The application of plant growth-promoting rhizobacteria in Solanum lycopersicum production in the agricultural system: a review

Survey methodology

To ensure an inclusive and impartial investigation of literature and to carry out the review’s objectives, a comprehensive investigation of published articles on the activity of plant growth-promoting bacteria mechanism of action was employed following the method of Mayak, Tirosh & Glick (2004), Olanrewaju, Glick & Babalola (2017). It is however intended for agriculture, food safety, and sustainability. Search results were gathered and complied employing the online endnote library system. This helped to arranged useful article embedded in the context. However, we appraised the titles, abstracts and the conclusion of the literature to determine the useful ones.

Effects of various chemical derivatives on crops

Chemical derivatives have been used for a long time for ameliorating the soil’s richness and aid bountiful harvests in agricultural practice. Fertilizers, insecticides, fungicides, and herbicides, among others, have been applied by farmers on farmland but this has raised health concerns for accumulating toxic chemicals in human tissue, animals, and plants (Ajilogba, Babalola & Ahmad, 2013). Subsequently, health concerns about accumulating toxic chemicals in human tissue, animals, and plants have arisen. It even pollutes the environment, especially aquatic lives, thereby causing suffocation of water organisms and other health hazards to humanity (Khalid et al., 2017b). Chemicals used on farmland entered human circulatory systems by inhalation, oral ingestion, or through the process of diffusion through the skin (Verla et al., 2019). Pesticides are mostly known to show long-term persistence in food materials like fruits and vegetables (Gallo et al., 2020). In addition, some individuals are hypersensitive or allergic to this chemical already in their system, causing various illnesses like cardiac disease, respiratory disorder, and musculoskeletal weakness (Khalid et al., 2017).

Various challenges have been encountered due to the application of synthetic insecticides, herbicides, fungicides, and other chemical derivatives (Lorsban or chlorpyrifos). They have amounted to plant diseases creating microbial resistance genes and are therefore resistant to these chemical derivatives (Ajilogba & Babalola, 2013).

Having experienced problems caused by the derivatives mentioned above, the entire globe is trying to produce healthy, ecologically friendly crops without chemicals. An alternative to lessen the application of chemicals in farming systems is to apply microbial inoculants (Chen et al., 2019). They are called biofertilizers, biostimulants, or biopesticides and improve the soil’s fertility. In addition, they encourage crop growth and prevent spoilage organisms from invading the crop plants. These organisms are primarily in the rhizosphere of healthy growing plants. Their aim is for a natural and ecological equilibrium (Omomowo, Adedayo & Omomowo, 2020).

PGPR effect on tomato productivity and their mode of action

Regarding agricultural practices, PGPR is used for its potential to increase tomato plant development and improve tomato plant protection from various infections and non-living factors like salinity and drought (Numan et al., 2018). PGPR is found on the tomato plants’ organs such as the root surface attached to or in the soil (and therefore called rhizobacteria), or the endophyte, which is the interior parts of the plant (Jambon et al., 2018). They produce innate procedures which promote the nutrient rate of assimilation as a biostimulant and quality of crops (Emmanuel & Babalola, 2020). PGPR has been a potential living composition of nano-biological fertilizers that can aid plant growth and development and avoid the development of dependent fungi (Gouda et al., 2018).

PGPR assists and encourages the development of the tomato plant through direct or indirect mechanisms (Berger, Baldermann & Ruppel, 2017). There are various ways by which PGPR promotes tomato plant growth as observed in Table 1. This procedure can be performed independently or in a group, especially with the rhizobacteria beneficial to the tomato plants. The characters that result in the direct promotion are called the natural mechanism of plant growth. Here beneficial compounds are provided to host plants and produce nutrient assimilation from the rhizosphere. On the other hand, indirect mechanisms are those characters that disallow the operating of one or more spoilage organisms of a tomato plant (Ajilogba & Babalola, 2013).

Soils containing microbial communities and huge organic matter require less fertilizer than naturally managed soils (Mahal et al., 2019). The huge microbial process is a typical example in soils frequently considered when applying organic nutrient sources. Phytomicrobiome research explains how to show a particular plant-microbe relationship that directly assists plant nutrition (Vishwakarma et al., 2020).

