Complete sequence of a 641-kb insertion of mitochondrial DNA in the <i>Arabidopsis thaliana</i> nuclear genome

Fields, Peter D.; Waneka, Gus; Naish, Matthew; Schatz, Michael C.; Henderson, Ian; Sloan, Daniel B

doi:10.1101/2022.02.22.481460

Cited by 5 publications

(7 citation statements)

References 43 publications

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“…First, it was important to determine whether the msh1 mutant background altered the relative numbers of organellar genome copies. Second, numts (i.e., copies of mitochondrial DNA inserted into the nuclear genome) are known to be present in the Arabidopsis thaliana nuclear genome ( 102 – 104 ), and we wanted to correct for this in our heteroplasmy analysis.…”

Section: Methodsmentioning

confidence: 99%

“…For mitochondria, both primer sets amplify numts, so the values were adjusted based on the number of numt copies. The amplified regions of cox2 and rps12 are present at one and three numt copies, respectively, in the Arabidopsis nuclear genome ( 104 ). These values were subtracted from the calculated values of mitochondrial copies per genome before averaging to obtain a final value.…”

Section: Methodsmentioning

confidence: 99%

“…These values were subtracted from the calculated values of mitochondrial copies per genome before averaging to obtain a final value. Our mitochondrial SNVs of interest (mt91017 and mt334038) are both present in three copies in the Arabidopsis nuclear genome ( 104 ).…”

Section: Methodsmentioning

confidence: 99%

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Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Broz

Keene

Gyorfy

et al. 2022

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

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The fate of new mitochondrial and plastid mutations depends on their ability to persist and spread among the numerous organellar genome copies within a cell (heteroplasmy). The extent to which heteroplasmies are transmitted across generations or eliminated through genetic bottlenecks is not well understood in plants, in part because their low mutation rates make these variants so infrequent. Disruption of MutS Homolog 1 ( MSH1 ), a gene involved in plant organellar DNA repair, results in numerous de novo point mutations, which we used to quantitatively track the inheritance of single nucleotide variants in mitochondrial and plastid genomes in Arabidopsis . We found that heteroplasmic sorting (the fixation or loss of a variant) was rapid for both organelles, greatly exceeding rates observed in animals. In msh1 mutants, plastid variants sorted faster than those in mitochondria and were typically fixed or lost within a single generation. Effective transmission bottleneck sizes ( N ) for plastids and mitochondria were N ∼ 1 and 4, respectively. Restoring MSH1 function further increased the rate of heteroplasmic sorting in mitochondria ( N ∼ 1.3), potentially because of its hypothesized role in promoting gene conversion as a mechanism of DNA repair, which is expected to homogenize genome copies within a cell. Heteroplasmic sorting also favored GC base pairs. Therefore, recombinational repair and gene conversion in plant organellar genomes can potentially accelerate the elimination of heteroplasmies and bias the outcome of this sorting process.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Broz

Keene

Gyorfy

et al. 2022

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

View full text Add to dashboard Cite

show abstract

“…First, it was important to determine whether the msh1 mutant background altered the relative numbers of organellar genome copies. Secondly, numts (nuclear mitochondrial DNA, i.e., copies of mitochondrial DNA inserted into the nuclear genome) are known to be present in the A. thaliana nuclear genome [96][97][98] and we wanted to correct for this in our heteroplasmy analysis.…”

