Microbial partnerships and molecular mechanisms in plant stress physiology for climate-resilient and sustainable farming

Abstract

Main conclusion

Plant-microbial partnerships and their underlying molecular mechanisms are indispensable, natural drivers of improved nutrient acquisition and stress tolerance in the face of climate-driven environmental challenges. Modern multi-omics tools, when coupled with artificial intelligence and synthetic biology, enable the precise design of targeted bioinoculants and synthetic microbial consortia. Translating these advanced microbiome-based strategies into scalable, field-level agricultural applications provides a sustainable path toward securing global food production while maintaining soil health.

Abstract

Global climate change imposes multifaceted abiotic and biotic stresses on crops, disrupting physiological and molecular processes and threatening agricultural productivity. Plant-associated microbes represent an underexplored yet powerful ally in enhancing crop resilience. This review presents current knowledge of plant–microbe interactions and the molecular mechanisms governing plant stress physiology, with an emphasis on climate-resilient and sustainable farming. Hence, ever-changing environmental cues pose a significant burden on agricultural productivity, and plant-associated microbial communities modulate a cascade of physiological and molecular responses, including production of phytohormones, signaling, regulation of reactive oxygen species homeostasis, and activation of plant immune responses to help plants withstand stress and enhance productivity. Moreover, root exudates, phytohormones, and quorum sensing mediate the central communication networks, facilitating plant–microbe cross talk. Additionally, the advances in OMICs approaches aid in disentangling the molecular underpinnings of these interactions by providing mechanistic insights and potential candidate gene targets for crop improvement and stress resilience. In the post-genomic era, integrating artificial intelligence and big data analysis to optimize microbiome-based strategies for sustainable agriculture is a new frontier for disentangling plant–microbe symbiosis to improve soil health, enhance crop yields, and improve stress tolerance. Thus, by integrating the ecological, physiological, and molecular perspectives, this review highlights the transformative potential of harnessing plant–microbe symbiosis for climate-resilient and sustainable agriculture.

Highlights

This review provides an up-to-date synthesis of plant–microbe interactions and their molecular roles in enhancing plant tolerance to multiple abiotic and biotic stresses under climate change scenarios. It integrates physiological, molecular, and omics-based perspectives across diverse microbial groups, including bacteria, fungi, archaea, and viruses. The review also highlights the potential of microbial symbiosis, together with emerging OMICS, AI, and Big Data approaches, to improve climate resilience and support sustainable agriculture.

Introduction

Being sessile, plants are continually challenged by a myriad of environmental stresses. These cues impede the plant physiological processes and eventually compromise growth, development, and productivity (Yuan et al. 2024). Abiotic and biotic stresses severely hinder plant performance, resulting in substantial yield losses and posing a major challenge to meeting the rising food demand to feed the growing global population (Atta et al. 2023). Thus, plants have evolved highly sophisticated and intricate stress-adaptive mechanisms that involve a complex, regulated interplay of morphological, physiological, molecular, and cellular adjustments to ensure survival under stressful conditions. These intricate mechanisms are orchestrated by a complex regulatory network involving signaling molecules such as abscisic acid (ABA) and reactive oxygen species (ROS), which are crucial mediators in stress perception, signal transduction, and governing response mechanisms (Renzetti et al. 2025; Zhang et al. 2025a, b).

Beyond these endogenous molecular stress response mechanisms, plants often make symbiotic associations with microorganisms. Microbes, omnipresent in nature, possess remarkable metabolic versatility that enhances plant growth and development, increases productivity, and mitigates the impacts of stresses (Chukwudi et al. 2025). Such interactions enable plants to develop local and systemic defense mechanisms. Beneficial microorganisms such as endophytes, arbuscular mycorrhizal fungi (AMF), and plant growth-promoting rhizobacteria (PGPRs) hold immense promise for improving crop resilience and productivity through nutrient acquisition, physiological response modulation, and contributing to the adaptive plant metabolism and overall health (Liu et al. 2025a, b, c, d; Yusuf et al. 2025). The interaction between plants and microbes is a two-way process, in which plants secrete a wide array of metabolites, including phenolics, amino acids, sugars, and organic acids, that selectively shape microbial communities. In turn, microbes influence plant gene expression through lipo-chitooligosaccharides, volatile organic compounds (VOCs), and other small signaling molecules (Pantigoso et al. 2022). This two-way communication establishes a dynamic and responsive molecular network that is highly sensitive to environmental cues (Liu et al. 2025a, b, c, d). They profoundly influence plant health, growth, and stress resilience by reducing the need for synthetic fertilizers and pesticides, leading to more environmentally friendly and economically viable farming practices that enhance biodiversity and soil fertility (Ahmad et al. 2023). Nowadays, exploring sustainable alternatives, particularly microbial formulations, has transitioned from a theoretical consideration to an absolute necessity. Thus, this review elucidates the intricate molecular dialogues between plants and microbes in the age of artificial intelligence (AI) and big data for agricultural sustainability and stress resilience.

Role of microbes for sustainable agriculture and soil health

Microbes play a vital role in sustainable agriculture by driving nutrient cycling, enhancing soil fertility, promoting plant health, improving soil structure, pest control, and aiding in environmental remediation (Kruščić et al. 2025). By enhancing carbon sequestration and improving soil aggregation, microbial communities play a crucial role in mitigating climate change and maintaining long-term soil fertility, making them indispensable for building resilient, productive, and environmentally friendly agroecosystems, thereby reducing the need for synthetic fertilizers (Brar et al. 2024). Certain bacteria, such as Rhizobium and Bradyrhizobium spp., form symbiotic associations with legume plants, inhabiting root nodules and converting atmospheric nitrogen (N₂) into ammonia (NH₃) for plant use. This biological nitrogen fixation process reduces the dependence on synthetic fertilizers and minimizes environmental pollution. Beneficial bacteria also enhance soil aggregation and stability by producing polysaccharides and other adhesives that bind soil particles, thereby improving soil structure, reducing erosion, and enhancing water infiltration and retention (Trivedi et al. 2018). They also play a role in bioremediation, with genera like Pseudomonas and Bacillus capable of degrading hydrocarbons, pesticides, heavy metals, and other pollutants, thereby detoxifying soils and restoring ecosystem health. Additionally, bacteria play a crucial role in the formation and stabilization of soil organic matter, thereby promoting carbon sequestration and mitigating climate change by storing atmospheric CO₂ in stable soil carbon pools (Ramesh et al. 2019).

Fungi drive soil carbon cycling by decomposing organic matter into stable organic carbon, sequestering CO₂, and helping mitigate the impacts of climate change on soil health (Enebe et al. 2025). For instance, saprotrophic fungi break down complex organic matter, including cellulose and lignin, to release nitrogen, phosphorus, and carbon, thereby enhancing soil fertility and enriching plant nutrition. Moreover, in phosphorus-poor soils, mycorrhizal fungi form root symbioses and extend their root systems to enhance phosphorus and water uptake (Volk 2013). Key genes such as GvPT (phosphate transport) (Sbrana et al. 2022), Fus3 (MAPK signaling pathway) (Hamel et al. 2012), and Scp1 (cysteine-rich proteins) (Liu et al. 2007) facilitate fungal symbiosis with plants by enabling nutrient exchange and fungal growth. Stress-response genes, such as SOD1 (Wang et al. 2022a, b) and HSP70 (Tian et al. 2023), enhance fungal survival under adverse conditions, thereby indirectly maintaining soil structure. Through their hyphal structures and the secretion of polysaccharides, fungi form stable soil aggregates that improve soil structure, water retention, infiltration, and resistance to erosion. Certain fungi also produce enzymes that degrade pollutants, including hydrocarbons, pesticides, and toxic metals, through enzymatic processes, thereby contributing to soil detoxification and environmental cleanup (Navina et al. 2024).

