Rates and patterns of molecular evolution in inbred and outbred Arabidopsis

Molecular Biology and Evolution

Volumn 19, Issue 9, 2002, Pages 1407-1420

  Wright, Stephen I ^a   Lauga, Beatrice ^a,b   Charlesworth, Deborah ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITÉ DE PAU ET DES PAYS DE L'ADOUR   (France)

Author keywords

Arabidopsis; Codon bias; Deleterious mutation; Inbreeding; Intron size

Indexed keywords

AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; BRASSICA; CODON USAGE; FERTILIZATION; GENE EXPRESSION; GENETIC RECOMBINATION; INBREEDING; INTRON; MATING SYSTEM; MAXIMUM LIKELIHOOD METHOD; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTBREEDING; OUTCROSSING; POPULATION SIZE; SPONTANEOUS MUTATION; BIOLOGICAL MODEL; BREEDING; CLASSIFICATION; CODON; GENE; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETICS; GENOME; MOLECULAR GENETICS; MUTAGENESIS; POPULATION DENSITY; STATISTICAL MODEL;

ARABIDOPSIS; ARABIDOPSIS LYRATA; ARABIDOPSIS THALIANA; BRASSICA; BRASSICACEAE; EMBRYOPHYTA;

ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BREEDING; CODON; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME, PLANT; INTRONS; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; POLYMORPHISM, GENETIC; POPULATION DENSITY;

EID: 0036729901     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a004204     Document Type: Article

References (99)

