Institute for Plant Sciences, University of Cologne, The Cluster of Excellence on Plant Sciences (CEPLAS) Köln, Nordrhein-Westfalen, Germany
Mutualistic fungi play a pivotal role in plant health, yet the molecular strategies that enable them to colonize diverse hosts, coordinate with bacterial partners, and stabilize microbiome function remain largely unexplored. Using Serendipita indica as a model, we show that beneficial root endophytes deploy effectors with evolved multifunctionality, modularity, and synergy to promote host compatibility, suppress microbial competitors, and mitigate pathogen-induced damage. We characterize multifunctional effectors such as SiDLD1, a member of the DELD family, which facilitates fungal accommodation by scavenging host-derived reactive oxygen species at entry sites and regulating iron homeostasis, while also restricting Bipolaris sorokiniana through suppression of lipid peroxidation and ferroptotic-like cell death. We describe modular effectors like PEPSI6, a member of a novel prion-like protein family targeted to host plastids, which interacts with plastid-resident proteins and undergoes host-mediated cleavage to release an antimicrobial peptide that protects the fungal niche. Synergistic effector pairs further modulate host immunity by generating infochemicals such as deoxyadenosine from host substrates or degrading acetylated xylan in monocot roots, achieving emergent functions not possible individually. Rather than merely evading host defenses, beneficial fungi orchestrate mutualism through multifunctional and coordinated effector networks that promote compatibility and shape microbial communities. These expanded effector roles and their interactions with other microbiota-derived molecules offer a mechanistic foundation for engineering stable consortia with built-in stress protection.