Evolution of trans-isoprenyl diphosphate synthases in the plant kingdom

Terpenoid metabolism is essential across all life forms. Trans-isoprenyl diphosphate synthases (IDSs) are universally conserved enzymes that produce isoprenyl diphosphates of varying chain lengths, serving as precursors for diverse terpenoid metabolites. However, the evolution of IDS genes within the plant kingdom (Archaeplastida) remains unresolved. Here, we reconstruct the evolutionary trajectory of IDS genes in Archaeplastida using comprehensive genomic mining and phylogenetic analyses. We infer that the last common ancestor of the plant kingdom possessed 4 distinct IDS genes: 2 from the eukaryotic host encoding farnesyl diphosphate synthase (FPPS) and polyprenyl diphosphate synthase using farnesyl diphosphate as substrate (PPPSF), and 2 from the cyanobacterial endosymbiont encoding geranylgeranyl diphosphate synthase (GGPPS) and polyprenyl diphosphate synthase using geranylgeranyl diphosphate as a substrate (PPPSGG). While all the cyanobacterial-derived genes have been retained, the host-derived GGPPS was lost in the Archaeplastida ancestor. Most IDSs are nuclear-encoded, yet GGPPS in glaucophytes and PPPSGG in both glaucophytes and rhodophytes are plastid-encoded, indicating lineage-specific endosymbiotic gene transfer. One representative plastid-encoded PPPSGG shares catalytic properties with its nuclear-encoded counterparts. Among different lineages of the plant kingdom, the GGPPS subfamily is substantially expanded in vascular plants, consistent with the diversification of terpenoid metabolism in these later diverged lineages of land plants. Together, these findings reveal a dual origin and a complex evolutionary trajectory of IDS genes in the plant kingdom, shaped by endosymbiotic gene transfer, differential gene retention, and lineage-specific expansion.