Journal of Plant Research

, Volume 118, Issue 4, pp 247–255 | Cite as

A new scenario of plastid evolution: plastid primary endosymbiosis before the divergence of the “Plantae,” emended

Current Topics in Plant Research

Abstract

A recent hypothesis on the origin of eukaryotic phototrophs proposes that red algae, green plants (land plants plus green algae), 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 endosymbiotic events involving a phototrophic eukaryote and a host cell. However, the phylogenetic relationships among the three lineages of primary photosynthetic eukaryotes remained unresolved because previous nuclear multigene phylogenies used incomplete red algal gene sequences derived mainly from Porphyra (Rhodophyceae, one of the two lineages of the Rhodophyta), and lacked sequences from the Cyanidiophyceae (the other red algal lineage). Recently, the complete nuclear genome sequences from the red alga Cyanidioschyzon merolae 10D of the Cyanidiophyceae were determined. Using this genomic information, nuclear multigene phylogenetic analyses of various lineages of mitochondrion-containing eukaryotes were conducted. Since bacterial and amitochondrial eukaryotic genes present serious problems to eukaryotic phylogenies, basal eukaryotes were deduced based on the paralogous comparison of the concatenated α- and β-tubulin. The comparison demonstrated that cellular slime molds (Amoebozoa) represent the most basal position within the mitochondrion-containing organisms. With the cellular slime molds as the outgroup, phylogenetic analyses based on a 1,525-amino acid sequence of four concatenated nuclear genes [actin, elongation factor-1α( EF-1α), α-tubulin, and β-tubulin] resolved the presence of two large, robust monophyletic groups and the basal eukaryotic lineages (Amoebozoa). One of the two groups corresponded to the Opisthokonta (Metazoa and Fungi), whereas the other included various lineages containing primary and secondary plastids (red algae, green plants, glaucophytes, euglenoids, heterokonts, and apicomplexans), Ciliophora, Kinetoplastida, dinoflagellates, and Heterolobosea, for which the red algae represented the most basal lineage. Therefore, the plastid primary endosymbiosis likely occurred once in the common ancestor of the latter group, and the primary plastids were subsequently lost in the ancestor(s) of organisms within the group that now lacks primary plastids. A new concept of Plantae was proposed for phototrophic and nonphototrophic organisms belonging to this group on the basis of their common history of plastid primary endosymbiosis. This new scenario of plastid evolution is discussed here, and is compared with recent genome information and findings on the secondary endosymbiosis of the Euglena plastid.

Keywords

Eukaryotes Evolution Outgroup Plantae Plastid primary endosymbiosis Red algae 

Notes

Acknowledgments

I am grateful to Professor T. Cavalier-Smith (University of Oxford, UK) and Mr. T. Nakada (University of Tokyo, Japan) for their kind comments and discussion on the plastid evolution. This work was supported by Grant-in-Aid for Creative Scientific Research (No. 16GS0304) and by Grant-in-Aid for Scientific Research on Priority Areas (c) “Genome Biology” (No. 1320611) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

