Intergenomic recombination of mitochondrial genomes in a somatic hybrid plant

Rothenberg, Madge; Boeshore, Maury L.; Hanson, Maureen R.; Izhar, S.

doi:10.1007/bf00381175

Cited by 87 publications

(19 citation statements)

References 20 publications

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“…The fate of the mitochondria and mitochondrial DNA after zygote fusion is unknown. Mitochondrial fusion is presumed to occur in higher plants, since segregation and/or recombination of mitochondrial DNA has been observed in plants regenerated from asexual fusions (32). Although a number of higher plants transmit chloroplast genes biparentally in crosses, and cell fusions regularly segregate progeny homoplasmic for the chloroplast genotypes of the two parents (33)(34)(35), there is but one unequivocal report of chloroplast gene recombination.…”

Section: Resultsmentioning

confidence: 99%

Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas.

Boynton¹,

Harris²,

Burkhart³

et al. 1987

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

138

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Physical differences between organelle genomes of the interfertile species Chlamydomonas reinharodt and Chlamydomonas smithii have been used to demonstrate that sexual zygotes transmit chloroplast and mitochondrial DNA from opposite mating types. Processes responsible can be separated functionally and genetically, although both are controlled by mating type. In vegetative diploids, chloroplast and mitochondrial genomes are transmitted biparentally, but a 1-kilobase insert present in the C. smithy mitochondrial genome spreads unidirectionally to all C. reinhardti genomes in a manner reminiscent of the intron found in the mitochondrial 21S rRNA gene of wA strains of yeast.

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Section: Resultsmentioning

confidence: 99%

Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas.

Boynton¹,

Harris²,

Burkhart³

et al. 1987

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

138

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“…On the other hand, the evidence of mtDNA complementation and recombination clearly indicates that mitochondrial fusion does occur in other organisms, such as S. cerevisiae (10), Chlamydomonas spp. (6), and plants (39,46). However, it has also been found in yeast cells that, in p+ x p+ crosses, mtDNA mixing is not extensive and appears to be limited to that portion of the zygote which gives rise to medial buds and, furthermore, that the sorting of mtDNA is controlled differently from that of the bulk matrix protein constituents (3).…”

Section: Discussionmentioning

confidence: 99%

Complementation of mutant and wild-type human mitochondrial DNAs coexisting since the mutation event and lack of complementation of DNAs introduced separately into a cell within distinct organelles.

1994

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The rules that govern complementation of mutant and wild-type mitochondrial genomes in human cells were investigated under different experimental conditions. Among mitochondrial transformants derived from an individual affected by the MERRF (myoclonus epilepsy associated with ragged red fibers) encephalomyopathy and carrying in heteroplasmic form the mitochondrial tRNALYS mutation associated with that syndrome, normal protein synthesis and respiration was observed when the wild-type mitochondrial DNA exceeded 10% of the total complement. In these transformants, the protective effect of wild-type mitochondrial DNA was shown to involve interactions of the mutant and wild-type gene products. Very different results were obtained in experiments in which two mitochondrial DNAs carrying nonallelic disease-causing mutations were sequentially introduced within distinct organelles into the same human mitochondrial DNA-less (p°) cell. In transformants exhibiting different ratios of the two genomes, no evidence of cooperation between their products was observed, even 3 months after the introduction of the second mutation. These results pointed to the phenotypic independence of the two genomes. A similar conclusion was reached in experiments in which mitochondria carrying a chloramphenicol resistance-inducing mitochondrial DNA mutation were introduced into chloramphenicol-sensitive cells. A plausible interpretation of the different results obtained in the latter two sets of experiments, compared with the complementation behavior observed in the heteroplasmic MERRF transformants, is that in the latter, the mutant and wild-type genomes coexisted in the same organelles from the time of the mutation. This would imply that the way in which mitochondrial DNA is sorted among different organelles plays a fundamental role in determining the oxidative-phosphorylation phenotype in mammalian cells. These results have significant implications for mitochondrial genetics and for studies on the transmission and therapy of mitochondrial DNA-linked diseases.Despite the large number of studies on the expression of artificially produced mitochondrial DNA (mtDNA) mutations and the phenotype of somatic cell hybrids and cybrids, information on mitochondrial genome interactions in mammalian cells is still very limited. The dependence of such interactions on the distribution of the mtDNA molecules among the mitochondria, which changes continuously throughout division and, possibly, fusion of the organelles, and the difficulty of investigating mtDNA sorting in a cell account in part for the present lack of understanding of how much the mitochondrial genomes interact in mammalian cells. The recent discovery of a variety of mtDNA mutations associated with diseases in humans (47) and the growing evidence of accumulation of mtDNA mutations with aging in somatic tissues (12-14, 19, 43) have raised a number of questions about the occurrence and frequency of intermixing of mutant and wild-type mtDNA and/or their products within a cell and the role that co...

