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Rhizosphere competence and applications of plant growth-promoting rhizobacteria in food production – A review

March 2024
Scientific African 23(1):e02081

March 2024
23(1):e02081

DOI:10.1016/j.sciaf.2024.e02081

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CC BY 4.0

Authors:

Blessing Chidinma Nwachukwu-Igiehon

University of the Witwatersrand

Olubukola Oluranti Babalola

Ahmed Idris Hassen

Agricultural Research Council, South Africa

Some commercially produced PGPR, mechanisms of action, and plant responses.

…

Some PGPR use as a biocontrol agent against diseases and pathogens of different plants.

…

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Content uploaded by Olubukola Oluranti Babalola

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Scientic African 23 (2024) e02081

Available online 11 January 2024

(http://creativecommons.org/licenses/by/4.0/).

Rhizosphere competence and applications of plant

growth-promoting rhizobacteria in food production – A review

Blessing Chidinma Igiehon

, Olubukola Oluranti Babalola

Ahmed Idris Hassen

Food Security and Safety Focus Area, Faculty of Natural and Agricultural Sciences, North-West University, Private Mail Bag X2046, Mmabatho

2735, South Africa

School of Molecular and Cell Biology, Faculty of Science, University of the Witwatersrand, Private Bag 3, Johannesburg, 2050, South Africa

Agricultural Research Council, Plant Health and Protection (ARC-PHP). P. bag X134, Queenswood 0121, Pretoria, South Africa

Department of Plant and Soil Science, Faculty of Science, Engineering and Agriculture, University of Venda. P. bag X5050, 0950 Thohoyandou,

Limpopo, South Africa

ARTICLE INFO

Editor: DR B Gyampoh

Keywords:

Agricultural sustainability

Agro-products

Chemical inputs

Climate smart agriculture

Plant-microbial interactions

Rhizosphere colonization

ABSTRACT

Sustainable food production, among other non-intensive production systems, involves the

important interactions of myriads of plant growth-promoting microorganisms, plant, soil, soil

fauna, and production of utilizable carbon in the rhizosphere capable of enhancing soil health,

plant growth, and protection that lead to increased crop productivity. Plant growth-promoting

rhizobacteria (PGPR) including symbiotic rhizobia and free-living rhizobacteria possess traits

that help to enhance plant growth due to their many modes of action that start with the ability to

colonize both the intracellular and extracellular rhizosphere niche in their search for a carbon

source and reduction in the free use and quantity of agrochemicals. In the past few decades, the

focus on developing biosafety agro-products has shifted from agrochemical-based applications to

a more sustainable system without posing negative impacts on the soil microora or fauna. The

present review focuses on the application of PGPR inoculants on soils and seeds to improve

biological nitrogen xation, solubilization of phosphate, and secretion of phytohormones

required for growth, especially application in a pressured environment. We discuss how PGPR

enhances nutritional regulation and hormonal balance in plants, bacterial taxa enrichment, and

improvement of carbon sources utilization benecial for plant growth. We highlight the antag-

onistic and synergistic interactions with microorganisms within the rhizosphere and beyond in

bulk soil which indirectly boosts plant growth rate and induces resistance against phytopatho-

gens. While soil-borne pathogens continually oppose the functions of these microorganisms,

PGPR has improved diverse strategies in the form of agro-compatibility, root colonization,

nutrient, iron, and space competition, systemic resistance, antibiotics synthesis, lytic acid,

hydrogen cyanide, and siderophore production for advanced food production. Finally, we high-

lighted the roles of PGPR in phytoremediation, techniques of applying microbial inoculants to

enhance plant growth and commercialization of PGPR products and the challenges developing

countries have to defeat.

* Corresponding author.

E-mail address: olubukola.babalola@nwu.ac.za (O.O. Babalola).

Contents lists available at ScienceDirect

Scientic African

journal homepage: www.elsevier.com/locate/sciaf

https://doi.org/10.1016/j.sciaf.2024.e02081

Received 21 September 2022; Received in revised form 5 January 2024; Accepted 9 January 2024

Scientic African 23 (2024) e02081

Introduction

Intensive agricultural practices that include the prolonged use of inorganic fertilizers and chemical pesticides have led to huge

agricultural and ecological damage. The excessive use of chemical fertilizers exerts damaging impacts on soil microorganisms, altering

the fertility status of soil and polluting the environment. The progressive increase in human population is projected at more than 9

billion by 2050 worldwide. According to the United Nations, Africa’s share of the global population is predicted to grow from 17% in

2020 to 26% by 2050 and 39% by 2100, while Africa’s most populous nation, Nigeria population is expected to surpass that of the

United States by the 2050 [1,2].

Sustainable food production has become the main need to improve food security globally, particularly in developing nations.

Ensuring food security is one of the challenging tasks faced by many nations in developing countries. Such challenge faced by mankind

in the past decades has resulted in an impending negative effect on the human race which needs to be addressed without delay [3]. One

of the problems in addressing food security is that the ecosystem is already under stress and more people are undernourished. This

makes it very difcult to conquer the challenge of food security in many developing nations [4].

Moreover, the majority of farmers especially in developing nations practice substantive farming, but nowadays the rise in

mechanized farming practice and the use of agrochemicals as external inputs are out of control, which adversely affect the soil

environment and biodiversity [5,6]. Crop yield in the majority of the developing nations is the lowest compared to the developed

nations of the world. Many of these developing countries lose crops worth billions of US dollars yearly; the intensive agricultural

practices destroy the ecosystem, land degradation, diseases, and pest infestation. Still, some countries in developing countries such as

Nigeria, South Africa, Zambia, Ethiopia, Mozambique, and Liberia rely on agriculture and have experienced an increase in their gross

domestic product (GDP) growth in agriculture [7].

Although the advantageous outcomes of chemical-based fertilizers and pesticides are instantaneous, the indiscriminate and pro-

longed usage of these harmful chemicals in agriculture is dangerous [8]. Articial chemical inputs in the form of chemical fertilizers

and pesticides destroy the soil structure, resulting in the depletion of available nutrients, contamination of water resources that alter

the soil biological population, and degradation of the environment [9,10]. They ultimately pose negative impacts on crop yield and

increased susceptibility towards biotic and abiotic stresses. Furthermore, humans are exposed to these harmful chemicals through the

possible entrance from the food chain as heavy metals [11]. The resultant effects of these dangerous chemicals used for agricultural

purposes over time cause illnesses including cancers in humans and also pollute the environment [8].

The progressive increase in food production is essential for the development and continuity of developing countries and poor

economies. Recently, many new agricultural technological innovations have evolved and should be implemented by policymakers

because the growth and development of nations would rely on advanced and environmentally friendly technologies such as hybrid

disease-resistant species, modern management practices, and climatic modied seeds [9,12]. The acceptance of these technologies by

farmers is quite slow, due to some negative consequences over time, high cost, and dependability. With respect to these concerns, the

use of novel agricultural benecial microorganisms for sustainable agriculture will be an alternative strategy to increase crop yield

without having any long-term negative effects on the ecosystem [13,14].

Rhizosphere competence refers to the ability of any microorganism to grow, function, and compete with others for critical nutrients

and exudates generated by plant roots, as well as their ability to colonize the root surface of host plants in rhizospheric soil [9,12]. Most

indigenous soil microorganisms, in particular rhizobacteria residing in the vicinity of plant roots, perform different benecial in-

teractions with plants and play critical roles in sustainable agriculture by improving soil quality and health, and making nutrients

readily available to plants [15]. These distinctive groups of microorganisms possess characteristics to stimulate plant growth due to

their interactions with the rhizosphere and are called plant growth-promoting rhizobacteria (PGPR) [16,17]. PGPR interacts and

carefully selects their mutual partners through natural selection, creation of host specicity, and sensitivity to environments where

microbial diversity is few [18]. PGPR improves plant growth through different mechanisms such as increasing the availability of

nutrients to plants and producing essential metabolites without inuencing the environment negatively. Additionally, PGPR stimulates

the solubilization of phosphorus and other nutrients, increases iron acquisition in plants through the production of siderophore,

produces antibiotics and other compounds that prevent the growth of phytopathogens, bioremediation of contaminated soils, can help

plants tolerate abiotic stress such as extreme temperatures, salinity and drought, and also mitigate the adverse effects of various

stresses [9,10].

Most PGPRs can survive adverse environmental conditions such as drought, salinity stress, unavailability of nutrients, and high

heavy metal contamination [9]. PGPR triggers major biological functions in the soil but also have been engineered to improve crop

productivity through healthy competition in the soil and breakdown of nutrients [8,19]. Plant growth-promoting rhizobacteria (PGPR)

have been found to have numerous benecial effects on plant growth, health, and development, as well as on the environment. The

application of PGPR in sustainable agriculture and environmental remediation has the potential to improve crop nutrition, increase

crop production, enhance crop yield, and disease management, and mitigate environmental hazards caused by the misuse and overuse

of chemicals. However, the efcacy of PGPR in promoting plant growth and development depends on the particular bacterial strain

and the conditions in which it is used. Consequently, the selection of a specic strain is critical in obtaining maximum benets in terms

of improved plant growth and development [10,16,17]. This review aims to present the various mutualistic interactions of PGPR with

plant roots in the rhizosphere, its major plant growth-promoting traits, and mechanisms of action, as well as the commercialization of

PGPR products and the challenges developing countries have to overcome, are also discussed.

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

Rhizosphere: the ‘epicenter’ of microbial activities

The rhizosphere region connects the plant roots to the soil from which organic and inorganic substances and signaling molecules

are transferred into other soil regions allowing lasting mineralization processes controlled by agricultural important microorganisms

and their activities [20,21]. The rhizosphere houses numerous groups of organisms interacting with the plants and other

Table 1

Some commercially produced PGPR, mechanisms of action, and plant responses.

