A comparative analysis of whole plastid genomes from the apiales: Expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions

Stephen R. Downie, Robert K. Jansen

Research output: Contribution to journalArticle

Abstract

Previous mapping studies have revealed that the frequency and large size of inverted repeat junction shifts in Apiaceae plastomes are unusual among angiosperms. To further examine plastome structural organization and inverted repeat evolution in the Apiales (Apiaceae + Araliaceae), we have determined the complete plastid genome sequences of five taxa, namely Anthriscus cerefolium (154,719 base pairs), Crithmum maritimum (158,355 base pairs), Hydrocotyle verticillata (153,207 base pairs), Petroselinum crispum (152,890 base pairs), and Tiedemannia filiformis subsp. greenmanii (154,737 base pairs), and compared the results obtained to previously published plastomes of Daucus carota subsp. sativus and Panax schin-seng. We also compared the five Apiaceae plastomes to identify highly variable noncoding loci for future molecular evolutionary and systematic studies at low taxonomic levels. With the exceptions of Crithmum and Petroselinum, which each demonstrate a ∼1.5 kilobase shift of its LSC-IRB junction (JLB), all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structural organization, gene arrangement, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to the LSC-IRA junction (JLA). These insertions (of 1,463 and 345 base pairs, respectively) show no sequence similarity to any other region of their plastid genomes, and BLAST searches of the Petroselinum insert resulted in multiple hits to angiosperm mitochondrial genome sequences, indicative of a mitochondrial to plastid transfer of DNA. A comparison of pairwise sequence divergence values and numbers of variable and parsimony-informative alignment positions (among other sequence characteristics) across all introns and intergenic spacers >150 base pairs in the five Apiaceae plastomes revealed that the rpl32-TrnL, trnE-TrnT, ndhF-rpl32, 5′rps16-TrnQ, and trnT-psbD intergenic spacers are among the most fast-evolving loci, with the trnD-TrnY-TrnE-TrnT combined region presenting the greatest number of potentially informative characters overall. These regions are therefore likely to be the best choices for molecular evolutionary and systematic studies at low taxonomic levels. Repeat analysis revealed direct and inverted dispersed repeats of 30 base pairs or more that may be useful in population-level studies. These structural and sequence analyses contribute to a better understanding of plastid genome evolution in the Apiales and provide valuable new information on the phylogenetic utility of plastid noncoding loci, enabling further molecular evolutionary and phylogenetic studies on this economically, ecologically, and medicinally important group of flowering plants.

Original languageEnglish (US)
Pages (from-to)336-351
Number of pages16
JournalSystematic Botany
Volume40
Issue number1
DOIs
StatePublished - Jan 1 2015

Fingerprint

Apiales
Plastid Genomes
transfer DNA
Plastids
plastid DNA
plastid
Base Pairing
contraction
genome
Petroselinum
Apiaceae
DNA
angiosperm
Angiosperms
Angiospermae
Crithmum
intergenic DNA
loci
phylogenetics
Anthriscus cerefolium

Keywords

  • Apiaceae
  • Araliaceae
  • intergenic spacer regions
  • intracellular transfer
  • plastid DNA

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Plant Science

Cite this

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title = "A comparative analysis of whole plastid genomes from the apiales: Expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions",
abstract = "Previous mapping studies have revealed that the frequency and large size of inverted repeat junction shifts in Apiaceae plastomes are unusual among angiosperms. To further examine plastome structural organization and inverted repeat evolution in the Apiales (Apiaceae + Araliaceae), we have determined the complete plastid genome sequences of five taxa, namely Anthriscus cerefolium (154,719 base pairs), Crithmum maritimum (158,355 base pairs), Hydrocotyle verticillata (153,207 base pairs), Petroselinum crispum (152,890 base pairs), and Tiedemannia filiformis subsp. greenmanii (154,737 base pairs), and compared the results obtained to previously published plastomes of Daucus carota subsp. sativus and Panax schin-seng. We also compared the five Apiaceae plastomes to identify highly variable noncoding loci for future molecular evolutionary and systematic studies at low taxonomic levels. With the exceptions of Crithmum and Petroselinum, which each demonstrate a ∼1.5 kilobase shift of its LSC-IRB junction (JLB), all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structural organization, gene arrangement, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to the LSC-IRA junction (JLA). These insertions (of 1,463 and 345 base pairs, respectively) show no sequence similarity to any other region of their plastid genomes, and BLAST searches of the Petroselinum insert resulted in multiple hits to angiosperm mitochondrial genome sequences, indicative of a mitochondrial to plastid transfer of DNA. A comparison of pairwise sequence divergence values and numbers of variable and parsimony-informative alignment positions (among other sequence characteristics) across all introns and intergenic spacers >150 base pairs in the five Apiaceae plastomes revealed that the rpl32-TrnL, trnE-TrnT, ndhF-rpl32, 5′rps16-TrnQ, and trnT-psbD intergenic spacers are among the most fast-evolving loci, with the trnD-TrnY-TrnE-TrnT combined region presenting the greatest number of potentially informative characters overall. These regions are therefore likely to be the best choices for molecular evolutionary and systematic studies at low taxonomic levels. Repeat analysis revealed direct and inverted dispersed repeats of 30 base pairs or more that may be useful in population-level studies. These structural and sequence analyses contribute to a better understanding of plastid genome evolution in the Apiales and provide valuable new information on the phylogenetic utility of plastid noncoding loci, enabling further molecular evolutionary and phylogenetic studies on this economically, ecologically, and medicinally important group of flowering plants.",
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T1 - A comparative analysis of whole plastid genomes from the apiales

T2 - Expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions

AU - Downie, Stephen R.

