microorganisms

Review
Plant Growth-Promoting Rhizobacteria for Sustainable
Agricultural Production
Luana Alves de Andrade, Carlos Henrique Barbosa Santos, Edvan Teciano Frezarin, Luziane Ramos Sales
and Everlon Cid Rigobelo *

Agricultural and Livestock Microbiology Graduate Program, School of Agricultural and Veterinarian Sciences,
São Paulo State University (UNESP), São Paulo 14884-900, Brazil; [email protected] (L.A.d.A.);
[email protected] (C.H.B.S.); [email protected] (E.T.F.); [email protected] (L.R.S.)
* Correspondence: [email protected]

Abstract: Rhizosheric bacteria with several abilities related to plant growth and health have been
denominated Plant Growth-Promoting Rhizobacteria (PGPR). PGPR promote plant growth through
several modes of action, be it directly or indirectly. The benefits provided by these bacteria can
include increased nutrient availability, phytohormone production, shoot and root development,
protection against several phytopathogens, and reduced diseases. Additionally, PGPR can help plants
to withstand abiotic stresses such as salinity and drought and produce enzymes that detoxify plants
from heavy metals. PGPR have become an important strategy in sustainable agriculture due to the
possibility of reducing synthetic fertilizers and pesticides, promoting plant growth and health, and
enhancing soil quality. There are many studies related to PGPR in the literature. However, this review
highlights the studies that used PGPR for sustainable production in a practical way, making it possible
to reduce the use of fertilizers such as phosphorus and nitrogen and fungicides, and to improve
nutrient uptake. This review addresses topics such as unconventional fertilizers, seed microbiome
for rhizospheric colonization, rhizospheric microorganisms, nitrogen fixation for reducing chemical
fertilizers, phosphorus solubilizing and mineralizing, and siderophore and phytohormone production
for reducing the use of fungicides and pesticides for sustainable agriculture.

Citation: de Andrade, L.A.; Santos, Keywords: food production; nitrogen fixation; phosphorus solubilization; siderophores
C.H.B.; Frezarin, E.T.; Sales, L.R.;
Rigobelo, E.C. Plant
Growth-Promoting Rhizobacteria for
Sustainable Agricultural Production. 1. Introduction
Microorganisms 2023, 11, 1088.
Plant growth-promoting rhizobacteria (PGPR) are free-living bacteria that colonize
https://doi.org/10.3390/
plant roots and promote plant growth. PGPR may promote plant growth by using their own
microorganisms11041088
metabolism (solubilizing phosphates, producing hormones, or fixing nitrogen), by directly
Academic Editor: Hitoshi Miyasaka affecting the plant metabolism (increasing the uptake of water and minerals), enhancing
root development, increasing the enzymatic activity of the plant, by “helping” other
Received: 30 March 2023
Revised: 12 April 2023
beneficial microorganisms to enhance their action on the plant, or by suppressing plant
Accepted: 18 April 2023
pathogens [1–3]. They protect plants indirectly by competing with pathogens for scarce
Published: 21 April 2023 nutrients, biocontrolling pathogens by producing aseptic-activity compounds, synthesising
fungal cell wall lysing enzymes, and inducing systemic responses in host plants. PGPR may
help plants to thrive under abiotic stress by improving the plant fitness, stress tolerance, and
pollution remediation. Additional data and greater knowledge of bacterial features driving
Copyright: © 2023 by the authors. plant-growth promotion might motivate and stir the development of creative solutions
Licensee MDPI, Basel, Switzerland. utilizing PGPR in highly changeable environmental and climatological settings [4].
This article is an open access article
distributed under the terms and 2. The Use of Unconventional Fertilizers
conditions of the Creative Commons Agricultural production’s challenge is constantly increasing agricultural production
Attribution (CC BY) license (https://
and improving its quality, processing, and storage. Plant cultivation requires increasing
creativecommons.org/licenses/by/
the yield through the effective use of mineral fertilizers. It is well known that applying
4.0/).

Microorganisms 2023, 11, 1088. https://doi.org/10.3390/microorganisms11041088 https://www.mdpi.com/journal/microorganisms

