Plastome-Wide Nucleotide Substitution Rates Reveal Accelerated Rates in Papilionoideae and Correlations with Genome Features Across Legume Subfamilies

Abstract

This study represents the most comprehensive plastome-wide comparison of nucleotide substitution rates across the three subfamilies of Fabaceae: Caesalpinioideae, Mimosoideae, and Papilionoideae. Caesalpinioid and mimosoid legumes have large, unrearranged plastomes compared with papilionoids, which exhibit varying levels of rearrangement including the loss of the inverted repeat (IR) in the IR-lacking clade (IRLC). Using 71 genes common to 39 legume taxa representing all the three subfamilies, we show that papilionoids consistently have higher nucleotide substitution rates than caesalpinioids and mimosoids, and rates in the IRLC papilionoids are generally higher than those in the IR-containing papilionoids. Unsurprisingly, this pattern was significantly correlated with growth habit as most papilionoids are herbaceous, whereas caesalpinioids and mimosoids are largely woody. Both nonsynonymous (dN) and synonymous (dS) substitution rates were also correlated with several biological features including plastome size and plastomic rearrangements such as the number of inversions and indels. In agreement with previous reports, we found that genes in the IR exhibit between three and fourfold reductions in the substitution rates relative to genes within the large single-copy or small single-copy regions. Furthermore, former IR genes in IR-lacking taxa exhibit accelerated rates compared with genes contained in the IR.

A Repertory of Rearrangements and the Loss of an Inverted Repeat Region in Passiflora Chloroplast Genomes

“…1990 ). In addition, the rates of nucleotide substitution in genes of the IRLC-papilionoids are generally higher than those found in the IR-containing papilionoids ( Schwarz et al. 2017 ).…”

Plastome phylogenomic study of Gentianeae (Gentianaceae): widespread gene tree discordance and its association with evolutionary rate heterogeneity of plastid genes

“…Estimating nucleotide substitution rates among different genes and different functional groups provided insight into the diverse selection regimes acting on plastomes evolution (e.g. [ 16 , 20 , 22 ]). In Poaceae [ 34 ] and Geraniaceae [ 17 ], it has been reported that genes encoding subunits involved in photosynthetic processes, such as NAD(P)H dehydrogenase (NDH), ATP synthase (ATP), photosystems I and II (PSA and PSB), and cytochrome b6f complex (PET), exhibit relatively lower nucleotide substitution rates than other functional groups of genes.…”

“…Similar patterns have been previously documented, such as RPL and RPS genes were shown to be highly accelerated in Geraniaceae [ 20 , 28 ] and RPO genes in Annonaceae, Passifloraceae and Geraniaceae [ 52 ]. In addition , accD, clpP, ycf1 , and ycf2 had the most accelerated rates [ 22 ] as detected in plastomes of Silene (Caryophyllaceae), and clpP and ycf1 were found to have the highest d N values among genes in legumes [ 16 ]. In the present study, ycf1 and matK had the highest d N value, and ycf2 had the highest d N /d S value.…”

“…These characteristics may vary among different genes or functional groups of genes and are of great importance in our understanding of plastome evolution and phylogenetic inference. Additionally, the correlation between evolutionary rate and gene characteristics can be invoked as an explanation of the primary impetus of plastome evolution [ 16 , 20 , 34 , 35 ].…”

The Origin and Early Evolution of the Legumes are a Complex Paleopolyploid Phylogenomic Tangle closely associated with the Cretaceous-Paleogene (K-Pg) Boundary

“…Furthermore, chloroplast genes have highly heterogeneous substitution rates across legumes, leading to a wellresolved topology in core Papilionoideae but poor resolution in other lineages, particularly Caesalpinioideae (Figs 2C & S1-4). It has long been known that there is significant variation in rates of chloroplast sequence evolution among plant lineages (Bousquet et al, 1992) and previous analyses of single chloroplast genes (Lavin et al, 2005) and legume chloroplast genomes (Dugas et al, 2015;Schwarz et al, 2017;Wang et al, 2018) have suggested substantial variation in rates of molecular evolution among legume lineages. Because branch model Dn/Ds ratio tests do not provide evidence for different selective forces on photosynthesis genes across legumes, this pattern may rather be related to life-history strategies in the 50Kb-inversion clade, which includes many herbaceous plants of short stature (Lanfear et al, 2013) and shorter generation times (Smith & Donoghue, 2008), especially in the vicioid clade where the highest rates are found (Fig.…”