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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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The five sets of repeats identified in rearrangement of the moss mtDNA present in Amborella mtDNA.For recombination events r1, r2, and 4, the very short repeats (10–13 bp in sizes) inferred to have mediated non-reciprocal recombination via the MMBIR pathway are in blue, while the left and right flanking sequences that are shared by two of the three extant examples of those repeats shown here are in green or red, respectively. Events r3 and r6 are reciprocal recombination events mediated by longer repeats, of either 84 bp (trnS) or 295 bp (a portion of rrnL), respectively.
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pone.0137532.g007: The five sets of repeats identified in rearrangement of the moss mtDNA present in Amborella mtDNA.For recombination events r1, r2, and 4, the very short repeats (10–13 bp in sizes) inferred to have mediated non-reciprocal recombination via the MMBIR pathway are in blue, while the left and right flanking sequences that are shared by two of the three extant examples of those repeats shown here are in green or red, respectively. Events r3 and r6 are reciprocal recombination events mediated by longer repeats, of either 84 bp (trnS) or 295 bp (a portion of rrnL), respectively.

Mentions: Five of the eight rearrangements invoked under this model can be rationalized based on identified repeats (Fig 7 and below). Specifically, the predicted crossover products of certain repeats identified within Anomodon, or between Anomodon and non-moss regions in Amborella and/or other angiosperms, correspond precisely to what is observed at certain rearrangement junctions in Amborella. Three of these putatively repeat-mediated rearrangements occurred at very short repeats (10–13 bp in length). Studies of plant mtDNA recombination suggest that recombination at such short repeats takes place via a microhomology-mediated break-induced replication (MMBIR) mechanism [27,28] that leads to a duplicative, non-reciprocal cross-over event, i.e., only one of the two potential recombination products is produced, and the DNA substrate used for the recombination is preserved in its pre-recombination form. For example, if such recombination occurred across very short direct repeats, then either the circularized DNA between the repeats, or the union of the sequences flanking them, would be produced, but not both, and in either case the recombination substrate would be preserved. The other two inferred repeat-mediated rearrangements occurred non-duplicatively via reciprocal recombination across longer repeats (84 and 295 bp in length).


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)

The five sets of repeats identified in rearrangement of the moss mtDNA present in Amborella mtDNA.For recombination events r1, r2, and 4, the very short repeats (10–13 bp in sizes) inferred to have mediated non-reciprocal recombination via the MMBIR pathway are in blue, while the left and right flanking sequences that are shared by two of the three extant examples of those repeats shown here are in green or red, respectively. Events r3 and r6 are reciprocal recombination events mediated by longer repeats, of either 84 bp (trnS) or 295 bp (a portion of rrnL), respectively.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0137532.g007: The five sets of repeats identified in rearrangement of the moss mtDNA present in Amborella mtDNA.For recombination events r1, r2, and 4, the very short repeats (10–13 bp in sizes) inferred to have mediated non-reciprocal recombination via the MMBIR pathway are in blue, while the left and right flanking sequences that are shared by two of the three extant examples of those repeats shown here are in green or red, respectively. Events r3 and r6 are reciprocal recombination events mediated by longer repeats, of either 84 bp (trnS) or 295 bp (a portion of rrnL), respectively.
Mentions: Five of the eight rearrangements invoked under this model can be rationalized based on identified repeats (Fig 7 and below). Specifically, the predicted crossover products of certain repeats identified within Anomodon, or between Anomodon and non-moss regions in Amborella and/or other angiosperms, correspond precisely to what is observed at certain rearrangement junctions in Amborella. Three of these putatively repeat-mediated rearrangements occurred at very short repeats (10–13 bp in length). Studies of plant mtDNA recombination suggest that recombination at such short repeats takes place via a microhomology-mediated break-induced replication (MMBIR) mechanism [27,28] that leads to a duplicative, non-reciprocal cross-over event, i.e., only one of the two potential recombination products is produced, and the DNA substrate used for the recombination is preserved in its pre-recombination form. For example, if such recombination occurred across very short direct repeats, then either the circularized DNA between the repeats, or the union of the sequences flanking them, would be produced, but not both, and in either case the recombination substrate would be preserved. The other two inferred repeat-mediated rearrangements occurred non-duplicatively via reciprocal recombination across longer repeats (84 and 295 bp in length).

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