Skip to main content
Log in

Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times

  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Fifty-eight homologous protein sequences from the completely sequenced chloroplast genomes ofZea mays, Oryza sativa, Nicotiana tabacum, Pinus thunbergii, Marchantia polymorpha andPoryphyra purpurea were investigated. Analyzed individually, only 40 of the 58 proteins gave the true, known topology for these species. Trees constructed from the concatenated 14295 amino acid alignment and from automatically generated subsets of the data containing successively fewer polymorphisms were used to estimate theNicotiana-Zea andPinus-angiosperm divergence times as 160 and 348 million years, respectively, with an uncertainty of about 10%. These estimates based upon phylogenetic analysis of protein data from complete chloroplast genomes are in much better accordance with current interpretations of fossil evidence than previous molecular estimates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Beck, C. B., 1960a: Connection betweenArchaeopteris andCallixylon. — Science131: 1524–1525.

    Google Scholar 

  • —, 1960b: The identity ofArchaeopteris andCallixylon. — Brittonia12: 351–368.

    Google Scholar 

  • —, 1970: The appearance of gymnospermous structure. — Biol. Rev.45: 379–400.

    Google Scholar 

  • Bousquet, J., Strauss, S. H., Doersken, A. H., Price, R. A., 1992: Extensive variation in the evolutionary rate ofrbcL gene sequences among seed plants. — Proc. Natl. Acad. Sci. USA89: 7844–7848.

    PubMed  Google Scholar 

  • Brandl, R., Mann, W., Sprinzl, M., 1992: Estimation of the monocot-dicot age through tRNA sequences from the chloroplast. — Proc. Roy. Soc. London B249: 13–17.

    Google Scholar 

  • Cai, C., Ouyang, S., Wang, Yi., Fang, Z., Rong, J., Geng, L., Li, X., 1996: An Early Silurian vascular plant. — Nature379: 592.

    Google Scholar 

  • Chaw, S.-M., Sung, H.-M., Long, H., Zharkikh, A., Li, W.-H., 1994: Phylogeny of the major subclasses of angiosperms and date of the monocot-dicot divergence. — Amer. J. Bot.81: S146.

    Google Scholar 

  • —, 1997: Molecular phylogeny of gymnosperms and seed plant evolution: analysis of 18S rRNA sequences. — Molec. Biol. Evol.14: 56–68.

    PubMed  Google Scholar 

  • Cleal, C., 1989: Evolution in hidden forests? — Nature339: 16.

    PubMed  Google Scholar 

  • Clegg, M., 1990: Dating the monocot-dicot divergence. — Trends Ecol. Evol.5: 1–2.

    Google Scholar 

  • Cornet, B., 1986: The leaf venation and reproductive structures of a Late Triassic angiosperm,Sanmiguelia lewisii. — Evol. Theory7: 231–309.

    Google Scholar 

  • —, 1993: Dicot-like leaf and flowers from the Late Triassic tropical Newark supergroup rift zone, USA. — Mod. Geol.19: 81–99.

    Google Scholar 

  • Crane, P. R., 1988: Review ofCornet, B., The leaf venation and reproductive structures of a Late Triassic angiosperm,Sanmiguelia lewisii. — Taxon36: 788–789.

    Google Scholar 

  • —, 1993: Time for angiosperms. — Nature366: 631–632.

    Google Scholar 

  • —, 1989: Critique ofMartin & al. ‘Angiosperm Origins’. — Nature342: 131.

    PubMed  Google Scholar 

  • —, 1995: The origin and early diversification of angiosperms. — Nature374: 27–33.

    Google Scholar 

  • Delwiche, C. F., Palmer, J. D., 1996: Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. — Molec. Biol. Evol.13: 873–882.

    PubMed  Google Scholar 

  • Doyle, J. A., Donoghue, M. J., 1986: Seed plant phylogeny and the origin of the angiosperms: an experimental cladistic approach. — Bot. Rev.52: 321–431.

    Google Scholar 

  • Eedwards, D., Duckett, J. G., Richardson, J. B., 1995: Hepatic characters in the earliest land plants. — Nature374: 635–636.

    Google Scholar 

  • Erendorfer, F., 1976: Evolutionary significance of chromosomal differentiation patterns in gymnosperms and primitive angiosperms. — InBeck, C. B., (Ed.): Origin and early evolution of angiosperms, pp. 220–240. — New York: Columbia University Press.

    Google Scholar 

  • —, 1991: Evolution und Systematik. — InSitte, P., Ziegler, H., Ehrendorfer, F., Bresinsky, A., (Eds): Lehrbuch der Botanik für Hochschulen (“Strasburger”), 33rd edn, pp. 712–731. — Stuttgart: G. Fischer.

    Google Scholar 

  • Endress, P., 1994: Floral structure and evolution of primitive angiosperms: recent advances. — Pl. Syst. Evol.192: 79–97.

    Google Scholar 

  • Fraser, N. C., Grimaldi, D. A., Olsen, P. E., Axsmith, B., 1996: A Triassic Lagerstätte from eastern North America. — Nature380: 615–619.

    Google Scholar 

  • Friedmann, W., 1990: Double fertilization inEphedra, a non-flowering seed plant: its bearing on the origin of angiosperms. — Science247: 951–954.

    Google Scholar 

  • —, 1992: Evidence for a pre-angiosperm origin of endosperm: implications for the evolution of flowering plants. — Science255: 336–339.

    Google Scholar 

  • —, 1994: The evolution of embryogeny in seed plants and the developmental origin and early history of endosperm. — Amer. J. Bot.81: 1468–1486.

