Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence.

We examined the tempo and mode of mitochondrial DNA (mtDNA) evolution in six species of crucifers from two genera, Brassica and Raphanus. 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.

Unusual structure of geranium chloroplast DNA: A triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families.

Physical and gene mapping studies reveal that chloroplast DNA from geranium (Pelargonium hortorum) has sustained a number of extensive duplications and inversions, resulting in a genome arrangement radically unlike that of other plants. At 217 kilobases in size, the circular chromosome is about 50% larger than the typical land plant chloroplast genome and is by far the largest described to date, to our knowledge. Most of this extra size can be accounted for by a 76-kilobase inverted duplication, three times larger than the normal chloroplast DNA inverted repeat. This tripling has occurred primarily by spreading of the inverted repeat into regions that are single copy in all other chloroplast genomes. Consequently, 10 protein genes that are present only once in all other land plants are duplicated in geranium. At least six inversions, occurring in both the inverted repeat and large single-copy region, must be postulated to account for all of the gene order differences that distinguish the geranium genome from other chloroplast genomes. We report the existence in geranium of two families of short dispersed repeats and hypothesize that recombination between repeats may be the major cause of inversions in geranium chloroplast DNA.

Unicircular structure of the Brassica hirta mitochondrial genome.

Restriction mapping studies reveal that the mitochondrial genome of white mustard (Brassica hirta) exists in the form of a single circular 208 kb chromosome. The B. hirta genome has only one copy of the two sequences which, in several related Brassica species, are duplicated and undergo intramolecular recombination. This first report of a plant mitochondrial DNA that does not exist in a multipartite structure indicates that high frequency intramolecular recombination is not an obligatory feature of plant mitochondrial genomes. Heterologous filter hybridizations reveal that the mitochondrial genomes of B. hirta and B. campestris have diverged radically in sequence arrangement, as the result of approximately 10 large inversions. At the same time, however, the two genomes are similar in size, sequence content, and primary sequence.

Tricircular mitochondrial genomes of Brassica and Raphanus: reversal of repeat configurations by inversion.

We constructed complete physical maps of the tripartite mitochondrial genomes of two Crucifers, Brassica nigra (black mustard) and Raphanus sativa (radish). Both genomes contain two copies of a direct repeat engaged in intragenomic recombination. The outcome of this recombination in black mustard is to interconvert a 231 kb master chromosome with two subgenomic circles of 135 kb and 96 kb. In radish, a 242 kb master chromosome interconverts with subgenomic circles of 139 kb and 103 kb. The recombination repeats are 7 kb in size in black mustard and 10 kb in radish, and are nearly identical except for two insertions in the radish repeat relative to the black mustard one. The two repeat configurations present on the master chromosome of black mustard are located on the subgenomes of radish and vice-versa. To explain this, we postulate the existence of an evolutionarily intermediate mitochondrial genome in which the recombination repeats were (are) present in an inverted orientation. The recombination repeats described for these two species are completely different from those previously found in the closely related species B. campestris, implying that such repeats are created and lost frequently in plant mitochondrial DNAs and making it less than likely that recombination occurs in a site-specific manner.