Bioinoculant-induced plant resistance is modulated by interactions with resident soil microbes

Background: Entomopathogenic fungi are increasingly used as bio-inoculants to enhance crop growth and resistance. When applied to rhizosphere soil, they interact with resident soil microbes, which can affect their ability to colonize and induce resistance in plants as well as modify the structure of the resident soil microbiome, either directly through interactions in the rhizosphere or indirectly, mediated by the plant. The extent to which such direct versus indirect interactions between bio-inoculants and soil microbes impact microbe-induced resistance in crops remains unclear. This study uses a split-root system to examine the effects of direct versus indirect (plant-mediated) interactions between an entomopathogenic fungus, Metarhizium brunneum, and resident soil microbes on induced resistance in tomato against two-spotted spider mites. Additionally, the study explores how these interactions influence the composition and diversity of soil fungal and bacterial communities. Results: Resident soil microbes reduced the efficacy of M. brunneum to induce resistance against spider mites. This reduction occurred not only when resident microbes directly interacted with the bio-inoculant but also when they were spatially separated within the root system, indicating plant-mediated effects. M. brunneum inoculation did not affect rhizosphere microbial diversity but led to changes in fungal and bacterial community composition, even when these communities were not in direct contact with the inoculant. Conclusion: This research highlights the impact of both direct and plant-mediated interactions between bio-inoculants and resident soil microbes on bio-inoculant-induced pest resistance in crop plants and underscores the importance of assessing potential adverse effects of fungal bio-inoculants on native soil communities.

背景：虫生真菌（Entomopathogenic fungi）作为生物接种剂（bio-inoculants）的应用日益广泛，可促进作物生长并提升作物抗性。当将其施加于根际（rhizosphere）土壤后，虫生真菌会与土著土壤微生物发生相互作用，此类相互作用可从两方面产生影响：一是影响其定殖能力与诱导植物抗性的效果，二是改变土著土壤微生物组的结构，具体路径包括根际内的直接相互作用，以及经由植物介导的间接途径。目前尚不清楚生物接种剂与土壤微生物间的直接与间接相互作用，会在多大程度上影响微生物诱导的作物抗性。本研究采用分根系统（split-root system），探究虫生真菌布氏绿僵菌（Metarhizium brunneum）与土著土壤微生物间的直接、间接（植物介导）相互作用，对番茄抵御二斑叶螨（two-spotted spider mites）的诱导抗性的影响。此外，本研究还探讨了上述相互作用如何调控土壤真菌与细菌群落的组成及多样性。
结果：土著土壤微生物会削弱布氏绿僵菌诱导植株抵御叶螨的效果。这种效果减弱不仅出现在土著微生物与生物接种剂直接相互作用的场景中，当二者在根系中空间分隔时同样存在，这提示存在植物介导的作用途径。布氏绿僵菌接种并未改变根际微生物的多样性，但却使真菌与细菌群落的组成发生显著变化，即便这些群落并未与接种剂直接接触。
结论：本研究凸显了生物接种剂与土著土壤微生物间的直接相互作用及植物介导的相互作用，对生物接种剂诱导作物产生抗虫性的效果的影响；同时强调了评估真菌类生物接种剂对土著土壤群落潜在负面影响的重要性。