Plant mitochondrial genome evolution can be explained by DNA repair mechanisms

Abstract

Plant mitochondrial genomes are notorious for their large and variable size, nonconserved open reading frames of unknown function, and high rates of rearrangement. Paradoxically, the mutation rates are very low. However, mutation rates can only be measured in sequences that can be aligned--a very small part of plant mitochondrial genomes. Comparison of the complete mitochondrial genome sequences of two ecotypes of Arabidopsis thaliana allows the alignment of noncoding as well as coding DNA and estimation of the mutation rates in both. A recent chimeric duplication is also analyzed. A hypothesis is proposed that the mechanisms of plant mitochondrial DNA repair account for these features and includes different mechanisms in transcribed and nontranscribed regions. Within genes, a bias toward gene conversion would keep measured mutation rates low, whereas in noncoding regions, break-induced replication (BIR) explains the expansion and rearrangements. Both processes are types of double-strand break repair, but enhanced second-strand capture in transcribed regions versus BIR in nontranscribed regions can explain the two seemingly contradictory features of plant mitochondrial genome evolution--the low mutation rates in genes and the striking expansions of noncoding sequences.

Keywords: Arabidopsis; DNA repair; mitochondrial genome; mutation rate.

Fig. 1.—

Repeats H1, H2, and H3. (A) Diagram of the Col-0 genome with a few genes indicated as landmarks and showing the 1.8 kb insertion and other copies of its repeats. (B) Alignment of repeats H1, H2, and H3. Mutations are indicated in red, and boxes surround the likely origins of the H3 sequence.

Fig. 2.—

Model of two types of DNA repair. The blue and red lines indicate different sequences. (A) The consequences of coordination of both ends following a break. (B) The consequences of invasion of a single DNA end, which ultimately leads to genome expansions. Invasion occurs at an ectopic site due to a small region of homology.