PGPR Product/ Country Plant Mode of action Plant response References

Paenibacillus helianthi sp. nov.,

Streptomyces sp., B. subtillis

BIOVED, AgBio, USA,

Hungary, Italy

Sunower Nitrogenase activity;

nitrogen xation

Increased nutrient content and

dry weight

[26–28]

thivervalensis, Azospirillum,

brasilense, Paenibacillus

polymyxa,

Lipoferum, Pseudomonas

putida, Serratia

marcescen, P. uorescens,

AtEze, Spot-Less,

BlightBan, frostban,

Bio-save- USA, India,

Iran, Pakistan, Brazil

Maize (Zea

mays)

The hydrolytic enzyme,

phosphate solubilization,

Siderophore and IAA

production

Increase tolerance to salt;

Increase plant leaf and height

[10,29]

Pantoea agglomerans RK-92,

, B. megaterium TV-91C,

B. subtilis TV-17C, B.

megaterium TV-87A,

Bacillus megaterium TV-

3D, B.

megaterium KBA-10

EcoGuard, Kodiak,

Subtilex, Yeild-Shield,

Companion, Bioyield,

-USA, Turkey

Cauliower

(Brassica

oleracea L.)

Nitrogen xation,

Phosphate solubilization,

IAA production

Nitrogenase activity, phosphate

solubilization,

IAA production,

Increased mineral nutrient uptake

[29]

Bacillus, B.

amyloliquefaciens, Bacillus

subtilis, B. pumilus,

P. uorescens,

Serratia marcescens

BIOVED, HiStick N/T,

Mepplus– USA, Brazil,

India, Egypt, Hungary

Tomato

(Solanum

lycopersicum)

Siderophore and IAA

production, phosphate

solubilization

Nitrogen xation,

antiviral activity

Increased crop yield and nutrient

uptake,

nutrient content,

biologically controls viral

pathogens

[29]

B.cereus, E. cloacae, B acillus

drentensis, Providencia

vermicola

Ama-2, Rhizobium, B.

pumilus Sol-1,

Brevundimonas

Kro13, Alcaligenes sp.

Mal-4,

Kluyvera ascorbata

SUD165, P.

putida, Ochrobactrum,

Sonata, Serenade-

USA, Saudi Arabia,

India,

Egypt, Pakistan,

Bangladesh

Mung bean

(Vigna radiata)

N-xing and phosphate

solubilization Siderophore

and IAA production,

Activities of nitrogenase,

ACC-deaminase, and

acetylene reducing

Increases nutrient uptake,

Enhance gaseous

exchange, photosynthetic

pigments, and water retention.

Improved growth and

seed yield, Increases the

stimulation of mung bean plant

growth reduces Pb and Cd uptake

decreases the toxic effect of

chromium to seedlings by

reducing Cr (VI) to Cr (III)

[30]

Bacillus spp.,

B. amyloliquefaciens

Germany, USA, Iran,

China

Cotton

(Gossypium)

Antibiotic activity; N-xing

and

phosphate solubilization,

Production of plant

hormones

(auxins, cytokinins, and

gibberellins)

General improves growth and

biocontrol of phytopathogens

[31]

Bacillus simplex T7,

Pseudomonas putida BA-8

Ecosoil-USA, Turkey Grapes

(Vitaceae

family)

Antibiotic activity, IAA

production, phosphate

solubilization,

N- xation

Promote

grafting capacity at

nursery conditions

[26,29]

B. polymyxa (LAB/BP/01)

B. subtilis

Inomix ® biostimulant

Spain

Cereals Production of antimicrobial

compounds and metabolites

induced plant resistance to

pathogens, uptake of

nutrients

Improve plant growth and control

of pathogens

[27]

Azospirillum sp. Nitrox ®Cuba Wheat, barley,

carrot,

maize, cabbage

Secretion of hormones,

nitrogen xation

Enhance nutrient and water

uptake, stimulate root

development, generally promote

plant growth

[32]

B. subtillis BR62, Rhizobium sp.

base formulation

Peanibacillum durus PD74

Micosat F® cereal

Italy Mamezo®,

Processing Seeds®,

Hyper Coating Seeds

® Japan

Tomato,

soybean,

cereals, beet,

legumes,

sunower

Nitrogen xation, HCN

production, produce

enzymes that can destroy

the cell wall of pathogenic

fungi

Increase plant height, shoot dry

weight and nodules

[21]

Azotobacter, P. uorescens,

phosphobacteria

Greenmax Agro Tech

Life, Gmax, Biosink

-India

A wide range of

plants

Nitrogen xation Solubilize

phosphate, produce

siderophore, alkaline

phosphatase and IAA

Increase crop yield, nutrient

uptake, resistant phytopathogens

[33]

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

microorganisms, such as archaea, bacteria, fungi, and their environment [22]. Most microorganisms found in the rhizosphere improve

plant growth through different mechanisms.

Plants typically secrete and discharge a signicant amount of carbon xed by photosynthesis, and the soil microbial community

and their roots use the majority of these discharged materials known as root exudates, which include primary metabolites (organic

acids, sugars, inorganic ions, vitamins, amino acids, enzymes, purine, and gaseous molecules) as a source of food [9,10]. Collection of

these root exudates has been performed using both qualitative and metabolomic approaches, including sampling root exudates from

plants grown on soil and obtaining root exudates from in vitro cultures or hydroponic grown plants. However, in root exudates the

composition of soil will be instantly changed which is attributed to their adsorption to the soil particles as well as microbial degra-

dation, actually, the exudation from soil microbial communities also modies plant exudation prole [23]. Due to the challenges of

root exudation from plants grown in the eld and the low reproducibility of the process many factors inuence the exudation process

such as biotic and abiotic stress conditions like toxic ions, such as trace elements (heavy metal ions), extreme temperature, high salinity

(generating both ion toxicity and osmotic stress), nutrient starvation (P deciency) and water status, has led to other approaches which

exclude the extension of soil-culture [7].

Plant culture in articial eld conditions can modify exudate composition, factors such as aeration in vitro culture or hydroponic

cultures in temporary immersion systems (ITS) have impacted on root exudate composition and plant development. The main benet

of these in vitro sterile systems is the reproducible exudation pattern which is important to understand the effects of stress factors and

nutrient deciency [24]. Hence, some researchers highly recommend this method for exudate collection to prevent the presence of

rhizosphere microorganisms with the ability to affect the composition of root exudate [25]. In some cases, root exudates are collected

from in vitro or hydroponic cultures using plants grown in the soil while in most studies root exudation is from in vitro or hydroponic

cultures, where the liquid medium containing compounds is obtained. In respect to this, root exudates are collected by various

physicochemical processes, which include through sorption lters buried in the ground [26] or extraction processes with different

solid or chemical-phase extraction. The in vitro methods allow the culture of excised organs such as shoots or roots or entire plants.

However, this can inuence root exudate composition, because many studies have reported that root exudation is affected by the

presence of shoots in the culture, as they are in control of the CO

absorption by photosynthesis. In some plants such as watermelon

[27], and a combination of eggplant and tomato [28], the modication in the aerial tissues and as changing the scion of grafted plants

were reported to affect root exudation processes.

Moreover, traditional stationary methodologies of culture for obtaining root exudates from in vitro-cultured plant tissues. Recently,

many automated TIS have evolved, some allow forced ventilation, CO

enrichment, culture hairy roots and cell suspensions. The rst

and one of the most commonly used systems is RITA® (Recipient `

a Immersion Temporaire Automatique) which was originally

developed for plant mass propagation and also has been approved for metabolites from root culture capable of reducing hyperhydricity

challenges in plant material grown in vitro. The major advantage is that ITS substantially increases metabolite and biomass production,

hence their use for obtaining specic metabolites from root exudates. Some metabolites obtained from root cultures using TIS are

betalains from Beta vulgaris (beet) having colorant and antioxidant properties [24].

These plants’ exudates have various available nutrients, playing a signicant role in attracting different groups of microorganisms

to the rhizosphere [19]. Besides, the available nutrients in plants, they also depend on the interactions among microorganisms in the

rhizosphere using these exudates, thereby creating a connection between microorganisms and plants [29]. The capability of micro-

organisms to colonize the host plant roots and improve soil health is determined by the efciency and success of PGPR as an inoculant

for crops [30]. Examples of commercially available PGPR are listed in Table 1. Only microbial species that can strive and survive the

competition in the rhizosphere are effective in expressing many genes and communication between cells through quorum sensing (a

cell-to-cell microbial communication process that uniquely controls various physiological and metabolic activities) can emerge as

promising PGPR [18].

Benecial plant-microbial interactions that exist in the rhizosphere between the plant roots and the microorganisms can be

mutualistic (both organisms benet from each other), commensalistic (one of the organisms benets, while the otherobtains neither

benet nor harm), and amensalistic (one of the organisms is harmed while the other is unaffected) forming the bases for rhizobacteria

to improve crop yield [6]. However, for rhizobacteria to be classied as PGPR, it must be able to colonize the root surface, to can

survive, proliferate, and compete with other indigenous and nonresident microbiota [34]. Above all, it should promote plant growth

[35]. In our recent study, Firmicutes (17 to 51%), Proteobacteria (18 to 36%), and Actinobacteria (7 to 38%) were the most abundant

PGPR characterized in the sunower rhizosphere soil. These rhizosphere microbiomes are part of the complex food web that utilizes

the large quantity of nutrients released by the plant and have been widely recognized to enhance plant health and growth [34]. Similar

studies have postulated that plants may modify the rhizosphere microbiome to their advantage by selectively stimulating microor-

ganisms with distinctive features that are benecial to plant growth and health [5,6]. In the rhizosphere, many bacterial species have

been recorded to symbolically interact with host plants as a result release organic plant growth-promoting substances in the form of

exudates as important nutrients for soil bacterial growth and metabolic roles. This has been achieved by studying various microbial

species, and their functional roles through next-generation sequencing techniques, the plant cultivars, and the rhizosphere. PGPR

demonstrates different mechanisms of action generally to promote plant growth either directly or indirectly, or both [36].

