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. 1996 Jun;143(2):777–788. doi: 10.1093/genetics/143.2.777

Mitochondrial Intronic Open Reading Frames in Podospora: Mobility and Consecutive Exonic Sequence Variations

C H Sellem 1, Y d'Aubenton-Carafa 1, M Rossignol 1, L Belcour 1
PMCID: PMC1207336  PMID: 8725226

Abstract

The mitochondrial genome of 23 wild-type strains belonging to three different species of the filamentous fungus Podospora was examined. Among the 15 optional sequences identified are two intronic reading frames, nad1-i4-orf1 and cox1-i7-orf2. We show that the presence of these sequences was strictly correlated with tightly clustered nucleotide substitutions in the adjacent exon. This correlation applies to the presence or absence of closely related open reading frames (ORFs), found at the same genetic locations, in all the Pyrenomycete genera examined. The recent gain of these optional ORFs in the evolution of the genus Podospora probably account for such sequence differences. In the homoplasmic progeny from heteroplasmons constructed between Podospora strains differing by the presence of these optional ORFs, nad1-i4-orf1 and cox1-i7-orf2 appeared highly invasive. Sequence comparisons in the nad1-i4 intron of various strains of the Pyrenomycete family led us to propose a scenario of its evolution that includes several events of loss and gain of intronic ORFs. These results strongly reinforce the idea that group I intronic ORFs are mobile elements and that their transfer, and comcomitant modification of the adjacent exon, could participate in the modular evolution of mitochondrial genomes.