Microorganisms 2023, 11, 1088 2 of 16

mineral fertilizers of the optimal standards to the soil is important for improving soil condi-
tion, increasing its fertility, and inducing the productivity of crops [5]. Many agronomic
practices may need to be adjusted to maximize food production yield and quality. Thus,
agronomic packages must be continuously modified. In recent years, many investigators
have applied biofertilizers to minimize the environmental pollution which results from
mineral fertilizers and also to reduce their costs [6]. The use of waste to produce liquid
fertilizers in terms of sustainable agriculture is a promising practice that could help food
production. Pajura et al. [7] wrote a fascinating review discussing the challenge faced by
the fertilizer industry to produce sufficient nutrients for plant growth using more energy-
efficient and environmentally friendly methods. The production of liquid fertilizers from
waste materials that exhibit fertilizer properties is proposed as a solution to reduce the
exploitation of natural resources and implement elements of a circular economy. The review
highlights the current regulations in Poland and the European Union aimed at promoting a
circular economy and the need to obtain fertilizers containing valuable plant nutrients from
organic waste or recycled materials. The review also identifies the waste materials used as
substrates to produce fertilizers and their important chemical properties for plant growth
and development. The study also emphasizes the importance of this line of research and
the need to look for other waste groups for reuse within the circular economy framework.
Luo et al. [8] investigated the effects of a new organic–inorganic-compound fertilizer on
the growth, yield formation, and aroma biosynthesis of fragrant rice. The fertilizer was
made with organic matter, urea, superphosphate, potassium chloride, zinc sulfate, and
lanthanum chloride. The study was conducted over four years, and three treatments
were used: no fertilizer, traditional fertilizer, and the new organic–inorganic-compound
fertilizer. The results showed that the new fertilizer significantly increased the grain yield,
effective panicle number, seed-setting rate, chlorophyll content, net photosynthetic rate,
aboveground biomass, and 2-acetyl-1-pyrroline content in fragrant rice compared to other
treatments. The study suggested that the new fertilizer could achieve a high yield and
grain content in fragrant rice production. Dhawi et al. [9] discussed the benefits of using
plant growth-promoting microorganisms (PGPMs) in hydroponics and vertical farming
systems. The controlled environment in these systems allows for maximizing the use of
PGPMs. The authors recommend a synchronized PGPM treatment using a biostimulant
extract added to the hydroponic medium while also pre-treating seeds or seedlings with a
microbial suspension for aquaponic and aeroponic systems. The global market for vertical
farming is predicted to reach more than USD 10.02 billion by 2027 due to the sustainable use
of space, reduction in water use, lack of pesticides, and the implementation of user-friendly
technology for environmental control and harvesting.

3. Seed Microbiome for Rhizospheric Colonization

Seeds contain several endophytic microorganisms, especially bacteria, that the plant
selects due to their many benefits [10–12]. Initially, these microorganisms colonize the
rhizosphere, then they inhabit the plant tissue as endophytes and later are transferred
to the seeds [13]. In many sources, endophytes play a crucial role in seed germination,
conservation, and development, and these microorganisms are found in the soil. The
results suggest that the plant selects these microorganisms from the rhizosphere because
of the benefits they provide to the plant to guarantee their presence when the seeds are
planted [14]. Like any plant organ, seed endophyte colonization relies on different chemical
compositions. Moreover, the defence mechanism hinders high population density inside
the plant organ, which could provoke an infection due to quorum sensing [15,16].
Endophyte seeds are transmitted vertically from the roots to the stem. Unlike distant
rhizobacteria, bacterial endophytes interact tightly with the growing embryo in the germi-
nation stage. Seed endophytes can help the seedlings to grow and develop by solubilizing
potassium and phosphorus, generating the growth of several hormone levels, such as
cytokinin and auxin, and fixing N. Endophyte seeds also benefit plants with resistance
to biotic and abiotic stressors and better overall fitness [17,18]. Pal et al. [19] isolated
Microorganisms 2023, 11, 1088 3 of 16

twenty-three microbial endophytes (bacteria) from maize seeds, and 70% of them presented
the ability to synthesize auxin, 74% demonstrated several abilities, including the ability
to solubilize phosphate, and all the isolates showed the ability to fix nitrogen. In their
study, several isolates showed antagonistic action against phytopathogenic fungi such as
Fusarium sp. and Rhizoctonia solani, indicating their potential for biocontrol. Jana et al. [20]
identified seed rice bacteria such as Bacillus sp., Citrobacter sp., Flavobacterium sp., and
Pantoa sp., which had not previously been isolated from rice cultivar seeds. Citrobacter
produced the most indole acetic acid (IAA), gibberellin, and hydrogen cyanide (HCN)
among the isolates tested. At the same time, Pantoa demonstrated the maximum efficiency
for phosphate and potassium solubilization and ammonia production. These findings
imply that the endophytes of separated seeds can aid plant growth and development while
assisting host plants in their battle against several phytopathogens, such as fungi and
bacteria, in sustainable production.

4. Rhizospheric Microorganisms
The portion of the soil close to the roots that suffers nutritional interference from
the roots is named rhizosphere [18,21]. Plants perform photosynthesis, and depending
on the plant species, they invest 10 to 40% of their photosynthetic metabolites in the
rhizosphere through rhizodeposition. Through rhizodeposition, the rhizospheric soil is
fertilized and enriched with nutrients, amino acids, and organic energetic molecules such
as carbohydrates [22,23]. Fertilization of the rhizosphere exerts a significant influence and
changes the soil microbiota near the roots. Plants modulate rhizospheric microorganisms
through plant physiological factors that govern plant–microorganisms interactions and by
the composition of their exudates [24]. The composition of the microorganisms in the roots
is selected, and the population of the root microbiome takes place in two stages. The first
stage is rhizosphere colonization, accomplished by a subgroup of microorganisms from the
nonrhizosphere soil and bulk soil. In the second stage, the phyllosphere and endosphere
are colonized by a subset of microorganisms from the rhizosphere [25].
Several factors affect the halobionts of plants and modulate the microbiome composi-
tion. A holobiont is a set of a plant’s genome with its microbiome’s genome. Despite the
fact that unlike plants grown under different conditions, they have the same groups of
microorganisms. The group of microorganisms that persists in different plants is called the
core microbiome. The core microbiome is formed by factors common to different plants.
On the other hand, plant-specific factors result in associations with microorganisms that
are not part of the core microbiome. Rhizospheric microorganisms obtain nutrients and
energy molecules in the rhizosphere from rhizodeposition and border cells eliminated by
the roots. In this sense, the larger is the root volume the greater is the deposition and
elimination of these molecules and, consequently, the energy and nutrient availability to
the microbial population of the rhizosphere. On the other hand, a more significant devel-
opment of the plant’s shoot increases its photosynthetic efficiency and the generation of
energy molecules [26]. In this sense, these microorganisms are called phytostimulants. They
synthesize phytohormones while gaining excellent benefits for themselves and promoting
shoot and root development [27]. Phytohormones play an essential role in increasing
microorganism survival by cancelling plant defence against themselves [27,28].
Another way in which PGPR can promote plant growth is by inducing systemic
resistance (ISR) and systemic acquired resistance (SAR) in plants. These are defence
mechanisms that plants use to protect themselves against pathogenic bacteria, viruses,
and fungi [29]. ISR is triggered by non-pathogenic microorganisms and starts in the
root, extending to the shoot [30]. This defence response is dependent on ethylene and
jasmonic acid signalling in the plant. In contrast, SAR is typically activated by necrotic
pathogenic bacteria, and the signalling molecules that play important role in plant growth
and defence [31].
Microorganisms 2023, 11, 1088 4 of 16

