Introduction

Globally, diverse oilseed crops are cultivated for edible oil production to safeguard humans from malnutrition and related illnesses [1]. Their production rate differs from one country to another due to adaptation and growth under different weather conditions by region (e.g., temperate, tropical, and subtropical) [2]. The major type of oilseed crops are canola, groundnut, palm oil, sunflower, soybean, peanut, rapeseed, and cottonseed [3]. In 2020/2021, statistics of USDA showed an account of 362.05 soybeans, 68.87 rapeseed, 49.46 sunflower seed, 47.79 peanuts, and 41.80 of cottonseed, 19.96 palm kernel, and 5.75 copra world oilseed production (million metric tons) with soybean estimated of about a 90% production in the USA [4]. Also, in Sub-Saharan Africa, Nigeria produces and exports a larger percentage of soybean annually.

Soybeans are leguminous plants in the family Fabaceae. Interest in soybean cultivation relies on their economic value, the edible oil-producing potential of about 20%, and protein content of 20–25% [5]. Notably, soybeans serve as an inexpensive and excellent source of high-quality edible oil and protein for humans as compared to other leguminous crops and animal protein [6], and can be a supplement food source for livestock. Yet, soybean’s market value and maximum utilization are less explored in many countries [7]. Soybean can be processed into composite food products, substituting animal proteins, i.e., eggs, meat, and milk.

The uncertainties and challenges facing soybean cultivation may include poor and inefficient farming systems, drought, disease invasion, pest attack, lack of disease-resistant cultivars, etc. [8,9,10]. Diseases such as stem and root blight, bacterial leaf blight, downy mildew, bacterial pustule, rust, purple seed stain, frog-eye leaf spot, brown spot, charcoal rot, and soybean mosaic virus are the most common peculiar to soybean [11]. The control of disease in plants and crops under storage can be achieved by either biological, chemical, or physical means. Therefore, adopting proper control measures against phytopathogens in soybean can sustain plant health and crop productivity.

From antiquity, farmers adopted diverse cropping systems (crop rotation, mixed farming, organic farming, etc.) and agricultural practices (e.g., agrochemicals, irrigation, and harrowing) to mitigate bottlenecks limiting the cultivation of soybean and other food crops. Over time, agrochemical use has been a major concern to environmentalists, ecologists, and microbiologists due to the negative impact on the ecosystem [12, 13]. The peculiarity of these challenges is not limited to soybean cultivation alone, but other economical food crops.

In recent times, research efforts are on the increase to devise a sustainable means of improving soybean, and other food crop production in order to help solve food scarcity, hunger, and malnutrition [14]. Because of the environmental threats posed by the synthetic fertilizer application and the incessant population increase, the need to employ biorational approaches and sustainable measures to enhance soybean production has become imperative. Naturally, soybean houses endophytic microbes capable of increasing the nitrogen pool in the soil to enhance plant nutrition for higher productivity [15]. The natural occurrence of these nitrogen-fixing bacteria is a promising way to reclaim lost soil nutrients for food production to meet the demand of the ever-growing population and relieve farmers of the cost and over-dependence on chemical fertilizers by farmers. Thus, harnessing endophytic bacteria as bioinoculants to oppose chemical fertilizers is critical as the best alternative.

The plant root endosphere represents discreet regions occupied by diverse, endophytic microorganisms [16], where these microbes exhibit mutualistic, neutral, or antagonistic relationships with the host plants. The emphasis on the root-associated bacteria will be most considered in this review, as soybean root nodules naturally contain diverse nitrogen-fixing bacteria (NFB) [17]. The complementary effects of root-associated bacteria and root nodule NFB can positively influence plant growth and survival under nitrogen-limiting soils [18]. Here we emphasize that the nitrogen-fixing potential of endophytic bacteria in leaves, stems, seeds, flowers, ovules, etc. may be of greater importance in plant growth when compared to root nodules NFB only. Nevertheless, comparative studies of these bacteria from various plant organs upon inoculation under greenhouse and field experiments are required to ascertain this claim, requiring further studies.

The molecular insights into plant–microbe interactions have unveiled important functions of some endophytic microbes, which suggests their maximum exploration as bioinoculants in sustaining plant growth and health [19]. For instance, a few beneficial nodule endophytic microbes associated with soybeans have been assessed under greenhouse and field trials to enhance soybean yield and in vitro screening for their antimicrobial properties against phytopathogens [20].

The interdependence of endophytic bacteria with the host plants confers beneficial effects in soybeans and other food crops, such that it stimulates plant growth promoters, antibiosis activity against phytopathogens for plant health, defense against oxidative stress, and yield enhancement without any pathogenic effects [21, 22]. Limited information is available in the literature on the plant growth stimulation and biocontrol potential of endophytic bacteria inhabiting soybean, thus limiting their ecological services. Nevertheless, exploring endophytic bacteria as bioinoculants can provide several opportunities in mitigating diverse agricultural problems, such as biotic and abiotic stress, and climate change. Furthermore, addressing the challenges and uncertainties limiting plant microbiome biotechnologically will ultimately reveal the amazing realities of incorporating endophytic resources from soybean and other food crops into agricultural management. Our review brings to light the endophytic microbial dynamics of soybeans and current status of plant microbiome research for sustainable agriculture.

