DNA Repair and the Stability of the Plant Mitochondrial Genome.

Nicolas Chevigny,José Manuel Gualberto,Frédérique Lotfi,Déborah Schatz-Daas

doi:10.3390/ijms21010328

Abstract

The mitochondrion stands at the center of cell energy metabolism. It contains its own genome, the mtDNA, that is a relic of its prokaryotic symbiotic ancestor. In plants, the mitochondrial genetic information influences important agronomic traits including fertility, plant vigor, chloroplast function, and cross-compatibility. Plant mtDNA has remarkable characteristics: It is much larger than the mtDNA of other eukaryotes and evolves very rapidly in structure. This is because of recombination activities that generate alternative mtDNA configurations, an important reservoir of genetic diversity that promotes rapid mtDNA evolution. On the other hand, the high incidence of ectopic recombination leads to mtDNA instability and the expression of gene chimeras, with potential deleterious effects. In contrast to the structural plasticity of the genome, in most plant species the mtDNA coding sequences evolve very slowly, even if the organization of the genome is highly variable. Repair mechanisms are probably responsible for such low mutation rates, in particular repair by homologous recombination. Herein we review some of the characteristics of plant organellar genomes and of the repair pathways found in plant mitochondria. We further discuss how homologous recombination is involved in the evolution of the plant mtDNA.

Highlights

The mitochondrion stands at the center of cell energy metabolism
Simpler organisms can have a higher number of mitochondrial genes, with the notable example of the protist Reclinomonas americana that has a 69-kb mtDNA coding for about 100 genes [13]
We focus on those better studied that have unequivocally been demonstrated to be present in plant mitochondria, which are base excision repair (BER) and homologous recombination (HR)

Summary

Structure of Plant Organellar Genomes

The mitochondrial as well as the chloroplast genomes are packaged in nucleoprotein complexes called nucleoids, similar to those of bacterial chromosomes [28,29]. In contrast to the recombination involving large repeats, the ectopic recombination between intermediate-size repeats and microhomologies is infrequent, usually asymmetric, and not reversible [1,54,55] These rare recombination events contribute to the heteroplasmic state of the mtDNA, and are responsible for the different populations of mtDNA, called sublimons, that can co-exist in the same individual, often less than one copy per cell [54,56]. The available data suggest that plant mtDNA is divided into several subgenomic molecules obtained by recombination events, dispersed in the different mitochondria of a cell according to their fusion and fission How such a collection of linear or circular subgenomes replicates is still not understood. The degradation of organellar DNA by exonucleases could be a mean for rapid access to phosphate when plants are exposed to nutrient-deficient conditions [72]

Repair Mechanisms in the Mitochondria of Plants

Direct Repair

Recombination Pathways in Plant Mitochondria

Findings

HR Pathways and the Evolution of the Plant mtDNA