According to Salehi et al. (2019), a vegetable crop like tomatoes is a horticultural crop that promotes its consumer’s health due to the nature of certain nutrients found in them. Tomatoes contain nutrients and antioxidants, which include oxalic acid and ascorbic acid. These antioxidants in tomatoes are known to neutralise toxic free radicals in the blood circulation, reduce cholesterol levels and prevents high blood pressure (Mallick, 2021). When a crop seedling is inoculated with an actinomycete strain of rhizobacterium, the considerable amount of glucose, fructose, nitrate, maleate, zinc, and phosphorus are found embedded in the harvested fruit (Gouda et al., 2018).

PGPR promotes plant growth and resistance

The production of phytohormones by PGPR has important attributes on the growth and health status of the tomato plant (Vasseur-Coronado et al., 2021). These hormones are important signaling molecules that control the defense mechanism and growth of tomato plants. The auxin hormone (Indole acetic acid (IAA)) is a spectacular hormone produced in the rhizosphere of a healthy plant (Poveda et al., 2021). Phytohormones do exist in synthetic and non-synthetic forms and are sub-divided into five classes based on their sameness and their effect on plants. Some hormones required to regulate the growth of plants are known as synthetic hormones and are classed as chemically, naturally, or organically as produced by PGPR that may be obtained through several processes (Seenivasagan & Babalola, 2021). PGPRs produce phytohormones thereby indicating their advantages to the tomato plants and the rhizosphere they inhabit. The basis of phytohormone for the activity of plant growth-promotion of natural biostimulators is ascribed to improving tomato growth (Kapadia et al., 2021). Therefore PGPR ameliorates tomato plant growth and as well improves the production of auxins (IAA), gibberellin (GA), and salicylic acid (SA) in plants. Below is concise information of some phytohormones which include IAA, cytokinin (CK), ethylene (ET), GA, and SA likewise growth regulators like nitric oxide and polyamines produced by tomato and other plants.

Soil microorganisms’ effect on tomato plant growth promotion

The narrow soil zone extends on all sides of developing tomato plant roots. It corresponds to a significant area for the activity of microbes in the plant rhizosphere (De La Fuente Canto et al., 2020). A large number of taxonomic microbes include prokaryotic organisms (viruses, bacteria, and archaea) and eukaryotic organisms (algae, arthropods, fungi, nematodes, and protozoa) inhabit this soil. Bacteria and fungi contain mostly prevalent units revealing elementary ecological purposes (Mazière et al., 2021). PGPR is designated and assists plant development as free-living bacteria inhabiting soil flourish well and competitively inhabit the plant roots (Basu et al., 2021).

The diverse bacteria members, an essential part of the microbiota found in the soil, manufacture and liberate various modulatory compounds from the vicinity of the plants’ root that assists its growth (Khoshru et al., 2020). The contribution of nutrient acquisition enhancement by plants determines plants’ health by PGPRs, thereby keeping them safe from phytopathogenic microbes and enhancing resistance to non-living factors (Backer et al., 2018). Different genera of PGPR strains possess the potential of biological control activities, promote resistance to foliar spoilage organisms, improve crop yields, enhance nodulation in legumes, and promote the seedlings’ occurrence (Rozier et al., 2017; Kalam, Basu & Podile, 2020). The bacteria are Acinetobacter, Aeromonas, Agrobacterium, Allorhizobium, Arthrobacter, Azoarcus, Azorhizobium, Azospirillum, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Caulobacter, Chromobacterium, Delftia, Enterobacter, Flavobacterium, Frankia, Gluconacetobacter, Klebsiella, Mesorhizobium, Micrococcus, Paenibacillus, Pantoea, Pseudomonas, Rhizobium, Serratia, Streptomyces, Thiobacillus, and other reported PGPRs (Ankati & Podie, 2018; Kalam, Basu & Podile, 2020).

