Journal of Environmental Management 273 (2020) 111118

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Journal of Environmental Management

journal homepage: http://www.elsevier.com/locate/jenvman

Review

Unlocking the potential of plant growth-promoting rhizobacteria on soil

health and the sustainability of agricultural systems
Zobia Khatoon a, Suiliang Huang a, Mazhar Rafique b, Ali Fakhar c, Muhammad Aqeel Kamran d,
Gustavo Santoyo e, *
a
Key Laboratory of Pollution Processes and Environmental Criteria of the Ministry of Education, Key Laboratory of Urban Ecological Environment Rehabilitation and
Pollution Control of Tianjin, Numerical Stimulation Group for Water Environment, College of Environmental Science and Engineering Nankai University, Tianjin,
300350, China
b
Department of Soil Science, The University of Haripur, 22630, KPK, Pakistan
c
Department of Soil Science, Sindh Agricultural University, Tandojam, Pakistan
d
Department of Environmental Sciences, Zhejiang University, China
e
Genomic Diversity Laboratory, Institute of Biological and Chemical Research, Universidad Michoacana de San Nicolas de Hidalgo, 58030, Morelia, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: The concept of soil health refers to specific soil properties and the ability to support and sustain crop growth and
PGPR productivity, while maintaining long-term environmental quality. The key components of healthy soil are high
Rhizosphere populations of organisms that promote plant growth, such as the plant growth promoting rhizobacteria (PGPR).
Bioinoculants
PGPR plays multiple beneficial and ecological roles in the rhizosphere soil. Among the roles of PGPR in agro­
Environmental cleanup
ecosystems are the nutrient cycling and uptake, inhibition of potential phytopathogens growth, stimulation of
plant innate immunity, and direct enhancement of plant growth by producing phytohormones or other metab­
olites. Other important roles of PGPR are their environmental cleanup capacities (soil bioremediation). In this
work, we review recent literature concerning the diverse mechanisms of PGPR in maintaining healthy conditions
of agricultural soils, thus reducing (or eliminating) the toxic agrochemicals dependence. In conclusion, this re­
view provides comprehensive knowledge on the current PGPR basic mechanisms and applications as biocontrol
agents, plant growth stimulators and soil rhizoremediators, with the final goal of having more agroecological
practices for sustainable agriculture.

1. Introduction Another important issue worldwide is related to environmental

The requirement of quality food in the form of nutrients and
balanced diet is one of the major challenges currently being faced in
feeding the ever increasing world population. The nonjudicious use of
chemical fertilizers for increasing agricultural yield is harming the
agroecosystems (Alavaisha et al., 2019). Similarly, chemical pesticides
used for controlling plant diseases and insect pests have caused harmful
effects on the natural predators of insects, such as world bee pop­
ulations, soil biota, as well as land and aquatic flora and fauna
(McLaughlin and Mineau, 1995). Of course, agrochemicals also cause
diverse toxic effects on human health (Pelosi et al., 2014). Thus, agri­
cultural practices which involve an increased use of chemical pesticides
result in depletion, modification, and/or complete loss of indigenous
and beneficial microbiodiversity.
sustainability. It is well known that anthropogenic activities are
responsible for causing environmental deterioration along with
affecting soil heath; destroying plants habitat, growth and development;
resulting in depleted nonrenewable resources (Harte, 2007). To contain
the ever increasing demand and overuse of synthetic chemicals, keeping
in mind their long-term detrimental effects on global agroecosystems,
we are in dire need of developing, adopting, and promoting environ­
ment sustainable approaches. Thus, sustainable agriculture is vitally
important in this era because it provides the potential to meet our future
agricultural needs, something that cannot be achieved by using con­
ventional and toxic agricultural practices, which are detrimental to the
environment (Santoyo et al., 2017). For example, fertilizer run off from
conventional agriculture is the chief source in the creation of dead zones
with low oxygen where survival of marine life becomes difficult.

* Corresponding author.
E-mail address: gsantoyo@umich.mx (G. Santoyo).

