Intron size correlates positively with recombination rate in Caenorhabditis elegans (original) (raw)

Abstract

A negative correlation between intron size and recombination rate has been reported for the Drosophila melanogaster and human genomes. Population-genetic models suggest that this pattern could be caused by an interaction between recombination rate and the efficacy of natural selection. To test this idea, we examined variation in intron size and recombination rate across the genome of the nematode Caenorhabditis elegans. Interestingly, we found that intron size correlated positively with recombination rate in this species.

Full Text

The Full Text of this article is available as a PDF (139.2 KB).

Selected References

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

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Castillo-Davis Cristian I., Mekhedov Sergei L., Hartl Daniel L., Koonin Eugene V., Kondrashov Fyodor A. Selection for short introns in highly expressed genes. Nat Genet. 2002 Jul 22;31(4):415–418. doi: 10.1038/ng940. [DOI] [PubMed] [Google Scholar]
  5. Comeron J. M., Kreitman M. The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces. Genetics. 2000 Nov;156(3):1175–1190. doi: 10.1093/genetics/156.3.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Comeron Josep M., Kreitman Martin. Population, evolutionary and genomic consequences of interference selection. Genetics. 2002 May;161(1):389–410. doi: 10.1093/genetics/161.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cremer T., Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001 Apr;2(4):292–301. doi: 10.1038/35066075. [DOI] [PubMed] [Google Scholar]
  8. Cáceres Javier F., Kornblihtt Alberto R. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 2002 Apr;18(4):186–193. doi: 10.1016/s0168-9525(01)02626-9. [DOI] [PubMed] [Google Scholar]
  9. Deutsch M., Long M. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 1999 Aug 1;27(15):3219–3228. doi: 10.1093/nar/27.15.3219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dibb N. J. Why do genes have introns? FEBS Lett. 1993 Jun 28;325(1-2):135–139. doi: 10.1016/0014-5793(93)81429-4. [DOI] [PubMed] [Google Scholar]
  11. Duret L., Marais G., Biémont C. Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics. 2000 Dec;156(4):1661–1669. doi: 10.1093/genetics/156.4.1661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hanke J., Brett D., Zastrow I., Aydin A., Delbrück S., Lehmann G., Luft F., Reich J., Bork P. Alternative splicing of human genes: more the rule than the exception? Trends Genet. 1999 Oct;15(10):389–390. doi: 10.1016/s0168-9525(99)01830-2. [DOI] [PubMed] [Google Scholar]
  14. Hawkins J. D. A survey on intron and exon lengths. Nucleic Acids Res. 1988 Nov 11;16(21):9893–9908. doi: 10.1093/nar/16.21.9893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Kent W. J., Zahler A. M. Conservation, regulation, synteny, and introns in a large-scale C. briggsae-C. elegans genomic alignment. Genome Res. 2000 Aug;10(8):1115–1125. doi: 10.1101/gr.10.8.1115. [DOI] [PubMed] [Google Scholar]
  17. Lamond A. I., Earnshaw W. C. Structure and function in the nucleus. Science. 1998 Apr 24;280(5363):547–553. doi: 10.1126/science.280.5363.547. [DOI] [PubMed] [Google Scholar]
