Promoting sustainable agriculture by exploiting plant growth-promoting rhizobacteria (PGPR) to improve maize and cowpea crops

Direct mechanisms

Nitrogen fixation

Nitrogen (N₂) is an essential macronutrient for the plant. Atmospheric nitrogen (N₂) is present in large quantities in the air and cannot be directly assimilated by plant roots. However, due to the biological fixation of nitrogen by microorganisms, this nitrogen (N₂) is transformed into ammonia (NH₃) following an enzymatic reaction catalyzed by the enzyme nitrogenase which the roots can easily absorb. Microorganisms capable of biologically fixing atmospheric nitrogen (N₂), commonly known as “diazotrophs”, are able to do so in association with plant roots. Bacteria can achieve biological nitrogen fixation in a symbiotic or non-symbiotic relationship. In the former case, this occurs with legumes or other higher plants such as alder (Alnus spp). In the second case, it is carried out by heterotrophic or autotrophic bacteria living in the plant rhizosphere (Aasfar et al., 2021; Sickerman, Hu & Ribbe, 2019). The use of biological PGPR inoculants, which can fix nitrogen, on crops has benefits such as improved growth, and disease management. Nitrogen-fixing PGPR has been reported as a valuable source of nitrogen for sustainable crop production and maintenance of soil fertility (Singh et al., 2017). Examples of diazotrophic bacteria living freely in the rhizosphere and providing available nitrogen to many plants, thus promoting their growth, include the genera Azotobacter, Bacillus, Anabaena, Azospirillum, Klebsiella, Paenibacillus and Rhodobacter (Grobelak, Napora & Kacprzak, 2015). Numerous symbiotic bacteria have reported, among which are identified the genera Frankia spp, associated with some dicotyledonous species, Rhizobium spp, associated with legumes and other Azospirillum spp associated with grasses (Pankievicz et al., 2019; Singh et al., 2017).

Phosphate (P) solubilization

Phosphorus (P) plays an essential role in the growth and development of plants. It is available in large quantities in soils in organic and inorganic forms (Ahemad & Kibret, 2014). Generally, not more than 5% of these two available forms are soluble so the plants cannot be directly absorb them. In this case, the PGPR strains can solubilize these phosphates in an assimilable form for good absorption by the roots of the plant. The solubilization and mineralization of phosphorus depend on the action of the soil bacteria (Liang et al., 2019). The solubilization of inorganic phosphates occurs through the production of dissolving mineral compounds such as organic acids, siderophores, protons, hydroxyl ions, and CO₂ (Sharma et al., 2013). These organic acids, along with their carboxyl and hydroxyl ions, chelate cations or reduce pH, enabling the release of phosphorus (P) (Usha & Padmavathi, 2012). The mineralization of organic phosphorus, occurs through the hydrolysis of phosphoric esters by the action of phosphatases (Alori, Glick & Babalola, 2017). PGPR uses different methods to transform insoluble phosphates present in the soil into soluble forms, thus becoming assimilable by plants. PGPRs primarily employ the following methods: (i) the release of complex compounds and inorganic solvents such as hydroxyl ions, organic acid anions, CO_2, and protons; (ii) the release of extracellular enzymes; and (iii) the release of phosphate upon substrate degradation (Oleńska et al., 2020). Bacteria from the genera Bacillus, Pseudomonas, Serratia, and Enterobacter have been reported to solubilize insoluble phosphate compounds, promoting plant growth and yield (Kumar et al., 2008; Stein, 2005).

–Potassium (K) solubilization

Potassium (K) is an essential macronutrient for plant growth. However, concentrations of soluble potassium in soil are generally deficient, and over 90% of potassium in soil is insoluble, making potassium unavailable to plants (Parmar & Sindhu, 2013). However, many microorganisms, including certain bacterial species that establish mutual relationships with plants, are able to solubilize potassium in the soil (Setiawati & Mutmainnah, 2016). Rhizobacteria mainly use the production of organic acids, inorganic acids, and protons as their main mechanisms for solubilizing potassium (Maurya, Meena & Meena, 2014; Meena et al., 2015). Studies have reported that PGPRs capable of solubilizing potassium, such as Paenibacillus sp., Bacillus edaphicus, Acidothiobacillus and Pseudomonas, release potassium in a manner accessible to plants from insoluble sources present in soils, thus promoting optimal plant growth (Liu, Lian & Dong, 2012).