https://doi.org/10.1016/j.jenvman.2020.111118
Received 11 April 2020; Received in revised form 13 July 2020; Accepted 19 July 2020
Available online 1 August 2020
0301-4797/© 2020 Elsevier Ltd. All rights reserved.
Z. Khatoon et al.
Similarly, fertile soils are becoming acidic due to the heavy application
of chemical fertilizers (Slepetiene et al., 2020). The challenge of
increasing productivity while maintaining environmental stability ne­
cessitates educating farmers and helping them to understand and adopt
innovative and appropriate farming practices.
The role of plant growth-promoting rhizobacteria or PGPR, have
been gaining attention for decades, due to their ability to enhance plant
development and their role as promising agents for stress management
in plants. Soil is the natural habitat for microorganisms that are bene­
ficial for plant crops (Probanza et al., 2002). They are involved in a
number of soil processes that determine overall plant health, crop yields,
and productivity (Santoyo et al., 2017). For the successful functioning of
microbial inoculants and their impact on soil health, extensive efforts
have been made for investigating indigenous soil microbial diversity,
their distribution, and behavior in soil habitats (Chenniappan et al.,
2019). Growth stimulating bacteria, such as PGPR, are able to improve
soil health through different mechanisms like nitrogen fixation, phos­
phate solubilization, heavy metal sequestering, phytohormones pro­
duction (i.e., indole acetic acid, gibberellins or cytokinins),
mineralization of soil organic matter, decomposition of crop residues,
suppression of phytopathogens, among others, making them useful for
plants to grow even in nutrient deficient soils (He et al., 2019; Shameer
and Prasad, 2018).
In addition, PGPR provide valuable information to the biotechnology
industry because they offer countless new genes and biochemical
pathways to probe for enzymes, antibiotics, and various other useful
compounds. Hence, PGPR occupy a prominent place in agriculture
(Etesamiet al., 2018; Glick, 2012; Majeed et al., 2018). To utilize PGPR
in an effective way, it is necessary to understand the mechanisms
through which they influence soil health and in turn ensure sustain­
ability in agriculture. Therefore, the main objective of this study is to
highlight the mechanisms used by PGPR, their role in improving soil
health and increasing agricultural yield on sustainable grounds.
2. The rhizosphere as an ecosystem
Rhizosphere is defined as the zone surrounding the roots which is
directly influenced by plant roots secretions (Hartmann et al., 2009).
Microbial activities in this zone are essential for plants functioning as
they help in the uptake of nutrients and protect against pathogens attack
(Kibbey and Strevett, 2019). The plant, the soil, and the microbes all
interact with each other to carry out and influence various processes that
contribute to plant health and productivity (Ahmed et al., 2019). It is
well documented that successful plant growth promotion is because of
the rhizobacterial association and communication with plant roots
within the rhizosphere. During the process of root colonization, PGPR
increase the availability of nutrients in the rhizosphere, thus promoting
plant growth and development (Kumari et al., 2019). As mentioned,
rhizosphere is that compartment of soil which is directly influenced by
plant roots. Various compounds released by plants in the form of root
exudates provide a unique environment in the rhizosphere which in­
cludes sugars, amino acids, organic acids, flavonoids, proteins, and fatty
acids, etc. (Badri et al., 2009). Some root exudates function as signals
either as repellents against various pathogens or to aggregate beneficial
microbes, thus functioning as attractants on the bases of physiological
status, plant species, and microorganisms (Ahmed et al., 2019). Root
exudates serve as messenger molecules between roots and rhizobacterial
species in the rhizospheric soil (Lucini et al., 2019). Therefore, root
exudates are essential growth substrates for soil microbes playing a vital
role in plant growth promotion as well as in inducing defenses against
phytopathogens. This rhizodeposition, which encompasses root border
cells, root debris, root exudates, lysates, mucilage and mucigel, is the
chief reservoir of organic carbon in the soil (Pausch and Kuzyakov,
2018). It has been reported that rhizodeposits provide energy to soil
microbes for the solubilization of essential nutrients in soil organic
matter, thus increasing soil fertility and promoting plant growth
2
Journal of Environmental Management 273 (2020) 111118
(Bowsher et al., 2018). The availability of all these nutrients makes the
rhizosphere a highly competitive microecosystem, in which all and
every one of the residents fight each other to colonize the best root zones
and occupy ecological niches for survival. Under these circumstances,
rhizobacteria contain diverse biological strategies, which have evolved
and improved to succeed in such harsh conditions.
3. Role of rhizobacteria in plant growth promotion and soil
health
Plant growth promoting rhizobacteria is an umbrella term that spe­
cifically defines those bacterial species that greatly impact plant growth,
yield, and disease resistance through different modes of actions by
making a healthy and competitive association with plant root systems
(Prasad et al., 2019). They occupy a prominent place in agriculture
because of their participation in soil fertlilization through biofixation
and biosolubilization of essential nutrient elements along with the
production of plant growth regulators (Compant et al., 2019). PGPR
possess the ability to improve nutrients levels of economically important
crops by also increasing their antioxidant activities, phenolic contents,
and photosynthetic pigments (Singh et al., 2019a). It has been reported
that inoculation of PGPR such as Azotobacter, Pseudomonas and Bacillus
species have improved the nutrient contents or nutritional values of
some of the most important crops and vegetables, including lettuce and
soybean (Alori and Babalola, 2018). They employ different direct and
indirect mechanisms for the regulation of plant growth and improving
soil health. Moreover, the characteristics of an ideal PGPR (Harish et al.,
2019) make them extremely suitable due to their biological features
such as high rhizosphere competence, easy to mass multiply, enhance­
ment of plant growth, development and yield, suppression of pathogens,
broad spectrum of action, environment friendly, and compatibility with
other rhizobacterial species (Santoyo et al., 2012).
PGPR have a high adaptability in diverse soil environments, due to
their biochemical plasticity to metabolize a number of natural and
xenobiotic compounds. Considering their useful effects and mechanism
of action, it is not surprising that the combined application of PGPR
treatments have been proven more efficient than a single treatment
alone in inhibiting pathogens (Kumar et al., 2019). Hence, PGPR serve
as the most active ingredients in biofertilizer formulation. They can also
be classified on the basis of their beneficial effects. Numerous forms and
mechanisms of PGPR are largely harnessed to obtain agricultural traits.
Table 1 presents the names of the many PGPR species that contain
beneficial mechanisms and play important roles as bioremediators,
biostimulants, and bioprotectors of plant crops.
Soil is the natural habitat for plant growth promoting rhizobacteria
where they play a significant role in soil processes and the determination
of plant productivity. Almost all the beneficial activities within the soil
take place in the presence of other soil microbes, including the degra­
dation of crop residues, synthesis of soil organic matter, breakdown of
soil organic matter, biofixation and biosolubilzation of nutrients, which
increase soil fertility and plant productivity (Chaparro et al., 2012). The
importance of soil moisture for PGPR colonization cannot be neglected
as it is an essential condition for their association in the rhizosphere
(although, of course, there are also other relevant factors) (Vargas et al.,
2019).
The association of PGPR with plant roots is brought about by the
synthesis of various biomolecules which in turn increase soil fertility
(Kumar and Verma, 2019). They possess the ability to act on plant res­
idues where they are involved in decomposition and mineralization of
complex organic molecules (Raheem et al., 2019). These mineralized
organic compounds then get mixed with the soil and improve soil health.
Moreover, they also synthesize different phytohormones which greatly
impact root structure.
Rhizobacteria possess the ability to enhance nutrient contents in the
soil. Nitrogen is an essential nutrient for all types of microorganisms and
is an integral part of proteins, nucleic acids, and some other major
Z. Khatoon et al.
Table 1
The role of bulk and rhizosphere bacteria in plantbiofertilization (mainly by fixing nitrogen in legume symbiosis), biostimulation (mainly by producing phytohor­
mones), bioprotection (exerted by direct biocontrol of potential phytopathogens or induction of plant resistance system) andsoil bioremediation (polluted environment
cleaners). IAA: Indole-3-acetic; HCN: Hydrogen Cyanide.
Bacterial species
Acetobacter diazotrophicus
Azotobacter chroococcum
Advenella kashmirensis
Agrobacterium radiobacter
Achromobacter xylosoxidans
Azospirillum diazotrophicus
Azospirillum brasilense
Azospirillum brasilense
Azospirillum lipoferum
Bacillus aerius
Bacillus amyloliquefaciens
Bacillus atrophaeus
Bacillus anthracis
Bacillus aryabhattai
Bacillus circulans
Bacillus cereus
Bacillus filamentosus
Bacillus endophyticus
Bacillus firmus
Bacillus macroides
Bacillus megaterium
Bacillus mojavensis
Bacillus mucilaginosus
Bacillus oryzicola
Bacillus panthothenticus
Bacillus pseudomycoides
Bacillus siamensis
Bacillus sonorensis
Bacillus sphaericus
B. stearothermophilus
Bacillus subtilis
B. pantothenticus
Bacillus pumilus
Bacillus tequilensis
Bacillus thuringiensis
Bacillus velezensis
Beijerinckia indica.
Burkholderia vietnamiensis
Bradyrhizobium japonicum
Brevibacillus brevis
Journal of Environmental Management 273 (2020) 111118
Role Exerted mechanisms Beneficiated plant Reference
Biofertilization Nitrogen fixation – Mehmood et al.. (2018)
Biostimulation Gibberellin production Cereals Verma et al. (2001)
Bioprotection Siderophore production – Zhang et al. (2019)