The Soybean Microbiome

It is essential to evaluate the diversity and population of endophytes in soybean plants in different environments, as a knowledge of this would serve as a background to promote their usage as biofertilizers, soil amendments, plant growth enhancers, and biocontrol agents with the overall aim of increasing different plant yield. Despite the success recorded in soybean’s endophytic microbiome research with promises to achieve future agricultural productivity [10, 15, 23], there is still a need for further studies. Sustaining plant health is paramount, as it is relatively mirrored in crop yield. The antimicrobial compounds and metabolites naturally found in economical plants, coupled with the biocontrol potential of some endophytic microbes, can contribute to plant health by reducing plant pathogenicity [24]. Inefficient control of plant pathogens results in yield loss to crops [25]. To help ameliorate these threats, in vitro screening of novel endophytic bacteria from economic plants for antimicrobial activity became important in identifying targeted biocontrol agents to specific pathogens in the host plants [26].

Taking account of key certain environmental factors that influence microbial community structure by monitoring different ecological niches is vital to ascertain specific environmental factors influencing microbial diversity in plants. For instance, in the phyllosphere, a limited supply of nutrients, ultraviolet light, humidity, temperature, oxygen concentration, pH, etc. influence the microbiome in this niche [27]. In the root endosphere, pathogens, nutrient deposition, and versatility might be key factors influencing the diversity of the microbes in different plants. The effect of ultraviolet “B” has been reported to influence the bacterial community structure in the soybean phyllosphere [28]. The factors (geographical location, carbohydrates, amino acids, and other soil nutrients) influence the microbial diversity in the root endosphere [29]. The soil-inhabiting microbes and some phyllosphere endophytic microbes can withstand high ultraviolet radiation due to the presence of pigments, i.e., melanin, xanthomonadine, and carotenoids [30]. The microorganisms found in the same ecological niche can be differentiated based on their characterization, genetic composition, and metabolic activities [30].

Plant endosphere ecology comprises microbial domains found in the below (root, sometimes seeds) and above (stem, leaf, seed, flower, and ovule) plant parts [31]. The microbial population and diversity in the plant root may be dissimilar compared to the other plant parts. The root endophytes are influenced by the exudate-secondary metabolites released into the soil-root environment [32]. Mina, Pereira, Lino-Neto, and Baptista [33] stated that the endophyte diversity in the different organs of a particular plant is mediated by the physical and chemical properties. This claim was relative to soybean as de Almeida Lopes, Carpentieri‐Pipolo, Oro, Stefani Pagliosa, and Degrassi [34] observed a similarity in the diversity of microorganisms in soybean.

Endophytic Bacteria Associated with Soybeans

Studies on the functional traits exhibited by endophytic bacteria associated with soybean and Arabidopsis aim to reveal their significance in agriculture, industry, and medicine [15, 35]. The effects of some endophytic bacteria from legumes and other food crops on plant growth are presented in Table 1. Hence, the advantages of beneficial endophytic bacteria (e.g., plant production, growth, secondary metabolites) found in different food crops from various plant habitats remains crucial in plant growth promotion, inducing plant tolerance to harsh environmental conditions and disease control. These researchers reported Citrobacter freundii and Enterobacter asburiae from the root and stem; Kosakonia cowanii, Pantoea agglomerans, and Variovorax paradoxus from the root and leaf; Staphylococcus aureus from the stem and leaf; and Enterobacter ludwigii from the root, stem, and leaf of soybean. Likewise, Dubey, Saiyam, Kumar, Hashem, Abd_Allah and Khan [15] and Brunda, Jahagirdar, and Kambrekar [36] also isolated Bacillus pumilus from the stem and leaf of the soybean plant, which aligns closely with the claims of de Almeida Lopes, Carpentieri‐Pipolo, Oro, Stefani Pagliosa, and Degrassi [34], who observed similar bacterium in different organs of soybean. Hence, it is crucial to carry out more research to have a deeper understanding of the inherent factors affecting the diversity of endophytes in different plant parts for maximum exploration in solving agricultural problems.

Table 1 Effects of some endophytic bacteria from legumes and other food crops on plant growth
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The selection of endophytic bacteria based on taxonomy and functions can help understand diverse bacteria communities in different plants [37]. Plants of the same species may have different bacteria compositions and associations, depending on the location, genotype, cropping system, climatic conditions, and growth stage [38].

The genomic data available on the microbes from soybean with unique metabolic features reveal their genetic variation. The notable genes involved in flagella biosynthesis (flg, fil, flh), chemotaxis (cheABRVWZ, mpc), IAA synthesis (trpABCDE), nitrogen fixation (iscU), and phosphate solubilization (pstABCS) identified in the genome of Pseudomonas fluorescens BRZ63 isolated from rapeseed may be responsible for the bacterium functions in enhancing plant growth and disease control [39]. A study by Adeleke, Ayangbenro, and Babalola [40] reported genes involved in nitrogen fixation, phosphate transport and solubilization, siderophore production, secretion systems, iron transport, flagella, flagella biosynthesis, and phytohormones in the genome of endophytic Bacillus cereus T4S isolated from sunflower, which enhanced sunflower yield. Furthermore, studies should also be intensified on soybean to unravel the genes in their different endophytes, enhancing plant growth.

Plant–microbe cooperation can modulate the transfer of certain genetic traits in the host plant by genome modulation, which may assist plants in acquiring novel traits and in boosting their adaptation mode of actions in diverse environments. The level of genetic communication in the root-soil interface facilitates microbial infiltration into the plants [41]. However, the similar genetic complexity between rhizosphere microbes and endophytic microbes provide new insights into their colonization pattern into the root endosphere and become endophytes [42]. Therefore, the mechanisms employed by soybean endophytic microbes in plant growth promotion need to be understood to ascertain their roles in the plant endosphere.

Endophytic Fungi Associated with Soybean

Providing information on endophytic fungi (EF) inhabiting the root of soybean can help unravel the prospects of soybean in sustainable crop production. The plant growth–promoting attributes of bacteria and fungi inhabiting the root of plants may share significant similarities depending on the sample type, isolation source, and growth conditions [43, 44]. EF employs multifunctional strategies for plant growth and protection against biotic and abiotic stressors [45]. Unraveling the community structure and complex plant–microbe synergies in the host plants has made the science of endophyte interesting as a way of maximizing their bio-products (bioinoculants) to ensure food security [46, 47].

