Plastome evolution at the edge: structural rearrangements, IR expansion, and gene flux in Hypericaceae (Malpighiales)

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.

To explore plastome evolution across Hypericaceae, we sequenced 12 complete chloroplast genomes representing seven genera from the three major tribes, Hypericeae, Vismieae, and Cratoxyleae, and two outgroup plastomes from Clusiaceae. Comparative analysis of 281 Malpighiales plastomes showed that Hypericaceae differ significantly in total plastome size and SSC region length, while LSC and IR regions showed no significant differences.. Plastome sizes in Hypericaceae ranged from 138 to 176 kb, reflecting extensive structural variation, multiple inversions, IR expansions, and lineage-specific rearrangements. Cratoxyleae exhibited a relatively conserved plastome structure with one major inversion and minimal gene loss, representing the most stable lineage within the family. Species within Vismieae showed markedly expanded IR regions, while Hypericeae exhibited frequent gene and intron losses associated with structural instability. In Hypericum, genes such as matK and accD were relocated into or near the IR regions, accompanied by lineage-specific ORFs likely formed through repeat-mediated recombination. Several genes (rpl23, rpl32, rps7, rps16, infA, ycf1, ycf2) showed independent losses across the family. Across the Hypericaceae, the protein-coding genes matK, accD and clpP also showed domain-disrupting expansions, potentially impacting their functional roles.

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.