  18. Mahy Nicola L., Perry Paul E., Gilchrist Susan, Baldock Richard A., Bickmore Wendy A. Spatial organization of active and inactive genes and noncoding DNA within chromosome territories. J Cell Biol. 2002 May 6;157(4):579–589. doi: 10.1083/jcb.200111071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Marais G., Mouchiroud D., Duret L. Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci U S A. 2001 Apr 24;98(10):5688–5692. doi: 10.1073/pnas.091427698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marais Gabriel, Piganeau Gwenaël. Hill-Robertson interference is a minor determinant of variations in codon bias across Drosophila melanogaster and Caenorhabditis elegans genomes. Mol Biol Evol. 2002 Sep;19(9):1399–1406. doi: 10.1093/oxfordjournals.molbev.a004203. [DOI] [PubMed] [Google Scholar]
  21. Mourier Tobias, Jeffares Daniel C. Eukaryotic intron loss. Science. 2003 May 30;300(5624):1393–1393. doi: 10.1126/science.1080559. [DOI] [PubMed] [Google Scholar]
  22. Ogata H., Fujibuchi W., Kanehisa M. The size differences among mammalian introns are due to the accumulation of small deletions. FEBS Lett. 1996 Jul 15;390(1):99–103. doi: 10.1016/0014-5793(96)00636-9. [DOI] [PubMed] [Google Scholar]
  23. Ophir R., Graur D. Patterns and rates of indel evolution in processed pseudogenes from humans and murids. Gene. 1997 Dec 31;205(1-2):191–202. doi: 10.1016/s0378-1119(97)00398-3. [DOI] [PubMed] [Google Scholar]
  24. Petrov D. A., Hartl D. L. High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol. 1998 Mar;15(3):293–302. doi: 10.1093/oxfordjournals.molbev.a025926. [DOI] [PubMed] [Google Scholar]
  25. Petrov D. A., Hartl D. L. Pseudogene evolution and natural selection for a compact genome. J Hered. 2000 May-Jun;91(3):221–227. doi: 10.1093/jhered/91.3.221. [DOI] [PubMed] [Google Scholar]
  26. Petrov D. A., Lozovskaya E. R., Hartl D. L. High intrinsic rate of DNA loss in Drosophila. Nature. 1996 Nov 28;384(6607):346–349. doi: 10.1038/384346a0. [DOI] [PubMed] [Google Scholar]
  27. Robertson H. M. The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. Genome Res. 2000 Feb;10(2):192–203. doi: 10.1101/gr.10.2.192. [DOI] [PubMed] [Google Scholar]
  28. Russell C. B., Fraga D., Hinrichsen R. D. Extremely short 20-33 nucleotide introns are the standard length in Paramecium tetraurelia. Nucleic Acids Res. 1994 Apr 11;22(7):1221–1225. doi: 10.1093/nar/22.7.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shabalina S. A., Kondrashov A. S. Pattern of selective constraint in C. elegans and C. briggsae genomes. Genet Res. 1999 Aug;74(1):23–30. doi: 10.1017/s0016672399003821. [DOI] [PubMed] [Google Scholar]
  30. Shabalina S. A., Ogurtsov A. Y., Kondrashov V. A., Kondrashov A. S. Selective constraint in intergenic regions of human and mouse genomes. Trends Genet. 2001 Jul;17(7):373–376. doi: 10.1016/s0168-9525(01)02344-7. [DOI] [PubMed] [Google Scholar]
  31. Shabalina S. A., Ogurtsov A. Y., Kondrashov V. A., Kondrashov A. S. Selective constraint in intergenic regions of human and mouse genomes. Trends Genet. 2001 Jul;17(7):373–376. doi: 10.1016/s0168-9525(01)02344-7. [DOI] [PubMed] [Google Scholar]
  32. Stein L., Sternberg P., Durbin R., Thierry-Mieg J., Spieth J. WormBase: network access to the genome and biology of Caenorhabditis elegans. Nucleic Acids Res. 2001 Jan 1;29(1):82–86. doi: 10.1093/nar/29.1.82. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tanabe Hideyuki, Müller Stefan, Neusser Michaela, von Hase Johann, Calcagno Enzo, Cremer Marion, Solovei Irina, Cremer Christoph, Cremer Thomas. Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4424–4429. doi: 10.1073/pnas.072618599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Venter J. C., Adams M. D., Myers E. W., Li P. W., Mural R. J., Sutton G. G., Smith H. O., Yandell M., Evans C. A., Holt R. A. The sequence of the human genome. Science. 2001 Feb 16;291(5507):1304–1351. doi: 10.1126/science.1058040. [DOI] [PubMed] [Google Scholar]