Being sessile in nature, plants need to withstand changing environmental conditions to ensure their survival. Adapting to fluctuating conditions, plants require the adoption of various sophisticated mechanisms by molecular, physiological, or morphological changes. Emerging research in plant science is very less concerned with the rhizospheric microbial community shaped by the biochemical compounds present in the root exudates delivering adaptive capabilities during stressful environmental conditions. However, it is very interesting that plants themselves invest up to 40% of their photosynthetically assimilated carbon as exudates into the rhizosphere primarily composed of a wide range of compounds, e.g., a blend of amino acids, compound sugars, and organic acids (Canarini et al., 2019; Bhutia et al., 2023). Plants are endowed with the capability to alter plant rhizospheric microbes by natural means such as root exudation, which is crucial for plant growth and development. The root exudation pattern of crop wild relatives is attracting much attention nowadays, as root exudates modulating the rhizosphere microbiome might have the potential to substitute the use of chemicals in agricultural fields (Preece and Peñuelas, 2020). Recently, scientists have developed the concept of entropy-based engineering of the rhizosphere, which targets more production using less input (Zhang et al., 2022). With the advances in understanding the role of root exudates in modulating the rhizospheric microbial community, it can be correlated that under any environmental constraints, root exudation pattern changes, resulting in the alteration of the root-associated microbiome. Understanding the role of root exudates is not possible without discussing various environmental conditions that can play pivotal roles in shaping the rhizospheric microbial community. Changing climatic conditions exert pressure on the plants, which are ultimately executed by the roots in shaping the root system architecture (RSA), depending upon the plant developmental stages and genotypes (Dabhi et al., 2021; Sarita et al., 2022). The RSA helps in the better adaptation of the plants through enhanced nutrient acquisition and by modulating the rhizospheric microbial community. In addition to RSA, various edaphic factors like soil pH, soil temperature, aeration, and physicochemical characteristics have a great influence on determining the microbial community of the rhizosphere (Ling et al., 2022). Root exudation pattern and rhizosphere microbiome structure also change in accordance with the type of soil where the plant grows (İnceoğlu et al., 2012).

In addition to the above-listed edaphic conditions determining the composition and quantity of root exudates, it also firmly depends upon specific plant species or host genotype, prevailing environmental conditions, and the stress status of the plant. The root exudates act as a signalling molecule and help in recruiting beneficial root-associated mutualists, like Pseudomonas, Bacillus, Trichoderma, and mycorrhizal species (Pieterse et al., 2014), and eradicate harmful microbes in the rhizosphere, resulting in shifting the microbial community composition. Plant-associated rhizospheric microbes assist their host in a variety of activities, ranging from nutrient acquisition to defence against herbivores (Malacrinò et al., 2021), by activating induced systemic resistance (ISR) where root-specific transcription factor MYB72, phytohormones like salicylic acid (SA), volatile organic compounds (VOCs), and defence regulatory proteins play a critical role (Pineda et al., 2010; Pieterse et al., 2014). Plants respond robustly against insects and pathogens attacks by priming their leaf tissues with the help of ISR rather than directly activating the defence-related genes (Pineda et al., 2010). Traditionally, the main objectives underlying plant growth-promoting microorganism research include plant growth stimulation and yield enhancement. Understanding the role of root exudation in altering microbial community dynamics has recently emerged and attracted much attention. Further, the rhizospheric microbes and their molecular mechanisms involved in plant–plant interaction for establishing social networking systems have been studied in detail. The mycorrhizal fungal associations and the parasitic plants play significant roles in generating wired social networking systems. In contrast, root exudates and VOCs establish a wireless social networking system among the neighbouring plants (Park and Ryu, 2021; Sharifi and Ryu, 2021).

This review highlights various biotic stress-inducing factors that result in the amendment of rhizospheric microbial community composition. Firstly, we gave an overview of the microbes generally found in the rhizosphere followed by the role of different environmental factors (major biotic factors) influencing the host root exudates composition in the recruitment of either beneficial or pathogenic microbes. Secondly, we discussed the importance of root exudates in influencing the community structure of plant microbiomes. Further, based on various studies, we have tried to decipher the importance of positive and negative below-ground interactions in influencing plant resilience against varied environmental circumstances.