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Selected References

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  1. Bechhofer D. H., Hue K. K., Shub D. A. An intron in the thymidylate synthase gene of Bacillus bacteriophage beta 22: evidence for independent evolution of a gene, its group I intron, and the intron open reading frame. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11669–11673. doi: 10.1073/pnas.91.24.11669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belcour L., Begel O. Mitochondrial genes in Podospora anserina: recombination and linkage. Mol Gen Genet. 1977 May 20;153(1):11–21. doi: 10.1007/BF01035991. [DOI] [PubMed] [Google Scholar]
  3. Bell-Pedersen D., Quirk S., Clyman J., Belfort M. Intron mobility in phage T4 is dependent upon a distinctive class of endonucleases and independent of DNA sequences encoding the intron core: mechanistic and evolutionary implications. Nucleic Acids Res. 1990 Jul 11;18(13):3763–3770. doi: 10.1093/nar/18.13.3763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown T. A., Davies R. W., Ray J. A., Waring R. B., Scazzocchio C. The mitochondnal genome of Aspergillus nidulans contains reading frames homologous to the human URFs 1 and 4. EMBO J. 1983;2(3):427–435. doi: 10.1002/j.1460-2075.1983.tb01440.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burger G., Scriven C., Machleidt W., Werner S. Subunit 1 of cytochrome oxidase from Neurospora crassa: nucleotide sequence of the coding gene and partial amino acid sequence of the protein. EMBO J. 1982;1(11):1385–1391. doi: 10.1002/j.1460-2075.1982.tb01327.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burger G., Werner S. The mitochondrial URF1 gene in Neurospora crassa has an intron that contains a novel type of URF. J Mol Biol. 1985 Nov 20;186(2):231–242. doi: 10.1016/0022-2836(85)90100-7. [DOI] [PubMed] [Google Scholar]
  7. Colleaux L., Michel-Wolwertz M. R., Matagne R. F., Dujon B. The apocytochrome b gene of Chlamydomonas smithii contains a mobile intron related to both Saccharomyces and Neurospora introns. Mol Gen Genet. 1990 Sep;223(2):288–296. doi: 10.1007/BF00265065. [DOI] [PubMed] [Google Scholar]
  8. Colleaux L., d'Auriol L., Betermier M., Cottarel G., Jacquier A., Galibert F., Dujon B. Universal code equivalent of a yeast mitochondrial intron reading frame is expressed into E. coli as a specific double strand endonuclease. Cell. 1986 Feb 28;44(4):521–533. doi: 10.1016/0092-8674(86)90262-x. [DOI] [PubMed] [Google Scholar]
  9. Cooper A. A., Stevens T. H. Protein splicing: self-splicing of genetically mobile elements at the protein level. Trends Biochem Sci. 1995 Sep;20(9):351–356. doi: 10.1016/s0968-0004(00)89075-1. [DOI] [PubMed] [Google Scholar]
  10. Cummings D. J., Domenico J. M. Sequence analysis of mitochondrial DNA from Podospora anserina. Pervasiveness of a class I intron in three separate genes. J Mol Biol. 1988 Dec 20;204(4):815–839. doi: 10.1016/0022-2836(88)90044-7. [DOI] [PubMed] [Google Scholar]
  11. Cummings D. J., McNally K. L., Domenico J. M., Matsuura E. T. The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr Genet. 1990 May;17(5):375–402. doi: 10.1007/BF00334517. [DOI] [PubMed] [Google Scholar]
  12. Cummings D. J., Michel F., McNally K. L. DNA sequence analysis of the 24.5 kilobase pair cytochrome oxidase subunit I mitochondrial gene from Podospora anserina: a gene with sixteen introns. Curr Genet. 1989 Dec;16(5-6):381–406. doi: 10.1007/BF00340719. [DOI] [PubMed] [Google Scholar]
  13. Dalgaard J. Z., Garrett R. A., Belfort M. A site-specific endonuclease encoded by a typical archaeal intron. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5414–5417. doi: 10.1073/pnas.90.12.5414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. De Jonckheere J. F., Brown S. Loss of the ORF in the SSUrDNA group I intron of one Naegleria lineage. Nucleic Acids Res. 1994 Sep 25;22(19):3925–3927. doi: 10.1093/nar/22.19.3925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Field D. J., Sommerfield A., Saville B. J., Collins R. A. A group II intron in the Neurospora mitochondrial coI gene: nucleotide sequence and implications for splicing and molecular evolution. Nucleic Acids Res. 1989 Nov 25;17(22):9087–9099. doi: 10.1093/nar/17.22.9087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gimble F. S., Thorner J. Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature. 1992 May 28;357(6376):301–306. doi: 10.1038/357301a0. [DOI] [PubMed] [Google Scholar]
  17. Hawse A., Collins R. A., Nargang F. E. Behavior of the [mi-3] mutation and conversion of polymorphic mtDNA markers in heterokaryons of Neurospora crassa. Genetics. 1990 Sep;126(1):63–72. doi: 10.1093/genetics/126.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Jacquier A., Dujon B. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell. 1985 Jun;41(2):383–394. doi: 10.1016/s0092-8674(85)80011-8. [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. Lecellier G., Silar P. Rapid methods for nucleic acids extraction from Petri dish-grown mycelia. Curr Genet. 1994 Feb;25(2):122–123. doi: 10.1007/BF00309536. [DOI] [PubMed] [Google Scholar]
  22. Levra-Juillet E., Boulet A., Séraphin B., Simon M., Faye G. Mitochondrial introns aI1 and/or aI2 are needed for the in vivo deletion of intervening sequences. Mol Gen Genet. 1989 May;217(1):168–171. doi: 10.1007/BF00330957. [DOI] [PubMed] [Google Scholar]
  23. Loizos N., Tillier E. R., Belfort M. Evolution of mobile group I introns: recognition of intron sequences by an intron-encoded endonuclease. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11983–11987. doi: 10.1073/pnas.91.25.11983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Macreadie I. G., Scott R. M., Zinn A. R., Butow R. A. Transposition of an intron in yeast mitochondria requires a protein encoded by that intron. Cell. 1985 Jun;41(2):395–402. doi: 10.1016/s0092-8674(85)80012-x. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Mota E. M., Collins R. A. Independent evolution of structural and coding regions in a Neurospora mitochondrial intron. Nature. 1988 Apr 14;332(6165):654–656. doi: 10.1038/332654a0. [DOI] [PubMed] [Google Scholar]
  28. Paquin B., Laforest M. J., Lang B. F. Interspecific transfer of mitochondrial genes in fungi and creation of a homologous hybrid gene. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11807–11810. doi: 10.1073/pnas.91.25.11807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pel H. J., Grivell L. A. The biology of yeast mitochondrial introns. Mol Biol Rep. 1993 Jun;18(1):1–13. doi: 10.1007/BF01006890. [DOI] [PubMed] [Google Scholar]
  30. Sellem C. H., Belcour L. The in vivo use of alternate 3'-splice sites in group I introns. Nucleic Acids Res. 1994 Apr 11;22(7):1135–1137. doi: 10.1093/nar/22.7.1135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sharma M., Ellis R. L., Hinton D. M. Identification of a family of bacteriophage T4 genes encoding proteins similar to those present in group I introns of fungi and phage. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6658–6662. doi: 10.1073/pnas.89.14.6658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shub D. A., Gott J. M., Xu M. Q., Lang B. F., Michel F., Tomaschewski J., Pedersen-Lane J., Belfort M. Structural conservation among three homologous introns of bacteriophage T4 and the group I introns of eukaryotes. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1151–1155. doi: 10.1073/pnas.85.4.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Séraphin B., Boulet A., Simon M., Faye G. Construction of a yeast strain devoid of mitochondrial introns and its use to screen nuclear genes involved in mitochondrial splicing. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6810–6814. doi: 10.1073/pnas.84.19.6810. [DOI] [PMC free article] [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]

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