The Complete Chloroplast Genome Sequence of Pelargonium × hortorum: Organization and Evolution of the Largest and Most Highly Rearranged Chloroplast Genome of Land Plants

Abstract

The chloroplast genome of Pelargonium x hortorum has been completely sequenced. It maps as a circular molecule of 217,942 bp and is both the largest and most rearranged land plant chloroplast genome yet sequenced. It features 2 copies of a greatly expanded inverted repeat (IR) of 75,741 bp each and, consequently, diminished single-copy regions of 59,710 and 6,750 bp. Despite the increase in size and complexity of the genome, the gene content is similar to that of other angiosperms, with the exceptions of a large number of pseudogenes, the recognition of 2 open reading frames (ORF56 and ORF42) in the trnA intron with similarities to previously identified mitochondrial products (ACRS and pvs-trnA), the losses of accD and trnT-ggu and, in particular, the presence of a highly divergent set of rpoA-like ORFs rather than a single, easily recognized gene for rpoA. The 3-fold expansion of the IR (relative to most angiosperms) accounts for most of the size increase of the genome, but an additional 10% of the size increase is related to the large number of repeats found. The Pelargonium genome contains 35 times as many 31 bp or larger repeats than the unrearranged genome of Spinacia. Most of these repeats occur near the rearrangement hotspots, and 2 different associations of repeats are localized in these regions. These associations are characterized by full or partial duplications of several genes, most of which appear to be nonfunctional copies or pseudogenes. These duplications may also be linked to the disruption of at least 1 but possibly 2 or 3 operons. We propose simple models that account for the major rearrangements with a minimum of 8 IR boundary changes and 12 inversions in addition to several insertions of duplicated sequence.

Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions

“…Pelargonium X hortorum contains the most highly rearranged angiosperm plastid genome sequenced to date (16), and based on restriction site mapping studies, plastid genomes in other Geraniaceae are also highly rearranged (17). A significant positive correlation between rates of nucleotide substitutions and genome rearrangements was recently shown for plastid genomes (18).…”

“…Geraniaceae are an ideal group to study plastid genome evolution, because they are highly rearranged (16,17). In this study, we examine rates and patterns of sequence evolution across Geraniaceae and provide evidence for major locus-and lineage-specific substitution rate increases.…”

“…Second, Geraniaceae plastid genomes are structurally unusual. The plastid genome of Pelargonium X hortorum exhibits unprecedented levels of change in both gene order and content (16). This genome also contains the largest IR, along with numerous dispersed repeats contributing to increased genome size and potential rearrangement hotspots.…”

Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae)

“…Changes in this highly conserved organization of plastid genomes have been utilized to resolve phylogenetic relationships among major clades in a number of angiosperm families, including Asteraceae (Jansen and Palmer, 1987;Kim et al, 2005), Berberidaceae (Kim and Jansen, 1995), Cactaceae (Wallace and Cota, 1996), Campanulaceae (Cosner et al, 2004), Leguminosae (Bruneau et al, 1990;Lavin et al, 1990;Doyle et al, 1995;Doyle et al, 1996), Geraniaceae (Chumley et al, 2006), Lobeliaceae (Knox et al, 1993), Oleaceae , Onagraceae (Hachtel et al, 1991;Greiner et al, 2008), Poaceae (Doyle et al, 1992), and Ranunculaceae (Hoot and Palmer, 1994;Johansson, 1999). The types of changes that have been used include inversions, loss of the 22-25 kb IR which contains a duplicated set of rRNA and tRNA genes, expansion/contraction of the IR, and gene/intron loss (Downie and Palmer, 1992).…”

“…Thus, the legumes represent one of only a few angiosperm families that have experienced multiple, plastid genomic rearrangements and gene/intron losses , and serve as an excellent choice in which to investigate contrasting patterns of plastid DNA evolution. Others families known to have comparable plastid genomic rearrangements include Asteraceae (two inversions; Jansen and Palmer, 1987;Kim et al, 2005), Campanulaceae (up to 42 inversions, two gene losses, 8 putative transpositions; Cosner et al, 1997Cosner et al, , 2004Haberle et al, 2008), Geraniaceae (12 inversions, 8 IR boundary changes; Chumley et al, 2006), Lobeliaceae (11 inversions; Knox et al, 1993), Oleaceae (4 inversions, 1 gene loss, 1 intron loss, 5 gene duplications; Lee et al, 2007), Poaceae (3 inversions, 3 gene losses, 2 intron losses; Doyle et al, 1992), and Ranunculaceae (9 inversions, 1 intron loss; Hoot and Palmer, 1994;Johansson, 1999).…”