Phytohormone-Producing Rhizobacteria and Their Role in Plant Growth

Abstract

Phytohormone-producing rhizobacteria are a group of beneficial bacteria residing in the rhizosphere that have the unique ability to produce, release, and also modulate phytohormones such as auxins, cytokinins, gibberellins, ethylene, and jasmonic acid (JA). This work explores a diverse group of rhizobacteria that possess the ability to synthesize and secrete phytohormones and their effects on the growth of different plants. Indole-3-acetic acid (IAA) is a commonly produced hormone by many rhizobacteria that include Azospirillum brasilense, Pseudomonas putida, and Pseudomonas fluorescens. IAA producers promote plant growth through multiple mechanisms. Gibberellic acid (GA3) produced by certain species of rhizobacteria, which include Serratia marcescens and Bacillus licheniformis, enhances plant height and biomass in different crops. Cytokinins are produced by rhizobacteria, including Bacillus, Pseudomonas, and Azospirillum. Few rhizobacteria strains also produce abscisic acid (ABA). For example, A. brasilense produces abscisic acid, which can regulate the plant water status and enhance drought tolerance in different crops. Several rhizobacteria, including P. fluorescens, P. putida, and Pseudomonas aeruginosa, have been reported to induce JA production in plants, promoting defense responses against pathogens. Overall, this work indicates that rhizobacteria produce key phytohormones, enabling them to promote plant growth through multifarious ways, and hence phytohormone-producing rhizobacteria are potential input in agricultural production.

1. Introduction

Rhizosphere is the soil volume under the physical and biological influence of the root, including the root tissues colonized by microorganisms. Rhizosphere bacteria (rhizobacteria) are a group of bacteria competent in colonizing the root environment. About 2–5% of rhizobacteria, when reintroduced by plant inoculation in a soil containing competitive microflora, exert a beneficial effect on plant growth and are termed as plant growth-promoting rhizobacteria (PGPR) [1]. Plant growth-promoting rhizobacteria display a wide array of mechanisms to promote the development of plants. Among the different mechanisms, diverse PGPR can alter root architecture and promote plant development due to their ability to synthesize and secrete plant hormones (phytohormones) that include indole-3-acetic acid (IAA), gibberellins (GAs), cytokinins, and certain volatiles, hence they are termed phytostimulators [2]. The capacity of rhizobacteria to produce phytohormones is strain specific [3].

The PGPR stimulatory effect comes from a manipulation of the complex and balanced network of plant hormones that are directly involved in growth or stimulation of the root formation. For instance, the biosynthesis of IAA by various PGPR has been demonstrated to enhance root proliferation [4]. Bacteria use this phytohormone to interact with plants as part of their colonization strategy, including phytostimulation and avoidance of basal plant defense mechanisms. Moreover, it has recently been indicated that IAA can also be a bacterial signaling molecule and can therefore have a direct effect on bacterial physiology. Similarly, PGPB-synthesized gibberellins can increase plant stem growth, alter the dormancy of germinating seeds, and increase leaf and fruit senescence [5]. In the same way, PGPB-produced cytokinins are important for the establishment of interaction between plants and bacteria and also alleviate the damage engendered by different abiotic stresses [6, 7]. PGPR, which acquire the enzyme, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, facilitate plant growth and development by decreasing ethylene levels, inducing salt tolerance, and reducing drought stress in plants [8].

So far, there are many research findings and reviews focused on specific types of phytohormones produced by a specified species or different species of rhizobacteria and its growth effects on specific plants [9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20]. However, this chapter provides a comprehensive highlight of the biosynthesis of major phytohormones in diverse groups of rhizobacteria and their effects on the growth of different plant species. Hence, this chapter is tremendously important to enhance our mechanistic understanding of the diversity of phytohormone-producing rhizobacteria and their effects on plant growth for potential application in agriculture.

2. Phytohormone production in rhizobacteria

The majority of PGPR can synthesize, or modulate the concentrations of, several phytohormones. The major phytohormones produced by the diverse rhizobacteria are discussed below.

2.1 Indole-3-acetic acid (IAA)

Indole-3-acetic acid (IAA), a key plant hormone involved in regulating various physiological processes, plays a crucial role in plant growth and development. It is also a commonly produced hormone by many rhizobacteria. IAA is primarily produced via tryptophan-dependent and tryptophan-independent pathways by rhizobacteria. The study of the different IAA biosynthetic pathways has revealed that there is a high degree of similarity between bacterial and plant pathways. Six different IAA biosynthetic bacterial pathways have been identified, five of them tryptophan-dependent [21]. It is important to note that different bacteria may employ different pathways for IAA biosynthesis, and the presence of specific enzymes can vary among bacterial species or strains. Additionally, bacteria can use multiple pathways simultaneously or switch between different pathways depending on the environmental conditions and nutrient availability. The major pathways of IAA biosynthesis in bacteria are:

2.1.1 Indole-3-pyruvic acid (IPA) pathway

The indole-3-pyruvic acid (IPA) pathway in bacteria involves the conversion of tryptophan to IPA, followed by the decarboxylation of IPA to indole-3-acetaldehyde, and the subsequent oxidation of indole-3-acetaldehyde to indole-3-acetic acid (IAA). IAA biosynthesis by the indole-3-pyruvic acid (IPA) pathway in bacteria involves the following steps:

1. The first step involves the conversion of the amino acid tryptophan to indole-3-pyruvic acid (IPA) by the enzyme tryptophan aminotransferase. This enzyme transfers an amino group from tryptophan to a ketone group, resulting in the formation of IPA.

