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

IF 4.3 1区 农林科学 Q1 ENTOMOLOGY
Yu-Xiao Liu, Wen-Hao Han, Jun-Xia Wang, Feng-Bin Zhang, Shun-Xia Ji, Yu-Wei Zhong, Shu-Sheng Liu, Xiao-Wei Wang
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Abstract

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.

Abstract Image

JA/SA 的不同诱导决定了植物对连续啃食叶片和韧皮部的昆虫的防御能力
植物面临一系列昆虫食草动物的攻击,并进化出复杂的防御方法来对付各种昆虫的取食策略。然而,人们对植物如何应对具有不同取食模式的食草动物的连续攻击并协调其多样化的防御机制知之甚少。在这项研究中,我们揭示了诱导性茉莉酸(JA)积累对啃叶昆虫的响应可增强植物对连续啃叶昆虫(毛虫)和噬髓昆虫(粉虱)侵袭的抵抗力和排斥力。相反,组成型水杨酸(SA)积累和粉虱诱导型水杨酸(SA)积累只能增强防御后期粉虱入侵的能力。通过评估野生型、JA 缺乏型和 SA 缺乏型植物上食草动物的表现和偏好,我们发现 JA/SA 水平能调节植物对初始和连续食草动物的抵抗力。值得注意的是,毛虫或粉虱攻击导致的 JA 或 SA 积累不会对另一种化合物的组成水平产生实质性影响,尽管它们之间存在拮抗作用。此外,在烟草中施用外源 JA 能有效抵御毛虫和粉虱的连续攻击,其功效超过 SA,尽管会影响生长。我们的发现表明,植物可以针对具有不同取食模式的初始昆虫和连续昆虫定制防御策略。JA/SA反应及其错综复杂的交叉对话促进了这种定制的防御,同时也考虑到了生长-防御的权衡。
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来源期刊
Journal of Pest Science
Journal of Pest Science 生物-昆虫学
CiteScore
10.40
自引率
8.30%
发文量
114
审稿时长
6-12 weeks
期刊介绍: Journal of Pest Science publishes high-quality papers on all aspects of pest science in agriculture, horticulture (including viticulture), forestry, urban pests, and stored products research, including health and safety issues. Journal of Pest Science reports on advances in control of pests and animal vectors of diseases, the biology, ethology and ecology of pests and their antagonists, and the use of other beneficial organisms in pest control. The journal covers all noxious or damaging groups of animals, including arthropods, nematodes, molluscs, and vertebrates. Journal of Pest Science devotes special attention to emerging and innovative pest control strategies, including the side effects of such approaches on non-target organisms, for example natural enemies and pollinators, and the implementation of these strategies in integrated pest management. Journal of Pest Science also publishes papers on the management of agro- and forest ecosystems where this is relevant to pest control. Papers on important methodological developments relevant for pest control will be considered as well.
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