Limits...
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.

Show MeSH
Region of horizontal transfer from the mitochondrial genome to the plastome of Asclepias syriaca. (A) Diagram of the A. syriaca plastome and homologous regions of the mitochondrial genome. The mtDNA insert in the plastome and homologous regions in the mitochondrial genome are indicated by black boxes. (B) Sequencing depth of the A. syriaca plastome surrounding the mtDNA insert and the homologous region of the mitochondrial genome.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3814198&req=5

evt140-F1: Region of horizontal transfer from the mitochondrial genome to the plastome of Asclepias syriaca. (A) Diagram of the A. syriaca plastome and homologous regions of the mitochondrial genome. The mtDNA insert in the plastome and homologous regions in the mitochondrial genome are indicated by black boxes. (B) Sequencing depth of the A. syriaca plastome surrounding the mtDNA insert and the homologous region of the mitochondrial genome.

Mentions: Sequencing and assembly of a 158,719-bp A. syriaca plastome (GenBank: KF386166) confirmed a 2,427-bp insertion in the rps2–rpoC2 intergenic spacer (2,677 bp total length; fig. 1A) relative to other angiosperms in the asterid clade (ca. 80,000 species). This insertion is also present in the plastome of a second A. syriaca individual (GenBank: JF433943.1) that we previously sequenced (Straub et al. 2011; Ku et al. 2013), and this region in the newly sequenced individual differs by the insertion of 21 bp, 16 of which are repeated upstream of the insertion, and deletion of 21 bp that comprises a direct repeat in the first individual. The rps2–rpoC2 intergenic spacer ranges from 208 to 327 bp in 28 other photosynthetic asterid species with plastomes in GenBank (table 2). Blast (Altschul et al. 1997) searches of the GenBank nucleotide database using the A. syriaca rps2–rpoC2 spacer region as a query returned high confidence hits to plant mitochondrial genomes, including grape (Vitis vinifera), papaya (Carica papaya), and watermelon (Citrullus lanatus). The putatively homologous mitochondrial region includes rpl2, confirming that the A. syriaca plastome contains a pseudogene (ψrpl2) consisting of the second exon of mitochondrial rpl2. Assembly of the approximately 690 kb milkweed mitochondrial genome from the same individual that we used for plastome sequencing revealed that it contains sequences homologous to the inserted segment in the plastome (fig. 1A), which are split between two regions of 1,091 and 1,401 bp, and separated by 55,845 bp in the master circle of the contemporary A. syriaca mitochondrial genome.Fig. 1.—


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)

Region of horizontal transfer from the mitochondrial genome to the plastome of Asclepias syriaca. (A) Diagram of the A. syriaca plastome and homologous regions of the mitochondrial genome. The mtDNA insert in the plastome and homologous regions in the mitochondrial genome are indicated by black boxes. (B) Sequencing depth of the A. syriaca plastome surrounding the mtDNA insert and the homologous region of the mitochondrial genome.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt140-F1: Region of horizontal transfer from the mitochondrial genome to the plastome of Asclepias syriaca. (A) Diagram of the A. syriaca plastome and homologous regions of the mitochondrial genome. The mtDNA insert in the plastome and homologous regions in the mitochondrial genome are indicated by black boxes. (B) Sequencing depth of the A. syriaca plastome surrounding the mtDNA insert and the homologous region of the mitochondrial genome.
Mentions: Sequencing and assembly of a 158,719-bp A. syriaca plastome (GenBank: KF386166) confirmed a 2,427-bp insertion in the rps2–rpoC2 intergenic spacer (2,677 bp total length; fig. 1A) relative to other angiosperms in the asterid clade (ca. 80,000 species). This insertion is also present in the plastome of a second A. syriaca individual (GenBank: JF433943.1) that we previously sequenced (Straub et al. 2011; Ku et al. 2013), and this region in the newly sequenced individual differs by the insertion of 21 bp, 16 of which are repeated upstream of the insertion, and deletion of 21 bp that comprises a direct repeat in the first individual. The rps2–rpoC2 intergenic spacer ranges from 208 to 327 bp in 28 other photosynthetic asterid species with plastomes in GenBank (table 2). Blast (Altschul et al. 1997) searches of the GenBank nucleotide database using the A. syriaca rps2–rpoC2 spacer region as a query returned high confidence hits to plant mitochondrial genomes, including grape (Vitis vinifera), papaya (Carica papaya), and watermelon (Citrullus lanatus). The putatively homologous mitochondrial region includes rpl2, confirming that the A. syriaca plastome contains a pseudogene (ψrpl2) consisting of the second exon of mitochondrial rpl2. Assembly of the approximately 690 kb milkweed mitochondrial genome from the same individual that we used for plastome sequencing revealed that it contains sequences homologous to the inserted segment in the plastome (fig. 1A), which are split between two regions of 1,091 and 1,401 bp, and separated by 55,845 bp in the master circle of the contemporary A. syriaca mitochondrial genome.Fig. 1.—

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