2. The enzyme tryptophan aminotransferase catalyzes the reaction by transferring the amino group from tryptophan onto a molecule called α-ketoglutarate, forming glutamate and IPA.

3. Indole-3-pyruvic acid (IPA) can be further converted to indole-3-acetaldehyde by a decarboxylation reaction. This conversion is catalyzed by the enzyme indole-3-pyruvate decarboxylase. The decarboxylation reaction involves the removal of a carboxyl group from IPA, resulting in the formation of indole-3-acetaldehyde.

4. The final step in the biosynthesis of IAA via the IPA pathway is the conversion of indole-3-acetaldehyde to indole-3-acetic acid (IAA) by the enzyme indole-3-acetaldehyde dehydrogenase. This enzyme catalyzes the oxidative conversion of indole-3-acetaldehyde into IAA, with the addition of a molecule of nicotinamide adenine dinucleotide (NAD⁺) as a coenzyme.

Several bacteria have been reported to produce indole-3-acetic acid (IAA) through the indole-3-pyruvic acid (IPA) pathway. One example is Azospirillum brasilense, a well-known plant growth-promoting rhizobacterium (PGPR), which synthesizes IAA via the IPA pathway [10]. Another bacterium of interest is Bacillus amyloliquefaciens, which produces IAA through the IPA pathway and is associated with promoting plant growth in various crops [15, 22]. Additionally, bacteria belonging to the genus Pseudomonas, such as P. putida and Pseudomonas fluorescens, have been reported to produce IAA via the IPA pathway and show positive effects on plant growth [21]. Other rhizobacteria, such as Azospirillum lipoferum, Enterobacter amnigenus, Enterobacter cloacae, Klebsiella oxytoca, and Bacillus cereus, are also known to produce IAA through the IPA pathway [23]. It should be noted that the ability to produce IAA may vary among strains within a bacterial species.

2.1.2 Indole-3-acetamide (IAM) pathway

This pathway involves the conversion of tryptophan to indole-3-acetamide by enzymes such as tryptophan monooxygenase. Indole-3-acetamide is then further metabolized to IAA through various enzymatic reactions. IAA biosynthesis by the indole-3-acetamide (IAM) pathway in bacteria involves the following steps:

1. Tryptophan uptake: Bacteria take up tryptophan, an amino acid, from their surroundings.

2. Conversion of tryptophan to indole-3-acetamide (IAM): Tryptophan is enzymatically converted to indole-3-acetamide (IAM) inside the bacterial cell. This conversion is facilitated by enzymes such as tryptophan monooxygenase.

3. Conversion of IAM to IAA: The produced indole-3-acetamide (IAM) is further transformed into indole-3-acetic acid (IAA) by the action of the enzyme indole-3-acetamide hydrolase.

4. Regulation of IAA production: The production of IAA via the IAM pathway is regulated by various factors, including environmental conditions and the presence of plant signaling molecules.

5. Release of IAA: The synthesized IAA can be released by the bacteria into the surrounding environment through diffusion or active secretion. Once released, IAA can have diverse effects on plant growth and development.

There are several bacteria that have been reported to produce indole-3-acetic acid (IAA) through the indole-3-acetamide (IAM) pathway. One such bacterium is E. cloacae, which synthesize IAA from tryptophan via the IAM pathway and have positive effects on plant growth promotion. Another bacterium of interest is Enterobacter asburiae, which produce IAA through the IAM pathway and are associated with increased root elongation and improved nutrient uptake in plants. Additionally, bacteria belonging to the genus Klebsiella, such as Klebsiella pneumoniae and K. oxytoca, were reported to produce IAA via the IAM pathway and show beneficial effects on plant growth, including enhanced root development and biomass accumulation [23]. Other rhizobacteria that produce IAA through IAM pathway include A. brasilense, P. fluorescens, Bacillus subtilis, and Rhizobium leguminosarum [21, 23].

2.1.3 Indole-3-acetonitrile (IAN) pathway

The indole-3-acetonitrile (IAN) pathway is another route through which bacteria can produce indole-3-acetic acid (IAA). IAA biosynthesis by the IAN pathway in bacteria involves the following steps:

1. Tryptophan uptake: Bacteria acquire tryptophan, an amino acid, either from their environment or through de novo synthesis.

2. Conversion of tryptophan to indole-3-acetonitrile (IAN): Inside the bacterial cell, tryptophan is enzymatically converted to indole-3-acetonitrile (IAN) through the activity of an enzyme called tryptophan aminotransferase. This involves the removal of the carboxyl group from tryptophan and the addition of a nitrile group.

3. Conversion of IAN to indole-3-acetaldoxime (IAOx): The indole-3-acetonitrile (IAN) is then converted to indole-3-acetaldoxime (IAOx) by the action of a nitrilase enzyme. This step involves the hydrolysis of the nitrile group to form an aldoxime group.

4. Conversion of IAOx to IAA: The indole-3-acetaldoxime (IAOx) is further converted to indole-3-acetic acid (IAA) through a series of enzymatic steps. These steps involve the oxidation of IAOx to an intermediate called indole-3-acetamide (IAM) and subsequent hydrolysis of IAM to IAA by an amidase enzyme.

