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

J Chris Blazier,Tracey A Ruhlman,Mao-Lun Weng,Jamal S M Sabir,Sumaiyah K Rehman,Robert K Jansen

doi:10.1038/srep24595

J Chris Blazier, Tracey A Ruhlman + Show 4 more

Open Access

https://doi.org/10.1038/srep24595

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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.

Highlights

Identified highly divergent rpoA sequences encoded in the plastomes of P. x hortorum and Passiflora biflora, no further data are available for Annona
The inverted repeat (IR) has greatly expanded at both the IRB/small single copy (SSC) and IRB/large single copy (LSC) boundaries
Gene order is highly conserved compared to the ancestral plastid genome organization for angiosperms[7] with a single inversion involving six genes in the LSC (Fig. S1)

Summary

Introduction

Identified highly divergent rpoA sequences encoded in the plastomes of P. x hortorum and Passiflora biflora, no further data are available for Annona. No other plastome is known to harbor multiple paralogs of this gene, and it is difficult to judge which, if any, of these divergent genes are functional. It is unclear whether they have diverged due to positive or relaxed selection or by some unusual, locus-specific neutral process. It is possible that rpoA has been transferred to the nucleus and that the divergence of the gene reflects relaxed selection on the plastid copy in the wake of its functional replacement by a nuclear paralog. Illegitimate recombination is evident in the large changes in the inverted repeat (IR) boundaries in all three lineages

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Conclusion