Stoichiometric Shifts in the Common Bean Mitochondrial Genome Leading to Male Sterility and Spontaneous Reversion to Fertility

Janska, Hanna; Sarria, Rodrigo; Wołoszyńska, Magdalena; Arrieta-Montiel, Maria P.; Mackenzie, Sally A.

doi:10.2307/3870719

Cited by 50 publications

(101 citation statements)

References 31 publications

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“…Furthermore, extensive analysis of plant mtDNA with a variety of gel electrophoresis techniques suggests that linear, rather than circular, forms are most predominant in vivo (8). These different forms may be present in widely differing stoichiometries (9), and recent evidence suggests, under certain circumstances, relative copy number may determine plant phenotype (10).…”

mentioning

confidence: 99%

Genomic context influences the activity of maize mitochondrial cox2 promoters

Lupold

Caoile²,

Stern³

1999

Proc. Natl. Acad. Sci. U.S.A.

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Plant mitochondrial genomes are highly recombinogenic, with a variety of species-specific direct and inverted repeats leading to in vivo accumulation of multiple DNA forms. In maize, the cox2 gene, which encodes subunit II of cytochrome c oxidase, lies immediately downstream of a 0.7-kilobase direct repeat, which is present in two copies in the 570-kilobase master chromosome. Promoters for cox2 exist upstream of both of these copies, in regions we have termed A and B. Three region B promoters are active for cox2 transcription in the master chromosome, whereas two region A promoters are active for cox2 transcription after recombination across the direct repeats. We have measured the proportion of genomes carrying region A or B upstream of cox2 in maize seedlings and found a ratio of approximately 1:6. Promoter strength, based on run-on transcription assays, shows a ratio of 1:4 for region A to region B promoters. These data allowed us to predict the relative contributions of region A and B to mitochondrial transcript accumulation, based on a simple product of genome-form abundance and promoter strength. When promoter use was determined by using quantitative reverse transcriptase-PCR, however, we found that region A promoters were used at an unexpectedly high rate when upstream of cox2 and used less than expected when not upstream of cox2. Thus, the use of this set of promoters seems to respond to genomic context. These results suggest a role for intragenomic and intergenomic recombination in regulating plant mitochondrial gene expression.

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mentioning

confidence: 99%

Genomic context influences the activity of maize mitochondrial cox2 promoters

Lupold

Caoile²,

Stern³

1999

Proc. Natl. Acad. Sci. U.S.A.

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“…These substoichiometric forms have been estimated at levels as low as one copy per every 100-200 cells (19). Generally, the rapid shifting process involves only a single subgenomic DNA molecule, often containing recombination-derived chimeric sequences, and the process is apparently reversible (18,20). Genomic shifting can alter plant phenotype because the process activates or silences mitochondrial sequences located on the shifted molecule.…”

mentioning

confidence: 99%

“…First reported in maize (17) as the stable presence of subgenomic mitochondrial DNA molecules within the genome at nearly undetectable levels, the process seems to be highly dynamic. Mitochondrial genomic shifting involves rapid and dramatic changes in relative copy number of portions of the mitochondrial genome over the time of one generation (18). These substoichiometric forms have been estimated at levels as low as one copy per every 100-200 cells (19).…”

mentioning

confidence: 99%

“…Genomic shifting can alter plant phenotype because the process activates or silences mitochondrial sequences located on the shifted molecule. Observed phenotypic changes have included plant tissue culture properties (20), leaf variegation and distortion (16), and spontaneous reversion to fertility in cytoplasmic male sterile crop plants (18,21). It has been postulated that substoichiometric shifting may have evolved to permit the species to create and retain mitochondrial genetic variation in a silenced but retrievable form (22).…”

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confidence: 99%

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Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS

Abdelnoor

Yule

Elo

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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228

243

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The plant mitochondrial genome is retained in a multipartite structure that arises by a process of repeat-mediated homologous recombination. Low-frequency ectopic recombination also occurs, often producing sequence chimeras, aberrant ORFs, and novel subgenomic DNA molecules. This genomic plasticity may distinguish the plant mitochondrion from mammalian and fungal types. In plants, relative copy number of recombination-derived subgenomic DNA molecules within mitochondria is controlled by nuclear genes, and a genomic shifting process can result in their differential copy number suppression to nearly undetectable levels. We have cloned a nuclear gene that regulates mitochondrial substoichiometric shifting in Arabidopsis. The CHM gene was shown to encode a protein related to the MutS protein of Escherichia coli that is involved in mismatch repair and DNA recombination. We postulate that the process of substoichiometric shifting in plants may be a consequence of ectopic recombination suppression or replication stalling at ectopic recombination sites to effect molecule-specific copy number modulation.

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“…This latter ®nding could indicate that the LL strain is no longer susceptible to suppression by defective mtDNAs caused by plasmid integration. Further characterization of this strain might shed light on this important yet poorly understood process of suppression, which appears to be involved in a variety of mitochondrially related phenomena in fungi (Griths 1992), as well as in cytoplasmic male-sterility in plants (Janska et al 1998), and mitochondrial myopathies of mice and humans (Wallace 1999).…”

Section: Pms4416 Is a Unique Retroplasmid Variantmentioning

confidence: 99%

Senescence associated with the over-replication of a mitochondrial retroplasmid in Neurospora crassa

Stevenson

Fox²,

Kennell³

2000

Mol Gen Genet

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Mitochondrial DNA rearrangements and deletions are a prevailing feature of ®lamentous fungal cultures that undergo senescence. In Neurospora spp., strains containing the Mauriceville and Varkud mitochondrial retroplasmids routinely senesce at elevated temperatures, a process that is initiated by the integration of variant forms of the plasmids into the mitochondrial genome. Here, we describe a strain that is phenotypically distinguishable from previously characterized senescent strains and show that senescence can occur in the absence of plasmid integration and associated alterations in mitochondrial DNA. The MS4416 strain contains a unique variant of the Mauriceville retroplasmid, and undergoes senescence at highly predictable frequencies at 37°, 25°a nd 18°C. Decline in vegetative growth rate correlates with increased levels of the variant plasmid and alterations in the synthesis of mitochondrially encoded proteins, suggesting that plasmid over-replication interferes with mitochondrial translation. We also report the isolation of a mutant strain that escapes senescence yet still maintains high levels of the variant plasmid. Its ability to tolerate a growth-suppressive retroplasmid suggests that there are mechanisms in Neurospora which compensate for the deleterious eects that plasmid over-replication has on mitochondrial function.

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Stoichiometric Shifts in the Common Bean Mitochondrial Genome Leading to Male Sterility and Spontaneous Reversion to Fertility

Cited by 50 publications

References 31 publications

Genomic context influences the activity of maize mitochondrial cox2 promoters

Genomic context influences the activity of maize mitochondrial cox2 promoters

Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS

Senescence associated with the over-replication of a mitochondrial retroplasmid in Neurospora crassa

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