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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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Evolutionary relationships of the Asclepiadoideae (Apocynaceae) and results of PCR and NGS surveys of the size of the rps2–rpoC2 intergenic spacer in the plastome and for the presence of ψrpoC2 in the mitochondrial genome downstream of rpl2. The topology of the phylogenetic tree of the relationships among tribes of Asclepiadoideae and subtribes of Asclepiadeae is a summary of the plastome phylogeny obtained in this study (fig. 4) augmented with the relationships of major clades not sampled here, as indicated by previous phylogenetic studies of ptDNA sequences (Liede 2001; Liede and Täuber 2002; Rapini et al. 2003; Liede-Schumann et al. 2005; Rapini et al. 2007; Livshultz 2010). The hash mark represents horizontal transfer of DNA from the mitochondrial genome to the plastome in the common ancestor of Asclepiadeae. The circles and squares represent PCR and NGS screening of the size of the rps2–rpoC2 intergenic spacer and presence of ψrpoC2, respectively. The colors of the circles and squares indicate which method was used. Details of species sampling are given in table 1.
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evt140-F2: Evolutionary relationships of the Asclepiadoideae (Apocynaceae) and results of PCR and NGS surveys of the size of the rps2–rpoC2 intergenic spacer in the plastome and for the presence of ψrpoC2 in the mitochondrial genome downstream of rpl2. The topology of the phylogenetic tree of the relationships among tribes of Asclepiadoideae and subtribes of Asclepiadeae is a summary of the plastome phylogeny obtained in this study (fig. 4) augmented with the relationships of major clades not sampled here, as indicated by previous phylogenetic studies of ptDNA sequences (Liede 2001; Liede and Täuber 2002; Rapini et al. 2003; Liede-Schumann et al. 2005; Rapini et al. 2007; Livshultz 2010). The hash mark represents horizontal transfer of DNA from the mitochondrial genome to the plastome in the common ancestor of Asclepiadeae. The circles and squares represent PCR and NGS screening of the size of the rps2–rpoC2 intergenic spacer and presence of ψrpoC2, respectively. The colors of the circles and squares indicate which method was used. Details of species sampling are given in table 1.

Mentions: To place the transfer event into an evolutionary context, we surveyed 22 other species of Apocynaceae to determine whether they shared the mitochondrial segment of DNA in the rps2–rpoC2 intergenic spacer (table 1). First, we used PCR to screen 17 species spanning three of four subfamilies of Apocynaceae, with sampling concentrated in Asclepiadoideae, the subfamily to which A. syriaca belongs, to determine whether the spacer region was similar in size to that observed in A. syriaca, or whether it was more typical of other asterids (fig. 2). All members of tribe Asclepiadeae (subfamily Asclepiadoideae) with successful PCR amplification had spacer regions as large as or larger than A. syriaca. The large spacer region was also present in Eustegia (table 1), an enigmatic monotypic African genus that, while possessing synapomorphic features of tribe Asclepiadeae (Bruyns 1999), has been resolved in phylogenetic analyses of plastid sequence data alternatively as sister to the rest of the Asclepiadeae (Liede 2001) or as the sister group of the tribes Marsdenieae and Ceropegieae (Rapini et al. 2003; Meve and Liede 2004; Rapini et al. 2007). Members of tribes Fockeeae, Marsdenieae, and Ceropegieae of Asclepiadoideae and subfamilies Secamonoideae, Periplocoideae, and Apocynoideae did not show evidence of an insertion in the spacer region (table 1).Fig. 2.—


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)

Evolutionary relationships of the Asclepiadoideae (Apocynaceae) and results of PCR and NGS surveys of the size of the rps2–rpoC2 intergenic spacer in the plastome and for the presence of ψrpoC2 in the mitochondrial genome downstream of rpl2. The topology of the phylogenetic tree of the relationships among tribes of Asclepiadoideae and subtribes of Asclepiadeae is a summary of the plastome phylogeny obtained in this study (fig. 4) augmented with the relationships of major clades not sampled here, as indicated by previous phylogenetic studies of ptDNA sequences (Liede 2001; Liede and Täuber 2002; Rapini et al. 2003; Liede-Schumann et al. 2005; Rapini et al. 2007; Livshultz 2010). The hash mark represents horizontal transfer of DNA from the mitochondrial genome to the plastome in the common ancestor of Asclepiadeae. The circles and squares represent PCR and NGS screening of the size of the rps2–rpoC2 intergenic spacer and presence of ψrpoC2, respectively. The colors of the circles and squares indicate which method was used. Details of species sampling are given in table 1.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3814198&req=5

evt140-F2: Evolutionary relationships of the Asclepiadoideae (Apocynaceae) and results of PCR and NGS surveys of the size of the rps2–rpoC2 intergenic spacer in the plastome and for the presence of ψrpoC2 in the mitochondrial genome downstream of rpl2. The topology of the phylogenetic tree of the relationships among tribes of Asclepiadoideae and subtribes of Asclepiadeae is a summary of the plastome phylogeny obtained in this study (fig. 4) augmented with the relationships of major clades not sampled here, as indicated by previous phylogenetic studies of ptDNA sequences (Liede 2001; Liede and Täuber 2002; Rapini et al. 2003; Liede-Schumann et al. 2005; Rapini et al. 2007; Livshultz 2010). The hash mark represents horizontal transfer of DNA from the mitochondrial genome to the plastome in the common ancestor of Asclepiadeae. The circles and squares represent PCR and NGS screening of the size of the rps2–rpoC2 intergenic spacer and presence of ψrpoC2, respectively. The colors of the circles and squares indicate which method was used. Details of species sampling are given in table 1.
Mentions: To place the transfer event into an evolutionary context, we surveyed 22 other species of Apocynaceae to determine whether they shared the mitochondrial segment of DNA in the rps2–rpoC2 intergenic spacer (table 1). First, we used PCR to screen 17 species spanning three of four subfamilies of Apocynaceae, with sampling concentrated in Asclepiadoideae, the subfamily to which A. syriaca belongs, to determine whether the spacer region was similar in size to that observed in A. syriaca, or whether it was more typical of other asterids (fig. 2). All members of tribe Asclepiadeae (subfamily Asclepiadoideae) with successful PCR amplification had spacer regions as large as or larger than A. syriaca. The large spacer region was also present in Eustegia (table 1), an enigmatic monotypic African genus that, while possessing synapomorphic features of tribe Asclepiadeae (Bruyns 1999), has been resolved in phylogenetic analyses of plastid sequence data alternatively as sister to the rest of the Asclepiadeae (Liede 2001) or as the sister group of the tribes Marsdenieae and Ceropegieae (Rapini et al. 2003; Meve and Liede 2004; Rapini et al. 2007). Members of tribes Fockeeae, Marsdenieae, and Ceropegieae of Asclepiadoideae and subfamilies Secamonoideae, Periplocoideae, and Apocynoideae did not show evidence of an insertion in the spacer region (table 1).Fig. 2.—

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