Skip to main content
SpringerLink
Log in

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

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1

Similar content being viewed by others

References

  1. J Adachi PJ Waddell W Martin M Hasegawa (2000) ArticleTitlePlastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J Mol Evol 50 348–358 Occurrence Handle1:CAS:528:DC%2BD3cXivFyjur8%3D Occurrence Handle10795826

    CAS  PubMed  Google Scholar 

  2. JO Andersson AJ Roger (2002) ArticleTitleA cyanobacterial gene in nonphotosynthetic protists—An early chloroplast acquisition in Eukaryotes? Curr Biol 12 115–119 Occurrence Handle10.1016/S0960-9822(01)00649-2 Occurrence Handle1:CAS:528:DC%2BD38XhtVKru7o%3D Occurrence Handle11818061

    Article  CAS  PubMed  Google Scholar 

  3. SL Baldauf AJ Roger I Wenk-Siefert WF Doolittle (2000) ArticleTitleA kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290 972–977 Occurrence Handle10.1126/science.290.5493.972 Occurrence Handle1:CAS:528:DC%2BD3cXnvVWksL0%3D Occurrence Handle11062127

    Article  CAS  PubMed  Google Scholar 

  4. D Bhattacharya L Medlin (1995) ArticleTitleThe phylogeny of plastids: A review based on comparisons of small subunit ribosomal RNA coding regions. J Phycol 31 489–498 Occurrence Handle1:CAS:528:DyaK2MXos1Gls7Y%3D

    CAS  Google Scholar 

  5. JH Camin RR Sokal (1965) ArticleTitleA method for deducing branching sequences in phylogeny. Evolution 19 311–326

    Google Scholar 

  6. T Cavalier-Smith (2002) ArticleTitleChloroplast evolution: Secondary symbiogenesis and multiple losses. Curr Biol 12 R62–R64 Occurrence Handle10.1016/S0960-9822(01)00675-3 Occurrence Handle1:CAS:528:DC%2BD38XhtVKrurg%3D Occurrence Handle11818081

    Article  CAS  PubMed  Google Scholar 

  7. CF Delwiche (1999) ArticleTitleTracing the thread of plastid diversity through the tapestry of life. Am Nat 154 164–177 Occurrence Handle10.1086/303291

    Article  Google Scholar 

  8. CF Delwiche JD Palmer (1997) The origin of plastids and their spread via secondary symbiosis. D Bhattacharya (Eds) Origin of algae and their plastids. Springer-Verlag Wien 53–86

    Google Scholar 

  9. MW Fawley CM Lee (1990) ArticleTitlePigment composition of the scaly green flagellate Mesostigma viride (Micromonadophyceae) is similar to that of the siphonous green alga Bryopsis plumosa (Ulvophyceae). J Phycol 26 666–670 Occurrence Handle1:CAS:528:DyaK3MXltFSis78%3D

    CAS  Google Scholar 

  10. J Felsenstein (1985) ArticleTitleConfidence limits on phylogenies: an approach using bootstrap. Evolution 38 16–24

    Google Scholar 

  11. T Friedl (1997) The evolution of the green algae. D Bhattacharya (Eds) Origin of algae and their plastids. Springer-Verlag Wien 87–101

    Google Scholar 

  12. LE Graham LW Wilcox (2000) Algae. Prentice Hall Upper Saddle River, NJ

    Google Scholar 

  13. V Hannaert E Saavedra F Duffieux JP Szikora DJ Rigden PAM Michels FR Opperdoes (2003) ArticleTitlePlant-like traits associated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci USA 100 1067–1071 Occurrence Handle10.1073/pnas.0335769100 Occurrence Handle1:CAS:528:DC%2BD3sXhtF2gtro%3D Occurrence Handle12552132

    Article  CAS  PubMed  Google Scholar 

  14. T Itoh W Martin M Nei (2002) ArticleTitleAcceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA 99 12944–12948 Occurrence Handle10.1073/pnas.192449699 Occurrence Handle1:CAS:528:DC%2BD38XnvFGht7s%3D Occurrence Handle12235368

    Article  CAS  PubMed  Google Scholar 

  15. M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111–120 Occurrence Handle7463489

    PubMed  Google Scholar 

  16. AM Lambowitz M Belfort (1993) ArticleTitleIntrons as mobile genetic elements. Ann Rev Bichem 62 587–622 Occurrence Handle10.1146/annurev.bi.62.070193.003103 Occurrence Handle1:CAS:528:DyaK3sXlvFKltL0%3D

    Article  CAS  Google Scholar 

  17. W Martin RG Herrmann (1998) ArticleTitleGene transfer from organelles to the nucleus: How much, what happens, and why? Plant Physiol 118 9–17 Occurrence Handle1:CAS:528:DyaK1cXmtV2msLs%3D Occurrence Handle9733521

