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. 1984 Jul 25;12(14):5837–5852. doi: 10.1093/nar/12.14.5837

On the evolutionary descent of organisms and organelles: a global phylogeny based on a highly conserved structural core in small subunit ribosomal RNA.

M W Gray, D Sankoff, R J Cedergren
PMCID: PMC320035  PMID: 6462918

Abstract

To probe the earliest evolutionary events attending the origin of the five known genome types (archaebacterial, eubacterial, nuclear, mitochondrial and plastid), we have analyzed sequences corresponding to a ubiquitous, highly conserved core of secondary structure in small subunit rRNA. Our results support (i) the existence of three primary lineages (archaebacterial, eubacterial, and nuclear), (ii) a specific eubacterial ancestry for plastids and mitochondria (plant, animal, fungal), and (iii) an endosymbiotic, evolutionary origin of the two types of organelle from within distinct groups of eubacteria (blue-green algae (cyanobacteria) in the case of plastids, nonphotosynthetic aerobic bacteria in the case of mitochondria). In addition, our analysis suggests (iv) a biphyletic origin of mitochondria, with animal and fungal mitochondria branching together but separately from plant mitochondria, and (v) a monophyletic origin of plastids. The method described here provides a powerful and generally applicable molecular taxonomic approach towards a global phylogeny encompassing all organisms and organelles.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brosius J., Palmer M. L., Kennedy P. J., Noller H. F. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4801–4805. doi: 10.1073/pnas.75.10.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carbon P., Ebel J. P., Ehresmann C. The sequence of the ribosomal 16S RNA from Proteus vulgaris. Sequence comparison with E. coli 16S RNA and its use in secondary model building. Nucleic Acids Res. 1981 May 25;9(10):2325–2333. doi: 10.1093/nar/9.10.2325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carbon P., Ehresmann C., Ehresmann B., Ebel J. P. The complete nucleotide sequence of the ribosomal 16-S RNA from Excherichia coli. Experimental details and cistron heterogeneities. Eur J Biochem. 1979 Oct 15;100(2):399–410. doi: 10.1111/j.1432-1033.1979.tb04183.x. [DOI] [PubMed] [Google Scholar]
  4. Cedergren R. J. An evaluation of mitochondrial tRNA gene evolution and its relation to the genetic code. Can J Biochem. 1982 Apr;60(4):475–479. doi: 10.1139/o82-056. [DOI] [PubMed] [Google Scholar]
  5. Cedergren R. J., Sankoff D., LaRue B., Grosjean H. The evolving tRNA molecule. CRC Crit Rev Biochem. 1981;11(1):35–104. doi: 10.3109/10409238109108699. [DOI] [PubMed] [Google Scholar]
  6. Cox R. A., Kelly J. M. Structural aspects of eukaryotic ribosomes. Biochem Soc Symp. 1982;47:11–48. [PubMed] [Google Scholar]
  7. Crick F. H. The origin of the genetic code. J Mol Biol. 1968 Dec;38(3):367–379. doi: 10.1016/0022-2836(68)90392-6. [DOI] [PubMed] [Google Scholar]
  8. Dron M., Rahire M., Rochaix J. D. Sequence of the chloroplast 16S rRNA gene and its surrounding regions of Chlamydomonas reinhardii. Nucleic Acids Res. 1982 Dec 11;10(23):7609–7620. doi: 10.1093/nar/10.23.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dunn R., McCoy J., Simsek M., Majumdar A., Chang S. H., Rajbhandary U. L., Khorana H. G. The bacteriorhodopsin gene. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6744–6748. doi: 10.1073/pnas.78.11.6744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eperon I. C., Anderson S., Nierlich D. P. Distinctive sequence of human mitochondrial ribosomal RNA genes. Nature. 1980 Jul 31;286(5772):460–467. doi: 10.1038/286460a0. [DOI] [PubMed] [Google Scholar]
