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. 1988 Mar 25;16(6):2705–2715. doi: 10.1093/nar/16.6.2705

Evidence of natural selection to maintain a functional domain outside of the 'core' in a large subclass of group I introns.

R A Collins 1
PMCID: PMC336399  PMID: 2452404

Abstract

Comparison of three closely-related, homologous Group I introns reveals conservation of RNA secondary structure and some primary sequence outside of the characteristic Group I core structure. Further examination of forty Group I introns showed that all can be placed into one of two categories based on the length of the "loop L5" region (subtended by the base-paired sequences P and Q): short (21 to 38 bases) or long (59 to 295 bases). Despite the large variation in size and sequence, all nineteen of the long L5 introns share a common structure whose features include an adenine-rich bulge at a fixed distance from the P-Q pairing. This bulge is flanked by base-paired regions of greater than or equal to 6 base pairs on the core-proximal side and greater than or equal to 3 base pairs on the distal side. In the core-proximal helix there are a large number and high proportion of deviations from the consensus sequence that maintain base-pairing. These naturally-occurring compensatory base substitutions provide compelling phylogenetic support for the existence of this pairing and indicate that the conserved structure has a function in vivo.

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Selected References

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

  1. Anziano P. Q., Hanson D. K., Mahler H. R., Perlman P. S. Functional domains in introns: trans-acting and cis-acting regions of intron 4 of the cob gene. Cell. 1982 Oct;30(3):925–932. doi: 10.1016/0092-8674(82)90297-5. [DOI] [PubMed] [Google Scholar]
  2. Bonitz S. G., Coruzzi G., Thalenfeld B. E., Tzagoloff A., Macino G. Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrme oxidase. J Biol Chem. 1980 Dec 25;255(24):11927–11941. [PubMed] [Google Scholar]
  3. Borst P., Grivell L. A. One gene's intron is another gene's exon. Nature. 1981 Feb 5;289(5797):439–440. doi: 10.1038/289439a0. [DOI] [PubMed] [Google Scholar]
  4. Burke J. M., Belfort M., Cech T. R., Davies R. W., Schweyen R. J., Shub D. A., Szostak J. W., Tabak H. F. Structural conventions for group I introns. Nucleic Acids Res. 1987 Sep 25;15(18):7217–7221. doi: 10.1093/nar/15.18.7217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burke J. M., Breitenberger C., Heckman J. E., Dujon B., RajBhandary U. L. Cytochrome b gene of Neurospora crassa mitochondria. Partial sequence and location of introns at sites different from those in Saccharomyces cerevisiae and Aspergillus nidulans. J Biol Chem. 1984 Jan 10;259(1):504–511. [PubMed] [Google Scholar]
  6. Carey J., Lowary P. T., Uhlenbeck O. C. Interaction of R17 coat protein with synthetic variants of its ribonucleic acid binding site. Biochemistry. 1983 Sep 27;22(20):4723–4730. doi: 10.1021/bi00289a017. [DOI] [PubMed] [Google Scholar]
  7. Cech T. R., Tanner N. K., Tinoco I., Jr, Weir B. R., Zuker M., Perlman P. S. Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3903–3907. doi: 10.1073/pnas.80.13.3903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cech T. R. The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell. 1986 Jan 31;44(2):207–210. doi: 10.1016/0092-8674(86)90751-8. [DOI] [PubMed] [Google Scholar]
  9. Climie S. C., Friesen J. D. Feedback regulation of the rplJL-rpoBC ribosomal protein operon of Escherichia coli requires a region of mRNA secondary structure. J Mol Biol. 1987 Dec 5;198(3):371–381. doi: 10.1016/0022-2836(87)90287-7. [DOI] [PubMed] [Google Scholar]
  10. Collins R. A., Lambowitz A. M. RNA splicing in Neurospora mitochondria. Defective splicing of mitochondrial mRNA precursors in the nuclear mutant cyt18-1. J Mol Biol. 1985 Aug 5;184(3):413–428. doi: 10.1016/0022-2836(85)90291-8. [DOI] [PubMed] [Google Scholar]
