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Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (apocynaceae).

Straub SC, Cronn RC, Edwards C, Fishbein M, Liston A - Genome Biol Evol (2013)

Bottom Line: We sequenced the 158 kb plastome and the 690 kb mitochondrial genome of common milkweed (Asclepias syriaca [Apocynaceae]) and found evidence of intracellular HGT for a 2.4-kb segment of mitochondrial DNA to the rps2-rpoC2 intergenic spacer of the plastome.Although the plastome insertion has been maintained in all lineages of Asclepiadoideae, it shows minimal evidence of transcription in A. syriaca and is likely nonfunctional.Furthermore, we found recent gene conversion of the mitochondrial rpoC2 pseudogene in Asclepias by the plastid gene, which reflects continued interaction of these genomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University.

ABSTRACT
Horizontal gene transfer (HGT) of DNA from the plastid to the nuclear and mitochondrial genomes of higher plants is a common phenomenon; however, plastid genomes (plastomes) are highly conserved and have generally been regarded as impervious to HGT. We sequenced the 158 kb plastome and the 690 kb mitochondrial genome of common milkweed (Asclepias syriaca [Apocynaceae]) and found evidence of intracellular HGT for a 2.4-kb segment of mitochondrial DNA to the rps2-rpoC2 intergenic spacer of the plastome. The transferred region contains an rpl2 pseudogene and is flanked by plastid sequence in the mitochondrial genome, including an rpoC2 pseudogene, which likely provided the mechanism for HGT back to the plastome through double-strand break repair involving homologous recombination. The plastome insertion is restricted to tribe Asclepiadeae of subfamily Asclepiadoideae, whereas the mitochondrial rpoC2 pseudogene is present throughout the subfamily, which confirms that the plastid to mitochondrial HGT event preceded the HGT to the plastome. Although the plastome insertion has been maintained in all lineages of Asclepiadoideae, it shows minimal evidence of transcription in A. syriaca and is likely nonfunctional. Furthermore, we found recent gene conversion of the mitochondrial rpoC2 pseudogene in Asclepias by the plastid gene, which reflects continued interaction of these genomes.

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Gene conversion between the plastid rpoC2 and mitochondrial ψrpoC2 genes of A. syriaca. (A) Plot of percent identity between homologous regions of the plastome and mitochondrial genomes of A. syriaca over a 20-bp sliding window. Green indicates 100% identity, brown <100% but at least 30% identity, and red <30% identity. Gap positions in the alignment were considered to have no identity. (B) ML phylogeny of plastid rpoC2 and mitochondrial ψrpoC2 sequences. The numbers above or below the branches are bootstrap support values. Plastid gene sequences are indicated in green and mitochondrial pseudogene sequences in black. In the absence of gene conversion or other confounding factors, both the plastid and mitochondrial sequences should produce monophyletic groups with identical branching orders; however, strongly supported placement of the A. syriaca mitochondrial pseudogene sequence in the plastid clade indicates sufficient gene conversion to affect the outcome of the phylogenetic analysis.
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evt140-F5: Gene conversion between the plastid rpoC2 and mitochondrial ψrpoC2 genes of A. syriaca. (A) Plot of percent identity between homologous regions of the plastome and mitochondrial genomes of A. syriaca over a 20-bp sliding window. Green indicates 100% identity, brown <100% but at least 30% identity, and red <30% identity. Gap positions in the alignment were considered to have no identity. (B) ML phylogeny of plastid rpoC2 and mitochondrial ψrpoC2 sequences. The numbers above or below the branches are bootstrap support values. Plastid gene sequences are indicated in green and mitochondrial pseudogene sequences in black. In the absence of gene conversion or other confounding factors, both the plastid and mitochondrial sequences should produce monophyletic groups with identical branching orders; however, strongly supported placement of the A. syriaca mitochondrial pseudogene sequence in the plastid clade indicates sufficient gene conversion to affect the outcome of the phylogenetic analysis.

Mentions: Pairwise divergence between rpoC2 and ψrpoC2 in A. syriaca was 0.011 substitutions per site, which is much less than the pairwise divergence observed between the plastome insert and the homologous regions of the mitochondrial genome (fig. 5A), indicating the possibility of more recent exchange between the two genomes. To test for evidence of gene conversion, we informatically assembled the ψrpoC2 sequences for species with sequenced plastomes and obtained Sanger sequences for portions of the pseudogene in A. syriaca, Eustegia, and Telosma to confirm the informatically assembled sequences. Low sequencing depth of the mitochondrial genome and/or the apparent presence of more than one rpoC2 pseudogene prevented the mitochondrial sequences of Araujia and A. nivea from being successfully assembled. Phylogenetic analysis of the successfully determined mitochondrial sequences and the plastid homologs (690 variable of 4,222 total characters; −ln likelihood −11896.01) indicated that there has indeed been recent recombination between the plastid gene and the mitochondrial pseudogene in A. syriaca, as the mitochondrial sequence is strongly supported to share more recent ancestry with plastid sequences than with mitochondrial sequences from other species (fig. 5B). Some of the other mitochondrial sequences share single-nucleotide polymorphisms with the plastid sequence from the same species and may be mosaics containing smaller tracts of gene conversion (Hao and Palmer 2009; Hao et al. 2010) than what we observed in A. syriaca and which are too short to affect the placement of the sequences in the phylogenetic analysis (Hao and Palmer 2011).Fig. 5.—


Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (apocynaceae).

