Widespread genome duplications throughout the history of flowering plants

Genome Research

Volumn 16, Issue 6, 2006, Pages 738-749

  Cui, Liying ^a,b   Wall, P Kerr ^a,b   Leebens Mack, James H ^a,b   Lindsay, Bruce G ^a   Soltis, Douglas E ^c   Doyle, Jeff J ^e   Soltis, Pamela S ^d   Carlson, John E ^a,b   Arumuganathan, Kathiravetpilla ^f   Barakat, Abdelali ^a,b   Albert, Victor A ^g   Ma, Hong ^a,b   DePamphilis, Claude W ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e Department of Obstetrics Gynecology   (United States)

^f BENAROYA RESEARCH INSTITUTE   (United States)

^g UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACORUS; AGE DISTRIBUTION; ANGIOSPERM; ARABIDOPSIS; ARTICLE; AVOCADO; ESCHSCHOLTZIA; EXPRESSED SEQUENCE TAG; FLOWERING; GENE DUPLICATION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOME; GENOME ANALYSIS; GYMNOSPERM; LOBLOLLY PINE; NUPHAR; PARALOGY; PINE; POLYPLOIDY; PRIORITY JOURNAL; SOLANUM; SOYBEAN; SPECIES COMPARISON;

ANGIOSPERMS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; GYMNOSPERMS; MODELS, GENETIC; MODELS, STATISTICAL; PHYLOGENY; POLYPLOIDY;

ACORACEAE; ACORUS AMERICANUS; AMBORELLA; ANIMALIA; ARISTOLOCHIACEAE; CORE EUDICOTYLEDONS; ESCHSCHOLZIA CALIFORNICA; GNETALES; GYMNOSPERMAE; LAURACEAE; LIRIODENDRON TULIPIFERA; MAGNOLIACEAE; MAGNOLIIDS; MAGNOLIOPHYTA; NUPHAR; NUPHAR ADVENA; NUPHAR LUTEA; NYMPHAEA MEXICANA; NYMPHAEACEAE; PAPAVERACEAE; PERSEA AMERICANA; POACEAE; SARUMA HENRYI; WELWITSCHIA MIRABILIS;

EID: 33744822985     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.4825606     Document Type: Article

References (84)