Archaea remain considerably less explored in agricultural systems than bacteria and fungi, and current evidence suggests that most archaeal contributions to plant productivity occur indirectly through soil biogeochemical processes rather than well-defined symbiotic associations. Many archaeal taxa function primarily as free-living microorganisms that regulate nutrient availability and greenhouse gas fluxes within the rhizosphere. For example, ammonia-oxidizing archaea such as Nitrosopumilus maritimus catalyze the first step of nitrification by converting NH₃ to nitrite (NO₂⁻) through ammonia monooxygenase, thereby influencing soil nitrogen turnover and improving plant nitrogen availability (Qin et al. 2024). Through this activity, archaea regulate nitrogen pools accessible to plants and shape rhizosphere microbial community dynamics. Archaea also play important roles in carbon and sulfur cycling, processes that indirectly affect plant health and soil fertility. In anaerobic plant-associated environments such as waterlogged soils or wetland rhizospheres, methanogenic archaea including Methanobacterium, Methanosarcina, Methanococcus, Methanosaeta, and Methanomicrobium generate methane (CH₄) from CO₂, acetate, or methylated compounds through the methyl-coenzyme M reductase pathway encoded by the mcrA gene (Thauer et al. 2008). Conversely, anaerobic methanotrophic archaea can oxidize methane back to CO₂ through reverse methanogenesis, regulating methane emissions from soil environments (Hallam et al. 2003). In the sulfur cycle, sulfur-reducing archaea such as Pyrococcus and Archaeoglobus utilize dissimilatory sulfite reductase and adenosine−5′-phosphosulfate reductase to reduce sulfate (SO₄²⁻) or sulfite (SO₃²⁻) to hydrogen sulfide (H₂S), whereas sulfur-oxidizing archaea such as Sulfolobus oxidize elemental sulfur through sulfur oxygenase-reductase pathways (Löffler et al. 2020). Although direct plant–archaea symbioses remain poorly characterized, through these metabolic activities, archaeal communities can modify the chemical and redox environment of the rhizosphere, influence microbial community dynamics, enhance nutrient use efficiency, and contribute to plant tolerance to environmental stresses. Their metabolic versatility, including participation in nitrogen transformations and regulation of greenhouse gas fluxes, may also indirectly enhance rhizosphere stability and nutrient retention. Thus, even if these interactions generally lack specialized symbiotic structures comparable to those observed in bacterial or fungal symbioses, they represent functional rhizosphere partnerships that may contribute to plant resilience and ecosystem stability (Wrede et al. 2012; Siliakus et al. 2017). Additionally, archaeal lineages adapted to extreme environments possess stress-resistant metabolic systems that could theoretically contribute to plant resilience under harsh environmental conditions (Siliakus et al. 2017). Future research integrating metagenomics, transcriptomics, and rhizosphere ecology is therefore required to determine whether archaeal taxa form direct functional partnerships with plants or predominantly operate as free-living drivers of soil ecosystem processes.

Viruses are not only associated with plant diseases but also play valuable roles in sustainable farming. Some viruses serve as biological control agents against insect pests, targeting specific species and reducing the reliance on chemical pesticides (Abd-Alla et al. 2020). Cucumber mosaic virus, tobacco mosaic virus, and potato virus can also trigger systemic acquired resistance in plants, enhancing their natural defenses and improving overall plant and soil health (Shopova et al. 2020). Bacteriophages regulate soil bacterial populations, influencing nutrient cycling, soil fertility, and microbial community dynamics (Wang et al. 2024a). Additionally, viruses such as bean common mosaic virus and maize dwarf mosaic virus can serve as indicators of environmental health and soil quality, with viral monitoring providing insights into ecosystem dynamics and potential agricultural threats (Liang et al. 2024).

Plant–microbe interaction for abiotic stress tolerance

Global climate change stands as one of the biggest challenges to sustainable agriculture. Rising atmospheric CO₂ levels, elevated temperatures, erratic precipitation patterns, and increasing frequency of extreme weather events profoundly alter plant-environment interactions (Yuan et al. 2024). These climatic perturbations intensify both abiotic and biotic stressors, negatively affecting plant growth, development, reproduction, and productivity (Fig. 1). Plant-associated microbes mitigate abiotic stress by triggering physiological, biochemical, and molecular responses that enhance root system architecture, regulate ion uptake and nutrient metabolism, and the production of osmolytes and antioxidants (Liu et al. 2020a, b). Variation in the magnitude of these responses across host–microbe pairings may occur and likely reflect differences in microbial colonization efficiency, microbial metabolic traits, plant root architecture, transporter gene repertoires, and host genetic background.

Fig. 1.

An overview of plant stresses and response mechanisms in the era of global climate change

Drought stress tolerance

Reduced water availability induces oxidative stress, disrupts cellular homeostasis, and impairs photosynthesis, triggering plant transcription factors such as DREBs, MYB, and NAC, to activate protective downstream genes encoding dehydrins and osmolytes (Joshi et al. 2016; Nour et al. 2024). Beneficial microbes enhance these intrinsic plant responses through interconnected mechanisms including osmotic adjustment, antioxidant regulation, hormonal cross talk, structural root modification, and transcriptional reprogramming (Parmar et al. 2025. While response intensity varies across specific host–microbe pairings, literature widely confirms microbial convergence on these core defensive mechanisms (Table 1).

Table 1.

Some selected beneficial microbes and mechanisms of action for their potential role in mitigating the adverse effects of abiotic stress in plants

S. No	Abiotic stress	Plant species	Beneficial microbes	Mechanism of action	References
1	Drought stress	Arabidopsis thaliana	Bacillus megaterium	Changed the root architectural systems, increased ABA production and ROS scavenging, promoted plant growth, and produced volatile organic compounds like pentyl furan	Zhou et al. 2016
2		Brassica oxyrrhina	Pseudomonas libanensis TR1 P. reactans Ph3R3	Enhanced growth, pigment accumulation, and water content	Ma et al. 2016
3		Cicer arietinum L	Pseudomonas putida	Controlled responsive gene expression and maintained water content, osmolyte, membrane structure, and germination rate	Tiwari et al. 2016
4		Glycine max	Pseudomonas putida	Enhanced the secretion of gibberellins	Kang et al. 2014
5		Lycopersicon esculentum L	Bacillus megaterium	Increased auxin and cytokinin biosynthesis, as well as polyamine regulation	Nascimento et al. 2020
			Bacillus amyloliquefaciens	Increased capacity to create biofilms. Increased stress-responsive genes, such as lea, tdi65, and ltpg2	Wang et al. 2019a
			Streptomyces sp.	Altered the expression of ERF1 and WRKY70 under drought stress	Abbasi et al. 2020
6		Oryza sativa L	Pseudomonas flourescens	Activated genes involved in the ABA-mediated signaling cascade, including bZIP1, AP2-EREBP, and Hsp20	Saakre et al. 2017
7		Sorghum bicolor L	Bacillus sp.	Increased phosphate solubilization, siderophores, and auxin production	Grover et al. 2021
8		Triticum aestivum L	Piriformospora indica	Promoted nutrient and water absorption, improved root growth, biomass, water, and chlorophyll, and modulated antioxidant molecules	Hosseini et al. 2017
9		Zea mays L	Burkholderia phytofirmans	Enhanced growth through improving photosynthetic activity and carbohydrate metabolism	Naveed et al. 2014
10	Salinity stress	Arabidopsis thaliana	Klebsiella sp.	Modulates the expression of RbcL and WRKY1 genes	Sapre et al. 2018
11		Capsicum annuum L	Bacillus spp.	ACC deaminase promotes stress tolerance and reduces ethylene production in plants	Wang et al. 2018
12		Cicer arietinum L	Mesorhizobium ciceri	ACC-deaminase gene expression decreased the negative influence of salt stress and enhanced plant–rhizobium interaction	Brígido et al. 2013
13		Glycine max	Stenotrophomonas rhizophila ep-17	Enhanced root, dry weight, shoot length, uptake of P and N, and nodule number	Egamberdieva et al. 2016
14		Hordeum vulgare L	Hartmannibacter diazotrophicus	ACC deaminase enhanced root and shoot dry weight and plant growth	Suarez et al. 2015
15		Oryza sativa L	Enterobacter sp.	Promoted seedling growth, reduced ethylene production, and increased antioxidant enzyme activity	Sarkar et al. 2018a
16		Solanum lycopersicum L	Streptomyces sp.	Proline and ACC deaminase production and plant growth promotion	Palaniyandi et al. 2014
17		Triticum aestivum L	Dietzia natronolimnaea	Regulation of ABA signaling cascade, genes linked to the SOS pathway, tissue-specific responses of ion transporters	Bharti et al. 2016
18	Toxic metal stress	Brassica nigra	Microbacterium sp., Curtobacterium sp.	Reduced Zn, Pb, Cu, and As concentration and effect	Román-Ponce et al. 2017
19		Clethra barbinervis	Phialocephala fortinii, Rhizodermea veluwensis, and Rhizoscyphus sp	Improved K absorption in shoots and decreased the concentrations of Cd, Zn, Pb, Cu, and Ni in roots	Yamaji et al. 2016
20		Glycine max	Paecilomyces formosus, Sphingomonas sp.	Arsenic stress tolerance	Bilal et al. 2018
21		Helianthus annuus	Ralstonia eutropha, Chryseobacterium humi	Reduced Zn and Cd toxicity	Marques et al. 2013
22		Oryza sativa L	Bacillus strains	Improved plant growth-promoting traits and reduced the harmful effects of cadmium	Ali et al. 2022b
23		Triticum aestivum L	Bacillus cereus, Pseudomonas moraviensis	Alleviation of Cu, Cr, Co, Cd, Ni, Mn,, and Pb toxicity	Hassan et al. 2017
24		Zea mays L	Enterobacter, Leifsonia, Klebsiella, Bacillus	Improved resistance to Cd toxicity	Ahmad et al. 2016
25	Heat stress	Cucumis sativus	Thermomyces sp.	Increase in antioxidant enzyme activities, soluble proteins, flavonoids, saponins, and total sugars	Ali et al. 2018
26		Solanum tuberosum L	Ochrobactrum cytisi	Improved the mitotic index of root meristem cells, the number of roots, the number of leaves, and the length of shoots	Burygin et al. 2019
27		Sorghum bicolor L	Pseudomonas sp. AMK-P6	Increased antioxidant enzyme activities and heat tolerance	Ali et al. 2009
28		Triticum aestivum L	Bacillus safensis and Ochrobactrum pseudogrignonens	Increased antioxidant enzyme activity and reduced chloroplast and membrane injury	Sarkar et al. 2018b
29	Cold stress	Capsicum annum	Pseudomonas frederiksbergensis	Increased IAA and ACC deaminase activity	Choudhury et al. 2021
30		Cucumis sativus L	Rhizophagus irregularis	Improved photosynthetic rates and transpiration rates	Ma et al. 2019
31		Triticum aestivum L	Bacillus spp.	Regulating phytohormone gene expression and increasing plant growth under cold stress	Zubair et al. 2019
32		Vitis vinifera	Burkholderia phytofirmans	Improved tolerance to low temperature	Theocharis et al. 2012

