Diverse selective modes among orthologs/paralogs of the chalcone synthase (Chs) gene family of Arabidopsis thaliana and its relative A. halleri ssp. gemmifera

Molecular Phylogenetics and Evolution

Volumn 44, Issue 2, 2007, Pages 503-520

  Wang, Wei Kuang ^a   Schaal, Barbara A ^b   Chiou, You Mei ^a   Murakami, Noriaki ^c   Ge, Xue Jen ^d   Huang, Chi Chun ^a   Chiang, Tzen Yuh ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

Arabidopsis halleri ssp. gemmifera; Arabidopsis thaliana; Chalcone synthase (Chs) genes; Gene duplication; Orthologs; Paralogs; Selective modes

Indexed keywords

ACYLTRANSFERASE; CHALCONE SYNTHASE;

ARABIDOPSIS; ARTICLE; CLASSIFICATION; ENZYMOLOGY; EXON; GENETICS; PHYLOGENY; PLANT CHROMOSOME;

ACYLTRANSFERASES; ARABIDOPSIS; CHROMOSOMES, PLANT; EXONS; PHYLOGENY;

ARABIDOPSIS; ARABIDOPSIS HALLERI; ARABIDOPSIS THALIANA;

EID: 34447287781     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2007.05.006     Document Type: Article

References (107)

