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

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 ? 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.

SUBMITTER: Blazier JC

PROVIDER: S-EPMC4834550 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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

Blazier J Chris JC Ruhlman Tracey A TA Weng Mao-Lun ML Rehman Sumaiyah K SK Sabir Jamal S M JS Jansen Robert K RK

Scientific reports 20160418

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 a ...[more]

PMID: 27087667

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Project description:Background and aimsFully mycoheterotrophic plants derive carbon and other nutrients from root-associated fungi and have lost the ability to photosynthesize. While mycoheterotroph plastomes are often degraded compared with green plants, the effect of this unusual symbiosis on mitochondrial genome evolution is unknown. By providing the first complete organelle genome data from Polygalaceae, one of only three eudicot families that developed mycoheterotrophy, we explore how both organellar genomes evolved after loss of photosynthesis.MethodsWe sequenced and assembled four complete plastid genomes and a mitochondrial genome from species of Polygalaceae, focusing on non-photosynthetic Epirixanthes. We compared these genomes with those of other mycoheterotroph and parasitic plant lineages, and assessed whether organelle genes in Epirixanthes experienced relaxed or intensified selection compared with autotrophic relatives.Key resultsPlastomes of two species of Epirixanthes have become substantially degraded compared with that of autotrophic Polygala. Although the lack of photosynthesis is presumably homologous in the genus, the surveyed Epirixanthes species have marked differences in terms of plastome size, structural rearrangements, gene content and substitution rates. Remarkably, both apparently replaced a canonical plastid inverted repeat with large directly repeated sequences. The mitogenome of E. elongata incorporated a considerable number of fossilized plastid genes, by intracellular transfer from an ancestor with a less degraded plastome. Both plastid and mitochondrial genes in E. elongata have increased substitution rates, but the plastid genes of E. pallida do not. Despite this, both species have similar selection patterns operating on plastid housekeeping genes.ConclusionsPlastome evolution largely fits with patterns of gene degradation seen in other heterotrophic plants, but includes highly unusual directly duplicated regions. The causes of rate elevation in the sequenced Epirixanthes mitogenome and of rate differences in plastomes of related mycoheterotrophic species are not currently understood.

Dataset Information

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

Publications

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

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