The EF which forms part of plant lifestyle with a strong affinity in the root endosphere due to the presence of cell organelle (mycelia) can be explored in agriculture [48,49,50]. Despite the ecological services of plant-associated EF, there is still a need to further investigate EF associated with soybean. For instance, the biocontrol potential of EF isolated from rapeseed against Botrytis cinerea and Sclerotinia sclerotiorum, which causes gray mold and Sclerotinia stem root, has necessitated further their exploration [51]. A study by Sallam, Ali, Seleim, and Bagy [10] reported antagonistic activity of the endophytic fungus Trichoderma spp. isolated from the soybean against Rhizoctonia solani, which reduces their effect on soybean yield under greenhouse experiments. Other research findings (to mention but a few) on the plant growth promotion and antifungal attributes of EF against plant pathogens were evident in literature due to phytohormone and metabolite secretions [25, 51,52,53].

The biotechnological potential of diverse EF in the production of therapeutic agents and antibiotics revealed their beneficial effect on plant immunity and growth enhancement [54]. The mechanism of action and factors influencing the diversity of root-associated endophytic bacteria and root-associated EF may be similar, possibly based on the same source of identification. Some identifiable EF isolated from the root, stem, and leaves of soybean with detailed biological activities for sustainable plant health includes Trichoderma asperellum, T. longibrachiatum, and T. atroviride [10], Colletotrichum spp., Pestalotiopsis spp., Botryosphaeria spp., Diaporthe spp. [55], and Fusarium, Alternata [56]. Despite their multifaceted attributes in plant growth promotion, disease suppressiveness, stress alleviation, metal reduction, and nutrient mineralization [57,58,59], there is still a need for more studies into the EF colonizing the root of soybean.

Methodologies and Bottlenecks Limiting the Endophytic Study

The identification of endophytes in their host plants is somewhat difficult because some endophytic microbes might not be easy to culture in the laboratory [60], while some are viable but non-culturable. Hence, the use of culture-dependent and culture-independent methods remain important as the case may be. In the use of culture-dependent methods, the population of microbes are easily evaluated, while in contrast, the culture-independent methods are more useful in assessing the entire microbiome in the samples [61]. Culture-dependent methods, which involve microbial isolation on nutrient-rich microbiological media under specific revolutionized growth conditions, are important to determine microbial physiology and genes and screening for plant growth-promoting traits [62].

Conversely, this technique is laborious, revealing detailed microbial diversity and networking in econiches. Also, the proliferation of undesirable microorganisms on the cultured plates, which compete for nutrients needed by the desirable microorganisms, has been identified as a major challenge when isolating endophytic microbes by culturing methods [63]. Hence, the application of culture-independent methods is profound in characterizing yet-to-be cultured microorganisms. Authors Alain and Querellou [64], Torsvik and Ovresas [65], and Afzal, Shinwari, Sikandar, and Shahzad [63] stated that culturable bacteria represent about 0.0001–1% of the total endophytes in plants. Hence, the interest of researchers on purposeful research design should be considered before selecting a method for isolating endophytic microbes.

Endophytes can be cultured on agar plates, and then microbial DNA can be extracted before carrying out polymerase chain reaction (PCR). Garcias-Bonet, Arrieta, de Santana, Duarte, and Marbà [66] employed a commercial DNA extraction kit specific for plant DNA extraction to extract microbial endophytic DNA and used primer meant for the bacteria domain to carry out the PCR procedure. However, it should be noted that when amplifying a specific region of bacteria DNA, the mitochondria and chloroplast DNA found in plants may have a close resemblance to that of endophytes; hence, this method might not be too appropriate. In this light, next-generation sequencing is recommended without denaturing gradient gel electrophoresis (DGGE) analysis. Piccolo, Ferraro, Alfonzo, Settanni, Ercolini, Burruano, and Moschetti [67] demonstrated the use of fluorescence in situ hybridization (FISH) technique in studying endophytic microbes. However, this can only be done in the natural habitat, thus making the laboratory isolation complicated.

On the other hand, Ikeda, Kaneko, Okubo, Rallos, Eda, Mitsui, Sato, Nakamura, Tabata, and Minamisawa [68] developed a procedure to enrich bacterial cells when isolating unculturable endophytes from the stem of a soybean by fractionalizing the homogenated soybean stem. This method was achieved by differential centrifugation and Nycodenz density gradient centrifugation. This method proved effective compared to when DNA was isolated from the soybean stem due to the higher intensity and number of amplicons of the bacteria when the efficiency of the bacteria cell was fortified using ribosomal intergenic spacer analysis. Equally, Lundberg, Yourstone, Mieczkowski, Jones, and Dangl [69] also worked on an improved technique for 16S ribosomal rRNA sequencing, where unique template molecules were tagged before PCR by mapping amplicon sequences (to their original templates), which help to prevent error and bias arising from the amplification process. This method uses a base pair sequence with a higher temperature (melting) than the primer set, which is designed to attach to the host’s DNA.

The culture-independent methods are more advanced due to attention drawn to them which facilitated more research to improve them. For instance, a modern analytical approach has been documented to advance the science of the plant microbiome [70]. The use of combined stable isotope probing (SIP) and nanoscale secondary ion mass spectrometry techniques (NanoSIMS) coupled with advanced Raman spectroscopy-based single cell–based methods have been envisaged in studying plant microbiome in situ and to determine their biological functions in the bioremediation of complex pollutants from metal-polluted soil [71]. More importantly, the specific metabolic functions of endophytic microbes can be better understood by combining SIP with other molecular methods, such as qPCR, finger printing, and cloning.