The soil is an overwhelming reservoir of microbial diversity. It has been estimated that 1 g of soil can carry billions of bacterial cells belonging to thousands of different taxa having crucial functions in plants and the environment. These microbial complexes establish an association between plant and rhizosphere and are also considered as the plant’s second genome (Berendsen et al., 2012). Hiltner in 1904 defined rhizosphere as the soil region that is directly associated with plant roots. With a deeper understanding of the rhizosphere as the hotspot of soil biogeochemical cycles, the definition of rhizosphere has been extended. Based on the paradigm of various soluble compounds and gaseous molecules, a new concept of rhizosphere has been developed, which defines it as the portion of soil involving the root system, up to which gaseous exchange by means of diffusion can take place (de la Porte et al., 2020). Contemporary investigations in understanding the rhizosphere microbiome have revealed that the host plant’s genetic makeup is also involved in the alterations of the rhizomicrobiota. The rhizosphere microbiome is very important for the fitness of the host, and the manipulation of the rhizosphere microbiota is presumed to provide a solution for climate-resilient crop production (Pieterse et al., 2016). A competitive battle in the rhizosphere is going on among different types of microorganisms competing for plant-derived nutrients, resulting in their interactions with the roots (Li et al. 2021b). For instance, arbuscular mycorrhizal fungi (AMF) are reported to colonize approximately 71% of terrestrial plants exhibiting complex interaction patterns in various plants except for plants belonging to Brassicaceae, Chenopodiaceae, Polygonaceae, Amaranthaceae, and Caryophyllaceae (Wang and Qiu, 2006; Fernández et al., 2019). Complex chemical signalling between the host plant and AMF results in enhanced plant nutrient acquisition and protection of the plants from pathogen infection (Dowarah et al., 2021). Sensing the varied environmental stimuli, the microbiome structure of the soil changes, which is further interlinked with the nature of the soil and the plant species involved in the recruitment of microbes (Garbeva et al., 2008). İnceoğlu et al. (2012), from their investigation, reported that the type of soil functions as a determining factor in structuring the rhizospheric microbial community. Based on the rhizospheric effect, they concluded that potato cultivars grown on different soil types recruited diverse communities of microbes with diverse functional abilities. Five types of potato cultivars were collected from loamy and sandy soil regions and found that bacterial communities in the loamy soil rhizosphere show more affinity towards carbohydrates and amino acids, while communities reported from the sandy soil rhizosphere have shown a higher affinity towards polymers, alcohols, and nucleotide-based carbon sources, which were secreted out by the roots as exudates. Despite these natural signalling cues, a new concept of “entropy” has been introduced in the area of agricultural research, which tries to emphasize that the lower the entropy, the more ordered the rhizospheric interactions, which can ensure proper utilization of energy and resources by the plant (Zhang et al., 2022).

Plenty of research on soil microbial communities revealed that soil around the root region has a high density of microbes such as Actinomycetes, bacteria, and fungi, with higher activity rather than the bulk soil, a phenomenon known as the “rhizosphere effect” (Philippot et al., 2013; Bakker et al., 2020). However, as compared to bulk soil, the rhizosphere harbours a less diverse group of microbes (Philippot et al., 2013; Bakker et al., 2020). Depending upon environmental stimuli, the rhizosphere acquires selective microbes from the bulk soil. In the rhizosphere, the most prominently reported bacterial groups are the Acidobacteria, Bacteroidetes, Firmicutes, Planctomycetes, and Proteobacteria (Uroz et al., 2010; Bulgarelli et al., 2012; Dastogeer et al., 2020). Moreover, some bacterial communities like Actinobacteria and Xanthomonadaceae are scarcely present in the rhizosphere as compared to the bulk soil (Bulgarelli et al., 2012; Dastogeer et al., 2020). It has also been reported that the rhizosphere is predominantly colonized by mycorrhizal fungi that are estimated to be associated with approximately 80% of all land plants providing N and P for proper growth and development (van der Heijden et al., 2015; Weng et al., 2022). This symbiotic interaction between the mycorrhizae and the roots of higher plants has great significance in shaping the terrestrial ecosystem, as it can regulate the carbon and other nutrient cycles of the earth.