References

  1. Andersson JO, Roger AJ (2002) A cyanobacterial gene in nonphotosynthetic protists—an early chloroplast acquisition in Eukaryotes? Curr Biol 12:115–119Google Scholar
  2. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86Google Scholar
  3. Baldauf SL, Doolittle WF (1997) Origin and evolution of the slime molds (Mycetozoa). Proc Natl Acad Sci USA 94:12007–12012Google Scholar
  4. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977Google Scholar
  5. Bapteste E, Brinkmann H, Lee JA, Moore DV, Sensen CW, Gordon P, Duruflé L, Gaasterland T, Lopez P, Müller M, Philippe H (2002) The analysis of 100 genes supports the grouping of three highly divergent amoebae: dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci USA 99:1414–1419Google Scholar
  6. Bhattacharya D, Medlin L (1995) The phylogeny of plastids: a review based on comparisons of small subunit ribosomal RNA coding regions. J Phycol 31:489–498Google Scholar
  7. Bold HC, Wynne JM (1985) Introduction to the algae, 2nd edn. Prentice-Hall, Englewood Cliffs, NJGoogle Scholar
  8. Bolivar I, Fahrni JF, Smirnov A, Pawlowski J (2001) SSU rRNA-based phylogenetic position of the genera Amoeba and Chaos (Lobosea, Gymnamoebia): the origin of gymnamoebae revisited. Mol Biol Evol 18:2306–2314Google Scholar
  9. Burger G, Saint-Louis D, Gray MW, Lang F (1999) Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11:1675–1694Google Scholar
  10. Cavalier-Smith T (1998) Nemomonada and the origin of animals and fungi. In: Coombs GH, Vickerman K (eds) Evolutionary relationships among Protozoa. Kluwer Academic, Dordrecht, pp 375–407Google Scholar
  11. Cavalier-Smith T (2002a) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12:R62–R64Google Scholar
  12. Cavalier-Smith T (2002b) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354Google Scholar
  13. Cavalier-Smith T (2003) The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. Int J Syst Evol Microbiol 53:1741–1758Google Scholar
  14. Ciniglia C, Yoon HS, Pollio A, Pinto G, Bhattacharya D (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol Ecol 13:1827–1838Google Scholar
  15. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154:164–177Google Scholar
  16. Drouin G, Moniz de Sá M, Zuker M (1995) The Giardia lamblia actin gene and the phylogeny of eukaryotes. J Mol Evol 41:841–849Google Scholar
  17. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, Makarova KS, Ostrowski M, Oztas S, Robert C, Rogozin IB, Scanlan DJ, Tandeau de Marsac N, Weissenbach J, Wincker P, Wolf YI, Hess WR (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100:10020–10025Google Scholar
  18. Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426Google Scholar
  19. Felsenstein J (2002) PHYLIP (Phylogeny Inference Package) version 3.6a3. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  20. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511Google Scholar
  21. Gross W, Lenze D, Nowitzki U, Weiske J, Schnarrenberger C (1999) Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene 230:7–14Google Scholar
  22. Hannaert V, Saavedra E, Duffieux F, Szikora JP, Rigden DJ, Michels PAM, Opperdoes FR (2003) Plant-like traits associated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci USA 100:1067–1071Google Scholar
  23. Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20:1730–1735Google Scholar
  24. Hartman H, Fedorov A (2002) The origin of eukaryotic cell: a genomic investigation. Proc Natl Acad Sci USA 99:1420–1425Google Scholar
  25. Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993) Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388Google Scholar
  26. Hashimoto T, Sánchez LB, Shirakura T, Müller M, Hasegawa M (1998) Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci USA 95:6860–6865Google Scholar
  27. Itoh T, Martin W, Nei M (2002) Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci USA 99:12944–12948Google Scholar
  28. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. CABIOS 8:275–282Google Scholar
  29. Keeling PJ, Doolittle WF (1996) Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol Biol Evol 13:1297–1305Google Scholar
  30. Keeling PJ, Inagaki Y (2004) A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1alpha. Proc Natl Acad Sci USA 101:15380–15385Google Scholar
  31. Krepinsky K, Plaumann M, Martin W, Schnarrenberger C (2001) Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach. Cyanobacterial genes for chloroplast and cytosolic isoenzymes encoded in eukaryotic chromosomes. Eur J Biochem 268:2678–2686Google Scholar
  32. Leander BS (2004) Did trypanosomatid parasites have photosynthetic ancestors? Trends Microbiol 12:251–258Google Scholar
  33. Margulis L, Dolan MF, Guerrero R (2000) The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci USA 97:6954–6959Google Scholar
  34. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251Google Scholar
  35. Matsuzaki M, Misumi O, Shin-IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657Google Scholar
  36. McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959Google Scholar
  37. Montegut-Felkner AE, Triemer RE (1997) Phylogenetic relationships of selected euglenoid genera based on morphological and molecular data. J Phycol 33:512–519Google Scholar
