Factors Affecting Organelle Genome Stability in Physcomitrella patens

Odahara, Masaki

doi:10.3390/plants9020145

Cited by 9 publications

(7 citation statements)

References 50 publications

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“…Instead, characterization of cytoplasmic genomes in these mutants has revealed structural rearrangements resulting from ectopic recombination between small repeats (16,28,29,32). These findings have led to the prevailing view that the primary role of MSH1 is in recombination surveillance rather than in correction of mismatches or damaged bases (28,30,(33)(34)(35)(36), as is the case for some other members of the mutS gene family (37). Numerous other genes have also been identified as playing a role in mitochondrial and plastid recombination (21).…”

Section: Significancementioning

confidence: 99%

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

Waneka

Broz

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

116

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Mitochondrial and plastid genomes in land plants exhibit some of the slowest rates of sequence evolution observed in any eukaryotic genome, suggesting an exceptional ability to prevent or correct mutations. However, the mechanisms responsible for this extreme fidelity remain unclear. We tested seven candidate genes involved in cytoplasmic DNA replication, recombination, and repair (POLIA,POLIB,MSH1,RECA3,UNG,FPG, andOGG1) for effects on mutation rates in the model angiospermArabidopsis thalianaby applying a highly accurate DNA sequencing technique (duplex sequencing) that can detect newly arisen mitochondrial and plastid mutations even at low heteroplasmic frequencies. We find that disruptingMSH1(but not the other candidate genes) leads to massive increases in the frequency of point mutations and small indels and changes to the mutation spectrum in mitochondrial and plastid DNA. We also used droplet digital PCR to show transmission of de novo heteroplasmies across generations inmsh1mutants, confirming a contribution to heritable mutation rates. This dual-targeted gene is part of an enigmatic lineage within themutSmismatch repair family that we find is also present outside of green plants in multiple eukaryotic groups (stramenopiles, alveolates, haptophytes, and cryptomonads), as well as certain bacteria and viruses.MSH1has previously been shown to limit ectopic recombination in plant cytoplasmic genomes. Our results point to a broader role in recognition and correction of errors in plant mitochondrial and plastid DNA sequence, leading to greatly suppressed mutation rates perhaps via initiation of double-stranded breaks and repair pathways based on faithful homologous recombination.

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Section: Significancementioning

confidence: 99%

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

Waneka

Broz

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

116

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“…Instead, characterization of cytoplasmic genomes in these mutants has revealed structural 76 rearrangements resulting from ectopic recombination between small repeats (24,25,28). These 77 findings have led to the prevailing view that the primary role of MSH1 is in recombination 78 surveillance rather than in correction of mismatches or damaged bases (24,26,(29)(30)(31)(32), as is the 79 case for some other members of the mutS gene family (33). Numerous other genes have also been 80 identified as playing a role in mitochondrial and plastid recombination (20).…”