Among beneficial microbes in the soil community, bacterial species are the most abundant and helpful. Saravanan et al. (2020) gave the following full details of the action of bacteria in the soil: they help stimulate plant growth after the production of the certain phytohormone responsible for the development of plants; they return nutrients to the plants by fixing nitrogen back to the soil; they promote soil structure; they act against spoilage organisms which can destroy the crop plants. Therefore, PGPR is naturally more beneficial to the soil that they colonize.

According to Basu et al. (2021), a putative PGPR strain possesses plant promoting-growth characteristics and promotes growth once it has been inoculated into a plant. Below are the features of PGPRs in the rhizosphere soil of a tomato as stated by Guerrieri et al. (2020): they are eco-friendly and rhizosphere-competent; they promote plant growth and development; they exhibit a broad spectrum of actions; physical fractures like high temperature, oxidants, radiations, desiccation, should be tolerated by the PGPRs; there is positive interaction between them and other bacteria in the soil; they should be capable of adhering to the plant root after being inoculated in the rhizosphere, and they should be able to demonstrate better competitive skills over rhizobacterial communities already existing in the rhizosphere as shown in Fig. 2.

Solubilisation of phosphorus

For a healthy plant to grow and develop, phosphorus is one of the main elements required. The element is readily available and found in the soil. Since this element is present primarily in an insoluble form, rhizobacteria in the soil help solubilize the phosphorus, making it usable by plants by accumulation and transformation of phosphate to plant roots. The following symptoms are present in phosphorus-deficient plants: purple coloration of the underside of the older leaves due to accumulation of anthocyanin pigment (Pongrac et al., 2020).

The tomato plant absorbs phosphate quickly due to the high absorption surface area gradient of the plant’s root. Rhizobacteria are known to solubilize insoluble phosphate, which is why they are culturable on growth media in the laboratory by showing the area of phosphate solubilization (Santoro et al., 2021). These media contain various constituents like aluminum, iron, tricalcium phosphate, rock phosphate, and hydroxylapatite. The following bacteria can solubilize phosphorus in the soil: Burkholderia, Azobacter, Pseudomonas, Bacilli, Enterobacter, Citrobacter, Pantoea, among others (Kaur et al., 2017). During the solubilization of insoluble organic phosphorus, two enzymes are involved in the process: phytase and phosphatase. Bacteria produce organic compounds like gluconate, citrate, ketogluconate, tartrate, lactate, oxalate, which help solubilize inorganic phosphate (Babalola et al., 2021).

Nitrogen fixation

Nitrogen fixation can be defined as the process by which nitrogen present in the atmosphere is converted to ammonia by nitrogen-fixing bacteria for plants to utilize (Yilihamu et al., 2020). Nitrogen is among the essential ingredients needed by the tomato plant. It increases leaves’ size and quality. Its deficiency in plants results in limited growth of plants and yellowing of plant leaves (chlorosis) (Caradonia et al., 2019). Certain microbes add nitrogen to biofertilizers and have become a significant concern for researchers due to their environmentally friendly nature. Certain bacterial strains help fix atmospheric nitrogen and ensure its availability for tomato plant utilization (Masood, Zhao & Shen, 2020). Some examples are Enterobacter, Bacillus, Azobacter, Klebsiella, Serratia, Azospirillum, Arthrobacter, Gluconacetobacter, and Pseudomonas. This microorganism forms a symbiotic relationship with plants by adding the atmospheric nitrogen, and the plant, in return, houses them in their rhizospheric soil (Rozier et al., 2017). Cyanobacteria and Azolla can also implement required nitrogen by plants, as reported by (Akhtar et al., 2021).

Potassium solubilization

Potassium is one of the macro components needed by plants. Chemically, it can be used to produce NPK fertilizer. However, tomato plants absorb potassium as an ion that can readily be leached and lost through soil runoff (Sardans & Peñuelas, 2021). This element is required in plants to promote the formation of sugar for protein synthesis, root growth, and cell division in plants. A significant deficiency experienced on plants lacking potassium is leaf edge chlorosis. The economic importance of the defect is that the chlorosis is irreversible even if one adds the potassium later.

