Compartmentalized above- and belowground defenses in Tanacetum vulgare are tailored to localized antagonists

Abstract Specialized metabolites, specially terpenoids, play a key role in plant defense. However, how terpenoid diversity governs inducible chemistry and root architectural development remain poorly understood. We used a combination of high-throughput root phenotyping and targeted metabolite profiling to examine three leaf terpenoid chemotypes of common tansy (Tanacetum vulgare). Using a phenotyping platform, we tested whether (i) root-chewing wireworms induce root terpenoids locally and alter shoot terpenoids systemically, (ii) phloem-feeding aphids elicit chemotype-dependent responses, and (iii) chemotypes differ in root-system development. After root establishment, the plants were exposed to wireworms (Agriotes spp.) and aphids (Macrosiphoniella tanacetaria), both separately and together, and were then monitored for 60 days. The chemotypes differed in inducible chemistry and root architecture. Chemotype 1 developed the fastest-growing root systems and the highest root:shoot ratios. Wireworms increased stored root sesquiterpenoid levels by more than twofold in chemotypes 1 and 2, whereas chemotype 3 was largely unresponsive. Aphids didn‘t alter root terpenoids, but significantly increased leaf monoterpenoid emissions in chemotype 1 without affecting stored pools. Therefore, storage and emission were decoupled and depended on both organ and chemotype. Our analysis reveals a compartmentalized, chemotype-specific defense strategy in tansy, highlighting the coordinated regulation of the root system and inducible chemistry. Highlight In Tanacetum vulgare, wireworms boost root sesquiterpenoids and aphids elevate leaf monoterpenoid emissions; chemotype governs terpenoid defense and root system architecture. Competing Interest Statement The authors have declared no competing interest.