Dos Santos and Olivares [72] reported the use of microcosm combined with bacteria stocks as a reference to determine bacteria assemblage in the root of plants and their plant growth-promoting potential. Also, Hartman, van der Heijden, Roussely-Provent, Walser, and Schlaeppi [73] reported a microcosm approach in elucidating the bacteria diversity and function in the root of red clover. Furthermore, Hartman, van der Heijden, Roussely-Provent, Walser, and Schlaeppi [73] revealed a significant reduction in the growth of red clover upon mono-inoculation with Flavobacterium compared to the co-inoculation of red clover with root microbiome, which enhanced plant growth by reducing the negative effect of mono-inoculation of red clover with Flavobacterium. Finally, a microcosm study performed by Eldridge, Travers, Val, Ding, Wang, Singh, and Delgado‐Baquerizo [74] reported diverse microbiome and their functions on 15 plant species growing in terrestrial habitats to reveal the preference of plant-associated microbes and their importance in plant germination. It will be interesting to fashion out how these modern approaches can be employed in the science of endophytes to better understand endosphere biology.

Different molecular approaches exist for the identification of endophytic bacteria and the combination of recent molecular approaches, such as genome sequencing and metagenome. The use of DNA extracted from the root of plants can be employed in unraveling microbial community structure and functions in soybean. The extracted DNA from plant tissues after surface sterilization with water, hypochlorite, or ethanol for endophytic studies might contain a certain proportion of plant DNA, which is needed to be depleted using appropriate sequencing techniques and plantforms (e.g., Illumina, PacBio, and DNA fingerprinting). Many techniques exist for DNA fingerprinting. These include restriction fragment length polymorphism (RFLP), simple sequence repeat (SSR), terminal-RFLP, rapid amplified polymorphic DNA, amplified fragment length polymorphism, inter-SSR, single-stranded conformation polymorphism, and DGGE [75]. The analysis of diverse plant microbiomes based on genetic composition can be achieved by the real-time polymerase chain reaction, FISH, automated version of ribosomal intergenic spacer analysis, terminal restriction fragment length polymorphisms, and DGGE, and phospholipid and fatty acid have also been documented [72, 76,77,78].

It is noteworthy to understand the use of molecular methods in identifying yet-to-be microbial endophytes by using appropriate methods to maximally recover endophytic DNA after the extraction process. The advent of PCR-based approaches in the Plant-Microbial Genome Project has provided vast advantages and opportunities for the detection, multiplication, quantification, and synthesis of copies of DNA in large amounts, differentiated from one another [79]. PCR techniques have been widely employed for the detection of diverse genes responsible for microbial functions [80]. The PCR and DNA sequencing aims at measuring the presence, taxonomy, and functions of plant microbiome from various samples, although, despite the importance of these techniques, there are limitations surrounding the PCR amplification process and DNA sequencing, mostly when extracting DNA from plant samples. The limitations include (i) contamination during the DNA extraction for PCR reaction and library preparation which may affect the DNA integrity, resulting in result errors and false outcome; (ii) primers’ design which require some previous sequence information; and (iii) the specific PCR product obtained during amplification process may be altered from one microbe to another based on non-specific binding of primers to other identical targeted sequences [81]. Piccolo, Ferraro, Alfonzo, Settanni, Ercolini, Burruano, and Moschetti [67] demonstrated the use of FISH technique in studying endophytic microbes; however, this can only be done in the natural habitat, thus making the laboratory isolation complicated. Furthermore, addressing these limitations specific to sequences may help devise approaches for the normalization of sequenced data to reveal microbial composition in its entirety. The use of PCR coupled with other sequence-based approaches is promising with more insights into plant microbiome gene combinations [71].

The advent of advanced molecular techniques for endophytes’ identification has succeeded in DNA fingerprinting, for instance, the use of omics approaches where DNA is retrieved from bacteria to evaluate the diversity, functions, genes, metabolites, transcripts, and proteins with the aid of next-generation sequencing. The DNA fingerprinting methods have been overtaken by more technical procedures, such as metagenomics which involves DNA extraction from the total bacteria population using next-generation sequencing [82]. This method has proven to better unravel the total endophytes from plant tissues compared to the fingerprinting techniques. Aside from omics approaches, the use of microscopy techniques, epifluorescence light microscopy, bright-field light microscopy, interferential and differential contrast light microscopy, scanning electron, and transmission electron microscopy in determining visual evidence of microbial colonization patterns in plants, has been documented [72, 76, 83].

The use of culture-independent techniques, which involved DNA/RNA extraction from environmental samples coupled with omics approaches, has revolutionized the science of endophyte microbiology in generating large sequence datasets. This next-generation sequencing approach involving no DNA cloning has been employed to unveil the community structure, diversity, taxonomic and functional profiling, metabolites, and metabolic pathways of the plant microbiome [72]. So far, the few research efforts utilizing next-generation sequencing from soybeans and other food crops revealed their taxonomic and functional attributes of endophytes in different plant species (Table 2).

Table 2 Shotgun metagenome findings of endophyte from legumes and food crops
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Furthermore, addressing these limitations specific to sequences may help devise approaches for the normalization of sequenced data to reveal microbial composition in its entirety. The use of PCR coupled with other sequence-based approaches is promising with more insights into plant microbiome gene combinations [71]. The combination of recent molecular approaches, such as genome sequencing and metagenome using DNA extracted from the root of plants, can be employed in unraveling microbial community structure and functions in soybean. More importantly, the specific metabolic functions of endophytic microbes can be better understood by combining SIP with other molecular methods, such as qPCR, finger printing, and cloning.