–Siderophores production

Siderophores are low molecular weight compounds that play a crucial role in microbial-plant interactions in the rhizosphere (Shanmugaiah et al., 2015). In general, the iron (Fe) available in the soil is not directly assimilable by plants because it is trivalent hydroxide Fe3+. molecules of siderophores are therefore produced and secreted by bacteria, which facilitates the assimilation of iron by plants. Catecholates/phenolates, hydroxamates, and carboxylates are the different groups of siderophores that exist on the chemical level. They are classified according to their chemical role in iron chelation. The siderophores produced by PGPR have a strong affinity for iron, enabling them to sequester even low concentrations of iron in the soil (Saha et al., 2016). In their study, Kumar et al. (2018) highlighted that the inoculation of siderophore-producing PGPRs, and the use of their consortium positively impacted wheat growth and development. The production of siderophores by PGPRs plays an essential role in biological control, as it restricts the availability of iron to harmful plant pathogens, thus keeping them away from the sources of iron needed for their development (Shanmugaiah et al., 2015). The use of iron-chelating hydroxamate siderophores produced by the P. aeruginosa strain was associated with growth inhibition of the pathogens R. solani and C. gloeosporioides in chili plants, as demonstrated in the study by Sasirekha & Srividya (2016). In addition, the presence of PGPR in the soil promotes the production of siderophores, enabling plants to reduce heavy metal toxicity in stressful environments (Ayangbenro & Babalola, 2017).

–ACC deaminase

Another important direct mechanism is the exhibition of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity by PGPR. PGPR-producing ACC enzyme is capable of hydrolyzing ACC to α-ketobutyrate and ammonia, which could reduce the high level of ethylene in plants. Indeed, the high level of ethylene in plants could decrease plant growth and lead to their death. This is the case for the ethylene content in plants (del Carmen Orozco-Mosqueda, Glick & Santoyo, 2020; Singh et al., 2015; Tiwari, Duraivadivel & Sharma, 2018). In stressful environmental conditions, ACC oxidase and ACC synthase activity in plants increase, leading to increased ethylene production. PGPRs that produce the ACC deaminase enzyme can help plants mitigate the negative effects of stress by promoting their adaptation and survival in these stressful conditions. This is achieved by reducing the amount of ACC available for conversion to ethylene, enabling plants to better cope with environmental stress (del Carmen Orozco-Mosqueda, Glick & Santoyo, 2020). A study by Vocciante et al. (2022) revealed an interaction between ACC deaminase activity and IAA action in the plant. Indeed, the action of the IAA on the plant could stimulate ACC synthase transcription, which would help lead to an elevation of ethylene levels in the plant. In the plant, the high level of ethylene in the plant induces an inhibitory response to the production of IAA, which leads to an inhibition of the growth of the plants. Several studies have demonstrated that the application of PGPRs producing the ACC deaminase enzyme confers on plants increased tolerance to various environmental stresses (Pourbabaee et al., 2016; Saikia et al., 2018). Interestingly, the ACC-deaminase gene has been signaled in some bacterial strains, which include Burkholderia, Achromobacter, Azospirillum, Agrobacterium, Ralstonia, Rhizobium, Pseudomonas and Enterobacter (Gamalero & Glick, 2015).

