Communication between Plants and Rhizosphere Microbiome: Exploring the Root Microbiome for Sustainable Agriculture

Plant roots host numerous microorganisms around and inside their roots, forming a community known as the root microbiome. An increasing bulk of research is underlining the influences root-associated microbial communities can have on plant health and development. However, knowledge on how plant roots and their associated microbes interact to bring about crop growth and yield is limited. Here, we presented (i) the communication strategies between plant roots and root-associated microbes and (ii) the applications of plant root-associated microbes in enhancing plant growth and yield. This review has been divided into three main sections: communications between root microbiome and plant root; the mechanism employed by root-associated microbes; and the chemical communication mechanisms between plants and microbes and their application in plant growth and yield. Understanding how plant root and root-associated microbes communicate is vital in designing ecofriendly strategies for targeted disease suppression and improved plant growth that will help in sustainable agriculture. Ensuring that plants become healthy and productive entails keeping plants under surveillance around the roots to recognize disease-causing microbes and similarly exploit the services of beneficial microorganisms in nutrient acquisition, stress mitigation, and growth promotion.


Introduction
The orthodox methods of attaining improved agricultural output are not environmentally sustainable. For instance, the superfluous and prolonged application of artificial agrochemicals results in soil nutrients depletion and water pollution as well as environmental degradation [1]. If nothing is done to mitigate the effect of the excessive and prolonged use of agrochemicals, coupled with the human population predicted to hit 9.9 billion by 2030, there will be a decline in the amount of food resources available to feed the world [2]. Hence, sustainable agricultural practices like the use of biological materials is a necessity for restoring soil fertility, feeding the ever-increasing population, and improving the agroecosystem resilience [3].
Plant microbiome nexuses could provide a prospect to develop schemes for sustainable agricultural practices [4]. Plants take up water and nutrients through the root system, which is inhabited and bounded by a multifaceted microbial community referred to as the root microbiome [5]. The root microbiome is a significant driver for plant yield, health, and ecosystem functioning because it is the intersection point between a plant and the ecosphere [6]. Furthermore, it serves as a receptacle of extra genes that plants can acquire when required [7]. The root microorganisms are recruited from several microorganisms found in bulk soil, which is the basic factor influencing the composition of the root microbiome [8]. It is also vital to note that the plant genotype also contributes to the final composition  Understanding the concept and relevance of the root microbiome to plant health will improve our insight into the colossal power of these tiny giants in ecosystem function. In found in bulk soil, which is the basic factor influencing the composition of the root microbiome [8]. It is also vital to note that the plant genotype also contributes to the final composition of these societies because plant-resultant substrates and exudates give the nutrient and physical niches of the rhizosphere [9]. These microorganisms form complex links that are established and controlled via antagonism, competition, nutrient cycling, and chemical communication facilitated by various groups of signaling molecules (Figures 1  and 2) [10].  Understanding the concept and relevance of the root microbiome to plant health will improve our insight into the colossal power of these tiny giants in ecosystem function. In Understanding the concept and relevance of the root microbiome to plant health will improve our insight into the colossal power of these tiny giants in ecosystem function. In recent years, research has focused on the composition and the structure of root microorganisms [11]. However, the multifarious communications between the root microbiome and the host are not entirely understood. These interactions could facilitate the release of elicited the root-specific transcription factor MYB72 and further led to the production and emission of MYB72-controlled β-glucosidase BGLU42-reliant scopolin and scopoletin, respectively, resulting in a well-established niche for microbial consortiums and resistance profits for the host plant against Verticillium dahlia and Fusarium oxysporum (soil-borne fungal pathogens). Bacterial assemblages connected with plant roots contribute a vital role in subduing soil-borne pathogens, and multispecies probiotic associations could boost disease suppression efficiency. For example, Hu, et al. [30] reported that the addition of Pseudomonas consortia in Solanum lycopersicum rhizosphere microbiome reduced Ralstonia solanacearum concentration and lessened the disease incidence because of the meddling and increased resource competition with the pathogen. Similarly, an increase in the Pseudomonas consortia richness resulted in increased plant biomass and effective absorption of nutrients in Solanum lycopersicum plants.
Root-related microbes likewise produce communicating compounds ranging from antibiotics, organic acids, volatile signals, phytohormones, extracellular enzymes and quorum-sensing molecules (QSMs) (Figure 2) [31]. These compounds aid the relationship between plant roots and microbes associated with facilitating plant growth. For instance, Nacyl-L-homoserine lactones (quorum-sensing molecules) were reported by Ortiz-Castro [32] to influence the lateral root formation, root system architecture, primary root growth, and root hair development of Arabidopsis thaliana in their post-embryonic stage. Bacterial strains such as Bacillus amyloliquefaciens L3 use communicating molecules like volatile organic compounds to stimulate reactions in fungi and plants and generate induced systemic resistance (ISR) in plants, consequently the eliciting expression of defense genes that mitigate the negative effect of viruses, oomycetes, bacteria, and fungi on plants [33][34][35][36]. Root-resultant exudates, apart from aiding plant fitness and longevity, also benefit microorganisms that use them as a resource (carbon-rich products with other nutrients) that supports microbial multiplication [37][38][39].
Alongside different rhizodeposits produced in the rhizosphere, different hormones are also produced that aid plant-microbe communication cascades [18]. These hormones include abscisic acid, auxin, cytokinins, gibberellin, and peptide hormones that regulate plant growth and development. Several plant growth-promoting rhizobacteria have been reported to produce indole acetic acid in a chemically defined medium with tryptophan precursor [40,41]. Auxin production enhances seed germination, nutrient uptake, and root growth and development [18,42]. For instance, cytokinin was found to stimulate cell division, inhibit root elongation, and affect root hair development [43], while gibberellin was reported to alter many physiological and developmental processes in plants by promoting seed germination, stem elongation, flowering, and fruit setting in plants [44]. Gibberellin also facilitates cell-to-cell communication [18].
In the past, microbial ecologists used to face big challenges in investigating multifaceted microbial societies. However, today the tide has changed thanks to methodological advances like the high throughput deoxyribonucleic acid sequencing machinery that provides comprehensive information on the composition and structure of microbial groups [45][46][47]. With the availability of many sequence datasets from environmental samples, the focus now is to go beyond alpha and beta diversity and look more at the interactions between microbial taxa and their host [48,49]. To obtain a more profound understanding of plant-root-microbe interactions, new tools are being developed. For instance, exometabolomics have been developed to dissect cross-feeding between root microorganisms and plants when root exudates serve as the only carbon source for the cultivation of the rhizosphere microbes [50]. With this tool, it is now possible to know the main compound controlling plant-bacteria communications by comparing exometabolite datasets [51]. Another available tool is the synthetic microbial communities (SynComs) approach, which is used to expound and predict outputs caused by particular characteristics of bacterial consortia [52]. This SynComs approach was used by Lebeis, et al. [53], who revealed that the defense phytohormone salicylic acid modulates bacterial colonization of the roots of Arabidopsis. These available tools allow us to unknot the entangled networks of interactions of fundamental microbiomes or holobionts for efficiently using the root microbiome to intensify crops' nutrient procurement and fight against biotic and abiotic stress [54].

