Communication between plant roots and the soil microbiome; involvement in plant growth and development

Root-associated microbial communities have strong influences on the health and development of plants. Through the secretion of root exudates, the soil microbiome is impacted by plants, thereby steering plant-soil reactions. Considering the importance of root exudates in the establishment of symbiotic associations in the rhizosphere, it is quite clear that understanding the interaction between plant roots and the soil microbiome may prove beneficial. Here, we review the interaction between plant root exudates and microbial communities in the soil. The influence of these bioactive molecules on the structure and function of soil microbes is also considered. We additionally, deliberate on how plants determine the soil microbiome and how they extract nutrients from endophytes for the augmentation of their growth and development. A good perspective of the communication between plant roots and the soil microbiome could lead to increased crop production, thereby limiting the need for synthetic fertilizers.


Introduction
The rhizosphere is an intricate ecosystem inhabited by several organisms such as bacteria, fungi, nematodes, and arthropods.Augmented bacterial abundance and activity are features of the rhizosphere relative to bulk soil; it however, reportedly has lower diversity.In a complex manner, plant roots interact with microbial communities in the soil through chemical communication in the rhizosphere.Interactions with the complex microbial community known as the root microbiome have the prospective of inducing plant growth and development.Microorganisms are major contributors to nutrient cycles and facilitate the acquisition of nutrients by plants (Amoo and Babalola 2017;Lareen et al. 2016;Mhlongo et al. 2018).
The root microbiome has been regarded as the 'secondary genome' because host plants get compounds and qualities that are consequential from microbes there.For the formation of symbiotic associations with plants, beneficial molecules that can alter some plant traits are produced by rhizobacteria (Lareen et al. 2016;Mhlongo et al. 2018).Numerous organisms possess the ability to impact their local ecosystem thus altering individual functioning.Plants can influence the soil microbiota through the exudation of bioactive molecules into the rhizosphere.Root exudates characterize carbon and nitrogen substrates for the growth of microbes, and they consist of primary and secondary metabolites.Through the alteration of microbial communities, root exudate metabolites can steer plant-soil reactions.Root exudates influence microorganisms present in the rhizosphere by operating as repellants, signaling molecules, stimulants, or attractants (Olanrewaju et al. 2019).
The increasing population of humans has placed more demand on food production, and this has resulted in the overuse of synthetic fertilizers by some farmers.Fertilization has been reported to impact microbiome-mediated processes in plants such as modification of hormones and alteration of resource accessibility, which causes vicissitudes in competition among microbiota.Intensifying fertilizer application can alter the availability of nutrients crucial to plant growth (Amoo et al. 2021;Enebe and Babalola 2021).Understanding how plant roots and the soil microbiome communicate is important because various studies have highlighted the influences root-associated microbial communities have on the health and development of plants.
Here, the interactions between exudates produced by plant roots and soil microbes are discussed.We further discuss how hosts determine the microbiome and how plants extract nutrients from endosymbiotic microbes, thereby enhancing their growth and development.We conclude by pinpointing areas of prospective research necessary for the growth and development of plants.

Plant-root exudates and the soil microbiome
Plant-root exudation is a complex process involving factors that regulate carbon transport via the Munch's pressure flow hypothesis (Canarini et al. 2019).The hypothesis suggests that the movement of sap, which encompasses essential nutrients such as carbohydrates, is propelled by osmotic pressure gradients existing between source and sink tissues (Babst et al. 2022).Carbohydrates are loaded into the phloem at source regions (photosynthetic leaves), creating higher osmotic pressure, and flow toward sink regions (nonphotosynthetic areas) where they are unloaded for growth and storage (Hunt et al. 2023).
Root exudates establish an intricate and interconnected association between plants and the microbiome functioning as substrates and signalling molecules for microorganisms.These exudates establish a distinctive environment in the rhizosphere and can attract and instigate pathogenic and symbiotic associations in the rhizosphere (Hu et al. 2018).Previous studies have revealed that modifications in the composition and concentration of root exudates in maize, pea, wheat and sugar beet at different developmental stages have caused changes in the structure of fungal and bacteria (Chaparro et al. 2014;Garcia and Kao-Kniffin 2018).
Vesicle transport, diffusion, and ion channels are some mechanisms by which exudates are released by plant roots (Olanrewaju et al. 2019).Root exudates move outside the root tips through the plasma membrane either by active or passive transport to reach the cell walls (Olanrewaju and Babalola 2022).Low-molecular-weight compounds (Table 1) can pass through the plasma membrane using specific flow carriers.The specific flow carriers for amino acids are Usually Multiple Acids Move In and out Transporters (UMAMIT) (Besnard et al. 2016) or the CAT transporters (cationic amino acid) (Jungnickel et al. 2018).The SWEET transporters (Julius et al. 2017) carry sugars while organic acids use aluminum-activated malate transporter (ALMT) (Palmer et al. 2016).These carriers do not need to be attached to ATP to move through the plasma membrane, they use passive mediated transport.High-molecular-weight compounds (Table 1) use ATP dependent carriers such as ABC transporters and MATE (citrate); thereby passing through the plasma membrane by active transport.Once these compounds exit the plasma membrane, they move between cell walls of the cortex to the soil environment (Canarini et al. 2019).

