Environmental stress acts on both sides of the root–microbe interface. Drought, salinity and heat directly alter moisture, ion activity, temperature and the physical movement of molecules through soil, potentially favoring microbes able to tolerate those conditions. At the same time, they reprogram the plant. Changes in photosynthesis and source–sink relations can reduce the carbon available for root growth and rhizodeposition; low water potential can constrain hydraulics and root expansion; nutrient deficiency can activate specialized exudation programs; and oxidative stress can alter both secretion and microbial tolerance. Unplanted soil, sterile exudate transfer, split-root systems and grafting are therefore needed to distinguish environmental filtering from plant-mediated niche construction.

Carbon provides a particularly clear example of why abundance alone is inadequate evidence. Under drought and heat, plants may divert less photosynthate toward roots or alter the balance among sugars, organic acids, amino acids, osmolytes and specialized metabolites. Microbial features associated with carbohydrate use, iron acquisition or secondary-metabolite consumption may therefore identify the substrate landscape created by altered plant allocation, rather than a directed exchange. Exudation also has a physiological cost. A convincing analysis must measure photosynthesis, carbon transport to roots, exudation rate, microbial uptake and plant benefit, then ask whether the functional return exceeds the carbon invested. Long or pooled exudate collections can blur this calculation by integrating circadian and developmental changes while allowing microbes to consume or transform released compounds.

Water status and nutrient demand provide other well-defined control points. Under phosphate starvation, plants release strigolactones that stimulate mitochondrial activity and hyphal branching in arbuscular mycorrhizal fungi, increasing the likelihood of contact and phosphorus exchange. Iron deficiency activates MYB72-dependent coumarin secretion, which changes iron chemistry and favors bacteria with appropriate tolerance or metabolic capacity. In legumes, flavonoids bind the rhizobial NodD regulator, activate nod genes and initiate the Nod-factor-dependent processes required for root-hair response and nodulation. These pathways are not simple invitations to unlimited colonization: mycorrhizal fungi and rhizobia consume photosynthate, and plants can restrict colonization when nutrient demand is met. Recruitment is consequently a physiological trade-off among nutrient return, carbon expenditure, growth and defense.

Plant hormones and immunity determine the permissiveness in which microbial signals can be interpreted. Salicylic acid pathway perturbations can selectively change bacterial taxa without excluding the entire community, while jasmonate and ethylene effects differ among root compartments. Auxin contributes to root development and rhizobial infection, and abscisic acid coordinates stomatal closure, hydraulics, root growth and carbon allocation under drought. Direct receptor-level evidence that abscisic acid itself recruits microbes remains limited, so it is better treated as an upstream regulator of the root environment. The review also cautions that both excessive and insufficient immunity can disrupt assembly: dysfunction of the chromatin regulator IBM1 produces autoimmunity and reorganizes the Arabidopsis root microbiome.

Microbes decode those physiological outputs in several ways. Chemoreceptors can redirect movement toward particular exudate components, dedicated receptors can activate specialized responses, and transporters or catabolic pathways can provide a growth advantage without a classical signal receptor. Coumarin-responsive Pseudomonas, for instance, activates transport, stress and metabolic programs, while bacteria able to import and degrade root compounds may also change what neighboring organisms encounter. A compound can simultaneously act as an attractant, nutrient, antimicrobial, osmoprotectant or redox-active molecule. Its effect therefore depends on concentration, mixtures, release location, timing, plant immunity, community competition and microbial capacity. A single compound cannot be assigned recruitment specificity without testing those interacting conditions.

The strongest mechanistic examples connect a physiological trigger to biosynthesis, transport or release, a microbial decoder, a colonization response and a plant consequence. Transport is a critical part of this sequence: an ATP-binding cassette transporter in soybean links genistein export to rhizobial NodD activation, while differences in SWEET sugar transporters can organize microbial colonization along the Arabidopsis root axis. Spatial release, timing and immune context may be as important as molecular identity. Emerging evidence also implicates purines, pyrimidines, pipecolic-acid-associated profiles and compatible solutes. Salt-stressed wild soybean, for example, has been linked to purine-responsive Pseudomonas, and water-stressed wheat exudates containing choline and glycine betaine induced quaternary-ammonium transport and catabolism in Pseudomonas synxantha. These findings remain less causally complete than the flavonoid–NodD, strigolactone–mycorrhizal and coumarin systems.

Even after a community forms, its presence does not demonstrate a physiological benefit. Enrichment means a change in relative abundance; colonization requires verified root association; persistence requires temporal stability; functional activity requires a measured or expressed process; and benefit requires an improved plant phenotype in the specified context. These endpoints can diverge. A drought-enriched lineage may survive because it tolerates low water potential while only particular strains protect the plant. A synthetic community can establish in sterile material but fail among resident competitors. Similarly, microbial hormone production in culture is not evidence that the plant’s hormone network changes. Strong feedback studies require a targeted microbial perturbation, a corresponding change in host physiology, and rescue of the predicted phenotype through nutrient flux, hydraulic measurements, hormone reporters, redox imaging, growth and defense tests.

The proposed feedback can extend beyond a one-way benefit. Mycorrhizal colonization has been associated with coordinated changes in root and leaf aquaporins, faster recovery of stomatal conductance and carbon dioxide assimilation after drought, and in Lotus japonicus, the AM-colonization-linked gene LjNIP1;5. Microbial metabolites can also alter hormone balance, antioxidant capacity, compatible-solute pools and growth–defense allocation. A complete iterative loop is more demanding, however: a microbial change must alter a defined plant physiological variable or root output, and that altered plant state must then redirect subsequent microbiome assembly. The review identifies only limited examples that resolve all these steps in one time-resolved experiment. Most current evidence instead connects reciprocal processes across separate studies, such as phosphate starvation, coumarin release and microbial responses, without directly demonstrating a return effect on assembly.

For microbiome interventions, the review favors designs built around a falsifiable plant–microbe mechanism. Researchers could manipulate a plant biosynthetic pathway, transporter, secretion site, root architecture or immune state, then perturb a microbial receptor, chemotaxis module, transporter, catabolic pathway or stress-tolerance function. Synthetic communities are useful for this work: plant knockouts can test signal production, microbial mutants can test decoding, strain dropout can reveal keystone or redundant functions, and complementation or metabolite rescue can reconstruct the proposed chain. Colonization, persistence, activity and plant benefit must be measured separately, with failure to establish, loss of function and physiological costs treated as informative outcomes. Final validation should include resident soil communities, multiple plant genotypes, realistic stress fluctuations and field conditions, because a defined plant state may create a similar functional niche through different organisms without recruiting the same named taxon in every environment.

Subject of Research: Plant physiological control of root microbiome assembly and microbial feedback under environmental stress

Article Title: Plant physiological control of root microbiome assembly and feedback under environmental stress

Article References: Ge, M., Chen, Q., Wang, Y., Han, Y., Lian, F., Hou, S., Chen, X., Liu, J., Zhong, C., Zhang, Q., & Xu, X. (2026). Plant physiological control of root microbiome assembly and feedback under environmental stress. Frontiers in Microbiology, 17, 1974097. https://doi.org/10.3389/fmicb.2026.1974097

Image Credits: AI Generated

DOI: 10.3389/fmicb.2026.1974097

Keywords: plant stress physiology, root microbiome assembly, plant–microbe interactions, root exudates, microbial feedback, immune gating, environmental stress, nutrient signaling, rhizosphere ecology, synthetic communities, Plant, physiological