Plant rhizosphere microbiome is a result of interaction among plants, microbes, and associated environmental factors in either biotic or abiotic form or in alliance forming a tritrophic interaction (Badri et al., 2009). The plant species, its genotype, distinct tissue or organ, age and developmental state, ecosystem canopy type, immunity, etc., are some of the factors associated with the host plant, which can determine the rhizospheric microbial community (Dastogeer et al., 2020). Together, several plant-derived compounds like different alkaloids, phenolics, and terpenoids also have an important role in shaping the rhizosphere microbiome. Some of these plant-derived compounds are specific for some plants; e.g., glucosinolates are found predominantly in the Brassicaceae group (Dastogeer et al., 2020), and aglycone benzoxazinoids (BX) are produced by maize, which induces jasmonic acid-dependent resistance against herbivores (Hu et al., 2018).

In addition to the above-ground environmental factors and plant genotype, the rhizospheric microbial community composition relies also upon the soil texture and below-ground abiotic factors such as soil temperature, pH, and CO₂ concentration. Fierer et al. (2007) investigated and found that carbon availability in the soil can play a role in the regulation of certain bacterial community structures involving Acidobacteria, Bacteroidetes, and Betaproteobacteria. However, Lauber et al. (2009), in their study, revealed that soil pH has a remarkable effect on the regulation of soil microbiome structure. On the contrary, the temperature was found to modulate plant root interactions with rhizospheric microbes, where the rhizosphere was found to be more responsive to changing temporal conditions than the phyllosphere (Luo et al., 2020); e.g., roots colonized by mycorrhizal fungi shows greater resilience in temperature stressed condition, playing a key role in plant adaptation to high temperature (Usman et al., 2021).

In contrast to various environmental factors, biotic components such as pathogens, parasites, or mutualistic plant microbes, present at the phyllosphere or rhizosphere, perform a crucial role in shaping the rhizospheric microbial community by influencing the survival of plants during or post-stress conditions. Among various biotic factors, AMF actively takes part in shaping the rhizomicrobiota (Dowarah et al., 2021). AMF association with the plant root is a very complex process that requires coordination between plant and fungal signalling molecules. Roots having AMF associations are protected against pathogens as AMF helps in nutrient acquisition and repair of pathogen-damaged cells (Dowarah et al., 2021). Here, the root architecture plays an important role, as it was reported that AMF benefit the tap root system in a better way as compared to the fibrous root system (Yang et al., 2015). Frew and Price (2019) reported that under elevated CO₂ levels, both C3 and C4 plants produce a high amount of photosynthetically fixed C compounds. C4 plants allocate their excessive photosynthates in the rhizosphere with the help of root exudation, which leads to better AMF colonization, finally resulting in enhanced nutrient acquisition than that of C3 plants. Data on the underlying mechanism(s) involved in rhizosphere microbiome amendment under the influence of various stress conditions are limited. In this review, we have tried to highlight the role of biotic stresses in altering root exudate secretion patterns and also how the change in root exudate composition can influence the recruitment of the rhizospheric microbes during stress conditions.