PGPR improves plant growth directly by enhancing nutrient acquisition, mainly essential minerals such as phosphorus, vitamins,

and nitrogen from the environment. Furthermore, other growth factors such as enzymes, water, production of growth hormones,

solubilization of phosphorus, and iron sequestration by siderophore in the absence of pathogens [37,38]. Indirect mechanisms reduce

the effects of plant pathogens by protecting plants from phytopathogens. Indirect mechanisms such as competition, production of

antibiotics, antifungal metabolites, production of hydrogen cyanide, siderophore, and induced systemic resistance indirectly promote

plant growth [39].

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

Kloepper and Schroth [16] postulated how PGPR alters the rhizosphere niche; the authors buttressed the diverse effects of PGPR on

plant growth and development upon inoculation [36]. The application of microbial inoculants, such as PGPR is benecial for stim-

ulating plant roots for growth, pest control, plant stress control, and destruction of plant diseases leading to agricultural productivity

[37,38]. Plants naturally can ght against diseases, but the application of microbial inoculants as biocontrol agent help advance these

abilities.

Besides, numerous live microorganisms, such as Rhizobium, Anabaena, Pseudomonas, and Azotobacter species are used as microbial

inoculants to improve nutrient uptake and nutrient pool. These microbial inoculants can be incorporated into soil, seeds, and plants for

enhancing biofertilization and biostimulation serving as an eco-friendly and substitute to chemical fertilizers [39,40]. The synergistic

effect caused by microbial inoculants, and resident microorganisms improves plant nutritional activities that involve breaking down,

solubilization, and mobilization of nutrients, hence increasing crop yields have reduced the use of chemical fertilizers. The acceptance

and application of microbial inoculant as plant improving agent is spreading widely in many developed countries where agriculture is

the key driver of the economy [41]. Nevertheless, despite the numerous benets of PGPR, there are some toxic effects associated with

the use of PGPR, for example, when PGPR is used in contaminated soils may lead to the release of heavy metals into the environment

[8]. It is important to note that the toxic effects of PGPR are not well documented, and more research is needed to fully understand the

potential risks associated with their use. The overall benets of using PGPR in agriculture and environmental remediation outweigh

the potential risks, but caution should be exercised when selecting and using a particular bacterial strains [9,10,16,17].

Direct mechanisms of plant growth promotion by PGPR

Biofertilization

Biofertilization refers to the application of microbial inoculants on soil, plant surfaces, or seeds, which is important to enhance crop

production. The microbial inoculants colonize the rhizosphere and supply essential nutrients required for plant use resulting in

improved plant growth. The application of microbial inoculant improves the soil texture, such as soil porosity and soil aggregate

structure, etc. These biofertilizers with relatively low density have no negative impacts on the environment and are non-toxic in even

high concentrations without having any adverse effects on crops and underground water because they do not contain heavy metals

such as arsenic, mercury, lead, vanadium, and cadmium. Studies have proved that these heavy metals could alter the composition and

diversity of soil microbial population and nutrient cycling [42]. Ultimately, these chemicals could nd their way into the food chain

causing diseases such as stomach cancer [43].

Biofertilizers are formulated products of microbial inoculants in a liquid or powdered carrier containing PGPR as the active

ingredient which, when applied to the seeds or into the furrows,enhances plant growth and increases yield, in a wide range of agri-

cultural crops [42]. Many studies have documented the critical role biofertilizers play in maintaining soil health, promoting long-term

soil fertility, increasing organic farming, and reducing the use and application of chemical fertilizers [39,40]. To use biofertilizers,

there must be an efcient formulation of microbial inoculants, proper selection of suitable carriers, and construction of adequate

application methods.

In a study by O Babalola and A Akindolire [44] which characterized PGPR from rhizospheres of eight food crops plants in South

Africa, different PGPR strains belonging to Burkholderia gladioli, Vibrio uvialis, Serratia plymuthica, Pseudomonas uorescens, B. cepacia,

P. putida, S. caria, P. luteola, Erwinia spp, Aeromonas hydrophila, Rahnella aquatilis, Acinetobacter baumannii, A. calcoaceticus, Escher-

ichia vulneris, Proteus penneri, Ewingella americana, and Shigella spp. were being used with productive effects as biofertilizers. All these

strains produced hydrogen cyanide and ammonia to indicate their functions as biofertilizers in increasing crop productivity

Nitrogen xation

Nitrogen (N) is one of the most essential nutrients for plant growth and development that ultimately increases crop productivity.

Although atmospheric air is composed largely of N gas (N

) at 78 %, N is one of the most limiting nutrients for crop production

worldwide [45]. This is because atmospheric nitrogen (N

) is very stable due to the strong triple bond between the two N atoms that

require a large amount of energy to break, and thus plants cannot convert it to its usable form [46]. Only a few prokaryotic organisms

called diazotrophs have the enzymatic machinery to break the strong bond that held the two N atoms. Atmospheric N

is biologically

xed through symbiotic means by the root nodulating Rhizobia group or non-symbiotically by the free-living PGPR strains such as

Azospirillum and Azotobacter spp. and endophytes such as Cyanobacteria (Gluconoacetobacter diazotrophicus, Anabaena, Noctoc and

Azocarus) provide 7 and 80 kg N

per hectare annually [47]. This process of converting atmospheric N

into a usable form of N by the

enzymatic action of diazotrophs described above is called Biological Nitrogen Fixation (BNF).

The BNF is an economically benecial and eco-friendly alternative to chemical fertilizers and accounts for up to 290 million tonnes

of N per year providing N to plants [48]. For many years, rhizobia inoculants have been used for cultivating legumes as biofertilizers.

Like the developed world, many sub-Saharan African countries such as South Africa and Namibia use rhizobia inoculants for N uptake.

Due to its economic benets, rhizobia have been widely used as a substitute for chemical fertilizers frequently used to boost the

production of legumes [7].

The mechanism of N xation requires a complex enzyme system such as nitrogenase mainly encoded by the nif genes. The nif genes

are structural genes involved in the Fe protein activation, donation of an electron, activation of iron-molybdenum, and stimulation of

plant regulatory genes needed for the synthesis and function of enzymes [49]. The nif genes are primarily found as a cluster of around

20–24 kb with about seven operons of 20 proteins variants. The advantageous impacts of nif genes have been well documented. Some

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

studies have also proved that nif genes can improve N xation through genetic engineering. However, others argued how N xation

traits of plants could be enhanced and harnessed [7,50]. Nevertheless, the focus of these methods is still on promoting plant growth

and sustaining N levels in the soil. A diazotroph is any microorganism that can grow without any source of external N. Diazotrophic

microorganisms provide to the host plant xed N that can be exchanged for xed carbon which is then released as root exudates [51,

52].

Mineral solubilization and nutrient uptake

For a plant to grow optimally there is a need for adequate mineral nutrient supply. However, even with the presence of mineral

nutrients in the soil, plants may still show deciencies because of the unavailability and insolubility of essential mineral nutrients to

support plant growth. PGPR solubilizes mineral nutrients such as potassium (K), iron (Fe), and phosphorus (P), and then makes it

accessible for plant use [1].

P is the second major important mineral nutrient after N required for plant growth [53,54]. P is abundant in soil in both organic and

inorganic forms but is insoluble and the uptake of available P by plants is minimal [40]. PGPR triggers plant growth by enhancing P

solubilization. Plants absorb insoluble P forms such as monobasic (H

−

) and diabasic ions (HPO

2−

) ions. Unavailable P in the soil are

in insoluble forms such as phosphotriesters (organic), apatite (inorganic), phosphor monoesters, and soil phytate or inositol phosphate

[40]. Therefore to eradicate the challenge of P deciency in soils, phosphatic fertilizers are frequently applied to the soil by some

farmers [55]. To solve the problem, phosphate solubilizing activity of PGPR is important. PGPR mineralizes and solubilizes inorganic

phosphorus by improving the root system. Hence, provide the available forms of P to the plants serving as potential biofertilizers [9,

10].

PGPR solubilizes inorganic phosphate by secreting low molecular weight organic acids, such as carboxylic acids, lactic acid,

succinic acid, glycolytic acid, formic acid, fumaric acid, and propionic acid which lower the pH in the root area, consequently releases

the conned forms of phosphate such as Ca phosphate in calcareous soil [56]. Generally, organic phosphorus mineralization occurs by

various enzymes such as phytase and C-P lyases phosphatases that catalyze the hydrolysis of phosphoric esters [42].

Additionally, other mineral nutrients such as iron, and zinc are made available through the biosynthesis of compounds capable of

promoting plant growth. Although mineralization and phosphate solubilization can be impacted by environmental factors, they play a

critical role in agricultural sustainability, especially in soils short of P [57]. Another essential macronutrient is K. Naturally, the

accumulation of K in soils is minute and the majority of the K is found in silicate minerals or insoluble rocks. The short supply of K in

soil results in poor development of plant roots, tiny seeds, and low crop yields generally present as a concern to sustainable crop

production. The search for solutions to alleviate the shortfall of K in soils has led to the innovation of environmentally friendly and

economical options for K uptake by plants and to sustain the K in soils for improving crop production [29,41,58].