–Production of phytohormones (auxin, gibberellin, cytokinin, ethylene, abscisic acid)

Auxin, ethylene, cytokinin, gibberellin, and abscisic acid are the five main groups of plant hormones recognized by botanists. The production of growth phytohormones produced by PGPR influence seed germination, and root development facilitating good nutrient uptake, resulting in good vascular tissue and shoot development, good flowering, and full plant development (Adeleke & Babalola, 2021; Antar et al., 2021). These phytohormones also regulate hormone levels, influence photosynthetic processes favorable to plant growth and development, and activate defense responses against pathogens (Backer et al., 2018). These phytohormones were further discussed below:

Auxin, particularly indole-3-acetic acid (IAA), is a phytohormone present in plant-associated bacteria, playing a crucial role in various cellular and developmental processes throughout the bacterial life cycle. IAA is mainly produced in the rhizosphere of healthy plants and is involved in interactions between plants and bacteria. Its production is considered one of the key mechanisms promoting plant growth and development, notably by stimulating root formation and growth (Grobelak, Napora & Kacprzak, 2015; Luo, Zhou & Zhang, 2018; Poveda et al., 2021). In their study, Bashan, Holguin & De-Bashan (2004) showed that IAA production by Azospirillum, Agrobacterium, Pseudomonas, and Erwinia increases root hairs, root length, branching, and root area.

Cytokinins (CKs) play an essential role in the development of the vascular system, embryogenesis, nodule formation, and the response of plants to environmental variations. Their action is decisive in these processes (Hönig et al., 2018). CKs play a special role in interacting with auxin to counteract the aging process in plants. They act by modifying protein levels and promoting chlorophyll production in leaves, leading to a reduction in the yellowing of plant leaves (Guo et al., 2021).

Gibberellins (GA) produced by plant-associated microorganisms play a critical role in plant growth and development (Nett et al., 2017). Gibberellin controls the growth and development of the plant life cycle. Pre- and post-gibberellin control differs among cells and tissues, growth levels, environmental conditions, and plant species (Rizza & Jones, 2019).

Ethylene (E) is a growth phytohormone produced naturally by most plants and can induce multiple physiological changes at the molecular level in plants (Shaharoona et al., 2011). Ethylene production is essential role in apical meristem function and root development in plants. Depending on the particular plant species, ethylene concentration can affect plant growth, either stimulating or inhibiting it (Vandenbussche & Van Der Straeten, 2012). Certain plant-associated microorganisms can up regulate the enzyme ACC deaminase, which is responsible for the degradation of ACC, the precursor of ethylene in plants under stress. Under stress conditions, inoculation with these microorganisms can enhance plant growth and development, thereby reducing stress-induced ethylene production in the plant (Shaharoona et al., 2011).

Abscisic acid (ABA) is a plant hormone synthesized by plants in response to abiotic stress. Its role is to activate the expression of genes involved in stress resistance (Sah, Reddy & Li, 2016). ABA significantly impacts plant defense against bacterial and fungal pathogens and can induce different virus resistance mechanisms at any time of induction (Alazem & Lin, 2017). ABA can also affect seed germination inhibition, plant senescence induction, alongside fruit and leaf abscission (Munemasa et al., 2015).

Indirect mechanisms

Indirect mechanisms occur when the microorganisms counteract or prevent the damaging effects of pathogens on plants by synthesizing antibiotics and cell wall degrading lytic enzymes (Adeleke et al., 2022).

Antibiotics production

The main action used by PGPRs is to synthesize one or more antibiotics to counteract the harmful effects of plant pathogens. This mechanism involves inhibiting the growth of phytopathogens through the production of secondary metabolites with antifungal and/or antibiotic properties (Noumavo et al., 2016), thus sustaining plant and soil health. In their review, Prashar, Kapoor & Sachdeva (2013) highlighted that PGPRs can produce antibiotics such as lipopeptides, polyketides, and antifungal metabolites, which have pathogen-suppressive properties. Several researchers have also demonstrated that certain PGPR strains have promising potential as biocontrol agents to combat plant pathogens (Abdelmoteleb & González-Mendoza, 2020; Agbodjato et al., 2018; Viljoen et al., 2019). However, Glick (2015) mentioned in these works that an antibiotic known to control one pathogen on the plant may also be without a positive effect on another pathogen on the same plant. In this case, the bacterium synthesizing the antibiotic may show variable action in the field under different conditions. Riaz et al. (2021) stated that Bacillus thuringiensis (Bt) produces pest-killing proteins, which is why it is widely used to protect plants against pests. The intervention of biological agents such as PGPRs coupled with proper plant nutrition can improve the agricultural importance of different plant species (Jalal et al., 2023). Biopesticides incorporating PGPRs offer a sustainable, environmentally-friendly approach to combating plant pests and diseases.