  11. Fox G. E., Stackebrandt E., Hespell R. B., Gibson J., Maniloff J., Dyer T. A., Wolfe R. S., Balch W. E., Tanner R. S., Magrum L. J. The phylogeny of prokaryotes. Science. 1980 Jul 25;209(4455):457–463. doi: 10.1126/science.6771870. [DOI] [PubMed] [Google Scholar]
  12. Fox T. D., Leaver C. J. The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981 Nov;26(3 Pt 1):315–323. doi: 10.1016/0092-8674(81)90200-2. [DOI] [PubMed] [Google Scholar]
  13. Graf L., Roux E., Stutz E., Kössel H. Nucleotide sequence of a Euglena gracilis chloroplast gene coding for the 16S rRNA: homologies to E. coli and Zea mays chloroplast 16S rRNA. Nucleic Acids Res. 1982 Oct 25;10(20):6369–6381. doi: 10.1093/nar/10.20.6369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gray M. W., Doolittle W. F. Has the endosymbiont hypothesis been proven? Microbiol Rev. 1982 Mar;46(1):1–42. doi: 10.1128/mr.46.1.1-42.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gray M. W. Mitochondrial genome diversity and the evolution of mitochondrial DNA. Can J Biochem. 1982 Mar;60(3):157–171. doi: 10.1139/o82-022. [DOI] [PubMed] [Google Scholar]
  16. Gupta R., Lanter J. M., Woese C. R. Sequence of the 16S Ribosomal RNA from Halobacterium volcanii, an Archaebacterium. Science. 1983 Aug 12;221(4611):656–659. doi: 10.1126/science.221.4611.656. [DOI] [PubMed] [Google Scholar]
  17. Heckman J. E., Sarnoff J., Alzner-DeWeerd B., Yin S., RajBhandary U. L. Novel features in the genetic code and codon reading patterns in Neurospora crassa mitochondria based on sequences of six mitochondrial tRNAs. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3159–3163. doi: 10.1073/pnas.77.6.3159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hiesel R., Brennicke A. Cytochrome oxidase subunit II gene in mitochondria of Oenothera has no intron. EMBO J. 1983;2(12):2173–2178. doi: 10.1002/j.1460-2075.1983.tb01719.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huysmans E., Dams E., Vandenberghe A., De Wachter R. The nucleotide sequences of the 5S rRNAs of four mushrooms and their use in studying the phylogenetic position of basidiomycetes among the eukaryotes. Nucleic Acids Res. 1983 May 11;11(9):2871–2880. doi: 10.1093/nar/11.9.2871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jukes T. H. Evolution of the amino acid code: inferences from mitochondrial codes. J Mol Evol. 1983;19(3-4):219–225. doi: 10.1007/BF02099969. [DOI] [PubMed] [Google Scholar]
  21. Kobayashi M., Seki T., Yaginuma K., Koike K. Nucleotide sequences of small ribosomal RNA and adjacent transfer RNA genes in rat mitochondrial DNA. Gene. 1981 Dec;16(1-3):297–307. doi: 10.1016/0378-1119(81)90085-8. [DOI] [PubMed] [Google Scholar]
  22. Köchel H. G., Küntzel H. Nucleotide sequence of the Aspergillus nidulans mitochondrial gene coding for the small ribosomal subunit RNA: homology to E. coli 16S rRNA. Nucleic Acids Res. 1981 Nov 11;9(21):5689–5696. doi: 10.1093/nar/9.21.5689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Küntzel H., Köchel H. G. Evolution of rRNA and origin of mitochondria. Nature. 1981 Oct 29;293(5835):751–755. doi: 10.1038/293751a0. [DOI] [PubMed] [Google Scholar]
