Contrasting glucosinolate profiles in rapeseed genotypes shape the rizosphere-insect continuum and microbial detoxification potential in a root herbivore

Plant secondary metabolites are key mediators of plant–insect–microbiome interactions, yet their role in structuring functionally relevant insect-associated microbial communities remains poorly understood. Here, we combined a factorial experiment using Brassica napus genotypes differing in glucosinolates (GLS) content with distinct succession to investigate the eco-evolutionary dynamics of the microbiota of the root herbivore Delia radicum. Amplicon sequencing and microbial culturing revealed that both rhizospheric and gut microbial communities are shaped by plant genotype and soil legacy, with a subset of bacterial taxa shared across compartments. Notably, Pseudomonas brassicacearum, harboring the isothiocyanates (ITC) detoxifying gene saxA, was consistently recovered from both plant and insect habitats. Functional assays confirmed its capacity to degrade 2-phenylethyl isothiocyanate (PEITC), a major toxic GLS hydrolysis product. Other, gut derived microbial isolates exhibited heterogeneous response to PEITC, ranging from growth inhibition promotion or growth recovery after a prolonged lag phase. Despite the toxicity of ITC, insect fitness proxies were enhanced on GLS+ plants, suggesting microbiota-mediated adaptation to host chemical defenses. Our findings reveal a plant-genotype-specific filtering of environmentally acquired microbes and highlight the role of detoxifying symbionts in Delia radicum performance.

植物次生代谢物是植物-昆虫-微生物组互作的关键介导因子，然而其在构建具有功能相关性的昆虫关联微生物群落中的作用仍未得到充分阐释。本研究采用硫代葡萄糖苷（glucosinolates, GLS）含量存在差异的甘蓝型油菜（Brassica napus）基因型，并结合不同土壤演替历史开展析因实验，以探究植食性根蛆萝卜蝇（Delia radicum）的微生物组生态-进化动态。扩增子测序与微生物分离培养结果显示，根际与肠道微生物群落均受植物基因型和土壤遗留效应的调控，且不同生境间共享有部分细菌类群。值得注意的是，携带异硫氰酸酯（isothiocyanates, ITC）解毒基因saxA的芸苔假单胞菌（Pseudomonas brassicacearum）可在植物与昆虫两类生境中稳定分离得到。功能实验证实该菌能够降解2-苯乙基异硫氰酸酯（2-phenylethyl isothiocyanate, PEITC）——这是硫代葡萄糖苷的一类主要毒性水解产物。其余源自昆虫肠道的微生物分离株对PEITC则表现出异质性响应：部分菌株生长受到抑制，部分则在经历较长滞后期后恢复生长。尽管异硫氰酸酯具有毒性，但在携带GLS的植株上，萝卜蝇的适合度指标反而得到提升，这表明微生物组介导了昆虫对宿主化学防御的适应性。本研究揭示了植物基因型对环境获取微生物的特异性筛选作用，并阐明了解毒共生菌在萝卜蝇生存表现中的关键功能。