Plastome Evolution at the Edge: Structural Rearrangements, IR Expansion, and Gene Flux in Hypericaceae (Malpighiales)

Abstract Background The evolutionary history of the Hypericaceae Juss. family remains poorly understood despite previous phylogenomic efforts. A prior study on Hypericum ascyron revealed exceptional plastome rearrangements and gene loss events, prompting questions about whether such genomic patterns are unique to Hypericum or reflect broader evolutionary trends within the family. Results To explore plastome evolution across Hypericaceae, we sequenced 14 complete chloroplast genomes representing seven genera from the three major tribes: Hypericeae, Vismieae, and Cratoxyleae, alongside two genera from the related family Clusiaceae. Comparative analyses revealed extensive variation in plastome structure and gene content, including lineage-specific rearrangements, inversions, and expansions of inverted repeat (IR) regions. Notably, species within Vismieae exhibited significantly expanded IR regions. In Hypericum, unique lineage-specific open reading frames (ORFs) were identified, with genes such as accD and matK relocated into or near the IR regions, likely driven by repeat-mediated recombination. Multiple independent losses of genes (rpl23, rpl32, rps16, infA, ycf1, ycf2) and introns were observed across the family, particularly in Hypericeae, often accompanying structural rearrangements. Additionally, matK was translocated from its typical position within the trnK-UUU intron into the IR region, a rare event in angiosperm plastomes. The protein-coding genes accD and clpP also showed domain-disrupting expansions, potentially impacting their functional roles. Conclusions Our results demonstrate that plastome evolution in Hypericaceae is highly dynamic, characterized by substantial structural plasticity, gene loss, and lineage-specific innovation. These findings provide new insights into plastome diversification across the family and lay the groundwork for further phylogenomic and evolutionary studies within Malpighiales.