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. 1991 Dec;3(12):1349–1362. doi: 10.1105/tpc.3.12.1349

Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region.

M Singh 1, G G Brown 1
PMCID: PMC160097  PMID: 1840901

Abstract

To identify regions of the mitochondrial genome that potentially could specify the "Polima" (pol) cytoplasmic male sterility (CMS) of Brassica napus, transcripts of 14 mitochondrial genes from nap (male fertile), pol (male sterile), and nuclear fertility-restored pol cytoplasm plants were analyzed. Transcriptional differences among these plants were detected only with the ATPase subunit 6 (atp6) gene. Structural analysis of the atp6 gene regions of pol and nap mitochondrial DNAs showed that rearrangements in the pol mitochondrial genome occurring upstream of atp6 have generated a chimeric 224-codon open reading frame, designated orf224, that is cotranscribed with atp6. In CMS plants, most transcripts of this region are dicistronic, comprising both orf224 and atp6 sequences. Nuclear restorer genes at either of two distinct loci appear to specifically alter this transcript pattern such that monocistronic atp6 transcripts predominate. The differences in expression of this region appear to result, in part, from differential processing of a tRNA-like element comprising a tRNA pseudogene present immediately upstream of atp6 in both the sterile and fertile mitochondrial DNAs. Possible mechanisms by which expression of the orf224/atp6 locus and the Polima CMS trait may be specifically related are considered.

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Selected References

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  1. 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]
  2. Bailey-Serres J., Hanson D. K., Fox T. D., Leaver C. J. Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell. 1986 Nov 21;47(4):567–576. doi: 10.1016/0092-8674(86)90621-5. [DOI] [PubMed] [Google Scholar]
  3. Bland M. M., Levings C. S., 3rd, Matzinger D. F. The ATPase subunit 6 gene of tobacco mitochondria contains an unusual sequence. Curr Genet. 1987;12(7):475–481. doi: 10.1007/BF00419555. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Bonen L., Bird S., Belanger L. Characterization of the wheat mitochondrial orf25 gene. Plant Mol Biol. 1990 Nov;15(5):793–795. doi: 10.1007/BF00016131. [DOI] [PubMed] [Google Scholar]
  6. Bonen L., Boer P. H., McIntosh J. E., Gray M. W. Nucleotide sequence of the wheat mitochondrial gene for subunit I of cytochrome oxidase. Nucleic Acids Res. 1987 Aug 25;15(16):6734–6734. doi: 10.1093/nar/15.16.6734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Brown G. G., Auchincloss A. H., Covello P. S., Gray M. W., Menassa R., Singh M. Characterization of transcription initiation sites on the soybean mitochondrial genome allows identification of a transcription-associated sequence motif. Mol Gen Genet. 1991 Sep;228(3):345–355. doi: 10.1007/BF00260626. [DOI] [PubMed] [Google Scholar]
  9. Covello P. S., Gray M. W. RNA editing in plant mitochondria. Nature. 1989 Oct 19;341(6243):662–666. doi: 10.1038/341662a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Finnegan P. M., Brown G. G. Transcriptional and Post-Transcriptional Regulation of RNA Levels in Maize Mitochondria. Plant Cell. 1990 Jan;2(1):71–83. doi: 10.1105/tpc.2.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hanic-Joyce P. J., Spencer D. F., Gray M. W. In vitro processing of transcripts containing novel tRNA-like sequences ('t-elements') encoded by wheat mitochondrial DNA. Plant Mol Biol. 1990 Oct;15(4):551–559. doi: 10.1007/BF00017830. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  18. Lambowitz A. M., Perlman P. S. Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem Sci. 1990 Nov;15(11):440–444. doi: 10.1016/0968-0004(90)90283-h. [DOI] [PubMed] [Google Scholar]
  19. Makaroff C. A., Apel I. J., Palmer J. D. Characterization of radish mitochondrial atpA: influence of nuclear background on transcription of atpA-associated sequences and relationship with male sterility. Plant Mol Biol. 1990 Nov;15(5):735–746. doi: 10.1007/BF00016123. [DOI] [PubMed] [Google Scholar]
  20. Makaroff C. A., Apel I. J., Palmer J. D. The atp6 coding region has been disrupted and a novel reading frame generated in the mitochondrial genome of cytoplasmic male-sterile radish. J Biol Chem. 1989 Jul 15;264(20):11706–11713. [PubMed] [Google Scholar]
  21. 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]
  22. Makaroff C. A., Palmer J. D. Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol. 1988 Apr;8(4):1474–1480. doi: 10.1128/mcb.8.4.1474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Newton K. J., Knudsen C., Gabay-Laughnan S., Laughnan J. R. An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell. 1990 Feb;2(2):107–113. doi: 10.1105/tpc.2.2.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pruitt K. D., Hanson M. R. Transcription of the Petunia mitochondrial CMS-associated Pcf locus in male sterile and fertility-restored lines. Mol Gen Genet. 1991 Jul;227(3):348–355. doi: 10.1007/BF00273922. [DOI] [PubMed] [Google Scholar]
  25. Quagliariello C., Saiardi A., Gallerani R. The cytochrome oxidase subunit III gene in sunflower mitochondria is cotranscribed with an open reading frame conserved in higher plants. Curr Genet. 1990 Nov;18(4):355–363. doi: 10.1007/BF00318217. [DOI] [PubMed] [Google Scholar]
  26. Schuster W., Brennicke A. Conserved sequence elements at putative processing sites in plant mitochondria. Curr Genet. 1989 Mar;15(3):187–192. doi: 10.1007/BF00435505. [DOI] [PubMed] [Google Scholar]
  27. Stern D. B., Newton K. J. Isolation of plant mitochondrial RNA. Methods Enzymol. 1986;118:488–496. doi: 10.1016/0076-6879(86)18095-5. [DOI] [PubMed] [Google Scholar]
  28. Wahleithner J. A., Wolstenholme D. R. Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res. 1988 Jul 25;16(14B):6897–6913. doi: 10.1093/nar/16.14.6897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]

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