Chemical Communication Mechanisms between Plants and Microbes and Their Application in Plant Growth and Yield
Microorganisms use processes like enzymes release, induction of systemic resistance in host plants, antibiosis, and rhizospheric competence to stimulate plant-microbe communications, and these processes originated from chemical signaling [55]. Distinct chemical signal molecules produced by different microbes influence biofilm growth, sporulation, motility, conjugation, virulence, antibiotic production, and symbiosis as well as alter the soil pH and the microbial community [56]. Most of these chemicals are used to induce tolerance against biotic and abiotic stress. Cho, et al. [57] reported that Pseudomonas chlororaphis O6 produced 2R, 3R-butanediol in the presence of jasmonic acid, ethylene, and salicylic acid signaling pathways, increasing the tolerance to drought in Arabidopsis thaliana by increasing the proportion of closed stomata. Another study revealed that under salt stress conditions, Pseudomonas simiae strain AU produced volatile organic compounds that provided salt tolerance in soybean plants by decreasing sodium ion and increasing the amount of potassium and phosphorus content [58]. Their investigation further revealed that proline and chlorophyll content increased in the plant roots exposed to volatile organic compounds released by Pseudomonas simiae strain AU [58]. Some chemicals produced by microbes have the ability to activate a chain of physiological alterations that stimulate plant growth [59]. del Carmen Orozco-Mosqueda, et al. [60] reported that the release of dimethylhexadecylamine by Arthrobacter agilis UMCV2 increased iron obtainability in Medicago truncatula. This became possible due to (i) the dimethylhexadecylamine released by Arthrobacter agilis UMCV2 stimulating acidification in the root biome. (ii) This then promoted proton extrusion under an iron deficit. (iii) Finally, it led to an increase in ferric reductase activity. Fungal colonization primes the chemical protection development in plants by increasing the levels of fatty acid derivatives, alkaloids, terpenoids, and phenylpropanoid polyamine conjugates in plants; these compounds are emitted to prevent pests [61,62]. The plant root-associated microbes in mitigating abiotic and biotic stress, nutrient acquisition, and growth promotion must be promoted to enhance sustainable agriculture [63,64].

