Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome
Abstract
1. Introduction
2. Root Exudates: The Currency of Root Microenvironment Exchange
3. Rhizosphere Microbes-Mediated Plant Metabolic Reprogramming
| Plant Species | PGPM Strain | PGPM Type | Key Metabolic Changes | Function | References |
|---|---|---|---|---|---|
| Brassica napus L. | Bacillus amyloliquefaciens | Bacteria | flavonoid and anthocyanin biosynthesis ↑ | Plant growth-promoting | [53] |
| A. thaliana | P. simiae | Bacteria | MYB72/FRO2/IRT1/FIT ↑ | induced systemic resistance, iron acquisition | [54] |
| A. thaliana | P. simiae, P. capeferrum | Bacteria | MYB72/BGLU42 ↑, scopoletin ↑ | improved niche establishment for the microbial partner | [55] |
| A. thaliana | B. amyloliquefaciens, T. harzianum | Bacteria, Fungi | SA and JA/ET signaling pathways activation | induced systemic resistance | [60,61] |
| A. thaliana | T. harzianum | Fungi | MYB72 expression ↑, NO accumulation | ISR against Botrytis cinerea | [62] |
| Solanum lycopersicum (tomato) | Rhizosphere microbiome (undefined) | Microbial consortium | Azelaic acid hexose ↑, SIREM activation | Systemic metabolic reprogramming, stress resilience | [6] |
| Triticum aestivum (wheat) | Bacillus velezensis | Bacteria | Proline ↑, GABA ↑, flavonoids ↑ | Drought stress tolerance | [63] |
| Oryza sativa (rice) | Chlorella vulgaris, N2-fixing bacteria | Microalgae-bacteria consortium | Biomass ↑, N content ↑ | Enhanced N availability, improved germination | [64] |
| Glycine max (soybean) | Bradyrhizobium japonicum | Bacteria | Flavonoid exudation ↑, nodulation ↑ | N2 fixation enhancement | [65] |
| Cucumis sativus (cucumber) | PGPR consortium | Bacteria | Phenolic acids ↑, flavonoids ↑ | Resistance against Fusarium oxysporum | [66] |
| Chlamydomonas reinhardtii | Methylobacterium aquaticum | Alga, Bacteria | IAA (from alga) ↑, IAA (degraded by bacterium) ↓ | Mutualistic growth promotion |
4. Molecular Mechanisms of PGPMs-Induced Metabolic Reprogramming
4.1. Phytohormone Signaling: The Central Orchestrator
4.2. Transcriptional Reprogramming: Key Regulators and Their Targets
4.3. Epigenetic and Post-Translational Regulation
4.4. Regulation of Transporters: Gatekeepers of Exudation
5. Application Advantages of PGPMs Mediated Metabolic Reprogramming
5.1. Shaping a Disease-Suppressive Microbiome
5.2. Enhancing Abiotic Stress Tolerance
5.3. Improving Nutrient Acquisition and Use Efficiency
5.4. Toward Sustainable Agricultural Practices
6. Methodological Approaches and Future Directions
6.1. Integrated Multi-Omics: Unraveling Complex Interactions
6.2. Synthetic Microbial Communities: Testing Function in Defined Systems
6.3. Leveraging Plant Genetics and Genome Editing
6.4. Future Directions and Challenges
7. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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| PGPM Group | Representative Genera | Key Functions | Examples | References |
|---|---|---|---|---|
| Bacteria | Pseudomonas, Bacillus, Rhizobium, Azospirillum, Burkholderiar | N2 fixation, P solubilization, IAA production, ISR induction | P. simiae WCS417 induces ISR in Arabidopsis via MYB72; B. velezensis FZB42 promotes growth and suppresses pathogens in multiple crops | [36,37] |
| Fungi (AMF) | Rhizophagus, Funneliformis, Glomus | P and N acquisition, water uptake, soil aggregation | R. irregularis enhances P uptake in maize under low-P conditions; AMF colonization improves drought tolerance in wheat | [38,39] |
| Fungi (Biocontrol) | Trichoderma spp. | Mycoparasitism, antibiotic production, ISR induction | T. harzianum T-78 triggers ISR against Botrytis cinerea in Arabidopsis via MYB72 and NO signaling | [40] |
| Microalgae | Chlamydomonas, Chlorella, Scenedesmus | IAA production, O2 provision, biofilm formation | C. reinhardtii produces IAA via LAO1, promoting mutualism with Methylobacterium; Chlorella-bacteria consortia enhance N availability in rice | [30,41] |
| Cyanobacteria | Anabaena, Nostoc, Synechococcus | N2 fixation, EPS production, soil stabilization | Anabaena enhanced the length of cucumber seedling stems; cyanobacterial inoculants improve rice yield | [42,43] |
| Regulator/Transporter | Type | Induced by | Target Process/Metabolite | Function in Rhizosphere | References |
|---|---|---|---|---|---|
| MYB72 | Transcription Factor | Pseudomonas spp. | Coumarin biosynthesis | Iron chelation, pathogen suppression | [52,67,68] |
| ERF1 | Transcription Factor | JA/ET signaling | Antimicrobial synthesis | Broad-spectrum defense | [69,70,71] |