Biostimulation Cytokinin production – Ibal et al. (2018)
Bioprotection Antibiotics – Mohanram and Kumar
(2019)
Biofertilization Ammonia production Agricultural fields Akbar and Sultan (2016)
Biofertilization Nitrogen fixation Sugarcane (Saccharum officinarum) Steenhoudt and
Vanderleyden (2000)
Biofertilization Phosphate solubilization Maize (Zea mays), Wheat (Triticum aestivum Lucy et al. (2004)
L.) & Rice (Oryza sativa)
Biofertilization Nitrogen fixation Rice (Oryza sativa) Thomas et al. (2019)
Biostimulation IAA production Reclamation of Cereals Schillaci et al. (2019)
Bioremediation degraded land – Hungria et al. (2016)
Heavy metals uptake – (Kamnev et al., 2005)
Biostimulation Gibberellin production Rice (Oryza sativa) Cass�
an et al. (2001)
Bioprotection HCN production – San Fulgencio et al.
(2018)
Biostimulation Gibberellin production Rice (Oryza sativa) Shahzad et al. (2016)
Bioprotection Lipopeptides – (Gupta et al., 2015) (
Bioprotection Antibiotics Tomato (Solanumlycopersicum) Abdallah et al., 2018)
Bioprotection Bacteriocins – Chowdhury et al. (2015)
Biostimulation IAA production Soybean (Glycine Max L.) Bai et al. (2002)
Bioprotection Protease production Wheat (Triticum aestivum L.) Verma et al. (2016)
Biofertilization Zinc solubilization Soybean (Glycine Max L.) and Wheat Ramesh et al. (2014)
(Triticum aestivum L.)
Biofertilization Potassium solubilization Tomato (Solanum lycopersicum) Mehta et al. (2015)
Bioprotection Protease production – (Contesini et al., 2018)
Bioprotection Lipopeptides Bean (Phaseolus vulgaris) (Ongena and Jacques,
Bioprotection Acquired and induced systemic Tomato (Solanum lycopersicum) 2008)
Bioremediation resistance Soybean (Glycine Max L.) Hashami et al. (2019)
Amylase production – (Vaikundamoorthy et al.,
Industrial waste remediation – 2018)
Rao et al. (2010)
Biofertilization Zinc solubilization Alfalfa (Medicago sativa L.) Yahaghi et al. (2019)
Bioprotection Chitinase production Turmeric (Curcuma longa) Chauhan et al. (2016)
Bioprotection Siderophore production Rice (Oryza sativa) Chaiharn et al. (2009)
Biostimulation Gibberellin production Red peppers (Capsicum) Joo et al. (2005)
Biofertilization Phosphate solubilization Mung bean (Vigna radiata) Biswas et al. (2018)
Bioremediation Degradation of xenobiotic – Arora et al. (2018)
compounds and allelochemicals
Biofertilization Potassium solubilization Maize (Zea mays) Feng et al. (2019)
Biofertilization Potassium solubilization – Hu et al. (2006)
Bioprotection Lipopeptides Rice (Oryza sativa) Hossain et al. (2016)
Bioprotection Protease production Maize (Zea mays) Agbodjato et al. (2018)
Biofertilization Potassium solubilization Tea plants (Camellia sinensis) Pramanik et al. (2019)
Biostimulation Gibberellin production Arabidopsis mutants Hossain et al. (2019)
Bioprotection Lipopeptides –
Bioprotection Chitinase production Sweet and Chili peppers (Capsicum annuum Thilagar et al. (2018)
L.)
Biofertilization Zinc solubilization – Saravanan et al. (2004)
Biostimulation IAA production – Hun et al. (2003)
Bioprotection Amylase production – (Xie et al., 2020)
Biofertilization Ammonia production Maize (Zea mays) (Marques et al., 2010) (
Biostimulation IAA production Chickpea (Cicer arietinum) Ait-Kaki et al., 2014)
Biostimulation Cytokinin production Tomato (Solanum lycopersicum L.) Tahir et al. (2017)
Bioprotection Lipopeptides – (Abdeljalil et al., 2016)
Bioprotection Catalase production Cucumber (Cucumis sativus) Islam et al. (2016)
Bioremediation Degradation of xenobiotic – Nguyen and Ha (2019)
compounds and allelochemicals
Bioprotection HCN production Maize (Zea mays) Agbodjato et al. (2015)
BiostimulationBioprotection Gibberellin production Chitinase Stone pine (Pinus pinea L.) Probanza et al. (2002)
production Rice (Oryza sativa) Veliz et al. (2017)
Biofertilization Ammonia production – Chenniappan et al. (2019)
Bioprotection Lipopeptides – P�erez-García et al. (2011)
Bioprotection Lipopeptides Tomato (Solanum lycopersicum L.) Maize Cao et al. (2018)
(Zea mays) (Adeniji et al., 2019)
Biofertilization Nitrogen fixation – Gouda et al. (2018)
Biofertilization Zinc solubilization Rice (Oryza sativa) Vaid et al. (2014)
Biofertilization Nitrogen fixation Gibberellin Soybean (Glycine Max L.)– Kaneko et al. (2002)
Biostimulation production Tudzynski et al. (2018)
Biofertilization Ammonia production Cotton (Gossypium hirsutum) Nehra et al. (2016)
(continued on next page)
3
Z. Khatoon et al.
Table 1 (continued )
Bacterial species
Burkholderia cenocepacia
Enterobacter, Pantoea and
Klebsiella sp.
Enterobacter oryzae
Enterobacter asburiae
Enterobacter ludwigii
Enterobacter cloacae
Frankia casuarinae, F. inefficax,
F. irregularis, and
F. saprophytica.
Frateuria aurantia
Gluconacetobacter diazotrophicus
Herbaspirillum seropidacea
Klebsiella varricola
Klebsiella oxytoca
Klebsiella pneumoniae
Kocuriae rythromyxa
Komagataeibacter xylinus
Leifsonia flava
Lysinibacillus sphaericus
Mesorhizobium ciceri
Mesorhizobium loti
Methylobacterium extorquens
Microbacterium
hydrocarbonoxydans
Nitrosomonas europaea
Novosphingobium
pentaromativorans
Ochrobactrum sp. JAS2
Paenibacillus sp IITISM08.
Paenibacillus barengoltzii
Paenibacillus xylanexedens
Pantoea agglomerans
Pantoea allii
Paraburkholderia phytofirmans
Phyllobacterium myrsinacearum
Pseudomonas plecoglossicida
Pseudomonas azotoformans
Pseudoalteromonas tetraodonis
Pantoea agglomerans
Paenibacillus polymyxa
Planomicrobium okeanokoites
Pseudomonas cichorii
Pseudomonas aeruginosa
P. chlororaphis
Pseudomonas corrugate
Pseudomonas donghuensis
Pseudomonas extremorientalis
Pseudomonas strains CHA0,
CMR12a, and PCL1391.
P. entomophila
Pseudomonas diminuta
Role Exerted mechanisms
Biofertilization Phosphate solubilization
Biofertilization Phosphate solubilization
Biofertilization Nitrogen fixation
Bioremediation Degradation of xenobiotic
compounds and allelochemicals
Biofertilization Zinc solubilization
BioprotectionBioremediation Catalase production
Degradation of xenobiotic
compounds and allelochemicals
Biostimulation Cytokinin production
Biofertilization Potassium solubilization
Biofertilization Zinc solubilization
Biofertilization Nitrogen fixation
Zinc solubilization
Biofertilization Potassium solubilization
Bioprotection Cellulase production
Biofertilization Nitrogen fixation
Bioprotection Acquired and induced systemic
resistance
Biostimulation IAA production
Biostimulation Cytokinin production
Bioprotection Catalase production
Biofertilization Nitrogen fixation
Biofertilization Phosphate solubilization
Ammonia production
Biofertilization Nitrogen fixation
Biostimulation Cytokinin production
Biostimulation Cytokinin production
Bioprotection Amylase production
Biofertilization Ammonia production
Biofertilization Ammonia production
Biofertilization Ammonia production
Bioprotection HCN production
Bioprotection Chitinase production
Bioprotection Chitinase production
Biofertilization Zinc solubilization
Biostimulation IAA production
Bioprotection Lipopeptides
Bioremediation Heavy metals uptake
Biofertilization Phosphate solubilization
Biofertilization Potassium solubilization
Bioprotection Siderophore production
Biofertilization Potassium solubilization
Biostimulation Cytokinin production
Bioprotection Lipopeptides
Bioprotection Chitinase production
Bioprotection Protease production
Biofertilization Phosphate solubilization
Bioprotection Ammonia production HCN
Bioprotection production
Bioremediation Cellulase production
Heavy metals uptake
Bioprotection HCN production
Bioprotection Antibiotics
Bioprotection Cellulase production
Bioprotection HCN production
Biostimulation IAA production
Bioprotection Antibiotics
Bioprotection Acquired and induced systemic
resistance
Bioremediation Degradation of xenobiotic
compounds and allelochemicals
4
Journal of Environmental Management 273 (2020) 111118
Beneficiated plant Reference
Tobacco (Nicotiana tabacum L.) Liu et al. (2019)
Various Crops Chung et al. (2005)
Mangart and Jam (Acacia acuminate) Dinnage et al. (2019)
– Mukherjee and Das
(2014)
Wheat (Triticum aestivum L.) Singh et al. (2018b)
Alfalfa (Medicago sativa L.) Khalifa et al. (2016)
– Adebusoye et al. (2007)
– Nouioui et al. (2019)
Tobacco (Nicotiana tabacum L.) Subhashini (2015)
– Saravanan et al. (2007)
Gramineous plants (maize, sorghum, wheat Roncato-Maccari et al.
and rice) (2003)
Maize (Zea mays) Canellas et al. (2013)
Tobacco (Nicotiana tabacum L.) Zhang and Kong (2014)
Sugarcane (Saccharum officinarum) Bohra et al. (2019)
Maize (Zea mays) Kuan et al. (2016)
Peanut (Arachis hypogaea) (Sharma et al., 2019)
Peanut (Arachis hypogaea) Jiang et al. (2019)
Fruits Augimeri et al. (2015)
Columbine(Aquilegia viridiflora) Cai et al. (2018)
Rice (Oryza sativa) Shabanamol et al. (2018)
Chickpea (Cicer arietinum) Ahmad et al. (2008)
Lotus species(Arabidopsis thaliana) (Kaneko et al., 2000)
Maize (Zea mays) (Lohar et al., 2004)
Arabidopsis, barley, maize, and soybean Koenig et al. (2002)
Field mustard (Brassica campestris L.) Haque et al. (2016)
– Fujita et al. (2020)
– Ipek
_ et al. (2019)
Paddy rhizosphere soil Abraham and
Silambarasan (2016)
– (Rani et al., 2018b)
– Yang et al. (2016)
Wheat (Triticum aestivum L.) Verma et al. (2016)
Wheat (Triticum aestivum L.) Kamran et al. (2017)
Maize (Zea mays) Pereira and Castro (2014)
– Agamennone et al. (2019)
– Rajkumar et al. (2009)
Maize (Zeamays) Gurdeep and Reddy
Wheat (Triticum aestivum L.) (2015)
Rice, banana, maize, sorghum and wheat Saha et al. (2016)
– Sinha et al. (2019)
Tobacco (Nicotiana tabacum L.) Zhang and Kong (2014)
Lentil (Lens culinaris) Gupta et al. (2015)
Legumes Rosier et al. (2018)
Chickpea, maize, rice, soybean, sugarcane Kour et al. (2019)
and wheat
forest soil, arctic alpine-tundra soil, stream M€annist€
o and H€
aggblom
water, lake and mire sediments, lichen and (2006)
snow algae
Maize (Zea mays) Hameeda et al. (2008)
Field mustard (Brassica campestris L.) Ahemad and Khan (2012)
Elephant grass (Pennisetum purpureum), Lawrance et al. (2019)
Rice (Oryza sativa), Pea (Pisum sativa), Paramanandham et al.
Amaranthus, (2017)
Tomato (Solanum lycopersicum L.) Kumar et al. (2005)
Cheng et al. (2019)
Avocado (Persea americana) Arrebola et al. (2019)
Wheat (Triticum aestivum L.) (Yu et al., 2018)
– Trivedi et al. (2008)
Tomato (Solanum lycopersicum L.) Ossowicki et al. (2017)
Wheat (Triticum aestivum L.) Egamberdieva (2009)
– Flury et al. (2017)
– Vodovar et al. (2006)
– Divya and Kumar (2011)
(continued on next page)
Z. Khatoon et al. Journal of Environmental Management 273 (2020) 111118