5. Microorganisms Skills to Promote Plant Growth

As the population continues growing, commodity commercialization has been in-
creased, while the agricultural lands have been reduced due to soil degradation. The food
production sector has suffered high pressure to maintain its productivity [4]. This particular
situation requires the utilization of chemical fertilizers and pesticides. The excessive use of
these chemicals may provoke problems for the environment and human diseases. Current
agriculture needs alternatives that reduce cost production, environmental impact, and
dependence on input reduction without reducing productivity. In this way, microbial
agents, especially microorganisms, which show several abilities related to plant growth,
can be used as a helpful alternative [18,32,33].
The microorganisms might have a helpful, harmful, or neutral interaction with the
host plant. Microorganisms that provide several benefits to the plant have strong potential
for application as biopesticides and biofertilizers sustaining and improving crop protection
and output. The challenge is making farmers worldwide utilize biofertilizers and biological
control agents to reduce the use of chemical fertilizers and pesticides [4,34]. Microorganisms,
especially plant growth-promoting microorganisms, may interact with several crop plants,
improving their assistance to plant growth and development to resist pathogen attack and
to promote their development. Several metabolites produced by microorganisms have
been recognized, for commercial application, because of their helpful abilities to promote
plant growth, mass production, biocontrol efficiency, and adequate formulation [4,26].
Various biocomplexes have been identified, such as biopesticides and biofertilizers, that can
safeguard plants against both biotic and abiotic stresses. They accomplish this by generating
plant growth regulators and siderophores, improving nutrient absorption, enhancing yield,
and producing antagonistic compounds such as hydrolytic enzymes, antibiotics, volatile
compounds, and hydrogen cyanides [22].

5.1. Nitrogen Fixation for Reducing Chemical Fertilizers

Nitrogen (N) is essential for numerous crop production processes [35]. Their grain
productivity significantly depends on N input. As food demand continues growing, the
necessity of nitrogen has been increasing too [36]. Rice, maize, potatoes, and wheat are
crops that benefit from increased application of nitrogen fertilizer to improve their produc-
tivity. However, despite the relatively low efficiency in using nitrogen, which is mostly
due to processes such as ammonia volatilization, N leaching, and denitrification, rice cul-
tivation alone accounts for 21–25% of the world’s total N fertilizer application. This is
because nitrogen is the most essential macronutrient in plant physiology [37]. Nitrogen
is the most crucial nutrient required in large quantities for maize production as it plays
a significant role in the formation of amino acids, chlorophyll, adenosine triphosphate
(ATP), and nucleic acids. Therefore, increasing the application of nitrogen fertilizer for
maize cultivation is directly proportional to its yield potential [38]. Biological nitrogen
fixation (BNF) is one option for reducing reliance on chemical nitrogen fertilizers. Moreover,
BNF accounts for more than 60% of the fixed N on Earth. As a result, maximizing BNF in
agriculture is becoming increasingly important to fulfil the expanding global population’s
demand for food production. This optimization will need a thorough understanding of
the various nitrogen-fixing bacteria and their processes [39]. Jia et al. [40] identified and
used the nitrogen-fixing bacteria Kosakonia radicincitans from Pennisetum giganteum. These
researchers discovered a 25% reduction in chemical fertilizer combined with microorgan-
isms. This combination increased plant height, weight, chlorophyll content, soluble protein
content, soluble sugar content, vitamin C content, alkali hydrolysed nitrogen content, and
accessible phosphorus content. Song et al. [41] evaluated urea reduction for two years as
artificial N fertilizers replaced cyanobacteria Anabaena azotica in rice production. The results
revealed that substituting 50% urea for the cyanobacteria did not appreciably reduce rice
output. Additionally, the data revealed that traditional fertilization resulted in the highest
N loss, whereas substituting A. azotica for partial urea greatly decreased NH4+ − N and
NO3 − leaching losses. In addition, replacing 50% of urea with A. azotica towards the end
Microorganisms 2023, 11, 1088 5 of 16

