Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?
复制标题

食草动物诱导的挥发物能通过增加食草动物对自然病原体的敏感性来保护植物吗?

DOI:
10.1128/aem.01468-18
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发表时间:
2019-01-01
影响因子:
4.4
通讯作者:
Herrero, Salvador
Herrero, Salvador
中科院分区:
生物学2区
文献类型:
--
作者:
Gasmi, Laila;Martinez-Solis, Maria;Herrero, Salvador

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为了应对昆虫植食性,植物调动各种防御。防御反应包括释放食草动物诱导的植物挥发物(HIPVs),这些挥发物可以作为警告未受损组织和吸引食草动物天敌的信号。一些HIPV可以对草食动物的生存产生直接的负面影响,但还不清楚是通过什么机制。在这里,我们测试了暴露于HIPV使昆虫更容易受到自然病原体的假设。甜菜夜蛾幼虫暴露于吲哚和芳樟醇,而不是暴露于(Z)-3-己烯基乙酸酯,增加了对甜菜夜蛾核型多角体病毒(SeMNPV)的易感性。我们还发现,暴露于吲哚,而不是暴露于芳樟醇或(Z)-3-乙酸己烯酯,增加苏云金芽孢杆菌的致病性。其他实验显示,幼虫暴露于吲哚48小时后,微生物群组成发生了显着变化。总的来说,这些结果提供了证据,表明某些HIPV可以强烈增强毛虫对病原体的易感性,可能是通过对昆虫肠道微生物群的影响。这些发现表明HIPV可以保护植物免受草食性昆虫侵害的一种新机制。重要信息涉及昆虫害虫、其天敌、微生物和植物宿主的多营养相互作用越来越被认为是害虫管理中的相关因素。为了应对食草动物的攻击,植物激活了广泛的防御,旨在减轻损害。受攻击植物释放的植物挥发物(HIPVs)可以作为其他植物的启动信号,吸引天敌,对植食动物的生存有直接的负面影响。在目前的工作中,我们表明,昆虫暴露于诱导挥发物可以增加昆虫的易感性,自然发生在植物环境中的昆虫病原体。这些发现表明,植物挥发物通过影响昆虫与天然病原体的相互作用而发挥新的作用,这可能是由昆虫微生物群组成的改变介导的。此外,这项工作提供了证据,可选择的植物性状(生产的次生代谢产物),可以有影响的生态害虫,并可能在使用天然昆虫病原体的害虫管理策略的改进有关。
In response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. Some HIPVs can have a direct negative impact on herbivore survival, but it is not well understood by what mechanisms. Here, we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposure of the caterpillars of the noctuid Spodoptera exigua to indole and linalool, but not exposure to (Z)-3-hexenyl acetate, increased the susceptibility to Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV). We also found that exposure to indole, but not exposure to linalool or (Z)-3-hexenyl acetate, increased the pathogenicity of Bacillus thuringiensis. Additional experiments revealed significant changes in microbiota composition after forty-eight hours of larval exposure to indole. Overall, these results provide evidence that certain HIPVs can strongly enhance the susceptibility of caterpillars to pathogens, possibly through effects on the insect gut microbiota. These findings suggest a novel mechanism by which HIPVs can protect plants from herbivorous insects.IMPORTANCE Multitrophic interactions involving insect pests, their natural enemies, microorganisms, and plant hosts are increasingly being recognized as relevant factors in pest management. In response to herbivory attacks, plants activate a wide range of defenses that aim to mitigate the damage. Attacked plants release herbivore-induced plant volatiles (HIPVs), which can act as priming signals for other plants and attract natural enemies of herbivores, and which may have a direct negative impact on herbivore survival. In the present work, we show that exposure of the insects to the induced volatiles could increase the insects' susceptibility to the entomopathogens naturally occurring in the plant environment. These findings suggest a novel role for plant volatiles by influencing insect interactions with natural pathogens, probably mediated by alterations in the insect microbiota composition. In addition, this work provides evidence for selectable plant traits (production of secondary metabolites) that can have an influence on the ecology of the pests and could be relevant in the improvement of pest management strategies using natural entomopathogens.