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The Complete Moss Mitochondrial Genome in the Angiosperm Amborella Is a Chimera Derived from Two Moss Whole-Genome Transfers.

Taylor ZN, Rice DW, Palmer JD - PLoS ONE (2015)

Bottom Line: These results, combined with synteny analyses and other considerations, lead us to favor a model involving two successive moss-to-Amborella whole-genome transfers, followed by recombination that produced a single intact and chimeric moss mitochondrial genome integrated in the Amborella mitochondrial genome.Five of these events are associated with short-to-intermediate sized repeats.These findings reinforce and extend recent evidence for an important role of MMBIR in plant mitochondrial DNA evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington, Indiana, United States of America.

ABSTRACT
Sequencing of the 4-Mb mitochondrial genome of the angiosperm Amborella trichopoda has shown that it contains unprecedented amounts of foreign mitochondrial DNA, including four blocks of sequences that together correspond almost perfectly to one entire moss mitochondrial genome. This implies whole-genome transfer from a single moss donor but conflicts with phylogenetic results from an earlier, PCR-based study that suggested three different moss donors to Amborella. To resolve this conflict, we conducted an expanded set of phylogenetic analyses with respect to both moss lineages and mitochondrial loci. The moss DNA in Amborella was consistently placed in either of two positions, depending on the locus analyzed, as sister to the Ptychomniales or within the Hookeriales. This agrees with two of the three previously suggested donors, whereas the third is no longer supported. These results, combined with synteny analyses and other considerations, lead us to favor a model involving two successive moss-to-Amborella whole-genome transfers, followed by recombination that produced a single intact and chimeric moss mitochondrial genome integrated in the Amborella mitochondrial genome. Eight subsequent recombination events account for the state of fragmentation, rearrangement, duplication, and deletion of this chimeric moss mitochondrial genome as it currently exists in Amborella. Five of these events are associated with short-to-intermediate sized repeats. Two of the five probably occurred by reciprocal homologous recombination, whereas the other three probably occurred in a non-reciprocal manner via microhomology-mediated break-induced replication (MMBIR). These findings reinforce and extend recent evidence for an important role of MMBIR in plant mitochondrial DNA evolution.

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Two recombination models for the creation of a Ptychomniales/Hookeriales chimeric mitochondrial genome.These models differ only with respect to whether this chimeric moss genome is generated after (A) or before (B) integration of a moss genome into the Amborella mitochondrial genome. The nearly full-genome equivalent of moss mtDNA currently present in the Amborella mitochondrial genome (thin black lines) is divided into regions 1 and 2, with 1 corresponding to the roughly 60% of a moss genome-equivalent acquired from a member of the Hookeriales (thick green lines) and 2 the 40% acquired from a Ptychomniales-like donor (thick blue lines). Genomes are not shown to scale. Recombination sites are marked by open boxes. Recombination events are indicated by dotted lines. Both models show the same two recombination events, the first occurring intermolecularly between homologous moss G-M regions (see Fig 1, top) and the second intramolecularly between the A-J regions of a dimeric cointegrate moss genome that either is (A) or is not (B) already integrated within the Amborella genome. For what is meant by “lost”, see Results. To facilitate presentation and interpretation of these pathways, all molecules are shown as intact circular genomes. We recognize, however, that although plant mitochondrial genomes usually map/assemble as circular chromosomes, their in vivo conformation is probably a recombinationally dynamic population of circular and linear molecules of varying sizes [42,43].
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pone.0137532.g005: Two recombination models for the creation of a Ptychomniales/Hookeriales chimeric mitochondrial genome.These models differ only with respect to whether this chimeric moss genome is generated after (A) or before (B) integration of a moss genome into the Amborella mitochondrial genome. The nearly full-genome equivalent of moss mtDNA currently present in the Amborella mitochondrial genome (thin black lines) is divided into regions 1 and 2, with 1 corresponding to the roughly 60% of a moss genome-equivalent acquired from a member of the Hookeriales (thick green lines) and 2 the 40% acquired from a Ptychomniales-like donor (thick blue lines). Genomes are not shown to scale. Recombination sites are marked by open boxes. Recombination events are indicated by dotted lines. Both models show the same two recombination events, the first occurring intermolecularly between homologous moss G-M regions (see Fig 1, top) and the second intramolecularly between the A-J regions of a dimeric cointegrate moss genome that either is (A) or is not (B) already integrated within the Amborella genome. For what is meant by “lost”, see Results. To facilitate presentation and interpretation of these pathways, all molecules are shown as intact circular genomes. We recognize, however, that although plant mitochondrial genomes usually map/assemble as circular chromosomes, their in vivo conformation is probably a recombinationally dynamic population of circular and linear molecules of varying sizes [42,43].

Mentions: Fig 5 shows two variants of a two-step recombination pathway that would create the chimeric moss genome shown in Fig 1 (top) via recombination of mitochondrial genomes belonging to members of the Hookeriales and a Ptychomniales-like group. These pathways assume horizontal transfer of two entire moss mitochondrial genomes. This is a sound assumption given the evidence 1) that plant mitochondrial HGT is driven by fusion of whole mitochondria from donor and recipient plants and 2) that Amborella mtDNA has acquired at least four entire mitochondrial genomes via HGT [11].