of the rice season can result in better retention of soil nitrogen compared to conventional
fertilizers. This is because A. azotica has the ability to intercept, fix, and delay the release of
nitrogen, which can greatly benefit the N cycling dynamics of the soil, leading to significant
reductions in N leaching. Several studies have been conducted to evaluate the effects of
diazotroph microorganisms such as A. azotica on maize yield. Tapia-Garcia [42] discovered
the most common nitrogen-fixing endophyte, Burkholderia, associated with maize, has been
a significant breakthrough. Recent studies have confirmed that these isolates can densely
colonize maize tissues, leading to a significant increase in production. Sheoran [43] con-
ducted research to investigate maize–endophyte relationships and their influence on maize
output under both laboratory and field circumstances, and the association of Klebsiella
pneumoniae with Herbaspirillum seropedicae endophytes resulted in a considerable increase in
yield. Pandey et al. [44] experimented with local maize cultivars using Azotobacter chroococ-
cum and Azospirillum brasilense strains. Under tropical circumstances, they discovered a
considerable 1–1.5-fold increase in maize productivity.

5.2. Phosphorus Solubilizing and Mineralizing and Siderophore Production

Phosphorus (P) is a crucial macronutrient required for the growth and metabolism of
plants. However, when added to soil, P is quickly immobilized by metal cations (such as Al,
Fe, and Ca) or bound to mineral surfaces, which results in limited P availability for plant
uptake [45]. Phosphates participate in physiological and biochemical processes, such as
photosynthesis, root and stem development, flower and seed formation, crop maturation,
nitrogen fixation by legumes, and plant disease resistance. Phosphates are one of the most
important factors limiting agricultural production [46,47].
Wan et al. [48] conducted research to evaluate the potential of eight bacterial gen-
era, including Acinetobacter, Pseudomonas, Massilia, Bacillus, Arthrobacter, Stenotrophomonas,
Ochrobactrum, and Cupriavidus, to solubilize phosphorus. The results indicated that Acine-
tobacter exhibited a remarkable ability to solubilize phosphorus, making it a promising
candidate for enhancing soil fertility and quality [46]. Liu et al. [49] have shown that phos-
phorus solubilizing bacteria have the ability to secrete small molecular organic acids that
can dissolve inorganic phosphorus, which in turn can alter soil properties and indirectly
influence the microbial community in the rhizosphere. Pantigoso et al. [50] investigated the
effectiveness of bacteria such as Enterobacter cloacae, Pseudomonas pseudoalcaligenes, and Bacil-
lus thuringiensis in solubilizing plant-unavailable P in either inorganic (calcium phosphate)
or organic (phytin) forms. The study found that threonine played a vital role in promoting
bacterial solubilization and plant uptake of various nutrients. The authors also suggested
that specialized compounds exuded by these bacteria could be a promising approach to
unlock existing phosphorus reservoirs in croplands. Kour et al. [51] evaluated the abil-
ity of various genera of plant growth-promoting bacteria, including Bacillus, Enterobacter,
Pseudomonas, Staphylococcus, Acinetobacter, Klebsiella, and Proteus, to solubilize a significant
amount of phosphorus from soil samples collected from the Lesser Himalayas ecosystem.
The results indicated that these bacteria demonstrated a remarkable capacity to solubilize
phosphorus, suggesting their potential for enhancing soil fertility and plant growth. Thus,
these bacteria could be used for reducing the amount of phosphorus fertilizers.
Iron (Fe) is another essential mineral for plants. It typically occurs as Fe3+ and Fe2+ .
Iron in soil can take different forms, such as insoluble hydroxides and oxyhydroxides
in aerobic environments, making it unavailable for plant absorption. However, rhizo-
spheric bacteria secrete siderophores, which are low molecular weight iron chelators with
a high affinity for complex iron. Several plant growth-promoting rhizobacteria (PGPR)
species, including Enterobacter, Pseudomonas, Azotobacter, Bacillus, Serratia, and Rhizobium,
produce siderophores that can be either extracellular or intracellular, water-soluble, able
to solubilize iron from minerals or organic molecules under iron-limiting conditions, and
capable of forming stable complexes with heavy metals and radioactive particles. These
siderophore-producing PGPR strains are beneficial for enhancing plant growth and mitigat-
ing heavy metal toxicity in contaminated soils [52]. This capacity indirectly aids the host
Microorganisms 2023, 11, 1088 6 of 16

