DNA Repair and the Stability of the Plant Mitochondrial Genome

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.

MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes

“…mitochondrial and nuclear DNA, as evidenced by increased oxidative damage in the double mutant damaged bases in plant cytoplasmic genomes (9,(14)(15)(16)(17). In both mitochondria and plastids, there is often above 10 -3 errors per bp and much worse in certain sequence contexts (35) -setting a problematic noise threshold for accurate detection of rare variants.…”

Siberian larch (Larix sibirica Ledeb.) mitochondrial genome assembled using both short and long nucleotide sequence reads is currently the largest known mitogenome

“…Such dispersion may be explained by the abundance of noncoding and repeated elements [ 6 ]. In contrast to the relatively compact and tightly packed genomes of most animal mitochondria (~ 15–20 Kbp) [ 7 ], plant mitogenomes are enriched with introns, intergenic sequences, repetitive and mobile elements [ 8 ], and show a wide diversity in gene content and genomic architecture [ 9 , 10 ], although coding sequences are relatively conserved in the core mitochondrial genes [ 11 – 13 ].…”

The Dark Side of UV-Induced DNA Lesion Repair

“…Up to date, the presence of NER, an indisputably essential element of the nuclear DNA repair machinery in eukaryotes, has been reported neither in plant chloroplasts nor in the mitochondria [96].…”

“…Plants have been shown to possess homologs of proteins assigned to the BER pathway in animal and yeast cells. The currently available data indicate that in addition to nucleus, BER operates also in plant mitochondria and chloroplasts [96,113]. Activity of UNG (uracil DNA glycosylase), engaged in BER of uracil, a product of cytosine deamination, was observed in maize nuclear fraction and mitochondria of Arabidopsis, maize and potato [114][115][116].…”

“…This suggests predominant role of recombination-dependent processes in the repair of DSBs in mitochondria and chloroplasts (for a review of DNA repair in plant mitochondria and chloroplasts see: [96]). Based on the functions, plant homologs of bacterial proteins involved in HR can be classified into different groups including DNA protection (AtSSB1-single-stranded binding protein1, AtSSB2), loading of the recombinase (AtODB1-organellar DNA-binding protein1, AtWHY2-Whirly 2, AtOSB1-organellar single-stranded DNA binding protein1, AtOSB2, AtOSB3), formation of the synapsis (AtRECA2-RECA homolog2, AtRECA3), recombination regulation (AtRECX-RECX homolog, AtMSH1), branch migration (AtRADA-RADA-like protein, AtRECG1-ATP-dependent DNA helicase homolog RECG1), DNA synthesis and ligation (AtPOL IB, AtLIG1) [96,216,217]. Involvement of mechanisms similar to MMEJ and NHEJ in repair of DSBs in chloroplasts was also documented [218,219].…”