1. Abi-Rached, L., Gilles, A., Shiina, T., Pontarotti, P., and Inoko, H. 2002. Evidence of en bloc duplication in vertebrate genomes. Nat. Genet. 31: 100-105.
2. Adams, K.L., Cronn, R., Percifield, R., and Wendel, J.F. 2003. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. 100: 4649-4654.
3. Albert, V.A., Soltis, D.E., Carlson, J.E., Farmerie, W.G., Wall, P.K., Ilut, D.C., Solow, T.M., Mueller, L.A., Landherr, L.L., Hu, Y., et al. 2005. Floral gene resources from basal angiosperms for comparative genomics research. BMC Plant Biol. 5: 5.
4. Bell, C.D., Soltis, D.E., and Soltis, P.S. 2005. The age of the angiosperms: A molecular timescale without a clock. Evolution Int. J. Org. Evolution 59: 1245-1258.
5. Bennett, M.D., Leitch, I.J., Price, H.J., and Johnston, J.S. 2003. Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis Genome Initiative estimate of approximately 125 Mb. Ann. Bot. (Lond.) 91: 547-557.
6. Bierne, N. and Eyre-Walker, A. 2003. The problem of counting sites in the estimation of the synonymous and nonsynonymous substitution rates: Implications for the correlation between the synonymous substitution rate and codon usage bias. Genetics 165: 1587-1597.
7. Blanc, G. and Wolfe, K.H. 2004. Widespread paleopolyploidy in model plant species inferred from age distribution of duplicate genes. Plant Cell 16: 1667-1678.
8. Blanc, G., Barakat, A., Guyot, R., Cooke, R., and Delseny, M. 2000. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12: 1093-1101.
9. Blanc, G., Hokamp, K., and Wolfe, K.H. 2003. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137-144.
10. Bogart, J.P. 1979. Evolutionary implications of polyploidy in amphibians and reptiles. Basic Life Sci. 13: 341-378.
11. Borsch, T., Hilu, K.W., Quandt, D., Wilde, V., Neinhuis, C., and Barthlott, W. 2003. Noncoding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms. J. Evol. Biol. 16: 558-576.
12. Bowers, J.E., Chapman, B.A., Rong, J., and Paterson, A.H. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
13. Brysting, A.K. and Borgen, L. 2000. Isozyme analysis of the Cerastium alpinum C-arcticum complex (Caryophyllaceae) supports a splitting of C. arcticum Lange. Plant Syst. Evol. 220: 199-221.
14. Buzgo, M., Soltis, P.S., Kim, S., and Soltis, D.E. 2005. The making of a flower. Biologist 52: 149-154.
15. Cannon, S.B., Mitra, A., Baumgarten, A., Young, N.D., and May, G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 4: 10.
16. Darlington, C.D. 1937. Recent advances in cytology. P. Blakiston's Son & Co., Philadelphia, PA.
17. Darwin, C.D. 1903. More letters of Charles Darwin. John Murray, London.
18. De Bodt, S., Maere, S., and Van de Peer, Y. 2005. Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 20: 591-597.
19. Dehal, P. and Boore, J.L. 2005. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3: e314.
20. deWet, J.M. 1979. Origins of polyploids. Basic Life Sci. 13: 3-15.
21. Dong, Q., Schlueter, S.D., and Brendel, V. 2004. PlantGDB, plant genome database and analysis tools. Nucleic Acids Res. 32: D354-D359.
22. Duvall, M.R., Learn Jr., G.H., Eguiarte, L.E., and Clegg, M.T. 1993. Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon. Proc. Natl. Acad. Sci. 90: 4641-4644.
23. Edgar, R.C. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
24. Ewing, B. and Green, P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186-194.
25. Ewing, B., Hillier, L., Wendl, M.C., and Green, P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175-185.
26. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L., and Postlethwait, J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
27. Friedman, R. and Hughes, A.L. 2001. Gene duplication and the structure of eukaryotic genomes. Genome Res. 11: 373-381.
28. Gaut, B.S., Morton, B.R., McCaig, B.C., and Clegg, M.T. 1996. Substitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl. Acad. Sci. 93: 10274-10279.
29. Goldman, N. and Yang, Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11: 725-736.
30. Grant, V. 1963. The origin of adaptations. Columbia University Press, New York.
31. _. 1981. Plant speciation. Columbia University Press, New York.
32. Grant, D., Cregan, P., and Shoemaker, R.C. 2000. Genome organization in dicots: Genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc. Natl. Acad. Sci. 97: 4168-4173.
33. Gu, X., Wang, Y., and Gu, J. 2002. Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat. Genet. 31: 205-209.
34. Guindon, S. and Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
35. Hilu, K.W. 1993. Polyploidy and the evolution of domesticated plants. Am. J. Bot. 80: 2521-2528.
36. Hilu, K.W., Borsch, T., Mueller, K., Soltis, D.E., Soltis, P.S., Savolainen, V., Chase, M.W., Powell, M., Alice, L.A., Evans, R., et al. 2003. Angiosperm phylogeny based on matK sequence information. Am. J. Bot. 90: 1758-1776.
37. Hughes, A.L. 1999. Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J. Mol. Evol. 48: 565-576.
38. Hughes, A.L. and Friedman, R. 2003. 2R or not 2R: Testing hypotheses of genome duplication in early vertebrates. J. Struct. Funct. Genomics 3: 85-93.
39. Iseli, C., Jongeneel, C.V., and Bucher, P. 1999. ESTScan: A program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 138-148.
40. Karev, G.P., Wolf, Y.I., Berezovskaya, F.S., and Koonin, E.V. 2004. Gene family evolution: An in-depth theoretical and simulation analysis of non-linear birth-death-innovation models. BMC Evol. Biol. 4: 32.
41. Kellis, M., Birren, B.W., and Lander, E.S. 2004. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
42. Kim, S., Yoo, M.-J., Albert, V.A., Farris, J.S., Soltis, P.S., and Soltis, D.E. 2004. Phylogeny and diversification of B-function MADS-box genes in angiosperms: Evolutionary and functional implications of a 260-million-year-old duplication. Am. J. Bot. 91: 2102-2118.
43. Kramer, E.M. and Irish, V.F. 1999. Evolution of genetic mechanisms controlling petal development. Nature 399: 144-148.