plant in alleviating soil-caused heavy metal stress. Plants assimilate iron from siderophores
through a variety of mechanisms, including chelating and releasing iron, direct absorption
of siderophore–iron complexes, and ligand exchange. Siderophores play a dual function in
iron sequestration and mitigation of plant stress induced by heavy metals. Pseudomonads
generate siderophores with a high affinity for ferric ions [53]. It has been demonstrated that
the formation of siderophores by biocontrol pseudomonads suppresses phytopathogens
such as Aspergillus, Fusarium, and Pythium species [54]. Pyoverdine, a siderophore gen-
erated by pseudomonads, has been shown to reduce Fusarium-oxysporum-caused potato
wilt [55]. Peanuts and maize also inhibited the phytopathogens Fusarium moniliforme, Fusar-
ium graminearum, and Macrophomina phaseolina [55]. As a result, a lack of iron intake may be
growth-limiting. In soil, Fe is mostly unavailable in a ferric oxidation state (Fe3+ ), and it is
anticipated to generate insoluble hydroxides with extremely low solubility constants, ren-
dering it inaccessible to plants and rhizospheric bacteria [56]. On the other hand, the ferrous
(Fe2+ ) state is substantially more soluble and accessible to plants, but in the environment, it
easily oxidizes into Fe3+ , precipitating [57]. To persist in iron-deficient environments, most
microorganisms have evolved a high-affinity iron (Fe3+ ) absorption mechanism involving
siderophores and low-molecular-mass organic molecules (iron chelators). Siderophores
function as iron solubilizers by combining with Fe3+ on bacterial membranes and then
reducing it to Fe2+ , making it accessible to both themselves and plants in iron-deficient
environments [58]. The siderophores are ejected and recycled for iron transport after they
are liberated inside the cells. According to Sultana et al. [59] both soil salinity and Fe
deficiency negatively impact plant stem and root development, photosynthesis, transpira-
tion rates, chlorophyll concentration, and stomatal conductance. Searching for potential
siderophore-producing, salt-tolerant PGPR could be useful for cultivating salinity-affected
regions without the use of transgenic organisms. These plant growth-promoting bacteria,
Gluconacetobacter diazotrophicus and Azospirillum brasilense, were evaluated in [60]. In their
absence, iron can create hydroxamate and catechol-type siderophores, which chelate the
metal and facilitate its absorption. Iron, which is involved in physiological processes and
is a component of several essential compounds, is required by plants. Using the growth
index, leaf and root area, greenness index, total soluble phenolic compounds, and total iron
content, this study sought to assess the contribution of two siderophore-generating bacteria
to iron nutrition for strawberry plants. Strawberry plants were grown hydroponically in
Hoagland nutrient solution with a 16 h photoperiod, iron sources were altered, and each
bacterium was introduced. On day 60, the treatments with decreased iron had the maxi-
mum growth index, root area, greenness index, and iron content, whereas those without
iron addition had the lowest values. The study showed similar results between plants
inoculated with bacteria and those exposed to oxidized iron, compared to the untreated
plants and reduced iron. After 30 days, infected plants showed decreased levels of phenolic
compounds, which were higher in the iron-free and uninoculated treatments. Iron-deficient
plants with bacterial inoculation had low concentrations of phenolic compounds. The
study also found that G. diazotrophicus and A. brasilense siderophores can enhance iron
nutrition in hydroponically grown strawberry plants. Specifically, hydroxamates were more
effective than catechols in providing iron to the plants. According to Ferreira [61], another
important aspect to consider with siderophores in the environment is their potential for
abiotic degradation, which can occur through hydrolysis and/or oxidation mechanisms.
For siderophores containing hydroxamate moieties, hydrolysis can lead to the formation
of hydroxylamine groups, which in turn can reduce Fe3+ to Fe2+ . In laboratory studies,
hydrolysed products from coprogen (a trihydroxamate siderophore) were found to be
effective iron transporters for cucumber and maize plants. All of these facts point to a
putative siderophore usage strategy in which the presence of “sacrificial” moieties may
aid in reducing, dissolving, and delivering iron to (micro)organisms. The processes of
siderophore breakdown and mineral dissolution have also been altered by sunshine expo-
sure. The presence of chelated Fe, as well as the kind of siderophore, might cause distinct
effects. According to Ghazi [62], another critical aspect to consider regarding siderophores
Microorganisms 2023, 11, 1088 7 of 16

in the environment is their susceptibility to abiotic degradation, which can occur through
hydrolysis and oxidation mechanisms. In the case of siderophores containing hydroxamate
moieties, hydrolysis can lead to the formation of hydroxylamine groups, which can then
reduce Fe3+ to Fe2+ . In laboratory studies, researchers found that hydrolysed products from
coprogen, a trihydroxamate siderophore, were effective in transporting iron to cucumber
and maize plants. Kumar [63] evaluated the impact of four organophosphate pesticides,
namely, acephate, glyphosate, monocrotophos, and phorate, on soil microorganisms that
produce siderophores or plant growth-promoting rhizobacteria (PGPR). Five siderophore-
producing soil microorganisms, namely, Rhizobium leguminosarum, Pseudomonas fluorescens,
Azotobacter vinelandii, Bacillus brevis, and Salmonella typhimurium, were tested both indi-
vidually and in combination with the pesticides. Results of the siderophore generation
test showed a dose-dependent impact, and the impacts of the pesticide mixtures were
more substantial than those of the individual pesticides. The overall sequence of unfavor-
able effects on siderophore synthesis caused by the four pesticides was phorate, acephate,
monocrotophos, and glyphosate, which was consistent with the pesticides’ toxicity levels.
The study also found that the pesticides had the least effect on the PGPR strain Pseudomonas
fluorescens (13–66%), whereas Salmonella typhimurium had the least effect (20–75%). Pes-
ticides had the following unfavorable effects on PGPR strains: Bacillus brevis (19–80%),
Salmonella typhimurium (20–75%), Rhizobium leguminosarum (21–72%), Azotobacter vinelandii
(22–81%), and Pseudomonas fluorescens (13–66%). Additionally, the combination of glycine
and monocrotophos had little or no negative impact on the PGPR strains.

