Arbuscular mycorrhizal fungus alters the phyllosphere microbial community and modifies plant defences against co‐attack of pea aphid and pathogen

Abstract Arbuscular mycorrhizal fungi (AMF), pathogens and insect pests usually colonize or infect the same plant. Besides, AMF changes plant defence enzymes and metabolites under multiple biotic stresses and alters the interrelationship between plant, pathogen and insect. Pathogens and insects reshape the plant phyllosphere microbiome. Nevertheless, the complex effects in the phyllosphere microbiome are rarely studied, particularly for mesocosms where component organisms interact. This study used high‐throughput sequencing to survey alfalfa phyllosphere microbiome communities in the pea aphid ( Acyrthosiphon pisum ), foliar pathogen ( Phoma medicaginis ) and AMF ( Rhizophagus intraradices ) interactions. We determined the diversity and composition of the phyllosphere microbial community of alfalfa and analysed the relationship with plant defence enzymes and phytohormones across the pathogen, aphid and AMF treatments. The pathogen, aphid and AMF alone or combined changed the phyllosphere fungal diversity and composition in alfalfa leaves. Co‐attack of pathogen and aphid increased the phyllospheric fungal diversity compared to each stress applied individually on non‐AMF alfalfa leaves. Moreover, AMF enhanced and maintained the abundance of biocontrol microbes, particularly under pathogen and/or aphid stress. The increase of trypsin inhibitor (TI), salicylic acid (SA) and polyphenol oxidase (PPO) activity by co‐attack of the pathogen, aphid and AMF colonization is positively correlated with the alfalfa phyllosphere microbial diversity and community. Plant defence enzyme activity shows a significant correlation with the relative abundance of phyllospheric fungi, whereas jasmonic acid (JA) and SA levels are significantly correlated with the relative abundance of phyllospheric bacteria. We propose that AMF alters plant defence response, shaping phyllosphere microbes to address multiple biotic stresses, indicating its potential applications in enhancing plant resilience against pathogens and herbivore pests in agricultural production. Read the free Plain Language Summary for this article on the Journal blog.