Recombination and base composition: the case of the highly self-fertilizing plant Arabidopsis thaliana

Genome Biology

Volumn 5, Issue 7, 2004, Pages

  Marais, G ^a   Charlesworth, B ^a   Wright, S I ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b YORK UNIVERSITY   (Canada)

Author keywords

Additional Data File; Base Composition; Codon Bias; Codon Usage; Effective Population Size

Indexed keywords

PLANT DNA;

ARABIDOPSIS; ARTICLE; CODON; DNA BASE COMPOSITION; GC RICH SEQUENCE; GENETIC RECOMBINATION; GENETICS; INBREEDING;

ARABIDOPSIS; BASE COMPOSITION; CODON; DNA, PLANT; GC RICH SEQUENCE; INBREEDING; RECOMBINATION, GENETIC;

EID: 4143105022     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2004-5-7-r45     Document Type: Article

References (77)

1. Yu A, Zhao C, Fan Y, Jang W, Mungall AJ, Deloukas P, Olsen A, Doggett NA, Ghebranious N, Broman KW, Weber JL: Comparison of human genetic and sequence-based physical maps. Nature. 2001, 409: 951-953. 10.1038/35057185. DOI: 10.1038/35057185
2. Lercher MJ, Hurst LD: Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet. 2002, 18: 337-340. 10.1016/S0168-9525(02)02669-0. DOI: 10.1016/S0168-9525(02)02669-0
3. Tenaillon MI, Sawkins MC, Anderson LK, Stack SM, Doebley J, Gaut BS: Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.). Genetics. 2002, 162: 1401-1413.
4. Cutter AD, Payseur BA: Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol Biol Evol. 2003, 20: 665-673. 10.1093/molbev/msg072. DOI: 10.1093/molbev/msg072
5. Eyre-Walker A, Hurst LD: The evolution of isochores. Nat Rev Genet. 2001, 2: 549-555. 10.1038/35080577. DOI: 10.1038/35080577
6. Marais G, Mouchiroud D, Duret L: Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA. 2001, 98: 5688-5692. 10.1073/pnas.091427698. DOI: 10.1073/pnas.091427698
7. Marais G: Biased gene conversion: implications for genome and sex evolution. Trends Genet. 2003, 19: 330-338. 10.1016/S0168-9525(03)00116-1. DOI: 10.1016/S0168-9525(03)00116-1
8. Birdsell JA: Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol. 2002, 19: 1181-1197. DOI: 10.1093/oxfordjournals.molbev.a004176
9. Hey J, Kliman RM: Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics. 2002, 160: 595-608.
10. Carvalho AB, Clark AG: Intron size and natural selection. Nature. 1999, 401: 344-10.1038/43827. DOI: 10.1038/43827
11. Comeron JM, Kreitman M: The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces. Genetics. 2000, 156: 1175-1190.
12. Duret L, Marais G, Biemont C: Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics. 2000, 156: 1661-1669.
13. Rizzon C, Marais G, Gouy M, Biemont C: Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res. 2002, 12: 400-407. 10.1101/gr.210802. Article published online before print in February 2002. DOI: 10.1101/gr.210802
14. Bartolome C, Maside X, Charlesworth B: On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol. 2002, 19: 926-937. DOI: 10.1093/oxfordjournals.molbev.a004150
15. Williams EJ, Hurst LD: The proteins of linked genes evolve at similar rates. Nature. 2000, 407: 900-903. 10.1038/35038066. DOI: 10.1038/35038066
16. Betancourt AJ, Presgraves DC: Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci USA. 2002, 99: 13616-13620. 10.1073/pnas.212277199. DOI: 10.1073/pnas.212277199
17. Hellmann I, Ebersberger I, Ptak SE, Paabo S, Przeworski M: A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet. 2003, 72: 1527-1535. 10.1086/375657. DOI: 10.1086/375657
18. Pal C, Hurst LD: Evidence for co-evolution of gene order and recombination rate. Nat Genet. 2003, 33: 392-395. 10.1038/ng1111. DOI: 10.1038/ng1111
19. Smith JM, Haigh J: The hitch-hiking effect of a favourable gene. Genet Res. 1974, 23: 23-25. DOI: 10.1017/S0016672300014634
20. Charlesworth B, Morgan MT, Charlesworth D: The effect of deleterious mutations on neutral molecular variation. Genetics. 1993, 134: 1289-1303.
21. McVean GA, Charlesworth B: The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics. 2000, 155: 929-944.
22. Marais G, Mouchiroud D, Duret L: Neutral effect of recombination on base composition in Drosophila. Genet Res. 2003, 81: 79-87. 10.1017/S0016672302006079. DOI: 10.1017/S0016672302006079
