Root exudates play a pivotal role in shaping the rhizosphere microbiome, functioning as biochemical signals that mediate communication between plants and microorganisms (Figueroa-López et al., 2016; Berg et al., 2020; Poupin et al., 2023; Hacquard and Martin, 2024). These exudates comprise a diverse range of compounds, including sugars, amino acids, organic acids, and secondary metabolites, each serving a specific function in plant–microbe interactions. Studies have shown that root exudates serve as crucial signaling molecules, influencing microbial community composition and functionality by attracting beneficial microbes and deterring pathogens (Solomon and Janda, 2024a). Plants strategically release specific exudates to attract beneficial microorganisms such as nitrogen-fixing bacteria and mycorrhizal fungi, which enhance nutrient acquisition. For instance, legumes release flavonoids that attract nitrogen-fixing bacteria, thereby improving nitrogen availability for plant growth (Tian et al., 2010; Jacoby et al., 2020a; Marín et al., 2021; Chen and Liu, 2024; Wang et al., 2015). Beyond nutrient acquisition, root exudates are critical for pathogen defense and stress tolerance. Under stress conditions such as drought or salinity, plants release targeted exudates that recruit microbes with stress-alleviating properties. These microbes assist plants by improving water uptake, tolerating salinity, or producing growth-promoting hormones (Cao et al., 2024; El-Saadony et al., 2024).

Moreover, root exudates play a significant role in plant growth and development. They influence root architecture by promoting root branching, which increases the surface area available for nutrient and water uptake. Root exudates can also stimulate rhizosphere microbes capable of degrading pollutants, thereby contributing to soil bioremediation (Barreiro and Dί́az-Raviña, 2021; Saeed et al., 2021). Figure 1 illustrates the multifaceted roles of root exudates in plant–microorganism interactions, highlighting their importance in nutrient acquisition, stress mitigation, and soil health. The chemical composition of root exudates is highly complex and varies depending on plant species, developmental stages, and environmental conditions. The interaction between exudates and the diverse microbial community in the rhizosphere creates a dynamic system (Kumar and Pandey, 2013; Stringlis et al., 2018a; Lombardo et al., 2024). Understanding these interactions offers promising possibilities for sustainable agriculture, allowing for the manipulation of root exudates to enhance nutrient acquisition, improve stress tolerance, and boost plant defenses (Haney, 2021a). As research into the rhizosphere’s chemical language progresses, we gain insights into how plant–microbe interactions can improve crop productivity, soil health, and environmental sustainability (Pantigoso et al., 2022b).

Root exudates not only are important for attracting beneficial microbes but also play a role in regulating microbial populations. They can either attract or repel specific microorganisms, influencing the composition and behavior of the rhizosphere microbiome (Letters, 2014; Hardoim et al., 2015a; Rendueles and Ghigo, 2015; Teixeira et al., 2019; Siddique et al., 2022). For example, sucrose, a disaccharide secreted by plant roots, is involved in the colonization of beneficial gram-positive bacteria, such as Bacillus strains. This sugar triggers signaling pathways that enhance bacterial motility and biofilm formation, facilitating root colonization (Richter et al., 2023). Additionally, glucose, a chemoattractant for many fungal strains, also plays a role in bacterial colonization in the maize rhizosphere (Barrera-Galicia et al., 2021; Pantigoso et al., 2022b). Other sugar alcohols, like inositol, promote bacterial growth and processes such as chemotaxis, biofilm formation, and siderophore production (Hardoim et al., 2015a; Siddique et al., 2022; Richter et al., 2023). Flavonoids play an essential role in plant interactions with nitrogen-fixing bacteria. These compounds are structurally diverse and influence the composition of the microbiome in crops like Arabidopsis, rice, and maize. Flavonoids promote the growth of beneficial microbes and contribute to biological nitrogen fixation by encouraging the growth of Gluconacetobacter diazotrophicus (Liu et al., 2014; Wang X. et al., 2024). Phenolic compounds released by plants act as both defense mechanisms against pathogens and carbon sources for microbes. Coumarins, a type of phenolic secondary metabolite, show selective antimicrobial effects and can inhibit the growth of soil-borne pathogens while promoting beneficial microbes (Rosier et al., 2016; Xu and Dodd, 2022). Moreover, root volatiles [volatile organic compounds (VOCs)] are crucial for long-distance interactions in the soil. These compounds serve as signaling molecules or energy sources for microbes. The composition and concentration of VOCs can vary depending on microbial presence, influencing bacterial growth and competition (Marín et al., 2021). Some VOCs, such as terpenes, increase during pathogen infection, inhibiting pathogen growth while attracting beneficial microbes. Under nutrient limitation, VOCs can serve as info-chemicals, providing cues to beneficial bacteria in the rhizosphere (Stringlis et al., 2018a; Lombardo et al., 2024; Luo et al., 2024). Secondary metabolites like camalexin and benzoxazinoids, which are found in root exudates, help defend plants against pathogens and enrich the soil microbial community (Richter et al., 2023; Xu and Wang, 2023).