  11. Davies R. W., Waring R. B., Ray J. A., Brown T. A., Scazzocchio C. Making ends meet: a model for RNA splicing in fungal mitochondria. Nature. 1982 Dec 23;300(5894):719–724. doi: 10.1038/300719a0. [DOI] [PubMed] [Google Scholar]
  12. De La Salle H., Jacq C., Slonimski P. P. Critical sequences within mitochondrial introns: pleiotropic mRNA maturase and cis-dominant signals of the box intron controlling reductase and oxidase. Cell. 1982 Apr;28(4):721–732. doi: 10.1016/0092-8674(82)90051-4. [DOI] [PubMed] [Google Scholar]
  13. Garriga G., Lambowitz A. M. Protein-dependent splicing of a group I intron in ribonucleoprotein particles and soluble fractions. Cell. 1986 Aug 29;46(5):669–680. doi: 10.1016/0092-8674(86)90342-9. [DOI] [PubMed] [Google Scholar]
  14. Garriga G., Lambowitz A. M. RNA splicing in Neurospora mitochondria. The large rRNA intron contains a noncoded, 5'-terminal guanosine residue. J Biol Chem. 1983 Dec 25;258(24):14745–14748. [PubMed] [Google Scholar]
  15. Garriga G., Lambowitz A. M. RNA splicing in neurospora mitochondria: self-splicing of a mitochondrial intron in vitro. Cell. 1984 Dec;39(3 Pt 2):631–641. doi: 10.1016/0092-8674(84)90470-7. [DOI] [PubMed] [Google Scholar]
  16. Helmer-Citterich M., Morelli G., Macino G. Nucleotide sequence and intron structure of the apocytochrome b gene of Neurospora crassa mitochondria. EMBO J. 1983;2(8):1235–1242. doi: 10.1002/j.1460-2075.1983.tb01575.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hensgens L. A., Bonen L., de Haan M., van der Horst G., Grivell L. A. Two intron sequences in yeast mitochondrial COX1 gene: homology among URF-containing introns and strain-dependent variation in flanking exons. Cell. 1983 Feb;32(2):379–389. doi: 10.1016/0092-8674(83)90457-9. [DOI] [PubMed] [Google Scholar]
  18. Kan N. C., Gall J. G. The intervening sequence of the ribosomal RNA gene is highly conserved between two Tetrahymena species. Nucleic Acids Res. 1982 May 11;10(9):2809–2822. doi: 10.1093/nar/10.9.2809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kreike J., Schulze M., Pillar T., Körte A., Rödel G. Cloning of a nuclear gene MRS1 involved in the excision of a single group I intron (bI3) from the mitochondrial COB transcript in S. cerevisiae. Curr Genet. 1986;11(3):185–191. doi: 10.1007/BF00420605. [DOI] [PubMed] [Google Scholar]
  20. Lang B. F. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe: highly homologous introns are inserted at the same position of the otherwise less conserved cox1 genes in Schizosaccharomyces pombe and Aspergillus nidulans. EMBO J. 1984 Sep;3(9):2129–2136. doi: 10.1002/j.1460-2075.1984.tb02102.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lazowska J., Jacq C., Slonimski P. P. Sequence of introns and flanking exons in wild-type and box3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell. 1980 Nov;22(2 Pt 2):333–348. doi: 10.1016/0092-8674(80)90344-x. [DOI] [PubMed] [Google Scholar]
  22. Mannella C. A., Collins R. A., Green M. R., Lambowitz A. M. Defective splicing of mitochondrial rRNA in cytochrome-deficient nuclear mutants of Neurospora crassa. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2635–2639. doi: 10.1073/pnas.76.6.2635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McGraw P., Tzagoloff A. Assembly of the mitochondrial membrane system. Characterization of a yeast nuclear gene involved in the processing of the cytochrome b pre-mRNA. J Biol Chem. 1983 Aug 10;258(15):9459–9468. [PubMed] [Google Scholar]
  24. Michel F., Cummings D. J. Analysis of class I introns in a mitochondrial plasmid associated with senescence of Podospora anserina reveals extraordinary resemblance to the Tetrahymena ribosomal intron. Curr Genet. 1985;10(1):69–79. doi: 10.1007/BF00418495. [DOI] [PubMed] [Google Scholar]