AU - Jansen, Robert K.

PY - 2015/1/1

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N2 - Previous mapping studies have revealed that the frequency and large size of inverted repeat junction shifts in Apiaceae plastomes are unusual among angiosperms. To further examine plastome structural organization and inverted repeat evolution in the Apiales (Apiaceae + Araliaceae), we have determined the complete plastid genome sequences of five taxa, namely Anthriscus cerefolium (154,719 base pairs), Crithmum maritimum (158,355 base pairs), Hydrocotyle verticillata (153,207 base pairs), Petroselinum crispum (152,890 base pairs), and Tiedemannia filiformis subsp. greenmanii (154,737 base pairs), and compared the results obtained to previously published plastomes of Daucus carota subsp. sativus and Panax schin-seng. We also compared the five Apiaceae plastomes to identify highly variable noncoding loci for future molecular evolutionary and systematic studies at low taxonomic levels. With the exceptions of Crithmum and Petroselinum, which each demonstrate a ∼1.5 kilobase shift of its LSC-IRB junction (JLB), all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structural organization, gene arrangement, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to the LSC-IRA junction (JLA). These insertions (of 1,463 and 345 base pairs, respectively) show no sequence similarity to any other region of their plastid genomes, and BLAST searches of the Petroselinum insert resulted in multiple hits to angiosperm mitochondrial genome sequences, indicative of a mitochondrial to plastid transfer of DNA. A comparison of pairwise sequence divergence values and numbers of variable and parsimony-informative alignment positions (among other sequence characteristics) across all introns and intergenic spacers >150 base pairs in the five Apiaceae plastomes revealed that the rpl32-TrnL, trnE-TrnT, ndhF-rpl32, 5′rps16-TrnQ, and trnT-psbD intergenic spacers are among the most fast-evolving loci, with the trnD-TrnY-TrnE-TrnT combined region presenting the greatest number of potentially informative characters overall. These regions are therefore likely to be the best choices for molecular evolutionary and systematic studies at low taxonomic levels. Repeat analysis revealed direct and inverted dispersed repeats of 30 base pairs or more that may be useful in population-level studies. These structural and sequence analyses contribute to a better understanding of plastid genome evolution in the Apiales and provide valuable new information on the phylogenetic utility of plastid noncoding loci, enabling further molecular evolutionary and phylogenetic studies on this economically, ecologically, and medicinally important group of flowering plants.

AB - Previous mapping studies have revealed that the frequency and large size of inverted repeat junction shifts in Apiaceae plastomes are unusual among angiosperms. To further examine plastome structural organization and inverted repeat evolution in the Apiales (Apiaceae + Araliaceae), we have determined the complete plastid genome sequences of five taxa, namely Anthriscus cerefolium (154,719 base pairs), Crithmum maritimum (158,355 base pairs), Hydrocotyle verticillata (153,207 base pairs), Petroselinum crispum (152,890 base pairs), and Tiedemannia filiformis subsp. greenmanii (154,737 base pairs), and compared the results obtained to previously published plastomes of Daucus carota subsp. sativus and Panax schin-seng. We also compared the five Apiaceae plastomes to identify highly variable noncoding loci for future molecular evolutionary and systematic studies at low taxonomic levels. With the exceptions of Crithmum and Petroselinum, which each demonstrate a ∼1.5 kilobase shift of its LSC-IRB junction (JLB), all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structural organization, gene arrangement, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to the LSC-IRA junction (JLA). These insertions (of 1,463 and 345 base pairs, respectively) show no sequence similarity to any other region of their plastid genomes, and BLAST searches of the Petroselinum insert resulted in multiple hits to angiosperm mitochondrial genome sequences, indicative of a mitochondrial to plastid transfer of DNA. A comparison of pairwise sequence divergence values and numbers of variable and parsimony-informative alignment positions (among other sequence characteristics) across all introns and intergenic spacers >150 base pairs in the five Apiaceae plastomes revealed that the rpl32-TrnL, trnE-TrnT, ndhF-rpl32, 5′rps16-TrnQ, and trnT-psbD intergenic spacers are among the most fast-evolving loci, with the trnD-TrnY-TrnE-TrnT combined region presenting the greatest number of potentially informative characters overall. These regions are therefore likely to be the best choices for molecular evolutionary and systematic studies at low taxonomic levels. Repeat analysis revealed direct and inverted dispersed repeats of 30 base pairs or more that may be useful in population-level studies. These structural and sequence analyses contribute to a better understanding of plastid genome evolution in the Apiales and provide valuable new information on the phylogenetic utility of plastid noncoding loci, enabling further molecular evolutionary and phylogenetic studies on this economically, ecologically, and medicinally important group of flowering plants.

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KW - Araliaceae

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KW - intracellular transfer

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