Straub SC, Cronn RC, Edwards C, Fishbein M, Liston A - Genome Biol Evol (2013)

Gene conversion between the plastid rpoC2 and mitochondrial ψrpoC2 genes of A. syriaca. (A) Plot of percent identity between homologous regions of the plastome and mitochondrial genomes of A. syriaca over a 20-bp sliding window. Green indicates 100% identity, brown <100% but at least 30% identity, and red <30% identity. Gap positions in the alignment were considered to have no identity. (B) ML phylogeny of plastid rpoC2 and mitochondrial ψrpoC2 sequences. The numbers above or below the branches are bootstrap support values. Plastid gene sequences are indicated in green and mitochondrial pseudogene sequences in black. In the absence of gene conversion or other confounding factors, both the plastid and mitochondrial sequences should produce monophyletic groups with identical branching orders; however, strongly supported placement of the A. syriaca mitochondrial pseudogene sequence in the plastid clade indicates sufficient gene conversion to affect the outcome of the phylogenetic analysis.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3814198&req=5

evt140-F5: Gene conversion between the plastid rpoC2 and mitochondrial ψrpoC2 genes of A. syriaca. (A) Plot of percent identity between homologous regions of the plastome and mitochondrial genomes of A. syriaca over a 20-bp sliding window. Green indicates 100% identity, brown <100% but at least 30% identity, and red <30% identity. Gap positions in the alignment were considered to have no identity. (B) ML phylogeny of plastid rpoC2 and mitochondrial ψrpoC2 sequences. The numbers above or below the branches are bootstrap support values. Plastid gene sequences are indicated in green and mitochondrial pseudogene sequences in black. In the absence of gene conversion or other confounding factors, both the plastid and mitochondrial sequences should produce monophyletic groups with identical branching orders; however, strongly supported placement of the A. syriaca mitochondrial pseudogene sequence in the plastid clade indicates sufficient gene conversion to affect the outcome of the phylogenetic analysis.
Mentions: Pairwise divergence between rpoC2 and ψrpoC2 in A. syriaca was 0.011 substitutions per site, which is much less than the pairwise divergence observed between the plastome insert and the homologous regions of the mitochondrial genome (fig. 5A), indicating the possibility of more recent exchange between the two genomes. To test for evidence of gene conversion, we informatically assembled the ψrpoC2 sequences for species with sequenced plastomes and obtained Sanger sequences for portions of the pseudogene in A. syriaca, Eustegia, and Telosma to confirm the informatically assembled sequences. Low sequencing depth of the mitochondrial genome and/or the apparent presence of more than one rpoC2 pseudogene prevented the mitochondrial sequences of Araujia and A. nivea from being successfully assembled. Phylogenetic analysis of the successfully determined mitochondrial sequences and the plastid homologs (690 variable of 4,222 total characters; −ln likelihood −11896.01) indicated that there has indeed been recent recombination between the plastid gene and the mitochondrial pseudogene in A. syriaca, as the mitochondrial sequence is strongly supported to share more recent ancestry with plastid sequences than with mitochondrial sequences from other species (fig. 5B). Some of the other mitochondrial sequences share single-nucleotide polymorphisms with the plastid sequence from the same species and may be mosaics containing smaller tracts of gene conversion (Hao and Palmer 2009; Hao et al. 2010) than what we observed in A. syriaca and which are too short to affect the placement of the sequences in the phylogenetic analysis (Hao and Palmer 2011).Fig. 5.—

Bottom Line: We sequenced the 158 kb plastome and the 690 kb mitochondrial genome of common milkweed (Asclepias syriaca [Apocynaceae]) and found evidence of intracellular HGT for a 2.4-kb segment of mitochondrial DNA to the rps2-rpoC2 intergenic spacer of the plastome.Although the plastome insertion has been maintained in all lineages of Asclepiadoideae, it shows minimal evidence of transcription in A. syriaca and is likely nonfunctional.Furthermore, we found recent gene conversion of the mitochondrial rpoC2 pseudogene in Asclepias by the plastid gene, which reflects continued interaction of these genomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University.

ABSTRACT
Horizontal gene transfer (HGT) of DNA from the plastid to the nuclear and mitochondrial genomes of higher plants is a common phenomenon; however, plastid genomes (plastomes) are highly conserved and have generally been regarded as impervious to HGT. We sequenced the 158 kb plastome and the 690 kb mitochondrial genome of common milkweed (Asclepias syriaca [Apocynaceae]) and found evidence of intracellular HGT for a 2.4-kb segment of mitochondrial DNA to the rps2-rpoC2 intergenic spacer of the plastome. The transferred region contains an rpl2 pseudogene and is flanked by plastid sequence in the mitochondrial genome, including an rpoC2 pseudogene, which likely provided the mechanism for HGT back to the plastome through double-strand break repair involving homologous recombination. The plastome insertion is restricted to tribe Asclepiadeae of subfamily Asclepiadoideae, whereas the mitochondrial rpoC2 pseudogene is present throughout the subfamily, which confirms that the plastid to mitochondrial HGT event preceded the HGT to the plastome. Although the plastome insertion has been maintained in all lineages of Asclepiadoideae, it shows minimal evidence of transcription in A. syriaca and is likely nonfunctional. Furthermore, we found recent gene conversion of the mitochondrial rpoC2 pseudogene in Asclepias by the plastid gene, which reflects continued interaction of these genomes.

Show MeSH
Related in: MedlinePlus