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Journal of Molecular Evolution

, Volume 58, Issue 4, pp 424–441 | Cite as

Dating the Monocot–Dicot Divergence and the Origin of Core Eudicots Using Whole Chloroplast Genomes

  • Shu-Miaw Chaw
  • Chien-Chang Chang
  • Hsin-Liang Chen
  • Wen-Hsiung Li
Article

Abstract

We estimated the dates of the monocot–dicot split and the origin of core eudicots using a large chloroplast (cp) genomic dataset. Sixty-one protein-coding genes common to the 12 completely sequenced cp genomes of land plants were concatenated and analyzed. Three reliable split events were used as calibration points and for cross references. Both the method based on the assumption of a constant rate and the Li–Tanimura unequal-rate method were used to estimate divergence times. The phylogenetic analyses indicated that nonsynonymous substitution rates of cp genomes are unequal among tracheophyte lineages. For this reason, the constant-rate method gave overestimates of the monocot–dicot divergence and the age of core eudicots, especially when fast-evolving monocots were included in the analysis. In contrast, the Li–Tanimura method gave estimates consistent with the known evolutionary sequence of seed plant lineages and with known fossil records. Combining estimates calibrated by two known fossil nodes and the Li–Tanimura method, we propose that monocots branched off from dicots 140–150 Myr ago (late Jurassic–early Cretaceous), at least 50 Myr younger than previous estimates based on the molecular clock hypothesis, and that the core eudicots diverged 100–115 Myr ago (Albian–Aptian of the Cretaceous). These estimates indicate that both the monocot–dicot divergence and the core eudicot’s age are older than their respective fossil records.

Keywords

Chloroplast genome Divergence of monocot and dicot Angiosperm phylogeny Age of core eudicots Molecular clock Unequal rate 

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Notes

Acknowledgements

We thank Robert Friedman for critical comments on an early version of the manuscript and Yoshihiro Matsuoka and Shu-Shin Wu for help with the gene group assignment for the three grasses and other taxa. We also thank the two reviewers’ critical and valuable comments and suggestions. This work was supported in part by National Science Council Grant NSC912311B001103, and Academia Sinica Grant IB91 to S.M.C., and NIH Grant GM30998 to W.H.L.

