Treating tomato seeds with rutin generates jasmonate-dependent long-persisting priming of broadspectrum resistance to herbivores.

BACKGROUND As an environmentally friendly crop protection strategy, seed priming effectively induces plant immune responses against future stresses. Our previous study demonstrated that treating tomato (Solanum lycopersicum) seeds with the bioflavonoid rutin enhances resistance against the phloem-feeding whitefly (Bemisia tabaci). However, whether rutin seed treatment confers resistance to multiple herbivores and the mechanistic basis of defense priming in seeds remain unclear. Here, we investigated whether rutin seed treatment enhances tomato resistance against herbivores representing major feeding guilds and explored the role of phytohormone signaling in regulating defense priming. RESULTS We found that seeds were receptive to the bioflavonoid rutin, which established a primed state for herbivore resistance, resulting in a long-term increase in resistance to caterpillars, whiteflies and spider mites. Importantly, this induced resistance was not accompanied by an inhibition of plant growth and development. This primed resistance persisted for at least 8 weeks in plants grown from treated seeds, was associated with the accumulation of jasmonates in treated seeds and was dependent on the jasmonic acid (JA) signaling pathway. Moreover, we demonstrated the key role of high levels of jasmonates in rutin-treated tomato seeds for the induction of defense priming against herbivores by transgenic overexpression of the jasmonate biosynthetic gene during seed development. CONCLUSION Our results conclude that rutin seed treatment promotes jasmonate accumulation in seeds and primes JA-dependent anti-herbivore defenses in tomato without cost to growth. Harnessing seed priming may, therefore, provide new avenues for better crop protection in future agriculture. © 2025 Society of Chemical Industry.