Maintaining cellular turgor under water deficit is critical for plant drought tolerance. PGPRs and AMF sustain osmotic balance by stimulating the accumulation of osmolytes, including proline, soluble sugars, and trehalose. Mechanistically, these beneficial microbes upregulate essential host genes; Pseudomonas enhances P5CS for proline biosynthesis in maize, P. simiae induces protective LEA genes to shield cellular structures in soybean, Azospirillum upregulates NHX1 for ion homeostasis in rice, and Bacillus and AMF elevate TPS1 expression for robust cellular osmoprotection in barley (Lenoir et al. 2016; Vaishnav & Choudhary 2019; Bouremani et al. 2023; Abdelaal et al. 2024; Ferioun et al. 2024; Salman et al. 2025).

Drought-induced oxidative stress necessitates efficient ROS scavenging. Beneficial microbes mitigate oxidative damage across diverse crops by upregulating plant antioxidant machinery. Specifically, PGPRs elevate superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and glutathione S-transferase (GST) expressions alongside heat shock proteins (Tiwari et al. 2016; Shang et al. 2025). Concurrently, AMF inoculation enhances photosystem II efficiency, reduces electrolyte leakage, and stimulates antioxidant enzyme and flavonoid accumulation, preserving chlorophyll synthesis and growth under water deficit (Krishna et al. 2022; Manjunatha et al. 2022; Abdelaal et al. 2024).

Microbial regulation of phytohormones coordinates plant drought adaptation with growth maintenance. PGPRs synthesize indole−3-acetic acid (IAA) to enhance root elongation and branching, optimizing water and nutrient uptake (Chauhan et al. 2024). To counteract drought-induced, IAA-stimulated ethylene accumulation, which restricts growth, 1-aminocyclopropane−1-carboxylate (ACC), deaminase-producing PGPRs degrade the ethylene precursor ACC into ammonia and $\alpha$-ketobutyrate, sustaining development (Niu et al. 2018; Chandra et al. 2019). Furthermore, PGPRs modulate ABA pathways to optimize stomatal conductance and water use efficiency (Cheng et al. 2021; Ahmad et al. 2022). Simultaneously, AMF extend the root absorptive network via extraradical hyphae, increasing hydraulic conductance and photosynthetic rates (Zou et al. 2023; Yang et al. 2025b). AMF also enhance magnesium uptake and chlorophyll synthesis, bolstering CO₂ assimilation. Complementing hormonal control, PGPRs secrete exopolysaccharides to improve soil aggregation and moisture retention. Collectively, these microbial symbionts enhance phosphorus availability and drought resilience across diverse crops, though efficacy varies with host compatibility and environmental severity (Tiwari et al. 2016; Yadav et al. 2024).

Transcriptionally, beneficial microbes fine-tune canonical plant drought-responsive pathways (Chauhan et al. 2024). In T. aestivum, Paenibacillus polymyxa upregulates RD29A/B (Liu et al. 2020), while Bacillus amyloliquefaciens elevates DREB-1E and ERF-1B in Pennisetum glaucum to boost antioxidative defense (Murali et al. 2021). In Zea mays, Rhizophagus intraradices upregulates SWEET13, CHIT3, and RPL23A, optimizing sugar transport and reducing MDA (Chen et al. 2025). AMF similarly activate genes encoding luminal binding, 14–3–3, and MAPK signaling components, collectively amplifying stress resilience (Lenoir et al. 2016; Shang et al. 2025).

Salinity tolerance

Soil salinization severely limits global agricultural productivity by disrupting enzymatic activity, membrane integrity, and cellular metabolism (Zhao et al. 2020; Atta et al. 2023). Plants natively adapt by extruding Na⁺ via the salt overly sensitive (SOS) pathway and sequestering excess Na⁺ and Cl⁻ into vacuoles via Na⁺/H⁺ antiporters (Zhao et al. 2020; Bachani et al. 2022). Beneficial microbes augment these native defenses by regulating host ion transporters. PGPRs maintain Na⁺/K⁺ balance via high-affinity potassium transporters (HKT) and SOS-related genes; for instance, Pseudomonas putida, upregulates SOS1 and NHX1 in Arabidopsis thaliana to promote Na⁺ extrusion and vacuolar compartmentalization (Giannelli et al. 2023), while Rhizobium azibense improves ion balance and growth in Phaseolus vulgaris (Shahid et al. 2024). Concurrently, AMF limit Na⁺ uptake to preserve membrane integrity, Rubisco activity, and photosynthetic efficiency under salinity stress (Wang et al. 2019b). In cowpea, Rhizophagus clarus enhances K⁺/Na⁺ homeostasis and grain yield (Tavares et al. 2024). Molecularly, AMF colonization restores salt-suppressed SlSOS1 and SlSOS2 expression (Liu et al. 2023), while Rhizophagus irregularis modulates shoot-specific transporters (OsCHX15, OsAKT2/3) in rice to optimize systemic ion distribution under saline conditions (Hsieh et al. 2022).

Microbial inoculation amplifies plant antioxidant systems to combat salt-induced ROS. In wheat, Klebsiella sp. decreases MDA while elevating SOD, CAT, and POX activities (Singh & Jha 2017). Acinetobacter johnsonii enhances soil enzymes and nutrient uptake in maize (Shabaan et al. 2022). AMF elevates antioxidants in Allium sativum (Golubkina et al. 2020), while mycorrhizal co-inoculation in peanut upregulates antioxidant transcripts and suppresses proline catabolism (Qin et al. 2021).

Microbial symbiosis mitigates salinity-driven photosynthetic decline, stabilizing pigments and carbon metabolism. AMF improve gas exchange and water use efficiency in Ocimum basilicum (Elhindi et al. 2017) and delay chlorophyll degradation in S. lycopersicum (Xie et al. 2019). In rice, Rhizophagus irregularis regulates starch biosynthesis and phosphate transport genes (Hsieh et al. 2022), while Bacillus megaterium solubilizes phosphorus to promote root growth and biomass in salt-stressed wheat (Fadiji et al. 2023).

Hormonal modulation represents another layer of salinity stress response regulation. AMF modulate phytohormone balance, including cytokinins and gibberellins, to stimulate shoot growth and assimilate transport under salinity stress (Chowdhary & Songachan 2025). Transcriptomically, AMF reprogram salt-responsive host genes regulating cell wall modification (OsXTH19, expansins), phosphate transport, and ROS detoxification (Hsieh et al. 2022), alongside aquaporins and SOS components (Liu et al. 2023). This genotype-dependent molecular plasticity demonstrates that microbial symbiosis comprehensively reshapes integrated stress signaling networks rather than acting through isolated genes (Table 1).

Heat stress tolerance

Escalating CO₂ levels drive an increase in environmental temperature, exacerbating heat stress that denatures proteins, disrupts membranes, and induces ROS accumulation (Xie et al. 2023; Bolan et al. 2024). Symbiotic microbes enhance plant thermotolerance through physiological and osmotic adjustments (Table 1). For instance, AMF inoculation in heat-stressed soybeans improves photochemical efficiency and reduces canopy temperature by 5.4 °C (Jumrani et al. 2022). Similarly, Bacillus strains promote growth in Oryza sativa and confer extreme thermal (up to 70 °C) and osmotic resilience in Arabidopsis (Shekhawat et al. 2021; Ali et al. 2023a).

Beneficial microbes mitigate heat stress-induced oxidative damage by enhancing plant antioxidant defenses, phytohormone signaling, and thermotolerance memory. In maize, Bacillus and Pseudomonas consortia enhance CAT and POD activity, preserve photosynthetic pigments at 45±2 °C, and modulate stress-responsive transcripts like CAT2 and DHN2 (Ahmad et al. 2023; Notununu et al. 2024). In soybean, B. cereus SA1 maintains ROS homeostasis and K⁺ gradients by regulating ABA signaling via GmLAX3 and GmAKT2 (Khan et al. 2020), while Aspergillus aculeatus provides selective antioxidant regulation in Lolium perenne (Li et al. 2021).

