The heterogeneity of mitochondrial DNA in different tissues from the same animal

Coote, J. L.; Szabados, Gy.; Work, T. S.

doi:10.1016/0014-5793(79)80967-9

Cited by 21 publications

(7 citation statements)

References 14 publications

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“…Only a few examples of such a state have been reported (4,(31)(32)(33). The occurrence of a mtDNA polymorphism in a matemal lineage of Holstein cows has been an advantageous situation for the analysis of heteroplasmy; however, it has not been observed per se in any animal (34).…”

Section: Resultsmentioning

confidence: 99%

Mitochondrial DNA heteroplasmy in Drosophila mauritiana.

Solignac¹,

Monnerot²,

Mounolou³

1983

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

125

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Mitochondrial DNA extracted from an isofemale strain of Drosophila mauritiana (subgroup melanogaster) appeared to be heterogeneous in size. A short genome [S; 18,500 base pairs (bp)] and a longer one (L; 19,000 bp) coexist in the preparation. The additional 500 bp have been located within the A+T-rich region. Hpa I digest patterns suggest that the S genome may carry a duplication of a 500-bp sequence including an Hpa I site and that the L genome may carry a triplication of the same sequence. At the 30th generation of the isofemale strain, 60 female genotypes were examined individually. Half of the flies were pure either for the S or the L DNA. The remaining 50% exhibited various degrees of heteroplasmy for the two DNA types. Among metazoan animals, this D. mauritiana strain offers an exceptional situation with regard to the number of individuals heterogeneous for mtDNA and the relative stability of heteroplasmy through generations.In metazoan animals, the lack of mitochondrial mutants is compensated by the use of restriction endonucleases to study the heredity and the evolution of mitochondrial DNA. Three general features of animal mitochondrial genetics emerge from different analyses (1). (i) mtDNA is maternally inherited: the first evidences from interspecific hybridization experiments (2, 3) have been confirmed later by intraspecific crosses. (ii) Sequence differences are frequent between individuals within the same species and even within the same population (4-8). (iii) From the existence of interindividual differences, a heteroplasmic transitory phase might be expected; however, for each individual the mtDNA always appears as a molecular clone (6-10): the mtDNA is homogeneous for a given organ, and the DNA molecules are identical from one organ to another within an individual (4, 11). This last observation suggests a rapid purification of the mitochondrial genome.Drosophila mtDNA exhibits these general properties (12-14). In the course of a sequence variability study within the melanogaster subgroup of Drosophila, we analyzed numerous isofemale strains. As For physical mapping, mitochondria were isolated either from embryos, from virgin eggs, or from adult flies. mtDNA was purified on CsCl gradients. If necessary, a second purification was carried out on CsCI/4',6-diamidino-2-phenylindol-2.HCl (DAPI) gradients. Cleavage sites of nine restriction endonucleases were mapped by analysis of partial and complete single digests and of double digests. The digestion fragments were separated by vertical electrophoresis on 1% agarose or 4.5% acrylamide slab gels. HindIII/A phage and HindII/4X174 phage DNA digests were used as molecular weight standards for calibration. After electrophoresis the gels were stained by standard procedures with ethidium bromide and then photographed under short wave UV light.For individual mitochondrial genotype comparison, it was not possible to get from a single fly enough DNA for a slab gel analysis; so we used the progeny of each female fly under study. About 30 generations...

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Section: Resultsmentioning

confidence: 99%

Mitochondrial DNA heteroplasmy in Drosophila mauritiana.

Solignac¹,

Monnerot²,

Mounolou³

1983

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

125

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“…1980, and personal communication), or from placentas of more than 80 humans (Brown, 1980, and personal communication). We are aware of only a single report of heterogeneity in mtDNA from a single animal (Coote, Szabados & Work, 1979), and this interpretation is complicated by the possibility that the mtDNA's from the samples examined were not digested to completion); (3) mtDNA sequence heterogeneity is extensive among individuals of a species and sometimes among individuals within a local inter-breeding population (Upholt & Dawid, 1977;Avise et al 1979a, b;Brown & Wright, 1979).…”

Section: Introductionmentioning

confidence: 97%

Models of mitochondrial DNA transmission genetics and evolution in higher eucaryotes

et al. 1982

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The future value of mitochondrial DNA (mtDNA) sequence information to studies in population biology will depend in part on understanding of mtDNA transmission genetics both within cell lineages and between animal generations. A series of stochastic models has been constructed here based on various possibilities concerning this transmission. Several of the models generate predictions inconsistent with available data and, hence, their assumptions are provisionally rejected. Other models cannot yet be falsified. These latter models include assumptions that (1) mtDNA's are sorted through cellular lineages by random allocation to daughter cells in germ cell lineages; (2) the effective intracellular population sizes (n M 's) of mtDNA's are small; and (3) sperm may (or may not) provide a low level 'gene-flow' bridge between otherwise isolated female lineages. It is hoped that the models have helped to identify and will stimulate further empirical study of various parameters likely to strongly influence mtDNA evolution. In particular, critical experiments or measurements are needed to determine the effective sizes of mtDNA populations in germ (and somatic) cells and to examine possible paternal contributions to zygote mtDNA composition.