Root exudates are essential components in the chemical communication between plants and the rhizosphere microbiome (Zhang et al., 2023). These compounds act as energy sources, nutritional provisions, and signaling molecules that influence microbial activity (Chowdhury et al., 2011). The composition and quantity of root exudates vary with environmental conditions and plant growth stages, helping plants adapt to changes in nutrient availability, water stress, and pathogen presence. For instance, plants under nutrient stress may release organic acids to acquire scarce nutrients, while drought stress triggers the release of specific exudates to recruit microbes that aid in water retention and stress mitigation (Haney, 2021a; Pantigoso et al., 2022b; Richter et al., 2023).

Root exudates play a crucial role in shaping the rhizosphere, with their abundance and composition influenced by a variety of biotic and abiotic factors. Plant species and their genetic makeup are key determinants, as different species release distinct exudates to interact with specific microbes in the soil. For example, legumes release flavonoids to attract nitrogen-fixing bacteria, while grasses exude compounds that promote mycorrhizal fungal growth (Solomon and Janda, 2024a). Within a species, varieties and cultivars can also show variation in exudate profiles, impacting microbial interactions (Saeed et al., 2021). The developmental stage of the plant is another important factor. Seedlings generally release more sugars to support their rapid growth, while mature plants may shift to producing organic acids or secondary metabolites for nutrient acquisition and defense against pathogens (Teixeira et al., 2019). Environmental conditions, such as nutrient availability, water stress, and temperature, significantly affect exudate production. For example, nutrient-deficient plants may secrete more organic acids to enhance nutrient uptake, while drought-stressed plants may release specific exudates that attract microbes capable of mitigating water stress (Boot et al., 2013; Rosier et al., 2016; Canarini et al., 2017; Wu et al., 2022). Additionally, the presence of pathogens or beneficial microbes can trigger the release of specific compounds; pathogens may prompt the production of antimicrobial secondary metabolites, while beneficial microbes may stimulate exudates that enhance their growth (Ma et al., 2023). Environmental stressors like biotic (e.g., pathogen attack) and abiotic stress (e.g., soil salinity and drought) also shape the exudate composition, as plants release metabolites to counteract these challenges (Al-Khayri et al., 2023). Root system structure and age influence exudate dynamics, with plants of different root architectures potentially releasing different profiles of exudates and older roots typically releasing fewer exudates than younger ones (Ecevit et al., 2022). Soil characteristics, such as soil type and pH, also play a role in determining exudate composition, with plants in acidic soils potentially releasing more organic acids to solubilize nutrients (Hallama, 2019). Moreover, the microbial community in the rhizosphere can influence the exudate profile, as beneficial microbes may stimulate plants to release exudates that encourage their colonization, while pathogens may prompt defense-related exudates (60). Ultimately, the composition and quantity of root exudates are dynamic and depend on multiple factors, including plant species, environmental conditions, and microbial interactions, making them critical to plant–microbe communication and essential for plant growth, health, and sustainable agriculture (de Menezes et al., 2017; Jiang et al., 2021b).

Some studies indicate that root exudates attract beneficial microorganisms, influence the rhizosphere microbiome, and enhance plant performance (Vogel and Bai, 2016). Plants typically release 11%–40% of their photosynthetic yield into the rhizosphere as root exudates, which can be classified into low- or high-molecular-weight compounds. Low-molecular-weight compounds include a variety of molecules such as sugars, organic acids, amino acids, alcohols, volatile compounds, and other secondary metabolites (Lin et al., 2021; Poupin et al., 2023). High-molecular-weight compounds comprise mucilage (polysaccharides) and proteins, which tend to exhibit reduced variability while typically constituting a larger proportion of total exudates. Low-molecular-weight compounds, including sugars and amino acids, are primarily released through passive mechanisms such as diffusion, channel transport, and vesicular transport (Hardoim et al., 2015a; Wang et al., 2020). The export of sugars is facilitated by “sugars will eventually be exported transporters” (SWEETs) that function along a concentration gradient (Jiang et al., 2021b). Other compounds, such as secondary metabolites, proteins, and polysaccharides, are typically secreted into the rhizosphere via active mechanisms involving various membrane-bound proteins. For example, secondary metabolites—including flavonoids, phenolics, and hormones—are actively secreted into the rhizosphere through ATP-binding cassette (ABC) transporters or multidrug and toxic compound extrusion (MATE) transporters. Citrate, a low-molecular-weight compound, is specifically transported by MATE antiporters (Lin et al., 2021). Overall, the composition of root exudates and the mechanisms of their release are influenced by various factors including plant species, developmental stages, environmental conditions, and interactions with soil microorganisms, which collectively shape the rhizosphere dynamics (De Vleesschauwer et al., 2008).

