Substantial structural variation and repetitive DNA content contribute to intraspecific plastid genome evolution

Abstract

Abstract Background Plastids have highly conserved genomes in most land plants. However, in several families, plastid genomes exhibit high rates of nucleotide substitution and structural rearrangements among species. This elevated rate of evolution has been posited to lead to increased rates of plastid-nuclear incompatibilities (PNI), potentially acting as a driver of speciation. However, the extent to which plastid structural variation exists within a species is unknown. This study investigates whether plastid structural variation, observed at the interspecific level in Campanulaceae, also occurs within Campanula americana, a species with strong intraspecific PNI. We assembled multiple plastid genomes from three lineages of C. americana that exhibit varying levels of PNI when crossed. We then investigated the structural variation and repetitive DNA content among these lineages and compared the repetitive DNA content with that of other species within the family. Results We found significant variation in plastid genome size among the lineages of C. americana (188,309–201,788 bp). This variation was due in part to multiple gene duplications in the inverted repeat region. Lineages also varied in their repetitive DNA content, with the Appalachian lineage displaying the highest proportion of tandem repeats (~ 10%) compared to the Eastern and Western lineages (~ 6%). In addition, genes involved in transcription and protein transport showed elevated sequence divergence between lineages, and a strong correlation was observed between genome size and repetitive DNA content. Campanula americana was found to have one of the most repetitive plastid genomes within Campanulaceae. Conclusions These findings challenge the conventional view of plastid genome conservation within a species and suggest that structural variation, differences in repetitive DNA content, and divergence of key genes involved in transcription and protein transport may play a role in PNI. This study highlights the need for further research into the genetic mechanisms underlying PNI, a key process in the early stages of speciation.

Keywords

• Campanulaceae
• Chloroplast genome evolution
• Comparative genomics
• Cyto-nuclear incompatibility
• Plastid-nuclear incompatibility
• Repetitive DNA