The solubilization of K occurs through the secretion of organic acids by PGPR. Interestingly, PGPR such as Bacillus, Pseudomonas,

Burkholderia, and Paenibacillus species together with K solubilizing activity has been reported to provide the available forms of K to

plants [30,55,59]. These microbial communities are referred to as potassium-solubilizing microorganisms (PSM) because they release

unavailable K and make it accessible to plants. PGPR as potential biofertilizers can reduce the use of chemical fertilizers and

eco-friendly presents an approach for crop production.

Biostimulation, production of plant growth regulators and bioactive compounds

The process of modifying the soil environment, during which PGPR is excited to produce substances capable of promoting plant

growth is called biostimulation [58]. Biostimulants are biochemical substances that promote plant growth in the absence of pesticides,

nutrients, or soil improvers [60]. The chemical structure is closely related to that of natural plant hormones and the mode of action is

being estimated as the production of plant hormones or phytohormones [61]. Recently, PGPR based stimulants have been widely

applied in agricultural practices globally, in many African countries. PGPR based stimulants directly or indirectly improve crop quality

by enhancing nutrient uptake and tolerance to stresses such as salinity and drought [49,62]. Across the global markets, different PGPR

formulations have been registered and are commercially available. Some of the commercialized species are Enterobacter, Pseudomonas,

Variovarax, Serratia, Bacillus, Azobacter, and Azospirillium [60]. Although, their use in the cultivation of plants still presents a small

fraction worldwide [57].

Organic compounds required in minute concentrations capable of manipulating the physiological processes and regulating plant

growth are called phytohormones or plant growth regulators (PGRs) [63]. Phytohormones are phytostimulants that are chemical

compounds required for the physiological and biochemical development of plant growth. Pseudomonas, Bacillus, Acetobacter, Xan-

thomonas, Bradyrhizobium, Penicillium, and Aspergillus are some genera of PGPR capable of producing phytohormones [16,64,65].

Globally today, agricultural systems are frequently impacted by different stresses (biotic and abiotic) which often affect plant

growth and crop yield. Yearly, farmers experience 30-50% losses due to stress [64]. These stresses can be human induced or inherent.

The common abiotic stresses are drought, temperature, salinity, and accumulation of heavy metals. Hence, stimulates plants and PGPR

to produce the phytohormones. The phytohormones are found in minute amounts that exert control on the morphological, physio-

logical, and biochemical processes, even the structure and genetic expressions in plants, and facilitate plant-microbial interactions.

Therefore, it has had notable effects on soil microbial composition, soil fertility, and nutrient compositions, though the production of

these organic chemicals is efciently managed [29].

PGPR can enhance plant growth and development in stressed and natural conditions, therefore using competent microorganisms

could advance agricultural sustainability and environmental stability. In stressed soil environments, PGPR produces specic low

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

molecular compounds such as rhizobiotoxine around the rhizosphere capable of controlling phytopathogens by suppressing ethylene

production. Moreover, to increase survival under stressed conditions, particular bacteria transcription proteins regulate gene

expression in plants [29,47,64]. Arthrobacter sp. AF-163 produced phytochemicals capable of improving drought stress and crop

growth in sunower plants by altering membrane integrity and reactive oxygen species movement and also built up glycine, proline,

and betaine. Bacteria modulate the positive responses causing distinctive gene expression related to the activation and expression of

transcription factors, ethylene and salicylic biosynthesis in stressed conditions [53].

PGPR such as P. putida, Glucunobacter sp., Agrobacterium sp., Alcaligenes piechaudii, Micrococcus luteus, and Streptoverticillum sp.

synthesized high levels of ethylene, IAA, and hydrogen cyanide to reduce salt stress and enhance sunower plant root growth, as a

result improved root structure development, N content and nodule biomass [31,38,66]. PGPR producing auxin, cytokinins, and

gibberellins ameliorated antioxidant enzymes of different plants’ rhizosphere such as groundnut, lettuce and canola under gnotobiotic

conditions. Hence, the mechanisms of action improved signaling molecules that affect gene expression, plant growth and yields [63,

67]. Various PGPR such as Serratia, Rhizobium, and Pseudomonas species used as bioinoculants to cultivate common crops such as rice,

sunower, and legumes produced phytohormones involved in nodule formation and elongation of the root system [2,68,69].

A. thaliana seedlings treated with ACC tolerated drought when compared to the uninoculated seedlings, and also increased in root hair

length. Further investigation revealed that the mechanism is dependent on ethylene [50].

Sunower plant’s soil treated with Costus sp. triggered the production of phytohormones (auxins, cytokinins, and gibberellins) as a

result boosted the plants’ growth compared with chemical fertilizers [70]. Nonetheless, PGPR improves plant stress tolerance and

growth by reducing the use and damaging effects of inorganic fertilizers on soil health leading to environmental and agricultural

sustainability.

Siderophore production

Among the essential minerals abundant in the rhizosphere soil needed by plants is Fe, which is not readily available for plant and

bacterial use. Generally, ferric iron (Fe3+) is the major form of Fe on Earth but is insoluble. Plants and microorganisms require a

sufcient amount of Fe, which is of concern in the rhizosphere where there is a high competition of Fe by plants and microorganisms.

To alleviate this problem and make Fe readily available in the root region, PGPR secretes low molecular weight and high-afnity iron-

chelating compounds called siderophores [54].

Ever since the report by Kloepper and Schroth [16] on the occurrence of enhanced plant growth by siderophores produced by

P. uorescence, the role of siderophores produced by innumerable PGPR strains in plant growth promotion has been reported in many

studies [39,71]. Fig. 1 below indicates an in-vitro detection of siderophore production by PGPR isolates using the universal chemical

(CAS-agar plate) assay. PGPR strains P. uorescence KBS6-17, Serratia marcescens KBS-6H and Enterobacter sokazaki-NAS6B are shown

to produce siderophores conrmed by the change in the color of the blue CAS agar media into yellow and orange after inoculation and

incubation for 5 hours at room temperature [54].

Siderophores are grouped based on their functional capability as carboxylates and hydroxamates [58,72]. PGPR produces different

types of siderophores, such as ferroxamine and Pseudobactin that chelate in plant rhizosphere and as a pointer to show that plants are

Fig. 1. In-vitro production of siderophores on CAS-agar plates by PGPR strains P. uorescence KBS6-17 (A), S. marcescens KBS-6H and E. sokazaki-

NAS6B. The production of siderophores is indicated by a change in the color of the CAS agar into yellow and orange when the siderophores

sequester the Fe in the medium Source: [70].

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

capable of Fe uptake, which barely makes Fe accessible to pathogenic microora and halt pathogens from obtaining Fe [20].

Furthermore, PGPR species such as Streptomyces spp. reportedly produce siderophores comparable to those produced by the plants

[29,31,33]. Siderophores are known to be synthesized by microorganisms under iron deciency stress conditions hence, to assure the

growth and development of their cells. These microorganisms upsurge soluble iron in the soil, stimulate the chelation of iron, and make

it accessible for themselves and also for the plants [73,74]. Sunower plants inoculated with PGPR produced siderophores by stim-

ulating plant cell division that enhanced root growth compared to uninoculated plants [75]. The ferric siderophore complex produced

by P. putida and P. uorescens is taken up by plants, resulting in the restriction of microorganisms from accessing the Fe in plant roots

and other regions [58]. The siderophores synthesized by numerous PGPRs may be very useful for stimulating the absorption of iron in

an iron-decient environment by plants [76]. Also, the PGPR presence in soil induces the production of siderophores and helps plants

reduce the toxicity of heavy metals in the stressed environment [77].

Indirect mechanisms of plant growth promotion by PGPR

Biocontrol of phytopathogens

Globally, diseases damage many crops and before harvest, a large percentage is lost. Many farmers use chemicals to control pests

and this is becoming a concern due to health implications, hence PGPR offers a potential solution. Presently, awareness and acceptance

of biopesticides are on the rise globally. Biocontrol is the use of microorganisms to diminish the frequent occurrence of plant diseases.

Biopesticide selectively controls various organisms capable of causing diseases in plants without being toxic. PGPR is capable of

controlling various phytopathogenic microorganisms and uses at least one of the following mechanisms including competition with

pathogens for nutrients and specic ecological niches at the root region, the production of antibiotics and anti-fungicides, lytic

enzyme, hydrogen cyanide production, induced systemic resistance, and signal interference [31,66]. Some biocontrol agents are

highlighted in Table 2.

PGPR as a biocontrol agent exerts these mechanisms of action to antagonize pathogenic bacteria, fungi, and nematodes depending

on their severity. Pseudomonas uorescence is the most studied biocontrol agent because of its antagonistic actions against many

phytopathogens [69]. Besides, PGPR manipulates the involvement and application of important rhizobacteria and their metabolites in

suppressing the impact of phytopathogens, as a result, promotes plant health and minimizes loss during harvest [49,60]. Recently,

farmers’ interests and preferences have shifted to the application of integrated alternative pest control strategies that are viable,

inexpensive, and eco-friendly, including spore-forming Bacillus and other microorganisms with biocontrol ability [58]. Likewise,

Singh, et al. [78] reported that all ACCd producing PGPR isolates identied from sunower soil had an antagonistic effect on Fusarium

oxysporum that causes Fusarium wilt in the sunower. Furthermore, the ACCd producing PGPR exhibited a minimum of four plant

growth-promoting traits, including the production of phytohormones (IAA) and provided mineral nutrients, such as P and N xation

that signicantly improved seed and vegetative growth parameters of the sunower plant compared to the control.

PGPR produces antimicrobial secondary metabolites and siderophores to chelate Fe and conduct a multifactorial process that

stimulates induced systemic resistance and relies on various compounds, including volatiles and c-LP surfactin [69]. The combined

impacts of the strategies mentioned earlier would increase crop yield through adequate bioformulation of spores from viable PGPR and

concentrated culture supernatants with antimicrobial metabolites.