The advancement in plant microbiome studies has revealed certain traits, which mediate their functions, such as secondary metabolites, genetic information, proteins, and transcripts using culture-dependent and culture-independent techniques [84,85,86]. Modern approaches to studying diverse endophytic microbes and functions are being employed to understand the colonization pattern for plant–microbe interactions based on host specificity and signaling networking for microbial communications linked to root exudation [87]. The genes involved in flagellation, chemotaxis, motility, and biofilm formation has been reported in many bacteria strains, which facilitate their attachment/adherence, penetration, and colonization in the host plants [88, 89]. The host plants’ specific signal-networking and plant–microbe communications can reveal how microbes exhibit mutual relationships and antagonistic toward the phytopathogens by triggering host immune responses [12]. Aside from genes involved in beneficial bacterial colonization, other genes have also been documented to partake in microbial biological processes. For instance, the genes involved in carbohydrate metabolism, phytohormone synthesis, secretion systems, biocontrol activity, and oxidative stress identified in the genome of endophytic bacteria from sunflower, apricot, and poplar that are important in agriculture, biotechnology, and industry have been documented [90,91,92].

In line with the aforementioned approaches and conventional techniques, studying the plant microbiome can be easier. Hence, it is recommended to compare the different recovering or identifying endophytes. This would assist in selecting the best method to use to identify endophytic microbe from plant samples. On the other hand, both the culture-dependent and culture-independent methods of endophyte analysis can help have a broader view of the diversity and population of plant endophytes and their functional attributes in the ecosystem. Briefly, the advantages and disadvantages of the techniques and approaches employed in the study of plant-associated microbes are highlighted in Table 3.

Table 3 Some techniques and approaches of studying plant-associated microbes
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Complexity of Plant Microbiome in Plant Ecosystem

The microbes recruited into the plant endosphere and those inhabiting the external root environment contribute to plant growth in diverse ways, as shown in Fig. 1. Reports by Ku et al. [93] showed root surface and hair colonization by an endophytic bacterium, B. cereus, in Chinese cabbage, soybean, and wheat, with evidence in understanding the mode of actions of plant microbes and how they influence plant growth. Aside from endosphere and rhizosphere research findings, fewer studies have documented the microbiome inhabiting the antosphere, caulosphere, carposhere, and spermosphere. Research into microbiome in the plant environments, such as rhizosphere, root, seed, and stem, have been documented, and their possible use in agricultural biotechnology is profound.

Fig. 1
figure 1

Endophytic bacteria recruitment mechanisms and benefits in plant growth promotion. Key: IR, induced resistance; HCN, hydrogen cyanide; SAR, systemic acquired resistance

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For instance, Kumawat et al. [94] reported an increase in the growth, symbiotic efficacy, nutrient acquisition, and yield of soybean co-inoculated with endophytic Pseudomonas oryzihabitans and Bradyrhizobium spp. Also, an increase in the crop yield, oil content, antioxidant content, seed quality, carbohydrates, and chemical composition (protein and lipid) of soybean inoculated with endophytic Bacillus amyloliquefaciens has been reported by Sheteiwy et al. [23], which suggests their future exploration as bioinoculants in growing soybean under drought stress. Because plants harbor diverse number of microorganisms, the better understanding of their complexity and functional traits will help unraveled their biological activities.

Rhizosphere and Bulk Soil Microbiome

The rhizosphere (plant microhabitats) represents soil regions closer to the plant root environment [95]. The rhizosphere is often referred to as a “hotspot” for microbial activities due to the excess release of root exudates, which supply the required energy for microbial metabolic activities [96]. The response of soil microbes to the diverse chemical compounds and varied soil parameters, which favors soil microflora, can be an indicator for selecting them over others. The shaping of the rhizosphere microbiome can be a function of the quantity of exudate released from one plant to another. Some examples of secondary metabolite organic compounds include amino acids, phenols, organic acids, sugars, siderophores, polysaccharides, etc. When released from plant roots, it influences a higher microbial population in the rhizosphere than in bulk soil [97].

Bulk soil is the soil that is equidistance away from the rhizosphere region without root penetration [98]. The microbial inhabitant in the bulk soil can be less in diversity due to the fewer organic compounds than the rhizosphere soil inhabitants with identical species. Some examples of bacteria occupying the rhizosphere root environment include Bradyrhizobium diazoefficiens, Bacillus subtilis, B. velezensis, etc. [99,100,101]. High microbial colonization, diversity, and activities are easily mediated by rhizodeposition, reducing compared to the adjacent or bulk soil [102].

Usually, the variations in the rhizosphere microbial communities in soybean and other food crops can be linked to the geographical locations, growing seasons, crop rotation, plant growth stages, cultivars, farm practices, etc. The identification of diverse bacterial phyla, such as Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Gemmatimonadetes, and Proteobacteria from rhizosphere soils under the different growing conditions and soil types, has been reported with greater influence on the bacterial diversity [103, 104]. Hence, there is a need for further research to ascertain if the microbes present in soybean across multiple locations are different, since there is less information of the soybean rhizosphere microbial communities.

Due to the nodule formation in the root of soybean, the endosymbiotic relationship with nitrogen-fixing bacteria can be an advantage in releasing excess quality, and quantity of root exudate different from non-nodulating plants to help establish discreet microbial biomass in the rhizosphere [18]. High-throughput sequencing in determining the rhizosphere bacterial and fungal communities of rapeseed have revealed varied operational taxonomic units at seedling, flowering, and maturity stages [105]. The assessment of a bacterial community in rapeseed using a molecular ecology network with random matrix theory showed bacteria genera, such as Rhizobium, Flavobacterium, and Pseudomonas, at the network level [106].

