Structural variation and evolutionary dynamics of plastid genomes in the subgenus Lychnis (Silene, Caryophyllaceae): insights from genome rearrangements and substitution rates

石竹科蝇子草亚属(Lychnis)质体基因组的结构变异和进化动态:来自基因组重排和替换率的启示

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Abstract

BACKGROUND: Plastid genomes (plastomes) in land plants typically retain a conserved quadripartite structure; yet some angiosperm lineages exhibit extensive structural instability and accelerated sequence evolution. Here, we present a comparative plastome analysis of six species from the subgenus Lychnis (genus Silene, Caryophyllaceae) integrated with previously published plastomes. RESULTS: We identify eight large-scale inversions, three independent shifts of the inverted-repeat (IR) boundary, and a marked proliferation of dispersed repeats, implicating repeat-mediated recombination and altered recombination control in driving plastome reorganization. Gene content varied among Lychnis species, including the loss or pseudogenization of accD, infA, and rpl23. Transcriptome data reveal nuclear-encoded homologues with chloroplast-targeting signals, indicating functional replacement via plastid-to-nucleus gene transfer and recruitment of pre-existing nuclear paralogues. Plastid phylogenomic analyses recover the subgenus Lychnis as a strongly supported, monophyletic and early-diverging lineage within the genus Silene, showing that structural changes and substitution rate acceleration have arisen independently of those in other subgenera. Across the genus, synonymous and nonsynonymous substitution rates are elevated in a subset of non-photosynthetic genes, including accD and clpP, with lineage-specific episodes of positive selection detected on several branches. CONCLUSIONS: Together, these results point to a complex interplay between recombination dynamics, shifts in selective regime and plastid-nuclear interactions, and underscore plastome instability as an important driver of genome evolution within Silene and more broadly across angiosperms.

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