Induced systemic resistance (ISR)

Induced systemic resistance (ISR) is the defense capacity that plants acquire when stimulated adequately by various biological entities of rhizobacteria (Conrath et al., 2015; Mariutto et al., 2011). Conrath et al. (2015) explain PGPR-induced systemic resistance (ISR) as the defensive ability of plants in response to various pathogens. ISR manifests itself through different defense mechanisms, such as an increase in β-1,3 glucanase, chitinase, and peroxidase activity, as well as the accumulation of low-molecular-weight antimicrobial substances such as phytoalexins, and the formation of protective biopolymers such as lignin, callose and glycoproteins (Archana et al., 2011). Systemic resistance induced by exogenous chemical agents and pathogenic organisms is often referred to as systemic acquired resistance (SAR), while the protection conferred on plants by PGPRs is generally referred to as PGPR-induced systemic resistance (Adeleke & Babalola, 2022; Kloepper, Tuzun & Kuć, 1992). Using PGPR strains as an essential component of plant defense may increase their applicability and offer a practical approach to immunization (Annapurna et al., 2013; de Andrade et al., 2023).

–Lytic enzymes production

Another important feature of PGPRs in the biocontrol of plant pathogens is the production of lytic enzymes (usually extracellular) that degrade pathogen cell walls (Agbodjato et al., 2018; Egamberdieva et al., 2011; Kobayashi et al., 2002). Rhizosphere microbes produce hydrolytic enzymes that inhibit the growth of pathogens by degrading their cell walls, proteins, and DNA, making them safer, sustainable, and environmentally friendly biocontrol agents than chemical fungicides (Jadhav & Sayyed, 2016). Some PGPR produces enzymes such as chitinases, proteases, lipases, phosphatases, cellulases, β-glucanases, etc. that are capable of lysing the cell walls of many plants’ pathogenic fungi (Lanteigne et al., 2012; Mamta et al., 2012). Research by Karthika, Midhun & Jisha (2020) has also shown that certain enzymes such as proteases, amylases, β-1,3-glucanases, cellulases, lipases, and xylanases produced by strains of Bacillus cereus and Bacillus cepacia are capable of degrading the cell walls of various pathogenic microorganisms present in the soil. These hydrolytic enzymes secreted by PGPR can induce direct elimination of the activities of plant pathogens. Bacteria such as B. subtilis, B. cereus, B. thuringiensis and S. marcescens can secrete hydrolytic enzymes to control plant pathogens (Jadhav & Sayyed, 2016).

–Competition

Another mechanism unique to PGPR is their ability to compete as a biocontrol agent competes with and, in most cases, out-competes plant pathogens for either nutrients or binding sites in the rhizosphere of the host plant (Etesami & Maheshwari, 2018). This competition results in the blockage of phytopathogens from binding to plants until available nutrients are depleted, thus making it relatively impossible for them to increase and infect the plant. It has been reported that PGPR inoculants exhibit antifungal activity and can compete with pathogenic fungi such as Fusarium oxysporum (Ambrosini et al., 2015). In addition, Bacillus megaterium’s competitiveness in promoting tomato plant growth has also been reported (Lindström & Mousavi, 2020).

–Hydrogen cyanide (HCN) production

Hydrogen cyanide (HCN) is a volatile secondary metabolite that can inhibit the growth of pathogenic microorganisms and reduce negative effects on plant growth and development (Siddiqui et al., 2006). Rijavec & Lapanje (2016) also noted that HCN is recognized as a biocontrol agent due to its toxicity to plant pathogens. HCN can impact plant establishment or inhibit disease development, giving it strong potential to control of bacterial diseases in plants (Lanteigne et al., 2012). Several bacterial genera can produce HCN, notable among them include Alcaligenes, Bacillus, Aeromonas, Rhizobium and Pseudomonas (Alemu, 2016).

