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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Feb;85(4):1151–1155. doi: 10.1073/pnas.85.4.1151

Structural conservation among three homologous introns of bacteriophage T4 and the group I introns of eukaryotes.

D A Shub 1, J M Gott 1, M Q Xu 1, B F Lang 1, F Michel 1, J Tomaschewski 1, J Pedersen-Lane 1, M Belfort 1
PMCID: PMC279724  PMID: 3422485

Abstract

Three group I introns of bacteriophage T4 have been compared with respect to their sequence and structural properties. The introns include the td intervening sequence, as well as the two newly described introns in the nrdB and sunY genes of T4. The T4 introns are very closely related, containing phylogenetically conserved sequence elements that allow them to be folded into a core structure that is characteristic of eukaryotic group IA introns. Similarities extend outward to the exon sequences surrounding the three introns. All three introns contain open reading frames (ORFs). Although the intron ORFs are not homologous and occur at different positions, all three ORFs are looped-out of the structure models, with only the 3' ends of each of the ORFs extending into the secondary structure. This arrangement invites interesting speculations on the regulation of splicing by translation. The high degree of similarity between the T4 introns and the eukaryotic group I introns must reflect a common ancestry, resulting either from vertical acquisition of a primordial RNA element or from horizontal transfer.

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Selected References

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  1. Berg J. M. Potential metal-binding domains in nucleic acid binding proteins. Science. 1986 Apr 25;232(4749):485–487. doi: 10.1126/science.2421409. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Carlson J., Fuchs J. A., Messing J. Primary structure of the Escherichia coli ribonucleoside diphosphate reductase operon. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4294–4297. doi: 10.1073/pnas.81.14.4294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Chu F. K., Maley G. F., Maley F., Belfort M. Intervening sequence in the thymidylate synthase gene of bacteriophage T4. Proc Natl Acad Sci U S A. 1984 May;81(10):3049–3053. doi: 10.1073/pnas.81.10.3049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chu F. K., Maley G. F., Maley F. Mechanism and requirements of in vitro RNA splicing of the primary transcript from the T4 bacteriophage thymidylate synthase gene. Biochemistry. 1987 Jun 2;26(11):3050–3057. doi: 10.1021/bi00385a016. [DOI] [PubMed] [Google Scholar]
  8. Chu F. K., Maley G. F., West D. K., Belfort M., Maley F. Characterization of the intron in the phage T4 thymidylate synthase gene and evidence for its self-excision from the primary transcript. Cell. 1986 Apr 25;45(2):157–166. doi: 10.1016/0092-8674(86)90379-x. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Ehrenman K., Pedersen-Lane J., West D., Herman R., Maley F., Belfort M. Processing of phage T4 td-encoded RNA is analogous to the eukaryotic group I splicing pathway. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5875–5879. doi: 10.1073/pnas.83.16.5875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gott J. M., Shub D. A., Belfort M. Multiple self-splicing introns in bacteriophage T4: evidence from autocatalytic GTP labeling of RNA in vitro. Cell. 1986 Oct 10;47(1):81–87. doi: 10.1016/0092-8674(86)90368-5. [DOI] [PubMed] [Google Scholar]
  12. Hall D. H., Povinelli C. M., Ehrenman K., Pedersen-Lane J., Chu F., Belfort M. Two domains for splicing in the intron of the phage T4 thymidylate synthase (td) gene established by nondirected mutagenesis. Cell. 1987 Jan 16;48(1):63–71. doi: 10.1016/0092-8674(87)90356-4. [DOI] [PubMed] [Google Scholar]
  13. Kassavetis G. A., Zentner P. G., Geiduschek E. P. Transcription at bacteriophage T4 variant late promoters. An application of a newly devised promoter-mapping method involving RNA chain retraction. J Biol Chem. 1986 Oct 25;261(30):14256–14265. [PubMed] [Google Scholar]
  14. 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]
  15. Macdonald P. M., Kutter E., Mosig G. Regulation of a bacteriophage T4 late gene, soc, which maps in an early region. Genetics. 1984 Jan;106(1):17–27. doi: 10.1093/genetics/106.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McPheeters D. S., Christensen A., Young E. T., Stormo G., Gold L. Translational regulation of expression of the bacteriophage T4 lysozyme gene. Nucleic Acids Res. 1986 Jul 25;14(14):5813–5826. doi: 10.1093/nar/14.14.5813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Michel F., Dujon B. Genetic exchanges between bacteriophage T4 and filamentous fungi? Cell. 1986 Aug 1;46(3):323–323. doi: 10.1016/0092-8674(86)90651-3. [DOI] [PubMed] [Google Scholar]
  20. Pedersen-Lane J., Belfort M. Variable occurrence of the nrdB intron in the T-even phages suggests intron mobility. Science. 1987 Jul 10;237(4811):182–184. doi: 10.1126/science.3037701. [DOI] [PubMed] [Google Scholar]
  21. Rochaix J. D., Rahire M., Michel F. The chloroplast ribosomal intron of Chlamydomonas reinhardii codes for a polypeptide related to mitochondrial maturases. Nucleic Acids Res. 1985 Feb 11;13(3):975–984. doi: 10.1093/nar/13.3.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sjöberg B. M., Hahne S., Mathews C. Z., Mathews C. K., Rand K. N., Gait M. J. The bacteriophage T4 gene for the small subunit of ribonucleotide reductase contains an intron. EMBO J. 1986 Aug;5(8):2031–2036. doi: 10.1002/j.1460-2075.1986.tb04460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Standart N. M., Bray S. J., George E. L., Hunt T., Ruderman J. V. The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs. J Cell Biol. 1985 Jun;100(6):1968–1976. doi: 10.1083/jcb.100.6.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thelander L., Berg P. Isolation and characterization of expressible cDNA clones encoding the M1 and M2 subunits of mouse ribonucleotide reductase. Mol Cell Biol. 1986 Oct;6(10):3433–3442. doi: 10.1128/mcb.6.10.3433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tomaschewski J., Rüger W. Nucleotide sequence and primary structures of gene products coded for by the T4 genome between map positions 48.266 kb and 39.166 kb. Nucleic Acids Res. 1987 Apr 24;15(8):3632–3633. doi: 10.1093/nar/15.8.3632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]

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