Abstract
Each mitochondrion possesses a genome that encodes some of its own components. The nucleus encodes most of the mitochondrial proteins, including the polymerases and factors that regulate the expression of mitochondrial genes. Little is known about the number or location of these nuclear factors. B-A translocations were used to create dosage series for 14 different chromosome arms in maize plants with normal cytoplasm. The presence of one or more regulatory factors on a chromosome arm was indicated when variation of its dosage resulted in the alteration in the amount of a mitochondrial transcript. We used quantitative Northern analysis to assay the transcript levels of three mitochondrially encoded components of the cytochrome c oxidase complex (cox1, cox2, and cox3). Data for a nuclearly encoded component (cox5b) and for two mitochondrial genes that are unrelated to cytochrome c oxidase, ATP synthase alpha-subunit and 18S rRNA, were also determined. Two tissues, embryo and endosperm, were compared and most effects were found to be tissue specific. Significantly, the array of dosage effects upon mitochondrial genes was similar to what had been previously found for nuclear genes. These results support the concept that although mitochondrial genes are prokaryotic in origin, their regulation has been extensively integrated into the eukaryotic cell.
Full Text
The Full Text of this article is available as a PDF (497.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Birchler J. A. Dosage analysis of maize endosperm development. Annu Rev Genet. 1993;27:181–204. doi: 10.1146/annurev.ge.27.120193.001145. [DOI] [PubMed] [Google Scholar]
- Birchler J. A., Hiebert J. C. Interaction of the Enhancer of white-apricot with transposable element alleles at the white locus in Drosophila melanogaster. Genetics. 1989 May;122(1):129–138. doi: 10.1093/genetics/122.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birchler J. A. The genetic basis of dosage compensation of alcohol dehydrogenase-1 in maize. Genetics. 1981 Mar;97(3-4):625–637. doi: 10.1093/genetics/97.3-4.625. [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]
- Capaldi R. A. Structure and function of cytochrome c oxidase. Annu Rev Biochem. 1990;59:569–596. doi: 10.1146/annurev.bi.59.070190.003033. [DOI] [PubMed] [Google Scholar]
- Cone K. C., Burr F. A., Burr B. Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9631–9635. doi: 10.1073/pnas.83.24.9631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper P., Butler E., Newton K. J. Identification of a maize nuclear gene which influences the size and number of cox2 transcripts in mitochondria of perennial ++teosintes. Genetics. 1990 Oct;126(2):461–467. doi: 10.1093/genetics/126.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Droste M., Mollner S., Pfeuffer T. Localisation of an ATP-binding site on adenylyl cyclase type I after chemical and enzymatic fragmentation. FEBS Lett. 1996 Aug 5;391(1-2):209–214. doi: 10.1016/0014-5793(96)00735-1. [DOI] [PubMed] [Google Scholar]
- Fauron C., Casper M., Gao Y., Moore B. The maize mitochondrial genome: dynamic, yet functional. Trends Genet. 1995 Jun;11(6):228–235. doi: 10.1016/s0168-9525(00)89056-3. [DOI] [PubMed] [Google Scholar]
- Fox T. D., Leaver C. J. The Zea mays mitochondrial gene coding cytochrome oxidase subunit II has an intervening sequence and does not contain TGA codons. Cell. 1981 Nov;26(3 Pt 1):315–323. doi: 10.1016/0092-8674(81)90200-2. [DOI] [PubMed] [Google Scholar]
- Frolov M. V., Benevolenskaya E. V., Birchler J. A. Regena (Rga), a Drosophila homolog of the global negative transcriptional regulator CDC36 (NOT2) from yeast, modifies gene expression and suppresses position effect variegation. Genetics. 1998 Jan;148(1):317–329. doi: 10.1093/genetics/148.1.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guo M., Birchler J. A. Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science. 1994 Dec 23;266(5193):1999–2002. doi: 10.1126/science.266.5193.1999. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Dosage-dependent modification of position-effect variegation in Drosophila. Bioessays. 1996 May;18(5):401–409. doi: 10.1002/bies.950180510. [DOI] [PubMed] [Google Scholar]
- Herrin D. L., Schmidt G. W. Rapid, reversible staining of northern blots prior to hybridization. Biotechniques. 1988 Mar;6(3):196-7, 199-200. [PubMed] [Google Scholar]
- Hiesel R., Schobel W., Schuster W., Brennicke A. The cytochrome oxidase subunit I and subunit III genes in Oenothera mitochondria are transcribed from identical promoter sequences. EMBO J. 1987 Jan;6(1):29–34. doi: 10.1002/j.1460-2075.1987.tb04714.x. [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]
- Isaac P. G., Jones V. P., Leaver C. J. The maize cytochrome c oxidase subunit I gene: sequence, expression and rearrangement in cytoplasmic male sterile plants. EMBO J. 1985 Jul;4(7):1617–1623. doi: 10.1002/j.1460-2075.1985.tb03828.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kadowaki K., Kubo N., Ozawa K., Hirai A. Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals. EMBO J. 1996 Dec 2;15(23):6652–6661. [PMC free article] [PubMed] [Google Scholar]
- Laughnan J. R., Gabay-Laughnan S. Cytoplasmic male sterility in maize. Annu Rev Genet. 1983;17:27–48. doi: 10.1146/annurev.ge.17.120183.000331. [DOI] [PubMed] [Google Scholar]
- Levings C. S., 3rd Thoughts on Cytoplasmic Male Sterility in cms-T Maize. Plant Cell. 1993 Oct;5(10):1285–1290. doi: 10.1105/tpc.5.10.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lupold D. S., Caoile A. G., Stern D. B. Genomic context influences the activity of maize mitochondrial cox2 promoters. Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11670–11675. doi: 10.1073/pnas.96.20.11670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lupold D. S., Caoile A. G., Stern D. B. The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units. J Biol Chem. 1999 Feb 5;274(6):3897–3903. doi: 10.1074/jbc.274.6.3897. [DOI] [PubMed] [Google Scholar]
- Marienfeld J. R., Newton K. J. The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics. 1994 Nov;138(3):855–863. doi: 10.1093/genetics/138.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Messing J., Carlson J., Hagen G., Rubenstein I., Oleson A. Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. DNA. 1984;3(1):31–40. doi: 10.1089/dna.1.1984.3.31. [DOI] [PubMed] [Google Scholar]
- Monéger F., Smart C. J., Leaver C. J. Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J. 1994 Jan 1;13(1):8–17. doi: 10.1002/j.1460-2075.1994.tb06230.x. [DOI] [PMC free article] [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]
- Roman H. Mitotic Nondisjunction in the Case of Interchanges Involving the B-Type Chromosome in Maize. Genetics. 1947 Jul;32(4):391–409. doi: 10.1093/genetics/32.4.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh M., Brown G. G. Characterization of expression of a mitochondrial gene region associated with the Brassica "Polima" CMS: developmental influences. Curr Genet. 1993 Oct;24(4):316–322. doi: 10.1007/BF00336783. [DOI] [PubMed] [Google Scholar]
- Ulery T. L., Jang S. H., Jaehning J. A. Glucose repression of yeast mitochondrial transcription: kinetics of derepression and role of nuclear genes. Mol Cell Biol. 1994 Feb;14(2):1160–1170. doi: 10.1128/mcb.14.2.1160. [DOI] [PMC free article] [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]