Cascading effects of root microbial symbiosis on the development and metabolome of the insect herbivore Manduca sexta L

Root mutualistic microbes can modulate the production of plant secondary metabolites affecting plant–herbivore interactions. Still, the main mechanisms underlying the impact of root mutualists on herbivore performance remain ambiguous. In particular, little is known about how changes in the plant metabolome induced by root mutualists affect the insect metabolome and postlarval development. By using bioassays with tomato plants (Solanum lycopersicum), we analyzed the impact of the arbuscular mycorrhizal fungus Rhizophagus irregularis and the growth-promoting fungus Trichoderma harzianum on the plant interaction with the specialist insect herbivore Manduca sexta. We found that root colonization by the mutualistic microbes impaired insect development, including metamorphosis. By using untargeted metabolomics, we found that root colonization by the mutualistic microbes altered the secondary metabolism of tomato shoots, leading to enhanced levels of steroidal glycoalkaloids. Untargeted metabolomics further revealed that root colonization by the mutualists affected the metabolome of the herbivore, leading to an enhanced accumulation of steroidal glycoalkaloids and altered patterns of fatty acid amides and carnitine-derived metabolites. Our results indicate that the changes in the shoot metabolome triggered by root mutualistic microbes can cascade up altering the metabolome of the insects feeding on the colonized plants, thus affecting the insect development.

根系共生微生物（root mutualistic microbes）可调控植物次生代谢物（plant secondary metabolites）的产生，进而影响植物-植食性昆虫互作（plant–herbivore interactions）。然而，根系共生微生物对植食昆虫生长表现的影响背后的核心机制仍未明晰。具体而言，学界对根系共生微生物诱导的植物代谢组（plant metabolome）变化如何影响昆虫代谢组（insect metabolome）及幼虫后发育（postlarval development）的认知仍十分有限。本研究以番茄（Solanum lycopersicum）为实验材料，通过生物测定分析了丛枝菌根真菌（arbuscular mycorrhizal fungus）Rhizophagus irregularis与促生长真菌（growth-promoting fungus）Trichoderma harzianum对番茄与专食性植食昆虫烟草天蛾（Manduca sexta）之间互作的影响。研究发现，两类共生微生物的根系定殖会抑制昆虫的发育进程，包括变态发育（metamorphosis）。通过非靶向代谢组学（untargeted metabolomics）分析，我们发现共生微生物的根系定殖会改变番茄地上部分的次生代谢，使甾体糖苷生物碱（steroidal glycoalkaloids）的含量显著升高。进一步的非靶向代谢组学分析显示，共生微生物的根系定殖还会改变植食昆虫的代谢组，使其体内甾体糖苷生物碱的积累量上升，同时脂肪酸酰胺（fatty acid amides）与肉碱衍生代谢物（carnitine-derived metabolites）的代谢模式发生改变。本研究结果表明，根系共生微生物诱导的植物地上部分代谢组变化可产生级联效应，进而改变取食定殖植株的昆虫的代谢组，最终影响昆虫的发育进程。