Induction of systemic resistance

Some PGPR triggers physical or chemical changes that are related to plant defense, a process referred to as induced systemic

Table 2

Some PGPR use as a biocontrol agent against diseases and pathogens of different plants.

Plant Disease/pathogen PGPR References

Sunower Sunower wilt fungus Pseudomonas cepacia [27,28]

Beans Sclerotium rolfsii Pseudomonas cepacia [30]

Maize Corn earworm;

Fusarium miniforms

P. maltophila

Enterobacter agglomerans, P. cepacia strain 406 and 526

[32]

Rice Rice sheath blight

Rice root nematode

Rhizobium solani

Bacillus cereus, Streptomyces spp., combined with P. uorescens

and Burkholderia sp.,

P. uorescens Fp7 and Pf1

[56,74]

Tomato Cucumber mosaic virus;

Root knot nematode

B. pumilus, B. amyloliquifacians strain IN 937a;

P. chitinolytica

[29,75]

Wheat Septoria tritici

Other diseases

P. aeruginosa strain Leci; P. putida strain BK8661

Rhodococcus, Pseudomonas, Bacillus, Penicillium, and Beauveria

species

[53]

Barley Powdery mildew B. subtilis [32]

Sugar beet Fusarium oxysporum, Rhizopus stolonifer, Phona beta, Pythium

ultimum, Cyst nematode

P. uorescens F113

P. uorescens

[32]

Mung

bean

Root-knot and rot P. aeruginosa, B. subtilis [7,30]

Sugar cane Red rot P. uorescens other PGPR [53]

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Scientic African 23 (2024) e02081

resistance (ISR) through the action of various phytohormones [79]. It is the mechanisms by which PGPR protects plants from

phytopathogenic infection by eliciting the production of different metabolites such as jasmonic acid, salicylic acid, and ethylene which

is released in the form of stress response signaling within plants. The production of these chemicals within the plants stimulates-

stimulates their resistance ability against infection by various phytopathogens [36]. PGPRs such as Azospirillum, Bacillus, Enterobacter,

and Pseudomonas species have been used as active ingredients in many biofertilizer products by farmers worldwide to activate induced

systemic resistance. Such inoculants containing this PGPR are often applied on the seed coat before planting to initiate ISR against

pathogens such as Pseudomonas syringae and Erwinia trachephila that cause leaf spot and bacterial wilt, respectively [53]. Common ISR

elicitors are siderophore, MAMPs (when formed by pathogens are called Pathogen-Associated Molecular Patterns: PAMPs) are mi-

crobial molecules secreted by microorganisms, like chitin, agellin, and lipopolysaccharides [79], cyclic lipopeptides, antibiotics (2,

4-diacetylphoroglucinol) and some volatile compounds such as acetoin, ketones, 2,3-butanediol, alkanes, alcohols, suldes, alkanes,

esters and sesquiterpenes [38,47].

Antibiotics production

Soil-borne pathogens are known for their harmful effects on plant health and crop yield. Globally, many crops are destroyed due to

the devastating impacts of pathogens, which reduce crop yield, the severity is more in Africa where crop yield is reduced to

approximately 40% and harvests further to 20% [19,41]. Recently, antibiotic production has been among the research areas exten-

sively studied for the biocontrol of phytopathogens and has been the most effective treatment to suppress phytopathogens globally

[58].

Antibiotics are low molecular weight compounds, among their numerous functions is to inhibit the proliferation of pathogenic

microorganisms and their metabolic activities [80]. Antibiotic production is the major antagonistic activity to inhibit phytopathogen

growth, thus playing signicant roles in disease control and also can be used as biocontrol agents [66]. In recent times, antibiotics

produced by PGPR have been employed to suppress the negative impacts of pathogens in the plant root environment. Such antibiotics

include phycocyanin, oomycin-A, pyrrolnitrin, and 2,4-diacetyl phloroglucinol [39].

Studies have recorded that PGPR produces butyrolactones, zwittermycin A, xanthobaccin phenazine-1-carboxylic acids, pyrrol-

nitrin, kanosamine, iturins, fengycins phenazine, circullin, colistin, polymyxin, and 2,4-diacetylphloroglucinol (2,4-DAPG) with

biocontrol effects on phytopathogens, such as Fusarium oxysporum, Rhizoctonia solani, Podosphaera fusca, and S. griseoviridis that cause

plant diseases including leaf and seedling blight in rice, Fusarium root rot and tomato wilt [3,38,68].

These biochemicals are produced by Bacillus, Pseudomonas strains, Stenotrophomonas sp., and Streptomyces spp. as active chemicals

against phytopathogens [20,40,81]. Some plant species naturally produce antibiotics that control plant diseases and are also produced

by soil microorganisms, for example, Phloroglucinols [33,38,75,82]. The biocontrol agents control plant diseases and have contributed

to increasing crop productivity.

Competition for nutrients and binding sites

Additionally, poor soil health is a concern globally, PGPR capable of producing biochemical substances with inhibitory effects on

phytopathogens, has been used to improve soil health in many African countries such as Nigeria, Benin, and South Africa [2,44]. The

inoculated PGPR as a biocontrol agent competes and in most cases out-compete the phytopathogens either for nutrients or binding sites

in the host plant root region [49]. Such competition acts by constraining phytopathogens from binding to the plants, therefore making

it relatively impossible to proliferate and infect the plant. For example, nutrient competition is the biocontrol mechanism of Pythium

aphanidermatum [40].

Apart from inherent growth and availability of sufcient nutrients in the rhizosphere, some properties help PGPR compete

favorably with phytopathogens and enhance their survival. These properties include the presence of agella, chemotaxis, lip-

osaccharides, and the use of synthesized exudates [58]. In the ecological niche competition, PGPR dominates the niche and prevents

colonization by phytopathogens until the available nutrients, such as Fe are exhausted.

Recently, PGPR inoculants have been reported to have antifungal activity and compete against pathogenic fungi such as Fusarium

oxysporum [83]. Similarly, the competitiveness of Bacillus megaterium in improving tomato plant growth has also been reported [75].

PGPR most times works in close association with other biocontrol mechanisms to halt the actions of phytopathogens [47,71,84].

Hydrogen cyanide production

Many PGPR produce hydrogen cyanide (HCN) in a process called cyanogenesis. Some of these PGPRs can be inoculated into the soil

to stimulate the production of HCN [33]. HCN is a volatile, broad-spectrum antimicrobial compound implicated in the biocontrol of

phytopathogens associated with Fluorescent Pseudomonads [38]. The cyanide ion obstructs the action of metalloenzymes, especially

copper composed of cytochrome c oxidase. Secondary metabolite synthesized by Gram-negative bacteria is formed from glycine and

catalyzed by the enzyme HCN synthase which is encrypted by biosynthetic genes such as henA, henB, and henC [59].

Moreover, HCN stops the electron transport to the target cells and disrupts the energy supply leading to the death of organisms

[47]. The HCN interrupts the proper activities of enzymes and inhibits natural receptor mechanisms. Some strains of Fluorescent

Pseudomonads produce HCN and they have been implicated in the elimination of soil-borne pathogens [75]. PGPR such as P. uorescens

strain CHAO, Bacillus, Stenotrophomonas, Brevibacterium, and Pseudomonas species isolated from rhizosphere soil produced HCN that

inhibited the growth of pythium [33]. PGPR produces HCN in soil capable of altering the plant’s physiological activities by stimulating

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

the formation of root hair [80]. Rhizobacteria are undeniably important in preserving soil fertility and improving plant growth and

development. This improvement in growth occurs through a variety of pathways, however, some other studies show the opposite [85,

86]. Cyanide generation, for example, is recognized to be a feature of certain Pseudomonas species. Cyanide produced by bacteria is

seen as both a growth promoter and a growth inhibitor in this context. Likewise, cyanide functions as a biocontrol agent against certain

plant diseases [87], although it can also have negative effects on plant growth [88].

PGPR mitigation of abiotic stresses in plants

In many agricultural elds globally, crop productivity and yield are affected by many abiotic stresses that adversely affect crop

production. Abiotic stresses such as drought, salinity, metal toxicity, acidic soils and nutrient deciency (fertility stress) limit the

growth and productivity of various economically important crops in manyagricultural elds globally. Apart from the intensive agri-

cultural practices such as the prolonged use of external chemical inputs in many agricultural elds, the spreading impact of the global

climate change causes numerous abiotic stresses on major crops worldwide. The predominant abiotic stresses such as drought, high soil

salinity, nutrient deciency, acidic soils and metal toxicity signicantly reduce the growth and yield of most cultivated crops [89–91].

There are many mechanisms by which PGPR reduces the negative impacts of such abiotic stresses in plants and hence promotes

growth indirectly. PGPR has been used as a biofertilizers in the past few decades as an alternative strategy to reduce dependence on

chemicals while improving plant growth and yield in a sustainable way [92]. Many of these PGPRs have developed various mecha-

nisms to exert benecial effects on abiotic stress in plants. One of the mechanisms PGPR uses to alleviate abiotic stress in soils is by

producing the enzyme ACC deaminase. Upon inoculation of PGPR with this ability, the ACC deaminase lowers the plant ethylene level,

resulting in longer roots and providing relief frommany abiotic stresses. Examples of PGPR that signicantly alleviated different abiotic

stresses in numerous agriculturally important crops include Bacillus polymyxa under nutrient-decient stress, Azosprillum brasilense on

drought and salt stress, P. uorescence on salt stress, Pseudomonas uorescence, P. putida and Azosprillum lipoferum on drought to

mention a few [91]. Furthermore, Bradyrhizobium elkanii produces rhizobitoxine, which has a twofold impact. It can relieve the

deleterious effect of stress-induced ethylene production on nodulation because it is an inhibitor of ethylene synthesis [93]. Rhizobi-

toxine, on the other hand, is classied as a plant toxin since it causes foliar chlorosis in soybeans [94]. So far, the preceding discussion

has demonstrated that, while PGPR is very successful in promoting plant growth and development, a few bacterial species can limit

growth. However, this negative inuence may occur only under certain conditions and by certain features. As a result, selecting a

certain strain is critical for obtaining the greatest benets in terms of better plant growth and development.

