Abstract
Relatively little is known about the mechanisms that govern the expression of plant mitochondrial genomes. We have addressed this problem by analyzing the transcriptional activity of different regions of the maize mitochondrial genome using both in vivo and isolated mitochondrial pulse-labeling systems. The regions examined included the protein genes atpA, atp6, and coxII, the 26S, 18S, and 5S rRNA genes, and sequences surrounding the rRNA genes. The rRNAs were found to be transcribed at rates fivefold to 10-fold higher than the protein genes. These rate differences are comparable with the differences in abundance of these species in the total or steady-state RNA population. Pulse-labeled RNA unexpectedly detected transcription of all regions examined, including approximately 21 kilobases of presumed noncoding sequences flanking the rRNA genes for which stable transcripts were not detected. The results obtained with RNA labeled for short pulses in vivo and in isolated mitochondria were similar, suggesting that isolated mitochondria provide a faithful run-on transcription assay. Our results indicate that the absence in total RNA of transcripts homologous to a given region of maize mitochondrial DNA does not necessarily exclude transcriptional activity of that region and that both transcriptional and post-transcriptional processes play important roles in maize mitochondrial genome expression.
Full Text
The Full Text of this article is available as a PDF (2.1 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
- Bland M. M., Levings C. S., 3rd, Matzinger D. F. The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet. 1986 Jul;204(1):8–16. doi: 10.1007/BF00330180. [DOI] [PubMed] [Google Scholar]
- Boerner P., Mason T. L., Fox T. D. Synthesis and processing of ribosomal RNA in isolated yeast mitochondria. Nucleic Acids Res. 1981 Dec 11;9(23):6379–6390. doi: 10.1093/nar/9.23.6379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braun C. J., Levings C. S. Nucleotide Sequence of the F(1)-ATPase alpha Subunit Gene from Maize Mitochondria. Plant Physiol. 1985 Oct;79(2):571–577. doi: 10.1104/pp.79.2.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chao S., Sederoff R. R., Levings C. S. Partial Sequence Analysis of the 5S to 18S rRNA Gene Region of the Maize Mitochondrial Genome. Plant Physiol. 1983 Jan;71(1):190–193. doi: 10.1104/pp.71.1.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chao S., Sederoff R., Levings C. S., 3rd Nucleotide sequence and evolution of the 18S ribosomal RNA gene in maize mitochondria. Nucleic Acids Res. 1984 Aug 24;12(16):6629–6644. doi: 10.1093/nar/12.16.6629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christianson T., Rabinowitz M. Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase. J Biol Chem. 1983 Nov 25;258(22):14025–14033. [PubMed] [Google Scholar]
- Clayton D. A. Transcription of the mammalian mitochondrial genome. Annu Rev Biochem. 1984;53:573–594. doi: 10.1146/annurev.bi.53.070184.003041. [DOI] [PubMed] [Google Scholar]
- Dale R. M., Mendu N., Ginsburg H., Kridl J. C. Sequence analysis of the maize mitochondrial 26 S rRNA gene and flanking regions. Plasmid. 1984 Mar;11(2):141–150. doi: 10.1016/0147-619x(84)90019-2. [DOI] [PubMed] [Google Scholar]
- Dewey R. E., Levings C. S., 3rd, Timothy D. H. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell. 1986 Feb 14;44(3):439–449. doi: 10.1016/0092-8674(86)90465-4. [DOI] [PubMed] [Google Scholar]