Root exudation is the key mechanism by which plants maintain a homeostatic interaction with their below-ground environment. Plants exude various primary and secondary metabolites as root exudates, ultimately shaping the community structure of rhizosphere-dwelling microbes. The exact mechanism of root exudation is not yet clear, but to allocate the photosynthetically fixed C from the aerial plant parts to the soil, a mechanism similar to Munch’s hypothesis (Münch, 1930) is used by the plants, where diffusion plays a critical role (Canarini et al., 2019). According to Munch’s hypothesis, a concentration gradient between the source and sink organs, i.e., phloem and root tip generate turgor differences, eventually resulting in the translocation of metabolites from the phloem to the root tip and then to the soil (De Schepper et al., 2013; Ross-Elliott et al., 2017). Exudation of various metabolites from the root cells to the soil might involve facilitated diffusion, where concentration gradients act as a central force and specific transmembrane proteins help in the efflux of such molecules (Sasse et al., 2018). Specialised efflux carriers and channel proteins facilitate the secretion of primary metabolites like amino acids, organic acids, and sugars into the rhizosphere. For example, for amino acids, UMAMIT (usually multiple acids move in and out transporter), CAT (cationic amino acid transporter), and GDU (glutamine dumper) transporters, for organic acids, ALMT/malate (aluminium-activated malate transporter) and MATE/citrate transporters (multidrug and toxic compound extrusion), and sugar molecules, a family of transporters known as the SWEET transporter family are used by the plants (Canarini et al., 2019). Like primary metabolites, secondary metabolites also constitute a part of root exudates. Various secondary metabolites like phenolics, alkaloids, and terpenoids are transported into the rhizosphere with the help of ATP-binding cassette (ABC) transporters (Badri et al., 2009), whereas most of the primary metabolite transporters use passive transport as a mechanism of exudation, except MATE/citrate transporter having H⁺ coupled antiport activity (Meyer et al., 2010). A balance in the concentration gradient across the external and internal environment is maintained by the rhizospheric microbes as well as by the plants themselves. The exudates secreted out are consumed by various rhizospheric microbes, and a low concentration level is maintained in the external environment, enhancing root exudation (Canarini et al., 2019). With the help of phloem loading and transport (source activity), phloem unloading (sink activity), regulation of the expression of genes, or post-translational modifications of efflux carriers, plants might control the process of root exudation. Overall, the plant source-sink dynamics fundamentally regulate the allocation of photosynthates into the soil (Farrar and Jones, 2000; Savage et al., 2016). Moreover, plants modify their RSA depending on the concentration of primary metabolites at the root region, thus controlling the exudation process (Canarini et al., 2019; Bhutia et al., 2023). Modification in the efflux or influx of metabolites at the root region critically shapes the RSA where amino acids have a cascading influence in shaping the RSA. The expression of NRT2.1 transporter genes is mainly regulated by the amino acids, indicating the plant-soil N status (Nazoa et al., 2003). Glutamate is an important amino acid that functions similarly to the phytohormone auxin. A rapid increase in cytosolic Ca²⁺ and depolarization of the membrane is induced by glutamate, where an electrical signal similar to the synapsis of mammals is generated (Baluška and Mancuso, 2013; Ni et al., 2016). Additionally, a receptor family, known as the glutamate receptor-like (GLR) receptors, functions like amino-acid-gated Ca²⁺ ion channels and acts as a signal to convey the plant N status to the root (Brian and Lea, 2007; Vincill et al., 2012), thus shaping the RSA. The change in RSA, impacts the root exudation pattern by changing the composition of root exudates under various environmental conditions.

Since the exudation of various metabolites involves specialised carriers and takes place through facilitated diffusion, the molecular mechanisms involved in such processes may indirectly govern the mechanisms of root exudation. Further, studies on genes involved in shaping the RSA of plants might help in the detailed understanding of the root exudation mechanism.

The ability of plants to adapt and survive in an environment primarily depends upon their capacity to acquire resources and resist external perturbations, impacting growth and productivity. In non-homogeneous soil conditions, the plant roots perform a crucial function in the absorption of mineral and nutrient resources from the soil, either directly or in association with rhizospheric microbes. These microbes are presumed to be attracted by plant-specific root exudates under normal or stressful circumstances. Thus, nutrient supply effect root exudation mostly from the root apices, ultimately altering the nutrient dynamics and the soil microbiome structure (Paterson et al., 2006).