1. Abbot R.J., and Gomez M.F. Population genetic structure and outcrossing rate of Arabidopsis thaliana (L. ) Heynh. Heredity 62 (1989) 411-418
2. Alonso S., and Armour J.A.L. A highly variable segment of human subterminal 16p reveals a history of population growth for modern humans outside Africa. Proc. Natl. Acad. Sci. USA 98 (2001) 864-869
3. Barrier M., Robichaux R.H., and Purugganan M.D. Accelerated regulatory gene evolution in an adaptive radiation. Proc. Natl. Acad. Sci. USA 98 (2001) 10208-10213
4. Bishop J.G., Dean A.M., and Mitchell-Olds T. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl. Acad. Sci. USA 97 (2000) 5322-5327
5. Blanc G., Barakat A., Guyot R., Cooke R., and Delseny M. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12 (2000) 1093-1101
6. Blanc G., and Wolfe K.H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16 (2004) 1679-1691
7. Bergelson J., Stahl E., Dudek S., and Kreitman M. Genetic variation within and among populations of Arabidopsis thaliana. Genetics 148 (1998) 1311-1323
8. Bowers J.E., Chapman B.A., Rong J.K., and Paterson A.H. Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422 (2003) 433-438
9. Braverman J.M., Hudson R.R., Kaplan N.L., Langley C.H., and Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140 (1995) 783-796
10. Cain C.C., Saslowsky D.E., Walker R.A., and Shirley B.W. Expression of chalcone synthase and chalcone isomerase proteins in Arabidopsis seedlings. Plant Mol. Biol. 35 (1997) 377-381
11. Charlesworth D. Effects of inbreeding on the genetic diversity of populations. Phil. Trans. R. Soc. Lond. B. 358 (2003) 1051-1070
12. Charlesworth B., Morgan M.T., and Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics 134 (1993) 1289-1303
13. Charlesworth B., Morgan M.T., and Charlesworth D. The pattern of neutral molecular variation under the background selection model. Genetics 141 (1995) 1619-1632
14. Chen C.N., Chiang Y.C., Ho T.H.D., Schaal B.A., and Chiang T.Y. Coalescent processes and relaxation of selective constraints leading to contrasting genetic diversity at paralogs AtHVA22d and AtHVA22e in Arabidopsis thaliana. Mol. Phylogenet. Evol. 32 (2004) 616-626
15. Chiang Y.C., Schaal B.A., Chou C.H., Huang S., and Chiang T.Y. Contrasting selection modes at the Adh1 locus in outcrossing Miscanthus sinensis vs. inbreeding Miscanthus condensatus (Poaceae). Am. J. Bot. 90 (2003) 561-570
16. Chiang Y.C., Schaal B.A., Ge X.J., and Chiang T.Y. Range expansion leading to departures from neutrality in the non-symbiotic hemoglobin gene and the cpDNA trnL-trnF intergenic spacer in Trema dielsiana (Ulmaceae). Mol. Phylogenet. Evol. 31 (2004) 929-942
17. Coberly L.C., and Rausher M.D. Analysis of a chalcone synthase mutant in Ipomoea purpurea reveals a novel function for flavonoids: amelioration of heat stress. Mol. Ecol. 12 (2003) 1113-1124
18. De Meaux J., Goebel U., Pop A., and Mitchell-Olds T. Allele-specific assay reveals functional variation in the Chalcone synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution. Plant Cell 17 (2005) 676-690
19. De Meaux J., Pop A., and Mitchell-Olds T. Cis-regulatory evolution of chalcone-synthase expression in the genus Arabidopsis. Genetics 174 (2006) 2181-2202
20. Durbin M.L., McCaig B., and Clegg M.T. Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol. Biol. 42 (2000) 79-92
21. Fay J.C., and Wu C.I. Hitchhiking under positive Darwinian selection. Genetics 155 (2000) 1405-1413
22. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 (1999) 1531-1545
23. Fu Y.X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147 (1997) 915-925
24. Gleiss P.M., Stadler P.F., Wagner A., and Fell D.A. Small cycles in small wolds. Adv. Complex Syst. 4 (2001) 207-226
25. Golding G.B., and Strobeck C. Linkage disequilibrium in a finite population that is partially selfing. Genetics 94 (1980) 777-789
26. Halbrock K. Flavonoids. In: Stumpf P.K., and Conn E.E. (Eds). Biochemistry of Plants (1981), Academic Press, New York 425-456
27. Helariutta Y., Kotilainen M., Elomaa P., Kalkkinen N., Bremer K., Teeri T.H., and Albert V.A. Duplication and functional divergence in the chalcone synthase gene family of Asteraceae: evolution with substrate change and catalytic simplification. Proc. Natl. Acad. Sci. USA 93 (1996) 9033-9038
28. Hey, J., 2001. HKA: a computer program for tests of natural selection. Available from: .
29. Hooper S.D., and Berg O.G. On the nature of gene innovation: duplication patterns in microbial genomes. Mol. Biol. Evol. 20 (2003) 945-954
30. Howles P.A., Arioli T., and Weinman J.J. Nucleotide sequence of additional members of the gene family encoding chalcone synthase in Trifolium subterraneum. Plant Physiol. 107 (1995) 1035-1036
31. Hudson R.R., and Kaplan N.L. Gene trees with background selection. In: Golding B. (Ed). Non-Neutral Evolution: Theories and Molecular Data (1994), Chapman & Hall, London 140-153
32. Hudson R.R., Kreitman M., and Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics 116 (1987) 153-159
33. Hughes A.L., Green J.A., Garbayo J.M., and Roberts R.M. Adaptive diversification within a large family of recently duplicated, placentally expressed genes. Proc. Natl. Acad. Sci. USA 97 (2000) 3319-3323
