Arbuscular mycorrhizal fungi orchestrate belowground microbiomes in plant holobionts

The traditional model of plant-arbuscular mycorrhizal (AM) fungal coevolution, based solely on interactions between plants and AM fungi, became obsolete with the discovery of the critical roles that belowground microbiomes play in the function of mycorrhizal symbiosis. Based on insights into hyphosphere microbiota, we expand the plant-AM fungus-bacterium continuum into a multipartite AM fungal-orchestrated holobiont (H-AMF) framework, where AM fungi integrate plant roots with soil microbiota into a cross-kingdom ecological unit. A division of labor exists among plants, AM fungi, and hyphosphere microbes in the mycocentric H-AMF perspective. We summarize mechanisms by which AM fungi sustain cooperative relationships with plants and hyphosphere microbiota and propose holobiont-scale methodologies to advance understanding of plant-fungal-microbial interactions and their ecological functions.