Splicing Defective Mutants of the COXI Gene of Yeast Mitochondrial DNA: Initial Definition of the Maturase Domain of the Group II Intron AI2

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 1994 Jun 11

PMID 8029012

Citations 32

Authors

J V Moran

K L Mecklenburg

P Sass

S M Belcher

D Mahnke

A Lewin

P PERLMAN

Affiliations

Soon will be listed here.

Abstract

Six mutations blocking the function of a seven intron form of the mitochondrial gene encoding subunit I of cytochrome c oxidase (COXI) and mapping upstream of exon 3 were isolated and characterized. A cis-dominant mutant of the group IIA intron 1 defines a helical portion of the C1 substructure of domain 1 as essential for splicing. A trans-recessive mutant confirms that the intron 1 reading frame encodes a maturase function. A cis-dominant mutant in exon 2 was found to have no effect on the splicing of intron 1 or 2. A trans-recessive mutant, located in the group IIA intron 2, demonstrates for the first time that intron 2 encodes a maturase. A genetic dissection of the five missense mutations present in the intron 2 reading frame of that strain demonstrates that the maturase defect results from one or both of the missense mutations in a newly-recognized conserved sequence called domain X.

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References

Perlman P . Genetic analysis of RNA splicing in yeast mitochondria. Methods Enzymol. 1990; 181:539-58. DOI: 10.1016/0076-6879(90)81150-s. View

Halbreich A, Pajot P, Foucher M, Grandchamp C, SLONIMSKI P . A pathway of cytochrome b mRNA processing in yeast mitochondria: specific splicing steps and an intron-derived circular DNA. Cell. 1980; 19(2):321-9. DOI: 10.1016/0092-8674(80)90506-1. View

Bergantino E, Carignani G . Antibodies against a fused gene product identify the protein encoded by a group II yeast mitochondrial intron. Mol Gen Genet. 1990; 223(2):249-57. DOI: 10.1007/BF00265061. View

Anziano P, Butow R . Splicing-defective mutants of the yeast mitochondrial COXI gene can be corrected by transformation with a hybrid maturase gene. Proc Natl Acad Sci U S A. 1991; 88(13):5592-6. PMC: 51923. DOI: 10.1073/pnas.88.13.5592. View

Skelly P, Hardy C, Clark-Walker G . A mobile group II intron of a naturally occurring rearranged mitochondrial genome in Kluyveromyces lactis. Curr Genet. 1991; 20(1-2):115-20. DOI: 10.1007/BF00312773. View

Alexander N, Periman P, Hanson D, Mahler H . Mosaic organization of a mitochondrial gene: evidence from double mutants in the cytochrome b region of Saccharomyces cerevisiae. Cell. 1980; 20(1):199-206. DOI: 10.1016/0092-8674(80)90247-0. View

Macino G, Tzagoloff A . Assembly of the mitochondrial membrane system: sequence analysis of a yeast mitochondrial ATPase gene containing the oli-2 and oli-4 loci. Cell. 1980; 20(2):507-17. DOI: 10.1016/0092-8674(80)90637-6. View

Bonitz S, Coruzzi G, Thalenfeld B, 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; 255(24):11927-41. View

Lazowska J, Jacq C, SLONIMSKI 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; 22(2 Pt 2):333-48. DOI: 10.1016/0092-8674(80)90344-x. View

10.

Schmelzer C, Haid A, Grosch G, Schweyen R, Kaudewitz F . Pathways of transcript splicing in yeast mitochondria. Mutations in intervening sequences of the split gene COB reveal a requirement for intervening sequence-encoded products. J Biol Chem. 1981; 256(14):7610-9. View

11.

Hanson D, Lamb M, Mahler H, Perlman P . Evidence for translated intervening sequences in the mitochondrial genome of Saccharomyces cerevisiae. J Biol Chem. 1982; 257(6):3218-24. View

12.

de la Salle H, Jacq C, SLONIMSKI P . Critical sequences within mitochondrial introns: pleiotropic mRNA maturase and cis-dominant signals of the box intron controlling reductase and oxidase. Cell. 1982; 28(4):721-32. DOI: 10.1016/0092-8674(82)90051-4. View

13.

Lamb M, Anziano P, Glaus K, Hanson D, Klapper H, Perlman P . Functional domains in introns. RNA processing intermediates in cis- and trans-acting mutants in the penultimate intron of the mitochondrial gene for cytochrome b. J Biol Chem. 1983; 258(3):1991-9. View

14.

Hensgens L, Arnberg A, Roosendaal E, Van Der Horst G, van der Veen R, van Ommen G . Variation, transcription and circular RNAs of the mitochondrial gene for subunit I of cytochrome c oxidase. J Mol Biol. 1983; 164(1):35-58. DOI: 10.1016/0022-2836(83)90086-4. View

15.

Carignani G, Groudinsky O, Frezza D, Schiavon E, Bergantino E, SLONIMSKI P . An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit I of cytochrome oxidase in S. cerevisiae. Cell. 1983; 35(3 Pt 2):733-42. DOI: 10.1016/0092-8674(83)90106-x. View

16.

Perlman P, Mahler H . Genetics and biogenesis of cytochrome b. Methods Enzymol. 1983; 97:374-95. DOI: 10.1016/0076-6879(83)97150-1. View

17.

Michel F, Lang B . Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature. 1985; 316(6029):641-3. DOI: 10.1038/316641a0. View

18.

Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162(1):156-9. DOI: 10.1006/abio.1987.9999. View

19.

Carignani G, Netter P, Bergantino E, Robineau S . Expression of the mitochondrial split gene coding for cytochrome oxidase subunit I in S. cerevisiae: RNA splicing pathway. Curr Genet. 1986; 11(1):55-63. DOI: 10.1007/BF00389426. View

20.

McClure M . Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol. 1991; 8(6):835-56. DOI: 10.1093/oxfordjournals.molbev.a040686. View