5. Regulation of IAA production: The biosynthesis of IAA via the IAN pathway is regulated by various factors, including environmental conditions and the presence of plant signaling molecules.

6. Release of IAA: Finally, the synthesized IAA may be released by the bacteria into the surrounding environment through diffusion or active secretion.

There are several bacteria that have been reported to produce indole-3-acetic acid (IAA) through the indole-3-acetonitrile (IAN) pathway. One of the prominent bacteria known for IAN pathway-mediated IAA production is P. putida. P. putida strains have been reported to possess the nitrilase enzyme that converts indole-3-acetonitrile (IAN) to IAA, contributing to plant growth promotion. Additionally, other bacteria, such as Alcaligenes faecalis and Herbaspirillum seropedicae, were also identified for their ability to produce IAA through the IAN pathway [23].

2.1.4 The tryptamine (TAM) pathway

The tryptamine (TAM) pathway is another route through which bacteria can produce indole-3-acetic acid (IAA). The IAA biosynthesis via the TAM pathway in bacteria involves the following steps:

1. Tryptamine synthesis: The first step in the TAM pathway involves the synthesis of tryptamine, an intermediate compound. Bacteria possess specific enzymes, such as tryptophan decarboxylase, which catalyze the decarboxylation of tryptophan into tryptamine.

2. Tryptamine oxidation: After the synthesis of tryptamine, the next step involves the oxidation of tryptamine to produce indole-3-acetaldehyde (IAld). This reaction is facilitated by an enzyme called tryptamine 2-monooxygenase or tryptophan 2-monooxygenase. Molecular oxygen (O₂) acts as a co-substrate in this reaction, assisting in the conversion of tryptamine to IAld.

3. Conversion of IAld to indole-3-pyruvic acid (IPA): Indole-3-acetaldehyde (IAld) is subsequently converted into indole-3-pyruvic acid (IPA) through the action of a specific enzyme known as indole-3-acetaldehyde transaminase. This enzyme catalyzes the transamination of IAld with a keto acid, usually pyruvate, resulting in the formation of IPA.

4. Conversion of IPA to indole-3-acetamide (IAM): Indole-3-pyruvic acid (IPA) can be further transformed into indole-3-acetamide (IAM) by the action of indole-3-pyruvate decarboxylase or indole-3-pyruvate lyase. These enzymes catalyze the decarboxylation of IPA, leading to the formation of IAM.

5. Conversion of IAM to IAA: The final step in the TAM pathway involves the conversion of indole-3-acetamide (IAM) into indole-3-acetic acid (IAA). IAM hydrolase, also known as amidase, is the enzyme responsible for this conversion. IAM is hydrolyzed by IAM hydrolase to release a free carboxylic acid group, resulting in the formation of IAA.

Bacteria that produce indole-3-acetic acid (IAA) through the tryptamine (TAM) pathway have been reported in various studies. One of the well-known bacteria utilizing the TAM pathway is E. cloacae strains that possess tryptophan decarboxylase enzyme, which converts tryptophan into tryptamine and subsequently converts tryptamine to IAA, contributing to plant growth promotion [21]. Another bacterium identified for its IAA production through the TAM pathway is B. subtilis. B. subtilis strains produce IAA by the action of tryptophan decarboxylase, followed by the conversion of tryptamine to IAA [23].

It is important to note that the capacity to produce IAA through the TAM pathway can vary among bacterial strains within each species. Additionally, the production of IAA may also be influenced by various environmental factors and growth conditions. Therefore, further research is necessary to fully understand the diversity and functional significance of IAA production by rhizobacteria via the TAM pathway.

2.1.5 The tryptophan side-chain oxidase (TSO) pathway

The biosynthesis of indole-3-acetic acid (IAA) in rhizobacteria can also occur through the tryptophan side-chain oxidase pathway. The IAA biosynthesis via the tryptophan side-chain oxidase pathway in bacteria involves the following steps:

1. Tryptophan uptake: Rhizobacteria take up tryptophan from their surrounding environment.

2. Tryptophan side-chain oxidation: The first enzymatic step involves the oxidation of tryptophan’s side chain. This reaction is catalyzed by tryptophan side-chain oxidase (TSO). TSO converts tryptophan into indole-3-acetaldoxime (IAOx).

3. Indole-3-acetaldoxime (IAOx) reduction: In the next step, IAOx is reduced to indole-3-acetaldehyde (IAAld) by the enzyme IAOx reductase (IAOR). This conversion involves the transfer of electrons from a redox cofactor such as nicotinamide adenine dinucleotide phosphate hydrogen (NAD(P)H).

4. Indole-3-acetaldehyde conversion to IAA: The final step in the tryptophan side-chain oxidase pathway is the conversion of IAAld to IAA. This reaction is mediated by the enzyme indole-3-acetaldehyde dehydrogenase (IAAD). IAAD oxidizes IAAld, resulting in the formation of IAA.

Bacteria that produce indole-3-acetic acid (IAA) through the tryptophan side-chain oxidase (TSO) pathway have been identified in various studies. Examples of bacteria known for utilizing the TSO pathway are P. putida strains, and A. brasilense[23, 24]. It is important to note that the ability to produce IAA via the tryptophan side-chain oxidase pathway can vary among strains and species within genera.

