Microbiome-mediated plant immunity: Molecular signalling, community assembly, and emerging intergenerational feedback

Classical pattern-triggered (PTI) and effector-triggered (ETI) immunity, developed in single-pathogen systems, illuminates how plants recognise molecular threats but cannot fully explain immune homeostasis within the dynamic microbial communities plants encounter in nature. The extended plant immune system reframes immunity as a host-microbiome network sculpted by root exudates, yet two dimensions remain insufficiently integrated: the ecological rules translating recruited communities into systemic immune output, and the mechanisms by which holobiont state may carry over across generations. We propose that plant immune homeostasis is best analyzed as a three-node feedback circuit that we hypothesize closes across generations. Node 1 (molecular recruitment) integrates root exudate-mediated cross-kingdom signalling, in which primary and secondary metabolites jointly serve nutritional and immune-informative roles. Node 2 (ecological translation) is governed by dispersal, immune filtering, drift, priority effects, and functional redundancy, which together determine whether recruitment signals translate into immune buffering. Node 3 (intergenerational carry-over) comprises three mechanistically distinct routes-epigenetic reprogramming, seed microbiota transmission, and soil legacy-that range from provisionally established to largely hypothetical and whose field-scale validation remains limited. Treating this circuit, rather than the host or host-microbiome network, as the minimal unit of immune analysis generates testable predictions-linking functional redundancy to immune buffering, soil legacy to next-generation priming, and node-specific failure modes to dissociable signatures. This framing positions the holobiont across time (understood here as an analytical unit rather than an evolutionary one) as a tractable framework for hypothesis-driven plant immunity research.