Journal of Molecular Evolution

, Volume 33, Issue 3, pp 267–273 | Cite as

Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor

  • Susan E. Douglas
  • Seán Turner


The origin of plastids by either a single or multiple endosymbiotic event(s) and the nature of the progenitor(s) of plastids have been the subjects of much controversy. The sequence of the small subunit rRNA (Ssu rRNA) from the plastid of the chlorophyllc-containing algaCryptomonas ϕ is presented, allowing for the first time a comparison of this molecule from all of the major land plant and algal lineages. Using a distance matrix method, the phylogenetic relationships among representatives of these lineages have been inferred and the results indicate a common origin of plastids from a cyanobacterium-like ancestor. Within the plastid line of descent, there is a deep dichotomy between the chlorophyte/land plant lineage and the rhodophyte/chromophyte lineage, with the cyanelle ofCyanophora paradoxa forming the deepest branch in the latter group. Interestingly,Euglena gracilis and its colorless relativeAstasia longa are more related to the chromophytes than to the chlorophytes, raising once again the question of the origin of the euglenoid plastids.

Key words

Molecular phylogeny Plastid Algae Plant Small subunit RNA 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bhattacharya D, Elwood HJ, Goff LJ, Sogin ML (1990) Phylogeny ofGracilaria lemaneiformis (Rhodophyta) based on sequence analysis of its small subunit ribosomal RNA coding region. J Phycol 26:181–186CrossRefGoogle Scholar
  2. Cavalier-Smith T (1982) The origins of plastids. Biol J Linn Soc 17:289–306Google Scholar
  3. Cavalier-Smith T (1986) The Kingdom Chromista: origin and systematics. Prog Phycol Res 4:309–347Google Scholar
  4. Cavalier-Smith T (1987) Glaucophyceae and the origin of plants. Evol Trends Plants 1(2):75–78Google Scholar
  5. Douglas SE (1988) Physical mapping of the plastid genome from the chlorophyllc-containing alga.Cryptomonas ϕ. Curr Genet 14:591–598CrossRefGoogle Scholar
  6. Douglas SE, Durnford DG (1989) The small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is plastid encoded in the chlorophyllc-containing algaCryptomonas ϕ. Plant Mol Biol 13:13–20CrossRefPubMedGoogle Scholar
  7. Douglas SE, Durnford DG (1990a) Nucleotide sequence of the genes for ribosomal protein S4 and tRNAArg from the chlorophyllc-containing algaCryptomonas ϕ. Nucleic Acids Res 18:1903PubMedGoogle Scholar
  8. Douglas SE, Durnford DG (1990b), Sequence analysis of the plastid rDNA spacer region of the chlorophyllc-containing algaCryptomonas ϕ. DNA sequence. J DNA Sequencing Mapping 1:55–62Google Scholar
  9. Douglas SE, Durnford DG, Morden CW (1990) Nucleotide sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase fromCryptomonas ϕ: evidence supporting the polyphyletic origin of plastids. J Phycol 26:500–508CrossRefGoogle Scholar
  10. Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151PubMedGoogle Scholar
  11. Eschbach S, Wolters J, Sitte P (1991) Primary and secondary structure of the nuclear small subunit ribosomal RNA of the cryptomonadPyrenomonas salina as inferred from the gene sequence: evolutionary implications. J Mol Evol 32:247–252PubMedGoogle Scholar
  12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  13. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  14. Gibbs SP (1970) The comparative ultrastructure of the algal chloroplast. Ann NY Acad Sci 175:454–473Google Scholar
  15. Gibbs SP (1978) The chloroplasts ofEuglena may have evolved from symbiotic green algae. Can J Bot 56:2883–2889Google Scholar
  16. Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592PubMedGoogle Scholar
  17. Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5:294–299CrossRefPubMedGoogle Scholar
  18. Gray MW, Sankoff D, Cedergren RJ (1984) On the evolutionary descent of organisms and organelles: a global phylogeny based on a highly conserved core in small subunit ribosomal RNA. Nucleic Acids Res 12:5837–5852PubMedGoogle Scholar
  19. Gutell RG, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–216PubMedGoogle Scholar
  20. Hendriks L, de Baere R, van de Peer Y, Gorin A, de Wachter R (1991) The evolutionary position of the rhodophytePorphyra umbilicalis and the basidiomyceteLeucosporidium scottii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol Evol 32:167–177PubMedGoogle Scholar
  21. Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472PubMedGoogle Scholar
  22. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132Google Scholar
  23. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160Google Scholar
  24. Lenaers G, Scholi C, Bhaud Y, Saint-Hilaire D, Herzog M (1991) A molecular phylogeny of dinoflagellate protists (Pyrophyta) inferred from the sequence of 24S rRNA divergent domains D1 and D8. J Mol Evol 32:53–63CrossRefPubMedGoogle Scholar