23. Meunier J, Duret L: Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol. 2004, 21: 984-990. 10.1093/molbev/msh070. DOI: 10.1093/molbev/msh070
24. Charlesworth B: The effect of background selection against deleterious mutations on weakly selected linked variants. Genet Res. 1994, 63: 213-227. DOI: 10.1017/S0016672300032365
25. Eyre-Walker A: Recombination and mammalian genome evolution. Proc R Soc Lond B Biol Sci. 1993, 252: 237-243. DOI: 10.1098/rspb.1993.0071
26. Galtier N, Piganeau G, Mouchiroud D, Duret L: GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics. 2001, 159: 907-911.
27. Perry J, Ashworth A: Evolutionary rate of a gene affected by chromosomal position. Curr Biol. 1999, 9: 987-989. 10.1016/S0960-9822(99)80430-8. DOI: 10.1016/S0960-9822(99)80430-8
28. Kliman RM, Hey J: Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res. 2003, 81: 89-90. 10.1017/S0016672302006067. DOI: 10.1017/S0016672302006067
29. Abbott RJ, Gomes MF: Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity. 1989, 62: 411-418. DOI: 10.1038/hdy.1989.56
30. Berge G, Nordal I, Hestmark G: The effect of breeding systems and pollination vectors on the genetic variation of small plant populations within an agricultural landscape. OIKOS. 1998, 81: 17-29. DOI: 10.2307/3546463
31. Nordborg M: Linkage disequilibrium gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics. 2000, 154: 923-929.
32. Charlesworth D, Wright SI: Breeding systems and genome evolution. Curr Opin Genet Dev. 2001, 11: 685-690. 10.1016/S0959-437X(00)00254-9. DOI: 10.1016/S0959-437X(00)00254-9
33. Chiapello H, Lisacek F, Caboche M, Henaut A: Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene. 1998, 209: GC1-GC38. 10.1016/S0378-1119(97)00671-9. DOI: 10.1016/S0378-1119(97)00671-9
34. Duret L, Mouchiroud D: Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA. 1999, 96: 4482-4487. 10.1073/pnas.96.8.4482. DOI: 10.1073/pnas.96.8.4482
35. Wright SI, Lauga B, Charlesworth D: Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol. 2002, 19: 1407-1420. DOI: 10.1093/oxfordjournals.molbev.a004204
36. Comeron JM, Kreitman M, Aguade M: Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics. 1999, 151: 239-249.
37. Tachida H: Molecular evolution in a multisite nearly neutral mutation model. J Mol Evol. 2000, 50: 69-81.
38. Moriyama EN, Powell JR: Codon usage bias and tRNA abundance in Drosophila. J Mol Evol. 1997, 45: 514-523. DOI: 10.1007/PL00006256
39. Duret L: tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet. 2000, 16: 287-289. 10.1016/S0168-9525(00)02041-2. DOI: 10.1016/S0168-9525(00)02041-2
40. Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000, 408: 796-815. 10.1038/35048692. DOI: 10.1038/35048692
41. Bengtsson BO: Biased conversion as the primary function of recombination. Genet Res. 1986, 47: 77-80. DOI: 10.1017/S001667230002454X
42. Fingerman EG, Dombrowski PG, Francis CA, Sniegowski PD: Distribution and sequence analysis of a novel Ty3-like element in natural Saccharomyces paradoxus isolates. Yeast. 2003, 20: 761-70. 10.1002/yea.1005. DOI: 10.1002/yea.1005
43. Johnson LJ, Koufopanou V, Goddard MR, Hetherington R, Schafer SM, Burt A: Population genetics of the wild yeast Saccharomyces paradoxus. Genetics. 2004, 166: 43-52. DOI: 10.1534/genetics.166.1.43
44. Pal C, Papp B, Hurst LD: Does the recombination rate affect the efficiency of purifying selection? The yeast genome provides a partial answer. Mol Biol Evol. 2001, 18: 2323-2326. DOI: 10.1093/oxfordjournals.molbev.a003779
45. Jensen MA, True HL, Chernoff YO, Lindquist S: Molecular population genetics and evolution of a prion-like protein in Saccharomyces cerevisiae. Genetics. 2001, 159: 527-535.
46. Koch R, van Luenen HG, van der Horst M, Thijssen KL, Plasterk RH: Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res. 2000, 10: 1690-1696. 10.1101/gr.GR-1471R. DOI: 10.1101/gr.GR-1471R
47. Graustein A, Gaspar JM, Walters JR, Palopoli MF: Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics. 2002, 161: 99-107.