Furthermore, microbes reprogram phytohormone pathways and induce HSPs to prevent protein denaturation (Wang et al. 2014). Enterobacter sp. SA187 activates growth-promoting hormone networks and upregulates crucial HSPs (HSFA2, HSP101) and memory-associated genes (H3K4me3) in Arabidopsis (Sedaghatmehr et al. 2016; Liu et al. 2018; Shekhawat et al. 2020). Similarly, Bacillus strains induce diverse HSPs (15–100 kDa) in maize under 45–50 °C (Ahmad et al. 2023), establishing an integrated network that buffers hosts against thermal extremes.

Cold stress tolerance

Cold stress severely limits plant growth and development, yet its molecular and physiological tolerance mechanisms remain poorly understood (Feng et al. 2025). Cold tolerance in plants is a quantitative trait regulated by multiple genes and signaling pathways, which are regulated by TFs and other signaling pathways (Xu et al. 2020). PGPRs have been shown to alleviate cold stress in plants by inducing antioxidant, hormonal, photosynthetic, and other stress-related pathways (Table 1). They also influence cold-induced gene expression, such as the production of antifreeze proteins, which inhibit ice crystal formation within plant cells (Białoskórska et al. 2024). Additionally, they facilitate the accumulation of osmoprotectants that stabilize cell membranes against freezing (Bhat et al. 2020). In wheat, psychrophilic Bacillus spp. CJCL2, RJGP41, and the temperate B. velezensis FZB42 aid in cold stress tolerance by regulating ABA pathways, lipid peroxidation, and proline accumulation (Zubair et al. 2019). Also, the cold-tolerant Serratia marcescens strain SRM (MTCC 8708), isolated from Cucurbita pepo, markedly enhanced wheat seedling growth under low-temperature conditions (Selvakumar et al. 2008). Inoculation of the endophytic Burkholderia phytofirmans strain PsJN (Bp PsJN) also promoted Arabidopsis growth without altering photosynthetic parameters. Bacterial colonization strengthened mesophyll cell walls and the accumulation of pigments, as well as the reduced expression of RbcL and COR78 (Su et al. 2015). AMF-inoculated plants also exhibit an increased net photosynthesis rate at low temperatures. For instance, Cucumis sativus L. inoculated with Rhizophagus irregularis exhibited improved photosynthetic rates and transpiration rates under cold stress (Ma et al. 2019). AMF-inoculated maize plants also showed higher intercellular CO₂ concentration and stomatal conductance than non-inoculated plants and were protected from cold stress through enhanced chlorophyll synthesis (Li et al. 2020). In Antirrhinum majus under low temperature and weak light, Funneliformis mosseae and Glomus versiforme inoculation improved PSII efficiency, chlorophyll content, and stomatal conductance, while lowering NPQ and intercellular CO₂, resulting in higher biomass and root activity (Li et al. 2023). Similarly, in Arachis hypogaea cv., Funneliformis mosseae enhanced cold tolerance by boosting plant height, biomass, and photosynthetic efficiency, and improved water status (Bi & Zhou 2021).

Toxic metal stress tolerance

Heavy metal toxicity often leads to excessive ROS generation, disturbing redox homeostasis and accelerating plant cellular damage (Sperdouli 2022). Thus, bioremediation plays a significant role in treating toxic metal-contaminated soil. Microorganisms that survive in environments polluted with heavy metals employ various detoxification strategies, including biosorption, bioaccumulation, biotransformation, and biomineralization, which can be harnessed for ex situ or in situ bioremediation (Qattan 2025). Pseudomonas fluorescens (VUPF5, VUPF52) and Bacillus strains (B. cereus PRC95, B. subtilis PRC96) reduce plant damage under toxic metal conditions by improving nutrient uptake (Riseh et al. 2023). Beyond enhancing nutrient uptake, PGPRs help plants tolerate toxic metal stress by boosting antioxidant defenses, stress-related proteins, and producing exopolysaccharides that protect root tissues (Qadir et al. 2023), and stimulate enzymes such as metallothioneins and phytochelatins that bind and sequester metals (Tiwari & Lata 2018). Moreover, PGPRs mitigate metal toxicity through metal transport across membranes, biosorption and bioaccumulation in cell walls, entrapment in extracellular capsules, precipitation of metals, and detoxification via redox reactions (Table 1). Cd-resistant Ochrobactrum and Pb- and As-resistant Bacillus strains possess PGPR traits that support growth and bioremediation in rice (Pandey et al. 2013). Moreover, in Brassica indica, AMF inoculation increased photosynthetic pigment levels under Cd stress (Hashem et al. 2019). This increase is likely due to the extraradical hyphae adsorbing and immobilizing metals, thereby limiting their translocation into plant tissues. Rhizoglomus intraradices and Glomus etunicatum ameliorate the toxic effect of arsenic stress in T. aestivum by increasing the carotenoids, proline, α-tocopherol, cysteine, glutathione, non-protein thiols, and the activity of glutathione-S-transferase that facilitate the sequestration of arsenic into non-toxic complexes (Sharma et al. 2017). In Lolium species and Cicer arietinum, Rhizophagus irregularis mitigated beryllium toxicity by reducing the metal uptake, improving photosynthesis, and reducing oxidative damage, enhancing nitrogen and carbon metabolism (Sheteiwy et al. 2022).

Key genes, including GintABC1, GinZnT1, GmarMT1, and GrosMT1, play a crucial role in maintaining cellular redox balance under toxic metal stress (Yadav et al. 2023). Glomalin-related soil protein, primarily produced by Rhizophagus irregularis, binds heavy metals such as Cu and Al, particularly in acidic soils (Lenoir et al. 2016). Rhizophagus intraradices, Funneliformis coronatum, and Claroideoglomus claroideum consortia enhance Cd tolerance in Paspalum notatum by reprogramming primary metabolism, such as amino acids, organic acids, and trehalose−6-phosphate (Feng et al. 2024). Funneliformis mosseae enhances Cd tolerance in Suaeda salsa by modulating stress-responsive genes coding for osmotic adjustment, such as choline monooxygenase, mechanosensitive ion channels, metal chelation, and membrane stability (phosphoethanolamine N-methyltransferase 3), while downregulating light-harvesting complex genes to limit Cd-induced photodamage and suppression of Ca² channels (Cui et al. 2022).

Light stress tolerance

Plants rely on solar energy for growth through oxygenic photosynthesis; however, both insufficient and excessive light can impair their physiology (Khan et al. 2025). Despite limited studies and evidence available, beneficial bacteria might help plants tolerate light stress through a combination of molecular mechanisms (Villano et al. 2025). Under light stress, microorganisms can enhance plant resilience by modulating phytohormones, such as ABA, protecting plants from photo-oxidative damage, similar to their roles under salt or drought stress (Fadiji et al. 2023). High light exposure may also reshape microbial communities and vice versa, favoring UV-resistant species such as Bacillus coagulans and Clavibacter michiganensis (Villano et al. 2025). Likewise, Methylobacterium thrives under strong UV by producing UVA-absorbing compounds (Yoshida et al. 2017). These microbes improve tolerance to light stress through multiple mechanisms. For instance, Methylobacterium produces UV-absorbing compounds that act as a natural sunscreen for the leaves, protecting them from damage by reducing UV penetration. Recently, Villano et al. (2025) presented a viewpoint on the role of beneficial microbes in mitigating high-light stress; however, a clear understanding of mechanisms remain lacking. Light stress increases ROS production in chloroplasts, which can damage proteins, lipids, and nucleic acids. Certain bacteria, such as Bacillus, Pseudomonas, and Methylobacterium, can enhance plant tolerance by inducing antioxidant defenses, upregulating enzymes such as SOD, CAT, and APX, and modulating phytohormones. Additionally, some phyllosphere bacteria may produce UV-absorbing compounds, such as carotenoids and mycosporine-like amino acids, which directly shield plant tissues. Meanwhile, bacterial signals can activate stress signaling pathways, including MAPK cascades, leading to the expression of light- and stress-responsive genes, such as early light-inducible proteins (Pinto et al. 2011). More mechanistic research investigations are required to fully understand the role of beneficial microbes in mitigating light stress.

Plant–microbe interaction for biotic stress tolerance

Plants face biotic stress from a wide range of parasites, pests, and pathogens (Etesami 2025). Across diverse farming systems, biotic stresses from fungi, bacteria, viruses, nematodes, insects, and weeds (Shameer et al. 2019). For instance, bacterial and fungal parasites cause diseases such as gall, vascular wilts, leaf spots, and cankers (Sobiczewski et al. 2017; Mafakheri et al. 2022). Nematodes damage roots, leading to nutrient deficiency, stunted growth, and wilting (Osman et al. 2020). Viruses also induce both local and systemic symptoms, including chlorosis and stunting (Gao et al. 2025). Mites and insects harm plants through feeding or oviposition and can also transmit pathogens (War et al. 2012) (Fig. 1).