5.3. Phytohormone Production for Reducing Fungicides and Pesticides

The ability of plant growth-promoting bacteria (PGPB) to produce phytohormones
such as indole-3-acetic acid (IAA), cytokinin, and gibberellin can significantly affect the
hormonal balance of plants. IAA, in particular, can directly influence the plant’s endoge-
nous reservoir of auxin. The overall effect of bacteria-produced IAA on root development
depends on the total quantity of IAA available to the plant and the plant’s sensitivity to the
hormone, which may result in either a positive or negative effect. Bacterial auxin at modest
concentrations may stimulate growth. At optimal levels of endogenous auxin, introducing
auxin from a PGPR source may inhibit or suppress plant growth. The stimulation of lateral
and adventitious root growth by bacterial IAA improves nutrient uptake efficiency. In
addition, it promotes root exudation. This cycle proceeds as increased root exudation
leads to increased bacterial proliferation. However, it is also true that IAA production
alone cannot explain a plant’s ability to promote growth because it indirectly inhibits root
elongation [64]. Khan et al. [65] have determined that the excessive use of fungicides in
agriculture can lead to a significant accumulation of active residues in the soil, resulting in
negative impacts on crop health and yield. To investigate the potential positive interactions
of radish plants with fungicide-tolerant plant growth-promoting rhizobacteria, the response
of Raphanus sativus (white radish) to fungicides in the soil was analysed. PGPR were iso-
lated from cabbage and mustard rhizospheres. The isolates of fungicide-tolerant PGPR
were closely related to Pseudomonas spp. based on their morphological and biochemical
characteristics, as well as their fragmentary 16S rRNA gene sequences. This PGPR was
resistant to high concentrations of fungicides, including carbendazim and hexaconazole.
Even when exposed to fungicides, bacterial isolates generated plant growth stimulants,
although fungicides caused surface morphological distortion and changes in membrane
permeability, as evidenced by microscopic examinations. Fungicides significantly impacted
the germination efficiency, growth, and physiological development of R. sativus, and these
effects were alleviated when the plants were inoculated with PGPR isolates. The application
of carbendazim resulted in a reduction in whole dry biomass, a 54% decrease in whole
plant length, a decline in total chlorophyll, a drop in protein content, and a 29% decrease in
Microorganisms 2023, 11, 1088 8 of 16

carotenoid synthesis. However, using isolate on white radish cultivated in soil amended
with carbendazim improved plant growth and development, increasing whole plant dry
weight by 10%, overall plant length, and total chlorophyll content. Likewise, the isolate
enhanced plant performance by reducing proline, malondialdehyde, ascorbate peroxidase,
catalase, and glutathione reductase (4%). Incorporating both isolates can be a practical
approach for remediating fungicide-contaminated soil, as well as enhancing radish plant
growth while reducing fungicide inputs. Enhazi [66] conducted a study to assess the effi-
cacy of plant growth-promoting (PGP) rhizobacterial strains that are resistant to pesticide
toxicity. The researchers isolated Pseudomonas sp. From the rhizosphere of Vigna radiata (L.)
which produced various growth-regulating (GR) substances including indole-3-acetic acid,
1-aminocyclopropane ammonia-1-carboxylate (ACC) deaminase, and siderophores. One
strain, PGR-11, was found to thrive in growth media that was supplemented with high
concentrations of metalaxyl, carbendazim, and tebuconazole. Despite increasing pesticide
concentrations, Pseudomonas sp. Continued to synthesize PGP substances. The researchers
evaluated the phytotoxicity of the pesticides both in vitro and under pot-house condi-
tions using a Vigna radiata (L.) crop. The results showed that increasing concentrations
of chemical pesticides negatively impacted the growth, physiological and biochemical
features. However, pesticide-tolerant Pseudomonas sp. Relieved the toxicity and improved
the biological attributes of the plant. Bioinoculated plants showed significant enhancement
in germination attributes, dry biomass, symbiotic features, and yield features compared
to uninoculated plants. The aim of the study conducted by Huo et al. [67] was to evalu-
ate the potential of siderophore-producing rhizobacteria in bioremediating heavy metal
(HM) contamination in Panax ginseng. In vitro tests were conducted to assess the plant
growth-promoting characteristics and HM resistance of various isolates from the ginseng
rhizosphere. Based on these tests, Mesorhizobium panacihumi, a siderophore-producing
strain, was selected as the candidate for further experiments. In planta (pot tests) and
in vitro (medium tests) experiments were then conducted to investigate the capacity of
the SPR candidate to alleviate oxidative stress and enhance HM resistance in P. ginseng.
Results from the in vitro tests demonstrated that M. panacihumi had higher HM resistance
than the other tested isolates. In the in planta studies, two-year-old ginseng seedlings
exposed to a 25 mL (500 mM) Fe solution showed lower biomass and higher reactive oxy-
gen species levels than control seedlings. However, seedlings treated with 108 CFU mL−1
for 10 min showed increased biomass and levels of antioxidant genes and nonenzymatic
antioxidant compounds compared to untreated seedlings. These findings suggest that M.
panacihumi has the potential to enhance the growth and health of P. ginseng and could be
used to remediate heavy metal contamination in ginseng fields. In the study conducted by
Gao et al. [68], three Pseudomonas bacterial strains were evaluated, isolated from the rhizo-
sphere of Fe-efficient apple rootstocks. Indole acetic acid-like substances and siderophores
were found to be released by all three strains. In alkaline soil conditions, Fe-inefficient
rootstocks treated with these Pseudomonas strains showed increased plant biomass, root
growth, and Fe content. The production of pyoverdine, a siderophore that chelates Fe3+
and improves the bioavailability of Fe to plants, was observed in these bacteria. Pyoverdine
was extracted from the bacterial culture supernatant and used in hydroponic trials with a
Fe-deficient solution. These trials resulted in a significant reduction in chlorosis induced by
Fe deficiency and an improvement in Fe absorption.