  38. Morden CW, Delwiche CF, Kuhsel M, Palmer JD (1992) Gene phylogenies and the endosymbiotic origin of plastids. BioSystems 28:75–90Google Scholar
  39. Moreira D, Le Guyader H, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405:69–72Google Scholar
  40. Müllner AN, Angeler DG, Samuel R, Linton EW, Triemer RE (2001) Phylogenetic analysis of phagotrophic, phototrophic and osmotrophic euglenoids by using the nuclear 18S rDNA sequence. Int J Syst Evol Microbiol 51:783–791Google Scholar
  41. Nelissen B, Van de Peer Y, Wilmotte A, De Wachter R (1995) An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol 12:1166–1173Google Scholar
  42. Nozaki H (2004) A new scenario of plastid evolution and a new concept of “Plantae”. In: Abstract of the Twentieth International Symposium in conjunction with Award of the International Prize of Biology, Eukaryotic cells: their origin, evolution, and diversity. The National Science Museum, Tokyo, p 16Google Scholar
  43. Nozaki H, Matsuzaki1 M, Takahara M, Misumi1 O, Kuroiwa H, Hasegawa M, Shin-IT, Kohara Y, Ogasawara N, Kuroiwa T (2003a) The 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 56:485–497Google Scholar
  44. Nozaki H, Ohta N, Matsuzaki M, Misumi O, Kuroiwa T (2003b) Phylogeny of plastids based on cladistic analysis of gene loss inferred from complete plastid genome sequences. J Mol Evol 57:377–382Google Scholar
  45. Nozaki H, Matsuzaki1 M, Misumi1 O, Kuroiwa H, Hasegawa M, Higashiyama T, Shin-IT, Kohara Y, Ogasawara N, Kuroiwa T (2004) Cyanobacterial genes transmitted to the nucleus before divergence of red algae in the Chromista. J Mol Evol 59:103–113Google Scholar
  46. Nozaki H, Matsuzaki M, Misumi O, Kuroiwa H, Higashiyama T, Kuroiwa T (2005) Phylogenetic implications of the CAD complex from the primitive red alga Cyanidioschyzon merolae (Cyanidiales, Rhodophyta). J Phycol 41(3):652–657Google Scholar
  47. Oliveria MC, Bhattacharya D (2000) Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. Am J Bot 87:482–492Google Scholar
  48. Oudot-Le Secq M-P, Kloareg B, Loiseaux-De Goër S (2002) The mitochondrial genome of the brown alga Laminaria digitata: a comparative analysis. Eur J Phycol 37:163–172Google Scholar
  49. Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose-1, 6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3:1169–1175Google Scholar
  50. Preisfeld A, Berger S, Busse I, Liller S, Ruppel HG (2000) Phylogenetic analyses of various euglenoid taxa (Euglenozoa) based on 18S rDNA sequence data. J Phycol 36:220–226Google Scholar
  51. Prescott GW (1969) The algae: review. Otto Koeltz Science, KoenigsteinGoogle Scholar
  52. Rivero F, Dislich H, Glockner G, Noegel AA (2001) The Dictyostelium discoideum family of Rho-related proteins. Nucl Acids Res 29:1068–1079Google Scholar
  53. Smith GM (1955) Cryptogamic botany, vol 1. McGraw-Hill, New YorkGoogle Scholar
  54. South GR, Whittick A (1987) Introduction to psychology. Blackwell, OxfordGoogle Scholar
  55. Stechmann A, Cavalier-Smith T (2002) Rooting the eukaryote tree by using a derived gene fusion. Science 297:89–91Google Scholar
  56. Stechmann A, Cavalier-Smith T (2003) The root of the eukaryote tree pinpointed. Curr Biol 13:R665–R666Google Scholar
  57. Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA 94:4520–4525Google Scholar
  58. Stiller JW, Duffield ECS, Hall BD (1998) Amitochondriate amoebae and the evolution of DNA-dependent RNA polymerase II. Proc Natl Acad Sci USA 95:11769–11774Google Scholar
  59. Stiller JW, Riley J, Hall BD (2001) Are red algae plants? A critical evaluation of three key molecular data sets. J Mol Evol 52:527–539Google Scholar
  60. Strimmer K, Von Haesler A (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969Google Scholar
  61. Tachezy J, Sánchez LB, Müller M (2001) Mitochondrial type iron–sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18:1919–1928Google Scholar
  62. Tanikawa N, Akimoto H, Ogoh K, Chun W, Ohmiya Y (2004) Expressed sequence tag analysis of the dinoflagellate Lingulodinium polyedrum during dark phase. Photochem Photobiol 80:31–25Google Scholar
  63. Tovar J, Leon-Avila G, Sanchez LB, Sutak R, Tachezy J, van der Giezen M, Hernandez M, Muller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron–sulphur protein maturation. Nature 426:172–1766Google Scholar
  64. Van de Peer Y, Rensing SA, Maier UG, De Wachter R (1996) Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc Natl Acad Sci USA 93:7732–7736Google Scholar
  65. Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576Google Scholar
  66. Williams BA, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869Google Scholar
  67. Winker S, Woese CR (1991) A definition of the domains Archaea, Bacteria and Eucarya in terms of small subunit ribosomal RNA characteristics. Syst Appl Microbiol 14:305–310Google Scholar
  68. Yoon HS, Hackett JD, Bhattacharya D (2002) A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci USA 99:11724–11729Google Scholar

Copyright information

© The Botanical Society of Japan and Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of ScienceUniversity of TokyoTokyoJapan

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