The GIY‐YIG endonuclease domain of <i>Arabidopsis</i> MutS homolog 1 specifically binds to branched DNA structures

Fukui, Kenji; Harada, Akira; Wakamatsu, Taisuke; Minobe, Ai; Ohshita, Koki; Ashiuchi, Makoto; Yano, Takayuki

doi:10.1002/1873-3468.13279

Cited by 21 publications

(20 citation statements)

References 48 publications

(68 reference statements)

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“…We identified a putative mitochondrion-targeted MSH1 homologue in O. quekettii. MSH1 encodes a protein with six conserved domains (Kowalski et al, 1999) including domain VI, a GIY-YIG homing endonuclease, which is predicted to be responsible for specific DNA-binding and suppression of homologous recombination (Fukui et al, 2018) and is specific to only the plant form of the protein (Abdelnoor et al, 2006;Shedge et al, 2007). Domain VI is absent from nuclear localised homologues in plants (MSH2-MSH6) and from the yeast MSH1 protein (Abdelnoor et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns

Repetti

Jackson

Judd

et al. 2020

PeerJ

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Within the siphonous green algal order Bryopsidales, the size and gene arrangement of chloroplast genomes has been examined extensively, while mitochondrial genomes have been mostly overlooked. The recently published mitochondrial genome of Caulerpa lentillifera is large with expanded noncoding DNA, but it remains unclear if this is characteristic of the entire order. Our study aims to evaluate the evolutionary forces shaping organelle genome dynamics in the Bryopsidales based on the C. lentillifera and Ostreobium quekettii mitochondrial genomes. In this study, the mitochondrial genome of O. quekettii was characterised using a combination of long and short read sequencing, and bioinformatic tools for annotation and sequence analyses. We compared the mitochondrial and chloroplast genomes of O. quekettii and C. lentillifera to examine hypotheses related to genome evolution. The O. quekettii mitochondrial genome is the largest green algal mitochondrial genome sequenced (241,739 bp), considerably larger than its chloroplast genome. As with the mtDNA of C. lentillifera, most of this excess size is from the expansion of intergenic DNA and proliferation of introns. Inflated mitochondrial genomes in the Bryopsidales suggest effective population size, recombination and/or mutation rate, influenced by nuclear-encoded proteins, differ between the genomes of mitochondria and chloroplasts, reducing the strength of selection to influence evolution of their mitochondrial genomes.

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Section: Discussionmentioning

confidence: 99%

The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns

Repetti

Jackson

Judd

et al. 2020

PeerJ

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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).…”

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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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“…quekettii. MSH1 encodes a protein with six conserved domains (Kowalski et al, 1999) including Manuscript to be reviewed domain VI, a GIY-YIG homing endonuclease, which is predicted to be responsible for specific DNA-binding and suppression of homologous recombination (Fukui et al, 2018) and is specific to only the plant form of the protein (Abdelnoor et al, 2006;Shedge et al, 2007). Domain VI is absent from nuclear localized homologues in plants (MSH2-MSH6) and from the yeast MSH1 protein (Abdelnoor et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Peer Review #1 of "The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns (v0.1)"

Neustupa¹

2020

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Within the siphonous green algal order Bryopsidales, the size and gene arrangement of chloroplast genomes has been examined extensively, while mitochondrial genomes have been mostly overlooked. The recently published mitochondrial genome of Caulerpa lentillifera is large with expanded noncoding DNA, but it remains unclear if this is characteristic of the entire order. Our study aims to evaluate the evolutionary forces shaping organelle genome dynamics in the Bryopsidales based on the C. lentillifera and Ostreobium quekettii mitochondrial genomes. In this study, the mitochondrial genome of O. quekettii was characterised using a combination of long and short read sequencing, and bioinformatic tools for annotation and sequence analyses. We compared the mitochondrial and chloroplast genomes of O. quekettii and C. lentillifera to examine hypotheses related to genome evolution. The O. quekettii mitochondrial genome is the largest green algal mitochondrial genome sequenced (241,739bp), considerably larger than its chloroplast genome. As with the mtDNA of C. lentillifera, most of this excess size is from the expansion of intergenic DNA and proliferation of introns. Inflated mitochondrial genomes in the Bryopsidales suggest effective population size, recombination and/or mutation rate, influenced by nuclear-encoded proteins, differ between the genomes of mitochondria and chloroplasts, reducing the strength of selection to influence evolution of their mitochondrial genomes.

show abstract

The GIY‐YIG endonuclease domain of Arabidopsis MutS homolog 1 specifically binds to branched DNA structures

Cited by 21 publications

References 48 publications

The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns

The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns

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

Peer Review #1 of "The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns (v0.1)"

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