Two nuclear-directed means of suppressing a dominant mitochondrial mutation in common bean

R. Sarria, H. Janska, M. Arrieta-Montiel, A. Lyznik, Sally Mackenzie

Research output: Contribution to journalArticle

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Abstract

We have summarized recent work demonstrating two means by which the pvs- orf239 mitochondrial mutation in CMS common bean is suppressed by nuclear- directed mechanisms. These involve mitochondrial genomic shifts in relative DNA copy number, apparently reversible in nature and effective at suppressing pvs-orf239 gene expression, and posttranslational ORF239 protein turnover. Important questions still remain to be addressed. With regard to mitochondrial genomic shifts in DNA copy number, it remains to be seen how this mechanism operates functionally. The retention of mtDNA molecules at substoichiometric copy numbers far lower than one copy per cell may be the consequence of low-level DNA replication or rare recombination events. In the case of the CMS system in common bean, mapping evidence to date supports a hypothesis of pvs-orf239 retention on an autonomously replicating molecule that does not appear to be generated via recombination. This assumption is based on the lack of evidence for a pvs-orf239 configuration present in different genomic ('parental' and 'recombinant') environments, its complete suppression upon reversion (in the case of rare recombination, overall copy number would presumably remain unchanged), and its rapid reamplification under in organello incubation conditions shown to support replication. However, a model of replicative retention of the orf-239 sequence substoichiometrically over multiple generations would likely necessitate a tissue-specific mechanism for mitochondrial sequence retention, ensuring transmission of the sequence through development to reproductive tissues. We are currently testing this hypothesis. One important clue to the regulation of relative copy number in the mitochondrial genome should come with the isolation of nuclear genes regulating the genome shifting process. In CMS common bean, the nuclear gene Fr appears to effect the reversion phenomenon, since its introduction results in the copy number suppression of the pvs- containing mitochondrial DNA molecule (Mackenzie and Chase 1990; Vanhouten W and Mackenzie SA, manuscript in preparation). Identification of the Fr gene product should be useful in deducing the process underlying this shifting phenomenon that is common to so many plant species. The observation of ORF239 posttranslational regulation is particularly intriguing given the recent observations made by others that unedited transcripts in plant mitochondria are translationally competent (Gualberto et al. 1988; Lu and Hanson 1996; Lu et al. 1996; Phreaner et al. 1996). It remains to be seen whether the Lon- like protease identified in our studies will be shown to influence the turnover of aberrant gene products arising as a consequence of the editing process. In addition, it can be speculated that the Lon-like protease may be involved in mitochondrial stress response, since we have found it to be induced upon heat shock (Sarria R and Mackenzie SA, unpublished data). At this time the most enticing question still to be pursued is why, if ORF239 is rapidly turned over in vegetative tissues, is it not likewise eliminated from developing anther tissues. Transgenic studies of Lon expression during plant development are currently under way.

Original languageEnglish (US)
Pages (from-to)357-361
Number of pages5
JournalJournal of Heredity
Volume90
Issue number3
DOIs
StatePublished - May 1 1999

Fingerprint

Protease La
Genetic Recombination
Mutation
Mitochondrial DNA
Genes
Contagious Ecthyma
Mitochondrial Genome
Plant Development
Manuscripts
DNA
DNA Replication
Shock
Mitochondria
Hot Temperature
Observation
Genome
Gene Expression
Proteins

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Molecular Biology
  • Genetics
  • Genetics(clinical)

Cite this

Sarria, R. ; Janska, H. ; Arrieta-Montiel, M. ; Lyznik, A. ; Mackenzie, Sally. / Two nuclear-directed means of suppressing a dominant mitochondrial mutation in common bean. In: Journal of Heredity. 1999 ; Vol. 90, No. 3. pp. 357-361.
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Two nuclear-directed means of suppressing a dominant mitochondrial mutation in common bean. / Sarria, R.; Janska, H.; Arrieta-Montiel, M.; Lyznik, A.; Mackenzie, Sally.

In: Journal of Heredity, Vol. 90, No. 3, 01.05.1999, p. 357-361.

Research output: Contribution to journalArticle

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N2 - We have summarized recent work demonstrating two means by which the pvs- orf239 mitochondrial mutation in CMS common bean is suppressed by nuclear- directed mechanisms. These involve mitochondrial genomic shifts in relative DNA copy number, apparently reversible in nature and effective at suppressing pvs-orf239 gene expression, and posttranslational ORF239 protein turnover. Important questions still remain to be addressed. With regard to mitochondrial genomic shifts in DNA copy number, it remains to be seen how this mechanism operates functionally. The retention of mtDNA molecules at substoichiometric copy numbers far lower than one copy per cell may be the consequence of low-level DNA replication or rare recombination events. In the case of the CMS system in common bean, mapping evidence to date supports a hypothesis of pvs-orf239 retention on an autonomously replicating molecule that does not appear to be generated via recombination. This assumption is based on the lack of evidence for a pvs-orf239 configuration present in different genomic ('parental' and 'recombinant') environments, its complete suppression upon reversion (in the case of rare recombination, overall copy number would presumably remain unchanged), and its rapid reamplification under in organello incubation conditions shown to support replication. However, a model of replicative retention of the orf-239 sequence substoichiometrically over multiple generations would likely necessitate a tissue-specific mechanism for mitochondrial sequence retention, ensuring transmission of the sequence through development to reproductive tissues. We are currently testing this hypothesis. One important clue to the regulation of relative copy number in the mitochondrial genome should come with the isolation of nuclear genes regulating the genome shifting process. In CMS common bean, the nuclear gene Fr appears to effect the reversion phenomenon, since its introduction results in the copy number suppression of the pvs- containing mitochondrial DNA molecule (Mackenzie and Chase 1990; Vanhouten W and Mackenzie SA, manuscript in preparation). Identification of the Fr gene product should be useful in deducing the process underlying this shifting phenomenon that is common to so many plant species. The observation of ORF239 posttranslational regulation is particularly intriguing given the recent observations made by others that unedited transcripts in plant mitochondria are translationally competent (Gualberto et al. 1988; Lu and Hanson 1996; Lu et al. 1996; Phreaner et al. 1996). It remains to be seen whether the Lon- like protease identified in our studies will be shown to influence the turnover of aberrant gene products arising as a consequence of the editing process. In addition, it can be speculated that the Lon-like protease may be involved in mitochondrial stress response, since we have found it to be induced upon heat shock (Sarria R and Mackenzie SA, unpublished data). At this time the most enticing question still to be pursued is why, if ORF239 is rapidly turned over in vegetative tissues, is it not likewise eliminated from developing anther tissues. Transgenic studies of Lon expression during plant development are currently under way.

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