1. ABBOTT, R. J., and M. F. GOMES. 1989. Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity 62:411-418.
2. ACARKAN, A., M. ROSSBERG, M. KOCH, and R. SCHMIDT. 2000. Comparative genome analysis reveals extensive conservation of genome organisation for Arabidopsis thaliana and Capsella rubella. Plant J. 23:55-62.
3. AGUADÉ, M. 2001. Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H genes, in Arabidopsis thaliana. Mol. Biol. Evol. 18:1-9.
4. AKASHI, H. 1995. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics 139:1067-1076.
5. -. 1996. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics 144:1297-1307.
6. -. 1999. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151:221-238.
7. -. 2001. Gene expression and molecular evolution. Curr. Opin. Genet. Dev. 11:660-666.
8. ALTSCHUL, S. F., W. GISH, W. MILLER, E. W. MYERS, and D. J. LIPMAN. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
9. ALTSCHUL, S. F., T. L. MADDEN, A. A. SCHAFFER, J. ZHANG, Z. ZHANG, W. MILLER, and D. J. LIPMAN. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
10. ANTHONY, R. G., P. E. JAMES, and B. R. JORDAN. 1995. The cDNA sequence of a cauliflower apetala-1/squamosa homolog. Plant Physiol. 108:441-442.
11. BARTON, N. H. 2000. Genetic hitchhiking. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 355:1553-1562.
12. BAUDRY, E., C. KERDELHUE, H. INNAN, and W. STEPHAN. 2001. Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725-1735.
13. BENNETT, M. D., I. J. LEITCH, and L. HANSON. 1998. DNA amounts in two samples of angiosperm weeds. Ann. Bot. Suppl. A:121-134.
14. BERGE, G., I. NORDAL, and G. HESTMARK. 1998. The effect of breeding systems and pollination vectors on the genetic variation of small plant populations within an agricultural landscape. Oikos 81:17-29.
15. BERGELSON, J., E. STAHL, S. DUDEK, and M. KREITMAN. 1998. Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148:1311-1323.
16. BRAVERMAN, J. M., R. R. HUDSON, N. L. KAPLAN, C. H. LANGLEY, and W. STEPHAN. 1995. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783-796.
17. BRITSCH, L., J. DEDIO, H. SAEDLER, and G. FORKMANN. 1993. Molecular characterization of flavanone 3 beta-hydroxylases. Consensus sequence, comparison with related enzymes and the role of conserved histidine residues. Eur. J. Biochem. 217:745-754.
18. BROMHAM, L., D. PENNY, A. RAMBAUT, and M. D. HENDY. 2000. The power of relative rates tests depends on the data. J. Mol. Evol. 50:296-301.
19. BUSTAMANTE, C. D., R. NIELSEN, S. A. SAWYER, K. M. OLSEN, M. D. PURUGGANAN, and D. L. HARTL. 2002. The cost of inbreeding in Arabidopsis. Nature 416:531-534.
20. CARDAZZO, B., P. HAMEL, W. SAKAMOTO, H. WINTZ, and G. DUJARDIN. 1998. Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity. Gene 221:117-125.
21. CARR, S. M., and V. F. IRISH. 1997. Floral homeotic gene expression defines developmental arrest stages in Brassica oleracea L. vars. botrytis and italica. Planta 201:179-188.
22. CARVALHO, A. B., and A. G. CLARK. 1999. Intron size and natural selection. Nature 401:344.
23. CHARLESWORTH, B. 1992. Evolutionary rates in partionally self-fertilizing species. Am. Nat. 140:126-148.
24. -. 1994. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63:213-227.
25. CHARLESWORTH, B., and D. CHARLESWORTH. 1997. Rapid fixation of deleterious alleles can be caused by Muller's ratchet. Genet. Res. 70:63-73.
26. CHARLESWORTH, B., D. CHARLESWORTH, and M. T. MORGAN. 1990. Genetic loads and estimates of mutation rates in highly inbred plant populations. Nature 347:380-382.
27. CHARLESWORTH, B., M. T. MORGAN, and D. CHARLESWORTH. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
28. CHARLESWORTH, D., M. T. MORGAN, and B. CHARLESWORTH. 1993. Mutation accumulation in finite outbreeding and inbreeding populations. Genet. Res. 61:39-56.
29. CHARLESWORTH, D., and S. I. WRIGHT. 2001. Breeding systetas and genome evolution. Curr. Opin. Genet. Dev. 11:685-690.
30. CHEN, H.-H., Y.-Y. CHARNG, F. Y. SHANG, and J.-F. SHAW. 1998. Molecular cloning and sequencing of a broccoli cDNA (Accession No. AF047476) encoding an ETR-type ethylene receptor. (PGR98-088). Plant Physiol. 117:717.
31. CHIAPELLO, H., F. LISACEK, M. CABOCHE, and A. HENAUT. 1998. Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 209:GC1-GC38.
32. COMERON, J. M. 1995. A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J. Mol. Evol. 41:1152-1159.
33. -. 1999. K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15:763-764.
34. COMERON, J. M., and M. KREITMAN. 2000. The correlation between intron length and recombination in Drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156:1175-1190.
