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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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Phylogenetic evidence for two moss donors to Amborella mtDNA.These maximum likelihood trees were rooted based on the current best estimates of overall moss phylogeny [9,10,20–25]. The trees are labeled with shorthand names of the loci used in the analyses and with letters (A-J) that correspond to those in Figs 1 and 6 and Table 1. Amborella sequences are in red, Ptychomniales in blue, Hypnales in orange, and Hookeriales in green. Scale bars correspond to 0.01 substitutions per site. Bootstrap values >50% are shown, space permitting. Bootstrap values that support the monophyly of a clade comprising the Hypnales and Hookeriales are placed in light red boxes, those that support the placement of the Amborella sequences as sister to or within the Hookeriales are in green boxes, and those that support their placement as sister to the Ptychomniales are in blue boxes. Triangular branches indicate collapsed clades; these are given the name of a sampled genus belonging to the clade and a parenthetical number indicating how many taxa in the clade were sampled. In addition, the grade comprising the top part of tree J is not shown. For full sampling at these loci, see S1 Table. Dashed lines indicate branches whose lengths were reduced due to space constraints. Due to image size constraints only the relevant portion of a larger tree J is shown. The short stub of a dotted line indicating where tree J’s outgroup lineages were pruned.
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pone.0137532.g002: Phylogenetic evidence for two moss donors to Amborella mtDNA.These maximum likelihood trees were rooted based on the current best estimates of overall moss phylogeny [9,10,20–25]. The trees are labeled with shorthand names of the loci used in the analyses and with letters (A-J) that correspond to those in Figs 1 and 6 and Table 1. Amborella sequences are in red, Ptychomniales in blue, Hypnales in orange, and Hookeriales in green. Scale bars correspond to 0.01 substitutions per site. Bootstrap values >50% are shown, space permitting. Bootstrap values that support the monophyly of a clade comprising the Hypnales and Hookeriales are placed in light red boxes, those that support the placement of the Amborella sequences as sister to or within the Hookeriales are in green boxes, and those that support their placement as sister to the Ptychomniales are in blue boxes. Triangular branches indicate collapsed clades; these are given the name of a sampled genus belonging to the clade and a parenthetical number indicating how many taxa in the clade were sampled. In addition, the grade comprising the top part of tree J is not shown. For full sampling at these loci, see S1 Table. Dashed lines indicate branches whose lengths were reduced due to space constraints. Due to image size constraints only the relevant portion of a larger tree J is shown. The short stub of a dotted line indicating where tree J’s outgroup lineages were pruned.

Mentions: Top: Gene map of the 104.2-kb reference mitochondrial genome of the moss Anomodon [13] shown linearized within the cob intron to correspond to a diagrammatically favorable breakpoint, of several possible ones (see Results), of a donor moss genome immediately after its integration in Amborella mtDNA. Colored boxes and arrows indicate the position and relative orientation, respectively, of the seven blocks of synteny between the Anomodon genome and the four moss-derived regions in the Amborella genome (see Bottom). The black arrows (or portions thereof) and the bracket labeled “Ptychomniales-derived” indicate the location relative to Anomodon of a region of at least 32 kb in size, part or all of which (see first section of Discussion) was acquired by Amborella from a Ptychomniales-like donor, while the open arrows and bracket labeled “Hookeriales”-derived indicate the location relative to Anomodon of a region of at least 53 kb in size, part of all or which was acquired by Amborella from a Hookeriales donor. The thin lines indicate the maximum extent of the three regions of unassigned origin. The 16 loci used for phylogenetic analysis are marked by rectangles or lines labeled A-P (see Fig 2 and S1 Fig and Table 1). A filled rectangle indicates a Ptychomniales-like origin, an open rectangle a Hookeriales origin, and a thin line an unresolved origin. The four deletions and two duplications >100 bp in length in Amborella relative to Anomodon are marked by “Δ1-Δ4” and “dup1” and “dup2”, respectively. Bottom: Syntenic arrangement of genes in the four moss-derived regions (MoAm1-MoAm4) present in Amborella mtDNA.


