Skip to main content
RNA logoLink to RNA
. 2000 Oct;6(10):1339–1346. doi: 10.1017/s135583820000087x

Evolution of four types of RNA editing in myxomycetes.

T L Horton 1, L F Landweber 1
PMCID: PMC1370006  PMID: 11073211

Abstract

The myxomycete Physarum polycephalum requires extensive RNA editing to create functional mitochondrial transcripts. The cytochrome c oxidase subunit 1 (col) transcript exhibits a combination of editing forms not found together in any other eukaryotic RNA: 66 insertions of ribonucleotides (59 Cs, a single U, and three mixed dinucleotides) as well as base conversion of four Cs to Us (Gott et al., J Biol Chem, 1993, 268:25483-25486). Through a phylogenetic survey of col DNA genes and RNA transcripts in representative myxomycetes, we have decoupled the four types of editing in this lineage. Some myxomycetes share insertional editing with P. polycephalum, yet lack C--> U conversion, consistent with previous reports of separation of insertional and base conversion editing in P. polycephalum extracts (Visomirski-Robic & Gott, RNA, 1995, 3:821-837). Most remarkably, we detect unique evolutionary histories of the three different types of insertional editing, though these have been indistinguishable in vitro. For example, Clastoderma debaryanum exhibits insertions of Us, but not Cs or dinucleotides.

Full Text

The Full Text of this article is available as a PDF (812.4 KB).

