditis elegans has the structure of a self-regulated element. DNA Cell Biol. 1992 Mar;11(2):111–122. doi: 10.1089/dna.1992.11.111. [DOI] [PubMed] [Google Scholar]
- Shapiro J. A. Transposable elements as the key to a 21st century view of evolution. Genetica. 1999;107(1-3):171–179. [PubMed] [Google Scholar]
- Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
- Stephan W., Cho S. Possible role of natural selection in the formation of tandem-repetitive noncoding DNA. Genetics. 1994 Jan;136(1):333–341. doi: 10.1093/genetics/136.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sulston J. E., Brenner S. The DNA of Caenorhabditis elegans. Genetics. 1974 May;77(1):95–104. doi: 10.1093/genetics/77.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Surzycki S. A., Belknap W. R. Repetitive-DNA elements are similarly distributed on Caenorhabditis elegans autosomes. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):245–249. doi: 10.1073/pnas.97.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vieira C., Biémont C. Selection against transposable elements in D. simulans and D. melanogaster. Genet Res. 1996 Aug;68(1):9–15. doi: 10.1017/s0016672300033838. [DOI] [PubMed] [Google Scholar]