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)

Phylogenetic evidence for two moss donors to Amborella mtDNA.These maximum likelihood trees were rooted based on the current best estimates of overall moss phylogeny [9,10,20–25]. The trees are labeled with shorthand names of the loci used in the analyses and with letters (A-J) that correspond to those in Figs 1 and 6 and Table 1. Amborella sequences are in red, Ptychomniales in blue, Hypnales in orange, and Hookeriales in green. Scale bars correspond to 0.01 substitutions per site. Bootstrap values >50% are shown, space permitting. Bootstrap values that support the monophyly of a clade comprising the Hypnales and Hookeriales are placed in light red boxes, those that support the placement of the Amborella sequences as sister to or within the Hookeriales are in green boxes, and those that support their placement as sister to the Ptychomniales are in blue boxes. Triangular branches indicate collapsed clades; these are given the name of a sampled genus belonging to the clade and a parenthetical number indicating how many taxa in the clade were sampled. In addition, the grade comprising the top part of tree J is not shown. For full sampling at these loci, see S1 Table. Dashed lines indicate branches whose lengths were reduced due to space constraints. Due to image size constraints only the relevant portion of a larger tree J is shown. The short stub of a dotted line indicating where tree J’s outgroup lineages were pruned.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0137532.g002: Phylogenetic evidence for two moss donors to Amborella mtDNA.These maximum likelihood trees were rooted based on the current best estimates of overall moss phylogeny [9,10,20–25]. The trees are labeled with shorthand names of the loci used in the analyses and with letters (A-J) that correspond to those in Figs 1 and 6 and Table 1. Amborella sequences are in red, Ptychomniales in blue, Hypnales in orange, and Hookeriales in green. Scale bars correspond to 0.01 substitutions per site. Bootstrap values >50% are shown, space permitting. Bootstrap values that support the monophyly of a clade comprising the Hypnales and Hookeriales are placed in light red boxes, those that support the placement of the Amborella sequences as sister to or within the Hookeriales are in green boxes, and those that support their placement as sister to the Ptychomniales are in blue boxes. Triangular branches indicate collapsed clades; these are given the name of a sampled genus belonging to the clade and a parenthetical number indicating how many taxa in the clade were sampled. In addition, the grade comprising the top part of tree J is not shown. For full sampling at these loci, see S1 Table. Dashed lines indicate branches whose lengths were reduced due to space constraints. Due to image size constraints only the relevant portion of a larger tree J is shown. The short stub of a dotted line indicating where tree J’s outgroup lineages were pruned.
Mentions: Top: Gene map of the 104.2-kb reference mitochondrial genome of the moss Anomodon [13] shown linearized within the cob intron to correspond to a diagrammatically favorable breakpoint, of several possible ones (see Results), of a donor moss genome immediately after its integration in Amborella mtDNA. Colored boxes and arrows indicate the position and relative orientation, respectively, of the seven blocks of synteny between the Anomodon genome and the four moss-derived regions in the Amborella genome (see Bottom). The black arrows (or portions thereof) and the bracket labeled “Ptychomniales-derived” indicate the location relative to Anomodon of a region of at least 32 kb in size, part or all of which (see first section of Discussion) was acquired by Amborella from a Ptychomniales-like donor, while the open arrows and bracket labeled “Hookeriales”-derived indicate the location relative to Anomodon of a region of at least 53 kb in size, part of all or which was acquired by Amborella from a Hookeriales donor. The thin lines indicate the maximum extent of the three regions of unassigned origin. The 16 loci used for phylogenetic analysis are marked by rectangles or lines labeled A-P (see Fig 2 and S1 Fig and Table 1). A filled rectangle indicates a Ptychomniales-like origin, an open rectangle a Hookeriales origin, and a thin line an unresolved origin. The four deletions and two duplications >100 bp in length in Amborella relative to Anomodon are marked by “Δ1-Δ4” and “dup1” and “dup2”, respectively. Bottom: Syntenic arrangement of genes in the four moss-derived regions (MoAm1-MoAm4) present in Amborella mtDNA.

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