Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1985 Jan;4(1):197–204. doi: 10.1002/j.1460-2075.1985.tb02336.x

RNA processing in Neurospora crassa mitochondria: transfer RNAs punctuate a large precursor transcript.

G Burger, M Helmer Citterich, M A Nelson, S Werner, G Macino
PMCID: PMC554170  PMID: 3160579

Abstract

The pattern of transcripts arising from a large contiguous portion of the Neurospora crassa mitochondrial genome and the processing of these transcripts have been investigated. Evidence is presented for the transcription of a single, at least 12.5 kb, precursor RNA that contains sequences corresponding to the apocytochrome b (cob), tRNACys, cytochrome oxidase subunit 1 (CO I), tRNAArg and unidentified reading frame (URF) 1 genes. The two tRNA sequences serve as punctuation signals for the cleavage of this large transcript. Processing at the tRNACys and tRNAArg sequences directly generates the proposed CO I mRNA, as well as the mature 3' end of the cob transcripts. Moreover, three other sites have been identified that are specifically involved in further 5' end processing events. One of the two 5' end processing sites of the cob transcript shares homology with the 5' end processing sites of the mitochondrial 19S and 25S rRNA precursors. PstI palindromes do not act as processing signals because six of these palindromic sequences are present in the cob and CO I mRNAs.

Full text

PDF
197

Images in this article

201Fig. 4.
on p.201
202Fig. 5.
on p.202
203Fig. 6.
on p.203

Selected References

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

  1. Akins R. A., Lambowitz A. M. The [poky] mutant of Neurospora contains a 4-base-pair deletion at the 5' end of the mitochondrial small rRNA. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3791–3795. doi: 10.1073/pnas.81.12.3791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  4. Berlani R. E., Pentella C., Macino G., Tzagoloff A. Assembly of the mitochondrial membrane system: isolation of mitochondrial transfer ribonucleic acid mutants and characterization of transfer ribonucleic acid genes of Saccharomyces cerevisiae. J Bacteriol. 1980 Mar;141(3):1086–1097. doi: 10.1128/jb.141.3.1086-1097.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Browning K. S., RajBhandary U. L. Cytochrome oxidase subunit III gene in Neurospora crassa mitochondria. Location and sequence. J Biol Chem. 1982 May 10;257(9):5253–5256. [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Carmichael G. G., McMaster G. K. The analysis of nucleic acids in gels using glyoxal and acridine orange. Methods Enzymol. 1980;65(1):380–391. doi: 10.1016/s0076-6879(80)65049-6. [DOI] [PubMed] [Google Scholar]
  10. Chang D. D., Clayton D. A. Precise identification of individual promoters for transcription of each strand of human mitochondrial DNA. Cell. 1984 Mar;36(3):635–643. doi: 10.1016/0092-8674(84)90343-x. [DOI] [PubMed] [Google Scholar]
  11. Collins R. A., Lambowitz A. M. Structural variations and optional introns in the mitochondrial DNAs of Neurospora strains isolated from nature. Plasmid. 1983 Jan;9(1):53–70. doi: 10.1016/0147-619x(83)90031-8. [DOI] [PubMed] [Google Scholar]
  12. Friedman E. Y., Rosbash M. The syntheiss of high yields of full-length reverse transcripts of globin mRNA. Nucleic Acids Res. 1977 Oct;4(10):3455–3471. doi: 10.1093/nar/4.10.3455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garriga G., Bertrand H., Lambowitz A. M. RNA splicing in Neurospora mitochondria: nuclear mutants defective in both splicing and 3' end synthesis of the large rRNA. Cell. 1984 Mar;36(3):623–634. doi: 10.1016/0092-8674(84)90342-8. [DOI] [PubMed] [Google Scholar]
  14. Green M. R., Grimm M. F., Goewert R. R., Collins R. A., Cole M. D., Lambowitz A. M., Heckman J. E., Yin S., RajBhandary U. L. Transcripts and processing patterns for the ribosomal RNA and transfer RNA region of Neurospora crassa mitochondrial DNA. J Biol Chem. 1981 Feb 25;256(4):2027–2034. [PubMed] [Google Scholar]
  15. 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]
  16. Köchel H. G., Lazarus C. M., Basak N., Küntzel H. Mitochondrial tRNA gene clusters in Aspergillus nidulans: organization and nucleotide sequence. Cell. 1981 Feb;23(2):625–633. doi: 10.1016/0092-8674(81)90158-6. [DOI] [PubMed] [Google Scholar]
  17. Locker J. Analytical and preparative electrophoresis of RNA in agarose-urea. Anal Biochem. 1979 Oct 1;98(2):358–367. doi: 10.1016/0003-2697(79)90154-4. [DOI] [PubMed] [Google Scholar]
  18. Macino G., Morelli G. Cytochrome oxidase subunit 2 gene in Neurospora crassa mitochondria. J Biol Chem. 1983 Nov 10;258(21):13230–13235. [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  20. Montoya J., Gaines G. L., Attardi G. The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell. 1983 Aug;34(1):151–159. doi: 10.1016/0092-8674(83)90145-9. [DOI] [PubMed] [Google Scholar]
  21. Ojala D., Montoya J., Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981 Apr 9;290(5806):470–474. doi: 10.1038/290470a0. [DOI] [PubMed] [Google Scholar]
  22. Osinga K. A., De Haan M., Christianson T., Tabak H. F. A nonanucleotide sequence involved in promotion of ribosomal RNA synthesis and RNA priming of DNA replication in yeast mitochondria. Nucleic Acids Res. 1982 Dec 20;10(24):7993–8006. doi: 10.1093/nar/10.24.7993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Osinga K. A., De Vries E., Van der Horst G., Tabak H. F. Processing of yeast mitochondrial messenger RNAs at a conserved dodecamer sequence. EMBO J. 1984 Apr;3(4):829–834. doi: 10.1002/j.1460-2075.1984.tb01892.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Terpstra P., Holtrop M., Kroon A. M. A complete cleavage map of Neurospora crassa mtDNA obtained with endonucleases Eco RI and Bam HI. Biochim Biophys Acta. 1977 Apr 19;475(4):571–588. doi: 10.1016/0005-2787(77)90318-5. [DOI] [PubMed] [Google Scholar]
  25. Thalenfeld B. E., Bonitz S. G., Nobrega F. G., Macino G., Tzagoloff A. oli1 Transcripts in wild type and in a cytoplasmic "petite" mutant of yeast. J Biol Chem. 1983 Dec 10;258(23):14065–14068. [PubMed] [Google Scholar]
  26. Tu C. P., Cohen S. N. 3'-end labeling of DNA with [alpha-32P]cordycepin-5'-triphosphate. Gene. 1980 Jul;10(2):177–183. doi: 10.1016/0378-1119(80)90135-3. [DOI] [PubMed] [Google Scholar]
  27. Yin S., Heckman J., RajBhandary U. L. Highly conserved GC-rich palindromic DNA sequences flank tRNA genes in Neurospora crassa mitochondria. Cell. 1981 Nov;26(3 Pt 1):325–332. doi: 10.1016/0092-8674(81)90201-4. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES