<scp>MSH</scp>1 maintains organelle genome stability and genetically interacts with <scp>RECA</scp> and <scp>RECG</scp> in the moss Physcomitrella patens

Odahara, Masaki; Kishita, Yoshihito; Sekine, Yoshiaki

doi:10.1111/tpj.13573

Cited by 29 publications

(51 citation statements)

References 33 publications

(65 reference statements)

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“…Sandhu et al (2007) showed that modulation of MSH1 expression by RNA interference results in heritable CMS in tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum) plants. Our results here showed that RECX OEX led to higher induction of recombination in mtDNA than occurred upon MSH1 mutation in P. patens (Odahara et al, 2017). RECX OEX, which should be easier than RNA interference, may be another way to induce CMS in angiosperms.…”

Section: Discussionmentioning

confidence: 63%

“…The eFP expression profiles of RECX and other genes involved in the maintenance of organelle genome stability revealed a positive relationship between their expression, except for RECA2. RECG, MSH1A, MSH1B, and RECX function in both chloroplasts and mitochondria (Odahara et al, 2015b(Odahara et al, , 2017, but their gene expression increased with the increasing expression of mitochondrial RECA1 rather than chloroplast RECA2. Given that the effects of RECG, MSH1B, or RECX KO were more prominent in mtDNA than in cpDNA (Odahara et al, 2015b(Odahara et al, , 2017, this stronger relationship with mitochondrial RECA1 Figure 6.…”

Section: Discussionmentioning

confidence: 96%

“…However, MSH1 double and MSH1B single mutants exhibit organelle genome instability due to recombination between SDRs. Double mutation analysis showed that MSH1B interacts genetically with the HRR factors RECA2 and RECG in chloroplasts, and with RECG in mitochondria, to suppress recombination between SDRs (Odahara et al, 2017).…”

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RECX Interacts with Mitochondrial RECA to Maintain Mitochondrial Genome Stability

Odahara

Sekine

2018

Plant Physiol.

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The chloroplast and mitochondrial genomes are essential for photosynthesis and respiration, respectively. RECA and RECG, which are plant-specific homologs of the bacterial homologous recombination repair proteins RecA and RecG, maintain organelle genome stability by suppressing aberrant recombination between short dispersed repeats (SDRs) in the moss In this study, we analyzed the plant-specific factor RECX, a homolog of bacterial RecX that regulates RecA. RECX fused to GFP colocalized with mitochondrial RECA1 and chloroplast RECA2 on mitochondrial and chloroplast nucleoids, respectively. Knockout (KO) and overexpression (OEX) of did not alter the morphological phenotype. Analysis of mitochondrial DNA, however, showed that products from recombination between SDRs increased significantly in OEX mitochondria and modestly in KO mitochondria. By contrast, analysis of chloroplast DNA revealed no substantial alteration in the number of products from recombination between SDRs in KO and OEX chloroplasts. Yeast two-hybrid analysis revealed interactions between RECX and RECA1 and between RECX and RECA2. Expression profiles showed a positive correlation between and factors maintaining the stability of both organelle genomes and Collectively, these results suggest that RECX maintains mitochondrial genome stability, likely by modulating RECA1 activity, and that the compromised function of RECX induces mitochondrial genome instability.

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Section: Discussionmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 96%

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RECX Interacts with Mitochondrial RECA to Maintain Mitochondrial Genome Stability

Odahara

Sekine

2018

Plant Physiol.

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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).…”

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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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“…Nuclear genomes of P. patens and other plant species encode several homologs of bacterial HRR factors, although some homologs have not been identified in the genomes of P. patens and other plant species, on the basis of sequence similarity. [25] RecA is a key factor in HRR, as it binds to single-stranded DNA (ssDNA) and identifies homologous sequences to perform strand exchange between them [27]. Nuclear DNA of P. patens encodes two types of RecA homologs, RECA1 and RECA2, which show moderate sequence similarity.…”

Section: Plant Homologs Of Bacterial Proteins and Their Localizationmentioning

confidence: 99%

Factors Affecting Organelle Genome Stability in Physcomitrella patens

Odahara

2020

Plants

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Organelle genomes are essential for plants; however, the mechanisms underlying the maintenance of organelle genomes are incompletely understood. Using the basal land plant Physcomitrella patens as a model, nuclear-encoded homologs of bacterial-type homologous recombination repair (HRR) factors have been shown to play an important role in the maintenance of organelle genome stability by suppressing recombination between short dispersed repeats. In this review, I summarize the factors and pathways involved in the maintenance of genome stability, as well as the repeats that cause genomic instability in organelles in P. patens, and compare them with findings in other plant species. I also discuss the relationship between HRR factors and organelle genome structure from the evolutionary standpoint.

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MSH1 maintains organelle genome stability and genetically interacts with RECA and RECG in the moss Physcomitrella patens

Cited by 29 publications

References 33 publications

RECX Interacts with Mitochondrial RECA to Maintain Mitochondrial Genome Stability

RECX Interacts with Mitochondrial RECA to Maintain Mitochondrial Genome Stability

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

Factors Affecting Organelle Genome Stability in Physcomitrella patens

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