Table 1 (continued )
Bacterial species Role Exerted mechanisms Beneficiated plant Reference

Pseudomonas fluorescens Biofertilization Zinc solubilization - Potysz et al. (2016)

Pseudomonas fulva
Pseudomonas jessenii
Pseudomonas japonica
Pseudomonas koreensis
Pseudomonas moraviensis
Pseudomonas putida
Pseudomonas orientalis
Pseudomonas plecoglossicida
Pseudomonas protegens
Pseudomonas poae
Pseudomonas riboflavina
Pseudomonas stutzeri
Pseudomonas syringae
Pseudomonas vancouverensis
Pseudomonas veronii
Proteus vulgaris
Rhizobium meliloti
Rhizobium leguminosarum
Rhizobium phaseoli
Rhizobium pusense
Rhizobium radiobacter
Rhodococcus erythropolis
Serratia plymuthica
Serratia marcescens
Sinorhizobium meliloti
Staphylococcus saprophyticus
Streptomyces tendae
Streptomyces violaceusniger
Stenotrophomonas maltophilia
Stenotrophomonas rhizophila
Sphingomonas trueperi
Biostimulation Cytokinin production Arabidopsis Groβkinsky et al. (2016)
Bioprotection HCN production Wheat (Triticum aestivum L.) Weller (2007)
Antibiotics (Yang et al., 2017)
Biofertilization Phosphate solubilization Wheat (Triticum aestivum L.) Munir et al. (2019)
Bioprotection Siderophore production Scots pine (Pinus sylvestris L.) (Thiem et al., 2018)
Bioprotection Siderophore production Indian mustard (Brassica juncea) Rajkumar and Freitas
(2008)
Biofertilization Phosphate solubilization – Alaylar et al. (2020)
Bioprotection HCN production – Srivastava et al. (2019)
Bioremediation Reclamation of degraded land Wheat (Triticum aestivum L.) Hassan and Bano (2015)
Biofertilization Phosphate solubilization Tomato (Solanum lycopersicum L.) He et al. (2019)
Biostimulation Ammonia production – (Ahmad et al., 2012b)
Bioprotection Gibberellin production Field Mustard Kang et al. (2014)
Bioprotection Acquired and induced systemic Soybean (Glycine Max) Kumar et al. (2016)
Bioremediation resistance Mung bean (Vigna radiata) (Sharma et al., 2018)
Protease production Heavy metals – Thibodeaux et al. (2007)
uptake – Huang et al. (2019)
Biofertilization Potassium solubilization Rice (Oryza sativa L.) Khanghahi et al. (2019)
Biostimulation IAA production Pearl millet (Pennisetumglaucum) Arshad et al. (2019)
Biostimulation Gibberellin production Wild Pistachio Trees Etminani and Harighi
Bioprotection HCN production (2018)
Andreolli et al. (2019)
Biofertilization Zinc solubilization Siderophore Maize (Zea mays) Mumtaz et al. (2017)
Bioprotection production Tobacco (Nicotiana tabacum L.) Tian et al. (2009)
Bioremediation Heavy metals uptake – Abou-Shanab et al.
(2019)
Bioprotection Amylase production Cucumber (Cucumis sativus) Islam et al. (2016)
Bioprotection HCN production Kiwifruit (Actinidia deliciosa) Wicaksono et al. (2018)
Bioprotection Cellulase production Date palm (Phoenix dactylifera) Ferjani et al. (2019)
Bioremediation Reclamation of degraded land – (Rani et al., 2018a)
Biostimulation Cytokinin production Maize (Zea mays) Luo et al. (2019)
Bioprotection Siderophore production Soybean (Glycine Max L.) Rani et al. (2009)
Bioprotection Chitinase production – Naqvi and Moerschbacher
(2017)
Biostimulation Gibberellin production Rice (Oryza sativa L.) Yanni et al. (2001)
Biostimulation IAA production Common bean Volpiano et al. (2018)
Biofertilization Potassium solubilization Maize, banana,tobacco, sugarcane, Meena et al. (2015)
pigeonpea, and potato
Bioprotection Siderophore production – Ferreira et al. (2019)
Biofertilization Phosphate solubilization non-cropped, Chen et al. (2006)
undisturbed site
Bioprotection Chitinase production – Shameer and Prasad
(2018)
BioprotectionBioprotection Siderophore production Chitinase Field pumpkin Selvakumar et al. (2008)
Bioprotection production Protease production -(Poa pratensis) Rathore and Gupta (2015)
Zhang and Yuen (2000)
Biostimulation Cytokinin production Legumes Frugier et al. (2008)
Biostimulation IAA production Ornamental species Manzoor et al. (2019)
Bioprotection Siderophore production Helianthus annuus (Dimkpa et al., 2009a)
Bioprotection Antibiotics – Errakhi et al. (2016)
Biofertilization Nitrogen fixation Chickpea (Cicer arietinum L.) Abd-Alla et al. (2019)
Bioprotection Amylase production Maize (Zea mays) and Canola (Brassica Ghavami et al. (2017)
napus)
Biofertilization Nitrogen fixation Acacia acuminata Dinnage et al. (2019)

organic compounds. Because of its non-availability in the soil, PGPR
accumulate atmospheric nitrogen through the process of biological ni­
trogen fixation in the soil as well as in the plant roots (Ijaz et al., 2019).
Some of the PGPR can solubilize phosphate in the soil surface, thus
increasing the availability of phosphate ions in the soil which can be
easily taken up by the plant roots (Liu et al., 2019c). Such mechanisms
will be reviewed in detail below.
Various volatiles and other metabolites like antibiotics, hydrolytic
enzymes, and proteins produced by PGPR, get mixed into the soil and
function as soil conditioners for improving soil health (Prasad et al.,
2019). Various rhizobacterial species from different genera like Agro­
bacterium, Arthrobacter, Bacillus,Burkholderia, Collimonas, Enterobacter,
Paenibacillus, Pedobacter, Pseudomonas, Rahnella, Serratia have been re­
ported as the producers of volatile compounds and other antimicrobial
agents which inhibit the growth of soil borne fungal pathogens in turn
making soil fertile and healthy (Kanchiswamy et al., 2015; Chenniappan
et al., 2019). To mention a few examples, the volatiles dimethyl disul­
phide, 2,3-butanediol, furfural, dimethylhexadecylamine, propanoic
acid, butanoic acid, 5-hydroxy-methyl-furfural, β-caryophyllene, geo­
smin, 2-methyl isoborneol, 1-octen-3-ol, α-pinene, camphene, camphor,
methanol, and acetaldehyde are among the most frequently emitted
compounds by bacteria. Such volatiles have important implications in
the biocontrol of potential pathogens, stimulation of plant growth or
plant immune system, modulation of root-system architecture, among
many other roles (Hern� andez-Leo�n et al., 2015; Guti�errez-Luna et al.,
2010; Kanchiswamy et al., 2015; Rojas-Solís et al., 2018). In general, the
soil health gets improved through all these mechanisms and a healthy
soil body becomes a potential reservoir of macro and micronutrients
contributing towards good yields and long-term productivity (Summuna
et al., 2019).

