Journal of Molecular Evolution

, Volume 57, Issue 4, pp 377–382 | Cite as

Phylogeny of Plastids Based on Cladistic Analysis of Gene Loss Inferred from Complete Plastid Genome Sequences

  • Hisayoshi Nozaki
  • Njij Ohta
  • Motomichi Matsuzaki
  • Osami Misumi
  • Tsuneyoshi Kuroiwa
Article

Abstract

Based on the recent hypothesis on the origin of eukaryotic phototrophs, red algae, green plants, and glaucophytes constitute the “primary photosynthetic eukaryotes” (whose plastids may have originated directly from a cyanobacterium-like prokaryote via primary endosymbiosis), whereas the plastids of other lineages of eukaryotic phototrophs appear to be the result of secondary or tertiary endosymbiotic events (involving a phototrophic eukaryote and a host cell). Although phylogenetic analyses using multiple plastid genes from a wide range of eukaryotic lineages have been carried out, some of the major phylogenetic relationships of plastids remain ambiguous or conflict between different phylogenetic methods used for nucleotide or amino acid substitutions. Therefore, an alternative methodology to infer the plastid phylogeny is needed. Here, we carried out a cladistic analysis of the “loss of plastid genes” after primary endosymbiosis using complete plastid genome sequences from a wide range of eukaryotic phototrophs. Since it is extremely unlikely that plastid genes are regained during plastid evolution, we used the irreversible Camin-Sokal model for our cladistic analysis of the loss of plastid genes. The cladistic analysis of the 274 plastid protein-coding genes resolved the 20 operational taxonomic units representing a wide range of eukaryotic lineages (including three secondary plastid-containing groups) into two large monophyletic groups with high bootstrap values: one corresponded to the red lineage and the other consisted of a large clade composed of the green lineage (green plants and Euglena) and the basal glaucophyte plastid. Although the sister relationship between the green lineage and the Glaucophyta was not resolved in recent phylogenetic studies using amino acid substitutions from multiple plastid genes, it is consistent with the rbcL gene phylogeny and with a recent phylogenetic study using multiple nuclear genes. In addition, our analysis robustly resolved the conflicting/ambiguous phylogenetic positions of secondary plastids in previous phylogenetic studies: the Euglena plastid was sister to the chlorophycean (Chlamydomonas) lineage, and the secondary plastids from the diatom (Odontiella) and cryptophyte (Guillardia) were monophyletic within the red lineage.

Keywords

Evolution Camin-Sokal model Cladistic analysis Gene loss Phylogeny Plastids Plastid genes Primary plastid Secondary plastid 

Notes

Acknowledgements

This study was supported by Grant-in-Aid for Scientific Research on Priority Areas (c) “Genome Biology” from the Ministry of Education, Culture, Sports, Science and Technology, Japan (No. 1320611 to TK), and by the Program for the Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN; to TK and HN).

References

  1. 1.
    Adachi, J, Waddell, PJ, Martin, W, Hasegawa, M 2000Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA.J Mol Evol50348358PubMedGoogle Scholar
  2. 2.
    Andersson, JO, Roger, AJ 2002A cyanobacterial gene in nonphotosynthetic protists—An early chloroplast acquisition in Eukaryotes?Curr Biol12115119CrossRefPubMedGoogle Scholar
  3. 3.
    Baldauf, SL, Roger, AJ, Wenk-Siefert, I, Doolittle, WF 2000A kingdom-level phylogeny of eukaryotes based on combined protein data.Science290972977CrossRefPubMedGoogle Scholar
  4. 4.
    Bhattacharya, D, Medlin, L 1995The phylogeny of plastids: A review based on comparisons of small subunit ribosomal RNA coding regions.J Phycol31489498Google Scholar
  5. 5.
    Camin, JH, Sokal, RR 1965A method for deducing branching sequences in phylogeny.Evolution19311326Google Scholar
  6. 6.
    Cavalier-Smith, T 2002Chloroplast evolution: Secondary symbiogenesis and multiple losses.Curr Biol12R62R64CrossRefPubMedGoogle Scholar
  7. 7.
    Delwiche, CF 1999Tracing the thread of plastid diversity through the tapestry of life.Am Nat154164177CrossRefGoogle Scholar
  8. 8.
    Delwiche, CF, Palmer, JD 1997

    The origin of plastids and their spread via secondary symbiosis.