Root exudates contain various substances that serve as energy sources, nutrient supplies, and communication signals for plants and rhizosphere microorganisms, influencing the attraction or repulsion of specific microbial strains (Xu and Dodd, 2022; Boo et al., 2024). This study will examine specific compounds, including organic acids, amino acids, sugars, sugar alcohols, flavonoids, phenolic compounds, volatiles, and other secondary metabolites (see Table 1 ). These compounds function as nutrients, signals, or antimicrobial agents in the colonization process of beneficial soil rhizobacteria. For example, various organic acids, including malic, citric, fumaric, tartaric, and succinic acids, are essential nutrients and signaling molecules for beneficial soil rhizobacteria during the colonization process (De Vleesschauwer et al., 2008). Treatments with these acids have been shown to enhance soil physicochemical conditions and manipulate microbial community dynamics, promoting the growth and colonization of beneficial bacteria via mechanisms such as chemotaxis, bacterial motility, and biofilm formation (Stassen et al., 2021; Richter et al., 2023). For example, fumaric and tartaric acids positively influence biofilm formation in Hansschlegelia zhihuaiae by regulating proteins related to motility, which facilitates the degradation of certain herbicides. Additionally, oxalate serves as a carbon source specifically for beneficial Burkholderia species, while pathogenic strains are unable to utilize it, highlighting the selective roles of organic acids in rhizosphere dynamics (Xu et al., 2020; Barrera-Galicia et al., 2021; Coban et al., 2022).

Amino acids are critical components of root exudates that provide essential nitrogen sources for soil microbes, thereby stimulating the growth of beneficial rhizobacteria. Specific amino acids selectively enhance beneficial over pathogenic bacterial growth; for instance, histidine and aspartate are crucial in mediating the chemotactic response of Azorhizobium caulinodans (Kleber et al., 2015; Wu et al., 2024). However, amino acids can also support the proliferation of pathogenic bacteria, underscoring a complex interplay within microbial communities (Zhang et al., 2017). Sugars, particularly sucrose, serve as significant carbon sources and signaling molecules for rhizobacteria, influencing colonization dynamics. Sucrose triggers signaling cascades that activate motility in bacteria such as Bacillus subtilis, thus facilitating effective root colonization (Kumar and Pandey, 2013). Furthermore, sucrose induces the synthesis of antibiotics like surfactin, which enhances the competitive colonization efficacy of Bacillus. Other plant polysaccharides also contribute to biofilm formation and promote flagellar activity in bacteria, supporting robust colonization (Liu et al., 2014; Richter et al., 2023; Li et al., 2024).

Sugar alcohols, such as inositol, are significant in root exudates, where they function as both carbon sources and signaling molecules. Inositol promotes several microbiological processes, including bacterial chemotaxis and biofilm formation (Medina and Kutuzova, 2022). Its transport and secretion in plants are regulated by specific transporters, and its metabolism can boost bacterial colonization competence, emphasizing its functional significance in the rhizosphere (Nazir et al., 2014).

Flavonoids play a vital role in plant–bacteria interactions, especially nitrogen-fixing species (Yang et al., 2018). They attract specific microbial strains by modulating gene expression relevant to motility and biofilm production. Certain flavonoids have been associated with stress resilience in plants and the promotion of biological nitrogen fixation, illustrating the intricate relationships within plant–microbe dynamics (Kumar and Pandey, 2013; Xue et al., 2021). Phenolic compounds released by plants serve as signaling molecules and antimicrobial agents, attracting beneficial microbes while inhibiting the growth of pathogens through various mechanisms, thus enhancing plant defense mechanisms and favorably altering microbial community structures (Pierce et al., 2020). Root volatiles, including various VOCs, facilitate long-distance interactions within the rhizosphere and serve as signals regulating microbial growth and competition. VOCs can effectively attract beneficial bacteria while deterring pathogens, demonstrating diverse effects on microbial community composition that depend on environmental conditions (Li et al., 2024). Additionally, secondary metabolites in root exudates such as camalexin and benzoxazinoids are significant in mediating plant–microbe interactions. These compounds enhance the growth of beneficial microbial strains and contribute to plant defense against pathogens, thereby influencing the overall composition of the rhizosphere microbiome (Wang Y. et al., 2023).

In conclusion, the variety of compounds present in root exudates including organic acids, amino acids, sugars, flavonoids, and secondary metabolites plays crucial roles in shaping microbial communities and enhancing plant health. These complex interactions are fundamental for maintaining healthy soil ecosystems and sustainable agricultural practices.

The rhizosphere, the soil region directly influenced by plant roots, is a dynamic ecosystem teeming with microbial organisms that play a crucial role in plant growth and resilience. Effective management of this microbial community holds immense potential for improving plant adaptability and achieving sustainable agricultural practices (He et al., 2010; Saeed et al., 2021; Medina and Kutuzova, 2022). Table 2 summarizes a variety of microbes and crops, illustrating how rhizosphere engineering can harness indigenous plant microbes and foster beneficial plant–microbe interactions (Yang et al., 2018). The concept of the “core” microbiome is pivotal for understanding the microbial communities associated with plants. This core microbiome consists of a unique set of microbes specific to each plant species, which significantly influences plant health and development (Rendueles and Ghigo, 2015; Risely, 2020). These microbes are often inherited from parent plants, while the plant’s unique root exudates and signaling mechanisms further shape this microbiome. The plant microbiome encompasses a diverse and complex community of microorganisms that inhabit various plant structures, including roots, stems, leaves, flowers, and seeds. These microbial communities are integral to plant development, recovery, and overall health (Zu et al., 2012; Astapati and Nath, 2023).

