Genes Translocated into the Plastid Inverted Repeat Show Decelerated Substitution Rates and Elevated GC Content

Abstract

Plant chloroplast genomes (plastomes) are characterized by an inverted repeat (IR) region and two larger single copy (SC) regions. Patterns of molecular evolution in the IR and SC regions differ, most notably by a reduced rate of nucleotide substitution in the IR compared to the SC region. In addition, the organization and structure of plastomes is fluid, and rearrangements through time have repeatedly shuffled genes into and out of the IR, providing recurrent natural experiments on how chloroplast genome structure can impact rates and patterns of molecular evolution. Here we examine four loci (psbA, ycf2, rps7, and rps12 exon 2–3) that were translocated from the SC into the IR during fern evolution. We use a model-based method, within a phylogenetic context, to test for substitution rate shifts. All four loci show a significant, 2- to 3-fold deceleration in their substitution rate following translocation into the IR, a phenomenon not observed in any other, nontranslocated plastid genes. Also, we show that after translocation, the GC content of the third codon position and of the noncoding regions is significantly increased, implying that gene conversion within the IR is GC-biased. Taken together, our results suggest that the IR region not only reduces substitution rates, but also impacts nucleotide composition. This finding highlights a potential vulnerability of correlating substitution rate heterogeneity with organismal life history traits without knowledge of the underlying genome structure.

Recombination‐dependent replication and gene conversion homogenize repeat sequences and diversify plastid genome structure

“…A hallmark of gene conversion between repeated sequences is elevated GC content (Mugal et al, 2015). Recent studies have demonstrated that in addition to suppression of nucleotide substitution rates relative to single copy sequence, IR sequences experience GC‐biased gene conversion (Wu and Chaw, 2015; Li et al, 2016). The GC content of the M. emarginata plastome overall was high relative to typical land plants (mean 37.6%, >1000 species, Weng et al, 2016 a ) at 40.2%, yet it is not elevated relative to some other plastomes with atypical structure, i.e., long branch clade (LBC) Erodium (mean 44.1%, Blazier et al, 2016a) and Silene L. (mean 40.4%, calculated from complete plastomes on GenBank accessed 28 November 2016).…”

Order‐level fern plastome phylogenomics: new insights from Hymenophyllales

“…For phylogenetic analyses, we included only protein‐coding genes that were consistently present in the single copy regions (SC) across all sampled plastomes. Loci that had moved into or out of the IR were excluded because they exhibit significant substitution rate heterogeneities (Li et al., ). In total, 71 genes were included.…”

Lycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat

“…Plastomes of photoautotrophic land plants typically range from 120 to 160 kb in length, with c. 80 protein-coding genes, four rRNAs, and c. 30 tRNAs arranged into a structure that usually includes large and small single-copy (SC) regions (termed LSC and SSC) separated by a large inverted repeat (IR) in two copies (Wicke et al, 2011;Jansen & Ruhlman, 2012;Mower & Vickrey, 2018). One of the most notable effects of this genomic structure is that substitution rates are several times lower in the IR relative to SC regions (Wolfe et al, 1987;Perry & Wolfe, 2002;Li et al, 2016;Zhu et al, 2016). This reduction in IR substitution rates has been attributed to a copy-dependent repair mechanism such as biased gene conversion (Birky & Walsh, 1992), which may be facilitated by frequent intramolecular recombination between IR copies that produces two isomeric forms of the plastome (Bohnert & Loffelhardt, 1982;Palmer, 1983).…”