Foliar herbivory‐enhanced mycorrhization is associated with increased levels of lipids in root and root exudates

• Published in: The Journal of ecology Vol. 112; no. 4; pp. 701 - 716
• Main Authors: Xing, Zhenlong, Zhang, Zhongyue, Zhao, Yige, Biere, Arjen, Liu, Siqiao, Shi, Yu, Ding, Jianqing
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.04.2024
• Subjects: above‐below‐ground interaction; Abundance; Ambrosia artemisiifolia; arbuscular mycorrhizal fungi; Arbuscular mycorrhizas; carbon; Colonization; Community composition; community structure; Exudates; Exudation; Fatty acids; foliar‐herbivory; Fungi; Glomus; Herbivores; Herbivory; Insects; Lipids; Metabolites; Metabolomics; phenolic compounds; Phenols; Plants; Relative abundance; Rhizoplane; Rhizosphere; root exudates; Roots; Secretions; Soil ecology; species; vesicular arbuscular mycorrhizae; Wounding
• ISSN: 0022-0477; 1365-2745
• DOI: 10.1111/1365-2745.14272

Insect herbivory can affect interactions between plants and arbuscular mycorrhizal (AM) fungi through herbivore‐modified root carbon pools, while the specific metabolic changes underlying fungal responses to herbivory are poorly understood. Here we explored the impacts of foliar herbivory and mechanical wounding on AM colonisation and AM community composition of common ragweed (Ambrosia artemisiifolia) and the role of root metabolites in mediating these effects. Foliar insect herbivory enhanced AM colonisation, whereas mechanical wounding only enhanced AM colonisation in combination with application of caterpillar oral secretions. Meanwhile, the relative abundance of Glomus species was increased in root endosphere, rhizoplane and rhizosphere soils after foliar herbivory. Foliar herbivory also increased the concentrations of fatty acids in roots but decreased phenolics, and their concentrations were significantly correlated with AM colonisation. Addition of exudates from plants exposed to herbivory resulted in increases in AM colonisation of plants without herbivory. Moreover, widely targeted metabolomic analyses revealed that foliar herbivory enhanced the relative abundance of lipids and decreased phenols in root exudates. Synthesis. We show that plants can enhance their associations with arbuscular mycorrhizal (AM) fungi when subject to above‐ground herbivory, possibly mediated by herbivore‐induced increases in the levels of root lipids. Our findings highlight the role of root lipids in above‐below‐ground biological interactions, providing novel insights into plant‐AM fungi integrative responses to biotic stresses. 摘要 植食性昆虫通过改变根系碳库影响植物‐菌根真菌互作，然而对其背后的具体代谢变化所知甚少。 本研究探讨了昆虫取食与机械损伤对豚草菌根真菌定殖及群落组成的影响，解析了根系代谢物在其中的作用。 昆虫取食增加豚草菌根定殖率，然而机械损伤仅在与昆虫唾液结合时增加菌根真菌定殖率。同时，昆虫取食后豚草根内、根表和根际球囊霉属(Glomus)相对丰度增加。昆虫取食增加根系脂肪酸含量，但减少酚类物质含量，这两类物质与菌根定殖率显著相关。添加昆虫取食后的豚草根系分泌物能增加菌根定殖率。而且，广靶代谢组结果表明昆虫取食增加根系分泌物中脂类物质的相对丰度，降低酚类物质的相对丰度。 本研究发现植物遭受昆虫危害后能够增强它们与菌根真菌的联系，这可能与根系脂类物质的增加有关。我们的发现强调脂类物质在地上‐地下生物互作中的作用，为植物‐菌根真菌对生物胁迫的协同响应提供新视角。 The authors show that plants can enhance their associations with arbuscular mycorrhizal (AM) fungi when subject to above‐ground herbivory, possibly mediated by herbivore‐induced increases in the levels of root lipids. These findings highlight the role of root lipids in above‐below‐ground biological interactions, providing novel insights into plant‐AM fungi integrative responses to biotic stresses.