Limits...
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.

Show MeSH

Related in: MedlinePlus

Updated analysis of cox2 fails to support a Hypnales origin of this locus in Amborella.A) The bryophyte cox2 tree from Fig 1 of [7]. Amborella sequences are in red, Hypnales in orange, and Hookeriales in green. Bootstrap values >50% are shown. Scale bars correspond to 0.01 substitutions per site. B) Expanded taxon sampling of the 266-bp cox2 locus analyzed in A) and in [7]. C) Same taxon sampling as in B) but with the cox2 alignment expanded to 881 bp. D) The cox2 alignment used in B). Yellow highlights three characters responsible (see text) for the erroneous 2004 placement, as shown in A), of Amborella cox2 within Hypnales.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4664403&req=5

pone.0137532.g003: Updated analysis of cox2 fails to support a Hypnales origin of this locus in Amborella.A) The bryophyte cox2 tree from Fig 1 of [7]. Amborella sequences are in red, Hypnales in orange, and Hookeriales in green. Bootstrap values >50% are shown. Scale bars correspond to 0.01 substitutions per site. B) Expanded taxon sampling of the 266-bp cox2 locus analyzed in A) and in [7]. C) Same taxon sampling as in B) but with the cox2 alignment expanded to 881 bp. D) The cox2 alignment used in B). Yellow highlights three characters responsible (see text) for the erroneous 2004 placement, as shown in A), of Amborella cox2 within Hypnales.

Mentions: A total of 16 mitochondrial loci (labeled A-P in Fig 1, top, and Table 1) were analyzed with maximum likelihood using data sets that contained between 6 and 166 moss sequences (Figs 2, 3 and S1 Fig), most of which were generated by PCR amplification as part of this study (S1 Table). The non-uniform representation of PCR amplified taxa across loci reflects the variable success of PCR amplification reactions at different loci. The seven moss-synteny segments in Amborella (Fig 1) were represented by between one and six of these 16 loci, which range in length from 266 to 2,383 bp. All well supported regions in these 16 trees were consistent with generally accepted relationships along the ‘backbone’ of moss phylogeny and of the major pleurocarp groups [9,10,20–25]. Thirteen of these trees supported either of two placements of the moss DNA in Amborella, within (or sister to) the Hookeriales or sister to the Ptychomniales). The other three trees were inconclusive owing to poor resolution of the three homocostate pleurocarp orders, missing taxa, and/or generally weak bootstrap support.


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)

Updated analysis of cox2 fails to support a Hypnales origin of this locus in Amborella.A) The bryophyte cox2 tree from Fig 1 of [7]. Amborella sequences are in red, Hypnales in orange, and Hookeriales in green. Bootstrap values >50% are shown. Scale bars correspond to 0.01 substitutions per site. B) Expanded taxon sampling of the 266-bp cox2 locus analyzed in A) and in [7]. C) Same taxon sampling as in B) but with the cox2 alignment expanded to 881 bp. D) The cox2 alignment used in B). Yellow highlights three characters responsible (see text) for the erroneous 2004 placement, as shown in A), of Amborella cox2 within Hypnales.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0137532.g003: Updated analysis of cox2 fails to support a Hypnales origin of this locus in Amborella.A) The bryophyte cox2 tree from Fig 1 of [7]. Amborella sequences are in red, Hypnales in orange, and Hookeriales in green. Bootstrap values >50% are shown. Scale bars correspond to 0.01 substitutions per site. B) Expanded taxon sampling of the 266-bp cox2 locus analyzed in A) and in [7]. C) Same taxon sampling as in B) but with the cox2 alignment expanded to 881 bp. D) The cox2 alignment used in B). Yellow highlights three characters responsible (see text) for the erroneous 2004 placement, as shown in A), of Amborella cox2 within Hypnales.
Mentions: A total of 16 mitochondrial loci (labeled A-P in Fig 1, top, and Table 1) were analyzed with maximum likelihood using data sets that contained between 6 and 166 moss sequences (Figs 2, 3 and S1 Fig), most of which were generated by PCR amplification as part of this study (S1 Table). The non-uniform representation of PCR amplified taxa across loci reflects the variable success of PCR amplification reactions at different loci. The seven moss-synteny segments in Amborella (Fig 1) were represented by between one and six of these 16 loci, which range in length from 266 to 2,383 bp. All well supported regions in these 16 trees were consistent with generally accepted relationships along the ‘backbone’ of moss phylogeny and of the major pleurocarp groups [9,10,20–25]. Thirteen of these trees supported either of two placements of the moss DNA in Amborella, within (or sister to) the Hookeriales or sister to the Ptychomniales). The other three trees were inconclusive owing to poor resolution of the three homocostate pleurocarp orders, missing taxa, and/or generally weak bootstrap support.

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