Recent studies have illuminated intricate relationships between plants and their microbial associates. For instance, legumes release flavonoids into the rhizosphere, activating nod genes in rhizobia and leading to the formation of lipo-chito-oligosaccharides (LCOs) recognized by LysM receptor-like kinases (RLKs) in plant roots, which trigger root nodule formation (Hallama, 2019; Xu and Wang, 2023). Similarly, plants interact with arbuscular mycorrhizal fungi (AMF) through strigolactones, promoting the production of Myc factors that are also recognized by LysM RLKs, thus facilitating AMF invasion (Jiang et al., 2021a; Jiang et al., 2021b). These insights are central to developing strategies for engineering the rhizosphere microbiome, ensuring a balanced and resilient ecosystem that supports sustainable agricultural practices (Pierce et al., 2020). Establishing a state of homeostasis in root microbiomes involves understanding the complex interactions between plants and their microbial communities. The concept of fitness plays a vital role in this context, as plants and their microbiomes mutually adapt to environmental conditions, shaping their interactions (Li et al., 2024). The “extended phenotype” theory posits that the rhizomicrobiome is an inherited ecological characteristic of the plant (Wang Y. et al., 2023). However, the movement and composition of microorganisms within the rhizosphere are dynamic, changing with plant development and influencing the microbial community at different growth stages (Xue et al., 2021). These variations underscore the complexity of the rhizosphere and highlight the necessity for detailed studies to optimize it for sustainable agriculture.

The structure and diversity of plant microbial communities are shaped by several factors, including the plant’s species, genotype, age, developmental stage, health, and fitness (Jin et al., 2024). The genetic diversity of the host, including its genotype and species, plays a critical role in determining microbial outcomes in the rhizosphere (Vorholt et al., 2017). Studies indicate that different rice cultivars harbor distinct microbial communities, with some varieties showing higher populations of nitrogen-fixing bacteria. Interestingly, the host genome appears to have a greater influence on above-ground microbiota compared to those in the roots or rhizosphere (Franco-Duarte et al., 2019; Compant et al., 2025). Environmental conditions, both biotic and abiotic such as geographic location, soil quality, and climate, also significantly affect microbial composition (Blois et al., 2013; Jansson and Hofmockel, 2020; Itabangi et al., 2022; Astapati and Nath, 2023). These factors ( Figure 2 ) primarily influence the rhizosphere and phyllosphere microbiome, but host plant species and genotypes remain crucial for shaping these microbial communities. For example, drought stress has been shown to alter the rhizosphere and phyllosphere microbiome by promoting opportunistic pathogens (Figueroa-López et al., 2016). In addition to abiotic factors, biological factors such as interactions between resident microorganisms, pathogens, soil animals, and weeds also contribute to microbiome dynamics. A study examining microbiome diversity across continents and various plant species showed that soil nutrients and herbivores were key drivers of diversity (Letters, 2014; Butkovi and Gonz, 2021). These findings suggest that universal principles may predict microbial diversity across spatial scales and plant species.

Microbial interactions within SynComs significantly influence their effectiveness. Studies on extensive SynComs have revealed that while negative interactions are common between different microbial kingdoms (fungi, oomycetes, and bacteria), positive interactions tend to occur within the same kingdom (Richards et al., 2017; Bilal et al., 2021). This has important implications for plant growth and health. For instance, specific microbial groups can either enhance or inhibit plant growth depending on the microbial composition and competition dynamics ( Table 2 ). The presence or absence of specific microbial groups can greatly impact plant health and development, highlighting the importance of selecting the right microbial community members. Competition among bacterial strains, particularly within the rhizosphere, plays a crucial role in determining the fitness of nitrogen-fixing rhizobia and other beneficial microbes (López-Mondéjar et al., 2019; dos Santos et al., 2022). Understanding these interactions is key to optimizing SynComs for agricultural applications.

Plants and microbes communicate through specific chemicals, exchanging signals that regulate microbial behavior and plant growth. For example, plants release flavonoids and strigolactones to facilitate beneficial relationships with rhizobia and AMF (Starke et al., 2016; Bilal et al., 2017; Boo et al., 2024). Conversely, microorganisms produce quorum-sensing signal molecules to coordinate their activities, which in turn influence plant growth and immune responses (Zhuang et al., 2020). Legumes produce flavonoids that attract nitrogen-fixing rhizobia, enhancing nitrogen availability for host plants. This interaction exemplifies how plants recognize beneficial microorganisms through specific surface components and released chemicals, known as microorganism-associated molecular patterns (MAMPs) (Lee et al., 2020).

