The complete nucleotide sequences of the five genetically distinct plastid genomes of Oenothera , subsection Oenothera : I. Sequence evaluation and plastome evolution †

Abstract

The flowering plant genus Oenothera is uniquely suited for studying molecular mechanisms of speciation. It assembles an intriguing combination of genetic features, including permanent translocation heterozygosity, biparental transmission of plastids, and a general interfertility of well-defined species. This allows an exchange of plastids and nuclei between species often resulting in plastome–genome incompatibility. For evaluation of its molecular determinants we present the complete nucleotide sequences of the five basic, genetically distinguishable plastid chromosomes of subsection Oenothera (=Euoenothera) of the genus, which are associated in distinct combinations with six basic genomes. Sizes of the chromosomes range from 163 365 bp (plastome IV) to 165 728 bp (plastome I), display between 96.3% and 98.6% sequence similarity and encode a total of 113 unique genes. Plastome diversification is caused by an abundance of nucleotide substitutions, small insertions, deletions and repetitions. The five plastomes deviate from the general ancestral design of plastid chromosomes of vascular plants by a subsection-specific 56 kb inversion within the large single-copy segment. This inversion disrupted operon structures and predates the divergence of the subsection presumably 1 My ago. Phylogenetic relationships suggest plastomes I–III in one clade, while plastome IV appears to be closest to the common ancestor.

Mutational Pressure Drives Evolution of Synonymous Codon Usage in Genetically Distinct Oenothera plastomes

“…Therefore, high AT 3 (∼ 68.10%) and low GC 3 (∼ 31.70%) can be regarded as the major factors behind SCU variation in Oenothera plastomes similar to what has already been reported in Coffea arabica (5), Populus alba (51), and in both Nicotiana tabacum and Oryza sativa (26). Moreover, point mutations, repetitions, insertions/ deletions and inversions were reported to contribute to base compositional changes in Oenothera (30). The impact of these mutations may reflect in SCU variations across PCGs in Oenothera Influence of GC composition on SCU was further elucidated by correlation analysis between SCUO and GC composition at each codon positions.…”

“…have been completely sequenced (30) and revealed that all plastomes are genetically distinct due to wide nucleotide substitution, small insertions, deletions and repetitions (30). In addition, phylogenetic analysis proved that these plastomes differ from common ancestral origin of vascular plants by a 56 kb inversion within the large single copy region (30).…”

“…Genus Oenothera is considered to be well suited for understanding the various molecular aspects of speciation process as it is amongst well-characterized plant genera (30). The genus Oentothera has been regarded as an ideal model to study evolution of plant genomes (particularly plastids), since substantial information about its systematics and genetics are available (30).…”

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…The increased rates of aa substitution in fast lineages are only modest, and most of the sequence change is caused by indels (Sloan et al 2012a(Sloan et al , 2014a. Furthermore, even in species with typical, slow-evolving plastomes, it is primarily the catalytic C-terminal domain of AccD that is highly conserved, whereas the N-terminal domain, which is plant-specific and has an unknown function, accumulates substantial structural divergence (Greiner et al 2008a). The evolution of accD is further complicated in some angiosperm lineages by functional transfer to the nucleus (Magee et al 2010;Rousseau-Gueutin et al 2013) or by functional replacement with a duplicated and retargeted copy of the homomeric ACCase (Konishi and Sasaki 1994).…”

“…In particular, there is a large N-terminal extension of AccD that is highly variable among angiosperms (Greiner et al 2008a) and absent entirely from E. coli. Likewise, the C-terminal half of ACCA is also unique to plants.…”