5
Z. Khatoon et al.
4. Direct and indirect plant beneficial mechanisms exerted by
PGPR
PGPR exert direct and indirect plant growth promotion by producing
stimulating compounds, improving uptake of nutrients from soil or
protecting plants from pathogen infection (Orozco-Mosqueda et al.,
2018). Thus, PGPR maintain soil and plant health by producing an
arsenal of plant growth stimulating and antimicrobial compounds, some
of which can be excreted or diffused in solid medium, while others can
volatize. Examples of such compounds/mechanisms have been exten­
sively reviewed in several works (Glick, 2012). In fact, the importance of
detecting such mechanisms or the exertion of indirect mechanisms of
plant growth promotion has extensively demonstrated the beneficial
role of PGPR, with a great impact on sustainable agriculture (Santoyo
et al., 2019). Thus, several bioprotectant PGPR are now commercially
produced by different companies around the globe (Galindo et al.,
2013).
4.1. Biological nitrogen fixation
Biological nitrogen fixation (BNF) is the process of converting at­
mospheric elemental nitrogen into plant utilizable forms by nitrogen
fixing microorganisms using a complex enzyme system called as nitro­
genase (Masson-Boivin and Sachs, 2018). There are two main types of
BNF i.e., symbiotic nitrogen fixations which include the members of
Family Rhizobiaceae with leguminous plants (Dinnage et al., 2019) and
nonsymbiotic nitrogen fixation which involves the members of different
genera such as Arthrobacter, Acetobacter, Clostridium, Azotobacter, Ba­
cillus, Pseudomonas and Diazotrophicus, to mention but a few (Martins
et al., 2019). A major part of elemental nitrogen which comes into the
soil under natural conditions, is because of its fixation through beneficial
soil microorganisms like PGPR (Ji et al., 2019). Thus, plant microbe
interactions through biological nitrogen fixation contribute greatly in
the production of organic fertilizers (Kuypers et al., 2018).
Recent studies have shown that the Azospirillum species can supply a
sufficient amount of nitrogen to the sunflower and improve its yield and
productivity (Fukami et al., 2018). These bacteria may fix nitrogen up to
15 kg/ha/year and are also able to produce plant growth hormones like
indolacetic acid (IAA), thus helping plants in nutrients uptake,
improving plant growth and development (Aulakh et al., 2017). The use
of nitrogen fixing bacteria can reduce the applications of chemical fer­
tilizers, consequently lowering production cost. PGPR with nitrogen
fixing capacity can provide more soil organic nitrogen and other
essential nutrients in the soil body, thus resulting in lesser use of
chemical N fertilizers and increasing the availability of nutrients. In
addition, combined applications of different rhizobacterial species also
improve soil health and ensure sustainable agriculture compared to the
application of a single species. Recent studies have demonstrated that
common nitrogen fixers like rhizobia, do not always colonize or infect
the plant roots of leguminous plants, but they are usually coinhabiting
with diverse PGPR in other nonleguminous plants. In some cases, the
interaction of PGPR like the Pseudomonas species with Rhizobium sug­
gest a synergistic process to potentially form nodules and have better
nitrogen fixation capacities (Tilak et al., 2006). In some cases, horizontal
transfer of important nodulation and nitrogen fixation genes from
rhizobia to other Gammaproteobacteria (Pseudomonas) and Betapro­
teobacteria (Burkholderia) allows them to be able to form nodules in
roots of Robinia pseudoacacia (Shiraishi et al., 2010). These later works
highlight the important diverse interactions between common nitrogen
fixers, such as members of rhizobia and other saprophytic bacteria,
which are commonly known as plant growth stimulating species (San­
toyo et al., 2012).
4.2. Phosphate solubilization
Among the essential plant nutrients, phosphorus (P) is one of most
6
Journal of Environmental Management 273 (2020) 111118
important elements required for optimal plant growth and development.
It is involved in almost all major metabolic pathways occurring in plants
including photosynthesis, respiration, electron transport chain, biosyn­
thesis of macromolecules, and signal transduction, etc. (Khan et al.,
2010). Moreover, it also plays a role in improving root growth, seed
development, and normal crop maturity (Heydari et al., 2019). Plants
are able to absorb low amounts of phosphatic fertilizers because of their
fixation in the soil in the form of insoluble complexes (Alori et al., 2017).
Regular use of phosphatic fertilizers is not only costly but also not an
environmentally friendly approach. Under such circumstances, there is a
need to search for an environmentally friendly and ecologically safe
strategy for improving crop productivity in low P soils. Several PGPR
have been reported to be involved in the transformation of insoluble
phosphate complexes by using different mechanisms (Zaidi and Khan,
2005).
PGPR have been reported to be effective in making P available to
plants through solubilization and mineralization of complex P compo­
nents (Kafle et al., 2019). Typically, the solubilization of phosphorus
occurs because of the involvement of various organic acids produced by
soil bacteria . The production of organic acids by bacteria either in vitro
conditions or in field conditions, the results in chelating mineral ions
along with lowering the pH of the medium for bringing P into soil so­
lution (Zaheer et al., 2019). Another mechanism responsible for P-sol­
ubilization is known as mineralization which involves the breakdown of
complex organic P compounds into utilizable forms taken up by the
plants (Prasad et al., 2019). This mineralization process is catalyzed in
the presence of enzymes, most specifically, phosphatases and phytases
secreted by soil microbes (Wu et al., 2018). Phosphatases are enzymes
released extracellularly where they use organic forms of P as a substrate
and transform them into inorganic forms (Ghosh et al., 2018). Another
important class of enzymes i.e., phytases also plays an important role in
the release of P from phytic acid which is among the major components
of organic phosphorus in the soil (Puppala et al., 2019). Once the
organic and inorganic forms of P are transformed into simpler forms,
they can be easily taken up by the plants (Fig. 1). Considering the critical
effect of these phosphate solubilizing enzymes, it is highly desirable to
develop bacterial inoculants which have the ability to produce these
enzymes which could be a source of great practical value in sustainable
agriculture (Rathinasabapathi et al., 2018).
4.3. Potassium solubilization
Inoculation of potassium solubilizing PGPR has resulted in an
increased concentration of potassium in the soil as well as improved
potassium uptake by plants and enhanced growth of economically
important crops such as cotton, rape, pepper, cucumber, peanut, and
maize (Ashley et al., 2006). Potassium availability is one of the most
important factors in regulating cell growth such as development of hair
roots, growth of pollen tube, management of plant cellular osmotic
pressure, and transportation of various compounds in the plants (Ahmad
et al., 2018). Potassium solubilizing bacteria are able to transform
insoluble potassium present in soil into forms which can be easily taken
up and utilized by the plants (Etesami et al., 2017). A large number of
potassium solubilizing rhizobacteria (KSR) are present in the rhizo­
spheric soil compared with bulk soil. Potassium solubilizing bacteria can
release potassium form feldspar and aluminosilicate minerals present in
the soil (Bahadur et al., 2019).
The production of organic acids like citrate, oxalate, acetate, etc.
cause extensive degradation of clay silicates, mica, and feldspar from
sand stones, granite, calcite and dolomite of limestone. These organic
acids convert insoluble potassium into the soluble form of potassium
along with increasing the availability of nutrients to crop plants. It is
well documented that the Bacillus species can produce carboxylic acids
that largely solubilize potassium complexes in the soil in turn increasing
soil fertility and crop productivity as well (Majeed et al., 2018; Saha
et al., 2016). In the light of the above facts, it can be suggested that the
Z. Khatoon et al.
Fig. 1. Schematic portrayal of the potential mechanisms involved in plant growth promotion by phosphate solubilizing rhizobacteria.
application of KSR may contribute greatly to sustainable high yield, high
productivity, and enhanced soil fertility.
4.4. Zinc solubilization
In plants, zinc is mainly involved in the metabolism of carbohy­
drates, synthesis of cytochrome, detoxification of superoxide radicals;
zinc plays a role as a cofactor in many enzyme activities, stabilization of
ribosomal fractions, secretion of growth promoting hormones, cell
membrane integrity, establishment of floral tissues, and pollen tube
development, etc. (Kamran et al., 2017) (Fig. 2). Zinc deficiency leads to
reduced plant growth, yellowing of floral parts, reduced leaf size,
damaging grain quality, pollen formation, and root development (Cak­
mak, 2000). Plants can utilize zinc as divalent cation, but only a small
portion of zinc exists in the soluble form in the soil and rest of the zinc is
present in the form of insoluble complexes and minerals (Yahaghi et al.,
2019). Zinc deficiency issue can be solved by using zinc solubilizing
rhizobacteria (ZSR) which are the potential alternatives catering plant
zinc deficiency by mobilizing zinc complexes in the soil (Khan et al.,
2019). Various research studies have shown that the inoculation of ZSR
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Journal of Environmental Management 273 (2020) 111118
resulted in improved plant growth and increased zinc content in various
crops i.e., wheat, rice, and chickpea (Zaheer et al., 2019).
Solubilization of zinc is carried out by a number of mechanisms,
involving the secretion of various metabolites, proton extrusion or the
production of chelating compounds that result in deterioration of zinc-
complexes (Singh et al., 2018a). Moreover, production of organic and
inorganic acids like sulfuric acid, carbonic acid and nitric acids by ZSR
also facilitate the solubilization process of zinc (Costerousse et al.,
2018). Another reported mechanism for zinc solubilization is the pro­
duction of siderophores which are involved in chelating zinc com­
pounds, thus making them available to plants (Aeron et al., 2011).
It has been demonstrated in numerous studies that application of
certain species of the genus Bacillus, Pseudomonas and Serratia resulted
in increased zinc mobilization in wheat (7–12%) and soybean (Lef� evre
et al., 2014). Therefore, ZSR inoculation in crops might help us not only
to cope with the problems of malnutrition through improved nutrient
contents in the grains but also provide the best alternatives to zinc fer­
tilizers in the soils with available zinc sources.
Z. Khatoon et al. Journal of Environmental Management 273 (2020) 111118