–Exopolysaccharides (EPS) production

Exopolysaccharides (EPS) produced by PGPR enter the soil aggregates and modify their porosity (Alami et al., 2000). Bacterial EPS also combat salinity stress by limiting the amount of sodium in the soil (Upadhyay, Singh & Singh, 2011). Bacterial EPS, under water stress conditions, limits or delay the soil’s desiccation. On the other hand, in case of rainfall and flooding in the soil, the EPS block the dispersion of clays in the soil (Henao & Mazeau, 2009). Plants inoculated with PGPR bacteria showed tolerance to water stress through improved soil aggregation (Bashan, Holguin & De-Bashan, 2004) and soil structure (Sandhya et al., 2009a). The involvement of the EPSs produced by PGPR under salt stress and drought conditions was crucial in improving Helianthus annuus yield (Tewari & Arora, 2014). The production of EPS by PGPRs is a crucial feature that helps to enhance plant development during periods of drought. EPS enables the formation of hydrophilic biofilms around plant roots, protecting them from drying factors present in the soil (Rolli et al., 2015).

–Control abiotic stress and heavy metals by PGPR

Control abiotic stress

Climate change has increased the effects of environmental stressors and thus affected agricultural production worldwide. Indeed, the high quantities of soil and low water resources in soils, lead to a decrease in agricultural productivity, also leading to the abandonment of the affected lands which indirectly affects the food security of the population (Adeleke & Babalola, 2020; Ilangumaran & Smith, 2017). In this context, plants are often influenced by environmental stresses, such as biotic stress (fungi, bacteria, and viruses) and abiotic stress (pH, temperature, drought, salinity, contaminants, etc.), causing adverse effects on plant survival (Islam et al., 2016). Some PGPRs can increase crop yield by improving tolerance to abiotic stressors and phytopathogens. Kálmán et al. (2023) also mentioned in their study that PGPRs help reduce the negative effects of drought and stressful thermal conditions on plants. The synthesis of the ACC deaminase enzyme is the most studied among the different PGP traits involved in the drought tolerance of plants. PGPR maintains ethylene levels below inhibitory levels through the production of ACC deaminase, which leads to normal root growth by avoiding excess auxin and slowing down senescence under drought conditions (Marasco et al., 2013). Sandhya et al. (2009b) mentioned that Pseudomonas sp. inoculation of maize increased solutes and modified antioxidant status in drought conditions. Studies by Kour et al. (2020) showed that inoculation with the drought-tolerant, phosphorus-solubilizing strain Pseudomonas libanensis EU-LWNA-33 improved wheat growth and phosphorus uptake under drought conditions. According to studies by Jochum et al. (2019), inoculation of maize and wheat seedlings with Bacillus sp. 12D6 and Enterobacter sp. 16i delayed the onset of drought symptoms. The same authors also found that inoculation of wheat seed with Bacillus sp. (12D6) led to an increase in root length, while inoculation of maize seed with Bacillus sp. 12D6 and Enterobacter sp. 16i led to an increase in root length and surface area.