To deepen our understanding of these complex interactions, studies increasingly utilize synthetic microbial community (SynCom)-engineered microbial consortia that mimic natural communities in the rhizosphere. These consortia serve as powerful tools for investigating the dynamic relationships between plants and microbes, particularly in nutrient acquisition and stress response. Studies using SynComs have shown that plant immune signaling pathways are closely linked to microbial community composition. Certain combinations of beneficial microbes can enhance plant health and resilience under stress by modulating immune responses and fostering beneficial interactions (Fall et al., 2022). SynCom, a simplified and controllable microbial community, is an essential tool for validating plant holobiont interactions, identifying core microbiomes, and enhancing crop growth and stress resilience in plant microbiome studies (Hao et al., 2024). Therefore, by systematically varying SynCom composition, insights can be gained into how specific microbial interactions influence plant growth and stress tolerance.

In studies focused on evaluating the traits of plant growth-promoting rhizobacteria (PGPR), smaller SynComs were typically employed, emphasizing functional assessments over ecological analyses. This approach aimed to simplify the incorporation of the “community factor” or interactions responsible for varying outcomes. A top-down study investigated the natural bacterial community within the garlic rhizosphere to identify PGPR strains that positively influenced radish seedlings (Raphanus sativus) (Zhuang et al., 2020). Another study reported that greater richness in Pseudomonas communities contributes positively to both plant biomass and nutrient levels. Additionally, they revealed that multistrain microbial inoculants promote plant growth more consistently and effectively than individual strain inoculants (Sorensen et al., 2016).

Furthermore, smaller SynComs have been utilized to evaluate community impacts on various PGPR traits, including biocontrol and modulation of host immune responses. Another study examined the microbial community structures in diseased and healthy tomato plants, noting differences in the abundance of Gram-positive Actinobacteria and Firmicutes phyla linked to infection status. They created a SynCom comprising four Gram-positive species that, while not directly antagonistic to the pathogen, induced a heightened immune response. Notably, the duration of plant protection offered by SynCom exceeded that provided by the individual strains (Lee et al., 2020).

SynComs are increasingly being used to study these interactions and their role in shaping microbial communities in the rhizosphere. Studies using SynComs have shown that plant nutritional conditions and the presence of other microbes influence microbial colonization patterns, underscoring the significance of plant immune signaling in microbial community composition (Allison et al., 2014; Lee et al., 2019). Microorganisms play an essential role in improving tolerance to abiotic stresses such as drought, high salt levels, and extreme temperatures. They do this by producing biopolymers, osmolytes, and antioxidant enzymes (Bhardwaj et al., 2013; Thakur et al., 2017; Alster et al., 2018). For instance, Bacillus strains have been shown to enhance drought resistance in maize and wheat by stimulating root growth and improving water uptake (Ling et al., 2022; Zhong et al., 2024).

Microbial activities also enhance nutrient absorption by plants. Through nitrogen fixation, nutrient mobilization, and phytohormone synthesis, microorganisms help plants acquire vital nutrients such as nitrogen, phosphorus, and potassium (Egamberdieva et al., 2017). For example, rhizobial inoculants used in legume crops significantly improve nitrogen fixation, reducing the need for synthetic fertilizers. Additionally, microorganisms help plants resist diseases by producing defense enzymes and antimicrobial substances (Pan and Yu, 2011; Blume et al., 2012; Afridi et al., 2024).

Harnessing the plant microbiome presents significant potential for sustainable crop production. A thorough understanding of plant–microbe interactions is necessary to develop resilient agricultural systems (Morrison et al., 2016). Enhancing these interactions aids nutrient acquisition, promotes growth, and increases stress resistance. For example, PGPR, such as Bacillus, Pseudomonas, and Burkholderia, contribute through mechanisms like nitrogen fixation, nutrient mobilization, hormone production, and disease suppression (Fierer et al., 2012; dos Santos et al., 2022; Wang Y. et al., 2023). These microbes colonize root zones, improving nutrient uptake and suppressing pathogens. Moreover, PGPR can form synergistic relationships with mycorrhizal fungi, further enhancing nutrient absorption and soil health (Lee et al., 2020; Zhuang et al., 2020).

Figure 4 illustrates the sequential development of SynComs to optimize plant–microbe interactions for enhanced crop production. The process starts by identifying bacterial strains with plant growth-promoting traits, such as indole acetic acid (IAA) production (Corkidi et al., 2012). The genetic variability of these strains is assessed for compatibility (Kumar and Pandey, 2013; Zhong et al., 2024), followed by a systematic evaluation of their effects on plant growth under controlled conditions, and validation through greenhouse and field trials. Finally, the SynComs are optimized for large-scale application, resulting in improved crop growth, enhanced nutrient uptake, and increased disease resistance (Blankinship et al., 2011). The figure magnifies the root system, highlighting the interactions between SynComs and the rhizosphere, emphasizing their role in nutrient cycling and plant health, thus contributing to sustainable agriculture (Guo et al., 2018; Boo et al., 2024).