Fig. 2. Zinc solubilizing rhizobacteria as a potential candidate for the amelioration of plant health.

4.5. Production of phytohormones
Phytohormones or plant growth regulators are basically the sub­
stances synthesized by plants which act as signaling molecules and in­
fluence various physiological processes of plants at very low
concentrations such as cell elongation, apical dominance, tissue differ­
entiation, cell division, and intracellular communication (Cass� an et al.,
2014). On the basis of their structural composition and their response to
physiological processes taking place in the plants, they are classified into
five major classes: (1) Auxins, (2) Gibberellins, (3) Cytokinins, (4)

Fig. 3. Variable effects of signaling molecules (phytohormones) produced by PGPR in eliciting developmental changes in plants.

8
Z. Khatoon et al.
Ethylene, and (5) Abscisic acid (Fig. 3). The plants under environmental
stress conditions often maintain their levels of endogenous hormones to
combat the negative effects of stress conditions (Dimkpa et al., 2009b).
The production of phytohormones is widely distributed among bacteria
associated with plants and soil. Hormonal responses are fundamental to
the growth and development of plants. Phytohormones contribute
largely in alleviating biotic and abiotic stress conditions. Auxins, gib­
berellins, and cytokinins have been implicated in plant developmental
processes where they respond to various stress conditions and regulate
plant growth (Sytar et al., 2019). Below we detail the role of some of the
main phytohormones produced by bacteria and their roles in the regu­
lation of plant development. To have a deeper reading on plant re­
sponses to phytohormones, as well as other classes of microbial
regulating signals, we suggest other excellent recent reviews (Fahad
et al., 2015; Nascimento et al., 2018; Ortíz-Castro et al., 2009).
4.5.1. Auxins
Auxins are biologically active molecules involved in number of
physiological processes in plants. Several studies have shown that
growth rate of plants treated with auxins producing PGPR was signifi­
cantly enhanced in comparison to nontreated plants (Metoui Ben Mah­
moud et al., 2020). Auxins are required for cell elongation, division, and
differentiation processes. The expansion of root hairs has a response to
auxin gradient, i.e., auxins induce signaling pathways for root epidermal
hair cells (Nascimento et al., 2020). It is reported that 90% of the genes
related to root growth are positively regulated by auxins on the basis of
transcriptome sequencing data analysis (Zhang et al., 2018). Moreover,
auxin production by plant growth promoting rhizobacteria can modu­
late and improve the antioxidant system in economically important
crops such as wheat (Acun ~ a et al., 2019). PGPR reported for auxin
production include the Rhizobium, Pantoea, Agrobacterium, Pseudomonas,
and Bacillus species (Tabassum et al., 2017). Indole-3-acetic acid (IAA)
producing PGPR have also been implicated in alleviating metal stresses
by reducing metal sorption and stimulating antioxidant enzymes (Sal­
azar et al., 2016). In general, IAA production by PGPR can be the best
option for improving crop and biofertilizer production in the future
because there are many options to potentially alleviate stress conditions.
IAA, being the most important auxin, is synthesized through several
parallel pathways. Four tryptophan dependent pathways are mainly
involved in the microbial synthesis of IAA. These pathways are named
according to their intermediate compound as the indole-3-Acetamide
pathway, indole-3-pyruvic acid pathway, indole-3-acetonitrile
pathway, and the indole-3-tryptamine pathway (Imada et al., 2017).
The indole-3-pyruvic acid pathway represents the main route for IAA
production in PGPR. Enzymes involved in IAA production are normally
encoded by large families of genes which has challenged the identifi­
cation and characterization of individual pathways. L-tryptophan serves
as a major precursor for IAA production both in plants and bacteria. The
first step of this pathway is the transformation of tryptophan to
indole-3-pyruvate catalyzed by aminotransferases. In the second step,
indole-3-pyruvate is converted to IAA in the presence of
flavin-containing monooxygenases (Matthes et al., 2019). This two-way
conversion of tryptophan to IAA is the main auxin biosynthesis pathway
that plays a significant role in several developmental processes in plants.
4.5.2. Gibberellins
They are a group of tetracyclic diterpenoid carboxylic acid de­
rivatives involved in several developmental and physiological processes
in the plants. Gibberellins act as signaling molecules for host plants
under stress and nonstress conditions (Goswami and Suresh, 2020).
Gibberellin producing PGPR protects plants from biotic and abiotic
stress by modulating antioxidant levels by decreasing superoxide dis­
mutase, flavonoids, and radical scavengers (Goswami and Suresh,
2020). Gibberellins stimulate absorption of calcium ions and other nu­
trients which are effective in regulating salinity stress by decreasing
peroxidation of lipid membranes (Carlson et al., 2020). Moreover, the
9
Journal of Environmental Management 273 (2020) 111118
exogenous application of gibberellins increases soybean growth by
enhancing the level of daidzein and genistein, that is an indication of the
protective role of gibberellins during unfavorable conditions (Ahanger
et al., 2018). Inoculation of the GA-producing Bacillus and Pseudomonas
species in crops resulted in increased dry weight, fresh weight, and
moisture content compared with the untreated control.
Biosynthesis of Gibberellin starts from geranyl-geranyl diphosphate
(GCPP) through isopentenyl diphosphate that is a 5-carbon building
block for all terpenoid compounds (Salazar-Cerezo et al., 2018). In the
chloroplast of most plants, the basic isoprenoid unit (IPP) is generated
by two pathways: Mevalonic acid pathway (Cytoplasm), Methyl eryth­
ritol phosphate pathway (Plasmid). The full process can be divided into
three phases according to their sub cellular compartments and the en­
zymes involved. In the first step, ent-kaurene production is catalyzed by
enzymes located in proplastids. In the next step, ent-kaurene is oxidized
to GA12-aldehyde which constitutes the general GA precursor and is
further catalyzed by monooxygenases at the endoplasmic reticulum
sites. In the final step, catalysis is proceeded by di-oxygenases in the
cytosol of the cell (Zou et al., 2019).
Moreover, gibberellins are responsible for seed germination, the
flowering process, stem elongation, and fruit setting in several higher
plants (Martins et al., 2019). Plants that are sessile rely on finely tuned
responses to their hormones and other signaling components to regulate
their growth and developmental processes. Therefore, it is critical for
plants to tightly regulate their hormone signaling pathways.
4.5.3. Cytokonins
Cytokinins belong to a group of growth regulators that can control
several developmental processes throughout the plant life cycle
involving gametogenesis, root meristem specification, vascular devel­
opment, shoot and root growth, meristem homeostasis, and senescence.
Moreover, they mediate responses to environmental prompts like light,
stress, and nutrient conditions (Arkhipova et al., 2007). Most of the
bacteria are able to synthesize cytokinins, thus raising the cytokinin
contents in the soil and plants growing there (Zürcher and Müller,
2016). Therefore, when the root environment is inoculated with cyto­
kinin producing rhizobacteria, it results in stimulating plant growth in a
manner suggesting increased plant growth and improved soil health.
Under stress, for example drought, the cytokinin contents of the plants
get reduced, and in this case, application of cytokinins have been shown
to promote stomatal opening, probably by acting in concert with accu­
mulated abscisic acid (ABA) (Sahu et al., 2019). The microbe-mediated
increase in the level of cytokinin in the plants is widely reported (Sel­
vakumar et al., 2018). Therefore, cytokinin-producing bacteria
entwined with plant growth promotion can be used as indicators in plant
health management practices.
4.6. 1-aminocyclopropane-1-carboxylate (ACC) deaminase
Inoculations with 1-aminocyclopropane-1-carboxylate deaminase
(ACCD) producing bacterial strains are considered a potent biological
approach to regulate the growth and tolerance of the stressed plant by
decreasing ethylene levels (Etesami et al., 2020). Ethylene is a gaseous
plant hormone which stimulates plant growth and developmental pro­
cesses. It is produced by almost all organs and tissues in higher plants,
but in smaller amounts except during fruit development and ripening
stages. Its biosynthesis can be largely stimulated by adverse environ­
