Letter | Published:

Gene transfer to the nucleus and the evolution of chloroplasts

Naturevolume 393pages162165 (1998) | Download Citation



Photosynthetic eukaryotes, particularly unicellular forms, possess a fossil record that is either wrought with gaps or difficult to interpret, or both. Attempts to reconstruct their evolution have focused on plastid phylogeny, but were limited by the amount and type of phylogenetic information contained within single genes1,2,3,4,5. Among the 210 different protein-coding genes contained in the completely sequenced chloroplast genomes from a glaucocystophyte, a rhodophyte, a diatom, a euglenophyte and five land plants, we have now identified the set of 45 common to each and to a cyanobacterial outgroup genome. Phylogenetic inference with an alignment of 11,039 amino-acid positions per genome indicates that this information is sufficient — but just barely so — to identify the rooted nine-taxon topology. We mapped the process of gene loss from chloroplast genomes across the inferred tree and found that, surprisingly, independent parallel gene losses in multiple lineages outnumber phylogenetically unique losses by more than 4:1. We identified homologues of 44 different plastid-encoded proteins as functional nuclear genes of chloroplast origin, providing evidence for endosymbiotic gene transfer to the nucleus in plants.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1

    Palenik, B. & Haselkorn, R. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355, 265–267 (1992).

  2. 2

    Urbach, E., Robertson, D. L. & Chisolm, S. W. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355, 267–270 (1992).

  3. 3

    Helmchen, T. A., Bhattacharya, D. & Melkonian, M. Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into the evolutionary relationships of plastids. J. Mol. Evol. 41, 203–210 (1995).

  4. 4

    Van de Peer, Y., Rensing, S., Maier, U.- & De Wachter, R. Substitution rate calibraiton of small subunit RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc. Natl Acad. Sci. USA 93, 7744–7748 (1996).

  5. 5

    Melkonian, M. Systematics and evolution of the algae: Endocytobiosis and the evolution of the major algal lineages. Progr. Bot. 57, 281–311 (1996).

  6. 6

    Hallick, R. B.et al. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res. 21, 3537–3544 (1993).

  7. 7

    Kaneko, T.et al. Sequence analysis of the gneome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assigment of potential protein-coding regions. DNA Res. 3, 109–136 (1996).

  8. 8

    Martin, W. & Schnarrenberger, C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1–18 (1997).

  9. 9

    Saitou, N. & Nei, M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987).

  10. 10

    Adachi, J. & Hasegawa, M. Computer Science Monographs, No. 28. MOLPHY Version 2.3: Programs for Molecular Phylogenetics Based on Maximum Likelihood.(Institute of Statistical Mathematics, Tokyo, 1996).

  11. 11

    Akaike, H. Anew look at the statistical model identification. IEEE Trans. Autom. Contr. CA19, 716–723 (1974).

  12. 12

    Hedtke, B., Börner, T. & Weihe, A. Mitochondrial and chloroplast phage-like RNA polymerases in Arabidopsis. Science 277, 809–811 (1997).

  13. 13

    Naylor, G. J. P. & Brown, W. M. Structural biology and phylogenetic estimation. Nature 388, 527–528 (1997).

  14. 14

    Adachi, J. & Hasegawa, M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42, 459–468 (1996).

  15. 15

    Lockhart, P. J., Steel, M. A., Hendy, M. D. & Penny, D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11, 605–612 (1994).

  16. 16

    Lockhart, P. J., Larkum, A. W., Steel, M., Waddell, P. J. & Penny, D. Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis. Proc. Natl Acad. Sci. USA 93, 1930–1934 (1996).

  17. 17

    Gibbs, S. P. The chloroplast of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 56, 2883–2889 (1978).

  18. 18

    Cavalier-Smith, T. Kingdom Protozoa and its 18 phyla. Microbiol. Rev. 57, 953–994 (1993).

  19. 19

    Henze, K.et al. Anuclear gene of eubacterial origin in Euglena reflects cryptic endosymbioses during protist evolution. Proc. Natl Acad. Sci. USA 92, 9122–9126 (1995).

  20. 20

    Cavalier-Smith, T.et al. Cryptomonad nuclear and nucleomorph 18S rRNA phylogeny. Eur. J. Phycol. 31, 315–328 (1996).

  21. 21

    Kowallik, K. V., Stöbe, B., Schaffran, I., Kroth-Pancic, P. & Freier, U. The chloroplast genome of a chlorophyll a+c containing alga, Odontella sinensis. Plant Mol. Biol. Reptr. 13, 336–342 (1995).

  22. 22

    Löffelhardt, W. & Bohnert, H. J. in The Molecular Biology of Cyanobacteria (ed. Bryant, D. A.) 56–89 (Kluwer, Dordrecht, 1994).

  23. 23

    Wakasugi, T.et al. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of black pine Pinus thunbergii. Proc. Natl Acad. Sci. USA 91, 9794–9798 (1994).

  24. 24

    Herrmann, R. G. in Eukaryotism and Symbiosis (eds Schenk, H. E. A., Herrmann, R. G., Jeon, K. W. & Schwemmler, W.) 73–118 (Springer, Heidelberg, 1997).

  25. 25

    Lynch, M. Mutation accumulation in transfer RNAs: Molecular evidence for Muller's ratchet in mitochondrial genomes. Mol. Biol. Evol. 13, 209–220 (1996).

  26. 26

    Moran, N. A. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

  27. 27

    Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).

  28. 28

    Felsenstein, J. PHYLIP (Phylogeny inference package) manual, version 3.5c(Univ. Washington, Seattle, Dept Genetics, 1993).

  29. 29

    Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTALW: 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 (1994).

  30. 30

    Maier, R. M., Neckermann, K., Igloi, G. L. & Kössel, H. Complete sequence of maize chloroplast genome: Gene content, hotspots of divergence and the tuning of genetic information by transcript editing. J. Mol. Biol. 251, 614–628 (1995).

Download references


We thank R. G. Herrmann for discussion, H. Phillipe for comments on the manuscript, the Rechenzentrum der Universität Braunschweig for use of computer facilities, and the Deutsche Forschungsgemeinschaft (W.M. and K.V.K.) and the Ministry of Education, Science, Sports and Culture of Japan (M.H.) for financial support. B.S. is the recipient of a psotdoctoral stipend from the DFG; V.G. is the recipient of a Ph.D. stipend from DAAD.

Author information


  1. Institut für Genetik, Technische Universität Braunschweig, Spielmannstrasse, 38023 7, Braunschweig, Germany

    • William Martin
    • , Vadim Goremykin
    •  & Sabine Hansmann
  2. Botanisches Institut, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse, 40225 1, Düsseldorf, Germany

    • Bettina Stoebe
    •  & Klaus V. Kowallik
  3. The Institute of Statistical Mathematics, 4-6-7 Minami-Azabu, Minato-ku, 106, Tokyo, Japan

    • Masami Hasegawa


  1. Search for William Martin in:

  2. Search for Bettina Stoebe in:

  3. Search for Vadim Goremykin in:

  4. Search for Sabine Hansmann in:

  5. Search for Masami Hasegawa in:

  6. Search for Klaus V. Kowallik in:

Corresponding author

Correspondence to William Martin.

About this article

Publication history



Issue Date



Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.