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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 expression levels of the plastome insert and flanking operons in A. syriaca. The gray plot shows relative sequencing depth for plastome regions flanking the rps2–rpoC2 intergenic spacer; color scheme for plastid genes, plastid spacers, and the mitochondrial insert follows figures 1 and 3. (A) Expression of the 5′-end of rps2 and the flanking insert sequence. (B) Expression of the 3′-end of rpoC2 and flanking insert sequence, including ψrpl2. Plastome coordinates are given on the x axis and read depth on the y axis for both (A) and (B). Note that the scale is not the same in (A) and (B).
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evt140-F6: Gene expression levels of the plastome insert and flanking operons in A. syriaca. The gray plot shows relative sequencing depth for plastome regions flanking the rps2–rpoC2 intergenic spacer; color scheme for plastid genes, plastid spacers, and the mitochondrial insert follows figures 1 and 3. (A) Expression of the 5′-end of rps2 and the flanking insert sequence. (B) Expression of the 3′-end of rpoC2 and flanking insert sequence, including ψrpl2. Plastome coordinates are given on the x axis and read depth on the y axis for both (A) and (B). Note that the scale is not the same in (A) and (B).

Mentions: We evaluated transcriptome sequences derived from leaf tissue of the same A. syriaca individual used in genomic sequencing to determine whether the ψrpl2 exon was expressed at the level of mRNA. Our results show that the flanking operons from rpoC2 (including rpoB, rpoC1, and rpoC2) and rps2 (including rps2, atpA, atpI, and atpH) are actively transcribed in leaf tissue, but that transcripts representing the insert and the ψrpl2 exon are not abundant (fig. 6). The RPKM values for sense (and antisense) mapped reads were 3,298 (6), 854 (1), 149 (12), and 254 (12) for atpI, rps2, the insert, and rpoC2, respectively.Fig. 6.—


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 expression levels of the plastome insert and flanking operons in A. syriaca. The gray plot shows relative sequencing depth for plastome regions flanking the rps2–rpoC2 intergenic spacer; color scheme for plastid genes, plastid spacers, and the mitochondrial insert follows figures 1 and 3. (A) Expression of the 5′-end of rps2 and the flanking insert sequence. (B) Expression of the 3′-end of rpoC2 and flanking insert sequence, including ψrpl2. Plastome coordinates are given on the x axis and read depth on the y axis for both (A) and (B). Note that the scale is not the same in (A) and (B).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt140-F6: Gene expression levels of the plastome insert and flanking operons in A. syriaca. The gray plot shows relative sequencing depth for plastome regions flanking the rps2–rpoC2 intergenic spacer; color scheme for plastid genes, plastid spacers, and the mitochondrial insert follows figures 1 and 3. (A) Expression of the 5′-end of rps2 and the flanking insert sequence. (B) Expression of the 3′-end of rpoC2 and flanking insert sequence, including ψrpl2. Plastome coordinates are given on the x axis and read depth on the y axis for both (A) and (B). Note that the scale is not the same in (A) and (B).
Mentions: We evaluated transcriptome sequences derived from leaf tissue of the same A. syriaca individual used in genomic sequencing to determine whether the ψrpl2 exon was expressed at the level of mRNA. Our results show that the flanking operons from rpoC2 (including rpoB, rpoC1, and rpoC2) and rps2 (including rps2, atpA, atpI, and atpH) are actively transcribed in leaf tissue, but that transcripts representing the insert and the ψrpl2 exon are not abundant (fig. 6). The RPKM values for sense (and antisense) mapped reads were 3,298 (6), 854 (1), 149 (12), and 254 (12) for atpI, rps2, the insert, and rpoC2, respectively.Fig. 6.—

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