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. 1993 Aug 25;21(17):4073–4078. doi: 10.1093/nar/21.17.4073

Maxicircle DNA and edited mRNA sequences of closely related trypanosome species: implications of kRNA editing for evolution of maxicircle genomes.

L K Read 1, W R Fish 1, A M Muthiani 1, K Stuart 1
PMCID: PMC310006  PMID: 8396763

Abstract

kRNA editing produces functional mRNAs by uridine insertion and deletion. We analyzed portions of the apocytochrome b and NADH dehydrogenase subunits 7 and 8 (ND7 and 8) genes and their edited mRNAs in Trypanosoma congolense and compared these to the corresponding sequences in T.brucei. We find that these genes are highly diverged between the two species, especially in the positions of thymidines and in nucleotide transitions. Editing eliminates differences in encoded uridines producing edited mRNAs that are identical except for the nucleotide substitutions. The resulting predicted proteins are identical since all nucleotide substitutions are silent. A T.congolense minicircle-encoded gRNA which can specify editing of ND8 mRNA was identified. This gRNA can basepair with both T.congolense and T.brucei ND8 mRNA despite nucleotide transitions due to the flexibility of G:U base-pairing. These results illustrate how editing affects the characteristics of maxicircle sequence divergence and allows protein sequence conservation despite a level of DNA sequence divergence which would be predicted to be intolerable in the absence of editing.