Biotic stresses from fungi, bacteria, viruses, nematodes, insects, and weeds constrain farming systems, reducing yields by 31–42% (Shameer et al. 2019). Bacterial and fungal parasites cause galls, vascular wilts, leaf spots, and cankers (Sobiczewski et al. 2017; Mafakheri et al. 2022). Nematodes inflict root damage, inducing nutrient deficiencies, stunting, and wilting (Osman et al. 2020). Furthermore, viral infections prompt localized or systemic chlorosis and stunting (Gao et al. 2025), while insects and mites cause feeding injuries and transmit pathogens (War et al. 2012) (Fig. 1).

Through long co-evolution with plants, microbes shape plant health and plasticity. Beneficial rhizobacteria, particularly Bacillus spp. and Pseudomonas spp., have emerged as effective biocontrol agents (Table 2). For instance, Pseudomonas stutzeri, Bacillus subtilis, and B. amyloliquefaciens suppress the growth of Phytophthora capsici in cucumber. B. subtilis also controls Penicillium spp. and Rhizopus stolonifer during post-harvest, while B. amyloliquefaciens isolates significantly reduce F. oxysporum under greenhouse conditions (Al-Khayri & Khan 2024). Bacillus subtilis KU21, isolated from Rosmarinus officinalis roots, showed antagonistic activity against F. oxysporum, F. graminearum, and Rhizoctonia solani, where its P-solubilization ability was linked to the gdh gene activity (Sharma et al. 2024). In Chinese cabbage, both individual strains and consortia of PGPR enhance the plant yield and growth by inducing systemic resistance against black rot caused by Xanthomonas campestris pv. campestris (Liu et al. 2016). Studies have identified antimicrobial volatiles, such as sesquiterpenes (Minerdi et al. 2009), methyl 2-methylpentanoate, 1,3,5-trichloro-2-methoxybenzene (Cordovez et al. 2015), 2-methylfuran, 2-furaldehyde, 2-(methythio) benzothiazole, and murolool (Hol et al. 2015), as potential biocontrol agents. Beyond volatiles, chlorinated lipopeptides such as thanamycin and nunapeptin have been shown to suppress Rhizoctonia solani (Mendes et al. 2011). Similarly, conprimycin, a thiopeptide produced by Streptomyces, plays a suppressive role to Fusarium wilt in strawberry (Cha et al. 2016). In Arabidopsis, Bacillus cereus AR156 persuades induced systemic resistance against Pseudomonas syringae pv. tomato infection, which was achieved through salicylic acid–NPR1 signaling pathway. More specifically, leaf infiltration with AR156 activates systemic acquired resistance, expression of PR1 protein, and ROS homeostasis (Niu et al. 2016). Certain bacterial species, such as Pseudomonas and Bacillus, also produce hydrogen cyanide to suppresses root pathogens (Siddiqui et al. 2006). Pseudomonas strains also showed anti-insecticidal effect against Galleria mellonella via hydrogen cyanide activity (Flury et al. 2017). PGPRs also produce lytic enzymes such as proteases, cellulases, and chitinases that disrupt pathogen cell walls. For instance, Stenotrophomonas maltophilia strains W81 and 34S1 exhibit biocontrol activity against Pythium ultimum and summer patch disease through the production of extracellular chitinases and proteases (Kobayashi et al. 2002). Bacillus thuringiensis produces endotoxins, including crystalline δ-endotoxins, during the stationary growth phase, which are toxic to Lepidoptera, Coleoptera, and Diptera insects, as well as mites, nematodes, protozoa, and flukes (Jisha et al. 2013). These toxins are used directly as biopesticides and as genes for developing insect-resistant transgenic plants (Schünemann et al. 2014). Bacillus subtilis (BCB-19) and Bacillus megaterium (SB-9) caused significant larval mortality and growth inhibition in Helicoverpa armigera and Spodoptera litura (Gopalakrishnan et al. 2011). Additionally, B. amyloliquefaciens SF14 and SP10 reduced fruit brown rot disease burden in apple caused by Monilinia fructigena and M. laxa showing a comparable efficacy with the commercial biological control agents in semi-commercial trials (Lahlali et al. 2020).

Table 2.

Beneficial microbes for the control of biotic stress in plants

S. No	Plants species	Beneficial microbes	Biotic stresses	Mode of action	References
1	Arachis hypogaea	P. fluorescens	Sclerotium rolfsii	Improved root length, Production of 2,4 DAPG decreases stem rot	Asadhi et al. 2013
2	Brassica oleracea	Paenibacillus sp.	Xanthomonas campestris	Increased induced-systemic resistance and reduced disease severity	Ghazalibigla et al. 2016
3	Cucumis sativus	B. subtilis, P. fluorescens, and Azotobacter chroococcum	Cucumber mosaic cucumovirus	Higher1,3-glucanase, peroxidase activities, and production of PR protein	El-Borollosy & Oraby 2012
4	Glycine max	Bacillus subtilis BS-2301	Fusarium oxysporum, Phytophthora sojae, Sclerotinia sclerotiorum	Broad-spectrum biocontrol potential against various phytopathogens	Ayaz et al. 2024
5	Hordeum vulgare	P. fluorescens	Fusarium culmorum	Induced systemic resistance and expression of type III plant-peroxidase PR gene	Khan et al. 2006
6	Musa sp.	R. irregularis	R. solanacearum	Decreased bacterial wilt incidence and enhanced root architecture and systemic resistance	Lin et al. 2021
7	Oryza sativa	Bacillus sp. Pseudomonas sp.	Xanthomonas oryzae	Reduced disease with significant increase in growth parameters, polyphenoloxidase, phenylalanine-ammonia lyase, and peroxidase activities	Yasmin et al. 2016
		Bacillus spp. FZB42, NMTD17, and LLTC93	Rhizoctonia solani and Xanthomonas oryzae pv. oryzae	Controlled disease by regulating plant defense genes and enzymes	Ali et al. 2023b
8	Phyllanthus amarus	Bacillus, Brevibacillus, Lysinibacillus, Paenibacillus, Terribacillu,s and Jeotgalibacillus	Corynespora cassiicola	Increased ACC deaminase activity and chitinase enzyme production	Kadyan et al. 2013
9	Solanum lycopersicum	Bacillus atrophaeus	Meloidogyne incognita	VOCs significantly controlled the plant parasitic nematode and reduced the root galls of nematodes	Ayaz et al. 2021
10	Solanum tuberosum	Bacillus spp.	Pectobacterium carotovorum	Control disease and increase the storage time	Abd-El-Khair et al. 2021
11	Triticum aestivum	Bacillus subtilis ATCC6633	F. graminearum and F. verticillioides	Suppressed disease burden and reduced mycotoxin production	Yu et al. 2021
		Bacillus sp. s6, Pseudomonas sp.6 K	Aphid	Decreases aphid population and increases the number of spikelets, plant height, straw yield, grain yield, and productive tillers	Naeem et al. 2018
12	Zea mays	Pseudomonas sp. and Bacillus sp.	Macrophomina phaseolina, F. moniliforme, and F. graminearum	Siderophore production inhibits fungal growth	Pal et al. 2001

AMF help plants to build resistance against pathogens by competing for nutrients, inducing plant defense responses, modulating root exudates, strengthening structure through thicker cell walls, increased lignin and callose accumulation, and a reinforced cuticle, and possess direct antimicrobial activity through secondary metabolites, including flavonoids, terpenoids, and alkaloids (Zhao et al. 2022; Umer et al. 2025). AMF enhance plant disease resistance by activating induced systemic resistance that triggers the accumulation of pathogenesis-related proteins and antimicrobial antioxidant enzymes against necrotrophic and biotrophic pathogens (Upadhyay et al. 2025). For instance, colonization of R. irregularis in S. lycopersicum resulted in reduced susceptibility to F. oxysporum through the induction of systemic resistance, lignin deposition, and callose accumulation in roots, thereby strengthening its structural defense system (Wang et al. 2022a, b). The activation of induced systemic resistance triggers the production of volatile organic compounds, such as terpenes, green leaf volatiles, and methyl jasmonate, which inhibit pathogen growth and repel herbivores. Moreover, it acts as an airborne signal to host defense and primes neighboring plants for enhanced pathogen defenses (Sarkar & Sadhukhan 2023). Trichoderma controls soil-borne nematodes and fungal diseases, as well as leaf and panicle diseases of various plants, through multiple mechanisms, including parasitism, antagonism, antibiosis, competition, and inducing systemic resistance in plants. It also enhances nutrient use efficiency, plant growth, and reduces agrochemical pollution (Yao et al. 2023).

Plant–microbe communication networks

The plant–microbe communication network relies on inter and intra-kingdom chemical signaling, involving biosynthesis, transport, perception, and induction of physiological responses. Due to the high evolutionary and functional diversity of plants and microbes, signaling requires specificity to effectively reach its target (Venturi & Keel 2016). Bacteria perceive and transmit extracellular chemical signals through cascades of cytosolic response regulators that drive physiological responses and most response regulators have DNA-binding domains, while others exhibit enzymatic activity, regulate c-di-GMP, or interact directly with RNA or proteins (Tadrosova et al. 2025). Plants sense various innate and exogenous molecules through pattern recognition receptors (PRRs), and signals arise when microbial molecules interact with the extracellular ligand-binding domains of PRRs (Zipfel 2008). Primarily, plant–microbe communication is driven by root exudates, QS molecules, and phytohormones, which trigger molecular signaling cascades (Fig. 2).