    CAS  PubMed  Google Scholar 

  18. W Martin T Rujan E Richly A Hansen S Cornelsen T Lins et al. (2002) ArticleTitleEvolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99 12246–12251 Occurrence Handle10.1073/pnas.182432999 Occurrence Handle1:CAS:528:DC%2BD38XntlCks70%3D Occurrence Handle12218172

    Article  CAS  PubMed  Google Scholar 

  19. JE Maul JW Lilly L Cui CW dePamphilis W Miller EH Harris DB Stern (2002) ArticleTitleThe Chlamydomonas reinhardtii plastid chromosome: Islands of genes in a sea of repeats. Plant Cell 14 2659–2679 Occurrence Handle10.1105/tpc.006155 Occurrence Handle1:CAS:528:DC%2BD38XovF2qtbg%3D Occurrence Handle12417694

    Article  CAS  PubMed  Google Scholar 

  20. GI McFadden (2001) ArticleTitlePrimary and secondary endosymbiosis and the origin of plastids. J Phycol 37 951–959 Occurrence Handle10.1046/j.1529-8817.2001.01126.x

    Article  Google Scholar 

  21. AE Montegut-Felkner RE Triemer (1997) ArticleTitlePhylogenetic relationships of selected euglenoid genera based on morphological and molecular data. J Phycol 33 512–519 Occurrence Handle1:CAS:528:DyaK2sXkslOisrk%3D

    CAS  Google Scholar 

  22. CW Morden CF Delwiche M Kuhsel JD Palmer (1992) ArticleTitleGene phylogenies and the endosymbiotic origin of plastids. BioSystems 28 75–90 Occurrence Handle10.1016/0303-2647(92)90010-V Occurrence Handle1:CAS:528:DyaK3sXktVaitb4%3D Occurrence Handle1292669

    Article  CAS  PubMed  Google Scholar 

  23. AN Müllner DG Angeler R Samuel EW Linton RE Triemer (2001) ArticleTitlePhylogenetic analysis of phagotrophic, phototrophic and osmotrophic euglenoids by using the nuclear 18S rDNA sequence. Int J Syst Evol Micr 51 783–791

    Google Scholar 

  24. B Nelissen Y Van de Peer A Wilmotte R De Wachter (1995) ArticleTitleAn early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol 12 1166–1173 Occurrence Handle1:CAS:528:DyaK2MXovVOisLk%3D Occurrence Handle8524048

    CAS  PubMed  Google Scholar 

  25. H Nozaki M Matsuzaki M Takahara O Misumi H Kuroiwa M Hasegawa et al. (2003) ArticleTitleThe 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 Evol 56 485–497 Occurrence Handle10.1007/s00239-002-2419-9 Occurrence Handle1:CAS:528:DC%2BD3sXisV2qtr8%3D Occurrence Handle12664168

    Article  CAS  PubMed  Google Scholar 

  26. N Ohta M Matsuzaki O Misumi S Miyagishima H Nozaki K Tanaka et al. (2003) ArticleTitleComplete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Research 10 67–77 Occurrence Handle1:CAS:528:DC%2BD3sXjsFCqsLs%3D Occurrence Handle12755171

    CAS  PubMed  Google Scholar 

  27. K Ohyama H Fukuzawa T Kohchi H Shirai T Sano S Sano et al. (1986) ArticleTitleChloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322 572–574 Occurrence Handle1:CAS:528:DyaL28Xlt1ymt7o%3D

    CAS  Google Scholar 

  28. JD Palmer CF Delwiche (1998) The origin and evolution of plastids and their genomes. PS Soltis DE Soltis JJ Doyle (Eds) Molecular systematics of plants. II. DNA sequencing. Kluwer Academic Boston 375–409

    Google Scholar 

  29. A Preisfeld S Berger I Busse S Liller HG Ruppel (2000) ArticleTitlePhylogenetic analyses of various euglenoid taxa (Euglenozoa) based on 18S rDNA sequence data. J Phycol 36 220–226 Occurrence Handle10.1046/j.1529-8817.2000.99091.x Occurrence Handle1:CAS:528:DC%2BD3cXmslSmtrk%3D

    Article  CAS  Google Scholar 

  30. C Schmitz-Linneweber RM Maier JP Alcaraz A Cottet RG Herrmann R Mache (2001) ArticleTitleThe plastid chromosome of spinach (Spinacia oleracea): Complete nucleotide sequence and gene organization. Plant Mol Biol 45 307–315 Occurrence Handle1:CAS:528:DC%2BD3MXis1Kgt74%3D Occurrence Handle11292076