The quality and quantity of various root exudates with different compositions secreted from different locations of the root are mainly determined by root branching and RSA (Badri and Vivanco, 2009; Canarini et al., 2019). The root meristematic and elongation zone present above the root tip secrete amino acids like asparagine and threonine, while other amino acids like glutamic acid, valine, leucine, and phenylalanine are secreted from the root hairs, along with the whole root exuding aspartic acid ( Figure 1B ) (Haldar and Sengupta, 2015). Several discrete blends of phytochemicals from various plant species are also released from different parts of the root like the mature root regions and root cap and also from root hairs (Nguyen, 2009).

Exudation from the roots contributes to both positive and negative associations in the below-ground environment. Positive root–microbe associations involve mutualistic interactions between root and beneficial microorganisms like plant growth-promoting rhizobacteria (PGPR) and mycorrhizal fungi, while negative associations involve the interaction of roots with harmful organisms like pathogens, invertebrate herbivores, and parasitic plants (Badri et al., 2009). Plants produce diverse arrays of secondary metabolites such as phenolic compounds, alkaloids, and terpenoids, some of which are genus/species-specific (Bednarek and Osbourn, 2009; Dastogeer et al., 2020). For example, barley plants infected with Fusarium graminearum release exudates having a high concentration of phenolic compounds, which alters the rhizospheric microbial community to enhance the plants’ defence against F. graminearum (Phour et al., 2020; Afridi et al., 2022).

Microbial degradation of leaf litter and dead plant substances in the rhizosphere serve as key resources for plant growth and also participate in carbon storage in the ecosystem by releasing nutrients as a decomposition product (Schneider et al., 2012). Studies suggest that mucilage-degrading fungi (MDF) and other microbes actively work upon mucilage or root exudates and break them into small molecular weight compounds, which act as signalling molecules for the recruitment of various PGPR. Artemisia sphaerocephala, a remarkable plant of Asian cold deserts, was used in a study where mucilage-degrading microbes were isolated from the root–soil junction. From the study, it becomes evident that the MDF associated with the roots of A. sphaerocephala recruit bacterial groups like Actinobacteria, Firmicutes, Proteobacteria, and Verrucomicrobia towards the roots and regulate the rhizosphere microbiota (Hu et al., 2021). Further, microfluidics-based investigation for real-time study of plant–microbe interaction revealed that Bacillus subtilis exhibits chemotactic behaviour towards the root elongation zone, which might be due to the secretion of root exudates (Massalha et al., 2017; Sasse et al., 2018). In addition to that, Escherichia coli cells from the rhizosphere were excluded after the colonization of B. subtilis at the rhizospheric region of Arabidopsis thaliana (Massalha et al., 2017). Microbes belonging to the group Clostridium are presumed to be associated with the root meristematic region as they produce l-threonine dehydratase and l-serine dehydratase enzymes, which may catalyze dehydration and isomerization of root-secreted threonine and serine, respectively (Hofmeister et al., 1993), and might alter the root exudation pattern of the host plant. Clostridium spp. are also involved in the degradation of renewable complex compounds like lignocellulose and make it utilizable for the plants as a resource, ultimately maximizing the C substrate exploitation and yield of the plants ( Figure 1B ) (Du et al., 2020). The root tip actively associates with a number of bacterial groups and withstands numerous obstacles due to which the cells shed off and reform in a continual process. These damaged cell parts contain lignin, cellulose, and various organic compounds and are presumed to be degraded by the Streptomyces species, as it contains a large amount of extracellular enzymes such as cellulase, glucosidase, xylanase, and lignocellulase (Schrempf et al., 2007; Chater et al., 2010).

Since the plants encounter a range of above-ground and below-ground constraints in their lives, to cope with those factors, the plants secrete different blends of chemical compounds in the form of root exudates, which varies in different plants with respect to their age. Nevertheless, it is very difficult to understand the factors responsible for variation in root exudation, as it is an emerging area in plant biology, and more precise research needs to be performed in the future.