2.1.6 Tryptophan-independent pathways of IAA biosynthesis

Tryptophan-independent pathways have been proposed, for both bacteria and plants, but have yet further to be studied and proven. The tryptophan-independent pathways provide alternative routes for IAA synthesis in bacteria, allowing them to produce IAA, even under conditions where tryptophan availability may be limited. Further research is required to fully understand the regulation and significance of these tryptophan-independent pathways in bacterial IAA synthesis.

Understanding the biosynthesis of IAA in rhizobacteria is crucial, as it plays a significant role in plant-microbe interactions and can contribute to plant growth promotion and disease resistance. Further research is needed to explore the regulation, genetic determinants, and functional outcomes of IAA production through the different pathways in rhizobacteria.

2.2 Gibberellin (GA3)

Some rhizobacteria produce gibberellins, including gibberellic acid (GA3). One such bacterium is Serratia marcescens. Studies have shown that S. marcescens can produce GA3 and promote plant growth, particularly in the case of rice plants [25]. Another bacterium known for its ability to produce GA3 is Bacillus licheniformis. B. licheniformis that produce GA3 stimulate seed germination and enhance plant height and biomass in crops such as wheat and maize [26].

The biosynthesis pathway of gibberellin involves several enzymatic steps, including the conversion of geranylgeranyl diphosphate (GGDP) to ent-kaurene, which is then converted to GA12. GA12 is subsequently converted to GA3 through the action of various enzymes. Based on available research, the following are generalized steps of gibberellin biosynthesis pathway in bacteria:

1. Precursor molecule: The first step is the formation of a precursor molecule called geranylgeranyl diphosphate (GGDP). This molecule serves as the building block for the synthesis of the gibberellin skeleton.

2. Conversion to ent-kaurene: The next step involves the conversion of GGDP to ent-kaurene through the action of a specific enzyme called ent-copalyl diphosphate synthase (CPS) or kaurene synthase.

3. Conversion to GA12: In the subsequent step, ent-kaurene is converted to GA12 through the action of the enzyme ent-kaurene oxidase (KO). This enzyme catalyzes the oxidation of ent-kaurene, resulting in the formation of GA12.

4. Conversion to active gibberellins: GA12 can be further converted to various active gibberellins, including gibberellic acid (GA3). The specific enzymes involved in this conversion step in bacteria are not well characterized. However, in plants and fungi, the conversion of GA12 to GA3 is regulated by a series of enzymatic reactions, such as oxidations, reductions, and rearrangements.

It is important to note that the gibberellin biosynthesis pathway in bacteria may vary depending on the specific bacterial strain and environmental conditions. Further research is needed to elucidate the specific enzymes and genes involved in the gibberellin biosynthesis pathway in PGPR and to understand their regulation and significance in plant growth promotion.

2.3 Cytokinin

Cytokinins are primarily synthesized in plant tissues, but recent studies have revealed that certain rhizobacteria can also produce cytokinins. These bacteria possess specific enzymes called cytokinin synthases, which catalyze the conversion of precursor molecules into active cytokinins. Different types of rhizobacteria, including Bacillus, Pseudomonas, and Azospirillum, have been found to produce various forms of cytokinins, such as isopentenyladenine (iP), trans-zeatin (tZ), and cis-zeatin (cZ). P. fluorescens strain G20–18 has been shown to produce various forms of cytokinins, such as isopentenyladenine (iP) and zeatin (Z), which can positively impact plant growth and development [21]. Certain species of Rhizobium also produce cytokinins, including tZ and iP, which can promote root and shoot growth, enhance nutrient uptake, and improve the overall productivity of leguminous plants [18]. B. subtilis strains produce cytokinins, particularly kinetin (K) and zeatin (Z). These cytokinins have demonstrated positive effects on seed germination, root development, and overall plant growth [17].

The production of cytokinin by rhizobacteria is a complex process influenced by various factors. Some rhizobacteria have the ability to synthesize cytokinins via de novo pathways, while others are capable of modifying existing cytokinins found in the environment. The de novo synthesis pathway involves the conversion of isopentenyl pyrophosphate (IPP) and adenosine monophosphate (AMP) into different cytokinin forms through the action of cytokinin synthases [6]. Additionally, rhizobacteria can produce cytokinins by cleaving N⁶-(Δ2-isopentenyl) adenine ribonucleosides into active cytokinins through the action of cytokinin oxidases and nucleosidases.

Based on available research, cytokinin biosynthesis pathway in PGPR involves the following generalized steps:

1. The precursor molecule for cytokinin biosynthesis in rhizobacteria is isopentenyl diphosphate (IPP). Rhizobacteria can synthesize IPP through either the mevalonate or non-mevalonate pathways.

2. In rhizobacteria, the conversion of AMP (adenosine monophosphate) to adenosine is carried out by adenosine kinase.

3. Adenosine is then converted to isopentenyladenosine (iP) by the enzyme tRNA isopentenyltransferase (Taim1), which adds an isopentenyl group to the N⁶ position of adenosine. This step is analogous to the conversion of iAMP to iP in the plant pathway.

4. In some rhizobacteria, iP can undergo further modifications to form different types of cytokinins, such as N⁶-(Δ2-isopentenyl) adenine (2iP) or trans-zeatin (tZ). These modifications are catalyzed by enzymes such as cytokinin oxidase.

The final steps of cytokinin biosynthesis in rhizobacteria are not as well understood. It is believed that additional modifications and enzymatic reactions may occur to produce different forms of cytokinins, but further research is needed to fully elucidate these steps in rhizobacteria.