Chemical signals influencing microbial community structure and function in the soil microbiome
Employing chemical communication, plants can actively structure their environment.Plants exude organic substances into the soil thereby stimulating the growth of microbial communities in the soil.These microbes utilize this carbon pool as their principal supply.Organic compounds that characterize the majority of the molecules exuded into the soil by plants are emitted through a process known as rhizodeposition (Guerrieri et al. 2019).
Root exudates possess biological and chemical influences on their immediate environment playing roles in nutrient acquisition and interaction with soil organisms.Chemical signaling between plants and other organisms inhabiting the soil is the biological effect of root exudates.Through recruiting defensive organisms upon infection by insects/ pathogens or attracting beneficial microorganisms for the enhancement of nutrient uptake, plants can modify their rhizobiome (Pascale et al. 2020).
There are favorable chemicals released by the root exudates to microbes in the rhizosphere are called phytohormones, these chemicals have a key role in regulating the physiology of microorganisms in the plant rhizosphere for plant development (Bedini et al. 2018).Some of these classical phytohormones include flavonoids, strigolactones, and salicylic acid.

Flavonoids
Flavonoids are a diverse group of hormones in plants that are involved in growth, development, and reproduction.The absence of these hormones does not result in the immediate death of plants but rather long-term impairment of survivability.Flavonoid solvency and versatility in the soil differs.While glycosylation improves their solvency in water, flavonoid glycosides are rapidly deglycosylated by microorganisms leaving the more hydrophobic aglycone (Slámová et al. 2018).Soil microorganisms use these plant glycosides as a source of energy and control the degrees of the bioactive aglycone (Biernat et al. 2018).This prompts the expansion in microbial community structure and function and increased plant development and advancement (Jacoby et al. 2017).Infected plants such as legumes, soybeans, and alfalfa use flavonoids as the first defensive mechanism at the site of infection (Noor 2023).Flavonoids can add to plant growth and development by fixing the plant structures and tissues by balancing auxin (IAA) action, which can prompt the differentiation of tissues, advancement of callus and tylose development, and closing of the vascular system to prevent pathogen disease.It has also been discovered that the over-application of fertilizers influences the production of flavonoids.Deng et al. (2019) demonstrated that the overapplication of nitrogen fertilizers in Cyclocarya paliurus decreases the production of flavonoids and results in the decrease of the plant growth and development.

Strigolactones
Strigolactones signal molecules are released by plants when there are nitrogen and phosphate deficiencies.They respond to the reaction of plants to environmental stress.Carvalhais et al. (2019) demonstrated that strigolactones shape microbial communities and functions in the rhizosphere.They reported that plants producing strigolactones have a major influence on fungal diversity compared to bacterial diversity relative to plants that do not produce strigolactones.They attract arbuscular mycorrhizal fungi for symbiosis with roots in approximately 80% of vascular plants to increase the uptake of the mineral nutrients like phosphate and they, in turn, receive carbohydrates leading to plant growth and development (De Cuyper and Goormachtig 2017).For instance, strigolactones are found in mosses, liverworts, and in the alga Chara coralline, where they advance rhizoid development.Strigolactones also attract rhizobia for nodulation where bacteria fix nitrogen in exchange for carbohydrates.According to Nelson (2021), strigolactones have disadvantages because they can activate seed germination in parasitic weeds.These seeds attach to the plant roots and then obtain nutrients from it.