mental conditions, such as drought stress (Brijesh Singh et al., 2019). In
the rhizosphere, ACCD producing bacteria catalyze the reaction of ACC
into a-ketobutyrate and ammonium which are used as carbon and ni­
trogen sources (Glick et al., 1998; Orozco-Mosqueda et al., 2020). In the
presence of ACCD producing rhizobacteria, ACC secreted by plant roots
in the rhizospheric soil gets degraded and then secretion of ACC from the
roots is promoted, subsequently decreasing ACC contents both in roots
as well as in leaves. Most of the plants inoculated with ACCD producing
bacteria show better growth under stress conditions i.e., drought stress,
Z. Khatoon et al.
flooding, heavy metal contamination, salinity, among others, compared
with noninoculated plants (Nascimento et al., 2018; Sarkar et al., 2018).
Recent reports suggest novel roles of ACC deaminase on the modulation
of inhibitory ethylene levels by the free-living ACC
deaminase-producing bacterium Pseudomonas fluorescens YsS6 on facil­
itating the nodulation process of alpha- and beta-rhizobia (Nascimento
et al., 2019). Additionally, it is been proposed that ACCD activity in
PGPR, like the strain UW4 of Pseudomonas sp., act in synergy with other
bacterial mechanisms to counter the salt stress, like the production of
trehalose. Trehalose is an osmoprotectant against various types of stress,
such as salinity or drought, and has been found in various organisms,
including nitrogen fixing rhizobia (Orozco-Mosqueda et al., 2019).
Therefore, new roles are expected to be discovered between ACC
deaminase and other beneficial mechanisms of PGPR.
4.7. Siderophores
Natural soil health can be maintained only through the application of
PGPR, which can be effective bioprotectants (Karthik et al., 2017). One
of the first mechanisms described to inhibit phytopathogens is the pro­
duction of iron-chelating compounds or siderophores (Kloepper et al,
1980). Since iron (Fe3þ) is among the most important nutrients and is
particularly deficient in plants under stressful and/or calcareous con­
ditions, several PGPR produce siderophores (of different types, such as
bacillibactins, pyoverdines, cephalosporins, etc.) in response to low iron
levels in the soil, therefore, when it is limiting, PGPR can form
Fe3þ-siderophores complexes, making it unavailable for other patho­
genic microorganisms, such as pathogenic fungi. By contrast, the rhi­
zobacterial (or plant) siderophores chelate iron and make it available to
the plants (Sinha and Parli, 2020). Several studies have employed
siderophores-producing rhizobacteria as potential biocontrol agents,
since these iron chelating compounds have been involved in antifungal
action by depraving the plant pathogens of this important element (Fe)
(Kour et al., 2019).
4.8. Volatile organic compounds (VOCs)
PGPR (and other organisms) produce volatile organic compounds
(VOCs) with different roles and functions during interactions with plants
and other rhizosphere microorganisms (Bitas et al., 2013). There is
enormous evidence suggesting that VOCs have dual direct and indirect
action during plant growth promoting activities (Santoyo et al., 2019),
that is, rhizosphere VOCs are able to induce plant growth directly or
indirectly, by restricting the growth of potential phytopathogens. For
example, the volatile N,N-dimethylhexadecylamine (DMHDA) that is
produced by the rhizobacterium Arthrobacter agilis UMCV2 inhibit the
growth of Botrytis cinerea and P. cinnamomi in vitro, protecting plants
from their attack. At the same time, the DMHDA compound induces the
Fe-uptake mechanisms of M. truncatula seedlings under Fe-deficient
conditions (Orozco-Mosqueda et al., 2013; Vel� azquez-Becerra et al.,
2013). Other PGPR volatile compounds like the dimethyl disulphide
(DMSD) is able to promote plant growth by enhancing the sulfur
nutrition in Arabidopsis plants, as well as exerting an antagonistic action
against important plant pathogens like B. cinerea, and simultaneously
act as elicitor of defence responses in plants (ISR) (Huang et al., 2012;
Rojas-Solís et al., 2018).
A pioneering work published by Ryu et al. (2003) demonstrated the
role of volatile compounds, primarily 2,3-butanediol and acetoin, pro­
duced by beneficial Bacillus bacteria in promoting the growth of Arabi­
dopsis thaliana. On the other hand, the volatile hydrogen cyanide (HCN)
has an antagonistic action toward pathogens. It is important in con­
trolling pathogens by inhibiting electron transport chain leading to
death of the cells (Aloo et al., 2019). Many bacterial genera have the
ability to produce HCN including Bacillus spp. and Pseudomonas spp.
(Santoyo et al., 2012). An HCN producing trait by bacteria affect plant
establishment with great potential by controlling fungal diseases (Aarab
10
Journal of Environmental Management 273 (2020) 111118
et al., 2019). The HCN produced by PGPR not only act as a biocontrol
factor against phytopathogens but is also involved in geochemical pro­
cesses in the substrate, such as the chelation of metals. Therefore, this
VOC indirectly increases the availability of phosphate in the rhizo­
sphere, beneficiating the associated plants (Kumari et al., 2018; Rijavec
and Lapanje, 2016).
4.9. Hydrolytic enzyme production
PGPR produce and excrete several hydrolytic enzymes such as cel­
lulases, pectinases, proteases, catalases, and chitinases. The defense
related activities of these enzymes have been proven against various
phytopathogens. Chitin is major structural component of the fungal cell
wall. Plant growth promoting rhizobacteria target fungal cell walls by
secreting chitinases, thus resulting in chitin degradation. In this way,
chitinolytic bacteria inhibit fungal pathogens like gray mold phyto­
pathogen Botrytis cinerea, which is able to infect more than 200 plant
species. Thus, chitinolytic PGPR act by reducing the severity of plant
diseases caused by fungal or oomycete pathogens, and in turn, improve
plant growth indirectly (Martínez-Absalo�n et al., 2014; Hao et al., 2017).
Cellulase producing rhizobacteria easily hydrolyze cellulose to
glucose via the synergistic actions of enzymes such as glucanases, hy­
drolases, and glucosidases (Siqueira et al., 2020). It is well documented
that cellulase producing bacteria can be considered as antagonistic
agents of fungal diseases (Sadeghi et al., 2017). Cellulosic bacteria also
provide a carbon source in the soil rhizosphere to improve soil health
and sustain the nutrient balance through degrading cellulosic residues
(Behera et al., 2017). These cellulose producing bacteria can also be
used for the biological transformation of biomass into biofuels (Siqueira
et al., 2020). Compared with chemical conversions, cellulase mediated
conversion processes are considered as green and ecofriendly
approaches.
5. Environmental cleanup by PGPR
Bioremediation refers to the application of biological agents/bio­
logical processes for the cleanup of hazardous materials from the envi­
ronment (Sampaio et al., 2019). The use of bioremediation has provided
an alternative to traditional methods for remediating metal-polluted
soil. In metal-polluted soils, the natural role of metal resistant plant
growth-promoting rhizobacteria is more important to improve soil
properties than in conventional agricultural practices (Sharma and
Archana, 2016). Most of the metals are categorized as toxic, but there is
great variability among their toxicity levels. Cadmium (Cd) and Lead
(Pb) cause harm to the soil organism by binding to respiratory proteins
and via oxidative damage i.e., by the production of reactive oxygen
species (Ullah et al., 2019). Even the lower concentration of these metals
is harmful to soil microorganisms. Bulk and rhizosphere bacteria play
major roles in the biogeochemical cycling of heavy metals, thus resulting
in cleaning up contaminated soil. Table 2 lists the many examples of soil
and rhizosphere bacteria, most of them with plant growth-promoting
properties, on environmental cleanup of contaminated soils with
organic and inorganic pollutants.
5.1. Degradation of persistent organic pollutants by PGPR
Biodegradation of persistent organic pollutants (POPs) is studied
from two perspectives: oxidative degradation through aerobic bacteria
and dechlorination by anaerobic bacteria. In aerobic bioremediation,
PGPR make use of atmospheric oxygen to degrade contaminants (Mur­
ugan and Vasudevan, 2018). Biphenyl has been successfully utilized by
bacteria to aerobically stimulate remediation of pollutant contaminated
soil (Chakraborty and Das, 2016). During this process, oxidative
degradation of polychlorinated biphenyl (PCB) takes place using several
genes and their associated enzymes (Terzaghi et al., 2018). Major en­
zymes involved in POPs degradation are dehydrogenases, dioxygenases,
Z. Khatoon et al. Journal of Environmental Management 273 (2020) 111118