References

  1. 1.
    APG (Angiosperm Phylogeny Group)1998An ordinal classification for the families of flowering plants.Annal Mo Bot Gard85531533Google Scholar
  2. 2.
    Basinger, JF, Dilcher, DL 1984Ancient bisexual flowers.Science224511513Google Scholar
  3. 3.
    Bousquet, J, Strauss, SH, Doerksen, AH, Price, RA 1992Extensive variation in evolutionary rate of rbcL gene sequences among seed plants.Proc Natl Acad Sci USA8978447848PubMedGoogle Scholar
  4. 4.
    Bowe, LM, Coat, G, dePamphilis, CW 2000Phylogeny of seed plants based on all three genomic compartments: Extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers.Proc Natl Acad Sci USA9740924097CrossRefPubMedGoogle Scholar
  5. 5.
    Brandl, R, Mann, W, Sprintzl, M 1992Estimation of the monocot–dicot age through t-RNA sequences from the chloroplast.Proc R Soc Lond B2491317Google Scholar
  6. 6.
    Bremer, K 2000Early Cretaceous lineages of monocots flowering plants.Proc Natl Acad Sci USA9747074711CrossRefPubMedGoogle Scholar
  7. 7.
    Chase, MW,  et al. 1993Phylogenetics of seed plants: An analysis of nucleotide sequences from the plastid gene rbcL.Annal Ma Bot Gard80528580Google Scholar
  8. 8.
    Chase, MW 2000Higher-level systematics of the monocotyledons: An assessment of current knowledge and a new classification.Wilson, KLMorrison, DA eds. Monocots: Systematics and evolution.Commonwealth Scientific and Industrial Research OrganizationCollingwood, Australia316Google Scholar
  9. 9.
    Chaw, SM, Zharkikh, HA, Sung, HM, Lau, TC, Li, WH,  et al. 1997Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences.Mol Biol Evol145668PubMedGoogle Scholar
  10. 10.
    Chaw, SM, Parkinson, CL, Cheng, Y, Vincent, TM, Palmer, JD 2000Seed plant phylogeny inferred from all three plant genomes: Monophyly of extant gymnosperms and origin of Gnetales from conifers.Proc Natl Acad Sci USA9740864091PubMedGoogle Scholar
  11. 11.
    Clegg, MT, Gaut, BS, Learn, GH, Morton, . 1994Rates and patterns of chloroplast DNA evolution.Proc Natl Acad Sci USA9167956801PubMedGoogle Scholar
  12. 12.
    Crane, PR 1988Major clades and relationships in “higher” gymnosperms.Beck, CB eds. Origin and evolution of gymnosperms.Columbia University PressNew York,218272Google Scholar
  13. 13.
    Crepet, WL, Feldman, GD 1991The earliest remains of grasses in the fossil record.Am J Bot7810101014Google Scholar
  14. 14.
    Cronquist, A 1988The evolution and classification of fowering plants, 2nd ed.New York Botanical GardenBronx, NYGoogle Scholar
  15. 15.
    Darwin, C, Darwin, F, Seward, AC 1903More letters from Charles Darwin.D. AppletonNew YorkGoogle Scholar
  16. 16.
    Delevoryas, T, Hope, RC 1973Fertile coniferophyte remains from the Late Triassic Deep River Basin, North Carolina.Am J Bot60810818Google Scholar
  17. 17.
    Doyle, JA 1992Revised palynological correlations of the lower Potomac Group (USA) and the Cocobeach sequence of Gabon (Barremian-Aptian).Cretaceous Res13337349Google Scholar
  18. 18.
    Doyle, JA 1998Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales.Mol Phylogenet Evol9448462CrossRefPubMedGoogle Scholar
  19. 19.
    Doyle, JA, Donoghue, MJ 1987The origin of angiosperms: a cladistic approach.Friis, EMChaloner, WGCrane, PR eds. The origins of angiosperms and their biological consequences.Cambridge University PressCambridge1749Google Scholar
  20. 20.
    Gallois, JL, Achard, P, Green, G, Mache, R 2001The Arabidopsis chloroplast ribosomal protein L21 is encoded by a nuclear gene of mitochondrial origin.Gene274179185CrossRefPubMedGoogle Scholar
  21. 21.
