Common mycorrhizal networks enhance defense responses against pathogens in neighboring plants

Arbuscular mycorrhizal (AM) fungi can establish common mycorrhizal networks (CMNs) and assemble their own phyllosphere microbiome. Although the roles of the AM fungi in soil microbiomes have been extensively studied, little is known about the role of CMNs in collective community-level changes of the phyllosphere microbiome in response to infection by pathogens. Here, we explored the impact of CMNs that linked the donor white clover (<i>Trifolium repens</i> L.) plants infected with the pathogen <i>Stemphylium sarciniforme</i> on changes in defense compounds and the phyllosphere microbiome in receiver perennial ryegrass (<i>Lolium perenne</i> L.). This included examining plant defense enzymes, phytohormones, phyllosphere microbiome diversity, community structure, and network complexity. The donor clover infected with the pathogen and its linked receiver ryegrass through the CMNs had a higher activity of catalase along with higher levels of abundance-based coverage estimato (ACE), genera, and species richness in the receiver ryegrass. The pathogen infection of the donor clover altered the community structure of the phyllosphere microbiome in the receiver ryegrass, and the fungal network was significantly more complex. The activities of catalase and polyphenol oxidase exhibited a positive correlation with the alpha-diversity of the ryegrass phyllosphere fungi and also showed a significant positive relationship with the relative abundance of microbes associated with resistance to disease. In summary, this study revealed differences in the phyllosphere microbiomes of receiver ryegrass linked through CMNs to pathogen-infected and uninfected donor clovers. These changes in the phyllosphere microbiomes correlated with elevated levels of defense enzymes in the receiver ryegrass linked by white clover infected with pathogens, thus, potentially playing a role in plant defense against pathogens. These findings provide novel insights into the role of CMNs in reshaping phyllosphere microbiomes at the plant community levels under pathogen invasion.