Magnesium solubilisation

Magnesium is the primary element required for the structural component of chlorophyll. A tomato plant needs it to promote the function of plant enzymes to produce carbohydrates, fat, and nutrient absorption regulation (Kwon et al., 2019). Magnesium deficiency in plants leads to chlorosis in tomato leaves, and severe cases result in stunted growth (Bang et al., 2021). The PGPR was reported to produce several metabolites including siderophores, organic acids, and growth hormones, which promote solubilization of iron and magnesium to the plant (Asad et al., 2019).

Parasitic association

Parasites live and feed on other organisms called the host, and this host suffers due to the organism feeding on it. Fungal parasites explain the parasitic relationship between Stachybotrys elegans and R. solani, which shows the concentrations of different secondary metabolites (Latz et al., 2018; Carroll et al., 2021). Meloidogyne spp. is a parasitic nematode of tomato plants, most economically and globally significant. It is challenging to eradicate and control the parasites Meloidogyne spp., because of the parasite infection on the tomato plant. Chemical nematicides contribute to the high toxicity of the plant. Rhizobacteria have been a prominent alternative to control these parasites without negative impact on the tomato plant, animals, and other organisms feeding on it. Bacillus spp. was effective and acted as biocontrol agents for plant pests and diseases (Chen et al., 2020) because it has many functions, including fixing phosphate, increasing the plant’s growth, and much more (Franco-Sierra et al., 2020). According to Habazar et al. (2021), Bacillus spp. is a rhizobacterium employed to control Meloidogyne spp., to improve the growth and cultivation of tomatoes. Bacterial species Pasteuria penetrans also act on nematodes to decrease root-knots growth through a parasitic interrelation. This bacterium multiplies in infected nematodes, killing them or causing infertility among those that survive the action. Once giant spores produced by bacteria are attached to the growing nematodes present in the rhizosphere, the movement and penetration of these nematodes are reduced (Heinrichs & Muniappan, 2018). In particular, plants have promoted their defense mechanism to fight invading spoilage organisms (Köhl, Kolnaar & Ravensberg, 2019). Some plant genes are RNA-seq responsible for defense against a plant root spoilage organism, Verticillium dahlia (Berne et al., 2020). They produced a plant-based signal transduction pathway web, which was initiated to acknowledge elicitors with safety indication materials and Pathogen-Associated Molecular Patterns that observe microbes like those that essentially relate to the roots of the plant in their soil habitat. The association of microorganisms obtained in the greenhouse field can reveal their potential thereby encouraging the isolation of beneficial soil microbes that will possess parasitic and biological control characteristics on plant spoilage organisms (Mills, Ross & Hill, 2017).

Symbiotic association

Igiehon & Babalola (2018) reported that symbiosis is a mutual relationship or association that involves two or more organisms to benefit both. A typical example of this association is the nitrogen-fixing bacteria (rhizobacteria) and roots of tomato plants (Masood, Zhao & Shen, 2020), as observed in Fig. 2. Rhizobacteria manufactured certain materials to increase the development of their host plants. They also assist in fixing nitrogen to plants and obtain a mutualistic relationship while also yielding to living and nonliving factors (Devi et al., 2020). Compounds like 2, 3-butanediol, among others (volatile organic chemical), are released by some rhizobacteria that elicit induced systemic resistance (ISR) in the plant. These compounds diffuse diketopiperazines rhizosphere interrelated bacilli, producing lipopeptides, polyketides, biosurfactants, and siderophores with prominent signal factors that are involved in molecular cross-talks between members of plant microbiota (Andrić et al., 2021).

The compounds like butanediol are released by symbiont B. subtilis, which is known to inspire induced systemic resistance by tempering the transcription of Na ⁺conveyer in plants (Oleńska et al., 2020). Likewise, rhizobacteria are known to produce some materials that promote tomato root penetration during growth by reducing the penetration of the primary root and promoting the formation of the distal root (Khanna et al., 2019). Some bacteria, together with fungi, liberate auxin hormone that comes in contact with the signs of this material in the root region (Singh et al., 2019a). Yet, in the root endophyte, auxin derivatives released by Piriformo sporaindica do not showcase action in the root development of a barley plant but are primarily available for parasitic infection occurring at the root of the plant. These bacteria and fungi found at the root also initiate compounds (dimethyl disulfide and pyocyanin) that control the growth of plant roots by creating the procedure of signalling auxin (Khatoon et al., 2020).