Selected References

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

  1. Alfonzo J. D., Blanc V., Estévez A. M., Rubio M. A., Simpson L. C to U editing of the anticodon of imported mitochondrial tRNA(Trp) allows decoding of the UGA stop codon in Leishmania tarentolae. EMBO J. 1999 Dec 15;18(24):7056–7062. doi: 10.1093/emboj/18.24.7056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baldauf S. L., Doolittle W. F. Origin and evolution of the slime molds (Mycetozoa) Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12007–12012. doi: 10.1073/pnas.94.22.12007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barth C., Greferath U., Kotsifas M., Fisher P. R. Polycistronic transcription and editing of the mitochondrial small subunit (SSU ) ribosomal RNA in Dictyostelium discoideum. Curr Genet. 1999 Aug;36(1-2):55–61. doi: 10.1007/s002940050472. [DOI] [PubMed] [Google Scholar]
  4. Benne R., Van den Burg J., Brakenhoff J. P., Sloof P., Van Boom J. H., Tromp M. C. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986 Sep 12;46(6):819–826. doi: 10.1016/0092-8674(86)90063-2. [DOI] [PubMed] [Google Scholar]
  5. Dorit R. L., Ohara O., Gilbert W. One-sided anchored polymerase chain reaction for amplification and sequencing of complementary DNA. Methods Enzymol. 1993;218:36–47. doi: 10.1016/0076-6879(93)18006-x. [DOI] [PubMed] [Google Scholar]
  6. Gott J. M., Visomirski L. M., Hunter J. L. Substitutional and insertional RNA editing of the cytochrome c oxidase subunit 1 mRNA of Physarum polycephalum. J Biol Chem. 1993 Dec 5;268(34):25483–25486. [PubMed] [Google Scholar]
  7. Gott J. M., Visomirski L. M., Hunter J. L. Substitutional and insertional RNA editing of the cytochrome c oxidase subunit 1 mRNA of Physarum polycephalum. J Biol Chem. 1993 Dec 5;268(34):25483–25486. [PubMed] [Google Scholar]
  8. Hersberger M., Patarroyo-White S., Arnold K. S., Innerarity T. L. Phylogenetic analysis of the apolipoprotein B mRNA-editing region. Evidence for a secondary structure between the mooring sequence and the 3' efficiency element. J Biol Chem. 1999 Dec 3;274(49):34590–34597. doi: 10.1074/jbc.274.49.34590. [DOI] [PubMed] [Google Scholar]
  9. Janke A., Päbo S. Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res. 1993 Apr 11;21(7):1523–1525. doi: 10.1093/nar/21.7.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Katz L. A., Curtis E. A., Pfunder M., Landweber L. F. Characterization of novel sequences from distantly related taxa by walking PCR. Mol Phylogenet Evol. 2000 Feb;14(2):318–321. doi: 10.1006/mpev.1999.0695. [DOI] [PubMed] [Google Scholar]
  11. Landweber L. F., Gilbert W. Phylogenetic analysis of RNA editing: a primitive genetic phenomenon. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):918–921. doi: 10.1073/pnas.91.3.918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Landweber L. F., Gilbert W. RNA editing as a source of genetic variation. Nature. 1993 May 13;363(6425):179–182. doi: 10.1038/363179a0. [DOI] [PubMed] [Google Scholar]
  13. Landweber L. F. The evolution of RNA editing in kinetoplastid protozoa. Biosystems. 1992;28(1-3):41–45. doi: 10.1016/0303-2647(92)90006-k. [DOI] [PubMed] [Google Scholar]
  14. Mahendran R., Spottswood M. S., Ghate A., Ling M. L., Jeng K., Miller D. L. Editing of the mitochondrial small subunit rRNA in Physarum polycephalum. EMBO J. 1994 Jan 1;13(1):232–240. doi: 10.1002/j.1460-2075.1994.tb06253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Malek O., Lättig K., Hiesel R., Brennicke A., Knoop V. RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 1996 Mar 15;15(6):1403–1411. [PMC free article] [PubMed] [Google Scholar]
  16. Martin G., Keller W. Tailing and 3'-end labeling of RNA with yeast poly(A) polymerase and various nucleotides. RNA. 1998 Feb;4(2):226–230. [PMC free article] [PubMed] [Google Scholar]
  17. Maslov D. A., Avila H. A., Lake J. A., Simpson L. Evolution of RNA editing in kinetoplastid protozoa. Nature. 1994 Mar 24;368(6469):345–348. doi: 10.1038/368345a0. [DOI] [PubMed] [Google Scholar]
  18. Miller D., Mahendran R., Spottswood M., Costandy H., Wang S., Ling M. L., Yang N. Insertional editing in mitochondria of Physarum. Semin Cell Biol. 1993 Aug;4(4):261–266. doi: 10.1006/scel.1993.1031. [DOI] [PubMed] [Google Scholar]
  19. Navaratnam N., Fujino T., Bayliss J., Jarmuz A., How A., Richardson N., Somasekaram A., Bhattacharya S., Carter C., Scott J. Escherichia coli cytidine deaminase provides a molecular model for ApoB RNA editing and a mechanism for RNA substrate recognition. J Mol Biol. 1998 Jan 30;275(4):695–714. doi: 10.1006/jmbi.1997.1506. [DOI] [PubMed] [Google Scholar]
  20. Pring D., Brennicke A., Schuster W. RNA editing gives a new meaning to the genetic information in mitochondria and chloroplasts. Plant Mol Biol. 1993 Mar;21(6):1163–1170. doi: 10.1007/BF00023611. [DOI] [PubMed] [Google Scholar]
  21. Schuster W., Combettes B., Flieger K., Brennicke A. A plant mitochondrial gene encodes a protein involved in cytochrome c biogenesis. Mol Gen Genet. 1993 May;239(1-2):49–57. doi: 10.1007/BF00281600. [DOI] [PubMed] [Google Scholar]
  22. Schäfer G., Purschke W., Schmidt C. L. On the origin of respiration: electron transport proteins from archaea to man. FEMS Microbiol Rev. 1996 May;18(2-3):173–188. doi: 10.1111/j.1574-6976.1996.tb00235.x. [DOI] [PubMed] [Google Scholar]
  23. Shields D. C., Wolfe K. H. Accelerated evolution of sites undergoing mRNA editing in plant mitochondria and chloroplasts. Mol Biol Evol. 1997 Mar;14(3):344–349. doi: 10.1093/oxfordjournals.molbev.a025768. [DOI] [PubMed] [Google Scholar]
  24. Visomirski-Robic L. M., Gott J. M. Accurate and efficient insertional RNA editing in isolated Physarum mitochondria. RNA. 1995 Sep;1(7):681–691. [PMC free article] [PubMed] [Google Scholar]
  25. Visomirski-Robic L. M., Gott J. M. Insertional editing in isolated Physarum mitochondria is linked to RNA synthesis. RNA. 1997 Aug;3(8):821–837. [PMC free article] [PubMed] [Google Scholar]
  26. Visomirski-Robic L. M., Gott J. M. Insertional editing in isolated Physarum mitochondria is linked to RNA synthesis. RNA. 1997 Aug;3(8):821–837. [PMC free article] [PubMed] [Google Scholar]
  27. Visomirski-Robic L. M., Gott J. M. Insertional editing of nascent mitochondrial RNAs in Physarum. Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4324–4329. doi: 10.1073/pnas.94.9.4324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wang S. S., Mahendran R., Miller D. L. Editing of cytochrome b mRNA in physarum mitochondria. J Biol Chem. 1999 Jan 29;274(5):2725–2731. doi: 10.1074/jbc.274.5.2725. [DOI] [PubMed] [Google Scholar]

Articles from RNA are provided here courtesy of The RNA Society

RESOURCES