Abstract
Two nuclear genes, Fr and Fr2, have been identified that restore pollen fertility to cytoplasmic male sterile (CMS) common bean (Phaseolus vulgaris L.) by apparently distinct mechanisms. Whereas Fr2 appears to suppress the expression of a male sterility associated mitochondrial sequence (designated pvs), Fr restores pollen fertility by causing the elimination of this unusual mitochondrial DNA segment. To further investigate the mechanism of Fr action, Fr and Fr2 were cointroduced into the nucleus of a bean line containing the sterility inducing cytoplasm. When the effect of pvs was suppressed by Fr2, the presence of Fr no longer directed the elimination of the mitochondrial pvs sequence. This result suggests that the Fr function is dependent on proper expression of the pvs sequence. To evaluate the temporal and spatial patterns of Fr action, we undertook a polymerase chain reaction-based approach to trace the fate of the pvs sequence in different tissues of F(2) and F(3) fertile-restored plants derived from a genetic cross between a cytoplasmic male sterile line of common bean, CMS-Sprite (frfr), and fertility restorer line R351 (FrFr). We demonstrate that the Fr-directed disappearance of pvs sequence occurs during flower development. Elimination of the pvs sequence from developing megaspores results in permanent fertility restoration in the following generations. Genetic analysis demonstrated that permanent fertility restoration, that is, the complete elimination of pvs from reproductive tissues requires two doses of the Fr allele or the absence of fr in F(2) individuals. The effect of Fr was reversible until full fertility was achieved. On the basis of these results, we propose a model for the mechanism of pvs elimination by the Fr gene and discuss the dynamics of pvs-containing mitochondrial transmission in the presence of the Fr gene.
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Selected References
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- 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]
- Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
- Chase C. D. Expression of CMS-unique and flanking mitochondrial DNA sequences in Phaseolus vulgaris L. Curr Genet. 1994 Mar;25(3):245–251. doi: 10.1007/BF00357169. [DOI] [PubMed] [Google Scholar]
- Chase C. D., Ortega V. M. Organization of ATPA coding and 3' flanking sequences associated with cytoplasmic male sterility in Phaseolus vulgaris L. Curr Genet. 1992 Aug;22(2):147–153. doi: 10.1007/BF00351475. [DOI] [PubMed] [Google Scholar]
- Dawson A. J., Jones V. P., Leaver C. J. The apocytochrome b gene in maize mitochondria does not contain introns and is preceded by a potential ribosome binding site. EMBO J. 1984 Sep;3(9):2107–2113. doi: 10.1002/j.1460-2075.1984.tb02098.x. [DOI] [PMC free article] [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]
- Fauron C. M., Havlik M., Brettell R. I. The mitochondrial genome organization of a maize fertile cmsT revertant line is generated through recombination between two sets of repeats. Genetics. 1990 Feb;124(2):423–428. doi: 10.1093/genetics/124.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanson M. R. Plant mitochondrial mutations and male sterility. Annu Rev Genet. 1991;25:461–486. doi: 10.1146/annurev.ge.25.120191.002333. [DOI] [PubMed] [Google Scholar]
- Johns C., Lu M., Lyznik A., Mackenzie S. A mitochondrial DNA sequence is associated with abnormal pollen development in cytoplasmic male sterile bean plants. Plant Cell. 1992 Apr;4(4):435–449. doi: 10.1105/tpc.4.4.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Köhler R. H., Horn R., Lössl A., Zetsche K. Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol Gen Genet. 1991 Jul;227(3):369–376. doi: 10.1007/BF00273925. [DOI] [PubMed] [Google Scholar]
- Laver H. K., Reynolds S. J., Moneger F., Leaver C. J. Mitochondrial genome organization and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J. 1991 Sep;1(2):185–193. doi: 10.1111/j.1365-313x.1991.00185.x. [DOI] [PubMed] [Google Scholar]
- Mackenzie S. A., Chase C. D. Fertility Restoration Is Associated with Loss of a Portion of the Mitochondrial Genome in Cytoplasmic Male-Sterile Common Bean. Plant Cell. 1990 Sep;2(9):905–912. doi: 10.1105/tpc.2.9.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackenzie S. A., Pring D. R., Bassett M. J., Chase C. D. Mitochondrial DNA rearrangement associated with fertility restoration and cytoplasmic reversion to fertility in cytoplasmic male sterile Phaseolus vulgaris L. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2714–2717. doi: 10.1073/pnas.85.8.2714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martínez-Zapater J. M., Gil P., Capel J., Somerville C. R. Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell. 1992 Aug;4(8):889–899. doi: 10.1105/tpc.4.8.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Schapira A. H. Mitochondrial disorders. Curr Opin Genet Dev. 1993 Jun;3(3):457–465. doi: 10.1016/0959-437x(93)90120-e. [DOI] [PubMed] [Google Scholar]
- Singh M., Brown G. G. Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell. 1991 Dec;3(12):1349–1362. doi: 10.1105/tpc.3.12.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tzagoloff A., Myers A. M. Genetics of mitochondrial biogenesis. Annu Rev Biochem. 1986;55:249–285. doi: 10.1146/annurev.bi.55.070186.001341. [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]