Reprogramming the Plant Holobiont: From Microbiome Assembly to Durable, Eco-Sustainable Disease Defence
TL;DR
It is concluded that the future of eco-sustainable disease management depends not on replacing chemical inputs with a single microbial substitute, but on the capacity to design and manage functionally redundant, context-adapted microbial communities capable of sustaining plant resilience over time.
Abstract
Plants are no longer understood as autonomous organisms but as holobionts whose associated microbial communities co-determine growth, stress tolerance and disease outcomes. Decades of work on disease-suppressive soils, induced systemic resistance and biological control have established that individual beneficial microorganisms can protect crops, yet the field performance of single-strain inoculants remains inconsistent. This has driven a conceptual shift from introducing individual biocontrol agents towards understanding, assembling and deliberately "reprogramming" whole plant-associated microbial communities to achieve durable disease suppression. This review synthesises evidence across the rhizosphere, phyllosphere, endosphere and seed microbiomes to trace a conceptual progression: microbiome assembly, plant-microbiome-pathogen signalling, microbiome-mediated disease suppression, and microbiome reprogramming towards a resilient holobiont. We critically examine the shift from asking which organisms are present to asking what the microbiome is functionally doing, drawing on keystone-taxa and co-occurrence-network concepts, and we distinguish correlation from demonstrated causal contribution wherever the evidence allows. We organise reprogramming strategies into host-mediated, microbial, soil/agronomic and precision-engineering categories, and we critically evaluate synthetic microbial communities (SynComs), noting that laboratory- and greenhouse-validated consortia frequently lose efficacy under field conditions because of community instability, competitive exclusion by resident microbiota and environmental variability. Omics and computational tools are reshaping this field from descriptive surveys towards predictive, intervention-oriented science, but translation from mechanism to field-deployable products remains the central bottleneck. We conclude that the future of eco-sustainable disease management depends not on replacing chemical inputs with a single microbial substitute, but on the capacity to design and manage functionally redundant, context-adapted microbial communities capable of sustaining plant resilience over time.