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The origin of red algae and the evolution of chloroplasts

Abstract

Chloroplast structure and genome analyses support the hypothesis that three groups of organisms originated from the primary photosynthetic endosymbiosis between a cyanobacterium and a eukaryotic host: green plants (green algae + land plants), red algae and glaucophytes (for example, Cyanophora)1. Although phylogenies based on several mitochondrial genes support a specific green plants/red algae relationship2,3, the phylogenetic analysis of nucleus-encoded genes yields inconclusive, sometimes contradictory results3,4. To address this problem, we have analysed an alternative nuclear marker, elongation factor 2, and included new red algae and protist sequences. Here we provide significant support for a sisterhood of green plants and red algae. This sisterhood is also significantly supported by a multi-gene analysis of a fusion of 13 nuclear markers (5,171 amino acids). In addition, the analysis of an alternative fusion of 6 nuclear markers (1,938 amino acids) indicates that glaucophytes may be the closest relatives to the green plants/red algae group. Thus, our study provides evidence from nuclear markers for a single primary endosymbiosis at the origin of these groups, and supports a kingdom Plantae comprising green plants, red algae and glaucophytes5.

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Figure 1: Maximum likelihood tree of eukaryotic EF-2 protein sequences.
Figure 2: Maximum likelihood tree inferred from exhaustive analysis of fusions F1 (13 genes, 5,171 sites) (a) and F2 (6 genes, 1,938 sites) (b ); ML, NJ and MP bootstrap proportions are shown for the green plants/red algae and green plants/red algae/glaucophytes nodes, respectively.

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References

  1. Douglas,S. E. Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Dev. 8, 655–661 ( 1998).

    Article  CAS  Google Scholar 

  2. Burger,G., Saint-Louis,D., Gray,M. W. & Lang,B. F. Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea . Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11, 1675–1694 (1999).

    Article  CAS  Google Scholar 

  3. Ragan,M. & Gutell,R. Are red algae plants? Bot. J. Linn. Soc. 118, 81–105 (1995).

    Article  Google Scholar 

  4. Stiller,J. W. & Hall,B. D. The origin of red algae: implications for plastid evolution. Proc. Natl Acad. Sci. USA 94 , 4520–4525 (1997).

    Article  ADS  CAS  Google Scholar 

  5. Cavalier-Smith,T. Eukaryote kingdoms: seven or nine? Biosystems 14, 461–481 (1981).

    Article  CAS  Google Scholar 

  6. Martin,W. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162–165 (1998).

    Article  ADS  CAS  Google Scholar 

  7. Kumar,S. & Rzhetsky,A. Evolutionary relationships of eukaryotic kingdoms. J. Mol. Evol. 42, 183– 193 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Bhattacharya,D. & Weber,K. The actin gene of the glaucocystophyte Cyanophora paradoxa: analysis of the coding region and introns, and an actin phylogeny of eukaryotes. Curr. Genet. 31, 439–446 ( 1997).

    Article  CAS  Google Scholar 

  9. Philippe,H. & Laurent,J. How good are deep phylogenetic trees? Curr. Opin. Genet. Dev. 8, 616– 623 (1998).

    Article  CAS  Google Scholar 

  10. Swofford,D. L., Olsen,G. J., Waddell,P. J. & Hillis,D. M. in Molecular Systematics (eds Hillis, D. M., Moritz, C. & Mable, B. K.) 407–514 (Sinauer Associates, Sunderland, Massachusetts, 1996).

    Google Scholar 

  11. Hirt,R. P. et al. Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580–585 ( 1999).

    Article  ADS  CAS  Google Scholar 

  12. Fabrizio,P., Laggerbauer,B., Lauber,J., Lane,W. S. & Luhrmann,R. An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2. EMBO J. 16, 4092– 4106 (1997).

    Article  CAS  Google Scholar 

  13. Embley,T. M. & Hirt,R. P. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 624–629 (1998).

    Article  CAS  Google Scholar 

  14. Kishino,H. & Hasegawa,M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J. Mol. Evol. 29, 170–179 (1989).

    Article  ADS  CAS  Google Scholar 

  15. Graybeal,A. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47, 9–17 (1998).

    Article  CAS  Google Scholar 

  16. Hillis,D. M. Inferring complex phylogenies. Nature 383, 130–131 (1996).

    Article  ADS  CAS  Google Scholar 

  17. Bhattacharya,D. & Schmidt,H. A. in Origins of Algae and Their Plastids (ed. Bhattacharya, D.) 139– 148 (Springer, Vienna, New York, 1997).

    Book  Google Scholar 

  18. Moreira,D. Efficient removal of PCR inhibitors using agarose-embedded DNA preparations. Nucleic Acids Res. 26, 3309– 3310 (1998).

    Article  CAS  Google Scholar 

  19. Yamamoto,A., Hashimoto,T., Asaga,E., Hasegawa,M. & Goto,N. Phylogenetic position of the mitochondrion-lacking protozoan Trichomonas tenax, based on amino acid sequences of elongation factors 1alpha and 2. J. Mol. Evol. 44, 98– 105 (1997).

    Article  ADS  CAS  Google Scholar 

  20. Altschul,S. F., Gish,W., Miller,W., Myers,E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Philippe,H. MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res. 21, 5264– 5272 (1993).

    Article  CAS  Google Scholar 

  23. Swofford,D. L. PAUP: phylogenetic analysis using parsimony. Version 3.1.1. (Illinois Natural History Survey, Champaign, 1993).

  24. Adachi,J. & Hasegawa,M. MOLPHY version 2. 3: programs for molecular phylogenetics based on maximum likelihood. Comput. Sci. Monogr. 28, 1–150 ( 1996).

    Google Scholar 

  25. Strimmer,K. & von Haeseler,A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969 (1996).

    Article  CAS  Google Scholar 

  26. Kishino,H., Miyata,T. & Hasegawa, M. Maximum likelihood inference of protein phylogeny, and the origin of chloroplasts. J. Mol. Evol. 31, 151–160 (1990).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank P. Lopez, P. López-García and M. Müller for critical reading of the manuscript; C. R. Engel for DNA samples; G. Fryd for cultures; N. Narradon for technical help; and the Kazusa Institute, Marine Biological Laboratory, Sanger Centre, Stanford Centre, the Institute of Genomic Research and Tsukuba Laboratory for access to sequence data. D. M. is the recipient of a stipend from the Fondation des Treilles.

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Moreira, D., Le Guyader, H. & Philippe, H. The origin of red algae and the evolution of chloroplasts. Nature 405, 69–72 (2000). https://doi.org/10.1038/35011054

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