    Bhattacharya, D eds. Origin of algae and their plastids.Springer-VerlagWien5386
    Google Scholar
  9. 9.
    Fawley, MW, Lee, CM 1990Pigment composition of the scaly green flagellate Mesostigma viride (Micromonadophyceae) is similar to that of the siphonous green alga Bryopsis plumosa (Ulvophyceae).J Phycol26666670Google Scholar
  10. 10.
    Felsenstein, J 1985Confidence limits on phylogenies: an approach using bootstrap.Evolution381624Google Scholar
  11. 11.
    Friedl, T 1997

    The evolution of the green algae.

    Bhattacharya, D eds. Origin of algae and their plastids.Springer-VerlagWien87101
    Google Scholar
  12. 12.
    Graham, LE, Wilcox, LW 2000Algae.Prentice HallUpper Saddle River, NJGoogle Scholar
  13. 13.
    Hannaert, V, Saavedra, E, Duffieux, F, Szikora, JP, Rigden, DJ, Michels, PAM, Opperdoes, FR 2003Plant-like traits associated with metabolism of Trypanosoma parasites.Proc Natl Acad Sci USA10010671071CrossRefPubMedGoogle Scholar
  14. 14.
    Itoh, T, Martin, W, Nei, M 2002Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts.Proc Natl Acad Sci USA991294412948CrossRefPubMedGoogle Scholar
  15. 15.
    Kimura, M 1980A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.J Mol Evol16111120PubMedGoogle Scholar
  16. 16.
    Lambowitz, AM, Belfort, M 1993Introns as mobile genetic elements.Ann Rev Bichem62587622CrossRefGoogle Scholar
  17. 17.
    Martin, W, Herrmann, RG 1998Gene transfer from organelles to the nucleus: How much, what happens, and why?Plant Physiol118917PubMedGoogle Scholar
  18. 18.
    Martin, W, Rujan, T, Richly, E, Hansen, A, Cornelsen, S, Lins, T,  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
  19. 19.
    Maul, JE, Lilly, JW, Cui, L, dePamphilis, CW, Miller, W, Harris, EH, Stern, DB 2002The Chlamydomonas reinhardtii plastid chromosome: Islands of genes in a sea of repeats.Plant Cell1426592679CrossRefPubMedGoogle Scholar
  20. 20.
    McFadden, GI 2001Primary and secondary endosymbiosis and the origin of plastids.J Phycol37951959CrossRefGoogle Scholar
  21. 21.
    Montegut-Felkner, AE, Triemer, RE 1997Phylogenetic relationships of selected euglenoid genera based on morphological and molecular data.J Phycol33512519Google Scholar
  22. 22.
    Morden, CW, Delwiche, CF, Kuhsel, M, Palmer, JD 1992Gene phylogenies and the endosymbiotic origin of plastids.BioSystems287590CrossRefPubMedGoogle Scholar
  23. 23.
    Müllner, AN, Angeler, DG, Samuel, R, Linton, EW, Triemer, RE 2001Phylogenetic analysis of phagotrophic, phototrophic and osmotrophic euglenoids by using the nuclear 18S rDNA sequence.Int J Syst Evol Micr51783791Google Scholar
  24. 24.
    Nelissen, B, Van de Peer, Y, Wilmotte, A, De Wachter, R 1995An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences.Mol Biol Evol1211661173PubMedGoogle Scholar
  25. 25.
    Nozaki, H, Matsuzaki, M, Takahara, M, Misumi, O, Kuroiwa, H, Hasegawa, M,  et al. 2003The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids.J Mol Evol56485497CrossRefPubMedGoogle Scholar
  26. 26.
    Ohta, N, Matsuzaki, M, Misumi, O, Miyagishima, S, Nozaki, H, Tanaka, K,  et al. 2003Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae.DNA Research106777PubMedGoogle Scholar
  27. 27.
    Ohyama, K, Fukuzawa, H, Kohchi, T, Shirai, H, Sano, T, Sano, S,  et al. 1986Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA.Nature322572574Google Scholar
  28. 28.
    Palmer, JD, Delwiche, CF 1998