Interestingly, research on rhizosphere microbiome with the view of mapping out strategies for their incorporation into agriculture has been emphasized in recent times [107,108,109]. Nevertheless, the presence of pathogens may influence rhizosphere microbes in many ecological processes. Furthermore, the source of rhizosphere microbes is important as most of them may be introduced into the soil through seed planting [110].

Seed Microbiome

Aside from the rhizosphere microbiome [111], research advancements have shown microbial composition on the surface and internal tissue of seeds [76, 112] can be beneficial or pathogenic. The beneficial microbes influence seed growth at pre-germination, germination, flowering, and maturation stages [113]. The recruitment of microbiome in seeds can be achieved by vertical (from the mother plant) or horizontal (environment) transmission [114]. Vertical transmission of seed endophytes is believed to originate from the leaves and flowering parts. Upon planting into the soil, the seed undergoes imbibition, which enables them to absorb soil nutrients and then germinate. During the imbibition process, the release of metabolic compounds in the spermosphere region, i.e., soil-seed environment, creates an attractive environment for the soil microbes to compete with the natural soil pathogens [115]. At this stage, the seed microbiome infiltrate or release to the soil environment via horizontal transfer.

Seed endophytic bacteria and their mode of transmission enabled them to occupy diverse niches, such as the pericarp, seed embryo or cotyledon, and endosperm [116]. The transmission of seed endophytes may differ depending on the organ location. For instance, endophytic in the pericarp are horizontally transmitted, while those colonizing the endosperm and embryo are easily transmitted by vertical processes [117]. More research should be done on soybean to understand how endophytes are transferred in their root region.

Microscopy and high throughput sequencing approaches have been employed to characterize seed microbiome, especially endophytic bacteria in some leguminous plants [118]. Sánchez-López et al. [119] reported dominant endophytic bacteria phyla, Proteobacteria, Firmicutes, Chlamydiales, and Bacteroidetes while investigating endophytic bacteria in the seed of Low Rattlebox. Information on the microbial community structure of endophytic bacteria in the seed of soybean and other leguminous food crops using high-throughput sequencing are scanty in literature. Consequently, differentiating seed endophyte and soil microbiome are still less understood. Also, seed endophytes can be found in other plant parts via infiltration from the rhizosphere to the above ground level. Interestingly, the synergistic cooperation between the soil microbes and seed endophytes has contributed to plant health and nutrition [120].

Root and Shoot Microbiome

The root and shoot form a key component in the study of the plant microbiome [71]. The microbes found in the root and shoot can be less in number compared to the higher microbial profiling in the rhizosphere due to the nutrients and exudate secretion attributes [96, 121]. The detection of genes involved in bacteria attachment due to specialized cell organelles, such as fimbriae, flagella, and pili in the plant surface, assisted bacteria adhesion to the cell surfaces to form a biofilm [122]. The plant-bacteria interaction and transient within the plant tissue can result due to a rise in water flux during transpiratory processes in plants. Across the plant parts, the presence of the targeted microorganisms may be influenced by the organ location and accessibility to plant nutrients [123].

For microbes to efficiently colonize the host plant, the line of mode of actions involved includes (i) adherence to the root surface, (ii) multiplication, (iii) invasion from the external root environment, and (iv) colonization [124]. After the colonization process, the movement of endophytic microbe from the belowground to the shoot through microbial networking can be achieved. The type and quantity of nutrients available in the plant endosphere can modulate the extent of bacteria diversity. Adeleke et al. [61] and Jie et al. [125] reported diverse endophytic bacteria phyla Chloroflexi, Nitrospirae, Planctomycetes, Palescibacteria, Acidobacteria, Actinobacteria, Cyanobacteria, Saccharibacteria, Firmicutes, Gemmatimonadetes, Bacteroidetes, and Proteobacteria from the root of sunflower and soybean. Recently, endophytic bacteria genera Bacillus, Staphylococcus, Serratia, Stenotrophomonas, Pseudomonas, Enterobacteria, and Erwinia from healthy rapeseed has been reported as part of the shoot microbiome [25]. Endophytic bacteria in the external root environment are usually higher compared to the internal part of roots. In the findings by Adeleke et al. [61], the authors reported a dominant and high bacteria population in the root of growing sunflower compared to the stem due to the agricultural practices, geographical locations, plant type, organ location, etc., which contribute to the bacterial diversity.

The reason for microbial differences in the rhizosphere, endosphere, and phyllosphere can be biological, chemical, or physical factors, which may exert selective pressure on endophytic bacteria to infiltrate the root endosphere [126]. The endophytic microbiome tends to adjust to a plant environment with stable biomass, while the rhizosphere microbiome may vary due to niche complexity. Acknowledging the fact that plants harbor a multifunctional microbiome in the root and shoot can be a pointer to understanding factors that modulate the shape of the microbiome in plants.

Plant Growth Stimulation Attributes of Endophytic Bacteria

Beneficial plant microbiome helps in sustaining the ecosystem [100]. The ecological services range from plant growth promotion, pathogen control, phytoremediation, biofertilization, and abiotic stress mitigation to human safety [86, 127]. In recent times, the multifunctional attributes of endophytic microbes as plant growth stimulators and bioinoculants promise to revolutionize agriculture without negative ecological effects [128]. Also, the role of endophytic microbes in agricultural biotechnology has been focused on; yet, research is still ongoing to meet zero ecological threats for maximum food production [129]. Exploration of endophytic resources to provide alternative measures in ensuring a safe environment and sustainable agricultural productivity have been emphasized due to the negative impact of chemical fertilizers on the ecosystem [130].