It is important to note that the cytokinin biosynthetic pathway in rhizobacteria may vary among different species and strains. Additionally, the specific enzymes and genes involved in cytokinin biosynthesis in rhizobacteria are still being characterized, and there may be variations and additional steps yet to be discovered.

2.4 Abscisic acid (ABA)

Abscisic acid (ABA) is primarily synthesized in higher plants and is involved in various physiological processes, including seed dormancy, drought tolerance, and stomatal regulation. However, few PGPR strains were also reported to produce ABA. For example, A. brasilense was reported to produce ABA, which can regulate plant water status and enhance drought tolerance in different crops [27]. Certain species of Arthrobacter are also reported to produce ABA, contributing to improved water-use efficiency and stress adaptation in plants [28]. B. subtilis strains were reported to produce ABA and enhance plant stress tolerance, such as drought and salinity stress [20]. In addition, PGPR can also indirectly influence ABA levels and signaling in plants through their interactions with the plant microbiome and modulation of plant stress responses. PGPR strains reported to potentially influence ABA levels in plants are P. fluorescens, B. subtilis, Azospirillum spp., Azotobacter sp., Burkholderia spp., Rhizobium sp., and Enterobacter sp. [29].

The specific mechanisms and effectiveness of ABA production by these PGPR strains are still not well understood and require further investigation. Additionally, the production of ABA by PGPR can vary depending on environmental conditions and strain-specific factors. Research on the specific interactions between PGPR and ABA in plant-microbe interactions and further studies are needed to fully understand the role of PGPR in ABA production and signaling in plants.

2.5 Ethylene

Ethylene is a gaseous plant hormone that plays a significant role in many physiological processes, including seed germination, root initiation, flowering, fruit ripening, and response to biotic and abiotic stresses. Ethylene is predominantly produced by plants and also, certain bacteria have been reported to produce ethylene as well [30]. In Escherichia coli, Cryptococcus albidus, and a variety of other bacteria, ethylene is spontaneously produced at trace amounts via oxidation of 2-keto-4-methylthiobutyric acid (KMBA), a transaminated derivative of methionine produced in an NADH:Fe(III)EDTA oxidoreductase-mediated reaction that is enhanced under ammonia limitation (C/N = 20) [31, 32]. Formation of KMBA is proposed as a means to recover amino nitrogen from methionine, resulting in the spontaneous production of ethylene from KMBA. Another type of ethylene pathway found in Pseudomonas syringae utilizes α-ketoglutarate (AKG) and arginine as substrates in a reaction catalyzed by an ethylene-forming enzyme (EFE) [33].

In PGPR, the production of ethylene can be beneficial for plant growth promotion under certain conditions. However, many PGPR strains possess the enzyme ACC deaminase, which can mitigate the negative effects of ethylene by breaking down ACC, the precursor of ethylene, into α-ketobutyrate and ammonia. By reducing ACC levels and subsequently ethylene production in the plant, ACC deaminase-producing PGPR can alleviate ethylene-induced stress and enhance plant growth.

Some common examples of bacteria that produce 1-aminocyclopropane-1-carboxylate (ACC) deaminase are Pseudomonas spp.(P. fluorescens, P. putida, Pseudomonas aeruginosa) [34], E. cloacae [35], Azospirillum spp., Rhizobium spp., K. pneumoniae, S. marcescens, B. subtilis, and Burkholderia phytofirmans [19].

2.6 Jasmonic acid (JA)

Jasmonic acid (JA) is a plant hormone that is primarily synthesized in plants as a response to stress, such as herbivory or pathogen attack. Many plant growth-promoting rhizobacteria (PGPR) have been reported to induce jasmonic acid (JA) production in plants. PGPR stimulate JA production or exhibit JA-related effects in plants. Several species of Pseudomonas, including P. fluorescens, P. putida, and P. aeruginosa, were reported to induce JA production in plants, promoting defense responses against pathogens and insects [36]. Certain strains of B. subtilis, B. amyloliquefaciens, and Bacillus pumilus have been shown to enhance JA production in plants, contributing to induce systemic resistance against pathogens [37]. Some strains of Burkholderia exhibit JA-inducing activity in plants, contributing to enhanced disease resistance and plant growth promotion. Serratia plymuthica was reported to induce JA production in plants, promoting systemic resistance and plant growth. Certain strains of Azospirillum, such as A. brasilense and Azospirillum lipoferum, have been observed to stimulate JA synthesis in plants, resulting in enhanced growth, nutrient uptake, and tolerance to stresses [27].

It is important to note that the ability of PGPR to induce JA production can vary depending on the specific strain and plant species.

3. The role of phytohormone-producing rhizobacteria in plant growth

Generally, phytohormone-producing rhizobacteria promote plant growth directly through modulating endogenous plant hormone levels, increasing nutrient uptake, and enhancing plant tolerance to stresses. Based on the type of phytohormones produced by the rhizobacteria, the mechanisms of growth promotion also vary. The role of rhizobacteria producing the different types of phytohormones in plant growth is discussed.