    The origin and evolution of plastids and their genomes.

    Soltis, PSSoltis, DEDoyle, JJ eds. Molecular systematics of plants. II. DNA sequencing.Kluwer AcademicBoston375409
    Google Scholar
  29. 29.
    Preisfeld, A, Berger, S, Busse, I, Liller, S, Ruppel, HG 2000Phylogenetic analyses of various euglenoid taxa (Euglenozoa) based on 18S rDNA sequence data.J Phycol36220226CrossRefGoogle Scholar
  30. 30.
    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
  31. 31.
    Swofford, DL 2002PAUP* 4.0: Phylogenetic Analysis Using Parsimony, version 4.0b10.Sinauer Associates, Inc.Sunderland, MAGoogle Scholar
  32. 32.
    Turmel, M, Otis, C, Lemieux, C 1999The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: Insights into the architecture of ancestral chloroplast genomes.Proc Natl Acad Sci USA961024810253PubMedGoogle Scholar
  33. 33.
    Turmel, M, Otis, C, Lemieux, C 2002The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: Insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants.Proc Natl Acad Sci USA991127511280CrossRefPubMedGoogle Scholar
  34. 34.
    Van de Peer, Y, Rensing, SA, Maier, UG, De Wachter, R 1996Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae.Proc Natl Acad Sci USA9377327736CrossRefPubMedGoogle Scholar
  35. 35.
    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 Acad Sci USA9197949798PubMedGoogle Scholar
  36. 36.
    Wiley, EO, Siegel-Causey, D, Brooks, DR, Funk, VA 1991The compleat cladist: A primer of phylogenetic procedures. Special Publication No 19. Museum of Natural History.University of KansasLawrence, KSGoogle Scholar
  37. 37.
    Yoon, HS, Hackett, JD, Bhattacharya, D 2002aA single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis.Proc Natl Acad Sci USA991172411729Google Scholar
  38. 38.
    Yoon, HS, Hackett, JD, Pinto, G, Bhattacharya, D 2002bThe single, ancient origin of chromist plastids.Proc Natl Acad Sci USA991550715512Google Scholar
  39. 39.
    Zwickl, DJ, Hillis, DM 2002Increased taxon sampling greatly reduces phylogenetic error.Syst Biol51588598CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  • Hisayoshi Nozaki
    • 1
  • Njij Ohta
    • 2
  • Motomichi Matsuzaki
    • 3
  • Osami Misumi
    • 1
    • 4
  • Tsuneyoshi Kuroiwa
    • 5
  1. 1.Department of Biological SciencesGraduate School of Science, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033Japan
  2. 2.Department of Molecular Biology, Faculty of ScienceSaitama University, Shimo-Ohkubo, Saitama-shi, Saitama 338-8570Japan
  3. 3.Department of Biomedical ChemistryGraduate School of Medicine, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033Japan
  4. 4.Bio-oriented Technology Research Advancement Institution (BRAIN), Toranomon, Minato-ku, Tokyo 105-0001Japan
  5. 5.Department of Life ScienceCollege of Science, Rikkyo (St.Paul’s) University, Nishiikebukuro, Toshima-ku, Tokyo 171-8501Japan

Personalised recommendations