Salicylic acid
Salicylic acid is believed to be a plant defence strategy against plant pathogenic fungi across different plant genotypes.However, it has been reported to also influence the establishment of bacteria from specific families in the rhizosphere (Veach et al. 2019).According to the study conducted by (Benjamin et al. 2022), it was shown that tomatoes (Solanum lycopersicum) emit salicylic acid, which serves a dual purpose of pathogen defence and facilitation of symbiotic associations with beneficial microorganisms such as mycorrhizal fungi.This suggests that salicylic acid contributes to microbial structure and function.Salicylic acid incites plant defence chemical in Populus in response to an infectious pathogen.Salicylic acid also induces stimulants that influence litter decomposition (Veach et al. 2019) and fungal endophyte colonization in other Populus species, promoting plant development (Omomowo and Babalola 2019).

Determination of microbiome by host
Root exudates show great variability among various plant species, growth stages, and even cultivars, inside various root developmental stages of individual plants and considering different biotic and abiotic stress factors (Adeleke et al. 2022b;Vieira et al. 2020).As a result of these differences, rhizobacteria with corresponding substrate uptake inclinations are chosen (Vieira et al. 2019;Zhalnina et al. 2018).
For instance, C 3 (three-carbon compound via the Calvin cycle) and C 4 plants (four-carbon compound via the Calvin cycle) show dissimilarities in the kinds of exudates discharged into the rhizosphere (Chen et al. 2016).Predominant sugars in the two kinds of plants contrast, with the secretion of maltose, mannose, and ribose by C 3 plants and inositol, erythritol, and ribitol in C 4 plants (Olanrewaju et al. 2019).C 4 plants (e.g.maize, sugarcane, sorghum) ooze higher quantities of organic carbon and amino acids due to high photosynthetic efficiency and absence of photorespiration while C 3 plants (e.g.wheat, rye, oats, rice, cotton, sunflower) produce less organic carbon during photosynthesis due to photorespiration (Olanrewaju et al. 2019).This suggests that the microbial functions and community structure in C 4 plants are much more abundant than those in C 3 plants.
The potential link between C4 plants, nitrogen fixation, and increased root exudation presents a compelling perspective on nutrient acquisition strategies.C4 plants are known for their efficient water usage and carbon fixation, but a recent investigation reveals that some may also fix nitrogen (Schlüter et al. 2023).C4 plants increase root exudation to attract nitrogen-fixing bacteria, which is consistent with rhizosphere interactions.In nitrogen-deficient conditions, this hypothesized method might help C4 plants improve their nutrient uptake and perhaps depend more on nitrogen fixation than C3 plants.This dynamic interaction shows how plants modify their relationships with microbes to improve nutrient availability, affecting plant ecology and agricultural practices (Aluko et al. 2023).
Genotypic varieties in plants may likewise change rhizosphere microbiome communities, however to an exceptionally less degree (Liu et al. 2019).It was exhibited that even plants that fall under the same carbon fixation metabolic pathway can create distinctive root exudates from one another.For instance, (Vaughan et al. 2013) reported that the diterpene rhizathalene A was constitutively delivered and discharged from the roots of A. thaliana (C 3 plants) while Xuan et al. (2016) showed that diterpene momilactone A is delivered and emitted from the foundations of O. sativa (C 3 plants) seedlings into the rhizobiome, the molecules released by these plants are antimicrobial agents.Endogenous developments control varieties in root exudate arrangements (Olanrewaju et al. 2019).
According to previous studies, it has been proven that different stages in plant development have different impact on microbiome (Compant et al. 2019).The microbial diversity and function at seeding stages are much more abundant than in other plant stages such as vegetative, plant bolting and flowering since the plant roots discharge more root exudates at early plant stages than in developed plants (Olanrewaju et al. 2019).Microbial communities in young plants grow rapidly and can use simple substrates produced by these young plants.As these young plants mature, the root exudates they release shape the microbial structure and function by attracting beneficial microbes that degrade more complex substrates and reject infection-causing microorganisms.This results in slower growth rates and the dominance of specific microorganisms (Alawiye and Babalola 2019).
The host genotype also determines root exudates that selects for specific microorganisms that could be beneficial for plant growth and development and inhibition of pathogenic microorganisms.Through the secretion of a wide variety of compounds, roots may influence the soil microbial community both emphatically and adversely (David 2023).According to Wu and Yu (2019), the effect of root exudates of Eucalyptus urophylla and Acacia mearnsii on soil microbes under simulated warming climate conditions directly affected the biomass of microorganisms.It also indirectly affected the soil microbial community structure by altering the composition and content of plant root exudates.