Fig. 2 illustrates the mechanisms by which certain plant growth-promoting rhizobacteria elicit induction of systemic tolerance (IST)

in plants. In this interaction, various types of abiotic stresses such as drought, salinity, and fertility stress could be mitigated by the

production of certain bioactive compounds by the PGPR residing on the root surfaces. For instance, the secretion of cytokinins by the

Fig. 2. A schematic representation of how PGPR is involved in the mitigation of various abiotic stresses including drought, salinity, and nutrient

deciency (fertility) stress and elicit induced systemic tolerance (IST) in plants. PGPR stands for plant growth promoting rhizobacteria. Source: [70].

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

bacteria can result in the accumulation of abscisic acid (ABA) in the leaves, which elicits stomatal closure under drought stress.

Whereas the secretion of antioxidants and the enzyme ACC-deaminase by PGPR results in the degradation of reactive oxygen species

(ROS) and that of the ACC precursor respectively [95]. These processes elicit induced systemic tolerance (IST) in the plants against

drought and salt stress conditions and promote plant growth indirectly [38,47].

Lytic enzyme production

PGPR synthesizes extracellular enzymes known as lytic enzymes. These enzymes hydrolyze polymeric compounds such as protein,

cellulose, chitin, and hemicellulose as an important form of biocontrol [69]. Lytic enzyme as a multifunctional naturally occurring

protein protects plants from climatic factors, abiotic, and biotic conditions [58]. Lytic enzymes are secreted by PGPR to directly

suppress the activities and growth of different phytopathogens, which are of concern. The presence of lytic enzymes in soil degrades a

different range of compounds from the plant, and also destroys or digests fungal pathogen cell wall structure. The application of PGPR

in soil activates the most critical eco-friendly mechanism (hydrolytic enzyme production) for the suppression of soil pathogens [38].

Similarly, PGPR produces and stimulates benecial enzymes such as lipases, chitinases, proteases, and glucanases involved in the

lysis of the cell wall. These enzymes degrade plant residues and nonliving organic matter to obtain carbon nutrition. In an experiment,

Myxobacteria produces a lytic enzyme that has shown effectiveness against fungal phytopathogens [36]. Plant diseases such as

bipolaris leaf spot induced by Pythium sp. and Bipolaris sp. are reportedly suppressed by glucanase and beta-1, 3-glucanase produced by

Lysobacter and Lysobacter enzymogenes strain C3, respectively [5]. Furthermore, Serratia marcescens produces chitinase that has an

antagonistic effect on Sclerotium rolfsii. Nevertheless, hydrolytic enzymes directly control phytopathogens and save plants from

different biotic and abiotic stresses affecting sustainable agriculture [66].

Role of PGPR in phytoremediation

Green technology is an emerging eco-friendly and inexpensive strategy to improve agricultural soil contaminated with heavy

metals which results in advanced soil health [20]. Phytoremediation involves the use of specic plant cultivars, heavy metal tolerant,

and plant growth-promoting microorganisms [21]. Phytostabilization is a major strategy that makes up phytoremediation that uses a

particular plant cultivar to stabilize heavy metal contaminants, consequently reducing their bioavailability in soil [77].

For soil remediation to be considered efcient, it requires plants to intercept, take uptake up, accumulate, sequestrate, stabilize,

and translocate heavy metal contaminants [71]. Despite the potential of cleaning up heavy metals in the soil, phytoremediation is

faced with some factors that can slow down or stop the process [71]. For instance, such factors are nutrient availability, type of

pollutant, plant species, enzyme class, soil component, and pH [77]. The plant microbial community determines the success of the

phytoremediation process. Likewise, microbial biomass, soil enzymes, and microorganisms are major mediators of biological processes

and even serve as an indicator of heavy metal stress [20,39].

When heavy metal tolerant PGPR is inoculated into polluted soil, it stimulate plants to perform tasks such as heavy metal

sequestration, recycling nutrients, controlling pathogens, mineralization, sustaining soil structure, and detoxifying chemicals. As a

result, the plants release exudates including amino acids, phytohormones, vitamins, and proteins for the microorganism [15]. The soil

enzyme action responds quickly to metal stress, for example, catalase can degrade hydrogen peroxide (H

) and stop it from

contaminating soil organisms [37,96].

Correspondingly, enzyme activities involved in soil organic carbon (C) (saccharase and β-glucosidase), P (acid phosphatase), and N

(urease) cycles are considered important indices that present as the potential for soil enzyme synthesis by microbiomes [21,37].

Microbial community diversity reduces with increasing levels of heavy metals such as zinc (Zn) and cadmium (Cd) in soil [97,98]. In a

heavy metal polluted soil, Trigonella foenum-graceum and Brassica juncea with PGPR inoculated into the soil showed rapid degradation

of phenanthrene. This was a result of the high microbial population and exudates secreted by plants and root-associated microbial

consortium [21].

PGPR such as Pseudomonas sp. GHD-4 improved soil enzyme activities and enriched microbial community diversity by degrading

lead (Pb) and reducing its concentrations in soil [99]. Heavy metal contaminated rhizosphere soil inoculated with PGPR has been

reported to have greater microbial diversity compared to uninoculated soil [39]. PGPR involved in phytoremediation not only benets

plant growth but also improves soil quality [96].

Techniques of applying microbial inoculants to enhance plant growth

Microbial inoculants are made up of live microorganisms, mainly bacteria such as rhizobia or fungi capable of improving plant

growth and development. Besides, it could be a pure or mixed culture. Similarly, exists in solid or liquid form [100]. A good carrier for

preparing microbial inocula should provide a conducive environment for PGPR to live and grow, and also, have long cellular viability

at room temperature for two months and above. A suitable carrier is characterized by being ecologically friendly, easy to apply, stable,

and nontoxic toinoculants and plants; easy to sterilize using gamma-irradiation or autoclave, readily available and inadequate form. In

addition, have good pH buffering capacity, moisture absorption capacity, easy to process, and should be free from lump-forming

materials.

The carrier type determines the application of microbial inoculants. Solid microbial inoculant materials such as peat are bead-like

or granules are rich in organic matter and are used for microorganism immobilization [101]. In addition, liquid inoculants are mi-

crobial cultures in broth form rich in cell protectors and nutrients. Moreover, liquid inoculants can be suspensions in organic oils or

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

mineral or oil in water suspensions. In seed inoculation, liquid or powder microbial inoculants are used to coat the seeds. Likewise,

other methods of liquid inoculant applications are in-furrow or foliar application or spray on soil [100].

Again, other materials and techniques for carrying microorganisms are through lyophilization, industrial and agricultural residues,

and polymers for cell encapsulation [102]. Carriers from agricultural and industrial residues such as wheat bran, clay, sawdust, rice

bran, lignite powder, and peat can be augmented with inorganic or chitin containing media such as betonies, vermiculite, silicate, and

kaolin for soil or seed inoculation [103]. The use of different microbial inoculants around the world and in Africa over the past decades

has increased, resulting in higher crop yields.

Application methods of PGPR in eld

The applications of PGPR in eld condition have been studied extensively and reported. A variety of PGPR have been used as soil

bioinoculants intended to enhance the supply of nutrients to plants. Diverse species of PGPR such as Clostridia, Rhizobium, Bacillus,

Azotobacter, Klebsiella, and Azospirillum sp. have successfully been inoculated in the elds to understand the mechanisms and

effectiveness of PGPR to increase plant development and productivity. The benecial effects of inoculations of PGPR (Rhizobium

species including Sinorhizobium, Mesorhizobium, Allorhizobium, Bradyrhizobium etc.) has signicantly increase plant vegetative and

yield by nitrogen-xing symbiosis with leguminous plants [9]. Additionally, Clostridia was reportedly isolated from rice soils and their

interaction also increased after re-inoculating straw to elds which elevated the C to N ratio in the soil. Azospirillum has reportedly

increase wheat yields in both eld and greenhouse conditions. Azospirillum lipoferum increased rice yield to approximately 1.8 t ha−1

in a eld experiment [104].

N tracer techniques in a eld study showed that Azospirillum lipoferum and Azospirillum brasilense

contributed 7–12% of wheat plant nitrogen [105].

Many eld studies have conrmed that Azospirillum diazotrophicus isolated from rhizosphere soil increased sugarcane plant growth

by improving N to over 200 kgN ha

−1

year

−1

[103]. Acetobacter-sugarcane system has now become an active experimental model and

the diazotrophic character (nif+) is a signicant module of this system [106]. Azoarcus sp. BH72 isolated from Kallar grass (Leptochloa

fusa Kunth) colonized rice rhizosphere soils which reportedly improved microbial interactions and positively increased rice yield in

both eld and laboratory conditions [107]. In eld trials, many species of family Enterobacteriaceae include diazotrophs mainly those

isolated from the rhizosphere of agricultural plants with plant growth-promoting activity colonizes sugarcane, sorghum, rice, maize

and other crops [86]. Also, improvement of soybean yield, seed size, fat content and drought stress by microbial inoculation correlated

with enhancement in soil microbial assortment in the rhizosphere since it was previously reported by Igiehon et al. [108] that mi-

crobial communities could be affected by Rhizobium and mycorrhizal fungi inoculation as well as fertilizer amendment.