Effectively utilizing the plant microbiome to enhance plant health, growth, and productivity involves several strategic approaches. First, selecting plant types with unique root exudate profiles is crucial, as this promotes beneficial microbial communities and enriches plant–microbe interactions by attracting advantageous microbial populations through selective breeding (Singh and Siddiqui, 2010; Blagodatskaya and Kuzyakov, 2018; Velez et al., 2018). Second, optimizing nutrient management is essential for maintaining appropriate nutrient levels to reduce stress-induced changes in exudate composition; optimal management lessens plant stress and preserves microbiome functions, preventing detrimental alterations in root exudate patterns (Corkidi et al., 2012; Singh and Jha, 2016; Xiong et al., 2019; Yang et al., 2024). Lastly, actively introducing beneficial microorganisms into the rhizosphere can enhance plant development and bolster resistance to stress and disease, thereby improving crop productivity and resilience, which are vital for sustainable agriculture (Strickland and Rousk, 2010).

Transgenic crops have the potential to enhance nutritional value and resistance to pests. However, concerns about their impact on soil microbial populations persist. These plants can improve nutrient absorption and environmental resilience but may alter root exudate composition compared to non-transgenic plants. As a result, the changes in exudates can persist in the soil, significantly affecting the native microbiota (Zengler and Zaramela, 2018). Studies on the effects of transgenic crops on rhizosphere biota remain limited, with varying results due to factors such as crop type and trial duration. Some studies suggest that transgenic crops may negatively affect native species through gene flow or the repeated use of insecticides and herbicides (Nazir et al., 2017). However, other studies show that genetically modified crops, like Bt maize, can increase biomass without notable adverse effects on soil microbiota. These conflicting findings highlight the need for further research to fully understand the long-term impact of transgenic crops on soil microorganisms (He et al., 2023). A deeper understanding of plant–microbe interactions and microbial community dynamics is essential for developing a robust and resilient rhizosphere microbiome. Additionally, optimizing techniques such as seed priming or encapsulation for introducing beneficial microorganisms is critical for ensuring their effectiveness in the soil (Du et al., 2022). These advancements will support sustainable agricultural practices that maximize the benefits of transgenic crops while minimizing environmental risks.

Root exudates, a diverse mix of organic chemicals produced by plant roots, play a crucial role in shaping the rhizosphere microbiome. These exudates attract and select specific microbes, facilitating the assembly of SynComs (Marín et al., 2021; Hu et al., 2022). Plants actively customize the composition of root exudates to recruit groups of microorganisms that provide distinct beneficial functions. For instance, carbohydrates such as glucose and fructose attract microbes adept at sugar metabolism, while organic acids like malic and citric acids draw in phosphate-solubilizing bacteria (Yuan et al., 2021). Exudates also influence competition among microorganisms, promoting the growth of beneficial species while inhibiting harmful ones (Wang and Kuzyakov, 2023). Certain exudates can suppress fungal pathogen proliferation, creating a favorable environment for beneficial bacteria. Additionally, exudates establish gradients in the rhizosphere, leading to the spatial organization of microbial communities, which enhances cooperation among diverse microbial groups (Wang and Kuzyakov, 2024b).

Once established, the composition of root exudates continues to influence SynCom members, enhancing their beneficial roles. Exudates supply essential nutrients, promoting the growth and activity of these microbial communities (Cornforth and Foster, 2013). Sugars and organic acids serve as carbon and energy sources, while amino acids provide nitrogen and other vital elements. Previous studies have indicated that exudates can boost the activity of SynCom members involved in nutrient cycling, such as nitrogen fixation and phosphate solubilization (Heilbronner et al., 2021). Specifically, exudates stimulate the expression of genes responsible for nitrogenase synthesis in nitrogen-fixing bacteria (Pantigoso et al., 2022a; Timofeeva et al., 2023). Furthermore, they can induce SynCom members to produce antimicrobial substances, thereby increasing their effectiveness against pathogens (Klimek et al., 2021; Ma et al., 2023). This ability to encourage beneficial bacteria to generate antibiotics and lytic enzymes highlights the critical role of root exudates in fostering synergistic relationships within the rhizosphere (Pausch and Kuzyakov, 2018).

The interaction between root exudates and SynComs is mutually beneficial. SynComs can alter the composition and release of root exudates, creating a cycle that promotes plant development and resilience (Bais et al., 2010). By metabolizing specific compounds or emitting their own secondary metabolites, SynCom members can modify root exudate composition, thereby changing the attractiveness of the rhizosphere to other microorganisms (Wang and Kuzyakov, 2024c). Moreover, SynComs can regulate exudate release by influencing plant signaling pathways. Beneficial bacteria produce signaling molecules that trigger the release of specific exudates, promoting their own growth and activity (Torres et al., 2005). This dynamic not only improves nutrient availability but also enhances plant growth, ultimately strengthening the plant’s resilience to environmental stresses and pathogen attacks (Hanson et al., 2018).