    Gantt, JS, Baldauf, SL, Caline, PJ, Weeden, NF, Palmer, JD 1991Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron.EMBO J1030734078PubMedGoogle Scholar
  22. 22.
    Gaut, BS, Muse, SV, Clark, WD, Clegg, MT 1992Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants.J Mol Evol35292303Google Scholar
  23. 23.
    Gaut, BS, Muse, SV, Clegg, MT 1993Relative rates of nucleotide substitution in the chloroplast genome.Mol Phylogenet Evol28996CrossRefPubMedGoogle Scholar
  24. 24.
    Gaut, BS, Clark, LG, Wendel, JF, Clegg, MT, Muse, SV 1997Comparisons of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae).M Biol Evol14769777Google Scholar
  25. 25.
    Goremykin, VV, Hansmann, S, Martin, WF 1997Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times.Pl Syst Evol206337351Google Scholar
  26. 26.
    Goremykin, VV, Hirsch-Ernst, KI, Wolfl, S, Hellwig, FH 2003Analysis of the Amborella trichopoda chloroplast genome sequence suggests that Amborella is not a basal angiosperm.Mol Biol Evol2014991505CrossRefPubMedGoogle Scholar
  27. 27.
    APG (Angiosperm Phylogeny Group)GPWG (Grass Phylogeny Working Group)2001Phylogeny and subfamilial classification of the grasses (Poaceae).Ann Mo Bot Gard88373373Google Scholar
  28. 28.
    Gu, Z, Cavalcanti, ARO, Chen, FC, Bouman, P, Li, WH 2002Extent of gene duplication in the genomes of Drosophila, nematode, and yeast.Mol Biol Evol19256262PubMedGoogle Scholar
  29. 29.
    Hallick, RB, Bairoch, A 1994Proposals for the naming of chloroplast genes. III. Nomenclature for open reading frames encoded in chloroplast genomes.Plant Mol Biol Rep12S29S30Google Scholar
  30. 30.
    Hart, JA 1987A cladistic analysis of conifers: Preliminary results.J Arnold Arbor68296307Google Scholar
  31. 31.
    Herendeen, PS, Crane, PR 1995The fossil history of the monocotyledons.Rudall, PJCribb, PJCutler, DFHumphries, CJ eds. Monocotyledons: Systematics and evolution.Royal Botanic GardensKew121Google Scholar
  32. 32.
    Hiratsuka, J,  et al. 1989The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals.Mol Gen Genet217185194PubMedGoogle Scholar
  33. 33.
    Hughes, NF 1994The enigma ofangiosperm origins.Cambridge University PressCambridgeGoogle Scholar
  34. 34.
    Hupfer, H, Swiatek, M, Hornung, S, Hermann, RG, Maier, RM, Chiu, WL, Sears, B 2000Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome I of the five distinguishable euoenothera plastomes.Mol Gen Genet263581585PubMedGoogle Scholar
  35. 35.
    Ikeo, K, Ogihara, Y 2000 Triticum aestivum chloroplast, complete genome (unpublished)....Google Scholar
  36. 36.
    Katayama, H, Ogihara, Y 1996Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA.Curr Genet29572581CrossRefPubMedGoogle Scholar
  37. 37.
    Kato, T, Kaneko, T, Sato, S, Nakamura, Y, Tabata, S 2000Complete structure of the chloroplast genome of a legume, Lotus japonicus.DNA Res7323330PubMedGoogle Scholar
  38. 38.
    Kenrick, P, Crane, PR 1997The origin and early evolution of land plants.Nature3893339CrossRefGoogle Scholar
  39. 39.
    Kumar, S, Tamura, K, Jakobsen, IB, Nei, M 2001MEGA 2: Molecular evolutionary genetics analysis software.Arizona State UniversityTempeGoogle Scholar
  40. 40.
    Laroche, J, Li, P, Bousquet, J 1995Mitochondrial DNA and monocot–dicot divergence time.Mol Biol Evol1211511156Google Scholar
  41. 41.
    Li, WH, Graur, D 1991Fundamentals of molecular evolution.Sinauer AssociatesSunderland, MAGoogle Scholar
  42. 42.
    Li, WH, Tanimura, M 1987The molecular clock runs more slowly in man than in apes and monkeys.Nature3269396CrossRefPubMedGoogle Scholar
  43. 43.
    Lin, S, Wu, H, Jia, H, Zhang, P, Dixon, R, May, G, Gonzales, R, Roe, BA 2000 Medicago truncatula variety Jema Long A-17 chloroplast, complete sequence (unpublished)....Google Scholar