6. Nutrient Efficiency Units for Reducing Chemical Fertilizers

Over fifty percent of conventional nitrogen (N) fertilizer applied to cropping systems
can be lost to the environment, leading to water and air pollution. To sustain crop produc-
tivity without harming the environment, it is essential to implement farming methods that
ensure efficient fertilizer use. Utilizing biofertilizers with proven benefits for plant nutrition
Microorganisms 2023, 11, 1088 9 of 16

and soil health is one way to achieve this. In this context, the use of plant growth-promoting
rhizobacteria (PGPR) has gained considerable attention for improving plant nutrient uptake
and utilization. PGPR are known to promote plant growth through various mechanisms,
such as enhancing the availability of nutrients, increasing root biomass and area, and
improving the plant’s nutrient absorption capacity. Consequently, there is a growing
interest in exploring the potential of PGPR to enhance plant nutrient supply and promote
plant growth [69,70]. Biofertilizers containing PGPR are becoming more popular due to
their economic and environmental benefits. The global market for plant growth stimulants,
which include biofertilizers, is expected to grow by 12% annually [71]. In nutrient-deficient
agricultural environments, particularly in the tropics, plant development is often hindered
by insufficient nutrient availability. Most agricultural crops exhibit nutrient use efficiency
of less than 50% in many agricultural regions, exacerbating the problem [72]. Plant growth-
promoting rhizobacteria (PGPR) play a crucial role in regulating geochemical nutrient cycles
and making nutrients available to plants and the soil microbial community. Incorporating
these beneficial bacteria as bioinoculants can significantly increase nutrient availability in
the soil, reduce reliance on chemical fertilizers, minimize environmental contamination,
and promote sustainable agricultural practices [71,73].
Adopting sustainable agricultural practices that involve gradually reducing the use
of synthetic agrochemicals, increasing the utilization of biowaste-derived substances, and
harnessing the biological and genetic potential of crop plants and microbes is a viable
strategy to combat rapid environmental degradation, ensure high agricultural productivity,
and improve soil health [18]. In addition to the genetic manipulation of crop physiology
and metabolism for yield enhancement, particular members of the soil microbial commu-
nity, particularly those residing in the plant rhizosphere, may aid plants in preventing
or partially overcoming environmental stresses. The discovery and subsequent use of
biofertilizers and other microbial products, such as organic extracts and vermicompost
beverages, resulted from the search for environmentally friendly alternatives to hazardous
agrochemicals. These nontoxic and environmentally benign microbial products could
promote plant health and growth. Rahim [74] conducted an exhaustive investigation on
the effect of phosphorus on wheat and its phosphorus use efficacy. The production of grain
increased significantly. Plant growth-promoting rhizobacteria (PGPR) as biofertilizers and
biological control agents are a viable alternative to synthetic agrochemicals for crop pro-
duction [75,76]. Bashir et al. [77] determined from their research that the administration of
100 kg P per hectare of wheat has a significant impact on wheat production. It will increase
the biological productivity, plant height, number of tillers, P efficiency, harvest index, and
more. Rahim [74] conducted an exhaustive investigation on the effect of phosphorus on
wheat and phosphorus use efficacy.
The production of grain has increased significantly. Continuous research and vali-
dation are necessary for the creation of new products. The products should be evaluated
against various environmental conditions, including crop, climate, soil type, and agricul-
tural practices, in order to generate ranges of potentially useful microbial products. This
would result in a greater comprehension of their sustainable production potential and
practicability. Figure 1 shows a schematic representation of the steps required to isolate and
characterize bacteria that promote plant growth. Figure 2 shows a schematic representation
comparing uninoculated and inoculated plants with bacterial endophytes and several
abilities related to crop growth promotion and Figure 3 shows the modes of application
of PGPR. Table 1 summarises the bacterial species, abilities, experimental conditions, and
results promoted by the application in crops.
Microorganisms 2023, 11, 1088 10 of 16

Table 1. Bacterial species, abilities, experimental conditions, and results achieved by the application
in crops.

