Differential induction of JA/SA determines plant defense against successive leaf-chewing and phloem-feeding insects

Plants face an array of insect herbivores and have evolved complex defense approaches against various insect feeding strategies. However, little is known about how plants respond to successive attacks by herbivores with different feeding modes and coordinate their diverse defense mechanisms. In this study, we unveil that inducible jasmonic acid (JA) accumulation in response to leaf-chewing insects augments plant resistance and repellence to sequential leaf-chewing insect (caterpillar) and phloem-feeding insect (whitefly) infestations. Conversely, constitutive and whitefly inducible salicylic acid (SA) accumulation exclusively bolsters defense against later-stage whitefly invasion. Through assessments of herbivore performance and preferences on wild-type, JA-deficient, and SA-deficient plants, we show that JA/SA levels regulate plant resistance to both initial and sequential herbivores. Notably, JA or SA accumulation due to caterpillar or whitefly attacks does not substantially affect constitutive levels of the other compound, despite their antagonistic crosstalk. Furthermore, exogenous JA application in tobacco elicits efficient defense against successive caterpillar and whitefly assaults, surpassing SA's efficacy, albeit with associated growth penalties. Our discoveries demonstrate that plants can tailor their defense strategies against initial and sequential insects with different feeding modes. This customized defense is facilitated by JA/SA responses and their intricate cross-talk while taking account of the growth-defense trade-off.