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.

植物面临着一系列食草昆虫，并进化出了复杂的防御方法来抵御各种昆虫的摄食策略。然而，人们对植物如何应对不同取食方式的食草动物的连续攻击并协调其不同的防御机制知之甚少。在这项研究中，我们揭示了对咀嚼叶昆虫的诱导性茉莉酸（JA）积累增强了植物对连续咀嚼叶昆虫（毛毛虫）和韧皮部昆虫（粉虱）侵扰的抵抗力和驱避能力。相反，组成型和粉虱诱导的水杨酸（SA）积累专门增强了对后期粉虱入侵的防御。通过评估草食动物的表现和对野生型、JA 缺陷和 SA 缺陷植物的偏好，我们发现 JA/SA 水平调节植物对初始和后续食草动物的抗性。值得注意的是，由于毛毛虫或粉虱攻击而导致的 JA 或 SA 积累并不会显着影响其他化合物的组成水平，尽管它们具有拮抗串扰。此外，在烟草中施用外源 JA 可以有效防御连续的毛毛虫和粉虱攻击，超过 SA 的功效，尽管会产生相关的生长损失。我们的发现表明，植物可以针对不同进食模式的初始和后续昆虫制定防御策略。 JA/SA 的响应及其复杂的串扰促进了这种定制的防御，同时考虑了增长与防御的权衡。