  44. 44.
    Lockhart, PJ, Howe, CJ, Barbrook, AC, Larkum, AWD, Penny, D 1999Spectral analysis, systematic bias, and the evolution of chloroplasts.Mol Biol Evol16573576Google Scholar
  45. 45.
    Magallón, S, Sanderson, MJ 2001Absolute diversification rates in angiosperm clades.Int J Org Evol5517621780Google Scholar
  46. 46.
    Magallón, S, Crane, PR, Herendeen, PS 1999Phylogenetic pattern, diversity, and diversification of eudicots.Ann Mo Bot Gard86297372Google Scholar
  47. 47.
    Maier, RM, Neckermann, K, Igloi, GL, Kossel, H 1995Complete sequence of the maize chloroplast genome: Gene content, hotspots of divergence and fine tuning of genetic information by transcript editing.J Mol Biol251614628CrossRefPubMedGoogle Scholar
  48. 48.
    Martin, W, Gierl, A, Saedler, H 1989Molecular evidence for pre-Cretaceous angiosperm origin.Nature3394648CrossRefGoogle Scholar
  49. 49.
    Martin, W, Lagrange, T, Li, YF, Bisanz-Seyer, C, Mache, R 1990Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach.Curr Genet18553556PubMedGoogle Scholar
  50. 50.
    Martin, W, Lydiate, D, Brinkmann, H, Forkmann, G, Saedler, H, Cerff, R 1993Molecular phylogenies in angiosperm evolution.Mol Biol Evol10140162PubMedGoogle Scholar
  51. 51.
    Martin, W, Stoebe, B, Goremykin, V, Hansmann, S, Hasegawa, M, Kowallik, KV 1998Gene transfer to the nucleus and the evolution of chloroplasts.Nature393162165PubMedGoogle Scholar
  52. 52.
    Martin, W,  et al. 2002Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus.Proc Natl Acad Sci USA991224612251CrossRefPubMedGoogle Scholar
  53. 53.
    Mathews, S, Donoghue, MJ 1999The root of angiosperm phylogeny inferred from duplicate phytochrome genes.Science286947950CrossRefPubMedGoogle Scholar
  54. 54.
    Matsuoka, Y, Yamazaki, Y, Ogihara, Y, Tsunewaki, K 2002Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals.Mol Biol Evol1920842091PubMedGoogle Scholar
  55. 55.
    Millen, RS, Olmstead, RG, Adams, KL, Palmer, JD, Lao, NT, Heggie, L, Kavanagh, TA, Hibberd, JM, Gray, JC, Morden, CW, Calie, PJ, Jermiin, LS, Wolfe, KH 2001Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus.Plant Cell13645658PubMedGoogle Scholar
  56. 56.
    Miller, Jr CN 1977Mesozoic conifers.Bot Rev43217280Google Scholar
  57. 57.
    Miller, Jr CN 1988The origin of modern conifer families.Beck, CB eds. Origin and evolution of gymnosperms.Columbia University PressNew York448486Google Scholar
  58. 58.
    Muse, SV, Gaut, BS 1997Interlocus comparisons of the nucleotide substitution process in the chloroplast genome.Genetics146393399PubMedGoogle Scholar
  59. 59.
    Nicholas KB, Nicholas HB Jr (1997) GeneDoc: Analysis and visualization of genetic variation. http://www.cris.com/~Ketchup/genedoc.shtml
  60. 60.
    Nicholas, KJ, Tiffney, BH, Knoll, AH 1983Patterns in vascular land plant diversification.Nature303614616Google Scholar
  61. 61.
    Nickrent, DL, Parkinson, CL, Palmer, JD, Duff, RJ 2000Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants.Mol Biol Evol1718851895PubMedGoogle Scholar
  62. 62.
    Ogihara, Y, Isono, K, Kojima, T, Endo, A, Hanaoka, M, Shiina, T, Terachi, T, Utsugi, S, Murata, M, Mori, N, Takumi, S, Ikeo, K, Gojobori, T, Murai, R, Murai, K, Matsuoka, Y, Ohnishi, Y, Tajiri, H, Tsunewaki, K 2002Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA.Mol Gen Genomics266740746CrossRefGoogle Scholar
  63. 63.
    Ohyama, K, Fukuzawa, H, Kohchi, T, Shirai, H, Sano, T, Sano, S, Umesono, K, Shiki, Y, Takeuchi, M, Chang, Z, Aota, S, Inokuchi, H, Ozeki, H 1986Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA.Nature322572574Google Scholar