Heavy metals

Heavy metals, when discharged as effluents by industries, threaten the environment and public health. These heavy metals, usually consisting of mercury (Hg), cadmium (Cd), lead (Pb), arsenic (As), chromium (Cr), and antimony (Sb), affect the growth and yield of crops. Heavy metals are widespread pollutants, non-degradable, and therefore persistent in soils and a real environmental problem (Omomowo & Babalola, 2021; Wuana & Okieimen, 2011). Generally, heavy metals are toxic to plants which affect their growth. Nevertheless, some bacteria can neutralize the toxicity of these metals using negatively charged functional groups present in their cell wall. These functional groups enable interactions with positive metal ions, a phenomenon is known as metal biosorption (Syed & Chinthala, 2015). Bioremediation is one of the techniques used by microorganisms whereby their products are used to remove or immobilize contaminants in the environment without affecting the plant (Azubuike, Chikere & Okpokwasili, 2016). Ojuederie & Babalola (2017) also mentioned in their study that one of the important tools to restore eroded areas and heavy metal-contaminated sites is bioremediation. Rhizoremediation is, the use of rhizobacteria to remediate or immobilize these environmental contaminants. PGPRs are considered beneficial agents capable of enhancing plant growth by eliminating or reducing pollutants in the environment (Koul et al., 2019). Abiotic stresses, such as heavy metals, lead to ethylene and stress hormones synthesis in plants. In high ethylene concentrations, root growth and proliferation are negatively affected in soils contaminated with heavy metals. However, microorganisms producing the ACC deaminase enzyme are beneficial in promoting plant growth under conditions of heavy metal contamination. Indeed, microorganisms produce the ACC deaminase enzyme, which regulates the concentration of ACC, the ethylene precursor, thereby helping plants survive under stressful conditions. This ability of microorganisms to metabolize ACC is beneficial to plants and has been demonstrated in studies such as those by Mishra, Singh & Arora (2017). To date, several PGPRs have been recognized for their exceptional ability to degrade ethylene and various toxic chemicals such as solvents, organic compounds, and agricultural inputs. These findings are supported by studies such as those conducted by Backer et al. (2018). Indeed, to neutralize metal toxicity, PGPR can bind to negative functional groups in the cell wall, allowing interactions with positive metal ions (Syed & Chinthala, 2015). These authors reported in their study that Bacillus strains showed a significant level of lead biosorption (Syed & Chinthala, 2015). Wani & Khan (2014) also showed that Bradyrhizobium can be used to promote the growth of plants, as well as for the detoxification of heavy metals in soils polluted by these metals. Jiang et al. (2017) mentioned that high concentrations, rhizospheric bacteria such as Bacillus, Pseudomonas, Cupriavidus, and Acinetobacter showed tolerance to metals such as Pb, Cd, and Cu.

PGPR in the improvement of maize cultivation

Maize (Zea mays L.) is one of the world’s most widely cultivated annual tropical herbaceous plants. It is a staple food for many populations because of its nutritional value in food and feed and its use in industry (Revilla et al., 2022; Rouf Shah, Prasad & Kumar, 2016). To meet the rapidly increasing population, the need for maize will require highly sustainable production and resilient farming systems (Shiferaw et al., 2011). Huge amounts of chemical inputs are often used to increase crop yields, but the overuse of these chemicals has negative environmental consequences. In this context, using PGPR for its beneficial effects on agricultural production and environmental preservation is a better alternative for sustainable agriculture. Indeed, several studies have proven the beneficial effects of PGPR on the germination, growth, and yield of cereal crops (Agbodjato et al., 2016; Amogou et al., 2018). According to studies by Breedt, Labuschagne & Coutinho (2017), the use of Paenibacillus alvei, Bacillus pumilus, Bacillus safensis, and Brevundimonas vesicularis strains as bioinoculants resulted in maize yield improvements ranging from 24% to 34%. Due to their specific mechanisms of action, PGPRs have the ability to fix atmospheric nitrogen (N₂) and delay nitrogen remobilization in maize plants, resulting in increased crop yields (Kuan et al., 2016). These authors explain that this remobilization of Nitrogen in plants is mainly correlated with plant senescence leading to high maize cobs of up to 30.9% with reduced nitrogen (N) fertilizer application. Several authors have reported the positive effect of PGPR on the growth of maize (Adoko et al., 2020; Agbodjato et al., 2015; Amogou et al., 2019). Research by Pereira et al. (2011) also explored the effect of bioprotection by PGPRs on maize crops. Indeed, maize is often confronted with the worrying presence of the toxigenic fungus Fusarium. The application of certain PGPR strains, such as Microbacterium oleovorans and Bacillus amyloliquefaciens, in the form of corn seed coatings, demonstrated effective protection against the pathogenic fungus Fusarium verticillioides (Pereira et al., 2011). In a similar study conducted by Chen et al. (2021) in China, it was shown that inoculation of different PGPR strains such as Sinorhizobium sp. A15, Bacillus sp. A28, Enterobacter sp. P24 and Sphingomonas sp. A55 significantly impacted on maize growth and resulted in an increase in grain yield of 22–29%. The research carried out by Ghavami et al. (2017) revealed the potential of bacterial strains in mitigating drought stress in maize. Indeed, their study showed that inoculation of the Bacillus DHK strain with maize plants significantly increased plant biomass. Compared to the control group, the use of this strain led to a reduction in reactive oxygen species and an increase in antioxidant enzyme activity (Ghavami et al., 2017). In their study, Song et al. (2021) showed that inoculation with Azotobacter chroococcum promotes plant nutrient uptake and improves maize crop yield without negatively impacting soil stability. In their work, Marulanda et al. (2010) observed that inoculation of Bacillus megaterium into maize roots enhanced the ability of roots to absorb water in the presence of saline conditions. The Table 1 presented the Mechanism(s) involved in PGPR strains and their effects maize plants.