- Dewey R. E., Levings C. S., Timothy D. H. Nucleotide sequence of ATPase subunit 6 gene of maize mitochondria. Plant Physiol. 1985 Nov;79(3):914–919. doi: 10.1104/pp.79.3.914. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finnegan P. M., Brown G. G. Autonomously replicating RNA in mitochondria of maize plants with S-type cytoplasm. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5175–5179. doi: 10.1073/pnas.83.14.5175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finnegan P. M., Brown G. G. In organello transcription in maize mitochondria and its sensitivity to inhibitors of RNA synthesis. Plant Physiol. 1987 Sep;85(1):304–309. doi: 10.1104/pp.85.1.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaines G., Attardi G. Highly efficient RNA-synthesizing system that uses isolated human mitochondria: new initiation events and in vivo-like processing patterns. Mol Cell Biol. 1984 Aug;4(8):1605–1617. doi: 10.1128/mcb.4.8.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gelfand R., Attardi G. Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: the mature ribosomal and messenger ribonucleic acid species are metabolically unstable. Mol Cell Biol. 1981 Jun;1(6):497–511. doi: 10.1128/mcb.1.6.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gruissem W. Chloroplast gene expression: how plants turn their plastids on. Cell. 1989 Jan 27;56(2):161–170. doi: 10.1016/0092-8674(89)90889-1. [DOI] [PubMed] [Google Scholar]
- Iams K. P., Sinclair J. H. Mapping the mitochondrial DNA of Zea mays: Ribosomal gene localization. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5926–5929. doi: 10.1073/pnas.79.19.5926. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isaac P. G., Brennicke A., Dunbar S. M., Leaver C. J. The mitochondrial genome of fertile maize (Zea mays L.) contains two copies of the gene encoding the alpha-subunit of the F1-ATPase. Curr Genet. 1985;10(4):321–328. doi: 10.1007/BF00365628. [DOI] [PubMed] [Google Scholar]
- Levings C. S., 3rd, Brown G. G. Molecular biology of plant mitochondria. Cell. 1989 Jan 27;56(2):171–179. doi: 10.1016/0092-8674(89)90890-8. [DOI] [PubMed] [Google Scholar]
- Makaroff C. A., Palmer J. D. Extensive mitochondrial specific transcription of the Brassica campestris mitochondrial genome. Nucleic Acids Res. 1987 Jul 10;15(13):5141–5156. doi: 10.1093/nar/15.13.5141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marechal L., Runeberg-Roos P., Grienenberger J. M., Colin J., Weil J. H., Lejeune B., Quetier F., Lonsdale D. M. Homology in the region containing a tRNA(Trp) gene and a (complete or partial) tRNA(Pro) gene in wheat mitochondrial and chloroplast genomes. Curr Genet. 1987;12(2):91–98. doi: 10.1007/BF00434662. [DOI] [PubMed] [Google Scholar]
- Mueller D. M., Getz G. S. Transcriptional regulation of the mitochondrial genome of yeast Saccharomyces cerevisiae. J Biol Chem. 1986 Sep 5;261(25):11756–11764. [PubMed] [Google Scholar]
- Mulligan R. M., Maloney A. P., Walbot V. RNA processing and multiple transcription initiation sites result in transcript size heterogeneity in maize mitochondria. Mol Gen Genet. 1988 Mar;211(3):373–380. doi: 10.1007/BF00425688. [DOI] [PubMed] [Google Scholar]
- Stern D. B., Newton K. J. Mitochondrial gene expression in Cucurbitaceae: conserved and variable features. Curr Genet. 1985;9(5):395–404. doi: 10.1007/BF00421611. [DOI] [PubMed] [Google Scholar]
- Wettstein-Edwards J., Ticho B. S., Martin N. C., Najarian D., Getz G. S. In vitro transcription and promoter strength analysis of five mitochondrial tRNA promoters in yeast. J Biol Chem. 1986 Feb 25;261(6):2905–2911. [PubMed] [Google Scholar]
- Wintz H., Grienenberger J. M., Weil J. H., Lonsdale D. M. Location and nucleotide sequence of two tRNA genes and a tRNA pseudo-gene in the maize mitochondrial genome: evidence for the transcription of a chloroplast gene in mitochondria. Curr Genet. 1988 Mar;13(3):247–254. doi: 10.1007/BF00387771. [DOI] [PubMed] [Google Scholar]
- Wissinger B., Hiesel R., Schuster W., Brennicke A. The NADH-dehydrogenase subunit 5 gene in Oenothera mitochondria contains two introns and is co-transcribed with the 5 S rRNA gene. Mol Gen Genet. 1988 Apr;212(1):56–65. doi: 10.1007/BF00322444. [DOI] [PubMed] [Google Scholar]
- Young E. G., Hanson M. R. A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell. 1987 Jul 3;50(1):41–49. doi: 10.1016/0092-8674(87)90660-x. [DOI] [PubMed] [Google Scholar]