Plant mitochondrial DNA evolved rapidly in structure, but slowly in sequence

SummaryWe examined the tempo and mode of mitochondrial DNA (mtDNA) evolution in six species of crucifers from two genera,Brassica andRaphanus. The six mtDNAs have undergone numerous internal rearrangements and therefore differ dramatically with respect to the sizes of their subgenomic circular chromosomes. Between 3 and 14 inversions must be postulated to account for the structural differences found between any two species. In contrast, these mtDNAs are extremely similar in primary sequence, differing at only 1–8 out of every 1000 bp. The point mutation rate in these plant mtDNAs is roughly 4 times slower than in land plant chloroplast DNA (cpDNA) and 100 times slower than in animal mtDNA. Conversely, the rate of rearrangements is extraordinarily faster in plant mtDNA than in cpDNA and animal mtDNA.

[1]  J. Broach The yeast plasmid 2 mu circle. , 1982, Cell.

[2]  R. Kolodner,et al.  Physicochemical characterization of mitochondrial DNA from pea leaves. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[3]  G. Zurawski Evolution of Higher-Plant Chloroplast DNA-Encoded Genes: Implications for Structure-Function and Phylogenetic Studies , 1987 .

[4]  M. Stoneking,et al.  Mitochondrial DNA and two perspectives on evolutionary genetics , 1985 .

[5]  R. Sederoff,et al.  Evolution of DNA sequence organization in mitochondrial genomes of Zea. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Palmer,et al.  Physical and gene organization of mitochondrial DNA in fertile and male sterile sunflower. CMS-associated alterations in structure and transcription of the atpA gene. , 1988, Nucleic acids research.

[7]  J. Palmer,et al.  Tricircular mitochondrial genomes of Brassica and Raphanus: reversal of repeat configurations by inversion. , 1986, Nucleic acids research.

[8]  J. Palmer,et al.  Recombination sequences in plant mitochondrial genomes: diversity and homologies to known mitochondrial genes. , 1984, Nucleic acids research.

[9]  A. J. Bendich,et al.  The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae) , 1981, Cell.

[10]  J. Palmer,et al.  Chloroplast DNA evolution and the origin of amphidiploid Brassica species , 1983, Theoretical and Applied Genetics.

[11]  D. Clayton Transcription of the mammalian mitochondrial genome. , 1984, Annual review of biochemistry.

[12]  J. Palmer,et al.  Comparative organization of chloroplast genomes. , 1985, Annual review of genetics.

[13]  J. Palmer,et al.  Evolution of Chloroplast and Mitochondrial DNA in Plants and Algae , 1985 .

[14]  C. S. Levings,et al.  Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the texas male-sterile cytoplasm , 1986, Cell.

[15]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[16]  J. Palmer,et al.  Intraspecific variation and multicircularity in Brassica mitochondrial DNAs. , 1988, Genetics.

[17]  C. S. Levings,et al.  Comparison of the mitochondrial genome of Nicotiana tabacum with its progenitor species , 1985, Theoretical and Applied Genetics.

[18]  W. Brown The Mitochondrial Genome of Animals , 1985 .

[19]  W. Brown,et al.  Rapid evolution of animal mitochondrial DNA. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Palmer,et al.  An unusual mitochondrial DNA plasmid in the genus Brassica , 1983, Nature.

[21]  C. S. Levings The plant mitochondrial genome and its mutants , 1983, Cell.

[22]  D. Pring,et al.  Molecular Biology of Higher Plant Mitochondrial DNA , 1985 .

[23]  C. Mathieu,et al.  Physical and gene mapping of cauliflower (Brassica oleracea) mitochondrial DNA , 1984, Current Genetics.

[24]  M. Hanson,et al.  Mitochondrial DNA Sequence Divergence among Lycopersicon and Related Solanum Species. , 1986, Genetics.

[25]  W. Brown,et al.  EVOLUTION OF ANIMAL MITOCHONDRIAL DNA: RELEVANCE FOR POPULATION BIOLOGY AND SYSTEMATICS , 1987 .

[26]  C. Schardl,et al.  Mitochondrial DNA rearrangements associated with fertile revertants of S-type male-sterile maize , 1985, Cell.

[27]  J. Broach The yeast plasmid 2μ circle , 1982, Cell.

[28]  C. S. Levings,et al.  The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein , 1986, Molecular and General Genetics MGG.

[29]  P. Lebacq,et al.  Sal 1 restriction enzyme analysis of chloroplast and mitochondrial DNAs in the genus Brassica , 1981 .

[30]  J. Palmer,et al.  Tripartite structure of the Brassica campestris mitochondrial genome , 1984, Nature.

[31]  W. Brown,et al.  Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Allan C. Wilson,et al.  Mitochondrial DNA sequences of primates: Tempo and mode of evolution , 2005, Journal of Molecular Evolution.

[33]  J. Bailey-Serres,et al.  Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum , 1986, Cell.

[34]  M. Hanson,et al.  A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated , 1987, Cell.

[35]  Jeffrey D. Palmer,et al.  Unicircular structure of the Brassica hirta mitochondrial genome , 2004, Current Genetics.

[36]  Molecular botany: Wonders of chloroplast DNA , 1986, Nature.

[37]  J. Palmer,et al.  Isolation and structural analysis of chloroplast DNA , 1986 .

[38]  M. Clegg,et al.  The Nature of Nucleotide Sequence Divergence between Barley and Maize Chloroplast DNA. , 1984, Genetics.

[39]  R. Sederoff Molecular Mechanisms of Mitochondrial-Genome Evolution in Higher Plants , 1987, The American Naturalist.

[40]  Jeffrey D. Palmer,et al.  Extensive mitochondrial specific transcription of the Brassica campestris mitochondrial genome , 1987, Nucleic Acids Res..