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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 structural characters support a Ptychomniales-like (A) or Hookeriales (B) origin of portions of the moss mtDNA present in Amborella.Color scheme: Non-pleurocarps, black; Amborella, red; Ptychomniales, blue; Hypnales, orange; Hookeriales, green. Sequences within each color group are ordered phylogenetically. A) Part of the nad5 intron alignment used for the phylogenetic analysis of Fig 2J, showing a 9-bp deletion uniquely shared by Amborella and all examined Ptychomniales. Note that there is no homoplasy for this indel region in the many taxa examined in Fig 2J that were excluded from the alignment shown here. B) Alignment of a portion of the rrn5-to-rrnL region used for Fig 2B. Highlighted is a 6-bp conversion tract (see text) uniquely shared by Amborella and both examined Hookeriales.
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pone.0137532.g004: Two structural characters support a Ptychomniales-like (A) or Hookeriales (B) origin of portions of the moss mtDNA present in Amborella.Color scheme: Non-pleurocarps, black; Amborella, red; Ptychomniales, blue; Hypnales, orange; Hookeriales, green. Sequences within each color group are ordered phylogenetically. A) Part of the nad5 intron alignment used for the phylogenetic analysis of Fig 2J, showing a 9-bp deletion uniquely shared by Amborella and all examined Ptychomniales. Note that there is no homoplasy for this indel region in the many taxa examined in Fig 2J that were excluded from the alignment shown here. B) Alignment of a portion of the rrn5-to-rrnL region used for Fig 2B. Highlighted is a 6-bp conversion tract (see text) uniquely shared by Amborella and both examined Hookeriales.

Mentions: Two structural characters, whose regions were not included in the phylogenetic analyses, provide additional support for these two moss donors. A 9-bp deletion within intron 2 of nad5 is uniquely shared by Amborella and all examined Ptychomniales (Fig 4A), in agreement with phylogenetic analysis of this locus (Fig 2J). Conversely, a 6-bp tract in the spacer between rrn5 and rrnL (locus B) groups Amborella with all examined Hookeriales (Fig 4B), in agreement with phylogenetic analysis of this locus (Fig 2B). The CAGGCA sequence that comprises this tract in Amborella and Hookeriales is part of a larger, 22-bp tract that matches the 5’ end of rrnL with only one mismatch in both Anomodon and Amborella. Given this similarity and that these two regions are only about 200 bp apart, a conversion event from the rrnL region to the CAGGCA site early in Hookeriales evolution seems likely.


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 structural characters support a Ptychomniales-like (A) or Hookeriales (B) origin of portions of the moss mtDNA present in Amborella.Color scheme: Non-pleurocarps, black; Amborella, red; Ptychomniales, blue; Hypnales, orange; Hookeriales, green. Sequences within each color group are ordered phylogenetically. A) Part of the nad5 intron alignment used for the phylogenetic analysis of Fig 2J, showing a 9-bp deletion uniquely shared by Amborella and all examined Ptychomniales. Note that there is no homoplasy for this indel region in the many taxa examined in Fig 2J that were excluded from the alignment shown here. B) Alignment of a portion of the rrn5-to-rrnL region used for Fig 2B. Highlighted is a 6-bp conversion tract (see text) uniquely shared by Amborella and both examined Hookeriales.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0137532.g004: Two structural characters support a Ptychomniales-like (A) or Hookeriales (B) origin of portions of the moss mtDNA present in Amborella.Color scheme: Non-pleurocarps, black; Amborella, red; Ptychomniales, blue; Hypnales, orange; Hookeriales, green. Sequences within each color group are ordered phylogenetically. A) Part of the nad5 intron alignment used for the phylogenetic analysis of Fig 2J, showing a 9-bp deletion uniquely shared by Amborella and all examined Ptychomniales. Note that there is no homoplasy for this indel region in the many taxa examined in Fig 2J that were excluded from the alignment shown here. B) Alignment of a portion of the rrn5-to-rrnL region used for Fig 2B. Highlighted is a 6-bp conversion tract (see text) uniquely shared by Amborella and both examined Hookeriales.
Mentions: Two structural characters, whose regions were not included in the phylogenetic analyses, provide additional support for these two moss donors. A 9-bp deletion within intron 2 of nad5 is uniquely shared by Amborella and all examined Ptychomniales (Fig 4A), in agreement with phylogenetic analysis of this locus (Fig 2J). Conversely, a 6-bp tract in the spacer between rrn5 and rrnL (locus B) groups Amborella with all examined Hookeriales (Fig 4B), in agreement with phylogenetic analysis of this locus (Fig 2B). The CAGGCA sequence that comprises this tract in Amborella and Hookeriales is part of a larger, 22-bp tract that matches the 5’ end of rrnL with only one mismatch in both Anomodon and Amborella. Given this similarity and that these two regions are only about 200 bp apart, a conversion event from the rrnL region to the CAGGCA site early in Hookeriales evolution seems likely.

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