Can partial methylation explain the complex fragment patterns observed when plant mitochondrial DNA is cleaved with restriction endonucleases?

Bonen, Linda; Huh, T.Y.; Gray, Michael W.

doi:10.1016/0014-5793(80)80823-4

Cited by 28 publications

(12 citation statements)

References 26 publications

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“…In a variety of fungi, plants, and animals, the presence of methylated cytosine has been tested by paired restriction digests using isoschizomers that discriminate methylated and nonmethylated nucleotides. mtDNA from yeast, Neurospora, calf, rat, wheat, and muskmelon showed no difference between restriction patterns using these two enzymes (8,39,40). Our own results are consistent with the absence of methylation of mtDNA.…”

Section: Discussionsupporting

confidence: 81%

Evolution of DNA sequence organization in mitochondrial genomes of Zea

Sederoff¹,

Levings²,

Timothy³

et al. 1981

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

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Molecular mechanisms underlying the evolution of mtDNA in maize and three species of teosinte have been investigated. By using DNA transfer techniques and cloned fragments of maize mtDNA, changes in the position of homologous sequences in restriction digests were analyzed in related taxa. The resulting patterns indicate general conservation of sequence homology in all four species. One-third of the cloned fragments showed sequences conserved in homology and position of BamHI restriction fragments. Other fragments produced patterns indicating that extensive rearrangement of DNA sequences has taken place. In two cases, hybridization patterns revealed major changes in relative abundance of specific sequences that we believe are related to the molecular heterogeneity phenomenon of maize mtDNA. The evolution of mtDNA in these plants appears dramatically different from that in animal mtDNA, where base substitutions may account for most of the observed changes in restriction patterns.Evolution of higher plants must involve the distinct genomes of the nucleus, chloroplast, and mitochondrion. In the genus Zea, L., both organelle genomes show strict maternal inheritance (1-3) that greatly restricts the sources of variation for evolution provided by sexual cycles and biparental inheritance.In contrast to animal mtDNA, which typically has a size of 10 megadaltons (MDal) per mitochondrial genome, plant mtDNA is far more complex (4-10)-e.g., the maize mitochondrial genome has been estimated to be 320 MDal (8). In addition to larger size, plant mtDNA is characterized by molecular heterogeneity (4-7) observed as classes ofcircular chromosomes that vary in size and relative abundance. To learn about the molecular events that have occurred in the evolution of these unusual DNAs, we have directed our attention to the mtDNAs of maize and its closest relatives, the teosintes.Restriction enzyme digests of organelle DNAs from several races of teosinte have been analyzed previously (9). Groupings based on restriction patterns approximate the biosystematic relationships of the taxa. Perennial teosinte, Z. perennis (Hitch) Reeves and Manglesdorf, is the only tetraploid in the genus (2n = 40). Race Guatemala, Z. luxurians (Durieu and Ascherson) Bird, an annual diploid (2n = 20), is genetically the most distinct from maize. Another annual diploid race, Central Plateau, Zea mays ssp. mexicana (Schrader) Iltis, has close affinities to maize (11). Hybridization of teosinte and maize accompanied by introgression and differentiation has modified Zea populations to various degrees (11,12). Central Plateau (CP) was selected as representative of many annual teosintes; Guatemala (Gu) and perennial (ZP) teosinte were selected because their mtDNAs are distinct from each other and each differs greatly from maize and other teosintes (9). Although organelle DNA variation within these taxa has been recognized (9), the range of variation is not addressed in this study.Restriction digests fractionated on agarose gels and visualized by fluorescent s...

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Section: Discussionsupporting

confidence: 81%

Evolution of DNA sequence organization in mitochondrial genomes of Zea

Sederoff¹,

Levings²,

Timothy³

et al. 1981

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

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“…Angiosperm genomes are extensively methylated at cytosine residues in both CpG dinucleotides and CpNpG trinucleotides (Shapiro 1976;Bonen et al 1980;Gruenbaum et al 1981a), whereas in vertebrate genomes, only CpG is extensively methylated (Sinsheimer 1955;Gruenbaum et al 1981b;Nyce et al 1986). …”

Section: Introductionmentioning

confidence: 99%

Methylation sites in angiosperm genes

1992

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The extent to which CpG dinucleotides were depleted in a large set of angiosperm genes was, on average, very similar to the extent of CpG depletion in total angiosperm genomic DNA and far less than the extent of CpG depletion in vertebrate genes. Gene sequences from Arabidopsis thaliana, a dicotyledonous species with relatively low levels of total 5-methylcytosine, were just as CpG depleted as the angiosperm genes in general. Furthermore, levels of TpG and CpA, the potential deamination mutation products of methylated CpG, were elevated in A. thaliana genes, supporting a high rate of deamination mutation as the cause of the CpG deficiency. Using a method that takes into account the dinucleotide frequencies within each sequence of interest, we calculated the expected frequencies of CpNpG trinucleotides, which are also highly methylated in angiosperm genomes. CpNpG trinucleotides were not extensively enriched or depleted in the angiosperm genes. Two hypotheses could account for our results. Differential depletion of CpG and CpNpG within angiosperm genes and differential depletion of CpG in angiosperm and vertebrate genes could arise from different efficiencies of mismatch repair or from different levels of cytosine methylation in the cell lineages that contribute to germ cells.

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“…However, studies involving both plants and animals have attributed restriction enzyme variations to differences in nucleotide sequence rather than in methylation [S, [33][34][35][36]. The majority of the clones used in this study hybridized with only a single band in the N digestion pattern; a result one would not expect if sequences were partially modified.…”

Section: Discussionmentioning

confidence: 94%

Organization of mitochondrial DNA in normal and texas male sterile cytoplasms of maize

1981

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Recombinant DNA and hybridization techniques have been used to compare the organization of mitochondrial DNA (mtDNA) from normal (N) and Texas male sterile (T) cytoplasms of maize. Bum H1 restriction fragments of normal mtDNA were cloned and used in molecular hybridizations against Southern blots of Bum H I digested N and T mtDNA. Fifteen of the 35 fragments were conserved in both N and T as indicated by hybridization to comigrating bands in their restriction patterns. Only three fragments produced autoradiographs whose differences could reasonably be attributed to single changes in the cleavage site of the enzyme while approximately half (17/35) of the clones resulted in more complicated differences between N and T. The autoradiographs produced by these 17 clones indicated multiple cleavage site changes and/or sequence rearrangements of the mtDNA. Patterns of six of these 17 clones indicated partial duplication of the sequence and two showed variation in the intensity of hybridization between N and T, which may be related to the molecular heterogeneity phenomenon found in maize mitochondrial genomes. The large proportion of changes observed between N and T rntDNA indicates that rearrangements may have played an important role in the evolution of the maize mitochondrial genome.

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Can partial methylation explain the complex fragment patterns observed when plant mitochondrial DNA is cleaved with restriction endonucleases?

Cited by 28 publications

References 26 publications

Evolution of DNA sequence organization in mitochondrial genomes of Zea

Evolution of DNA sequence organization in mitochondrial genomes of Zea

Methylation sites in angiosperm genes

Organization of mitochondrial DNA in normal and texas male sterile cytoplasms of maize

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