Commercialization of PGPR products and challenges in developing countries

The green revolution has sadly introduced chemical pesticides, herbicides, and inorganic fertilizers into agricultural soils that ledto

huge damage to the soil environment in the form of pollutants. To resolve this problem, there is a need to design microbial consortia

that can help to solve aspects of plant growth potential and bioremediation [11].In many developed countries including the United

States of America, Australia, and Europe, and some developing countries like Brazil, Argentina, and India, there is a well-documented

success in the commercialization of PGPR products as biofertilizers and biocontrol agents [15,21,52]. Despite the numerous benets of

PGPR inoculants, their development and their commercial application in sustainable crop production and protection in developing

nations, particularly in Africa are still very scarce [15].

Developing PGPR into new microbial inoculants depends on initial laboratory screening assays that are aimed at detecting

particular PGPR traits such as phosphate solubilization, N xation, auxin biosynthesis, siderophore production, ACC deaminase ac-

tivity, antibiotic production to mention a few [38,52]. According to Vacheron et al. [109], auxin production by PGPR can have both

benecial and negative impacts on plant development. It is vital to keep in mind that the concentration of auxin determines its

effectiveness. For example, at low concentrations, it promotes plant development, whereas, at high quantities, it inhibits root growth

[110]. Screening of PGPR for these plant growth-promoting traits under in-vitro assays does not necessarily result in isolates that can

improve plant growth under eld conditions [14,15,102].

A major challenge in the commercialization of PGPR is developing consortia of highly efcient microorganisms with high rhizo-

sphere colonization and persistence [67]. PGPRs are frequently inoculated on plant materials but without a suitable carrier or

quantities, they do not allow effective colonization of the rhizosphere under eld conditions, especially due to competition with

indigenous soil macro and micro fauna [11]. Additional challenge emanates from soil management practices such as the fumigation of

soil with broad-spectrum biocidal fumigants that changes the biological community structure of the soil including introduced mi-

crobial inoculants [67,111].

The formulation of bioinoculants exceptionally for particular soil conditions reduces environmental challenges. Also, training

farmers and workers on how to expertly apply bioinoculants on crops is critical in the advancement and distribution of benecial

inocula [21]. The need to educate the general population and farmers on the advantages of formulated products containing benecial

microorganisms in agriculture and to explore the full richness of fertile land for sustainable food production is crucial [63].

Conclusion

There is a need for sufcient effort to be made to use and apply existing scientic knowledge for a better understanding of soil-

plant-microbial associations and their modes of action in nutrient acquisition and plant growth promotion. With the recent

B.C. Igiehon et al.

Scientic African 23 (2024) e02081

increase in the awareness and demand to use PGPR for a sustainable agroecological system, the need to substitute agrochemicals with

biological products made up of single or a consortium of elite PGPR is very crucial.

The application of PGPR in sustainable food production has the potential to boost crop production, enhance crop nutrition, yield,

and control of diseases, and reduce environmental hazards associated with chemical usage. The efcacy of PGPR in boosting plant

growth and development is dependent on the specic strain of bacteria and the conditions under which it is used. As a result, selecting

a certain strain is critical for obtaining the greatest benets in terms of better plant growth and development. There are many benets

of microbial inoculant products with PGPR as active ingredients. These include increased mineral nutrients availability and biocontrol

through antibiosis, and ISR, competition for essential nutrients such as Fe through the chelation effect of siderophores (the competition

must be carefully stated and understood by farmers for improved crop productivity). Genetic engineering of PGPR is an important

constituent in modern food production that will mitigate soil contaminants, environmental alteration, and destruction of soil ora and

fauna when properly harnessed specically in developing economies.

Further research on the long-term impacts of PGPR on soil health and ecosystem functioning is recommended to fully comprehend

PGPR’s application for sustainable food production. More research is needed to properly comprehend the possible benets and

drawbacks of PGPR in terms of sustainable food production. Furthermore, the discovery of new PGPR strains that are more efcient

and stable under varied environmental conditions can aid in improving PGPR’s effectiveness in encouraging plant growth and

development. Likewise, researching the interactions of PGPR with other microorganisms in the rhizosphere and beyond in bulk soil can

aid in better understanding the mechanisms by which PGPR stimulates plant growth and development. Also, we recommend the

advancement of new methods for the application of PGPR in agriculture, which can help improve the efciency and effectiveness of

PGPR in promoting plant growth and development. Still, promoting the implementation of PGPR in agriculture, given the expected

benets of PGPR in terms of biofertilization, biocontrol, and bioremediation, all of which have a benecial effect on crop productivity

and ecosystem functioning, encouragement should be given to its implementation.

Funding

National Research Foundation (NRF), South Africa/The World Academy of Science African Renaissance provided the Ph.D.

scholarship (UID121772) for BCI stipend.

The National Research Foundation, South Africa funded the work in OOB lab (UID123634).

CRediT authorship contribution statement

Blessing Chidinma Igiehon: Conceptualization, Validation, Data curation, Formal analysis, Writing – original draft, Writing –

review & editing. Olubukola Oluranti Babalola: Funding acquisition, Supervision, Validation, Writing – review & editing. Ahmed

Idris Hassen: Supervision, Validation, Writing – review & editing.

Declaration of competing interest

The authors declare no conicts of interest.

Acknowledgements

B.C.I appreciates the National Research Foundation South Africa/ The World Academy of Science (NRF-TWAS) (UID121772) for a

PhD stipend, O.O.B., acknowledges the National Research Foundation, South Africa for a grant (UID123634) that supported research

in her laboratory.

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Chlorpyrifos Degradation by Bacillus tropicus a Plant Growth Promoting Rhizobacteria

Article

Full-text available

Mar 2024
Biosci., Biotechnol. Res. Asia

Excessive use of organophosphate in modern farming to improve the crop productivity has cause pollution in soil, water and air which lead environmental as well as human hazards. Microbial fertility is adversely affected by the use of pesticides. Thus, the present study focused on the isolation and screening of effective isolates with multi-traits PGPR activities and further studied for chlorpyrifos pesticide degradation. The bacterial isolate DK5 was showing multiple PGPR activity, identified as Bacillus tropicus by 16S rRNA sequencing. The chlorpyrifos degradation by isolated Bacillus tropicuswas studied by using resting cell study. In HPLC analysis revealed that Bacillus tropicus degrade 60% chlorpyrifos after 48 hrs. of incubation followed by 99% after 72 hrs. of incubation. Generally, results of this study revealed that isolate DK5 identified as Bacillus tropicus can be used for the successfully removal of chlorpyrifos from contaminated soil and plant growth promotion.

Plant Growth-Promoting Rhizobacteria for Sustainable Agricultural Production

Article

Full-text available

Apr 2023

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.

Effects of Plant-Growth-Promoting Rhizobacteria on Soil Bacterial Community, Soil Physicochemical Properties, and Soil Enzyme Activities in the Rhizosphere of Alfalfa under Field Conditions

Article

Full-text available

Apr 2023
Diversity

Background: Inoculation with plant-growth-promoting rhizobacteria (PGPR) effectively increases plant growth in agriculture. However, the role of the rhizobiome in plant growth remains unclear. Methods: Biolog Ecoplate and 16S rRNA gene high-throughput sequencing techniques were used to analyze the changes in microbial community diversity, composition, and function after PGPR inoculation. Soil physicochemical and enzyme activities were also measured. Results: PGPR inoculation significantly promoted the growth of alfalfa. Using a Biolog Ecoplate, inoculation improved the metabolic activity and carbon source utilization of soil microorganisms. PGPR inoculation significantly increased the diversity and richness of the soil bacterial community in the rhizosphere of alfalfa and increased the relative abundance of key bacterial taxa such as Arthrobacter, Sphingomonas, and Bacillus, which are conducive to plant growth. Conclusions: Inoculation with PGPR enriched bacterial taxa and improved the utilization of carbon sources beneficial for plant growth. PGPR inoculation induced changes in microbial community diversity, and relevant functions in the rhizosphere contributed to alfalfa growth under field conditions.

Rhizosphere Bacteria in Plant Growth Promotion, Biocontrol, and Bioremediation of Contaminated Sites A Comprehensive Review of Effects and Mechanisms

Article

Full-text available

Sep 2021

Agriculture in the 21st century is facing multiple challenges, such as those related to soil fertility, climatic fluctuations, environmental degradation, urbanization, and the increase in food demand for the increasing world population. In the meanwhile, the scientific community is facing key challenges in increasing crop production from the existing land base. In this regard, traditional farming has witnessed enhanced per acre crop yields due to irregular and injudicious use of agro-chemicals, including pesticides and synthetic fertilizers, but at a substantial environmental cost. Another major concern in modern agriculture is that crop pests are developing pesticide resistance. Therefore, the future of sustainable crop production requires the use of alternative strategies that can enhance crop yields in an environmentally sound manner. The application of rhizobacteria, specifically, plant growth-promoting rhizobacteria (PGPR), as an alternative to chemical pesticides has gained much attention from the scientific community. These rhizobacteria harbor a number of mechanisms through which they promote plant growth, control plant pests, and induce resistance to various abiotic stresses. This review presents a comprehensive overview of the mechanisms of rhizobacteria involved in plant growth promotion, biocontrol of pests, and bioremediation of contaminated soils. It also focuses on the effects of PGPR inoculation on plant growth survival under environmental stress. Furthermore, the pros and cons of rhizobacterial application along with future directions for the sustainable use of rhizobacteria in agriculture are discussed in depth. Citation: Saeed, Q.; Xiukang, W.; Haider, F.U.; Kucerik, J.; Mumtaz, M.Z.; Holatko, J.; Naseem, M.; Kintl, A.; Ejaz, M.; Naveed, M.; et al.