From the multifaceted application perspective, the mechanisms employed by endophytic microbes immensely contribute to plant growth and health [22]. Microbes employ direct or indirect mechanisms in sustaining plant growth and health [131]. The core attributes of endophytic microbes in enhancing plant growth include nutrient acquisition and mineralization, phosphate solubilization, nitrogen fixation, siderophore and enzyme production, and synthesis of growth hormones, such as indole-3-acetic acid, gibberellic acid, and abscisic acid, while indirectly, ACC deaminase, exopolysaccharide, and hydrogen cyanide production by endophytic microbes contribute to plants survival under drought stress [132]. All the aforementioned processes, specifically, have been screened from endophytic microbes associated with sunflower and soybean [15, 40]. In addition, the suppression of phytopathogens through the induction of systemic resistance and antibiosis activities of endophytic microbes boost plant immunity against soil and host invading pathogens [133]. Also, findings by Zhao, Xu, and Lai [9] reported high inhibitory activity of soybean nodule endophytic bacterium Acinetobacter calcoaceticus against pathogenic fungus Phytophthora sojae due to their close association with the root of the plants.

Endophytic microbes are said to deliver effectively in enhancing plant growth due to their close interaction, colonization, less composition in plants, and non-exposure to harsh environmental conditions [134]. These attributes make endophytic studies interesting compared to the rhizosphere microbes. The synergistic effect of nodule endophytic bacteria, Pseudomonas aeruginosa (LSE-2) and Bradyrhizobium sp. (LSBR-3) from soybean, has been investigated as a source of bioinoculants and biofertilizers due to their root colonization potential through molecular crosstalk, which supports plant growth and nutrition [135].

Some endophytic microbes solubilize phosphate in natural form by producing organic acids, which lower soil pH and chelate iron for easy phosphate assimilation by plants in soluble form [136]. The ability of endophytic bacteria to produce phosphatases also helps in the mineralization of organic phosphorus [137]. In vitro screening of phosphate-solubilizing endophytic bacteria has been investigated from soybean, sunflower, and rapeseed [138,139,140]. For example, Acinetobacter calcoaceticus, Ochrobactrum haematophilum, B. panacihum, Bacillus subtilis, B. australimaris, B. thuringiensis, B. zhangzhouensis, and Lysinibacillus pakistanensis have been isolated from leguminous crops [9, 18, 30]. Kenasa, Nandeshwar, and Assefa [141] reported the identification of cowpea root endophytic bacteria, Pseudomonas putida, and Bacillus subtilis phosphate producers in their study. Also, a study by Yasmeen and Bano [142] reported an increase in soybean yield co-inoculated with phosphate-solubilizing bacteria, Rhizobium and Enterobacter.

The rhizobacteria in the root nodule of leguminous plants naturally fix nitrogen in the soil, which is needed for plant nutrition [18]. The nitrogen fixation potential of endophytic bacteria in the root nodules of leguminous crops, effectively, has enhanced the nitrogen pool in soil deficient in nitrogen supply [143]. The nitrogen fixation by endophytic bacteria may differ compared to rhizobacteria found in the root of legumes [144, 145]. Interestingly, exploration of the endophytic bacterium Gluconacetobacter diazotrophicus with exceptional nitrogen fixation in plants has long been reported in reclaiming nitrogen loss in the soil [146].

The ability of endophytic bacteria to produce siderophores also plays a major role in plant health sustainability [147]. For instance, biocontrol activity which limits iron supply to the pathogens, heavy metal reduction, and induction of systemic resistance can be linked to the siderophore compounds, i.e., catecholate and hydroxamate, produced by endophytic bacteria [148]. Diverse endophytic bacteria associated with soybean have been reported as siderophore producers [15]. Bhutani et al. [18] and Maheshwari et al. [149] reported siderophore-producing endophytic bacteria strains from legumes. The suppressive and biocontrol activity of endophytic Burkholderia contaminans against Macrophomina phaseolina causing root rot, stem rot, seedling blight, damping off, and charcoal rot in jute due to siderophore biosynthesis has been reported [150]. Since the presence of nitrogen-fixing and siderophore-producing bacteria has been established in soybean, other functions of these bacteria should be further studied.

Similarly, phytohormones, such as ethylene, IAA, cytokinins, and gibberellin, modulating plant growth via diverse pathways are evident in endophytic microbes [9]. Notably, IAA biosynthesis facilitates root development, which enables plants to absorb nutrients and water from the soil [151]. Tryptophan, which serves as a precursor for IAA production by endophytic microbes in a growth media, helps differentiate IAA-producing bacteria from non-IAA-producing bacteria [152]. Evidence of IAA and other phytohormones, such as gibberellin, and cytokinin production by endophytic bacteria to enhance plant growth, have been documented [63, 153]. Some endophytic bacteria, which produce 1-aminocyclopropane-1-carboxylate (ACC), a precursor for ethylene production, contribute to plant growth and are resilient to drought stress [154]. The ability of endophytic bacteria to circumvent the effect of pathogens by producing jasmonic acid, antibiotics, salicylic acid, volatile compounds, siderophore, and lipopolysaccharide, elicit induced systemic resistance, and abiotic stress amelioration in the host plants [155].

The actual mode of actions employed by endophytic bacteria in oilseed crop soybean is yet to be fully understood. Similarly, the biosynthesis and metabolism of reacting molecules as precursors for the synthesis of novel metabolites or enhancing already identified metabolites are poorly understood. The synthesis of secondary metabolites, such as alkaloids, terpenoids, phenols, organic acids, and flavonoids, which induce antibiosis, can be achieved by endophytic microbes specific to the host plants [156]. Some examples of purified secondary metabolites produced by endophytic bacteria from some economic plants with related biological functions are presented in Table 4. Information relating to secondary metabolites sourced from endophytic bacteria associated with soybean is less documented in the literature. Hence, research focusing on secondary metabolites from endophytic bacteria associated with soybean and their exploration will further reveal their bioprospecting in plant disease management.