35. COMERON, J. M., M. KREITMAN, and M. AGUADE. 1999. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151:239-249.
36. COMES, H. P., and J. W. KADEREIT. 1998. The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3:432-438.
37. DESALLE, R., and A. R. TEMPLETON. 1988. Founder effects and the rate of mitochondrial DNA evolution in Hawaiian Drosophila. Evolution 42:1076-1084.
38. DURET, L., and D. MOUCHIROUD. 1999. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96:4482-4487.
39. -. 2000. Determinants of substitution cates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17:68-74.
40. DVORAK, J., M. C. LUO, and Z. L. YANG. 1998. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics 148:423-434.
41. GORDO, I., and B. CHARLESWORTH. 2000. The degeneration of asexual haploid populations and the speed of Muller's ratchet. Genetics 154:1379-1387.
42. GRANT, M. R., J. M. McDOWELL, A. G. SHARPE, M. DE TORRES ZABALA, D. J. LYDIATE, and J. L. DANGL. 1998. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl. Acad. Sci. USA 95:15843-15848.
43. GRAUSTEIN, A., J. M. GASPAR, J. R. WALTERS, and M. F. PALOPOLI. 2002. Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161:99-107.
44. HAMRICK, J. L., and M. J. GODT. 1990. Allozyme diversity in plant species. Pp. 43-63 in A. H. D. BROWN, M. T. CLEGG, A. L. KAHLER, and B. S. WEIR, eds. Plant population genetics, breeding, and genetic resources. Sinauer, Sunderland, Mass.
45. HAUSER, M. T., B. HARR, and C. SCHLOTTERER. 2001. Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol. Biol. Evol. 18:1754-1763.
46. HELLER, J., and J. MAYNARD SMITH. 1979. Does Muller's ratchet work with selfing? Genet. Res. 32:289-294.
47. HILL, W. G., and A. ROBERTSON. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269-294.
48. JOHNSON, K. P., and J. SEGER. 2001. Elevated rates of nonsynonymous substitution in island birds. Mol. Biol. Evol. 18:874-881.
49. JUNGHANS, H., and M. METZLAFF. 1990. A simple and rapid method for the preparation of total plant DNA. Biotechniques 8:176.
50. KAWABE, A., H. INNAN, R. TERAUCHI, and N. T. MIYASHITA. 1997. Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana. Mol. Biol. Evol. 14:1303-1315.
51. KAWABE, A., K. YAMANE, and N. T. MIYASHITA. 2000. DNA polymorphism at the cytosolic phosphoglucose isomerase (PgiC) locus of the wild plant Arabidopsis thaliana. Genetics 156:1339-1347.
52. KEIGHTLEY, P. D., and A. EYRE-WALKER. 2000. Deleterious mutations and the evolution of sex. Science 290:331-333.
53. KIM, Y., and W. STEPHAN. 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765-777.
54. KIMURA, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge.
55. KLIEBENSTEIN, D. J., J. KROYMANN, P. BROWN, A. FIGUTH, D. PEDERSEN, J. GERSHENZON, and T. MITCHELL-OLDS. 2001. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126:811-825.
56. KLIMAN, R. M., and J. HEY. 1993. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10:1239-1258.
57. KOCH, M. A., B. HAUBOLD, and T. MITCHELL-OLDS. 2000. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17:1483-1498.
58. -. 2001. Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am. J. Bot. 88:534-544.
59. KUITTINEN, H., and M. AGUADE. 2000. Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thallana. Genetics 155:863-872.
60. KUSABA, M., K. DWYER, J. HENDERSHOT, J. VREBALOV, J. B. NASRALLAH, and M. E. NASRALLAH. 2001. Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13:627-643.
61. LANGLEY, C. H., B. P. LAZZARO, W. PHILLIPS, E. HEIKKINEN, and J. M. BRAVERMAN. 2000. Linkage disequilibria and the site frequency spectra in the su(s) and su(w(a)) regions of the Drosophila melanogaster X chromosome. Genetics 156:1837-1852.
62. LAWTON-RAUH, A. L., E. S. BUCKLER 4TH, and M. D. PURUGGANAN. 1999. Patterns of molecular evolution among paralogous floral homeotic genes. Mol. Biol. Evol. 16:1037-1045.
63. LI, X. F., R. J. SHEN, P. L. LIU, Z. C. TANG, and Y. K. HE. 2000. Molecular characters and morphological genetics of CAL gene in Chinese cabbage. Cell. Res. 10:29-38.
64. LIU, F., D. CHARLESWORTH, and M. KREITMAN. 1999. The effect of mating system differences on nucleotide diversity at the phosphoglucose isomerase locus in the plant genus Leavenworthia. Genetics 151:343-357.
65. LIU, F., L. ZHANG, and D. CHARLESWORTH. 1998. Genetic diversity in Leavenworthia populations with different inbreeding levels. Proc. R. Soc. Lond. B: Biol. Sci. 265:293-301.
66. MARAIS, G., D. MOUCHIROUD, and L. DURET. 2001. Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc. Natl. Acad. Sci. USA 98:5688-5692.