Effects of rhizosphere microbiome on plant growth and development
Various parts of plants harbor microorganisms that are structurally and functionally diverse e.g. the phyllosphere, endosphere, and rhizosphere microbiomes.Several taxa of microbes, such as bacteria, fungi, archaea, and viruses, occupy the rhizosphere of plants and this boosts the chances of interactions influencing nutrient dynamics affecting plant growth.The microbial community found in the rhizosphere play key roles in the growth and reproduction of plants (Garcia and Kao-Kniffin 2018;Lu et al. 2017).Through the production of phytohormones, such as auxins, cytokinins, gibberellins, and abscisic acid, the rhizosphere microbiome increases plant growth, protects against pathogens, and may help tolerate abiotic stresses like drought (Fadiji et al. 2023).Mutualistic symbionts and saprophytic microorganisms living at the root-soil interfaces are involved in nutrient cycling and the control of abiotic stress.Arbuscular mycorrhiza (AM) is an example of mutualistic symbionts and are also regarded as natural biofertilizers as they provide the host with water, nutrients, and pathogen protection, in exchange for photosynthetic products (Fasusi et al. 2023).AM establish beneficial interactions with most plant species by extending the root system to enhance nutrient uptake properties while saprophytic microorganisms are perceived for their ability to push nitrogen (N) fixation as well as phosphorus (P) rally; these two key procedures support plant development (Liu et al. 2018).According to a study conducted by Míguez-Montero et al. (2019), C. multiflorus, C. scoparius, C. balansae, and C. striatus leguminous species in water and phosphorus-deficient environment showed similar patterns of extending their root system when mineral nutrition was not sufficient in the soil to meet their physiological requirements.The rhizosphere microbiome also enhances stress resilience producing auxins, cytokinins, and gibberellins, increasing hormone levels in the host plant to intensify growth and development.
Microorganisms control diseases in plants through the inhibition of pathogenic microbial invasion by releasing antibiotics, lytic enzymes, or pathogen inhibiting volatile compounds (Compant et al. 2019).Different individuals from the rhizosphere microbiome can alienate soil-borne pathogens previously and during essential disease and optional spread on and in root tissues (Mhlongo et al. 2018).The rhizosphere microorganisms avert plant pathogens by antibiosis (Topolovec-Pintarić 2019) and opposition interference with quorum sensing affecting virulence and induced systemic resistance (Fleitas Martínez et al. 2019).

Mechanism of nutrient extraction from endosymbiotic microbes by plants
Endosymbiotic microbes refer to microorganisms that form a symbiotic association with a host organism, whereby they inhabit the host's cells or tissues and develop a mutually advantageous relationship (Sharma et al. 2023).Microbial endosymbionts offer their host plants a range of benefits comprising growth promotion, augmented disease protection, and enhanced tolerance against biotic and abiotic stresses.These endophytes promote plant growth by boosting nutrient acquisition.Certain plants are involved in 'nitrogen-transfer symbioses' is a in which plants partner with prokaryotes that fix nitrogen in connection with roots subsequently conveying nitrogen to plants e.g.actinorhizal and rhizobial symbioses (Martínez-Hidalgo and Hirsch 2017; White et al. 2018).In the context of phosphorus, arbuscular mycorrhizal fungi (AMF) enable plants get phosphorus.This symbiotic interaction allows the fungus to extend hyphae into the soil and release enzymes that break down insoluble phosphorus molecules, making it more available to plants (Agbodjato et al. 2022).In a similar vein, plants use the strategy of releasing siderophores into the rhizosphere to facilitate the uptake of iron.These siderophores act as chelating agents, effectively binding to iron ions and therefore increasing their solubility and accessibility for plant absorption (Roskova et al. 2022).This mechanism enhances the capacity of plant roots to effectively absorb iron, which is essential for several physiological functions.Collectively, these tactics highlight the ability of plants to interact with microorganisms as cooperative partners in mitigating nutritional deficiencies and enhancing overall development and well-being (Singh et al. 2022).In nutrient-limited soils, the discharge of exudates by plants intensifies.This increase in exudation possibly enhances the activities of microorganisms around plant roots and boosts the 'microbial mining' of nutrients.The cultivation of microbial communities' upsurges through the excretion of more exudates by plants under nutrient-limited conditions.Plants can be deemed to be 'farming' microbes by the emission of exudates (Jacoby et al. 2017).The rhizophagy cycle is an emerging ecological phenomenon where plants uptake bacteria or fungi as endophytes from the soil, subsequently utilizing reactive oxygen species (ROS) oxidation to break down these microorganisms (Fig. 1) (Verma et al. 2022).Rhizophagy involves the use of root exudates to enable bacteria enter root cells and survive and reproduce in plant tissues (Chiaranunt and White 2023).Plants produce ROS as a reaction to the presence of endophytes.ROS are highly reactive molecules that activate oxidative processes, leading to the degradation of endophytes and the subsequent release of nutrients, including nitrogen and phosphorus (Adeleke et al. 2022a).The assimilation of these nutrients supports the plant's development.Some bacteria, such as Klebsiella implicated in the rhizophagy cycle, have been reported to fix atmospheric nitrogen, while others lack this nitrogen-fixing ability.These bacteria that are unable to fix nitrogen, e.g., some species of Bacillus, only need to have proficiency in nutrient obtention from the rhizosphere by foraging from fungi, plants, or bacteria (Singh et al. 2018;White et al. 2018).Nutrient solubilization in the rhizosphere is made possible through the action of some symbiotic microorganisms and these solubilized nutrients can be taken up into the roots by root hairs.Bacteria linked to roots are usually capable of motion and can leave the plant root to obtain nutrients from the soil.They are also able to return to the plants to get supplementary carbon and nutrients from root exudates.Bacteria seem to be perfect transporters of micronutrients that are needed for the growth and development of plants.All nutrients obtained or produced by bacteria can be oxidatively mined from them through the process of rhizophagy (Verma and White 2019).