Section: Organellar Genome Copy Numbermentioning

confidence: 99%

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Broz

Keene

Gyorfy

et al. 2022

Preprint

Self Cite

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Because mitochondrial and plastid genomes exist at high cellular copy numbers, new mutations result in the co-occurrence of multiple alleles within a cell or individual, a phenomenon known as heteroplasmy. The extent to which heteroplasmies are transmitted across generations or eliminated through a sorting process involving successive genetic bottlenecks is not well understood in plants, in part because their low mutation rates make these variants so infrequent. We previously found that disruption of MutS Homolog 1 (MSH1), a nuclear gene involved in plant organellar DNA repair, results in numerous de novo point mutations, providing an unprecedented opportunity to explore the inheritance of these variants. Here, we used droplet digital PCR to quantitatively track the inheritance of single nucleotide variants (SNVs) in mitochondrial and plastid genomes of both wild-type Arabidopsis and msh1 mutants. We found that heteroplasmic sorting was rapid for both organelles, greatly exceeding the rates at which mitochondrial heteroplasmies are eliminated in animals. In msh1 mutants, plastid SNVs usually reached fixation or were lost within a single generation, indicating an effective transmission bottleneck size (N) of ~1. In contrast, mitochondrial heteroplasmies often persisted across generations but still exhibited a relatively narrow transmission bottleneck (N ≈ 4). Restoring MSH1 function in mitochondria increased the rate of heteroplasmic sorting (N ≈ 1.3), potentially due to its hypothesized role in promoting gene conversion as a mechanism of DNA repair, which is expected to homogenize genome copies within a cell. We also found that heteroplasmic sorting favored GC base pairs. Therefore, recombinational repair and gene conversion in plant organellar genomes may accelerate the elimination of heteroplasmies and bias the outcome of this sorting process.

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“…Considering the importance of epigenetic modifications in gene activity (Feng and Jacobsen 2011; Zhang, et al 2018) , the role of epigenetic silencing in the transcriptional inactivation of NUPGs/NUMGs should be explored. Three exemplary studies on the inactivation of NUPGs/NUMGs independently reported NUPTs/NUMTs as the alien nuclear genetic materials (like TEs) to be silenced through genomic defense (Zhang, et al 2020) , the important role of DNA methylation against NUPTs to maintain genome stability (Yoshida, et al 2019) , and the possible role of epigenetic modification in the silencing of a NUMT fragment in Arabidopsis (Fields, et al 2022) . However, these studies did not compare the DNA methylation patterns of NUPGs/NUMGs with the indigenous nuclear genes; moreover, the generality of their conclusions remained unclear.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary trajectory of organelle-derived nuclear DNAs in theTriticum/Aegilopscomplex species

Zhang¹,

Zhao²,

Li³

et al. 2022

Preprint

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Organelle-derived nuclear DNAs, nuclear plastid DNAs (NUPTs) and nuclear mitochondrial DNAs (NUMTs), have been identified in plants. Most, if not all, genes residing in NUPTs/NUMTs (NUPGs/NUMGs) are known to be inactivated and pseudogenized. However, the role of epigenetic control in silencing NUPGs/NUMGs and the dynamic evolution of NUPTs/NUMTs with respect to organismal phylogeny remain barely explored. Based on the available nuclear and organellar genomic resources of the Triticum/Aegilops complex species, we investigated the evolutionary fates of NUPTs/NUMTs in terms of their epigenetic silencing and their dynamic occurrence rates in the nuclear diploid genomes and allopolyploid subgenomes. NUPTs and NUMTs possessed similar genomic atlas, including preferential integration to the transposable element-rich intergenic regions and generating sequence variations in the nuclear genome. The global transcriptional silencing of NUPGs/NUMGs with disrupted and intact open reading frames can be mainly attributed to their repressive chromatin states, namely high levels of DNA methylation and low levels of active histone modifications. Phylogenomic analyses suggested that the species-specific and gradual accumulation of NUPTs/NUMTs accompanied the speciation processes. Moreover, based on further pan-genomic analyses, we found significant subgenomic asymmetry in the NUPT/NUMT occurrence, which accumulated during allopolyploid wheat evolution. Our findings provide novel insights into the dynamic evolutionary fates of organelle-derived nuclear DNA in plants.

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Complete sequence of a 641-kb insertion of mitochondrial DNA in the Arabidopsis thaliana nuclear genome

Cited by 5 publications

References 43 publications

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

Evolutionary trajectory of organelle-derived nuclear DNAs in theTriticum/Aegilopscomplex species

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