  25. Lewin RA (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256:735–737CrossRefGoogle Scholar
  26. Maid U, Zetsche K (1990) Nucleotide sequence of the plastid 16S rRNA gene of the red algaCyanidium caldarium. Nucleic Acids Res 18(13):3996PubMedGoogle Scholar
  27. Margulis L, Obar R (1985)Heliobacterium and origin of chrysoplasts. BioSystems 17:317–325CrossRefPubMedGoogle Scholar
  28. Markowicz Y, Loiseaux-de Göer S, Mache R (1988) Presence of a 16S rRNA pseudogene in the bi-molecular plastid genome of the primitive brown algaPylaiella littoralis. Evolutionary implications. Curr Genet 14:599–608CrossRefPubMedGoogle Scholar
  29. Morden CW, Golden SS (1989a)psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337:382–385CrossRefPubMedGoogle Scholar
  30. Morden CW, Golden SS (1989b)psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Corrigendum. Nature 339:400CrossRefGoogle Scholar
  31. Morden CW, Golden SS (1991) Sequence analysis and phylogenetic reconstruction of the genes encoding the large and small subunits of ribulose-1,5-bisphosphate carboxylase/oxygenase from the chlorophyll b containing prokaryoteProchlorothrix hollandica. J Mol Evol 32:379–395PubMedGoogle Scholar
  32. Neefs J-M, Van de Peer Y, Henriks L, De Wachter R (1990) Compilation of small ribosomal RNA sequences. Nucleic Acids Res 18 [Suppl]:2237–2247PubMedGoogle Scholar
  33. Olsen GJ (1987) Earliest phylogenetic branchings: comparing rRNA-based evolutionary trees inferred with various techniques. Cold Spring Harbor Symp Quant Biol 52:829–837Google Scholar
  34. Olsen GJ (1988) Phylogenetic analysis using ribosomal RNA. Methods Enzymol 164:793–812PubMedGoogle Scholar
  35. Perasso R, Baroin A, Liang HQ, Bachellerie JP, Adoutte A (1989) Origin of the algae. Nature 339:142–144CrossRefPubMedGoogle Scholar
  36. Pribnow D (1975) Nucleotide sequence of an RNA polymerase binding site at an early T7 promoter. Proc Natl Acad Sci USA 72:784–788PubMedGoogle Scholar
  37. Raven PH (1970) A multiple origin for plastids and mitochondria. Science 169:641–646PubMedGoogle Scholar
  38. Reith M, Douglas SE (1990) Localization of β-phycoerythrin to the thylakoid lumen ofCryptomonas ϕ does not require a transit peptide. Plant Mol Biol 15:585–592CrossRefPubMedGoogle Scholar
  39. Sanger F, Nicklen S, Coulsen AR (1977) Sequencing by chain termination with dideoxynucleotides. Proc Natl Acad Sci USA 74:5463–5467PubMedGoogle Scholar
  40. Seewaldt E, Stackebrandt E (1982) Partial sequence of 16S ribosomal RNA and the phylogeny ofProchloron. Nature 295:618–620CrossRefGoogle Scholar
  41. Siemeister G, Hachtel W (1990) Organization and nucleotide sequence of ribosomal RNA genes on a circular 73 kbp DNA from the colourless flagellateAstasia longa. Curr Genet 17:433–438CrossRefPubMedGoogle Scholar
  42. Sourdis J, Nei M (1988) Relative efficiencies of the maximum parsimony and distance matrix methods in obtaining the correct phylogenetic tree. Mol Biol Evol 5:298–311PubMedGoogle Scholar
  43. Turner S, Burger-Wiersma T, Giovannoni S, Mur LR, Pace NR (1989) The relationship of a prochlorophyteProchorothrix hollandica to green chloroplasts. Nature 337:380–382CrossRefPubMedGoogle Scholar
  44. van den Eyende H, de Baere R, de Roeck E, van de Peer Y, Vandenberghe A, Willikens P, de Wachter R (1988) The 5S ribosomal RNA sequences of a red algal rhodoplast and a gymnosperm chloroplast. Implications for the evolution of plastids and cyanobacteria. J Mol Evol 27:126–132PubMedGoogle Scholar
  45. Whatley JM, Whatley FR (1981) Chloroplast evolution. New Phytol 87:233–247Google Scholar
  46. Whatley JM, John P, Whatley FR (1979) From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc R Soc Lond B 204:165–187PubMedGoogle Scholar
  47. Wilhelm C (1987) The existence of chlorophyll c in the chl b-containing, light-harvesting complex of the green algaMantionella squamata (Prasinophyceae). Bot Acta 101:7–10Google Scholar
  48. Witt D, Stackebrandt E (1988) Disproving the hypothesis of a common ancestry for theOchromonas danica chrysoplast andHeliobacterium chlorum. Arch Microbiol 150:244–248CrossRefGoogle Scholar
  49. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  50. Woese CR, Debrunner-Vossbrinck B, Oyaizu H, Stackebrandt E, Ludwig W (1985) Gram-positive bacteria: possible photosynthetic ancestry. Science 229:762–765PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1991

Authors and Affiliations

  • Susan E. Douglas
    • 1
  • Seán Turner
    • 2
  1. 1.Institute of Marine BiosciencesNational Research CouncilHalifaxCanada
  2. 2.Department of Biology and Institute for Molecular and Cellular BiologyIndiana UniversityBloomingtonUSA

Personalised recommendations