mentioning

confidence: 99%

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

Waneka

Broz

et al. 2020

Preprint

101

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2Mitochondrial and plastid genomes in land plants exhibit some of the slowest rates of sequence 3 evolution observed in any eukaryotic genome, suggesting an exceptional ability to prevent or correct 4 mutations. However, the mechanisms responsible for this extreme fidelity remain unclear. We tested 5 seven candidate genes involved in cytoplasmic DNA replication, recombination, and repair (POLIA, 6 POLIB, MSH1, RECA3, UNG, FPG, and OGG1) for effects on mutation rates in the model 7 angiosperm Arabidopsis thaliana by applying a highly accurate DNA sequencing technique (duplex 8 sequencing) that can detect newly arisen mitochondrial and plastid mutations still at low 9 heteroplasmic frequencies. We find that disrupting MSH1 (but not the other candidate genes) leads 10 to massive increases in the frequency of point mutations and small indels and changes to the 11 mutation spectrum in mitochondrial and plastid DNA. We also used droplet digital PCR to show 12 transmission of de novo heteroplasmies across generations in msh1 mutants, confirming a 13 contribution to heritable mutation rates. This dual-targeted gene is part of an enigmatic lineage within 14 the mutS mismatch repair family that we find is also present outside of green plants in multiple 15 eukaryotic groups (stramenopiles, alveolates, haptophytes, and cryptomonads), as well as certain 16 bacteria and viruses. MSH1 has previously been shown to limit ectopic recombination in plant 17 cytoplasmic genomes. Our results point to a broader role in recognition and correction of errors in 18 plant mitochondrial and plastid DNA sequence, leading to greatly suppressed mutation rates 19 perhaps via initiation of double-stranded breaks and repair pathways based on faithful homologous 20 recombination.It has been apparent for more than 30 years that rates of nucleotide substitution in plant 24 mitochondrial and plastid genomes are unusually low (1,2). In angiosperms, mitochondrial and 25 plastid genomes have synonymous substitution rates that are on average approximately 16-fold and 26 5-fold slower than the nucleus, respectively (3). The fact that these low rates are evident even at 27 sites that are subject to relatively small amounts of purifying selection (4, 5) suggests that they are 28 the result of very low underlying mutation rates -a surprising observation especially when 29 contrasted with the rapid accumulation of mitochondrial mutations in many eukaryotic lineages (6,7). 30Although the genetic mechanisms that enable plants to achieve such faithful replication and 31 transmission of cytoplasmic DNA sequences have not been determined, a number of hypotheses 32 can be envisioned. One possibility is that the DNA polymerases responsible for replicating 33 mitochondrial and plastid DNA (8) might have unusually high fidelity. However, in vitro assays with 34 the two partially redundant bacterial-like organellar DNA polymerases in Arabidopsis thaliana, PolIA 35(At1g50840) and PolIB (At3g20540), have indicated that they are highly error-prone (9), with 36 misincorpo...

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“…This led to the conclusion that most damage to plant mitochondrial DNA is repaired by DSBR with further contribution by BER [4]. This implication of a major role for DSBR, which utilizes homologous DNA recombination, is supported by many studies that report the adverse effects of mutations in DNA recombination proteins on plant organelle integrity [1,3].…”

Section: Mechanisms For Plant Organelle Genome Replication and Repairmentioning

confidence: 96%

“…Plant organelle genomes, in particular those in mitochondria, contain repeat sequences that facilitate intramolecular recombination to generate various sub-genomic molecules. Recombination across these repeats, however, is regulated and suppressed by surveillance mechanisms including MSH1 and some Rec proteins [2,3]. MSH1 mutants in Psychomytrella show increased recombination across intermediate sized repeats relative to the wild-type [3].…”

Section: Mechanisms For Plant Organelle Genome Replication and Repairmentioning

confidence: 99%

Plant Organelle DNA Maintenance

Ahmad

Nielsen

2020

Plants

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Plant cells contain two double membrane bound organelles, plastids and mitochondria, that contain their own genomes. There is a very large variation in the sizes of mitochondrial genomes in higher plants, while the plastid genome remains relatively uniform across different species. One of the curious features of the organelle DNA is that it exists in a high copy number per mitochondria or chloroplast, which varies greatly in different tissues during plant development. The variations in copy number, morphology and genomic content reflect the diversity in organelle functions. The link between the metabolic needs of a cell and the capacity of mitochondria and chloroplasts to fulfill this demand is thought to act as a selective force on the number of organelles and genome copies per organelle. However, it is not yet clear how the activities of mitochondria and chloroplasts are coordinated in response to cellular and environmental cues. The relationship between genome copy number variation and the mechanism(s) by which the genomes are maintained through different developmental stages are yet to be fully understood. This Special Issue has several contributions that address current knowledge of higher plant organelle DNA. Here we briefly introduce these articles that discuss the importance of different aspects of the organelle genome in higher plants.

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Factors Affecting Organelle Genome Stability in Physcomitrella patens

Cited by 9 publications

References 50 publications

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

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

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

Plant Organelle DNA Maintenance

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