Table 4 Secondary metabolites originated from endophytic bacteria in plants and their bio-properties
Full size table

The biomolecules sourced from endophytic bacteria stand promising in agriculture, environment, industry, and human safety. Hence, genomic insights into plant microbiome aim to reveal their functions and activity in plant physiology and metabolism. Additionally, it is imperative to unravel soybean-associated endophytic bacteria’s biological functions and physiological attributes, using culture-dependent and culture-independent techniques to identify secondary metabolites in the bacteria genome [24]; making information available on secondary metabolites produced by endophytic bacteria will help find a solution to diverse agricultural problems.

Current Status of Plant Microbiome Collaborative Research

The interdisciplinary synergies among researchers in studying plant–microbe interactions continue to progress. Research efforts to study and explore endophytic bacteria from the leguminous crop as bioinoculants for plant growth and sustainable ecosystem have increased tremendously with driven biotechnological advances and low-cost analysis [124]. Interestingly, the commercialization of endophytic bioinoculants is possible in sustainable agriculture [128]. The computational knowledge about next-generation sequencing and other innovative techniques have informed scientists with accurate information on microbial diversity and related genes [109].

Better still, there is a need to develop robust bioinformatics tools and analytical techniques with the existing technologies to generate microbiome data as a guide for further experiments. Adeleke et al. [40] and Adeleke et al. [157] reported the genomic characterization of plant growth-promoting endophytic bacteria, Bacillus cereus T4S and Stenotrophomonas maltophilia JVB5 as copious sunflower growth enhancers. Furthermore, effort on the use of these endophytic bacteria as biocontrol agent against phytopathogens is expected to be investigated in the future studies. Employing this approach by ecologists, environmental and computational scientists, microbiologists, agriculturists, and industrialists aim to provide insights into plant microbiome research as a reference for further studies. Furthermore, understanding the dynamics and role of endophytic microbes in plants using up-to-date techniques and bioinformatics tools, however, can help develop multiple strategies in understanding their functions in diverse fields, such as agriculture, ecology, medicine, forensics, and exobiology.

The dominant bacteria phyla, Actinobacteria, Firmicutes, Proteobacteria, Bacteroidetes, and Chloroflexi in the root endosphere of food crops, such as maize, cowpea, sorghum, sunflower, soybean, have been reported using culture-independent techniques [61, 158, 159]. Yet, there is a need to investigate further using appropriate techniques to access plant growth-promoting endophytic bacteria in different legumes and other food crops under different climatic conditions. Hence, identifying these bacteria for bioinoculants formulation can serve as a pointer to achieving ecofriendly agriculture sustainably.

Conclusions

This review evaluates endophytic bacteria in soybean and other food crops. The bioprospecting of these bacteria enhances their potential for sustainable yield enhancement. Soybean was discussed as a reference crop for oilseed crops due to its economic importance, high yield, and nutritional value. Soybean harbors some endophytic microbes important in agriculture. Beneficial endophytic microbes inhabiting different parts of the plants can potentially contribute to the growth of soybeans and other food crops. For instance, root nodule bacteria and endophytic bacteria enhanced nitrogen fixation in soybean, which promotes their yield and other yield parameters, enhance immunity, and boost plant defense against diseases. However, the root endophytes are emphasized because of high metabolic activities occurring below ground level due to the high quantity of metabolite secretion, which contributes to plant physiological functions.

Different conventional and molecular techniques have been employed in the past to unravel endophytic microbes in some plants; nevertheless, each method comes with shortcomings. For instance, some endophytes can be difficult to culture on media despite their viability, such that culturing method can only unravel a lesser percentage (i.e., 0.1%) of endophytic populations. Hence, the advancement of endophytic microbes discovery using molecular techniques has proven more promising, although, with diverse challenges. Extracted endophytic bacteria DNA might contain traces of plant DNA, the chloroplast, and mitochondria DNA, which are identical to the targeted endophytic bacteria DNA [160]. Host depletion techniques have been employed to remove a substantial amount of plant DNA that might be present in the DNA extracted from the plant tissues. Conversely, the use of fluorescence in situ hybridization (FISH) is inefficient, because it can only be carried out in a natural habitat.

Oilseed crop soybean is economically important due to their high yield, and nutritional value. The mechanism employed by the endophytes present in the seed, shoot, leaves, roots, and other microbes inhabiting the rhizosphere, bulk soil in plant growth promotion, and disease control still needs to be emphasized, although some research information are available on them. The variation in the diversity and population of microbes inhabiting different plant parts can be due to difference in the geographical locations, cropping system, developmental stage of the plants and the farming practices adopted. These key factors may affect the crop yield, microbial diversity and their ability to produce secondary metabolites. It is therefore very important to understand the mechanisms behind the production of secondary metabolites in soybean as a measure to improve their production, oil content, antioxidant content, seed quality, carbohydrates, chemical composition, and yield in different environments and also as a model to the research of other crops. More research should also be carried out to help understand the use of endophytes in the agriculture, industry, and medical industries, owing to the production of bioproducts. Better still, there is a need to develop robust bioinformatics tools and analytical techniques with the existing technologies to generate microbiome data as a guide for further experiments. Employing this approach by ecologists, environmental and computational scientists, microbiologists, agriculturists, and industrialists aims to provide insights into plant microbiome research as a reference for further studies. Hence, the authors conclude and recommend that the current approaches highlighted in this review will be of help to researchers in understanding the dynamics, prospect, and potential of endophytic microbes in soybeans and other food crops as agricultural bio-input to ensure food security and sustainable agriculture.