3.1 The role of IAA-producing rhizobacteria in plant growth

The promotion of plant growth by IAA-producing rhizobacteria occurs through a range of mechanisms. IAA acts as a signaling molecule, participating in plant-microbe crosstalk and triggering plant responses. Rhizobacterial IAA stimulates the expression of genes involved in root elongation, nutrient uptake, and stress tolerance [21]. IAA promotes lateral root formation, making plants more efficient in accessing water and nutrients in the soil. IAA-producing rhizobacteria can enhance seed germination, increase seedling vigor, and improve plant tolerance to abiotic stresses such as drought, salinity, and heavy metal toxicity [38]. The intricate interplay between rhizobacteria-produced IAA and the host plants’ physiological responses contributes to improved crop productivity and quality.

Several IAA-producing rhizobacteria have been demonstrated to show positive growth effects on plant growth (Table 1). Rhizobium spp., including R. leguminosarum, have been found to produce IAA and promote root elongation, nutrient uptake, and overall plant growth [65]. Another example is Azospirillum spp., such as A. brasilense, which produces IAA and has been associated with enhanced root elongation, lateral root formation, and increased biomass in various crops [21, 66]. Additionally, bacteria from the genus Pseudomonas, such as P. putida and P. fluorescens, have been identified as IAA producers and have shown positive effects on plant growth, including increased shoot and root growth, improved nutrient uptake, and disease resistance [16, 67]. Therefore, IAA-producing rhizobacteria promote plant growth in multiple ways and they are potential bio inoculant.

Kinds of phytohormones	Phytohormone-producing rhizobacteria	Observed effect on plant	References
Indole-3-acetic acid (IAA)	Pseudomonas spp.	Increased the length of potato tubers and sprouting capacity	[39]
	Pseudomonas fluorescens	increased the length of coleoptiles of avena	[40]
	Pseudomonas fluorescens and Bacillus subtilis	increase root length, shoot length, root and shoot fresh and dry weight, on bacterial inoculated onion seeds	[41]
	Klebsiella strains significantly	increased root and shoot length of inoculated wheat seedlings	[42]
	Bacillus megaterium, Lactobacillus casei, Bacillus subtilis, Bacillus cereus, and Lactobacillus acidophilus,	increased growth and yield of wheat and maize	[43]
	Enterobacter spp.	increased plant biomass and enhanced; phytoextraction of metals (Ni, Zn, and Cr)	[44]
	Gluconacetobacter azotocaptans DS1, Pseudomonas putida CQ179, and Azospirillum lipoferum N7	increased root and shoot weight of corn when compared to uninoculated plants	[45]
	Microbacterium sp., Mycobacterium sp., Bacillus sp., and Rhizobium sp., Sphingomonas sp., Rhodococcus sp., Cellulomonas sp., Pseudomonas sp., and Micrococcus luteus	treatment of kidney bean cuttings with bacterial culture liquid promoted formation of a “root brush” with a location height 7.4- to 13.4-fold greater than the one in the control samples	[46]
	Pontibacter niistensis	a significant increase in the growth of cowpea	[47]
Cytokinins	Bacillus megaterium	growth promotion and root developmental responses in Arabidopsis thaliana and Proteus vulgaris seedlings	[48]
	Paenibacillus pofymyxa	promoted the growth of plants	[37]
	Rhizobium leguminosarum	promoted early seedling root growth of the nonlegumes such as canola (Brassica campestris cv. Tobin, Brassica napus cv. Westar) and lettuce (Lactuca sativa cv. Grand Rapids)	[49]
	Micrococcus luteus-chp37	increases in the number of leaves, shoot length, root length, and dry weight g-1 fresh weight in maize plants	[50]
Gibberellin	Bacillus cereus MJ-1	growth of red pepper plants (root and shoot) was enhanced	[51]
	Bradyrhizobium sp.	Phaseolus lunatus plants inoculated with the bacterium showed a marked internodal elongation	[52]
	Rhizobium leguminosarum	The Rhizobium-rice combination promotes root and shoot growth, thereby improving seedling vigor and increasing grain yield.	[53]
	Azospirillum sp. and; Bacillus; sp.	increased nitrogen (N) uptake seen after inoculation of wheat roots	[53]
	Azospirillum lipoferum	promoted the growth of both roots and shoots of maize seedlings under drought	[53]
	Acetobacter diazotrophicus	increased total carbohydrate accumulation in shoots of Sorghum bicolor	[53]
	Bacillus pumilus and Bacillus licheniformis	Both have strong growth-promoting activity (dwarf phenotype induced in Alnus glutinosa L. Gaertn. seedlings by Paclobutrazol (an inhibitor of gibberellin biosynthesis)) was effectively reversed by applications of extracts from medium incubated with both bacteria	[53]
	Bacillus licheniformis and Bacillus pumilus	enhanced growth of Pinus pinea plants	[53]
Abscisic acid (ABA)	Alcaligenes sp. and Bacillus pumilus	enhanced growth of sunflower (Helianthus annuusL.)	[54]
	Pseudomonas fluorescens	enhanced root growth, nutrient uptake, and overall wheat growth	[55]
	Bacillus subtilis	promoted a rapid recovery of the growth rates of shoots, as well as the wet and dry mass of roots potato (Solarium tuberosum L.)	[56]
	Azospirillum brasilense	treatment in maize plants enhanced plant growth, nitrogen fixation, and improved drought resistance	[28]
	Azotobacter chroococcum	induced stomatal closure, improved water-use efficiency, and enhanced plant growth in maize plants	[57]
Jasmonic acid (JA)	Alcaligenes sp., Bacillus pumilus	enhanced growth of sunflower; (Helianthus annuus L.)	[54]
	Azospirillum brasilense	treatment increased JA synthesis in maize plants, leading to improved root growth, nutrient uptake, and overall plant growth	[58]
	Bacillus pumilus	enhanced disease resistance and; overall plant growth in rice plants	[59]
	Pseudomonas; fluorescens	enhanced plant growth and stress; tolerance in Arabidopsis plants	[60]
Inhibition of ethylene biosynthesis (ACC))deaminase production)	Serratia and Aerococcus strains	most effective strains in improving the growth of wheat seedlings in water stress conditions	[61]
	Pseudomonas fluorescens biotype G (ACC-5)	eliminated the inhibitory effects of drought stress on the growth of peas and promoted growth	[62]
	Burkholderia caryophylli	increased the wheat growth and yield under an axenic condition	[63]
	Bradyrhizobium	promoted root and shoot growth as well as nodulation in a mung bean plant.	[64]

