Holobiont Plasticity Under Abiotic Stress: A Systems Biology Perspective on Plant–Bacteria–Fungi Interactions

ABSTRACT

Abiotic stress frequency and intensity are increasing, severely impacting plants' health, hence leading to significant crop yield losses (~20%–40% globally). In addition to modifying their genetic and physiological traits to increase stress tolerance, growing research revealed that plant–microbiome interaction plays a remarkable role in determining stress resilience. This review integrates physiological, ecological, and multi‐omics data suggesting holobiont plasticity is an unifying paradigm for mechanistic understanding of stress‐induced plant–microbe system reorganization. Abiotic stress causes rapid changes in plants' root metabolism and root exudate composition, which alter the release of organic acids, phenolics, osmolytes, and signaling compounds, which selectively change the microbial community's structure in the rhizosphere and endosphere. Microbial taxonomic diversity usually declines under stress conditions. Meanwhile, functional redundancy within the microbial communities is generally maintained or can increase. However, network connectivity may often remain stable or become stronger under stress, and the centrality of keystone taxa usually increases. These keystone microbes play a critical role in sustaining microbial community structure and function. Microbial regulation of phytohormones (such as auxin, ethylene, and abscisic acid), along with control of redox balance, osmotic adjustment, and nutrient cycling, improves plant water use, nutrient uptake, and root development. This often makes them more tolerant to stress by 15%–60% without increasing their biomass. Holobiont plasticity emerges as a quantifiable and potentially predictive characteristic of plant stress responses by integrating microbial network structure, functional gene profiles, metabolomic responsiveness, and host regulatory mechanisms. These responses function on ecological timescales (days to weeks), preceding the more gradual process of host genetic adaptation. This halobiont plasticity‐based framework shows promising potential but requires validation under field conditions to prove its robustness and applicability. This opens new avenues for microbiome‐assisted plant growth and development of a climate‐resilient agricultural system.