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Divergence of RNA polymerase α subunits in angiosperm plastid genomes is mediated by genomic rearrangement.

Blazier JC, Ruhlman TA, Weng ML, Rehman SK, Sabir JS, Jansen RK - Sci Rep (2016)

Bottom Line: Multiple lines of evidence indicated that the rpoA sequences are likely functional despite retaining as low as 30% nucleotide sequence identity with rpoA genes from outgroups in the same angiosperm order.The plastid genomes containing these divergent rpoA genes have experienced extensive structural rearrangement, including large expansions of the inverted repeat.We propose that illegitimate recombination, not positive selection, has driven the divergence of rpoA.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of Texas, Austin, TX 78712, USA.

ABSTRACT
Genes for the plastid-encoded RNA polymerase (PEP) persist in the plastid genomes of all photosynthetic angiosperms. However, three unrelated lineages (Annonaceae, Passifloraceae and Geraniaceae) have been identified with unusually divergent open reading frames (ORFs) in the conserved region of rpoA, the gene encoding the PEP α subunit. We used sequence-based approaches to evaluate whether these genes retain function. Both gene sequences and complete plastid genome sequences were assembled and analyzed from each of the three angiosperm families. Multiple lines of evidence indicated that the rpoA sequences are likely functional despite retaining as low as 30% nucleotide sequence identity with rpoA genes from outgroups in the same angiosperm order. The ratio of non-synonymous to synonymous substitutions indicated that these genes are under purifying selection, and bioinformatic prediction of conserved domains indicated that functional domains are preserved. One of the lineages (Pelargonium, Geraniaceae) contains species with multiple rpoA-like ORFs that show evidence of ongoing inter-paralog gene conversion. The plastid genomes containing these divergent rpoA genes have experienced extensive structural rearrangement, including large expansions of the inverted repeat. We propose that illegitimate recombination, not positive selection, has driven the divergence of rpoA.

No MeSH data available.


Related in: MedlinePlus

Representative maximum likelihood trees and dN/dS values for 12 taxa of Passifloraceae.(A) Likelihood scores for the matK and rpoA trees were lnL −7243.3426 and −4810.9045 lnL, respectively. Branches in bold are members of Passifloraceae. Bootstrap values greater than 50 are shown at the nodes. Scale bar indicates non-synonymous substitutions per codon. (B) Histogram of dN/dS ratios for seven genes for the Passifloraceae. For each gene, dN/dS values (y axis) are given for all branches of interest: the branch leading to the family as well as all internal and terminal branches. The primary branch of interest is the terminal branch to P. biflora, the only species with a divergent rpoA gene. The terminal branch to P. quadrangularis for rpoC1 has a dN/dS value >1, but this is likely an artifact, as the branch length is extremely short. The lack of a bar for rbcL is due to a dS value of 0.
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f3: Representative maximum likelihood trees and dN/dS values for 12 taxa of Passifloraceae.(A) Likelihood scores for the matK and rpoA trees were lnL −7243.3426 and −4810.9045 lnL, respectively. Branches in bold are members of Passifloraceae. Bootstrap values greater than 50 are shown at the nodes. Scale bar indicates non-synonymous substitutions per codon. (B) Histogram of dN/dS ratios for seven genes for the Passifloraceae. For each gene, dN/dS values (y axis) are given for all branches of interest: the branch leading to the family as well as all internal and terminal branches. The primary branch of interest is the terminal branch to P. biflora, the only species with a divergent rpoA gene. The terminal branch to P. quadrangularis for rpoC1 has a dN/dS value >1, but this is likely an artifact, as the branch length is extremely short. The lack of a bar for rbcL is due to a dS value of 0.

Mentions: The dN/dS ratio was calculated for the three different lineages of angiosperms. Seven plastid genes (rpoA, rpoB, rpoC1, rpoC2, ndhF, matK and rbcL) were analyzed in PAML for three datasets to compare the dN/dS ratio of rpoA to the other rpo genes as well as to other non-rpo plastid genes. These same seven genes were used to generate constraint trees for each dataset. Constraint tree topologies were identical to the matK trees for Annonaceae (Fig. 2A) and Passifloraceae (Fig. 3A). The seven gene constraint tree for Geraniaceae is shown as an inset in Fig. 4.