  25. Michel F., Dujon B. Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J. 1983;2(1):33–38. doi: 10.1002/j.1460-2075.1983.tb01376.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Michel F., Jacquier A., Dujon B. Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure. Biochimie. 1982 Oct;64(10):867–881. doi: 10.1016/s0300-9084(82)80349-0. [DOI] [PubMed] [Google Scholar]
  27. Morelli G., Macino G. Two intervening sequences in the ATPase subunit 6 gene of Neurospora crassa. A short intron (93 base-pairs) and a long intron that is stable after excision. J Mol Biol. 1984 Sep 25;178(3):491–507. doi: 10.1016/0022-2836(84)90235-3. [DOI] [PubMed] [Google Scholar]
  28. Nelson M. A., Macino G. Three class I introns in the ND4L/ND5 transcriptional unit of Neurospora crassa mitochondria. Mol Gen Genet. 1987 Feb;206(2):318–325. doi: 10.1007/BF00333590. [DOI] [PubMed] [Google Scholar]
  29. Nobrega F. G., Tzagoloff A. Assembly of the mitochondrial membrane system. DNA sequence and organization of the cytochrome b gene in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1980 Oct 25;255(20):9828–9837. [PubMed] [Google Scholar]
  30. Noller H. F., Kop J., Wheaton V., Brosius J., Gutell R. R., Kopylov A. M., Dohme F., Herr W., Stahl D. A., Gupta R. Secondary structure model for 23S ribosomal RNA. Nucleic Acids Res. 1981 Nov 25;9(22):6167–6189. doi: 10.1093/nar/9.22.6167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nomiyama H., Sakaki Y., Takagi Y. Nucleotide sequence of a ribosomal RNA gene intron from slime mold Physarum polycephalum. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1376–1380. doi: 10.1073/pnas.78.3.1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pustell J., Kafatos F. C. A convenient and adaptable package of computer programs for DNA and protein sequence management, analysis and homology determination. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):643–655. doi: 10.1093/nar/12.1part2.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Romaniuk P. J., Lowary P., Wu H. N., Stormo G., Uhlenbeck O. C. RNA binding site of R17 coat protein. Biochemistry. 1987 Mar 24;26(6):1563–1568. doi: 10.1021/bi00380a011. [DOI] [PubMed] [Google Scholar]
  34. Trinkl H., Wolf K. The mosaic cox1 gene in the mitochondrial genome of Schizosaccharomyces pombe: minimal structural requirements and evolution of group I introns. Gene. 1986;45(3):289–297. doi: 10.1016/0378-1119(86)90027-2. [DOI] [PubMed] [Google Scholar]
  35. Waring R. B., Brown T. A., Ray J. A., Scazzocchio C., Davies R. W. Three variant introns of the same general class in the mitochondrial gene for cytochrome oxidase subunit 1 in Aspergillus nidulans. EMBO J. 1984 Sep;3(9):2121–2128. doi: 10.1002/j.1460-2075.1984.tb02100.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Waring R. B., Davies R. W. Assessment of a model for intron RNA secondary structure relevant to RNA self-splicing--a review. Gene. 1984 Jun;28(3):277–291. doi: 10.1016/0378-1119(84)90145-8. [DOI] [PubMed] [Google Scholar]
  37. Waring R. B., Davies R. W., Scazzocchio C., Brown T. A. Internal structure of a mitochondrial intron of Aspergillus nidulans. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6332–6336. doi: 10.1073/pnas.79.20.6332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weiss-Brummer B., Rödel G., Schweyen R. J., Kaudewitz F. Expression of the split gene cob in yeast: evidence for a precursor of a "maturase" protein translated from intron 4 and preceding exons. Cell. 1982 Jun;29(2):527–536. doi: 10.1016/0092-8674(82)90169-6. [DOI] [PubMed] [Google Scholar]
  39. Wollenzien P. L., Cantor C. R., Grant D. M., Lambowitz A. M. RNA splicing in neurospora mitochondria: structure of the unspliced 35S precursor ribosomal RNA detected by psoralen cross-linking. Cell. 1983 Feb;32(2):397–407. doi: 10.1016/0092-8674(83)90459-2. [DOI] [PubMed] [Google Scholar]
  40. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]

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