Table 1.

The effects of inoculation of some phytohormone-producing rhizobacteria on the growth of different plants.

3.2 The role of GA3-producing rhizobacteria in plant growth

GA3-producing rhizobacteria play a significant role in promoting plant growth. The production of GA3 by rhizobacteria positively influences plant growth by stimulating seed germination, root development, stem elongation, flowering, and fruit development [68]. There are several rhizobacteria that have been reported to produce gibberellic acid (GA3) and have shown effects on plant growth (Table 1). One example is the bacterium B. licheniformis, which has been found to produce GA3 and promote plant growth by stimulating seed germination, increasing stem elongation, and enhancing overall biomass production [52]. Another example is A. brasilense, a well-known plant growth-promoting rhizobacterium (PGPR), which produces GA3 and has been shown to improve plant growth characteristics, including increased shoot and root growth, nutrient uptake, and yield in various crops [14]. Additionally, GA3-producing species from the genus Pseudomonas, including P. putida and P. fluorescens, have been reported to produce GA3 and exhibit effects on plant growth, such as enhanced shoot and root development, improved flowering, and increased crop yield [9, 13]. These studies highlight the potential of GA3-producing rhizobacteria in promoting plant growth and provide insights for their utilization in agriculture.

3.3 The role of cytokinin-producing rhizobacteria in plant growth

The role of cytokinin-producing rhizobacteria in plant growth is multifaceted and can have several positive effects. Cytokinins are known to stimulate cell division and growth in plants. Rhizobacteria that produce cytokinins can enhance this process in plant roots, leading to increased root mass and overall plant growth [55]. Cytokinins produced by rhizobacteria can improve nutrient uptake in plants, particularly essential minerals like nitrogen, phosphorus, and potassium [56, 57]. This is because cytokinins influence root architecture and development, leading to increased surface area and absorption capacity. Cytokinins play a crucial role in regulating plant responses to various abiotic and biotic stresses [69]. Rhizobacteria that produce cytokinins can help enhance the plant’s stress tolerance by promoting antioxidant activity, reducing oxidative damage, and stimulating defense mechanisms (Table 1). For instance, Bacillus subtilis strain has been shown to promote growth in lettuce plants by producing cytokinins [70]. Similarly, P. fluorescens strain G20–18 has been found to stimulate shoot and root growth in Arabidopsis through its cytokinin production [71]. Azospirillum spp., including A. brasilense, have been reported to promote germination, root and shoot development in corn (Zea mays L.) and soybean (Glycine max L.) through cytokinin synthesis and other growth hormones [72]. Furthermore, certain strains of Rhizobium bacteria produce cytokinins that facilitate nodule formation and growth in leguminous plants [59]. From these findings, one can conclude that cytokinin-producing bacteria enhance plant growth, although further research is needed to understand the mechanisms by which these bacteria interact with plants and modulate cytokinin levels.

It is important to note that the effectiveness of cytokinin-producing rhizobacteria can vary depending on the specific plant species, environmental conditions, and the overall microbial community present in the rhizosphere.

3.4 The role of abscisic acid (ABA)-producing rhizobacteria in plant growth

The role of abscisic acid (ABA)-producing rhizobacteria in plant growth is multifaceted and can have several positive effects. PGPR strains that produce ABA or enhance its production in plants may help improve the plant’s ability to withstand periods of water stress and drought [29]. Treatment of different plants with P. fluorescens, which are known to produce ABA, enhanced root growth, nutrient uptake, and overall plant growth [58]. Another study by Sorokan et al. [60] showed that B. subtilis 26D in plant tissues promoted a rapid recovery of the growth rates of shoots, as well as the wet and dry mass of roots potato (Solanum tuberosum L.) after the pest attack, which we associate with the maintenance of a high level of IAA, ABA, and cytokinins in their tissues. Similarly, a study by Zeffa et al. [66] demonstrated that A. brasilense treatment enhanced plant growth, nitrogen fixation, and improved drought resistance in maize plants. Azotobacter chroococcum is another example of rhizobacteria-producing ABA and its treatment induced stomatal closure, improved water-use efficiency, and enhanced plant growth in maize plants [73].

It is important to note that the effect of plant growth-promoting rhizobacteria (PGPR) producing abscisic acid (ABA) on plant growth can vary depending on several factors, including the specific strain of PGPR, the plant species, environmental conditions, and the overall balance of plant hormones.

Further research is needed to fully understand and optimize the use of ABA-producing PGPR for enhancing plant growth and stress tolerance.