48. Felix MA: Genomes: a helpful cousin for our favourite worm. Curr Biol. 2004, 14: R75-R77. DOI: 10.1016/j.cub.2003.12.050
49. Li WH: Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol. 1987, 24: 337-345. DOI: 10.1007/BF02134132
50. Bernardi G: The compositional evolution of vertebrate genomes. Gene. 2000, 259: 31-43. 10.1016/S0378-1119(00)00441-8. DOI: 10.1016/S0378-1119(00)00441-8
51. Akashi H, Kliman RM, Eyre-Walker A: Mutation pressure, natural selection, and the evolution of base composition in Drosophila. Genetica. 1998, 102-103: 49-60. 10.1023/A:1017078607465. DOI: 10.1023/A:1017078607465
52. Koch MA, Haubold B, Mitchell-Olds T: Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol. 2000, 17: 1483-1498. DOI: 10.1093/oxfordjournals.molbev.a026248
53. Bergelson J, Stahl E, Dudek S, Kreitman M: Genetic variation within and among populations of Arabidopsis thaliana. Genetics. 1998, 148: 1311-1323.
54. Pannell JR, Charlesworth B: Effects of metapopulation processes on measures of genetic diversity. Philos Trans R Soc Lond B Biol Sci. 2000, 355: 1851-1864. 10.1098/rstb.2000.0740. DOI: 10.1098/rstb.2000.0740
55. Bulmer M: The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991, 129: 897-907.
56. Maruyama T: Some invariant properties of a geographically structured finite population: distribution of heterozygotes under irreversible mutation. Genet Res. 1972, 20: 141-149. DOI: 10.1017/S0016672300013665
57. Nagylaki T: Geographical invariance in population genetics. J Theor Biol. 1982, 99: 159-172. DOI: 10.1016/0022-5193(82)90396-4
58. Nagylaki T: Fixation indices in subdivided populations. Genetics. 1998, 148: 1325-1332.
59. Cherry JL, Wakeley J: A diffusion approximation for selection and drift in a subdivided population. Genetics. 2003, 163: 421-428.
60. Whitlock MC: Fixation probability and time in subdivided populations. Genetics. 2003, 164: 767-779.
61. Roze D, Rousset F: Selection and drift in subdivided populations: a straightforward method for deriving diffusion approximations and applications involving dominance selfing and local extinctions. Genetics. 2003, 165: 2153-2166.
62. Wright SI, Le QH, Schoen DJ, Bureau TE: Population dynamics of an Ac-like transposable element in self- and cross-pollinating Arabidopsis. Genetics. 2001, 158: 1279-1288.
63. Morgan MT: Transposable element number in mixed mating populations. Genet Res. 2001, 77: 261-275. 10.1017/S0016672301005067. DOI: 10.1017/S0016672301005067
64. Wright SI, Agrawal N, Bureau TE: Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 2003, 13: 1897-1903.
65. Andolfatto P, Przeworski M: A genome-wide departure from the standard neutral model in natural populations of Drosophila. Genetics. 2000, 156: 257-268.
66. Wall JD, Andolfatto P, Przeworski M: Testing models of selection and demography in Drosophila simulans. Genetics. 2002, 162: 203-216.
67. Gouy M, Gautier C, Attimonelli M, Lanave C, di Paola G: ACNUC - a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comput Appl Biosci. 1985, 1: 167-172.
68. Entrez Genome. [http://www.ncbi.nlm.nih.gov:80/entrez/query.fcgi?db=Genome]
69. Supplementary data for Wright et al.: Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. [http://www.genome.org/cgi/content/full/13/8/1897/DC1]
70. Ikemura T: Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985, 2: 13-34.
71. Percudani R: Restricted wobble rules for eukaryotic genomes. Trends Genet. 2001, 17: 133-135. 10.1016/S0168-9525(00)02208-3. DOI: 10.1016/S0168-9525(00)02208-3
72. Directory of MPSS data pages. [http://mpss.udel.edu]
73. Hartl DL, Clark AG: Principles of Population Genetics. 1997, Sunderland, MA: Sinauer, 542-3
74. Nagylaki T: Evolution of a finite population under gene conversion. Proc Natl Acad Sci USA. 1983, 80: 6278-6281. DOI: 10.1073/pnas.80.20.6278
75. Pollak E: On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics. 1987, 117: 353-360.
76. Laporte V, Charlesworth B: Effective population size and population subdivision in demographically structured populations. Genetics. 2002, 162: 501-519.
77. Sueoka N: On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA. 1962, 48: 582-592. DOI: 10.1073/pnas.48.4.582