The plant mitochondrial genome: Dynamics and maintenance

Gualberto, José M.; Mileshina, Daria; Wallet, Clémentine; Niazi, Adnan; Weber-Lotfi, Frédérique; Dietrich, André

doi:10.1016/j.biochi.2013.09.016

Cited by 287 publications

(248 citation statements)

References 146 publications

Supporting

Mentioning

240

Contrasting

Unclassified

Order By: Relevance

“…The explanation must therefore be a combination of the available DNA repair pathways and selection on the DNA postrepair. Plant mitochondria have a short-patch base-excision repair system, at least for removal of uracil (Boesch et al 2009), but there is no evidence for long-patch base-excision repair or nucleotide-excision repair (Gualberto et al 2013). Genome evolution and the rearrangements seen in mutants suggest that DSB repair is an important process in plant mitochondria (Shedge et al 2007; Arrieta-Montiel et al 2009; Davila et al 2011; Janicka et al 2012; Miller-Messmer et al 2012; Christensen 2013).…”

Section: Discussionmentioning

confidence: 99%

Genes and Junk in Plant Mitochondria—Repair Mechanisms and Selection

Christensen

2014

Genome Biology and Evolution

113

View full text Add to dashboard Cite

Plant mitochondrial genomes have very low mutation rates. In contrast, they also rearrange and expand frequently. This is easily understood if DNA repair in genes is accomplished by accurate mechanisms, whereas less accurate mechanisms including nonhomologous end joining or break-induced replication are used in nongenes. An important question is how different mechanisms of repair predominate in coding and noncoding DNA, although one possible mechanism is transcription-coupled repair (TCR). This work tests the predictions of TCR and finds no support for it. Examination of the mutation spectra and rates in genes and junk reveals what DNA repair mechanisms are available to plant mitochondria, and what selective forces act on the repair products. A model is proposed that mismatches and other DNA damages are repaired by converting them into double-strand breaks (DSBs). These can then be repaired by any of the DSB repair mechanisms, both accurate and inaccurate. Natural selection will eliminate coding regions repaired by inaccurate mechanisms, accounting for the low mutation rates in genes, whereas mutations, rearrangements, and expansions generated by inaccurate repair in noncoding regions will persist. Support for this model includes the structure of the mitochondrial mutS homolog in plants, which is fused to a double-strand endonuclease. The model proposes that plant mitochondria do not distinguish a damaged or mismatched DNA strand from the undamaged strand, they simply cut both strands and perform homology-based DSB repair. This plant-specific strategy for protecting future generations from mitochondrial DNA damage has the side effect of genome expansions and rearrangements.

show abstract

Section: Discussionmentioning

confidence: 99%

Genes and Junk in Plant Mitochondria—Repair Mechanisms and Selection

Christensen

2014

Genome Biology and Evolution

113

View full text Add to dashboard Cite

show abstract

“…As to the shuffling of mtDNA sequences, it is promoted by the numerous repeated sequences present in plant mitochondrial genomes and involves (1) frequent homologous recombination (HR) via large repeated sequences, (2) ectopic recombination involving intermediate-size repeats (IRs), or (3) illegitimate recombination involving sequence microhomologies Gualberto et al, 2014). These recombination activities contribute to the intrinsic heteroplasmic state of plant mitochondrial genomes, in which alternative mitotypes coexist with the predominant mtDNA at substoichiometric levels (Small et al, 1989;Kmiec et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

The RECG1 DNA Translocase Is a Key Factor in Recombination Surveillance, Repair, and Segregation of the Mitochondrial DNA in Arabidopsis

et al. 2015

Self Cite

View full text Add to dashboard Cite

The mitochondria of flowering plants have considerably larger and more complex genomes than the mitochondria of animals or fungi, mostly due to recombination activities that modulate their genomic structures. These activities most probably participate in the repair of mitochondrial DNA (mtDNA) lesions by recombination-dependent processes. Rare ectopic recombination across short repeats generates new genomic configurations that contribute to mtDNA heteroplasmy, which drives rapid evolution of the sequence organization of plant mtDNAs. We found that Arabidopsis thaliana RECG1, an ortholog of the bacterial RecG translocase, is an organellar protein with multiple roles in mtDNA maintenance. RECG1 targets to mitochondria and plastids and can complement a bacterial recG mutant that shows defects in repair and replication control. Characterization of Arabidopsis recG1 mutants showed that RECG1 is required for recombination-dependent repair and for suppression of ectopic recombination in mitochondria, most likely because of its role in recovery of stalled replication forks. The analysis of alternative mitotypes present in a recG1 line and of their segregation following backcross allowed us to build a model to explain how a new stable mtDNA configuration, compatible with normal plant development, can be generated by stoichiometric shift.

show abstract

“…The origin of these repeats is often unclear, as are the mechanisms that underlie the propensity for mitogenomes to acquire repetitive sequences. From the >60 sequenced mitogenomes (Mower et al, 2012b;Gualberto et al, 2014;Liu et al, 2014), it is clear that plant mitogenomes vary widely in repeat content and composition, which, in conjunction with the phylogenetically widespread occurrence of large mitogenomes, lend support to the idea that multiple divergent repeated sequences are acquired independently during evolution (Andre et al, 1992). Consequently, as the presence of repeated sequences is associated with recombination in the mitogenome (Manchekar et al, 2006;Kitazaki and Kubo, 2010;Chen et al, 2017), the high structural variability (Ogihara et al, 2005), complexity, and multipartite organization of plant mtDNA (Abdelnoor et al, 2003) should come as little surprise.…”

Section: Characteristics Of Plant Mitochondrialmentioning

confidence: 99%