Arbuscular mycorrhizal fungus reshapes the rhizosphere microbiome of alfalfa in response to above‐ground attack by aphids and a fungal plant pathogen

Abstract Plants assemble beneficial rhizosphere microbiomes through a ‘cry for help’ mechanism upon pathogen or insect herbivore attack. The arbuscular mycorrhizal fungi (AMF) can influence the composition of microbial communities in the plant rhizosphere. However, their impacts on the rhizosphere microbiome in response to co‐attacks of pathogens and insect herbivores remain unknown. In this study, a mesocosm of alfalfa, Rhizophagus intraradices , Phoma medicaginis and Acyrthosiphon pisum was used to elucidate how AMF alter the plant rhizosphere microbiome and its responses to multiple biotic stresses. The AMF significantly increased the activity of soil acid phosphatase, urease and β‐glucosidase, causing an enhanced absorption of soil phosphorus by plants. The soil enzymes were also significantly and positively correlated with plant shoot properties, including polyphenol oxidase and peroxidase, salicylic acid (SA) and trypsin inhibitor (TI). Although all the AMF, P. medicaginis and aphids altered the rhizosphere microbiome of alfalfa, the AMF recruited beneficial microorganisms in the alfalfa rhizosphere in response to pathogens and aphid attacks. The multi‐interaction also increased the complexity and stability of the rhizosphere microbial network. Additionally, there is a significant correlation between soil enzyme activity, nitrate nitrogen, TI, SA, biomass, disease severity and the rhizosphere microbiome. Therefore, the AMF improves plant defence and soil biochemistry profiles and assists alfalfa in assembling beneficial rhizosphere microbiomes in response to P. medicaginis and aphid attacks. These findings are vital for understanding the interactions between transboundary species in above‐ and below‐ground systems altered by AMF in natural ecosystems. Read the free Plain Language Summary for this article on the Journal blog.