  64. 64.
    Palmer, JD 1985aComparative organization of chloroplast genomes.Annu Rev Genet19325354CrossRefGoogle Scholar
  65. 65.
    Palmer, JD 1985bEvolution of chloroplast and mitochondrial DNA in plants and algae.MacIntyre, RJ eds. Molecular evolutionary genetics.Plenum PressNew York131240Google Scholar
  66. 66.
    Parkinson, CL, Adams, KL, Palmer, JD 1999Multigene analyses identify the three earliest lineages of extant flowering plants.Curr Biol914851488CrossRefPubMedGoogle Scholar
  67. 67.
    Price, RA, Thomas, J, Strauss, SH, Gadek, PA, Quinn, CJ, Palmer, JD 1993Familial relationships of the conifers from rbcL sequence data.Am J Bot80172Google Scholar
  68. 68.
    Pryer, KM, Schneider, H, Smith, AR, Cranfill, R, Wolf, PG, Hunt, JS, Sipes, SD 2001Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants.Nature409618622CrossRefPubMedGoogle Scholar
  69. 69.
    Qiu, YL, Lee, J, Bernasconi-Quadroni, F, Soltis, DE, Soltis, PS, Zanis, M, Chen, Z, Savolainen, V, Chase, MW 1999The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes.Nature402404407CrossRefPubMedGoogle Scholar
  70. 70.
    Rai, HS, O’Brien, HE, Reeves, PA, Olmstead, RG, Graham, SW 2003Inference of higher-order relationships in the cycads from a large chloroplast data set.Mol Phylogenet Evol29350359CrossRefPubMedGoogle Scholar
  71. 71.
    Ramshaw, JAM, Richardson, DL, Meatyard, BT, Brown, RH, Richardson, M, Thompson, EW, Boulter, D 1972The time of origin of the flowing plants determined by using amino acid sequence data of cytochrome C.New Phytol71773779Google Scholar
  72. 72.
    Renzaglia, KS, Johnson, TH, Gates, HD, Whittier, DP 2001Architecture of the sperm cell of Psilotum.Am J Bot8811511163PubMedGoogle Scholar
  73. 73.
    Rost, B 1999Twilight zone of protein sequence alignments.Protein Eng128594CrossRefPubMedGoogle Scholar
  74. 74.
    Saito, N, Nei, M 1987The neighbor-joining method: A new method for reconstructing phylogenetic trees.Mol Biol Evol4406425PubMedGoogle Scholar
  75. 75.
    Sanderson, MJ 1997A nonparametric approach to estimating divergence times in the absence of rate constancy.Mol Biol Evol1412181231Google Scholar
  76. 76.
    Sanderson, MJ, Doyle, JA 2001Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data.Amer J Bot8814991516Google Scholar
  77. 77.
    Sato, S, Nakamura, Y, Kaneko, T, Asamizu, E, Tabata, S 1999Complete structure of the chloroplast genome of Arabidopsis thaliana.DNA Res6283290PubMedGoogle Scholar
  78. 78.
    Schmitz-Linneweber, C, Maier, RM, Alcaraz, JP, Cottet, A, Herrmann, RG, Mache, R 2001The plastid chromosome of spinach (Spinacia oleracea): Complete nucleotide sequence and gene organization.Plant Mol Biol45307315PubMedGoogle Scholar
  79. 79.
    Shinozaki, K,  et al. 1986The complete nucleotide sequence of tobacco chloroplast genome: Its gene organization and expression.EMBO J520432049Google Scholar
  80. 80.
    Soltis, DE,  et al. 2000Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequendes.Bot J Linn Soc133381461CrossRefGoogle Scholar
  81. 81.
    Soltis, PS, Soltis, DE, Chase, MW 1999Angiosperm phylogeny inferred from multiple genes: A research tool for comparative biology.Nature402402404PubMedGoogle Scholar
  82. 82.
    Soltis, PS, Soltis, DE, Savolainen, V, Crane, PR, Barraclough, TG 2002Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils.Proc Natl Acad Sci USA9944304435CrossRefPubMedGoogle Scholar
  83. 83.
    Stebbins, GL 1981Coevolution of grasses and herbivores.Ann Mo Bot Gard687576Google Scholar
  84. 84.