Photosynthetic machinery involving C3, C4, and CAM pathways categorizes the plants based on the specific pathway used during photosynthesis. The functioning mechanism of C3 and C4 plants vary based on the site of carbon fixation, and the initial stable compound forms and acts as a substrate during the dark reaction of photosynthesis, where C3 plants convert three carbon molecules (phosphoglycerate) and C4 plants convert four carbon molecules (oxaloacetate) into metabolically active organic compounds. The correlation between the root exudation pattern and the plant’s mode of photosynthesis shows that root exudate composition differs depending upon the mode of photosynthesis. The major constituents of root exudates vary in both the plant groups, and it has been found that C3 plants release a large amount of carbohydrates and organic carbons (Nabais et al., 2011), whereas C4 plants mostly secrete amino acids and organic acids as a major constituent of root exudates. In C3 plants, mainly mannose, maltose, and ribose constitute the exudates (Vranova et al., 2013), but in C4 plants, inositol, erythritol, and ribitol are found (Olanrewaju et al., 2019) ( Figure 2 ). Variability in the exudation pattern of C3 and C4 plants might have contrasting effects in shaping the rhizospheric microbial community. C4 plants in comparison to C3 plants are more tolerant to adverse environmental situations, but the role played by root exudates in C4 plants’ adaptability is not yet clear. It is evident that under elevated CO₂ levels, C4 plants allocate their excessive photosynthates in the rhizosphere with the help of root exudation, which leads to better AMF colonization finally resulting in enhanced nutrient acquisition by C4 plants (Frew and Price, 2019), which indicates the reason behind the better resilience of C4 plants in stress condition. Additionally, a large proportion of weeds fall under the category of C4 plants, exhibiting a wide range of adaptive behaviour under various environmental perturbations. Weeds secrete allelochemicals as their root exudates, attracting more beneficial microbes and resulting in better adaptation than the neighbouring crop plants (Trognitz et al., 2016; Trivedi et al., 2022).

C4 plants, like maize, induce JA-dependent resistance against herbivores (Spodoptera littoralis) due to the exudation of BX from the roots, which changes the rhizospheric microbial structure and makes the maize plants more resistant against the caterpillar attack (Hu et al., 2018). In contrast, tobacco plants infected with black shank disease caused by Phytophthora nicotianae can perform a pre-infection prevention strategy by exuding antimicrobial substances and lead to increased disease resistance by eliciting plant defence responses (Zhang et al., 2020). There are very few reports on studies elucidating the composition of the exudates according to the plant’s mode of photosynthesis and their influence on the rhizospheric microbial community. To have a comprehensive understanding, future research work on root exudate secretion mechanisms in C3 and C4 plants is warranted.

The secretion of root exudates as a signalling molecule can help in deciphering the plant’s stress status with the rhizospheric microbes and the neighbouring plants. Root exudates serve as organic carbon sources for rhizospheric microbes and their composition changes during plants’ interaction with pathogens or neighbouring plants either at above-ground or below-ground levels. Specific exudates are released under biotic stress conditions, thereby altering rhizospheric microbial community structure and promoting plant health by inducing SAR or ISR. Maintenance of a low-entropy state in the rhizosphere is important for creating equilibrium and promoting root–soil–microbe interactions by maximizing energy utilization, which optimizes localized nutrient supply. Further, a detailed understanding of entropy-based modulation of root exudates and the rhizomicrobiota in crops and crop wild relatives (CWRs) might pave the way for sustainable crop management. With the advances in molecular biology techniques, the root exudate compositions of various plants might be studied in detail under natural conditions. In addition, traits associated with root exudation of CWRs might have effective agronomic use in the future, as such type of traits might be exploited in the future to generate pest-resistant, fertilizer-independent, or weed-suppressive crops (Preece and Peñuelas, 2020). Furthermore, exploration of the rhizosphere microbiome structure of C3 and C4 plants under varied biotic stresses will help in designing specific agronomic strategies for these groups of plants. The molecular mechanisms governing the root exudation process are not very clear to date, but a detailed understanding of root exudation can provide a solution for effective stress management.

NA was responsible for writing guidance and manuscript preparation. IS and SK were responsible for writing the first draft of the review article. NA revised the article with IS and SK. All authors contributed to the article and approved the submitted version.