Root Microbiome Role in Abiotic Stress Tolerance
Crops are often exposed to physical stresses such as soil salinization, submergence, extreme temperatures, nutrient imbalances, and drought, to mention a few [65]. The fact that these stresses will intensify in the coming years makes them a big concern as plant growth, yield, and productivity will be hindered. To overcome these abiotic stresses, plants must undergo adaptive modifications or solicit the help of beneficial microbes to live and promote plant function [46,66]. Root-associated microbes can stimulate growth and defend the host via many molecular machinery in abiotic stress circumstances (Table 1). Ribeiro and Cardoso [67] revealed that strains of Bacillaceae, Enterobacteriaceae, and Pseudomonadaceae isolated from the Araucaria angustifolia root were tremendous plant growthpromoting bacteria. Some of these bacterial strains are P-solubilizing microbes that help the crops tolerate drought, salt, and extreme temperature conditions through the production of numerous phytohormones, antioxidants, and exopolysaccharides; the production of 1-aminocyclopropane-1-carboxylate deaminase; the enrichment of nutrient uptake; the production of many volatile compounds; and the initiation of the buildup of osmolytes. They also help in the regulation of stress-responsive genes [68,69]. Under drought settings, Yuwono, et al. [70] found that osmotolerant rhizobacterial inoculated with rice increased root and shoot dry weight. It was also proven that under stress conditions, these isolates produced betaine, signifying that the drought tolerance was because of the increase in osmolyte. They also revealed that the rhizobacteria-plant interaction led to indole acetic acid production. An under-drought experiment conducted by Ruiz-Lozano, et al. [71] showed that co-inoculation of Glomus mosseae and Bradyrhizobium japonicum in drought-stressed soybean plants resulted in increased leghemoglobin content, acetylene reductase activity, and protein content by 25%, 112%, and 15%, respectively, compared with well-watered soybean plants and plants colonized by Bradyrhizobium alone.
Root-associated microbes also use other strategies to retain ion homeostasis in plants facing salt stress. For instance, bacterial exopolysaccharides fix Na + and confine Na + inflow into the roots. They produced volatile organic compounds (VOCs) during stress conditions so that VOCs can activate high-affinity K + transporter (HKT1) reduction in roots and stimulate HKT1 in shoots, thereby restraining Na + entrance into roots and easing shoot-to-root Na + retransmission. The K + /Na + ratio is increased by arbuscular mycorrhizal fungi by immensely improving Ca 2+ and K + absorption and eluding the movement of toxic Na + under salty conditions. Furthermore, for effective water assimilation in saline-strained plants, roots' closely associated microbes control the processes of genes encrypting the plasma membrane integral proteins to aquaporin activity [72][73][74]. Boosting the antioxidative systems in plants for ROS (reactive oxygen species), scavenging, and producing polyamines and proline are among the mechanisms employed by root-associated microbes in mitigating salt stress in plants. Bano and Fatima [75] induced salt stress conditions and co-applied Pseudomonas and Rhizobium at the seedling stage of maize. Their findings showed that under sodium chloride conditions alone, a harmful effect on maize growth and development was observed. Furthermore, improved sodium chloride tolerance of maize upon co-inoculation with Pseudomonas and Rhizobium is linked with reduced electrolyte leakage, increased proline production, and conservation of leaf water contents. The improvement of nutrient uptake to boost plant survival under salt conditions is another mechanism employed by root-associated microbes. For instance, the introduction of Bacillus aquimaris to wheat plants resulted in a substantial rise in phosphorus, nitrogen, and potassium in wheat leaves (Upadhyay and Singh 2015). The root-associated microbe can also aid plants in withstanding high-or low-temperature conditions, either by increasing or decreasing anthocyanin, proline, and sugar contents. Barka et al., [76] reported that under low temperatures, grapevine plant bacterized with Burkholderia phytofirmans strain PsJN increased physiological activity and grapevine growth through a substantial increase in proline, starch deposition, carbohydrates, and phenol contents compared with the control.

