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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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A nearly full-length moss mitochondrial genome in Amborella mtDNA is very similar to the Anomodon moss genome.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.
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pone.0137532.g001: A nearly full-length moss mitochondrial genome in Amborella mtDNA is very similar to the Anomodon moss genome.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.

Mentions: Recent sequencing of the Amborella mitochondrial genome revealed that it contains roughly six mitochondrial genome equivalents of DNA acquired by HGT [11]. These include two genome equivalents from angiosperms, three from green algae, and one from mosses. Most of the moss-derived protein genes present in Amborella are clear pseudogenes; this and other considerations suggest that few if any of the foreign moss genes are functional [11]. The foreign moss mitochondrial “genome” consists of four tracts of contiguous moss-like DNA (designated herein as “Moss-in-Amborella” tracts MoAm1-MoAm4; see Fig 1, bottom) of lengths 48.1, 40.0, 9.3, and 4.4 kb that are located at widely separated positions in the Amborella mitochondrial genome [11]. These four regions are highly similar in sequence and structure to the 14 published moss mitochondrial mtDNAs [12–15]. Of greatest relevance, these 14 sequenced moss genomes are perfectly syntenic and very similar in size (all but two are between 100 and 110 kb in size). One of these genomes, the 104-kb Anomodon rugelii genome (Fig 1, top) [13], was used as a comparison genome by Rice et al. [11] to elucidate the boundaries, gene content, and gene order of the moss DNA present in Amborella. Together, the four moss regions in Amborella add up to a 102-kb, nearly complete, Anomodon-type mitochondrial genome, with only four genes (all of them tRNA genes) completely missing from Amborella (see Δ3 and Δ4 in Fig 1, top). One of the four regions (Fig 1, bottom, MoAm4) has perfect synteny to sequenced moss genomes, while each of the other three regions (Fig 1, bottom, MoAm1-MoAm3) is composed of two perfectly syntenic segments joined together, making for a total of seven syntenic segments (labeled 1–7 in Fig 1). We refer to these seven segments as “moss-synteny segments”.


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)

A nearly full-length moss mitochondrial genome in Amborella mtDNA is very similar to the Anomodon moss genome.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.
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Related In: Results  -  Collection

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pone.0137532.g001: A nearly full-length moss mitochondrial genome in Amborella mtDNA is very similar to the Anomodon moss genome.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.
Mentions: Recent sequencing of the Amborella mitochondrial genome revealed that it contains roughly six mitochondrial genome equivalents of DNA acquired by HGT [11]. These include two genome equivalents from angiosperms, three from green algae, and one from mosses. Most of the moss-derived protein genes present in Amborella are clear pseudogenes; this and other considerations suggest that few if any of the foreign moss genes are functional [11]. The foreign moss mitochondrial “genome” consists of four tracts of contiguous moss-like DNA (designated herein as “Moss-in-Amborella” tracts MoAm1-MoAm4; see Fig 1, bottom) of lengths 48.1, 40.0, 9.3, and 4.4 kb that are located at widely separated positions in the Amborella mitochondrial genome [11]. These four regions are highly similar in sequence and structure to the 14 published moss mitochondrial mtDNAs [12–15]. Of greatest relevance, these 14 sequenced moss genomes are perfectly syntenic and very similar in size (all but two are between 100 and 110 kb in size). One of these genomes, the 104-kb Anomodon rugelii genome (Fig 1, top) [13], was used as a comparison genome by Rice et al. [11] to elucidate the boundaries, gene content, and gene order of the moss DNA present in Amborella. Together, the four moss regions in Amborella add up to a 102-kb, nearly complete, Anomodon-type mitochondrial genome, with only four genes (all of them tRNA genes) completely missing from Amborella (see Δ3 and Δ4 in Fig 1, top). One of the four regions (Fig 1, bottom, MoAm4) has perfect synteny to sequenced moss genomes, while each of the other three regions (Fig 1, bottom, MoAm1-MoAm3) is composed of two perfectly syntenic segments joined together, making for a total of seven syntenic segments (labeled 1–7 in Fig 1). We refer to these seven segments as “moss-synteny segments”.

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