Divergence of RNA polymerase α subunits in angiosperm plastid genomes is mediated by genomic rearrangement.

Blazier JC, Ruhlman TA, Weng ML, Rehman SK, Sabir JS, Jansen RK - Sci Rep (2016)

Representative maximum likelihood trees and dN/dS values for 12 taxa of Passifloraceae.(A) Likelihood scores for the matK and rpoA trees were lnL −7243.3426 and −4810.9045 lnL, respectively. Branches in bold are members of Passifloraceae. Bootstrap values greater than 50 are shown at the nodes. Scale bar indicates non-synonymous substitutions per codon. (B) Histogram of dN/dS ratios for seven genes for the Passifloraceae. For each gene, dN/dS values (y axis) are given for all branches of interest: the branch leading to the family as well as all internal and terminal branches. The primary branch of interest is the terminal branch to P. biflora, the only species with a divergent rpoA gene. The terminal branch to P. quadrangularis for rpoC1 has a dN/dS value >1, but this is likely an artifact, as the branch length is extremely short. The lack of a bar for rbcL is due to a dS value of 0.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834550&req=5

f3: Representative maximum likelihood trees and dN/dS values for 12 taxa of Passifloraceae.(A) Likelihood scores for the matK and rpoA trees were lnL −7243.3426 and −4810.9045 lnL, respectively. Branches in bold are members of Passifloraceae. Bootstrap values greater than 50 are shown at the nodes. Scale bar indicates non-synonymous substitutions per codon. (B) Histogram of dN/dS ratios for seven genes for the Passifloraceae. For each gene, dN/dS values (y axis) are given for all branches of interest: the branch leading to the family as well as all internal and terminal branches. The primary branch of interest is the terminal branch to P. biflora, the only species with a divergent rpoA gene. The terminal branch to P. quadrangularis for rpoC1 has a dN/dS value >1, but this is likely an artifact, as the branch length is extremely short. The lack of a bar for rbcL is due to a dS value of 0.
Mentions: The dN/dS ratio was calculated for the three different lineages of angiosperms. Seven plastid genes (rpoA, rpoB, rpoC1, rpoC2, ndhF, matK and rbcL) were analyzed in PAML for three datasets to compare the dN/dS ratio of rpoA to the other rpo genes as well as to other non-rpo plastid genes. These same seven genes were used to generate constraint trees for each dataset. Constraint tree topologies were identical to the matK trees for Annonaceae (Fig. 2A) and Passifloraceae (Fig. 3A). The seven gene constraint tree for Geraniaceae is shown as an inset in Fig. 4.

Bottom Line: Multiple lines of evidence indicated that the rpoA sequences are likely functional despite retaining as low as 30% nucleotide sequence identity with rpoA genes from outgroups in the same angiosperm order.The plastid genomes containing these divergent rpoA genes have experienced extensive structural rearrangement, including large expansions of the inverted repeat.We propose that illegitimate recombination, not positive selection, has driven the divergence of rpoA.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of Texas, Austin, TX 78712, USA.

ABSTRACT
Genes for the plastid-encoded RNA polymerase (PEP) persist in the plastid genomes of all photosynthetic angiosperms. However, three unrelated lineages (Annonaceae, Passifloraceae and Geraniaceae) have been identified with unusually divergent open reading frames (ORFs) in the conserved region of rpoA, the gene encoding the PEP α subunit. We used sequence-based approaches to evaluate whether these genes retain function. Both gene sequences and complete plastid genome sequences were assembled and analyzed from each of the three angiosperm families. Multiple lines of evidence indicated that the rpoA sequences are likely functional despite retaining as low as 30% nucleotide sequence identity with rpoA genes from outgroups in the same angiosperm order. The ratio of non-synonymous to synonymous substitutions indicated that these genes are under purifying selection, and bioinformatic prediction of conserved domains indicated that functional domains are preserved. One of the lineages (Pelargonium, Geraniaceae) contains species with multiple rpoA-like ORFs that show evidence of ongoing inter-paralog gene conversion. The plastid genomes containing these divergent rpoA genes have experienced extensive structural rearrangement, including large expansions of the inverted repeat. We propose that illegitimate recombination, not positive selection, has driven the divergence of rpoA.

No MeSH data available.


Related in: MedlinePlus