Extensive Reorganization of the Plastid Genome of Trifolium subterraneum (Fabaceae) Is Associated with Numerous Repeated Sequences and Novel DNA Insertions

Abstract

The plastid genome of Trifolium subterraneum is 144,763 bp, about 20 kb longer than those of closely related legumes, which also lost one copy of the large inverted repeat (IR). The genome has undergone extensive genomic reconfiguration, including the loss of six genes (accD, infA, rpl22, rps16, rps18, and ycf1) and two introns (clpP and rps12) and numerous gene order changes, attributable to 14-18 inversions. All endpoints of rearranged gene clusters are flanked by repeated sequences, tRNAs, or pseudogenes. One unusual feature of the Trifolium subterraneum genome is the large number of dispersed repeats, which comprise 19.5% (ca. 28 kb) of the genome (versus about 4% for other angiosperms) and account for part of the increase in genome size. Nine genes (psbT, rbcL, clpP, rps3, rpl23, atpB, psbN, trnI-cau, and ycf3) have also been duplicated either partially or completely. rpl23 is the most highly duplicated gene, with portions of this gene duplicated six times. Comparisons of the Trifolium plastid genome with the Plant Repeat Database and searches for flanking inverted repeats suggest that the high incidence of dispersed repeats and rearrangements is not likely the result of transposition. Trifolium has 19.5 kb of unique DNA distributed among 160 fragments ranging in size from 30 to 494 bp, greatly surpassing the other five sequenced legume plastid genomes in novel DNA content. At least some of this unique DNA may represent horizontal transfer from bacterial genomes. These unusual features provide direction for the development of more complex models of plastid genome evolution.

Potential Functional Replacement of the Plastidic Acetyl-CoA Carboxylase Subunit (accD) Gene by Recent Transfers to the Nucleus in Some Angiosperm Lineages

“…Plastome organization, gene content, and gene order are generally well conserved among flowering plants. However, recent complete sequencing revealed that the plastomes in a few plant families, such as the Campanulaceae, Fabaceae, and Geraniaceae, are highly rearranged, causing the disruption of operons and loss of genes (Cosner et al, 1997;Cai et al, 2008;Haberle et al, 2008;Guisinger et al, 2011). It has been suggested that a higher number of repeat sequences present in these rearranged plastomes (Guisinger et al, , 2011 can promote illegitimate homologous recombination and cause these multiple structural changes (Maréchal and Brisson, 2010).…”

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.…”

Characterization and Phylogenetic Analysis of Chloroplast and Mitochondria Genomes from the Antarctic Polytrichaceae Species Polytrichum juniperinum and Polytrichum strictum

“…However, this small size does not interfere with the G + C content, which is high. The plastid genomes of the closest Polytrichum species have a GC percentage of 28% to 33% [21,22] and those of seed plants range between 34% and 40% [50]. Cai et al, observed high G + C contents in the chloroplast coding regions, and certain regions had higher percentages than others, such as the IR region with its four genes with high levels of G and C [51].…”

“…Some genes seem to have been lost multiple times in the chloroplast and mitochondrial genomes during evolution [50], and other genes appear to be present or absent only in particular clades. For example, diverse genes are lacking in mosses and liverworts, such as rps16; however, the gene is present in hornworts and some vascular plants.…”

“…The mitochondrial genome shows conservation between Antarctic Polytrichum species. Previous studies have shown that the structural evolution of the mitochondrial genome is highly conservative not only within each individual lineage but also across mosses; however, this is most evident when compared with more distant orders within the large group Bryophyta that shows some rearrangements that are very conserved [50]. The occurrence of some rearrangements was observed between Marchantia polymorpha mtDNA and P. patens, as these species diverged more than 375 million years ago [69].…”