44. Kramer, E.M., Dorit, R.L., and Irish, V.F. 1998. Molecular evolution of genes controlling petal and stamen development: Duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149: 765-783.
45. Ku, H.M., Vision, T., Liu, J., and Tanksley, S.D. 2000. Comparing sequenced segments of the tomato and Arabidopsis genomes: Large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. 97: 9121-9126.
46. Leebens-Mack, J., Raubeson, L.A., Cui, L., Kuehl, J.V., Fourcade, M.H., Chumley, T.W., Boore, J.L., Jansen, R.K., and dePamphilis, C.W. 2005. Identifying the basal angiosperm node in chloroplast genome phylogenies: Sampling one's way out of the Felsenstein zone. Mol. Biol. Evol. 22: 1948-1963.
47. Li, W.H. and Grauer, D. 1991. Fundamentals of molecular evolution. Sinauer Associates, Sunderland, MA.
48. Liu, B. and Wendel, J.F. 2003. Epigenetic phenomena and the evolution of plant allopolyploids. Mol. Phylogenet. Evol. 29: 365-379.
49. Lynch, M. and Conery, J.S. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
50. Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., and Van de Peer, Y. 2005. Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. 102: 5454-5459.
51. Makalowski, W. 2001. Are we polyploids? A brief history of one hypothesis. Genome Res. 11: 667-670.
52. Masterson, J. 1994. Stomatal size in fossil plants: Evidence for polyploidy in majority of angiosperms. Science 264: 421-424.
53. McLachlan, G.J., Peel, D., Basford, K.E., and Adams, P. 1999. The EMMIX software for the fitting of mixtures of normal and t-components. J. Stat. Softw. 4: 2.
54. McLysaght, A., Hokamp, K., and Wolfe, K.H. 2002. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31: 200-204.
55. Müntzing, A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21: 263-378.
56. Nei, M. and Gojobori, T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
57. Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, New York.
58. Otto, S.P. and Whitton, J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437.
59. Paterson, A.H., Bowers, J.E., and Chapman, B.A. 2004a. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. 101: 9903-9908.
60. Paterson, A.H., Bowers, J.E., Chapman, B.A., Peterson, D.G., Rong, J., and Wicker, T.M. 2004b. Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity. Curr. Opin. Biotechnol. 15: 120-125.
61. Remm, M., Storm, C.E., and Sonnhammer, E.L. 2001. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 314: 1041-1052.
62. Schlueter, J.A., Dixon, P., Granger, C., Grant, D., Clark, L., Doyle, J.J., and Shoemaker, R.C. 2004. Mining EST databases to resolve evolutionary events in major crop species. Genome 47: 868-876.
63. Schwarz, G. 1978. Estimating the dimension of a model. Ann. Statist. 6: 461-464.
64. Shoemaker, R.C., Polzin, K., Labate, J., Specht, J., Brummer, E.C., Olson, T., Young, N., Concibido, V., Wilcox, J., Tamulonis, J.P., et al. 1996. Genome duplication in soybean (Glycine subgenus soja). Genetics 144: 329-338.
65. Simillion, C., Vandepoele, K., Van Montagu, M.C., Zabeau, M., and Van de Peer, Y. 2002. The hidden duplication past of Arabidopsis thaliana. Proc. Natl. Acad. Sci. 99: 13627-13632.
66. Soltis, D.E. and Soltis, P.S. 1990. Isozyme evidence for ancient polyploidy in primitive angiosperms. Syst. Bot. 15: 328-337.
67. _. 1999. Polyploidy: Recurrent formation and genome evolution. Trends Ecol. Evol. 14: 348-352.
68. Soltis, P.S., Soltis, D.E., Zanis, M.J., and Kim, S. 2000. Basal lineages of angiosperms: Relationships and implications for floral evolution. Int. J. Plant Sci. 161: S97-S107.
69. Soltis, D.E., Soltis, P.S., and Zanis, M.J. 2002. Phylogeny of seed plants based on evidence from eight genes. Am. J. Bot. 89: 1670-1681.
70. Stebbins, G.L. 1950. Variation and evolution in plants. Columbia University Press, New York.
71. Stefanovic, S., Rice, D.W., and Palmer, J.D. 2004. Long branch attraction, taxon sampling, and the earliest angiosperms: Amborella or monocots? BMC Evol. Biol. 4: 35.
72. Vision, T.J., Brown, D.G., and Tanksley, S.D. 2000. The origins of genomic duplications in Arabidopsis. Science 290: 2114-2117.
73. Wang, H.C., Singer, G.A., and Hickey, D.A. 2004a. Mutational bias affects protein evolution in flowering plants. Mol. Biol. Evol. 21: 90-96.
74. Wang, J.P., Lindsay, B.G., Leebens-Mack, J., Cui, L., Wall, K., Miller, W.C., and dePamphilis, C.W. 2004b. EST clustering error evaluation and correction. Bioinformatics 20: 2973-2984.
75. Wang, W., Tanurdzic, M., Luo, M., Sisneros, N., Kim, H.R., Weng, J.K., Kudrna, D., Mueller, C., Arumuganathan, K., Carlson, J., et al. 2005. Construction of a bacterial artificial chromosome library from the spikemoss Selaginella moellendorffii: A new resource for plant comparative genomics. BMC Plant Biol. 5: 10.
76. Wolfe, K.H. and Shields, D.C. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.
77. Wolfe, K.H., Li, W.H., and Sharp, P.M. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. 84: 9054-9058.
78. Yang, Z. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.
79. Yang, Z. and Nielsen, R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17: 32-43.
80. Yu, J.J., Wang, W., Lin, S., Li, H., Li, J., Zhou, P., Ni, W., Dong, S., Hu, C., Zeng, J., et al. 2005. The genomes of Oryza sativa: A history of duplications. PLoS Biol. 3: e38.
81. Zahn, L.M., Kong, H., Leebens-Mack, J.H., Kim, S., Soltis, P.S., Landherr, L.L., Soltis, D.E., dePamphilis, C.W., and Ma, H. 2005a. The evolution of the SEPALLATA subfamily of MADS-box genes: A preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169: 2209-2223.
82. Zahn, L.M., Leebens-Mack, J., dePamphilis, C.W., Ma, H., and Theissen, G. 2005b. To B or Not to B a flower: The role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J. Hered. 96: 225-240.
83. Zanis, M.J., Soltis, D.E., Soltis, P.S., Mathews, S., and Donoghue, M.J. 2002. The root of the angiosperms revisited. Proc. Natl. Acad. Sci. 99: 6848-6853.
84. Zhang, J., Rosenberg, H.F., and Nei, M. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc. Natl. Acad. Sci. 95: 3708-3713.