    CAS  PubMed  Google Scholar 

  31. DL Swofford (2002) PAUP* 4.0: Phylogenetic Analysis Using Parsimony, version 4.0b10. Sinauer Associates, Inc. Sunderland, MA

    Google Scholar 

  32. M Turmel C Otis C Lemieux (1999) ArticleTitleThe complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: Insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96 10248–10253 Occurrence Handle1:CAS:528:DyaK1MXlvFensr4%3D Occurrence Handle10468594

    CAS  PubMed  Google Scholar 

  33. M Turmel C Otis C Lemieux (2002) ArticleTitleThe 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 USA 99 11275–11280 Occurrence Handle10.1073/pnas.162203299 Occurrence Handle1:CAS:528:DC%2BD38XmslSmtbs%3D Occurrence Handle12161560

    Article  CAS  PubMed  Google Scholar 

  34. Y Van de Peer SA Rensing UG Maier R De Wachter (1996) ArticleTitleSubstitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc Natl Acad Sci USA 93 7732–7736 Occurrence Handle10.1073/pnas.93.15.7732 Occurrence Handle1:CAS:528:DyaK28XksFSrtr4%3D Occurrence Handle8755544

    Article  CAS  PubMed  Google Scholar 

  35. T Wakasugi J Tsudzuki S Ito K Nakashima T Tsudzuki M Sugiura (1994) ArticleTitleLoss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91 9794–9798 Occurrence Handle1:CAS:528:DyaK2cXmvFChsro%3D Occurrence Handle7937893

    CAS  PubMed  Google Scholar 

  36. EO Wiley D Siegel-Causey DR Brooks VA Funk (1991) The compleat cladist: A primer of phylogenetic procedures. Special Publication No 19. Museum of Natural History. University of Kansas Lawrence, KS

    Google Scholar 

  37. HS Yoon JD Hackett D Bhattacharya (2002a) ArticleTitleA single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci USA 99 11724–11729 Occurrence Handle1:CAS:528:DC%2BD38XntFWqtrw%3D

    CAS  Google Scholar 

  38. HS Yoon JD Hackett G Pinto D Bhattacharya (2002b) ArticleTitleThe single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99 15507–15512 Occurrence Handle1:CAS:528:DC%2BD3sXjvVOg

    CAS  Google Scholar 

  39. DJ Zwickl DM Hillis (2002) ArticleTitleIncreased taxon sampling greatly reduces phylogenetic error. Syst Biol 51 588–598 Occurrence Handle10.1080/10635150290102339 Occurrence Handle12228001

    Article  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

    Hisayoshi Nozaki & Osami Misumi

  2. Department of Molecular Biology, Faculty of Science, Saitama University, Shimo-Ohkubo, Saitama-shi, Saitama 338-8570, Japan

    Njij Ohta

  3. Department of Biomedical Chemistry, Graduate School of Medicine, University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

    Motomichi Matsuzaki

  4. Bio-oriented Technology Research Advancement Institution (BRAIN), Toranomon, Minato-ku, Tokyo 105-0001, Japan

    Osami Misumi

  5. Department of Life Science, College of Science, Rikkyo (St.Paul’s) University, Nishiikebukuro, Toshima-ku, Tokyo 171-8501, Japan

    Tsuneyoshi Kuroiwa

Authors
  1. Hisayoshi Nozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Njij Ohta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Motomichi Matsuzaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Osami Misumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tsuneyoshi Kuroiwa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hisayoshi Nozaki.

Addendum

Addendum

During the submission of this paper (received on 13 February 2003), Grzebyk et al. (J. Phycol. 39: 259-267, April 2003 issue) published a minireview “Mesozoic radiation of eukaryotic algae the portable plastid hypothesis.” They showed a phylogenetic analysis of 15 plastids inferred from gene presence and gene loss in 256 plastid protein-coding genes using the Camin-Sokal parsimony method. Their phylogenetic results are essentially the same as those of the present paper in the phylogenetic positions of the Glaucophyta and the monophyly of the red secondary plastids. However, Grzebyk et al. (2003) did not resolve robustly basal phylogenetic relationships within the green lineage, and did not demonstrate the chlorophycean phylogenetic position of the euglenoid secondary plastids due to the lack of Chlamydomonas. Although they robustly resolved the sister relationships between the Glaucophyta and the green plastid lineage as well as between Chlorella and euglenoid plastids, these results were not accepted based on the “maintenance” of certain plastid genes (Grzebyk et al. 2003).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nozaki, H., Ohta, N., Matsuzaki, M. et al. Phylogeny of Plastids Based on Cladistic Analysis of Gene Loss Inferred from Complete Plastid Genome Sequences . J Mol Evol 57, 377–382 (2003). https://doi.org/10.1007/s00239-003-2486-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2486-6

Keywords

Search

Navigation