PGPR in the improvement of cowpea cultivation

Vigna unguiculata L., commonly known as cowpea, is a legume widely appreciated for its nutritional value widespread consumption, and considerable economic importance worldwide. It is one of the most important legumes in the world, containing excellent nutritional factors while offering several agronomic, environmental, and economic benefits. The nutritional values of the cowpea have been widely reported. It is exceptionally rich in several nutrients, particularly high protein content, antioxidants, polyunsaturated fatty acids, polyphenols, and dietary fibers (da Silva et al., 2018; Gonçalves et al., 2016).

To promote healthy and sustainable agriculture, PGPR are attracting more attention from researchers and agricultural promoters due to their beneficial effects in improving agricultural production and protecting crops in soils affected by biotic and abiotic stress. In their study, Udaya Shankar et al. (2009) demonstrated the efficacy of Bacillus spp. strains in protecting cowpea plants against the common bean mosaic virus (CBMV). These strains also improved cowpea plant growth by inducing resistance against CBMV, under laboratory and field conditions. Zaghloul et al. (2019) showed that the PGPR strains used are good for fertilization management and bio-control which reduce the amount of NPK chemical fertilization. The research work conducted by Rocha et al. (2019) revealed that cowpea fields could perform better if PGPR seed and AM fungal isolates were used in low-input farming systems. The work of Jayakumar, Nair & Radhakrishnan (2021) showed that identifying the properties of B. subtilis Dcl1 and demonstrating its probiotic effect on the plant Vigna unguiculata confirmed the potentialities of this strain as a biofertilizer, biocontrol, and bioremediation agent to improve agricultural productivity. Also, the study carried out by Juby et al. (2021) on cowpea has shown the beneficial application of the Bacillus Fcl1 endophyte to promote cowpea plant growth, even in the presence of toxic pesticides. In addition, these researchers demonstrated that the Bacillus Fcl1 strain can be used as a biological agent to mitigate the undesirable effects of toxic pesticides on plants. Table 2 presented the Mechanism(s) involved in PGPR strains and their effects on cowpea plants.

Importance of PGPR in maize and cowpea cultivation

The use of PGPR-based biological formulations as a substitute for chemical fertilizers and pesticides in maize and cowpea cultivation offers significant advantages for several reasons. These include promoting environmental sustainability, reducing production costs, and improving crop yields. Indeed, PGPRs are beneficial micro-organisms, and in view of their aforementioned mechanisms of action, their use can considerably reduce dependence on chemical fertilizers, which have harmful effects on the environment, such as soil and water pollution, heavy metal contamination of crops, and so on. Thus, growing maize and cowpea with PGPRs will improve yields, resist plant pathogens, preserve ecosystems, and mitigate the effects of climate change on the environment, increasing crop resilience. By using PGPRs, farmers can reduce their dependence on expensive chemical fertilizers that are sometimes inaccessible to all strata in rural areas. In addition, the use of PGPRs promotes the utilization of nutrients present in the soil, thereby optimizing yields and reducing expenditure on agricultural inputs. By using PGPRs in maize and cowpea cultivation, we can obtain higher-quality crops, with higher nutrient content and no heavy metals. This can help increase the market value of crops and satisfy consumers’ growing demands for quality products. This is a result of their ability to stimulate the plant immune system and boost resistance to environmental stresses such as drought, disease and pests, the use of PGPRs can enable farmers to reduce crop losses and ensure more sustainable agricultural production.