The development of SynComs in the rhizosphere is largely driven by root exudates, which are diverse organic compounds secreted by plant roots. These exudates serve as chemical signals to attract and selectively recruit beneficial microbes, facilitating the assembly of SynComs. This dynamic interaction is essential for strengthening plant–microbe relationships and supporting plant health and productivity (Wang et al., 2021). Soil-dwelling bacteria possess the ability to sense environmental signals and communicate through signaling molecules. This microbial signaling is pivotal in recruiting beneficial taxa, often drawn to specific root exudates. The selective recruitment of these microbes enhances the establishment of SynComs, promoting plant resilience and adaptability to environmental stresses (Kästner et al., 2021). Once recruited, beneficial microbes form direct interactions with plant roots, triggering physiological changes or activating stress responses. These interactions enable a symbiotic exchange, which improves nutrient uptake, disease resistance, and overall growth. The signaling molecules produced by microbes can influence plant signaling pathways, amplifying the benefits of these partnerships (LaRowe and Van Cappellen, 2011; Maurice et al., 2024).

Advances in microbial engineering techniques are depicted ( Figure 5 ) to improve the identification and optimization of root-associated microbial systems (RMS). Techniques such as liquid chromatography–mass spectrometry (LC–MS) and co-occurrence network analysis are instrumental in characterizing beneficial microbial taxa and their interactions (Gunina and Kuzyakov, 2022). These tools enable researchers to reconstruct tailored microbial communities that enhance nutrient cycling, stress tolerance, and overall plant performance (Gunina et al., 2017 ; Dı́az-Vallejo et al., 2021). Engineered SynComs provide a promising strategy for optimizing plant health and agricultural productivity. By fine-tuning microbial interactions and improving the functionality of specific strains, these designed communities significantly bolster plant resilience against abiotic and biotic stresses, thereby promoting sustainable agricultural practices (Heilbronner et al., 2021; Sabrina et al., 2021; Al-Khayri et al., 2023). Therefore, exudate-mediated SynCom formation represents a dynamic, mutually beneficial process that enhances both plant and microbial health. Understanding the complex interactions and signaling mechanisms involved in this process offers valuable insights for developing innovative strategies to make plants healthy and more stress tolerant (Klimek et al., 2021). These advancements hold immense potential for fostering sustainable agriculture and ensuring global food security (Klimek et al., 2021).

Selective breeding of plants to improve their interactions with microorganisms has become increasingly important. This process can lead to the selection of microbes that engage in beneficial interactions with plant roots and surrounding soil. For example, genes responsible for root structure and exudation can influence microbial communities in the rhizosphere (Tijhuis et al., 1993; Haney, 2021a). Mutations affecting root hair size and density can reduce microbial diversity, indicating that specific root characteristics impact the recruitment of beneficial microbes (Guhr et al., 2015). Studies involving maize have identified genetic loci that support the optimization of symbiotic relationships between plants and microbes (Wolf et al., 2013; Fan et al., 2017; Rivas-Franco et al., 2020). For instance, breeding crops to improve compatibility with symbiotic microorganisms, such as Epichloë endophytes or AMF, enhances their effectiveness. In ryegrass, selective breeding for endophyte alkaloid profiles has led to improved pest resistance and consistent trait expression (Calvin and Bassham, 1962; Rojas-Solís et al., 2018; Schimel, 2018; Zheng et al., 2018; Rolfe et al., 2019; Sharma et al., 2020; Wang and Kuzyakov, 2024b). Therefore, the goal is to enhance plant resilience against abiotic stress and improve nutritional quality. There is increasing interest in using plant-associated microbes to enhance plants’ ability to tolerate stress while reducing pesticide residues. Soil- and plant-associated microbes can degrade pesticides, thus improving the safety of plant products (Brunel et al., 2020; Dubey et al., 2020). Additionally, endophytes can help break down herbicides, providing a mechanism for herbicide resistance and effective weed management (Lemanceau et al., 2017; Deveau et al., 2018; Jacoby et al., 2020b; Compant et al., 2021; Pantigoso et al., 2022b; Wang Y. et al., 2024).

Advanced experimental techniques are essential for understanding microbial community diversity and plant–microbe interactions. Functional gene microarrays, such as PhytoChip and GeoChip, allow researchers to assess microbial processes and gain insights into the functional roles of microbial taxa within an ecosystem (Decleyre et al., 2015; Meidute et al., 2018). Real-time visualization of microbial colonization on plant roots is possible through fluorescence emission in situ, offering valuable data on microbial interactions in natural environments (Hardoim et al., 2015b; Sayre et al., 2023; Haney, 2021b). Molecular manipulation tools, such as gene silencing, transgenic technologies, and CRISPR/Cas9 gene editing, have become integral for studying plant–microbe interactions. These technologies allow for the investigation of genetic functions and the refinement of traits that benefit plant performance. CRISPR/Cas9, known for its precision, can be used to modify plant genes affecting root exudates and microbiome composition, thereby improving plant growth and resilience (Lo et al., 2022; Chen et al., 2024).

Moreover, synthetic biology and genetic engineering provide solutions to agricultural challenges, including pest resistance, nutrient efficiency, and environmental resilience. The application of these techniques holds the potential to enhance agricultural sustainability, increase crop yields, and address global food security concerns (Santı́n et al., 2016; Aplakidou et al., 2024). RNA interference (RNAi) is also an effective tool for improving disease resistance by targeting both transcriptional and posttranscriptional processes (Mason-Jones et al., 2022; Wang M. et al., 2023).