Perspectives for sustainable agriculture from the microbiome in plant rhizosphere

Article

Full-text available

May 2021

The ever-growing human population globally has resulted in the quest for solutions to the problem of hunger by providing food security. The importance of plant-root-associated microorganisms cannot be overlooked, plants rely on them. These root colonizers dominate the rhizosphere due to the abundance of available nutrients, relying on their host plant for nutrients and other essential requirements. The relationships between microbial communities and plants are controlled by the type of plant and microorganism involved. Advances in modern molecular techniques have led to the evolution of omic technology using nucleic acid molecules to study plant-microorganism associations capable of stimulating plant growth, improve yield, and induce disease suppression. This review elucidates the activities of microbial communities, especially nitrogen-fixing rhizobacteria associated with plant roots, nitrogen fixation as a mechanism of promoting plant growth, their importance, and the challenges employing bioinoculants. Prospecting plant growth promoters using omic technology will advance sustainable agriculture globally.

High-Throughput Sequencing Survey of Sunflower Soil

Article

Full-text available

Feb 2021

Plant rhizobiomes are responsible for major soil processes in the immediate plant environment, but our knowledge of the linkage between below-ground microbiota diversity and plant health is limited. We studied the bacterial and archaeal communities of sunflower rhizosphere organisms by comparing the composition of these communities to bulk soils at three farms in the North West province of South Africa. We evaluated and described a plethora of bacterial and archaeal taxa.

Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects

Article

Full-text available

Jan 2021

The quest for enhancing agricultural yields due to increased pressure on food production has inevitably led to the indiscriminate use of chemical fertilizers and other agrochemicals. Biofertilizers are emerging as a suitable alternative to counteract the adverse environmental impacts exerted by synthetic agrochemicals. Biofertilizers facilitate the overall growth and yield of crops in an eco-friendly manner. They contain living or dormant microbes, which are applied to the soil or used for treating crop seeds. One of the foremost candidates in this respect is rhizobacteria. Plant growth promoting rhizobacteria (PGPR) are an important cluster of beneficial, root-colonizing bacteria thriving in the plant rhizosphere and bulk soil. They exhibit synergistic and antagonistic interactions with the soil microbiota and engage in an array of activities of ecological significance. They promote plant growth by facilitating biotic and abiotic stress tolerance and support the nutrition of host plants. Due to their active growth endorsing activities, PGPRs are considered an eco-friendly alternative to hazardous chemical fertilizers. The use of PGPRs as biofertilizers is a biological approach toward the sustainable intensification of agriculture. However, their application for increasing agricultural yields has several pros and cons. Application of potential biofertilizers that perform well in the laboratory and greenhouse conditions often fails to deliver the expected effects on plant development in field settings. Here we review the different types of PGPR-based biofertilizers, discuss the challenges faced in the widespread adoption of biofertilizers, and deliberate the prospects of using biofertilizers to promote sustainable agriculture.

Elucidating the Rhizosphere Associated Bacteria for Environmental Sustainability

Article

Full-text available

Jan 2021

The abundance of nutrient accumulation in rhizosphere soils has placed the rhizosphere as an “epicenter” of bacterial concentrations. Nonetheless, over the years, little attention has been given to bacterial inoculants and soil-like substrates. The reason is that many farmers and experiments have focused on chemical fertilizers as an approach to improve plant growth and yield. Therefore, we focused on assessing the application of rhizosphere soil and its associated bacteria for biotechnological applications. This review has been structured into major subunits: rhizosphere soil as a treasure trove for bacterial community concentration, biodegradation of lignocellulose for biofuel production, rhizosphere soil and its bacteria as soil amendments, and the role of rhizosphere soil and its bacteria for bioremediation and biofiltration. Hence, the efficient use of rhizosphere soil and its bacteria in an environmentally friendly way can contribute to healthy and sustainable environments.

Exopolysaccharides Producing Bacteria for the Amelioration of Drought Stress in Wheat

Article

Full-text available

Oct 2020

This research was designed to elucidate the role of exopolysaccharides (EPS) producing bacterial strains for the amelioration of drought stress in wheat. Bacterial strains were isolated from a farmer’s field in the arid region of Pakistan. Out of 24 isolated stains, two bacterial strains, Bacillus subtilis (Accession No. MT742976) and Azospirillum brasilense (Accession No. MT742977) were selected, based on their ability to produce EPS and withstand drought stress. Both bacterial strains produced a good amount of EPS and osmolytes and exhibited drought tolerance individually, however, a combination of these strains produced higher amounts of EPS (sugar 6976 µg/g, 731.5 µg/g protein, and 1.1 mg/g uronic acid) and osmolytes (proline 4.4 µg/mg and sugar 79 µg/mg) and significantly changed the level of stress-induced phytohormones (61%, 49% and 30% decrease in Indole Acetic Acid (IAA), Gibberellic Acid (GA), and Cytokinin (CK)) respectively under stress, but an increase of 27.3% in Abscisic acid (ABA) concentration was observed. When inoculated, the combination of these strains improved seed germination, seedling vigor index, and promptness index by 18.2%, 23.7%, and 61.5% respectively under osmotic stress (20% polyethylene glycol, PEG6000). They also promoted plant growth in a pot experiment with an increase of 42.9%, 29.8%, and 33.7% in shoot length, root length, and leaf area, respectively. Physiological attributes of plants were also improved by bacterial inoculation showing an increase of 39.8%, 61.5%, and 45% in chlorophyll a, chlorophyll b, and carotenoid content respectively, as compared to control. Inoculations of bacterial strains also increased the production of osmolytes such asproline, amino acid, sugar, and protein by 30%, 23%, 68%, and 21.7% respectively. Co-inoculation of these strains enhanced the production of antioxidant enzymes such as superoxide dismutase (SOD) by 35.1%, catalase (CAT) by 77.4%, and peroxidase (POD) by 40.7%. Findings of the present research demonstrated that EPS, osmolyte, stress hormones, and antioxidant enzyme-producing bacterial strains impart drought tolerance in wheat and improve its growth, morphological attributes, physiological parameters, osmolytes production, and increase antioxidant enzymes.

Rhizobacteria inoculation benefits nutrient availability for phytostabilization in copper contaminated soil: Drivers from bacterial community structures in rhizosphere

Article

Feb 2019
APPL SOIL ECOL

Plant growth-promoting rhizobacteria (PGPR) and rhizobia are potentially advantageous in improving plant growth in heavy metal contaminated soils. However, only limited information is available in literature on the manner through which the co-inoculation of PGPR and rhizobia can potentially supply nutrients to benefit plant growth in heavy metal contaminated soil. Accordingly, this study investigated the effects of Paenibacillus mu-cilaginosus (PGPR) and Sinorhizobium meliloti (rhizobia) co-inoculation on soil nutrients, enzyme activities, and microbial biomass in copper (Cu) contaminated soil planted with alfalfa (Medicago sativa). Moreover, we assessed soil bacterial community structure using high-throughput Illumina sequencing of 16S rRNA genes. Results showed that PGPR and/or rhizobia inoculation improved alfalfa growth. In particular, we found that this co-inoculation approach decreased Cu accumulation (48.6%) in shoots compared to the control (uninoculated). Both partial least squares path modeling (PLS-PM) and the relative importance of regressors in the linear models identified that enzyme activities, microbial biomass, and microbial community structure in Cu contaminated soil were major controlling variables of soil nutrient availability. The co-inoculation treatment significantly increased soil carbon (C) and nitrogen (N) concentrations by increasing urease (55.6%), saccharase (29.5%), and β-glucosidase (31.4%) activities compared to the control. Furthermore, the rhizosphere microbial community structure in the co-inoculation treatment was mainly regulated by soil N concentrations (i.e., both total N and available N) while altering alpha diversity (α-diversity). The relative abundances of Firmicutes (including bio-markers of the Bacillus genus) and Acidobacteria were enriched in the co-inoculated treatment, which can potentially improve soil nutrient availability and subsequently benefit plant growth. These findings indicated that the co-inoculation of PGPR and rhizobia plays an important role in promoting plant growth in Cu contaminated soil. This is because this approach can increase soil nutrient availability by enhancing soil enzyme activities and regulating rhizosphere microbial community structure.

Legume Nitrogen Fixation and Soil Abiotic Stress: From Physiology to Genomics and Beyond

Chapter

Apr 2018

Legumes are important components of the nitrogen cycle on land. Agricultural systems have traditionally relied much on legumes for nitrogen input because many species are able to establish symbioses with diazotrophic bacteria (rhizobia) and thus trade metabolites and reduced compounds. Photosynthates produced in the leaves are allocated to the root nodule to supply the bacteroids with carbon, in exchange for reduced nitrogen (ammonia) produced by the rhizobia from atmospheric nitrogen. Despite its major significance to plant breeding and sustainable agriculture, the impact of abiotic stresses on nodule development and stability and on symbiotic nitrogen fixation remains poorly understood, particularly at the molecular level. However, the study of model legume species and the development of a plethora of resources, particularly the elucidation of the genome sequences of three legume species, are now revealing many traits of agricultural importance in legumes as well as other aspects that are not easily studied in other plant models, such as Arabidopsis or rice. In this chapter, we will discuss the effects of abiotic stresses, such as drought, phosphate deficiency and aluminium toxicity, on symbiotic nitrogen fixation and provide perspectives on molecular approaches to the analysis of stress responses in legumes.

Rhizosphere competence and applications of plant growth-promoting rhizobacteria in food production – A review

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