The mutualistic relationship often occurs in the rhizosphere between particular plants and microbes. These mutual relationships also occur between the microorganisms inhabiting the soil environment. Igiehon & Babalola (2017) reported the association of beneficial bacteria and arbuscular mycorrhizal (AMF) as a mutual relationship because the bacteria assist the fungi in a profound reciprocal relationship. At the same time, AMF improves bacterial intrusion ability and differences, though other advantages can be achieved in this relationship. Interactions do occur between fungi (Rhizopus) and bacteria (Burkholderia) which was regarded as a symbiotic association in the rhizosphere of tomatoes (Zhang et al., 2021). In the absence of the bacteria, the fungi will not produce spores, which reveals that both organisms depend on each other for reproduction and survival, i.e., the fungi live on the compound produced by the bacteria (Del Barrio-Duque et al., 2020).

Antagonistic association

This association is another form of interrelation between two or more organisms, either identical or different species. One organism dominates the other and prevents it from carrying out characteristics of life, including growth and feeding. In the tomato rhizosphere, antagonists produced specific chemicals which harmed other organisms. They produced enzymes such as lipases, protease, cellulases, and chitinases. These enzymes are the organic catalyst that can destroy or break down the cell walls of fungal spoilage organisms (Karthika, Varghese & Jisha, 2020). The rhizobacteria actions biologically controlled the spoilage organisms, which produced these materials to inhibit their features in the tomato rhizosphere soil (Guerrieri et al., 2020). Some microbes show important features inhibiting soft rot infection caused by fungi Rhizoctonia solani as observed in Table 3. These microbes include Proteobacteria, Firmicutes, and Actinobacteria (Piechulla, Lemfack & Kai, 2017). The fact obtained later explained how particular interrelations are essential to disease suppression. Inhibitory activity of bacteria to destroy R. solani on lettuce showed that bacteria possessed limited effect on rhizobacteria and endophytic fungi (Glick, 2020a). Zheng et al. (2018) gave another instance on the use of biological control bacteria on lettuce that inhibits the action of R. solani by fungal and bacterial species found on lettuce. This biocontrol mechanism of action explained the unexpected outcomes which were being explained due to the unfavorable effect on AMF. However, beneficial bacteria like some fluorescent Pseudomonas produce 2,4-diacetylphloroglucinol, an antifungal compound that was not injurious to AMF Glomus mosseae instead easily promoted inhabitation of root by mutualistic fungus species (Kabdwal et al., 2019). The fungal species may support the production of mycorrhizal apart from bacteria when they live on other fungal species. This shows that some fungi live on other species of fungi. Therefore, it is necessary to produce abstraction of fungus (mycorrhizal) for helping bacteria. This was because some species of fungi aider act against fungi that are not helpful and was noticed to promote mycorrhizal production (Giovannini et al., 2020).

Therefore, the quality of antifungals can be a reason for an antagonistic selection as biological control agents in the future. Rhizobium and Bacillus, among other rhizobacteria, are known to liberate siderophores which inhibit spoilage organisms from acquiring iron from the neighboring surroundings and thereby affecting spoilage organisms’ existence (Lurthy et al., 2020). This culminates in promoting plant growth and productivity.

Waghunde et al. (2021) reported that B. amyloliquefaciens, M. oleovorans, A. xylanus, and S. inulinus have shown high growth inhibition against fungi pathogens. Tiwari et al. (2021) explained how Bacillus subtilis was used to prevent the development of Aspergillus flavus and the poisonous aflatoxin the fungi produced on the farmland and while in storage. According to Alori & Babalola (2018a), various microorganisms, including Pseudomonads, Mitsuaria sp, and Rhizobia, produces biological control mechanism against spoilage organisms, with the latter suppressing Pythium disease, the former inhibiting Fusarium wilt and the mid-on bacteria reducing leaf spot of disease plant and more shown in Table 3.