Fig. 2.

Schematic representation of the mechanism of plant–microbe communication networks and molecular and biochemical dialogues mediating plant growth and stress resilience. The intricate plant–microbe communication fosters stress tolerance and soil stability through dynamic signaling pathways and molecular exchanges. Under stress conditions, microbes perceive and respond by secreting stress and microbe-associated molecular patterns, which trigger the downstream response pathways and are recognized by plant PRRs, including receptor-like kinases and proteins. Such recognition activates downstream signaling cascades, primarily MAPK pathways, Ca2+ fluxes, and ROS generation, which act as secondary messengers to regulate transcriptional and hormonal responses. Non-coding RNAs mediate the bi-directional regulatory loop between plants and microbes and fine-tune signaling specificity. In parallell, microbial secreted bio-chemicals such as VOCs, phytohormones, secondary metabolites, QS molecules, and exopolysaccharides enhance plant physiological responses and improve soil structure and stability. These molecular signals and responses lead to gene expression reprogramming and epigenetic modifications. Plant roots secrete secondary metabolites, such as flavonoids, which serve as cues for microbial recruitment and communication. Flavonoids activate node genes and facilitate nodule formation and nitrogen fixation in plant roots. Root exudates containing tryptophan stimulate microbial biosynthesis of IAA, which is crucial for improving root architecture, siderophore production, soil health, and overall plant health. Moreover, microbial phytohormones and signaling molecules, such as TIR1/AFB-IAA-ARF node, improves root architecture, mediate the regulation of stress-responsive genes and molecular pathways in plants, leading them to resilience. This bi-directional communication network and synergistic interaction between plants and microbes establishes and governs a molecular feedback loop for nutrient and water absorption, soil fertility, root development and architectural modification, plant health, and ROS homeostasis for stress tolerance

Root exudates as chemical signals

Plants release about 11–40% of their photosynthetic products into the rhizosphere as root exudates (Yusuf et al. 2025). Plant roots and microbiome communication involve a complex process that encompasses chemical, molecular, and physical interactions. It is largely regulated by root exudates and metabolites, including sloughed tissues and cells, H⁺ efflux, CO₂, mucilage, border cells, and proteins (Richter et al. 2024). PGPRs sense and utilize root exudates, which are rich in sugars, amino acids, organic acids, and secondary metabolites, as chemical signals to colonize the rhizosphere and activate plant stress responses. These serve as energy sources and signaling molecules that influence microbial activity. Sugars secreted by roots, such as sucrose, support the colonization of beneficial Gram-positive bacteria, like Bacillus, by activating signaling pathways that enhance motility and biofilm formation (Richter et al. 2024). Glucose also acts as a chemoattractant for fungi and supports bacterial colonization in plants (Pantigoso et al. 2022). Similarly, organic acids and sugars from tomato root exudates enhanced tomato growth and antifungal activity of Pseudomonas spp. (Kravchenko et al. 2003). Sugar alcohols, such as inositol, stimulate bacterial chemotaxis, growth, biofilm formation, and siderophore production (Richter et al. 2024). Flavonoids influence microbiome composition in Arabidopsis, rice, and maize, while promoting nitrogen fixation by stimulating beneficial microbes (Wang et al. 2024b). Cucumber root exudates attract B. amyloliquefaciens SQR9 (Liu et al. 2014), while fumaric acid from banana roots attracts B. subtilis N11 and promotes bacterial biofilm formation (Zhang et al. 2014). Moreover, certain VOCs, such as terpenes, released during pathogen attack, play a pathogen-suppressive role while attracting beneficial microbes (Luo et al. 2024). Other secondary metabolites, including camalexin and benzoxazinoids, strengthen pathogen defense and enrich microbial diversity in the soil (Xu et al. 2023).

Pants and microbes exchange signals, and the symbiosis begins with plant-produced flavonoids (2-phenyl-1,4-benzopyrone derivatives) that activate rhizobial nod genes. These genes encode lipo-chito oligosaccharides (LCOs or Nod factors), which act as secondary signals to initiate nodule formation (Fig. 2). Similarly, root exudates induce Myc signals in AMF, facilitating nutrient exchange where the fungus enhances root access to soil nutrients, especially phosphate, while the plant supplies carbohydrates (Oldroyd 2013). Plants also secrete strigolactones and cutin monomers as primary signals for AMF symbiosis, which can also be recognized by pathogens. In response, mycorrhizal fungi release mutualistic effectors, such as small secreted proteins (SSPs) that modulate host hormonal signaling and promote mycorrhization. For example, the ectomycorrhizal fungus Laccaria bicolor releases MiSSP7 during root interaction (Plett & Martin 2015). Moreover, ascaroside pheromones, signaling molecules produced by plant-parasitic nematodes, can induce the expression of defense genes and enhance resistance to bacterial infections in various plants (Manosalva et al. 2015). Root exudates also contain low-carbon molecules that serve as precursors for PGPR-derived phytohormones; for example, tryptophan, abundant in root tips, is a key precursor of IAA (Haichar et al. 2014) (Fig. 2).

Production of phytohormones

Certain bacteria secrete phytohormones such as cytokinins, auxins, and gibberellins, which enhance plant growth and stress resilience. These hormones regulate seed germination, organ development, and expansion by promoting cell elongation, division, and differentiation. Some genera of PGPRs produce IAA, including: Acetobacter, Acinetobacter, Azospirillum, Arthrobacter, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Herbaspirillum, Klebsiella, Mesorhizobium, Paenibacillus, Pantoea, Pseudomonas, Rhizobium, Rhodococcus, Serratia, Strenotophomonas, Streptomyces, and Rouxiella (Keswani et al. 2022; Oubaha et al. 2024). Microbial IAA influences plant root architecture, leading to increased root hair development and lateral root formation, which enhances the plant's ability to absorb nutrients and water from the soil (Etesami & Glick 2024). IAA interacts with auxin signaling pathways through the TIR1/AFB–IAA–ARF module, activating stress-responsive genes and remodeling root architecture (Liu et al. 2024) (Fig. 2). PGPR strains, including B. pumilus, B. licheniformis, Acetobacter sp., Bacillus sp., and Azospirillum sp., also produce gibberellin (Bottini et al. 2004) that promote plant growth and stress recovery by modulating the GA–DELLA signaling pathway, where GA perception leads to DELLA degradation, thus releasing growth-promoting TFs (Hedden & Sponsel 2015). Root development-promoting PGPRs such as Arthrobacter, Bacillus, Azospirillum, and Pseudomonas produce cytokinin (Naz et al. 2009). Cytokinin-producing bacteria regulate shoot–root signaling, delay senescence, and maintain photosynthetic activity in plants under stress conditions. Such cytokinin signaling is mediated by histidine kinase receptors and type-B response regulators (Gujjar & Supaibulwatana 2019). Similarly, Actinobacteria produce cytokinins, IAA, and glycine betaine-like compounds (Shutsrirung et al. 2013), which alleviate stress in various crops, including wheat (Singh & Jha 2016), maize (Mishra et al. 2017), chickpea (Zaheer et al. 2016), and A. thaliana (Contreras-Cornejo et al. 2009). ABA production has also been reported in rhizobacteria, including Proteus mirabilis, Klebsiella pneumoniae, Phaseolus vulgaris isolates, B. megaterium, and B. cereus (Karadeniz et al. 2006). Ethylene, ABA, and other phytohormones mediate several plant stress response pathways in plants (Verbon & Liberman 2016). Several microbes alter the ABA levels in the rhizosphere, either by producing ABA themselves or influencing the plant’s ABA biosynthesis process, which regulates stomatal function, osmotic adjustment, and ROS homeostasis under stress conditions, such as drought and heat. This is regulated by ABA-dependent signaling cascades involving PYR/PYL receptors, SnRK2 kinases, and PP2C phosphatases (Li et al. 2022). PGPRs also regulate ethylene signaling through ACC deaminase, a mechanism that involves lowering ethylene levels and preventing premature senescence (Mulugeta et al. 2025). This modulation influences the ethylene signaling pathway (ETR–CTR1–EIN2–EIN3), thereby sustaining plant growth during abiotic stress (Riyazuddin et al. 2020; Fortt et al. 2022).