67. MCVEAN, G. A., and B. CHARLESWORTH. 2000. The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155:929-944.
68. MCVEAN, G. A., and J. VIEIRA. 2001. Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila. Genetics 157:245-257.
69. NACHMAN, M. W. 2001. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet. 17:481-485.
70. NAIR, R. B., R. W. JOY IV, E. KURYLO, X. SHI, J. SCHNAIDER, R. S. DATLA, W. A. KELLER, and G. SELVARAJ. 2000. Identification of a CYP84 family of cytochrome P450-dependent mono-oxygenase genes in brassica napus and perturbation of their expression for engineering sinapine reduction in the seeds. Plant Physiol. 123:1623-1634.
71. NICHOLAS, K. B., H. B. NICHOLAS JR., and D. W. DEERFIELD II. 1997. GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4:14.
72. NORDBORG, M. 2000. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154:923-929.
73. NORDBORG, M., J. O. BOREVITZ, J. BERGELSON et al. (12 coauthors). 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 7:7.
74. OHTA, T. 1992. The nearly neutral model of molecular evolution. Annu. Rev. Ecol. Syst. 23:263-286.
75. -. 1993. Amino acid substitution at the Adh locus of Drosophila is facilitated by small population size. Proc. Natl. Acad. Sci. USA 90:4548-4551.
76. PANNELL, J. R., and B. CHARLESWORTH. 2000. Effects of metapopulation processes on measures of genetic diversity. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 355:1851-1864.
77. PETROV, D. A., E. R. LOZOVSKAYA, and D. L. HARTL. 1996. High intrinsic rate of DNA loss in Drosophila. Nature 384:346-349.
78. POLLAK, E. 1987. On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117:353-360.
79. PURUGGANAN, M. D., and J. I. SUDDITH. 1998. Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: nonneutral evolution and naturally occurring variation in floral homeotic function. Proc. Natl. Acad. Sci. USA 95:8130-8134.
80. -. 1999. Molecular population genetics of floral homeotic loci. Departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana. Genetics 151:839-848.
81. RODRIGUEZ-TRELLES, F., R. TARRIO, and F. J. AYALA. 1999. Switch in codon bias and increased cates of amino acid substitution in the Drosophila saltans species group. Genetics 153:339-350.
82. SAVOLAINEN, O., C. H. LANGLEY, B. P. LAZZARO, and H. FRÉVILLE 2000. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17:645-655.
83. SCHIERUP, M. H., B. K. MABLE, P. AWADALLA, and D. CHARLESWORTH. 2001. Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics 158:387-399.
84. SCHULTZ, S. T., M. LYNCH, and J. H. WILLIS. 1999. Spontaneous deleterious mutation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96:11393-11398.
85. SHARBEL, T. F., B. HAUBOLD, and T. MITCHELL-OLDS. 2000. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol. Ecol. 9:2109-2118.
86. SMITH, N. G., and A. EYRE-WALKER. 2001. Synonymous codon bias is not caused by mutation bias in G+C-rich genes in humans. Mol. Biol. Evol. 18:982-986.
87. STAHL, E. A., G. DWYER, R. MAURICIO, M. KREITMAN, and J. BERGELSON. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667-671.
88. TACHIDA, H. 2000. Molecular evolution in a multisite nearly neutral mutation model. J. Mol. Evol. 50:69-81.
89. TAJIMA, F. 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599-607.
90. TAKANO-SHIMIZU, T. 1999. Local recombination and mutation effects on molecular evolution in Drosophila. Genetics 153:1285-1296.
91. TAKEBAYASHI, N., and P. L. MORRELL. 2001. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88:1143-1150.
92. TARRIO, R., F. RODRIGUEZ-TRELLES, and F. J. AYALA. 2001. Shared nucleotide composition biases among species and their impact on phylogenetic reconstructions of the Drosophilidae. Mol. Biol. Evol. 18:1464-1473.
93. THOMPSON, J. D., D. G. HIGGINS, and T. J. GIBSON. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
94. WEINREICH, D. M., and D. M. RAND. 2000. Contrasting patterns of nonneutral evolution in proteins encoded in nuclear and mitochondrial genomes. Genetics 156:385-399.
95. WHITLOCK, M. C., and N. H. BARTON. 1997. The effective size of a subdivided population. Genetics 146:427-441.
96. WOLFE, K. H., W. H. LI, and P. M. SHARP. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84:9054-9058.
97. YANG, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
98. -. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568-573.
99. YOUNG, N. D., and C. W. DEPAMPHILIS. 2000. Purifying selection detected in the plastid gene matK and flanking ribozyme regions within a group II intron of nonphotosynthetic plants. Mol. Biol. Evol. 17:1933-1941.