| GRAS (e.g., NSP1) | Transcription Factor | AMF | Strigolactone biosynthesis | Hyphal branching, symbiosis | [72,73] |
| ALMT1 | Transporter | PGPM, Low Pi, Acid soil | Malate, Citrate efflux | P solubilization, pH modulation | [77,78,79] |
| ABC transporters | Transporter | Iron deficiency, PGPR | Coumarin secretion | Microbial recruitment, Fe uptake | [80,81] |
| Application Domain | Specific Mechanism | Representative PGPMs | Key Plant Metabolites/Processes |
|---|---|---|---|
| Shaping a disease-suppressive microbiome | Selective recruitment of beneficial microbes; direct production of pathogen-inhibiting compounds. | Pseudomonas spp. (e.g., P. simiae), Bacillus spp., specific fungi | Benzoxazinoids, phenolic acids, flavonoids, coumarins (e.g., scopoletin) |
| Enhancing abiotic stress tolerance | Improvement of soil environment (e.g., water retention); direct assistance in stress response (e.g., ion homeostasis, ROS scavenging). | Bacillus spp., Pseudomonas spp., AMF | Osmolytes (e.g., proline), exopolysaccharides, organic acids, ACC deaminase activity |
| Improving nutrient acquisition and use efficiency | Chelation of sparingly soluble nutrients; signaling molecules to promote beneficial symbioses. | Pseudomonas spp., Rhizobia, AMF, specific microalgae-N2-fixing bacteria consortia | Coumarins (e.g., scopoletin), organic acids (e.g., citrate, malate), flavonoids, SLs |
| Induce plant systemic resistance | ISR via JA/ET signaling pathways | Pseudomonas spp. (e.g., P. simiae, P. capeferrum), Bacillus spp. (e.g., B. amyloliquefaciens), Trichoderma spp. | MYB72 activation |
| Method | Core Principle | Advantages | Limitations |
|---|---|---|---|
| Multi-omics (genomics, transcriptomics, metabolomics, metatranscriptomics) | High-throughput molecular profiling to identify genes, transcripts, metabolites, and microbial functions | Comprehensive, unbiased, hypothesis-generating; reveals novel pathways and biomarkers | Data heterogeneity across platforms; distinguishing biological signals from technical artifacts; correlation ≠ causation; high cost and expertise required |
| SynComs | Defined consortia of culturable microbes designed to recapitulate key functions of native microbiomes | Reductionist approach enables causal testing of microbial interactions and functions; reproducible under controlled conditions | May oversimplify natural complexity; community stability uncertain under field conditions; requires extensive isolation and characterization |
| Genome Editing (CRISPR-Cas) | Precise modification of plant genes involved in signaling (e.g., MYB72), transport (e.g., ABC transporters), and exudate biosynthesis | Enables causal testing of gene function; potential to create “microbe-recruiting” crop varieties | Off-target effects; regulatory constraints; ecological risks (gene flow, non-target effects); trade-offs (carbon cost, pathogen susceptibility) |
| Advanced Formulation Technologies (nano-encapsulation, alginate microencapsulation, fluidized bed drying) | Physical protection of microbial cells to enhance survival during storage and after application | Extended shelf-life; protection from desiccation, temperature stress, and predation | Cost; scalability; carrier material biocompatibility; inconsistent field performance across soil types |
| Field-Omics | Longitudinal multi-omics monitoring under real-world agricultural conditions | Identifies environmental and agronomic factors governing PGPM success; validates lab findings in situ | High complexity; confounding variables; requires extensive replication across sites and seasons |
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Song, P.; Deng, Y.; Yu, Y.; Zhang, L.; Liu, Y. Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome. Microorganisms 2026, 14, 578. https://doi.org/10.3390/microorganisms14030578
Song P, Deng Y, Yu Y, Zhang L, Liu Y. Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome. Microorganisms. 2026; 14(3):578. https://doi.org/10.3390/microorganisms14030578
Chicago/Turabian StyleSong, Pei, Yue Deng, Yaoying Yu, Lei Zhang, and Yong Liu. 2026. "Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome" Microorganisms 14, no. 3: 578. https://doi.org/10.3390/microorganisms14030578
APA StyleSong, P., Deng, Y., Yu, Y., Zhang, L., & Liu, Y. (2026). Plant Growth-Promoting Microorganisms Mediate Plant Metabolic Reprogramming to Manage the Rhizospheric Microbiome. Microorganisms, 14(3), 578. https://doi.org/10.3390/microorganisms14030578

