Growth, signals, and survival: the evolutionary divergence of terpenoid metabolism in terrestrial plants.
Covering: primarily from 2011 to 2026Terpenoids are an ancient and immensely diverse class of natural products. Since their emergence more than two billion years ago alongside early biological membranes, terpenoid metabolism has undergone a vast expansion in both structure and function, which directly contributed to the ecological success of terrestrial plants. Biosynthetically derived from two isomeric five-carbon isoprenoid precursors, plant terpenoids include hemi-, mono-, sesqui-, di-, sester-, tri-, tetra-, and poly-, and mero-terpenoids, that exhibit extensive variation in chain length, structural scaffolds, and functional decoration. This large chemical space is generated via dynamic metabolic networks, in which functionally versatile enzymes - most notably scaffold-forming terpene synthases and tailoring cytochrome P450 monooxygenases - are assembled into combinatorial pathway modules to yield complex bioactive terpenoid structures. Lineage-specific expansion of the underlying gene families, driven by recurrent genome and gene duplications followed by functional divergence, have facilitated the evolution of both conserved and specialized metabolic branches and natural products. Functionally, conserved terpenoids act as phytohormones, signaling molecules, and pigments governing plant growth and development, whereas typically species-specific specialized terpenoids mediate dynamic plant-environment interactions, including pest and pathogen defenses, allelopathy, pollinator attraction, root-microbiome communication, and abiotic stress tolerance. Advances in genomics, metabolomics, and synthetic biology continue to accelerate the discovery of terpenoid structures, pathways, and functions at an ever-increasing pace. Elucidating the mechanisms that generate this diversity, and the multifaceted roles that terpenoids play in plant ecology and physiology not only deepens our understanding of the evolutionary history of terrestrial plants, but also unlocks new opportunities for biotechnological innovation, spanning terpenoid-derived therapeutics, biofuels, fragrances, polymers, agrochemicals, and many other bioproducts.