Suppression of Cytoplasmic Male Sterility by Nuclear Genes Alters Expression of a Novel Mitochondrial Gene Region

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 1991 Dec 1

PMID 1840901

Citations 77

Authors

M Singh

G G Brown

Affiliations

Soon will be listed here.

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.

Citing Articles

A Systematic Review and Developmental Perspective on Origin of CMS Genes in Crops.

Zhang X, Ding Z, Lou H, Han R, Ma C, Yang S Int J Mol Sci. 2024; 25(15).

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A Set of Molecular Markers to Accelerate Breeding and Determine Seed Purity of CMS Three-Line Hybrids in .

Zhang Y, An R, Song M, Xie C, Wei S, Wang D Plants (Basel). 2023; 12(7).

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Comparison of Mitochondrial Genomes between a Cytoplasmic Male-Sterile Line and Its Restorer Line for Identifying Candidate CMS Genes in .

Xuan L, Qi G, Li X, Yan S, Cao Y, Huang C Int J Mol Sci. 2022; 23(16).

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Global Patterns of Subgenome Evolution in Organelle-Targeted Genes of Six Allotetraploid Angiosperms.

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Comparative analysis of the complete mitochondrial genome sequences and anther development cytology between maintainer and Ogura-type cytoplasm male-sterile cabbage (B. oleracea Var. capitata).

Zhong X, Chen D, Cui J, Li H, Huang Y, Kang J BMC Genomics. 2021; 22(1):646.

PMID: 34493212 PMC: 8425178. DOI: 10.1186/s12864-021-07963-x.

References

Covello P, Gray M . RNA editing in plant mitochondria. Nature. 1989; 341(6243):662-6. DOI: 10.1038/341662a0. View

Bland M, Levings 3rd C, Matzinger D . The ATPase subunit 6 gene of tobacco mitochondria contains an unusual sequence. Curr Genet. 1987; 12(7):475-81. DOI: 10.1007/BF00419555. View

Makaroff C, Apel I, Palmer J . 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; 264(20):11706-13. View

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; 6(1):29-34. PMC: 553352. DOI: 10.1002/j.1460-2075.1987.tb04714.x. View

Makaroff C, Palmer J . Mitochondrial DNA rearrangements and transcriptional alterations in the male-sterile cytoplasm of Ogura radish. Mol Cell Biol. 1988; 8(4):1474-80. PMC: 363305. DOI: 10.1128/mcb.8.4.1474-1480.1988. View

Bonen L, Bird S, Belanger L . Characterization of the wheat mitochondrial orf25 gene. Plant Mol Biol. 1990; 15(5):793-5. DOI: 10.1007/BF00016131. View

Bonen L, Boer P, McIntosh J, Gray M . Nucleotide sequence of the wheat mitochondrial gene for subunit I of cytochrome oxidase. Nucleic Acids Res. 1987; 15(16):6734. PMC: 306136. DOI: 10.1093/nar/15.16.6734. View

Schuster W, Brennicke A . Conserved sequence elements at putative processing sites in plant mitochondria. Curr Genet. 1989; 15(3):187-92. DOI: 10.1007/BF00435505. View

Wahleithner J, WOLSTENHOLME D . Ribosomal protein S14 genes in broad bean mitochondrial DNA. Nucleic Acids Res. 1988; 16(14B):6897-913. PMC: 338341. DOI: 10.1093/nar/16.14.6897. View

10.

Lambowitz A, Perlman P . Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem Sci. 1990; 15(11):440-4. DOI: 10.1016/0968-0004(90)90283-h. View

11.

Dewey R, Levings C, Timothy D . Nucleotide sequence of ATPase subunit 6 gene of maize mitochondria. Plant Physiol. 1985; 79(3):914-9. PMC: 1074995. DOI: 10.1104/pp.79.3.914. View

12.

Newton K, Knudsen C, Gabay-Laughnan S, Laughnan J . An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell. 1990; 2(2):107-13. PMC: 159868. DOI: 10.1105/tpc.2.2.107. View

13.

Braun C, Levings C . Nucleotide Sequence of the F(1)-ATPase alpha Subunit Gene from Maize Mitochondria. Plant Physiol. 1985; 79(2):571-7. PMC: 1074929. DOI: 10.1104/pp.79.2.571. View

14.

Iams K, Sinclair J . Mapping the mitochondrial DNA of Zea mays: Ribosomal gene localization. Proc Natl Acad Sci U S A. 1982; 79(19):5926-9. PMC: 347023. DOI: 10.1073/pnas.79.19.5926. View

15.

Dewey R, Levings 3rd C, Timothy D . Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell. 1986; 44(3):439-49. DOI: 10.1016/0092-8674(86)90465-4. View

16.

Bailey-Serres J, Hanson D, Fox T, Leaver C . Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell. 1986; 47(4):567-76. DOI: 10.1016/0092-8674(86)90621-5. View

17.

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; 18(4):355-63. DOI: 10.1007/BF00318217. View

18.

Bland M, Levings 3rd C, Matzinger D . The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet. 1986; 204(1):8-16. DOI: 10.1007/BF00330180. View

19.

Pruitt K, Hanson M . Transcription of the Petunia mitochondrial CMS-associated Pcf locus in male sterile and fertility-restored lines. Mol Gen Genet. 1991; 227(3):348-55. DOI: 10.1007/BF00273922. View

20.

Stern D, Newton K . Isolation of plant mitochondrial RNA. Methods Enzymol. 1986; 118:488-96. DOI: 10.1016/0076-6879(86)18095-5. View