Extreme Reconfiguration of Plastid Genomes in the Angiosperm Family Geraniaceae: Rearrangements, Repeats, and Codon Usage

Abstract

Geraniaceae plastid genomes (plastomes) have experienced a remarkable number of genomic changes. The plastomes of Erodium texanum, Geranium palmatum, and Monsonia speciosa were sequenced and compared with other rosids and the previously published Pelargonium hortorum plastome. Geraniaceae plastomes were found to be highly variable in size, gene content and order, repetitive DNA, and codon usage. Several unique plastome rearrangements include the disruption of two highly conserved operons (S10 and rps2-atpA), and the inverted repeat (IR) region in M. speciosa does not contain all genes in the ribosomal RNA operon. The sequence of M. speciosa is unusually small (128,787 bp); among angiosperm plastomes sequenced to date, only those of nonphotosynthetic species and those that have lost one IR copy are smaller. In contrast, the plastome of P. hortorum is the largest, at 217,942 bp. These genomes have experienced numerous gene and intron losses and partial and complete gene duplications. Some of the losses are shared throughout the family (e.g., trnT-GGU and the introns of rps16 and rpl16); however, other losses are homoplasious (e.g., trnG-UCC intron in G. palmatum and M. speciosa). IR length is also highly variable. The IR in P. hortorum was previously shown to be greatly expanded to 76 kb, and the IR is lost in E. texanum and reduced in G. palmatum (11 kb) and M. speciosa (7 kb). Geraniaceae plastomes contain a high frequency of large repeats (>100 bp) relative to other rosids. Within each plastome, repeats are often located at rearrangement end points and many repeats shared among the four Geraniaceae flank rearrangement end points. GC content is elevated in the genomes and also in coding regions relative to other rosids. Codon usage per amino acid and GC content at third position sites are significantly different for Geraniaceae protein-coding sequences relative to other rosids. Our findings suggest that relaxed selection and/or mutational biases lead to increased GC content, and this in turn altered codon usage. We propose that increases in genomic rearrangements, repetitive DNA, nucleotide substitutions, and GC content may be caused by relaxed selection resulting from improper DNA repair.

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…In numerous angiosperm lineages, a subset of plastid genes, including clpP1 and accD, display accelerated evolutionary rates, but the causes of this recurring phenomenon have remained unclear (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Blazier et al 2016;Zhang et al 2016). We investigated the nuclear genes that contribute to the multisubunit complexes that include ClpP1 and AccD, and incorporated population genetic and structural data to distinguish between relaxed purifying selection and positive selection as drivers of elevated d N /d S values.…”

“…Within angiosperms, most plastid genomes are highly conserved in sequence and structure (Jansen et al 2007;Wicke et al 2011), but multiple independent lineages have experienced accelerated rates of aa substitution in similar subsets of nonphotosynthetic genes (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Zhang et al 2016). Several mechanisms have been hypothesized to explain these repeated accelerations including positive selection, reduced effective population size (N e ), altered DNA repair, changes in gene expression, and pseudogenization following gene transfer to the nucleus (see above citations).…”

Natural Variation in Sensitivity to a Loss of Chloroplast Translation in Arabidopsis

“…nonfunctional or missing altogether (Chumley et al, 2006;Guisinger et al, 2011;Straub et al, 2011;. This implies that a redundant nuclear gene remains to be identified because fatty acid biosynthesis is essential.…”

“…Several common herbicides target this novel enzyme (Kaundun, 2014). The chloroplast ycf1 gene is also absent from the Poaceae and is missing or disrupted in selected members of other families (Chumley et al, 2006;Magee et al, 2010;Guisinger et al, 2011;Straub et al, 2011;. The ycf2 gene is lost in many of these lineages as well.…”

The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms

“…Although "indel" is shorthand for insertion/deletion, bona fide insertions are rare in angiosperm plastomes: The vast majority of evolutionary changes result from point mutations, tandem duplications, deletions, and small-scale rearrangements such as hairpin inversions or RNA-mediated intron loss (3,25,26). Previous reports of naturally occurring insertion of foreign (extraplastid) DNA were appropriately cautious because small segments of foreign DNA in intergenic regions may not be readily identified in comparisons among distantly related species (27,28). The newly sequenced plastomes provide unequivocal evidence of large, foreign DNA insertions that apparently contain protein-coding genes, which is unprecedented among angiosperms and account for many, but not all, of the genome rearrangements.…”