PGPR Abilities Condition Results References

G. diazotrophicus Siderophore Increased iron in
Hydroponia [60]
and A. brasilense production the plants
Siderophore
Vase with
Pseudomonas sp. production and Iron acquisition [78]
vermiculite
PGPR properties
Lysinibacillus sp.
Improved seed
and Paenibacillus Seedling protection Maize in vase [19]
germination
dendritiformis
Protection against
Bacillus subtilis Seedling protection Pot experiment Cephalosporium [62]
maydis
Increased rice
IAA production
seedling
Bacillus sp. Phosphorus Greenhouse [79]
Increase P
solubilization
availability
Mesorhizobium Siderophore Reduced soil
Pot tests [67]
panacihumi production contamination
Bacillus sp.
Phytohormones
Citrobacter sp.
production; Reduced fungal
Citrobacter sp. Greenhouse [20]
siderophore; phytopathogens
Flavobacterium sp.
hydrogen cyanide
and Pantoea sp.
Improved
Protection against
Pseudomonas sp. Greenhouse cultivation of [65]
fungicide
radish plants
Pseudomonas
fluorescens
Rhizobium Protection against
Siderophore
leguminosarum Chamber organophosphate [80]
production
Bacillus brevis pesticides
Azotobacter
vinelandii
Chemical nitrogen
Anabaena azotica Nitrogen fixation Field experiment [41]
reduction
Brucella sp. and High production
Siderophore
Pseudomonas Field experiment in iron-deficient [81]
production
brassicae soil
Increased
Bacillus Siderophore
Field experiment production in [59]
aryabhattai production
iron-deficient soil
Rhodopseudomonas Phosphorus Improved soil
Greenhouse [82]
palustris solubilization fertility
Microorganisms 2023, 11, 1088
Microorganisms 2023, 11, x FOR PEER REVIEW 11 of 16
11 of 16

Microorganisms 2023, 11, x FOR PEER REVIEW 12 of 16

Figure 1. Schematic representation of the steps required to isolate and characterize bacteria that
Figure 1. Schematic
promote representation of the steps required to isolate and characterize bacteria that
plant growth.
promote plant growth.

Figure 2. This schematic diagram compares uninoculated plants with those that have been inoculated
Figure 2. This schematic diagram compares uninoculated plants with those that have been
with bacterial endophytes, illustrating several important benefits of this process for promoting plant
inoculated with bacterial endophytes, illustrating several important benefits of this process for
growth in crops. These benefits
promoting plant growthincludein increased aerial
crops. These growth,
benefits reduced
include susceptibility
increased to disease,
aerial growth, reduced
susceptibility
enhanced nutrient to disease, root
uptake, improved enhanced nutrient
growth, uptake,
reduced improved
presence root growth,
of harmful reduced presence
phytopathogens, and of
harmful phytopathogens, and induced systemic resistance. By harnessing the power
induced systemic resistance. By harnessing the power of beneficial bacteria within plants, farmers of beneficial
bacteria within plants, farmers can ensure healthier and more productive crops, leading to higher
can ensure healthier andbetter
yields and morefood
productive
security. crops, leading to higher yields and better food security.
 Figure 2. This schematic diagram compares uninoculated plants with those that have been
inoculated with bacterial endophytes, illustrating several important benefits of this process for
promoting plant growth in crops. These benefits include increased aerial growth, reduced
susceptibility to disease, enhanced nutrient uptake, improved root growth, reduced presence of
harmful phytopathogens, and induced systemic resistance. By harnessing the power of beneficial
Microorganisms 2023, 11, 1088 12 of 16
bacteria within plants, farmers can ensure healthier and more productive crops, leading to higher
yields and better food security.

Figure 3. Modes of application of PGPR.

Figure 3. Modes of application of PGPR.
7. Future Perspectives
Plant growth-promoting rhizobacteria (PGPR) are a group of beneficial soil bacteria
that colonize the root surface and promote plant growth and health via multiple mech-
anisms. PGPR can enhance plant growth by increasing nutrient availability, producing
plant growth hormones, stimulating root development, and protecting plants from diseases
and parasites. Plant growth-promoting rhizobacteria (PGPR) have a bright future. These
beneficial bacteria in agriculture and horticulture are gaining popularity due to their po-
tential to improve plant growth and reduce the use of synthetic fertilizers and pesticides,
and improve soil health. Future PGPR research will likely concentrate on developing new
strains of bacteria that are more effective at promoting plant growth and elucidating the
molecular mechanisms through which PGPR interact with plants. This could contribute to
developing agricultural practices that rely less on chemical inputs and are more efficient
and sustainable. The use of PGPR in biofertilizers and biopesticides is also anticipated to
increase. Biofertilizers containing PGPR can improve plant growth and yield by adding
nutrients to the soil and enhancing its fertility. Biopesticides containing PGPR can aid in
the sustainable and environmentally benign control of plant maladies and parasites. In
addition, the use of PGPR in crop breeding and genetic engineering could create cultivars
that are more resistant to abiotic and biotic stresses, such as drought, salinity, and plant
diseases. This could contribute to establishing more resilient and sustainable crop varieties
that can withstand changing environmental conditions and contribute to food security.
PGPR offer a sustainable and environmentally benign alternative to conventional agricul-
tural practices and have the potential to contribute to developing more sustainable and
resilient agriculture.

8. Conclusions
This review emphasizes the potential of biologically dependent instruments, specifi-
cally PGPR, to assist in addressing global food production issues. Before these tools can be
applied to real-world situations, it is evident that there are significant knowledge deficits
that must be filled. PGPR could be the key to sustainable crop productivity and efficient
nutrient management.
Microorganisms 2023, 11, 1088 13 of 16

Funding: We thanks Fapesp: process number: 2021/10821-8.

Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.

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