Root Microbiome Role in Nutrient Acquisition
Most micronutrients and macronutrients important for plant growth are available in the soil in insoluble forms. Plants devise several mechanisms for the acquisition of these nutrients in the soil. The plant root microbiome enhances the uptake of major micronutrients by mineralizing or solubilizing them and ensuring their bioavailability through acidification [85,86], secretion of hydrolytic enzymes such as phytase or phosphatase, excretion of proton, and production of siderophore [87]. Endophytes, rhizospheric microbiomes, and arbuscular mycorrhizal fungi (AMF) help the plant in the acquisition of nutrients from the soil through the solubilization of nutrients such as sulfur (S), potassium (K), calcium (Ca), iron (Fe), zinc (Zn), and phosphorus (P) [88][89][90]. Some notable root microbiome genera associated with maize, wheat rice, and legumes, such as Streptomyces, Pantoea, Citrobacter, Azospirillum, Bacillus, Herbaspirillum, Achromobacter, Gluconacetobacter, Burkholderia, Chryseobacterium, Bacillus, Klebsiella, Azotobacter, and Pantoea, have been reported to enhance plant development and growth via the uptake of micronutrients and stimulate the development of plant roots [91][92][93][94]. Siderophores secreted by endophytes aid plants' iron uptake from the soil; this is because iron cannot directly penetrate the plant cell even through transporters [95]. Root endophytes, such as Azoarcus, Herbaspirillum, Acetobacter, and diazotrophicus, have been reported to be active in nitrogen fixation. Some diazotrophic endophytic microbial communities, such as Bacillus, Gammaproteobacteria, and Actinobacteria, have been largely reported as atmospheric nitrogen fixers in rice [95][96][97]. Rhizobia, most importantly, Burkholderiales, form root nodules with legumes, which convert atmospheric nitrogen into ammonia, which is readily available to the plant, while the plant, Microorganisms 2023, 11, 2003 8 of 15 in return, produces carbon compounds [98,99]. Some root microbiomes such as Brevibacillus, Kineococcus, Microbacterium, Rhizobium, Burkholderia, Nocardia, Bacillus, Rhodococcus, Methylobacterium, Mesorhizobium, and Paenibacillus associated with Eucalyptus plant have been reported to be involved in the fixing of nitrogen [95,100]. A summary of other studies on the nutrient acquisition attributes of some plant root microbiomes is presented in Table 2.

Root Microbiome Role in Disease Suppression/Biocontrol
Insects and pathogens attack plants and retard their yield, growth, and health. However, plant root microbiomes have been reported to be a reservoir of many bioactive metabolites that can protect and enhance plant resistance against attacks from pathogens and pests [95]. Phyllospheric microorganisms isolated from different plants showed that an abundance of Firmicutes is capable of secreting volatile organic compounds active in the protection of crops from several fungal and bacterial pathogens/diseases [119]. The plant root microbiome protects the plant through induced systemic resistance (ISR) or antibiosis from insects, pathogens, and herbivores. Siderophores, antibiotics, salicylic acid, N-acyl homoserine lactones, lipopolysaccharide, jasmonic acid, and flagella secreted by endophytic bacteria have been reported to be capable of inducing systemic resistance in plants [120]. In addition, endophytic fungi, majorly of the phyla Glomeromycota, Basidiomycota, Ascomycota, and Zygomycota, are capable of secreting inhibitory compounds, some of which are terpenoids, polyketones, phenols, chlorinated compound, alkaloids, peptides, steroids, and flavonoids, which aid the protection of plants from insects, pathogens, and herbivores [121]. Actinomycetes have also been widely studied due to their ability to secrete notable antimicrobial compounds active against plant pathogens. Streptomyces spp. secretes many antimicrobial compounds such as indolo-sesquiterpene antimicrobial compounds, munumbicins, coronamycin, and kakadumycins [95,122,123]. Studies have also revealed that siderophore can induce ISR in plants and enhance biocontrol activities. For example, strains of endophytic methylobacterium successfully suppressed Xylella fastidiosa (a pathogen responsible for chlorosis in citrus trees) via siderophore production [63]. Rhizobiomes such as Actinobacteria, Proteobacteria, and Firmicutes have been linked with the inhibition of Rhizoctonia solani, which commonly attacks sugar beet [95], while Gammapro-teobacteria have also successfully inhibited the disease via non-ribosomal peptide synthesis (NRPS) [124]. A high abundance of bacteria such as Streptomyces, Bacillus, Paenibacillus, and Rhizobium in the root microbial community of cucumber was cultivated and monitored in suppressive soil [125]. A summary of similar studies on the biocontrol attributes of some plant root microbiomes is presented in Table 3.

Conclusions and Future Prospects
It is evident that plant-microbe signaling cascades are essential regulators of plant development and growth, and these signal molecules can alter the morphology and physiology of the host plant. Plants develop complex interactions and communicate with various microbes in their rhizosphere through different signals that affect plant growth and modulate the plant-specific core root microbiome. These signals, secreted by microand macro-symbionts, can enhance root development, increase nutrient and water uptake, and promote tolerance to biotic and abiotic stresses. As a result of the roles that plant growth-promoting organisms played in improving plant growth and yield, the role of plant-microbe signals in sustainable agriculture and the recovery of marginal lands cannot be overemphasized. It is, therefore, important to focus future research on the understanding of intra-and inter-communication that can lead to the identification of more signal molecules and similarly improve plant growth and development. There is a need to develop efficient technologies for isolating and identifying signal compounds useful for sustainable development.