Quorum sensing and microbial signaling molecules

Quorum sensing (QS) mediates inter- and intra-species signaling in the rhizosphere, allowing microbial communities to synchronize and develop their behavior through this communication signal. In Gram-negative bacteria, N-acyl homoserine lactones (AHLs) are the primary QS signals, which have been shown to modulate root growth, systemic resistance, and gene expression in plants. Many rhizosphere-associated proteobacteria, including Burkholderia, Pseudomonas spp., Ochrobacterum, Erwinia, Ralstonia, Serratia, and others, produce and respond to AHLs (Imran et al. 2014; Li et al. 2015). Other Gram-negative bacteria, such as Stenotrophomonas maltophilia and Burkholderia spp., also produce diffusible signal factors, including cis-2 unsaturated fatty acids, as QS molecules (Ryan et al. 2015). Fungal and bacterial communication is evident through the production of QS molecules by fungi, such as farnesol, tyrosol, γ-heptalactone, γ-butyrolactone, and dodecanol (Hartmann & Schikora 2012; Barriuso 2015). Oomycetes, in particular, release alcohol-based signals that are associated with plant developmental processes (Leeder et al. 2011). Such fungal–bacterial QS interactions serve as evolutionary strategies to outcompete neighbors for host colonization and space. Beyond microbial communication and signal exchange, QS regulates plant growth, nutrient uptake, and stress resilience through coordinated production of phytohormones, biofilms, and stress-responsive metabolites, as well as ROS homeostasis (Jung et al. 2020).

Molecular mechanisms of the plant–microbe interaction for stress tolerance

Plant–microbe interactions represent a fundamental component of plant adaptation to environmental stress, particularly under climate change-driven conditions where plants frequently encounter multiple stresses. Microbial communities associated with plant roots and tissues influence plant physiology, immunity, and stress resilience through complex molecular mechanisms. These interactions involve a dynamic exchange of signals that enable plants to perceive microbial partners and integrate microbial cues with endogenous stress-response pathways (Srivastava et al. 2025; Wankhade et al. 2025; Yusuf et al. 2025). Under combinatorial stresses, plant signaling networks that normally regulate immunity and abiotic stress tolerance become highly interconnected. The plant microbiome acts as a regulatory interface, modulating these pathways to allow plants to balance growth, immunity, and stress adaptation.

The initiation of plant–microbe interactions begins with host recognition mediated by molecular pattern recognition systems (Cheng et al. 2019). Plants perceive microbe-associated molecular patterns (MAMPs) such as flagellin (flg22), lipopolysaccharides, and chitin fragments through pattern recognition receptors (PRRs), including receptor-like kinases and receptor-like proteins (Monaghan & Zipfel 2012). Activation of these receptors trigger immune signaling cascades that involve calcium influx, ROS bursts, and MAPK activation (Cheng et al. 2019). However, under abiotic stress conditions, these signaling pathways are frequently altered. For example, drought or heat stress can shift the balance between immune signaling and stress-response pathways by modifying ROS homeostasis and hormonal regulation. Beneficial microbes intervene in these signaling nodes by modulating ROS-scavenging systems, hormone balance, and transcriptional networks, thereby preventing excessive defense activation while maintaining stress tolerance.

In mutualistic associations with AMF and PGPRs, plants recognize symbiotic molecules such as lipochitooligosaccharides (LCOs or Nod factors), which activate symbiosis-specific signaling pathways partially overlapping with immune networks (Qian et al. 2025). Environmental stresses modify these interactions by altering root-exudate composition and microbial recruitment. Under drought or salinity stress, plants release higher concentrations of organic acids, sugars, and secondary metabolites, thereby selectively recruiting stress-adapted microbial taxa. These microbes respond by producing signaling molecules, including VOCs, phytohormones, secondary metabolites, quorum-sensing signals, and exopolysaccharides that influence plant physiology and defense responses (Sharma et al. 2023; Wankhade et al. 2025). Through these signals, microbial communities reshape plant signaling pathways and help coordinate responses to multiple stressors (Fig. 2).

A major point of microbiome intervention occurs at central signaling hubs such as MAPK cascades, calcium signaling pathways, and ROS regulatory networks (Zhang & Zhang 2022). These hubs integrate both microbial signals and stress cues (Fig. 2). Microbial inoculation has also been shown to induce the expression of heat shock proteins, antioxidant genes, and dehydration-responsive transcription factors, illustrating how microbial signals converge with plant stress signaling networks to stabilize cellular homeostasis during combined stresses. Microbiome-mediated intervention also occurs through transcriptional regulation of canonical stress-response pathways. For example, microbial inoculation has been shown to enhance the expression of RD29A and RD29B, key drought-responsive genes associated with dehydration tolerance. Similarly, microbes can activate MAPK-related signaling components and genes involved in sugar transport, stress metabolism, and ROS detoxification, demonstrating that microbial symbiosis amplifies endogenous plant stress signaling. Moreover, microbial partners modulate ion homeostasis pathways by regulating genes associated with the SOS pathway and Na⁺/H⁺ antiporters, thereby improving Na⁺ extrusion and vacuolar sequestration of toxic ions. AMF additionally regulates aquaporin gene expression, improving water transport across membranes and maintaining cellular hydration during osmotic stress.

Recent evidence also highlights epigenetic and post-transcriptional mechanisms as emerging layers of microbiome-mediated stress adaptation. Microbial signals can influence DNA methylation patterns, chromatin structure, and the activity of regulatory noncoding RNAs that control stress-responsive genes (Wu & Fan 2025). These epigenetic modifications contribute to stress priming and memory, allowing plants previously associated with beneficial microbes to respond more rapidly and efficiently to recurring environmental stresses such as drought or heat waves. Overall, plant–microbe interactions under climate-driven environmental stress operate through multilayered molecular mechanisms that integrate immune signaling, hormone regulation, transcriptional reprogramming, and epigenetic control (Fig. 2).

OMICs approaches in studying plant–microbe-stress interactions

Studying plant–microbe interaction at the molecular level is challenging, but recent advances have positioned OMICs technologies as powerful tools (Sharma et al. 2022). By integrating multiple techniques, OMICs provides a systems-level understanding of biological complexity and generates valuable data on gene, protein, and metabolite variation to disentangle the mechanisms by which plants and microbes are associated either in partnership or as antagonists (Fig. 3).

Fig. 3.

Advances in microbiome studies supported with OMICS analysis and microbial engineering for sustainable and resilient agriculture. The potent candidate beneficial rhizobacteria could enhance plant performance under both control and stressed conditions via improving nutrient absorption, heavy metal absorption, and polycyclic aromatic hydrocarbons removal from polluted environments, phosphate solubilization, organic matter decomposition, nitrogen fixation, acting against pathobiome, and others. (a) Exploration and microbial and plant sample collection, (b, c) characterization and in vitro testing of potential microbes, (d) application of integrated OMICs for ideal candidate molecular profile and role in plant growth, development, and stress resilience, (e, f) mapping and selection of candidate genes and molecular pathways and engineering of microbes for better efficiency, (g) followed by detailed analysis and characterization supported with multi-OMICs approaches. Following the biosafety protocols, (h) the engineered microbe will be tested for in vitro and confined field conditions and, on passing rigorous trials, (i) it can help to enhance crop productivity and stress tolerance or (j) bioinoculants can be formulated from it and used in sustainable agriculture

Advances in genomics and next-generation sequencing (NGS) have enabled rapid whole-genome sequencing, de novo assemblies, and strain resequencing, and facilitate an understanding of how plants adapt to diverse biotic interactions beyond symbiosis (Chiquito-Contreras et al. 2024). Metagenomics studies reveal the diversity and functional potential of microbial communities in maintaining plant health in the face of global climate change scenarios. Advances from Sanger sequencing to NGS, including 16S rRNA and shotgun sequencing, have enabled the discovery of novel genes in plant–microbe interaction studies for crop improvement and stress resilience (Regalado et al. 2020). Epigenomics complements this by examining the heritable changes in gene expression that are independent of the underlying DNA sequence, providing insight into plant–microbe interactions, environmental adaptation, and transgenerational effects (Ali et al. 2022a).

Transcriptome analyses have revealed key genes involved in plant–microbe interactions, encompassing both mutualism and pathogenicity, and offered a deeper insight into the molecular understanding of the symbiosis. Using NGS, transcriptomics quantifies RNA molecules and links gene functions under specific conditions through methods like microarrays, SOLiD-SAGE, and RNA-seq (Chen et al. 2022). It detects regulatory changes, mutations, variants, differential gene expression, and alternative splicing events at a fine, deeper level. It allows for the analysis of the entire microbial communities using metatranscriptomics, and identifies differentially expressed genes, clarifies microbial physiology, and supports functional analysis of plant-associated microbiomes (Chen et al. 2022).

Plants synthesize a vast diversity of metabolites, each species having a unique metabolic profile (Saleem et al. 2025). Combining metagenomics and metabolomics can help to understand the soil microbial composition, functions, and their role in plant nutrient uptake and utilization and stress response (Varadharajan et al. 2025). Metabolomics has pointedly deepened the understanding of the genetic and biochemical foundations of plant and microbial traits that influence crop quality and productivity (Saleem et al. 2025).

During plant–microbe interactions, proteins play a crucial role in maintaining cellular homeostasis, signaling, and responding to stress. Proteomic analysis provides key insights into these processes, especially in unculturable microbes (Jain et al. 2024). Unlike traditional approaches, metaproteomics captures the protein diversity and abundance across entire microbial communities, providing a broader understanding of the mechanistic functions of microbial communities (Rane et al. 2022). Advanced methods such as mass spectrometry and chromatography are widely used to identify proteins and profile plant–microbe interactions.