Perspectives in agriculture: synthetic fertilizers and plant root-soil microbe communications
Various interacting factors can influence the structure of microbial communities in the soil.Farm management practices including fertilization, crop rotation, and tillage modify soil physicochemical properties thereby impacting microbial diversity and community composition (Nwachukwu et al. 2023).
The microbial community composition of conventionally managed systems varies from that of organic systems (Amoo and Fig. 2 The rhizosphere of the natural system vs that of artificial systems.The rhizosphere of the natural system: Plant roots release exudates which act as chemoattractant or repellent signalling to microorganisms in the rhizosphere.The cross-domain and cross-kingdom quorum-sensing system remains normal, resulting in the growth and production of healthy plants and increased crop yields.The rhizo-sphere of the artificial system: Plant roots release exudates that act as chemoattractant and repellents to microorganisms in the rhizosphere.The cross-domain and cross-kingdom quorum-sensing system decreases which result in poor growth and development thereby leading to reduced crop yields Babalola 2019).Concerning management, the influence of plants on microbial communities extends taxonomy, the network structure is also affected.Through alterations in pH instigated by synthetic fertilizers, soil acidification which implicitly enhances the abundance of acid-tolerant taxa may occur thereby influencing the structure of microbial communities.This could also trigger the alteration of the relative abundance of certain taxa (Li et al. 2017;Schmidt et al. 2019).
Towards meeting the food demand of an ever-increasing population, there is an over-application of synthetic fertilizers in most cases.When synthetic fertilizers are administered to soils, they get absorbed by plant roots thereby increasing crop yield (Chandini et al. 2019).It has been reported that the quorum-sensing system between the cross-domain and cross-kingdom microorganisms responds to environmental nutrition status.Over-fertilization results in the decrease of microbial communications thereby affecting the coordination of the microorganisms between cross-domain and crosskingdom.The motility, virulence, and biofilm formation also get affected resulting in a decrease in the microbial community (Fig. 2) (Paluch et al. 2020).

Conclusions and prospects
The intricate interactions between plant roots and their associated complex microbial communities can stimulate plant growth and development.Through the secretion of bioactive molecules into the rhizosphere by plants, the soil microbiome may be influenced resulting in the steering of plant-soil reactions by these root exudate metabolites.Due to the ever-increasing human population, more demand has been placed on food production and this has led to synthetic fertilizers being overused by some farmers.Escalating fertilizer application can alter the accessibility of nutrients crucial for plant growth.Plants can structure their environments using chemical communication through root exudates.These exudates are involved in the nourishment and development of plants and the signaling of molecules that facilitate communication in the rhizobiome.The effects of root-associated microbial communities on plant health and development have been emphasized by several studies and it is of utmost importance to understand the communication between plant roots and the soil microbiome.Such information could lead to an improvement of cultivating techniques that help in the maintenance of advantageous microbial communities and reduction of pathogenic microorganisms in the rhizosphere consequently resulting in enhanced plant growth and development.

Table 1
Composition of root exudates polysaccharides or long chains of sugar molecules develops a symbiotic relationship with the soil-dwelling fungi Proteins (HMWC) chitinases, glucanases, myrosinases Responsible for effective pathogen defense