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“…The present work demonstrates that no individual bluegill exhibits heteroplasmicity at a 5% or greater level that can be explained by paternal mtDNA transmission. If results of this study can be generalized to other groups where true heteroplasmicity may have been observed (e.g., Coote et al, 1979;Brown et al, 1983), the heterop1asmicity 4. Map positions and digestion profiles for the XbaI "a," "b," and "c" genotypes observed in bluegill.…”

Section: Transmission Genetics and Tests For Somatic Cell Heteroplasmmentioning

confidence: 99%

CHARACTERIZATION OF MITOCHONDRIAL DNA VARIABILITY IN A HYBRID SWARM BETWEEN SUBSPECIES OF BLUEGILL SUNFISH ( LEPOMIS MACROCHIRUS )

et al. 1984

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Genetic variation in mitochondrial have chosen an evolutionary setting (a DNA (mtDNA) has been studied in pop-local subspecies hybrid swarm) which ulations of mammals, Drosophila, and a should facilitate analysis of several posfew other higher animals (reviews in Av-sible features of mtDNA variation. Disise and Lansman, 1983;Brown, 1983). tinctive mtDNA genotypes contributed Among the noteworthy features of by the parental subspecies to the hybrid mtDNA variability pertinent to the anal-swarm are identified. As described later, ysis of evolutionary process are the fol-these provide a special opportunity to lowing: a rapid rate of evolution involv-recognize paternally-generated mtDNA ing primarily base substitutions plus very heteroplasmicity, if it does exist, both in small addition/deletions (Brown et al., somatic and germ cells. Study of the as-1979; Cann and Wilson, 1983); a re-sociation between allozyme and mtDNA markable stability of gene content and markers permits comparison of the evoarrangement; apparent mtDNA se-lutionary consequences ofbiparental verquence homogeneity (homoplasmicity) sus uniparental transmission of genoin somatic cells within an individual or-types across animal generations. We will ganism; extensive sequence polymor-also include a description of mtDNA sephism among con specifics; and maternal quence variation across a broader range transmission ofmtDNA to progeny. Em-of the species. At this macrogeographic pirical and conceptual reservations apply level, is the evolutionary divergence in to some of these generalities. For ex-mtDNA, reflecting matriarchal phylogample, low frequency mtDNA variants eny, concordant with the subspecies diswithin an individual would normally es-tributions defined by morphology and by cape empirical detection, and, given the allozymes encoded in the nuclear geubiquity of between-individual sequence nome? differences, it would seem that at least MATERIALS AND METHODS some transient mtDNA heteroplasmicity (perhaps in germ cell lineages) is ineviTaxa Examined table (see Olivo et al., 1983). Also, the Two subspecies of bluegill, originally consequential possibility remains that described by morphologic criteria, are some mtDNA molecules are successfully native to the southeastern United States transmitted to progeny from the male (Hubbs and Allen, 1944; Miller and parent (paternal leakage; but see Lans-Winn, 1951). Lepomis macrochirus purman et al., 1983).purescens, abundant in peninsular FlorThe main purpose of this study is to ida and Atlantic coastal streams, differs begin the characterization of mtDNA slightly in quantitative morphologic and polymorphism in another class of ver-physiologic features from L. m. macrotebrates-the fishes. Our approach has chirus, the bluegill inhabiting the Missisbeen to map mtDNA restriction site vari-sippi and other Gulfdrainages east to the ation in the bluegill sunfish (Lepomis Chattahoochee River in Georgia (Hubbs macrochirus;Centrarchidae), using a large and Lagler, 1958). A recent protein-elecnumber of restriction endo...

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The heterogeneity of mitochondrial DNA in different tissues from the same animal

Cited by 21 publications

References 14 publications

Mitochondrial DNA heteroplasmy in Drosophila mauritiana.

Mitochondrial DNA heteroplasmy in Drosophila mauritiana.

Models of mitochondrial DNA transmission genetics and evolution in higher eucaryotes

CHARACTERIZATION OF MITOCHONDRIAL DNA VARIABILITY IN A HYBRID SWARM BETWEEN SUBSPECIES OF BLUEGILL SUNFISH ( LEPOMIS MACROCHIRUS )

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