    Stebbins, GL 1987Grass systematics and evolution: Past, present and future.Sonderstrom, TRHilu, KHCampbell, CSVarkworth, ME eds. Grass systematics and evolution.Smithsonian Institution PressWashington, DC359367Google Scholar
  85. 85.
    Stewart, WN, Rothwell, GW 1993Paleobotany and the evolution of plants, 2nd ed.Cambridge University PressCambridgeGoogle Scholar
  86. 86.
    Stoebe, B, Martin, W, Kowallik, KV 1998Distribution and nomenclature of protein-coding genes in 12 chloroplast genomes.Plant Mol Biol Rep16243255CrossRefGoogle Scholar
  87. 87.
    Sun, G, Ji, Q, Dilcher, DL, Zheng, S, Nixon, KC, Wang, X 2002Archaefructaceae, a new basal angiosperm family.Science296899904CrossRefPubMedGoogle Scholar
  88. 88.
    Swiss-Prot Protein Knowledgebase (2003) List of chloroplast and cyanelle encoded proteins. http://bioinformatics.weizmann. ac.il/databases/swiss-prot/release/plastid.txt , released 28 Feb
  89. 89.
    Swofford, DL 1998PAUP 4.0 b1: Phylogenetic analysis using parsimony (and other methods).Sinauer AssociatesSunderland, MAGoogle Scholar
  90. 90.
    Tajima, F 1993Unbiased estimate of evolutionary distance between nucleotide sequences.Mol Biol Evol10677688PubMedGoogle Scholar
  91. 91.
    Takezaki, N, Rzhetsky, A, Nei, M 1995Phylogenetic test of the molecular clock and linearized trees.Mol Biol Evol12823833PubMedGoogle Scholar
  92. 92.
    Taylor, TN, Taylor, EL 1993The biology and evolution of fossil plants, 1st ed.Prentice HallEnglewood Cliffs, NJGoogle Scholar
  93. 93.
    Thomas, BA, Spicer, RA 1987The evolution and paleobiology of land plants.Croom HelmLondonGoogle Scholar
  94. 94.
    Thomasson, JR 1987Fossil grasses.Sonderstrom, TRHilu, KHCampbell, CSVarkworth, ME eds. Grass systematics and evolution.Smithsonian Institution PressWashington, DC18201986Google Scholar
  95. 95.
    Wakasugi, T, Tsudzuki, J, Ito, S, Nakashima, K, Tsudzuki, T, Sugiura, M 1994Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii.Proc Natl Aad Sci USA9197949798Google Scholar
  96. 96.
    Wakasugi, T, Nishikawa A, Yamada K, Sugiura M (2002) Complete nucleotide sequence of the chloroplast genome from a fern, Psilotum nudum (unpublished; available from NCBI, accession No. AP004638)Google Scholar
  97. 97.
    Whitfeld, PR, Bottemley, W 1983Organization and structure of chloroplast genes.Annu Rev Plant Physiol34279310CrossRefGoogle Scholar
  98. 98.
    Wikström, N, Savolainen, V, Chase, M 2001Evolution of the angiosperms: Calibrating the family tree.Proc R Soc Lond B26822112220CrossRefPubMedGoogle Scholar
  99. 99.
    Willis, KJ, McElwain, JC 2002The evolution of plants.Oxford University PressNew YorkGoogle Scholar
  100. 100.
    Wolfe, KH, Li, WH, Sharp, PM 1987Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs.Proc Natl Acad Sci USA8490549058PubMedGoogle Scholar
  101. 101.
    Wolfe, KH, Gouy, MY, Yang, W, Sharp, PM, Li, WH 1989Date of the monocot–dicot divergence estimated from chloroplast chloroplast DNA sequence data.Proc Natl Acad Sci USA8662016205PubMedGoogle Scholar
  102. 102.
    Yang, YW, Lai, KN, Tai, PY, Li, WH 1999Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and the other angiosperm lineages.J Mol Evol48597560PubMedGoogle Scholar
  103. 103.
    Zhang, W 2000Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data.Mol Phylogenet Evol15135146PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2004

Authors and Affiliations

  • Shu-Miaw Chaw
    • 1
  • Chien-Chang Chang
    • 1
  • Hsin-Liang Chen
    • 1
  • Wen-Hsiung Li
    • 2
  1. 1.Institute of BotanyAcademia Sinica, 128 Sec. 2, Academy Road, Taipei 115Taiwan
  2. 2.Department of Ecology and EvolutionUniversity of Chicago, Chicago, IL 60637USA

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