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Selected References

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

  1. Abraham J. M., Feagin J. E., Stuart K. Characterization of cytochrome c oxidase III transcripts that are edited only in the 3' region. Cell. 1988 Oct 21;55(2):267–272. doi: 10.1016/0092-8674(88)90049-9. [DOI] [PubMed] [Google Scholar]
  2. Bhat G. J., Koslowsky D. J., Feagin J. E., Smiley B. L., Stuart K. An extensively edited mitochondrial transcript in kinetoplastids encodes a protein homologous to ATPase subunit 6. Cell. 1990 Jun 1;61(5):885–894. doi: 10.1016/0092-8674(90)90199-o. [DOI] [PubMed] [Google Scholar]
  3. Bhat G. J., Lodes M. J., Myler P. J., Stuart K. D. A simple method for cloning blunt ended DNA fragments. Nucleic Acids Res. 1991 Jan 25;19(2):398–398. doi: 10.1093/nar/19.2.398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bienen E. J., Webster P., Fish W. R. Trypanosoma (Nannomonas) congolense: changes in respiratory metabolism during the life cycle. Exp Parasitol. 1991 Nov;73(4):403–412. doi: 10.1016/0014-4894(91)90064-4. [DOI] [PubMed] [Google Scholar]
  5. Blum B., Bakalara N., Simpson L. A model for RNA editing in kinetoplastid mitochondria: "guide" RNA molecules transcribed from maxicircle DNA provide the edited information. Cell. 1990 Jan 26;60(2):189–198. doi: 10.1016/0092-8674(90)90735-w. [DOI] [PubMed] [Google Scholar]
  6. Borst P., Fase-Fowler F., Weijers P. J., Barry J. D., Tetley L., Vickerman K. Kinetoplast DNA from Trypanosoma vivax and T. congolense. Mol Biochem Parasitol. 1985 May;15(2):129–142. doi: 10.1016/0166-6851(85)90114-8. [DOI] [PubMed] [Google Scholar]
  7. Feagin J. E., Abraham J. M., Stuart K. Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell. 1988 May 6;53(3):413–422. doi: 10.1016/0092-8674(88)90161-4. [DOI] [PubMed] [Google Scholar]
  8. Feagin J. E., Jasmer D. P., Stuart K. Apocytochrome b and other mitochondrial DNA sequences are differentially expressed during the life cycle of Trypanosoma brucei. Nucleic Acids Res. 1985 Jun 25;13(12):4577–4596. doi: 10.1093/nar/13.12.4577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Feagin J. E., Jasmer D. P., Stuart K. Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei. Cell. 1987 May 8;49(3):337–345. doi: 10.1016/0092-8674(87)90286-8. [DOI] [PubMed] [Google Scholar]
  10. Feagin J. E. RNA editing in kinetoplastid mitochondria. J Biol Chem. 1990 Nov 15;265(32):19373–19376. [PubMed] [Google Scholar]
  11. Fish W. R., Muriuki C. W., Muthiani A. M., Grab D. J., Lonsdale-Eccles J. D. Disulfide bond involvement in the maintenance of the cryptic nature of the cross-reacting determinant of metacyclic forms of Trypanosoma congolense. Biochemistry. 1989 Jun 27;28(13):5415–5421. doi: 10.1021/bi00439a015. [DOI] [PubMed] [Google Scholar]
  12. Gray M. W. Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol. 1989;5:25–50. doi: 10.1146/annurev.cb.05.110189.000325. [DOI] [PubMed] [Google Scholar]
  13. Jasmer D. P., Stuart K. Sequence organization in African trypanosome minicircles is defined by 18 base pair inverted repeats. Mol Biochem Parasitol. 1986 Mar;18(3):321–331. doi: 10.1016/0166-6851(86)90089-7. [DOI] [PubMed] [Google Scholar]
  14. Koslowsky D. J., Bhat G. J., Perrollaz A. L., Feagin J. E., Stuart K. The MURF3 gene of T. brucei contains multiple domains of extensive editing and is homologous to a subunit of NADH dehydrogenase. Cell. 1990 Sep 7;62(5):901–911. doi: 10.1016/0092-8674(90)90265-g. [DOI] [PubMed] [Google Scholar]
  15. Koslowsky D. J., Riley G. R., Feagin J. E., Stuart K. Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life cycle stages of Trypanosoma brucei. Mol Cell Biol. 1992 May;12(5):2043–2049. doi: 10.1128/mcb.12.5.2043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maslov D. A., Sturm N. R., Niner B. M., Gruszynski E. S., Peris M., Simpson L. An intergenic G-rich region in Leishmania tarentolae kinetoplast maxicircle DNA is a pan-edited cryptogene encoding ribosomal protein S12. Mol Cell Biol. 1992 Jan;12(1):56–67. doi: 10.1128/mcb.12.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nasir A., Cook G. A., Donelson J. E. Sequences of two kinetoplast minicircle DNAs of Trypanosoma (Nannomonas) congolense. Mol Biochem Parasitol. 1987 Jul;24(3):295–300. doi: 10.1016/0166-6851(87)90162-9. [DOI] [PubMed] [Google Scholar]
  18. Pollard V. W., Rohrer S. P., Michelotti E. F., Hancock K., Hajduk S. L. Organization of minicircle genes for guide RNAs in Trypanosoma brucei. Cell. 1990 Nov 16;63(4):783–790. doi: 10.1016/0092-8674(90)90144-4. [DOI] [PubMed] [Google Scholar]
  19. Read L. K., Corell R. A., Stuart K. Chimeric and truncated RNAs in Trypanosoma brucei suggest transesterifications at non-consecutive sites during RNA editing. Nucleic Acids Res. 1992 May 11;20(9):2341–2347. doi: 10.1093/nar/20.9.2341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Read L. K., Myler P. J., Stuart K. Extensive editing of both processed and preprocessed maxicircle CR6 transcripts in Trypanosoma brucei. J Biol Chem. 1992 Jan 15;267(2):1123–1128. [PubMed] [Google Scholar]
  21. Simpson L., Neckelmann N., de la Cruz V. F., Simpson A. M., Feagin J. E., Jasmer D. P., Stuart K. Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. J Biol Chem. 1987 May 5;262(13):6182–6196. [PubMed] [Google Scholar]
  22. Souza A. E., Myler P. J., Stuart K. Maxicircle CR1 transcripts of Trypanosoma brucei are edited and developmentally regulated and encode a putative iron-sulfur protein homologous to an NADH dehydrogenase subunit. Mol Cell Biol. 1992 May;12(5):2100–2107. doi: 10.1128/mcb.12.5.2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stuart K., Feagin J. E. Mitochondrial DNA of kinetoplastids. Int Rev Cytol. 1992;141:65–88. doi: 10.1016/s0074-7696(08)62063-x. [DOI] [PubMed] [Google Scholar]
  24. Stuart K. RNA editing in mitochondrial mRNA of trypanosomatids. Trends Biochem Sci. 1991 Feb;16(2):68–72. doi: 10.1016/0968-0004(91)90027-s. [DOI] [PubMed] [Google Scholar]
  25. Stuart K. RNA editing in trypanosomatid mitochondria. Annu Rev Microbiol. 1991;45:327–344. doi: 10.1146/annurev.mi.45.100191.001551. [DOI] [PubMed] [Google Scholar]
  26. Weiner A. M., Maizels N. RNA editing: guided but not templated? Cell. 1990 Jun 15;61(6):917–920. doi: 10.1016/0092-8674(90)90053-h. [DOI] [PubMed] [Google Scholar]

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