34. Huttley G.A., Durbin M.L., Glover D.E., and Clegg M.T. Nucleotide polymorphism in the chalcone synthase-A locus and evolution of the chalcone synthase multigene family of common morning glory Ipomoea purpurea. Mol. Ecol. 6 (1997) 549-558
35. Innan H., Tajima F., Terauchi R., and Miyashita N.T. Intragenic recombination in the Adh locus of the wild plant Arabidopsis thaliana. Genetics 143 (1996) 1761-1770
36. Ingvarsson P.K. A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution 56 (2002) 2368-2373
37. Irwin R.E., and Strauss S.Y. Flower color microevolution in wild radish: evolutionary response to pollinator-mediated selection. Am. Nat. 165 (2005) 225-237
38. Johnson E.T., and Dowd P.F. Differentially enhanced unsect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J. Agric. Food Chem. 52 (2004) 5135-5138
39. Jossec L.M., Wambach T., Labuda D., Sinnett D., and Levy E. Genetic diversity patterns in the SR-BI/II locus can be explained by a recent selective sweep. Mol. Biol. Evol. 21 (2004) 760-769
40. Kawabe A., and Miyashita N.T. DNA polymorphism in active gene and pseudogene of the cytosolic phosphoglucose isomerase (PgiC) loci in Arabidopsis halleri ssp. gemmifera. Mol. Biol. Evol. 20 (2003) 1043-1050
41. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16 (1980) 111-120
42. Klein R.G. The Human Career. Human Biological and Cultural Origins (1999), The University of Chicago Press, Chicago
43. Klein J., Sato A., Nagl S., and O'huigin C. Molecular trans-species polymorphism. Ann. Rev. Ecol. Syst. 29 (1998) 1-21
44. Koch M.A., Haubold B., and Mitchell-Olds T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17 (2000) 1483-1498
45. Koch M.A., Weisshaar B., Kroymann J., Haubold B., and Mitchell-Olds T. Comparative genomic and regulatory evolution: conservation and function of the Chs and Apetala3 promoters. Mol. Biol. Evol. 18 (2001) 1882-1891
46. Koes R.E., Spelt C.E., van den Elzen P.J.M., and Mol J.N.M. Cloning and molecular characterization of the chalcone synthase multigene family of Petunia hybrida. Gene 81 (1989) 245-257
47. Koes R., Verweij W., and Quattrocchio F. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10 (2005) 236-242
48. Kumar S., Tamura K., Jakobsen I.B., and Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17 (2001) 1244-1245
49. Kusaba M., Dwyer K., Hendershot J., Vrebalov J., Nasrallah J.B., and Nasrallah M.E. 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 (2001) 627-643
50. Li W.H. Evolution of duplicated genes. In: Nei M., and Koehn R.K. (Eds). Evolution of genes and proteins (1983), Sinauer, Sunderland, MA 14-37
51. Lin J.Z., Morrell P.L., and Clegg M.T. The influence of linkage and inbreeding on patterns of nucleotide sequence diversity at duplicate alcohol dehydrogenase loci in wild Barley (Hordeum vulgare ssp. spontaneum). Genetics 162 (2002) 2007-2015
52. Long M., and Thornton K. Gene duplication and evolution. Science 293 (2001) 1551
53. Lynch M. Gene duplication and evolution. Science 297 (2002) 945-947
54. Lynch M., and Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 290 (2000) 1151-1155
55. Macnair M.R., Bert V., Huitson S.B., Saumitou-Laprade P., and Petit D. Zinc tolerance and hyperaccumulation are genetically independent characters. Proc. R. Soc. Lond. B 266 (1999) 2175-2179
56. Martin C.R. Structure, function and regulation of the chalcone synthase. Internatl. Rev. Cytol. 147 (1993) 233-284
57. May G., Shaw F., Badrane H., and Vekemans X. The signature of balancing selection: fungal mating compatibility gene evolution. Proc. Natl. Acad. Sci. USA 96 (1999) 9172-9177
58. McDonald J.H., and Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 (1991) 652-654
59. Mitchell-Olds T. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16 (2001) 693-700
60. Mitchell-Olds T., and Schmitt J. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441 (2006) 947-952
61. Miyashita N.T., Innan H., and Terauchi R. Intra- and interspecific variation in the alcohol dehydrogenase locus region of wild plants Arabis gemmifera and Arabidopsis thaliana. Mol. Biol. Evol. 13 (1996) 433-436
62. Miyashita N.T. DNA variation in the 5′ upstream region of the Adh locus of the wild plants Arabidopsis thaliana and Arabis gemmifera. Mol. Biol. Evol. 18 (2001) 164-171
63. Miyashita N.T., Kawabe A., Innan H., and Terauchi R. Intra- and interspecific DNA variation and codon bias of the alcohol dehydrogenase (Adh) locus in Arabis and Arabidopsis species. Mol. Biol. Evol. 15 (1998) 1420-1429
64. Moore R.C., and Purugganan M.D. The early stages of duplicate gene evolution. Proc. Natl. Acad. Sci. USA 100 (2003) 15682-15687
65. Murray M.G., and Thompson W.F. Rapid isolation of high molecular weight DNA. Nucl. Acids Res. 8 (1980) 4321-4325
66. Nei M. Molecular Evolutionary Genetics (1987), Columbia University Press, New York
67. Nordborg M., Charlesworth B., and Charlesworth D. Increased levels of polymorphism surrounding selectively maintained sites in highly selfing species. Proc. R. Soc. Lond. B 263 (1996) 1033-1039
68. Nordborg M., and Donnelly P. The coalescent process with selfing. Genetics 146 (1997) 1185-1195
69. Nordborg M., and Innan H. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163 (2003) 1201-1213