“Rhizosphere microbiome engineering” ( Figures 6 , 7 ) depicts three stages of enhancing plant–microbe interactions to promote sustainable agriculture. In Figure 6 , the first stage focuses on traditional methods, such as soil management and microbial inoculants, to boost beneficial microbial populations. The second stage introduces emerging techniques that involve breeding plants for beneficial root exudate production and developing customized inoculants (Singer et al., 2016). The third stage emphasizes the role of genetic engineering and molecular methods, showcasing how these advanced techniques can be used to tailor plant traits for improved interactions with beneficial microbes, thereby enhancing nutrient acquisition, stress tolerance, and overall plant health. This integration of genetic engineering with microbiome strategies represents a progressive approach to achieving resilient agricultural systems (Rojas-Solís et al., 2018; Bai et al., 2023).

As depicted in Figure 8 , methodologies for optimizing bacterial strains to enhance sustainable agriculture are essential for improving crop production systems. The process begins with the isolation of promising bacterial strains through functional profiling, metagenomics, and biochemical analysis (Berendsen et al., 2012; Bulgarelli et al., 2013; Müller et al., 2016; Zhang et al., 2020; Solomon and Janda, 2024b). Following the isolation, genome sequencing is conducted to annotate and identify beneficial traits associated with plant growth promotion and stress resilience (Hacquard et al., 2015). Subsequently, the application of CRISPR gene editing allows for the refinement of these beneficial traits, ensuring that the selected strains can effectively support plant growth and enhance resilience to environmental stresses (Calvin and Bassham, 1962; Geldner, 2013; Carabotti et al., 2015; Berendsen et al., 2018; Cryan et al., 2019; Hulme et al., 2020). Finally, transcriptomic and proteomic analyses are employed to evaluate gene expression and protein functions, guiding the development of bacterial strains that improve nutrient uptake and provide biocontrol against pathogens (Yuan et al., 2018). This integrated approach underscores the potential of modern genomic techniques in leveraging beneficial microbes for sustainable crop production, offering innovative solutions to meet the challenges of food security and environmental sustainability (Bais et al., 2010; Hiruma et al., 2016; Bakker et al., 2018; Stringlis et al., 2018b; Finkel et al., 2019).

The rhizosphere, the soil region surrounding plant roots, represents a dynamic ecosystem where complex interactions between root exudates, SynComs, and diverse soil microorganisms shape plant health and nutrient availability. These interactions are largely mediated by root exudates, which vary in composition and concentration based on plant species, developmental stages, and environmental conditions (Brunel et al., 2020; Pascale et al., 2020). However, isolating the specific impacts of individual exudate components on SynCom members is challenging, given the competition among microbial species for limited resources. This complexity underscores the need for a more comprehensive understanding of the genetic and metabolic mechanisms underlying these interactions (Mark et al., 2005; DeAngelis et al., 2009; Micallef et al., 2009; Chaparro et al., 2013).

Despite significant advancements in microbial ecology, the application of SynComs in agricultural settings presents challenges, including regulating colonization, maintaining functional stability, and ensuring competitiveness against native microbes (Cavaglieri et al., 2009). Furthermore, spatial and temporal variability in management practices, such as tillage and fertilization, often affects the effectiveness of these microbial applications (Prando et al., 2024). Therefore, advancing our understanding of the mechanisms driving root colonization and microbial functionality is critical for achieving success in rhizosphere engineering.

Effective SynCom research requires careful consideration of experimental design, plant models, and environmental variables. Selecting well-established plant models can provide insights into microbiome dynamics and their influence on plant development. Additionally, external factors, such as soil composition and climate, should be incorporated into research frameworks to understand how these variables affect plant–microbe interactions (Stursova et al., 2012; Sheth et al., 2016; Seidel et al., 2024). Therefore, advancements in omics technologies metagenomics, metatranscriptomics, and metabolomics are transforming our understanding of microbial community dynamics in the rhizosphere. Metagenomics allows for the identification of genetic potential within microbial communities, while metatranscriptomics reveals active microbial functions, shedding light on their roles in nutrient exchange and plant health (Mackelprang et al., 2016; Haney, 2021b; Wang Y. et al., 2023). These insights can guide the development of more targeted microbial interventions for sustainable agriculture.

Omics technologies have revolutionized the study of rhizosphere dynamics. Metabolomics, for example, provides insights into small-molecule metabolites involved in plant–microbe symbiosis, which can inform strategies for improving plant resilience and optimizing agricultural practices (Bais et al., 2010; Lo et al., 2022). Integrating data from genomics, transcriptomics, metagenomics, and metabolomics facilitates a holistic understanding of microbial ecosystems, revealing regulatory networks and key metabolic pathways critical for plant–microbe interactions (Aplakidou et al., 2024). For instance, variations in root exudate levels correlate with specific microbial groups, emphasizing the importance of harnessing these chemical signals to enhance microbiome functionality (Tong et al., 2024). Despite these advancements, challenges remain, particularly in integrating data across molecular levels. Addressing these computational hurdles is essential to fully leverage the potential of multi-omics technologies in understanding and optimizing rhizosphere interactions.