3.5 The role of ACC deaminase-producing rhizobacteria on plant growth

The role of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing plant growth-promoting rhizobacteria (PGPR) in plant growth is significant. By reducing the levels of ACC in plants, ACC deaminase-producing PGPR can modulate ethylene biosynthesis and the ethylene response in plants. Ethylene is a plant hormone that can inhibit plant growth and development, particularly under stress conditions. The reduction in ethylene promotes plant growth and development by enhancing plant stress tolerance and improving overall plant performance under stressful conditions. ACC deaminase-producing bacteria can trigger systemic resistance in plants, making them more resistant to various pathogens. This is thought to be mediated by the modulation of ethylene signaling and the activation of defense mechanisms in plants.

Several reports indicated rhizobacteria-producing ACC deaminase promote plant growth (Table 1). ACC deaminase-producing strains of P. putida have been shown to improve plant growth in various crops by promoting root development, nutrient uptake, and stress tolerance [11, 34]. Another example is E. cloacae, a beneficial rhizobacterium, which produces ACC deaminase and has demonstrated positive effects on plant growth, particularly under stressful conditions including drought and salinity [39, 40]. Additionally, species from the genus Rhizobium, including R. leguminosarumand Rhizobium meliloti, have also been reported to produce ACC deaminase and exhibit beneficial effects on plant growth, especially in leguminous crops, by enhancing nodulation, nitrogen fixation, and overall yield [41, 59].

3.6 The role of jasmonic acid (JA)-producing rhizobacteria in plant growth

Rhizobacteria that can induce or enhance JA production in plants promote growth through different mechanisms. Rhizobacteria that enhance JA production in plants can induce systemic resistance in plants, making them more resistant to diseases and pests. For instance, a study by Kumar et al. [42] demonstrated that B. pumilus treatment increased JA levels in rice plants, leading to enhanced disease resistance and overall plant growth. A study by Creus et al. [43] demonstrated that A. brasilense treatment increased JA synthesis in maize plants, leading to improved root growth, nutrient uptake, and overall plant growth. Jasmonic acid stimulates the production of secondary metabolites, such as phenols, flavonoids, and defense-related compounds. These metabolites contribute to plant defense and other physiological processes. Rhizobacteria-produced JA can enhance the production of these beneficial compounds, thereby improving plant health and resilience [44].

It is important to note that the effects of rhizobacteria-induced JA production on plant growth can vary depending on the specific plant species, environmental conditions, and the concentration of JA produced. Additionally, the indirect modulation of JA by rhizobacteria may involve complex signaling pathways in plants.

4. Conclusions

Diverse group of rhizobacteria can synthesize, or modulate the concentrations, of several phytohormones and promote plant growth in different ways. Indole-3-acetic acid (IAA) is a commonly produced hormone by many rhizobacteria primarily via five tryptophan-dependent pathways. The promotion of plant growth by IAA-producing rhizobacteria occurs through a range of mechanisms. Exogenously produced IAA by rhizobacteria acts as a signaling molecule, participating in plant-microbe crosstalk and triggering plant responses. IAA-producing rhizobacteria can enhance seed germination, increase seedling vigor, and improve plant tolerance to abiotic stresses such as drought, salinity, and heavy metal toxicity. The complex interaction between rhizobacteria-produced IAA and the host plants’ physiological responses contributes to improved crop productivity, hence, IAA-producing rhizobacteria are a potential biostimulant used as biofertilizer. Gibberellin (GA3) is produced by certain group of rhizobacteria through biosynthesis pathway that involves several enzymatic steps, including the conversion of geranylgeranyl diphosphate (GGDP) to ent-kaurene, which is then converted to GA12 and which is subsequently converted to GA3 through the action of various enzymes. The inoculation of GA3-producing rhizobacteria in plants positively influences plant growth by stimulating seed germination, root development, stem elongation, flowering, and fruit development. Cytokinins are produced in certain rhizobacteria that possess specific enzymes called cytokinin synthases, which catalyze the conversion of precursor molecules (isopentenyl pyrophosphate (IPP) and adenosine monophosphate (AMP)) into active cytokinins. Rhizobacteria that produce cytokinins can enhance this process in plant roots, leading to increased root mass and overall plant growth. Abscisic acid (ABA) is also produced by certain PGPR strains while other strains enhance its production in plant. PGPR that produce or enhance ABA production in plants improve the plant’s ability to withstand periods of water stress and drought. Many PGPR strains possess the enzyme ACC deaminase, which can mitigate the negative effects of ethylene and has been shown to improve plant growth in various crops by promoting root development, nutrient uptake, and stress tolerance. Rhizobacteria that enhance jasmonic acid (JA) production in plants can induce systemic resistance in plants, making them more resistant to diseases and pests.

Overall, the production and modulation of phytohormones by PGPR have a profound impact on plant growth, development, and stress responses. Harnessing the potential of phytohormone-producing PGPR presents a promising avenue for sustainable agriculture, as it reduces the reliance on synthetic inputs and promotes eco-friendly plant growth promotion. Further research in understanding the mechanisms by which PGPR produce and functionally modulate phytohormones will contribute to the development of effective strategies for maximizing crop yields, enhancing plant resilience, and ensuring global food security.

Acknowledgments

I am very grateful to my wife Rahel Getachew and the entire family for their encouragement and support.

Conflict of interest

The authors declare no conflict of interest.