70. Oakley T., Gu Z., Abouheif E., Patel N.H., and Li W.H. Comparative methods for the analysis of gene-expression evolution: an example using yeast functional genomic data. Mol. Biol. Evol. 22 (2004) 40-50
71. Ohno S. Evolution by Gene Duplication (1970), Springer-Verlag, New York
72. Olsen K.M., Womack A., Garrett A.R., Suddith J.I., and Purugganan M.D. Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway. Genetics 160 (2002) 1641-1650
73. Parsch J., Meiklejohn C.D., and Hartl D. Patterns of DNA sequence variation suggest the recent action of positive selection in the janus-ocnus region of Drosophila simulans. Genetics 159 (2001) 647-657
74. Prince V.E., and Pickett F.B. Splitting pairs: the diverging fates of duplicated genes. Nat. Rev. Genet. 3 (2002) 827-837
75. Przeworski M. The signature of positive selection at randomly chosen loci. Genetics 160 (2002) 1179-1189
76. Ramos-Onsins S.E., Stranger B.E., Mitchell-Olds T., and Aguade M. Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166 (2004) 373-388
77. Rozas J., and Rozas R. DnaSP version 3.0: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15 (1999) 174-175
78. Sakuta M. Transcriptional control of chalcone synthase by environmental stimuli. J. Plant Res. 113 (2000) 327-333
79. Savolainen O., Langley C.H., Lazzaro B.P., and Freville H. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17 (2000) 645-655
80. Schein M., Yang Z.H., Mitchell-Olds T., and Schmid K.J. Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol. Biol. Evol. 21 (2004) 659-669
81. Schemske D., and Bierzychudek P. Evolution of flower color in the desert annual Linanthus parryae: Wright revised. Evolution 55 (2001) 1269-1282
82. Shimizu K.K., Cork J.M., Caicedo A.L., Mays C.A., Moore R.C., Olsen K.M., Ruzsa S., Coop G., Bustamante C.D., Awadalla P., and Purugganan M.D. Darwinian selection on a selfing locus. Science 306 (2004) 2081-2084
83. Simonsen K.L., Churchill G.A., and Aquadro C.F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141 (1995) 413-429
84. Small R.L., and Wendel J.F. Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol. Biol. Evol. 19 (2002) 597-607
85. Sommer H., and Saedler H. Structure of the chalcone synthase gene of Antirrhinum majus. Mol. Gen. Genet. 202 (1986) 429-434
86. Stephan W., Xing L., Kirby D.A., and Braverman J.M. A test of the background selection hypothesis based on nucleotide data from Drosophila ananassae. Proc. Natl. Acad. Sci. USA 95 (1998) 5649-5654
87. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105 (1983) 437-460
88. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 (1989) 585-595
89. Takahashi A., Tsaur S.C., Coyne J.A., and Wu C.I. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98 (2001) 3920-3925
90. The Arabidopsis Genome Initiative., 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
91. Thomson R., Pritchard J.K., Shen P., Oefner P.J., and Feldman M.W. Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. Proc. Natl. Acad. Sci. USA 97 (2000) 7360-7365
92. Todokoro S., Terauchi R., and Kawano S. Microsatellite polymorphism in natural populations of Arabidopsis thaliana in Japan. Jpn. J. Genet. 70 (1996) 543-554
93. Vision T.J., Brown D.G., and Tanksley S.D. The origins of genomic duplications in Arabidopsis. Science 290 (2000) 2114-2117
94. Wade H., Bibikova T.N., Valentine W.J., and Henkins C.I. Interactions within a network of phytochrome, crytochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J. 25 (2001) 675-685
95. Wagner A. Decoupled evolution of coding region and mRNA expression pattern after gene duplication: implications for the neutralist-selectionist debate. Proc. Natl. Acad. Sci. USA 97 (2000) 6570-6584
96. Wall J.D., Andolfatto P., and Przeworski M. Testing models of selection and demography in Drosophila simulans. Genetics 162 (2002) 203-216
97. Watterson G.A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7 (1975) 256-276
98. Winkel-Shirley B. Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol. 126 (2001) 485-493
99. Wright S.I., and Charlesworth B. The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168 (2004) 1071-1076
100. Wright S.I., and Gaut B.S. Molecular population genetics and the search for adaptive evolution in plants. Mol. Biol. Evol. 22 (2005) 506-519
101. Wu C.I. The genic view of the process of speciation. J. Evol. Biol. 14 (2001) 851-865
102. Wu J., Saupe S.J., and Glass N.L. Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc. Natl. Acad. Sci. USA 95 (1998) 12398-12403
103. Yang J., Huang J.X., Gu H., Zhong Y., and Yang Z.H. Duplication and adaptive evolution of the chalcone synthase genes of Dendranthema (Asteraceae). Mol. Biol. Evol. 19 (2002) 1752-1759
104. Yang, Z., 1999. Phylogenetic analysis by maximum likelihood (PAML). Version 2. University College London, England.
105. Yang Z., and Nielsen R. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J. Mol. Evol. 46 (1998) 409-418
106. Zhang L., Gaut B.S., and Vision T.J. Gene duplication and evolution. Science 293 (2001) 1551
107. Zhang L., Peek A.S., Dunams D., and Gaut B.S. Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics 162 (2002) 851-860