    Google Scholar 

  • Genetics Computer Group, 1994: Program manual for Version 8. — 575 Science Drive, Madison, Wisconsin, USA, 53711.

  • Goremykin, V. V., Bobrova, V. K., Pahnke, J., Troitsky, A. V., Antonov, A. S., Martin, W., 1996: Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition torbcL data do not support gnetalean affinities of angiosperms. — Molec. Biol. Evol.13: 383–396.

    PubMed  Google Scholar 

  • Hiratsuka, J., Shimada, H., Whittier, R., Ishibashi, T., Sakamoto, M., Mori, M., Kondo, C., Honji, Y., Sun, C.-R., Meng, B.-Y., Li, Y.-Q., Kanno, A., Nishizawa, Y., Hirai, A., Shinozaki, K., Sugiura, M., 1989: The 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. — Molec. Gen. Genet.217: 185–194.

    PubMed  Google Scholar 

  • Li, W.-H., 1989: A statistical test of phylogenies estimated from sequence data. — Molec. Biol. Evol.6: 424–435.

    PubMed  Google Scholar 

  • Maier, R. M., Neckermann, K., Igloi, G. L., Kössel, H., 1995: Complete sequence of maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. — J. Molec. Biol.251: 614–628.

    PubMed  Google Scholar 

  • Manhart, J. R., 1994: Phylogenetic analysis of green plantrbcL sequences. — Molec. Phylogeny Evol.3: 114–127.

    Google Scholar 

  • Martin, W., Gierl, A., Saedler, H., 1989: Molecular evidence for pre-Cretaceous angiosperm origins. — Nature339: 46–48.

    Google Scholar 

  • —, 1993: Molecular phylogenies in angiosperm evolution. — Molec. Biol. Evol.10: 140–162.

    PubMed  Google Scholar 

  • Nixon, K. C., Crepet, W. L., Stevenson, D., Friis, E. M., 1994: A reevaluation of seed plant phylogeny. — Ann. Missouri Bot. Gard.81: 484–533.

    Google Scholar 

  • 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., 1986: Chloroplast gene organisation deduced from complete sequence of liverwortMarchantia polymorpha chloroplast DNA. — Nature322: 572–574.

    Google Scholar 

  • Ramshaw, J. A. M., Richardson, D. L., Meatyard, B. T., Brown, R. H., Richardson, M., Thompson, E. W., Boulter, D., 1972: The time of origin of the flowering plants determined by using amino acid sequence data of cytochromsc. — New Phytol.71: 773–779.

    Google Scholar 

  • Reith, M., Munholland, J., 1995: Complete nucleotide sequence of thePorphyra purpurea chloroplast genome. — Pl. Molec. Biol. Reporter13: 333–335.

    Google Scholar 

  • Saitou, N., Nei, M., 1987: The neighbor-joining method: a new method for reconstructing phylogenetic trees. — Molec. Biol. Evol.4: 406–425.

    PubMed  Google Scholar 

  • Savard, L., Li, P., Strauss, S. H., Chase, M. W., Michaud, M., Bousquet, J., 1994: Chloroplast and nuclear gene sequences indicate Late Pennsylvanian time for the last common ancestor of extant seed plants. — Proc. Natl. Acad. Sci. USA91: 5163–5167.

    PubMed  Google Scholar 

  • Shear, W. A., 1991: The early development of terrestrial ecosystems. — Nature351: 283–289.

    Google Scholar 

  • Shinozaki, K., Ohme, M., Tanaka, M., Wakasugi, M., Hayashida, M., Matsubayashi, T., Zaita, N., Chunwongse, J., Obokata, J., Yamaguchi-Shinozaki, K., Ohto, C., Torazawa, K., Meng, B. Y., Sugita, M., Deno, H., Kamogashira, T., Yamada, K., Kusuda, J., Takaiwa, F., Kato, A., Tohdoh, N., Shimada, H., Sugiura, M., 1986: The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. — EMBO J.5: 2043–2049.

    Google Scholar 

  • Stewart, W. N., Rothwell, G. W., 1993: Paleobotany and the evolution of plants. — Cambridge: Cambridge University Press.

    Google Scholar 

  • Taylor, T. N., Taylor, E. L., 1993: The biology and evolution of fossil plants. — Englewood Cliffs: Prentice & Hall.

    Google Scholar 

  • Taylor, W. A., 1995: Spores in earliest land plants. — Nature373: 391–392.

    Google Scholar 

  • Thompson, J. D., Higgins, D. G., Gibson, T. J., 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.

    PubMed  Google Scholar 

  • Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., Sugiura, M., 1994: Loss of allndh genes as determined by sequencing the entire chloroplast genome of black pinePinus thunbergii. — Proc. Natl. Acad. Sci. USA91: 9794–9798.

    PubMed  Google Scholar 

  • Wettstein, R. von, 1914: Phylogenie der Pflanzen. — InHertwig, R., Von Wettstein, R. von, (Eds): Abstammungslehre, Systematik, Paläontologie, Biogeographie, pp. 439–452. — Leibzig: Teubner.

    Google Scholar 

  • Wolfe, K. H., Li, W.-H., Sharp, P., 1987: Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. — Proc. Natl. Acad. Sci. USA84: 9054–9058.

    PubMed  Google Scholar 

  • —, 1989: Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. — Proc. Natl. Acad. Sci. USA86: 6201–6205.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to William F. Martin.

Additional information

This paper is dedicated to emer. Univ.-Prof. DrFriedrich Ehrendorfer on the occasion of his 70th birthday.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goremykin, V.V., Hansmann, S. & Martin, W.F. Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times. Pl Syst Evol 206, 337–351 (1997). https://doi.org/10.1007/BF00987956

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00987956

Key words

Navigation