Plastome evolution and phylogenomic insights into the evolution of Lysimachia (Primulaceae: Myrsinoideae)

Abstract

Background: Lysimachia L., the second largest genus within the subfamily Myrsinoideae of Primulaceae, comprises approximately 250 species worldwide. China is the species diversity center of Lysimachia, containing approximately 150 species. Despite advances in the backbone phylogeny of Lysimachia, species-level relationships remain poorly understood due to limited genomic information. This study analyzed 50 complete plastomes for 46 Lysimachia species. We aimed to identify the plastome structure features and hypervariable loci of Lysimachia. Additionally, the phylogenetic relationships and phylogenetic conflict signals in Lysimachia were examined.

Results: These fifty plastomes within Lysimachia had the typical quadripartite structure, with lengths varying from 152,691 to 155,784 bp. Plastome size was positively correlated with IR and intron length. Thirteen highly variable regions in Lysimachia plastomes were identified. Additionally, ndhB, petB and ycf2 were found to be under positive selection. Plastid ML trees and species tree strongly supported that L. maritima as sister to subg. Palladia + subg. Lysimachia (Christinae clade), while the nrDNA ML tree clearly placed L. maritima and subg. Palladia as a sister group.

Conclusions: The structures of these plastomes of Lysimachia were generally conserved, but potential plastid markers and signatures of positive selection were detected. These genomic data provided new insights into the interspecific relationships of Lysimachia, including the cytonuclear discordance of the position of L. maritima, which may be the result of ghost introgression in the past. Our findings have established a basis for further exploration of the taxonomy, phylogeny and evolutionary history within Lysimachia.

Keywords: Conflict signature; Lysimachia; Phylogeny; Plastid genome; Primulaceae.

Fig. 1

The plastomes and their expansion/contraction of IR among Lysimachia species. a plastome map of Lysimachia. The genes belonging to different functional groups are shown in different colors, which are shown on the bottom left. Genes inside and outside of the external circle are transcribed in clockwise and counterclockwise directions, respectively. The inner circle represents the quadripartite structure, with two copies of the inverted repeat (IR_A and IR_B), an LSC, and an SSC region in black with GC content in dark gray and AT content in light gray. b Correlation of IR length and Lysimachia plastome size. c Boxplot of the IR length in three subgenera of Lysimachia

Fig. 2

Comparison of nucleotide diversity (Pi) values in Lysimachia plastomes. The X-axis shows the position of the midpoint of sliding windows (kb), while the Y-axis indicates the nucleotide diversity of each window

Fig. 3

Comparisons of d_N, d_S, and d_N/d_S of the protein-coding genes in Lysimachia

Fig. 4

Conflict signals between plastid and nrDNA phylogenies in Lysimachia. a The tanglegram of Lysimachia shows cytonuclear conflicts between the whole plastid ML tree (T1; left) and nrDNA ML tree (right). Eight major clades within Lysimachia are indicated by different colors, and the tangles among the group of L. maritima are highlighted. b Two hypotheses between two constraint phylogenies according to conflicting cytonuclear topologies using whole plastid datasets and the ratio of gene tree supports, conflicts and non-information. The focal branches we tested in two constraint topologies are shown with dotted lines. The bootstrap supports are shown above the focal branch, and three quartet metrics from quartet sampling analysis are shown below the focal branch. The colors in the legend indicate concordant, most common conflict, other conflicts, and non-informatics, respectively. c The difference in log-likelihoods (ΔlnL) of two hypotheses (T1 and T5) for each locus calculated in RAxML. The positive values of ΔlnL indicate T1-supported phylogenetic signals, while negative values support the T2 hypothesis. Only the genes with significant phylogenetic signals (ΔlnL > 2) are shown on the bar plot. ΔlnL values of T1 and T5 were showed with dark blue and yellow, respectively