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“…26). However, a reverse transcriptase could also be functional in recombination events that occur in plant mtDNAs (29,30), including exchanges that result in both sequence reorganizations and sequence duplications (see ref. 31).…”

Section: Discussionmentioning

confidence: 99%

A sequence encoding a maturase-related protein in a group II intron of a plant mitochondrial nad1 gene.

Wahleithner

Macfarlane

Wolstenholme

1990

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

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We have determined from nucleotide sequence analysis that the subterminal and terminal exons of a respiratory-chain NADH dehydrogenase subunit I gene in broad bean mitochondrial DNA (mtDNA) are separated by a group II intron. Within this intron is a 687-codon open reading frame that, from considerations of similarity between amino acid sequences predicted from this open reading frame and maturase-coding sequences in group II introns ofcertain fungal mitochondrial genes, appears to encode a maturase-related protein. Transcripts complementary to this broad bean sequence (designated a mat-r gene) were detected among RNAs isolated from broad bean mitochondria. Data obtained from DNADNA hybridizations indicated that soybean and corn mtDNAs also contain a mat-r gene and suggested that only one copy of this gene occurs in each plant mtDNA. The putative protein specified by the broad bean mat-r gene contains amino acid sequences characteristic of reverse transcriptases. Because of this, consideration is given to the possibility that the maturase-related protein may be functional in the mechanisms by which plant mtDNA sequences are rearranged and foreign sequences are incorporated into plant mtDNAs.Plant mitochondrial DNAs (mtDNAs) contain the genes for a number of subunits of proteins involved in oxidative phosphorylation and genes for three ribosomal proteins (rpS12, rpS13, and rpS14) (1-3). Introns have been reported only in some plant coxIf genes, in the corn and watermelon nadl genes, and in the nadS gene of Oenothera (4-7). Each of these introns is of the group II type found only in organelle genes (8, 9). Unlike the situation in yeast and other fungi, where some group II (and group I) introns encode enzymes (maturases) necessary for excision of the maturase-encoding intron from RNA transcripts of the gene (10-12), none of the aforementioned plant mitochondrial (mt) introns appears to encode a protein.In this paper, we report the occurrence within a group II RESULTSThe nucleotide sequence of a 4481-nucleotide-pair (ntp) segment of broad bean mtDNA is given in Fig. 1 and our analysis of this sequence is summarized in Fig. 2. Three regions of the amino acid sequence predicted from a 2061-ntp (687 codons) open reading frame within this sequence show considerable similarity to corresponding consecutive regions ofamino acid sequences of the maturase encoded by the all intron of the cytochrome c oxidase subunit I (coxI) gene of Saccharomyces cerevisiae and by the following fungal putative maturase gene-containing mt intron sequences (Fig. 3): aI2 of the coxI gene of S. cerevisiae (14), I and IA of the coxI gene of Podospora anserina (15,16), and bl of the cytochrome b (cob) gene of Schizosaccharomyces pombe (17). Because of these amino acid sequence similarities, we have designated the putative broad bean protein a maturase-related protein (MAT-R) and the sequence that encodes it a mat-r gene.The broad bean mat-r gene, like the S. cerevisiae, P. anserina, and Sc. pombe mat genes, is contained in a group II intro...

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Intergenomic recombination of mitochondrial genomes in a somatic hybrid plant

Cited by 87 publications

References 20 publications

Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas.

Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas.

Complementation of mutant and wild-type human mitochondrial DNAs coexisting since the mutation event and lack of complementation of DNAs introduced separately into a cell within distinct organelles.

A sequence encoding a maturase-related protein in a group II intron of a plant mitochondrial nad1 gene.

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