  24. Küntzel H., Piechulla B., Hahn U. Consensus structure and evolution of 5S rRNA. Nucleic Acids Res. 1983 Feb 11;11(3):893–900. doi: 10.1093/nar/11.3.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Maly P., Brimacombe R. Refined secondary structure models for the 16S and 23S ribosomal RNA of Escherichia coli. Nucleic Acids Res. 1983 Nov 11;11(21):7263–7286. doi: 10.1093/nar/11.21.7263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mankin A. S., Kopylov A. M., Bogdanov A. A. Modification of 18 S rRNA in the 40 S ribosomal subunit of yeast with dimethyl sulfate. FEBS Lett. 1981 Nov 2;134(1):11–14. doi: 10.1016/0014-5793(81)80539-x. [DOI] [PubMed] [Google Scholar]
  27. Raynal F., Michot B., Bachellerie J. P. Complete nucleotide sequence of mouse 18 S rRNA gene: comparison with other available homologs. FEBS Lett. 1984 Feb 27;167(2):263–268. doi: 10.1016/0014-5793(84)80139-8. [DOI] [PubMed] [Google Scholar]
  28. Reanney D. C. On the origin of prokaryotes. J Theor Biol. 1974 Nov;48(1):243–251. doi: 10.1016/0022-5193(74)90194-5. [DOI] [PubMed] [Google Scholar]
  29. Rubtsov P. M., Musakhanov M. M., Zakharyev V. M., Krayev A. S., Skryabin K. G., Bayev A. A. The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene from Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Dec 11;8(23):5779–5794. doi: 10.1093/nar/8.23.5779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Salim M., Maden B. E. Nucleotide sequence of Xenopus laevis 18S ribosomal RNA inferred from gene sequence. Nature. 1981 May 21;291(5812):205–208. doi: 10.1038/291205a0. [DOI] [PubMed] [Google Scholar]
  31. Sankoff D., Cedergren R. J., McKay W. A strategy for sequence phylogeny research. Nucleic Acids Res. 1982 Jan 11;10(1):421–431. doi: 10.1093/nar/10.1.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sor F., Fukuhara H. Séquence nucléotidique du gène de l'ARN ribosomique 15S mitochondrial de la levure. C R Seances Acad Sci D. 1980 Dec 8;291(12):933–936. [PubMed] [Google Scholar]
  33. Spencer D. F., Schnare M. N., Gray M. W. Pronounced structural similarities between the small subunit ribosomal RNA genes of wheat mitochondria and Escherichia coli. Proc Natl Acad Sci U S A. 1984 Jan;81(2):493–497. doi: 10.1073/pnas.81.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stiegler P., Carbon P., Ebel J. P., Ehresmann C. A general secondary-structure model for procaryotic and eucaryotic RNAs from the small ribosomal subunits. Eur J Biochem. 1981 Dec;120(3):487–495. doi: 10.1111/j.1432-1033.1981.tb05727.x. [DOI] [PubMed] [Google Scholar]
  35. Tohdoh N., Sugiura M. The complete nucleotide sequence of 16S ribosomal RNA gene from tobacco chloroplasts. Gene. 1982 Feb;17(2):213–218. doi: 10.1016/0378-1119(82)90074-9. [DOI] [PubMed] [Google Scholar]
  36. Tomioka N., Sugiura M. The complete nucleotide sequence of a 16S ribosomal RNA gene from a blue-green alga, Anacystis nidulans. Mol Gen Genet. 1983;191(1):46–50. doi: 10.1007/BF00330888. [DOI] [PubMed] [Google Scholar]
  37. Torczynski R., Bollon A. P., Fuke M. The complete nucleotide sequence of the rat 18S ribosomal RNA gene and comparison with the respective yeast and frog genes. Nucleic Acids Res. 1983 Jul 25;11(14):4879–4890. doi: 10.1093/nar/11.14.4879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Van Etten R. A., Walberg M. W., Clayton D. A. Precise localization and nucleotide sequence of the two mouse mitochondrial rRNA genes and three immediately adjacent novel tRNA genes. Cell. 1980 Nov;22(1 Pt 1):157–170. doi: 10.1016/0092-8674(80)90164-6. [DOI] [PubMed] [Google Scholar]
  39. Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Woese C. R., Gutell R., Gupta R., Noller H. F. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev. 1983 Dec;47(4):621–669. doi: 10.1128/mr.47.4.621-669.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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