Utilizing the OMICs data, engineering the rhizosphere microbiome has recently emerged as a strategy to increase crop production, advancing plant–microbiome interaction research by a step (Patyal et al. 2025). Synthetic biology also provides powerful tools for microbial engineering and optimizing plant–microbe interactions, enabling climate-smart farming and enhanced stress resilience. By designing microbial consortia, modifying targeted metabolic pathways, and introducing synthetic gene circuits, beneficial microbes can be tailored to enhance nutrient acquisition, modulate phytohormone signaling, and strengthen plant immunity under abiotic and biotic stresses (Fig. 3). Engineered microbes with traits such as nitrogen fixation, phosphorus solubilization, or stress-responsive metabolite production can reduce reliance on chemical inputs (Patyal et al. 2025). Thus, synthetic biology enables precise manipulation of plant genes involved in microbial recognition and signaling, fostering more efficient symbiosis for sustainable crop production in the face of climate change (Yang et al. 2025a; Zhang et al. 2025a). Engineering beneficial microbes with traits such as nutrient cycling, organic matter decomposition, stress tolerance, and disease resistance remains a major challenge, yet the regulatory guidelines are scarce in many countries (Orozco-Mosqueda et al. 2022).

Magnifying the role of microbiome for sustainable agriculture using AI and big data

The potential of microbes to reduce dependence on agrochemicals, maintain soil health, and improve crop productivity makes the plant microbiome a cornerstone of sustainable agriculture (Sawant et al. 2025). However, the immense diversity and dynamic structure of microbial communities, shaped by soil physicochemical properties, plant genotype, climatic conditions, and agricultural management practices, pose major challenges for their predictable and practical application. Recent advances in high-throughput sequencing and integrated multi-OMICS approaches have generated large datasets describing microbial diversity, gene expression, metabolite profiles, and ecological functions within agricultural systems. While these datasets offer unprecedented insight into plan-microbiome interactions, their complexity requires sophisticated computational tools to extract biologically meaningful patterns. Artificial intelligence (AI) and big data analytics have therefore emerged as transformative approaches for decoding microbiome complexity and translating microbial functions into actionable agricultural strategies (Zhang et al. 2025a).

Recent developments in computational biology demonstrate how machine learning and deep learning frameworks can predict microbiome behavior and plant performance under diverse environmental conditions. AI models are increasingly used to integrate multidimensional datasets including metagenomic profiles, environmental variables, crop phenotypes, and soil properties to identify microbial taxa or functional genes associated with nutrient acquisition, pathogen resistance, or abiotic stress tolerance (Fig. 4). For example, supervised learning approaches such as random forest and gradient boosting models have been applied to predict plant health outcomes from microbiome composition and environmental parameters, enabling the identification of microbial biomarkers linked to disease suppression or improved nutrient cycling (Deng et al. 2021; Zhao et al. 2023; Ma et al. 2026). Microbiome-informed models were used to enhance sustainable pathogen management (Buttrós et al. 2025).

Fig. 4.

Conceptual framework illustrating the application of AI and big data analysis for isolation, characterization, and validation of potent microbial strains for sustainable soil health and crop productivity; (a) isolation and identification of microbes form the rhizosphere and detailed analysis of potential beneficial microbes for plant growth and productivity, supported by (b) AI and big data algorithms and (c) soil parameter analysis and AI-assisted prediction (d) in the field condition with real-time monitoring and (e) multi-OMICS analysis. After sufficient data is collected, potent microbes will be chosen, validated, and recruited (f) for the development of low-cost and environmentally sustainable bioinoculants for application in sustainable agriculture

More recent studies employ deep neural networks and network-based inference models to reconstruct microbial interaction networks, allowing researchers to predict how microbial communities respond to changes in management practices, climate variability, or host genotype (Pace et al. 2025). AI has also accelerated progress in the design of synthetic microbial consortia, a key frontier in microbiome engineering for agriculture (Folorunso et al. 2026). Computational models can simulate metabolic exchanges and ecological interactions among microbial taxa to identify compatible microbial combinations that promote plant growth or stress resilience. Using genome-scale metabolic modeling, machine learning algorithms can predict cooperative or competitive relationships among microbes and forecast the stability of synthetic communities under specific environmental conditions. Such approaches allow researchers to rationally design microbial consortia tailored to particular crops, soil types, or climatic stresses, thereby enhancing soil fertility, nutrient uptake efficiency, and stress tolerance while reducing dependence on chemical fertilizers and pesticides (Zhao et al. 2023; Patyal et al. 2025). In addition, AI-driven optimization algorithms can iteratively refine microbial community compositions based on experimental feedback, enabling adaptive engineering of plant-beneficial microbiomes. Case studies using synthetic microbial communities (SynComs) in A. thaliana have demonstrated the reversal of dysbiosis, stabilization of microbial networks, and restoration of plant fitness through modulation of host immune responses and secondary metabolite production (Cheng et al. 2024). Disease-suppression research further indicates that SynComs can enhance plant health and reduce pathogen pressure in crop systems (Martins et al. 2023). Similarly, synthetic communities have been reported to stimulate growth and restructure rhizosphere microbial communities in pepper (You et al. 2025) and to enhance growth and stress resilience in field-grown sorghum (Fonseca-García et al. 2024), highlighting their broader potential for improving plant growth and productivity.

Another emerging frontier involves integrating microbiome data with precision agriculture technologies to enable real-time monitoring and management of crop systems. Remote sensing platforms, satellite imagery, and Internet of Things (IoT) sensors continuously collect data on soil moisture, temperature, crop growth, and environmental conditions. When combined with microbiome sequencing data, these datasets allow AI models to generate predictive insights about how microbial community dynamics influence crop performance across spatial and temporal scales. Consequently, farmers can receive data-driven recommendations for irrigation, fertilization, or disease management tailored to specific field conditions and crop growth stages (Mansoor et al. 2025). Such integrative frameworks represent a shift toward microbiome-informed precision agriculture, where microbial ecology becomes an active component of farm management strategies.

Despite these promising developments, several critical knowledge gaps and translational challenges remain in the widespread adoption of AI-driven microbiome technologies in agriculture. Microbiome datasets are highly heterogeneous and often generated using diverse sequencing platforms, experimental designs, and analytical pipelines, complicating data integration and cross-study comparisons. Consequently, understanding how microbial communities assemble, persist, and function under real field conditions remains a major research priority. Thus, the development of standardized data formats, interoperable databases, and reproducible analytical workflows is essential for enabling large-scale meta-analyses and improving the generalizability of AI models. Another limitation is that many machine learning models identify correlations rather than causal relationships between microbial communities and plant phenotypes, underscoring the need for rigorous experimental validation in controlled and field environments to develop reliable microbiome-based agricultural technologies. Additionally, adoption of advanced digital agriculture technologies remains challenging for smallholder farmers, particularly in developing regions where infrastructure, financial resources, and digital literacy may be limited (Vélez & Álvarez 2024; Hussein et al. 2025). Addressing these barriers requires equitable access to digital tools, targeted capacity-building initiatives, and participatory research frameworks involving farmers, extension professionals, policymakers, and researchers. Developing low-cost diagnostic technologies, standardized microbiome datasets, and user-friendly decision-support platforms that translate complex microbial information into practical farm management recommendations will be critical to translating AI-enabled microbiome insights into scalable agricultural solutions. Thus, by bridging the gap between microbiome discovery and field-level application, these integrative approaches could ultimately enable the development of resilient, microbiome-informed agricultural systems that support global food security while minimizing environmental impacts.

Trends and future perspectives

In the face of intensifying climate change, leveraging plant–microbe interactions offers a promising route for sustainable agriculture. Future research will focus on the design and large-scale application of microbial consortia and bioinoculants to enhance stress tolerance, nutrient and water use efficiency, and soil health. However, scaling microbiome-based solutions requires strict adherence to biosafety principles, risk assessment, and compliance with international and national regulations. Harmonizing plant–microbe innovations with biosafety frameworks and proper working principles will be crucial to ensuring environmental sustainability and safety. Integrating efficient and effective microbiome applications with regulatory guidelines will accelerate the transition toward climate-smart, sustainable, and safe agricultural systems that help achieve the goals of zero hunger and food for all.

Author contributions

TAG: conceptualization, data curation, validation, writing—original draft, writing—review and editing, prepared figures and table, resources. AYD: data curation, validation, writing—review and editing, resources. BA: data curation, validation, writing—review and editing. DM: data curation, validation, writing—review and editing. TGB: data curation, validation, writing—review and editing. BO: data curation, validation, writing—review and editing. ID: data curation, validation, writing—review and editing, investigation. FY: data curation, validation, writing—review and editing, investigation. NSM: data curation, validation, writing—review and editing, investigation.

Funding

The author(s) declare that no financial support was received for the creation and/or publication of this article.

Declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Declarations of generative AI

The authors declare that Grammarly (AI) was used for grammatical correction purposes.