The Complete Moss Mitochondrial Genome in the Angiosperm Amborella Is a Chimera Derived from Two Moss Whole-Genome Transfers.

Taylor ZN, Rice DW, Palmer JD - PLoS ONE (2015)

Two recombination models for the creation of a Ptychomniales/Hookeriales chimeric mitochondrial genome.These models differ only with respect to whether this chimeric moss genome is generated after (A) or before (B) integration of a moss genome into the Amborella mitochondrial genome. The nearly full-genome equivalent of moss mtDNA currently present in the Amborella mitochondrial genome (thin black lines) is divided into regions 1 and 2, with 1 corresponding to the roughly 60% of a moss genome-equivalent acquired from a member of the Hookeriales (thick green lines) and 2 the 40% acquired from a Ptychomniales-like donor (thick blue lines). Genomes are not shown to scale. Recombination sites are marked by open boxes. Recombination events are indicated by dotted lines. Both models show the same two recombination events, the first occurring intermolecularly between homologous moss G-M regions (see Fig 1, top) and the second intramolecularly between the A-J regions of a dimeric cointegrate moss genome that either is (A) or is not (B) already integrated within the Amborella genome. For what is meant by “lost”, see Results. To facilitate presentation and interpretation of these pathways, all molecules are shown as intact circular genomes. We recognize, however, that although plant mitochondrial genomes usually map/assemble as circular chromosomes, their in vivo conformation is probably a recombinationally dynamic population of circular and linear molecules of varying sizes [42,43].
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664403&req=5

pone.0137532.g005: Two recombination models for the creation of a Ptychomniales/Hookeriales chimeric mitochondrial genome.These models differ only with respect to whether this chimeric moss genome is generated after (A) or before (B) integration of a moss genome into the Amborella mitochondrial genome. The nearly full-genome equivalent of moss mtDNA currently present in the Amborella mitochondrial genome (thin black lines) is divided into regions 1 and 2, with 1 corresponding to the roughly 60% of a moss genome-equivalent acquired from a member of the Hookeriales (thick green lines) and 2 the 40% acquired from a Ptychomniales-like donor (thick blue lines). Genomes are not shown to scale. Recombination sites are marked by open boxes. Recombination events are indicated by dotted lines. Both models show the same two recombination events, the first occurring intermolecularly between homologous moss G-M regions (see Fig 1, top) and the second intramolecularly between the A-J regions of a dimeric cointegrate moss genome that either is (A) or is not (B) already integrated within the Amborella genome. For what is meant by “lost”, see Results. To facilitate presentation and interpretation of these pathways, all molecules are shown as intact circular genomes. We recognize, however, that although plant mitochondrial genomes usually map/assemble as circular chromosomes, their in vivo conformation is probably a recombinationally dynamic population of circular and linear molecules of varying sizes [42,43].
Mentions: Fig 5 shows two variants of a two-step recombination pathway that would create the chimeric moss genome shown in Fig 1 (top) via recombination of mitochondrial genomes belonging to members of the Hookeriales and a Ptychomniales-like group. These pathways assume horizontal transfer of two entire moss mitochondrial genomes. This is a sound assumption given the evidence 1) that plant mitochondrial HGT is driven by fusion of whole mitochondria from donor and recipient plants and 2) that Amborella mtDNA has acquired at least four entire mitochondrial genomes via HGT [11].

Bottom Line: These results, combined with synteny analyses and other considerations, lead us to favor a model involving two successive moss-to-Amborella whole-genome transfers, followed by recombination that produced a single intact and chimeric moss mitochondrial genome integrated in the Amborella mitochondrial genome.Five of these events are associated with short-to-intermediate sized repeats.These findings reinforce and extend recent evidence for an important role of MMBIR in plant mitochondrial DNA evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington, Indiana, United States of America.

ABSTRACT
Sequencing of the 4-Mb mitochondrial genome of the angiosperm Amborella trichopoda has shown that it contains unprecedented amounts of foreign mitochondrial DNA, including four blocks of sequences that together correspond almost perfectly to one entire moss mitochondrial genome. This implies whole-genome transfer from a single moss donor but conflicts with phylogenetic results from an earlier, PCR-based study that suggested three different moss donors to Amborella. To resolve this conflict, we conducted an expanded set of phylogenetic analyses with respect to both moss lineages and mitochondrial loci. The moss DNA in Amborella was consistently placed in either of two positions, depending on the locus analyzed, as sister to the Ptychomniales or within the Hookeriales. This agrees with two of the three previously suggested donors, whereas the third is no longer supported. These results, combined with synteny analyses and other considerations, lead us to favor a model involving two successive moss-to-Amborella whole-genome transfers, followed by recombination that produced a single intact and chimeric moss mitochondrial genome integrated in the Amborella mitochondrial genome. Eight subsequent recombination events account for the state of fragmentation, rearrangement, duplication, and deletion of this chimeric moss mitochondrial genome as it currently exists in Amborella. Five of these events are associated with short-to-intermediate sized repeats. Two of the five probably occurred by reciprocal homologous recombination, whereas the other three probably occurred in a non-reciprocal manner via microhomology-mediated break-induced replication (MMBIR). These findings reinforce and extend recent evidence for an important role of MMBIR in plant mitochondrial DNA evolution.

Show MeSH
Related in: MedlinePlus