Table 2
Employability of plant growth promoting rhizobacteria in transformation or degradation of persistent organic pollutants isolated from contaminated samples into
nonhazardous substances.
Soil/rhizosphere bacterial species or strain Contaminant remediated Source of isolation (Country) References

Bacillus subtilis Crþ3 Soil samples (India) Al-Gheethi et al. (2015)

Aeromonas veronii Azo dye (methylorange) Acclimated textile effluent Mnif et al. (2016)
Enterobacter cloacae Cdþ2 – Bhattacharya et al. (2018)
Bacillus cereus Crþ6 Yangtze River (China) Kumari et al. (2014)
Serratia marcescens Mnþ2 Waste water (Brazil) Queiroz et al. (2018)
Providencia sp.LLDRA6 Mnþ2 Soil simple Li et al. (2020)
Klebsiella pneumoniae Cdþ2 – Pramanik et al. (2017)
Enterobacter sp. Cdþ2 – Pramanik et al. (2018)
Acenetobacter calcoaceticus Asþ5 Soil sample Tripti (2018)
Alphaproteobacterium Coþ2 Anzali lagoon (Iran) Tajer-Mohammad-Ghazvini et al.
MTB-KTN90 (2016)
Pseudomonas aeruginosa Hgþ2 Sanitary landfill sample Imron et al. (2019)
Stenotrophomonas maltophilia Hgþ2 ASGM site (Gamia River) Niane et al. (2019)
Sphingopyxis sp.SE2 Hgþ2 Contaminated soil sample Mahbub et al. (2017)
Acineto bacter Nickle (Tolerance) Soil sample Costa et al. (2019)
Arthrobacter sp. Crþ6 Soil sample He et al. (2016)
Bacillus pumilus Chlorpyrifos Purchased Ahmad et al. (2012)
Rhizobium leguminosarum Cadmium Soil simple Pereira et al. (2006)
Rhizobium leguminosarum Niþ2 Sewage sludge treated soil sample Wani et al. (2008)
Rhizobium strain RL9 Nickle Nodules of lentil Wani and Khan (2013)
Cadmium –
Chromium
Lead
Copper
Rhizobium radiobacterMMSB60 Pb Soil sample El Aafi et al. (2015)
Mesorhizobium metallidurans Cadmium
Bacillus megaterium Cadmium Young spikes of hybrid Pennisetum Wu et al. (2019)
Bacillus megaterium Hydrolyzed polyscrylamide Soil sample Song et al. (2019)
(HPAM)
Bacillus megaterium Palladium – Chen et al. (2019)
Pseudomonas putida Lead Tannery effluent (water sample) (Nokman et al., 2019)
Chromium
Pseudomonas putida Phenol degradation – Niu et al. (2018)
Achromobacter sp. Quinclorac Soil sample Yang et al. (2020)
Bacillus cereus Chlorpyrifos Soil sample Duraisamy et al. (2018)
Gordoniasp.JAASI Chlorpyrifos (CP) –
Bacillus subtilis Chlorpyrifos Agricultural waste water
Tsukamurrella paurometabola Cadmium Soil sample (Thailand) Limcharoensuk et al. (2015)
Pseudomonas aeruginosa Cadmium –
Brevudimonas diminuta Arsenic Soil sample Singh et al. (2016)
Klebsiiella varricola Arsenic – Naureen and Rehman (2016)
Phyllobacterium myrsinacearum Cadmium Rhizosphere of Ma et al. (2013)
Zinc Sedunplumbizincicola
Pb
Bacillus mucilaginosus Zinc Soil sample Wu et al. (2006)
Copper
Pb
Burkholderia metalliresistens Cadmium Metal contaminated paddy soils of Guo et al. (2015)
Copper China
Pb
Zinc
Rahnella aquatilis Pb Root nodules of lentil Egamberdieva et al. (2016)
Photobacterium spp.MELDI Mercury Phragmites australis Mathew et al. (2015)
Pseudomonas koreensis Zinc Roots of Miscanthus sinensis Babu et al. (2015)
Copper
Arsenic
Cadmium
Pb
Pseudomonas nitroreducensAR-3 Chlorpyrifos Soil sample Aswathi et al. (2019)
Pseudomonas strain Ch1D Chlorpyrifos – Singh et al. (2009)
Bacillus aryabhattai Chlorpyrifos Soil of West Bengal Pailan et al. (2015)
Stenotrophomonas sp. Chlorpyrifos Industrial sludge (China) Kumar et al. (2018)
Serratia marcescens Diazinon Soil (Saudia Arabia) Wang and Liu (2016)
Ralstoniasp. DI-3 Diazinon Soil sample (China)
Achromobacter xylosoxidansJCp4 Chlorpyrifos – Akbar and Sultan (2016)
Psedumonas putidaPC1 and PC7 Caudusafos Soil sample Abo-Amer (2012)
Serratia marcescens Dichloro-diphenyl- Bidlan and Manonmani (2002)
trichloroethane
Alcaligenes strain KK Dichloro-diphenyl- Xie et al. (2011)
trichloroethane
Labrys portucalensisPCNB-21 Pentachloronitrobenzene (PCNB) (Li et al., 2011)
Rhodococcussp. IITRO3 Dichloro-diphenyl- Bajaj et al. (2014)
trichloroethane
(continued on next page)

11
Z. Khatoon et al.
Table 2 (continued )
Soil/rhizosphere bacterial species or strain Contaminant remediated
Chryseobacterium sp.PYR2 Organochlorinepesticides;
Hexachlorohexane (HCH)
Eubacterium limosumATCC 8486 Dichloro-diphenyl-
trichloroethane
Sphingobacteriumsp. DDT-6 Dichloro-diphenyl-
trichloroethane
Ochrobactrum sp. Dichloro-diphenyl-
trichloroethane
Bradyrhizobiumsp. 750 and heavy metal resistant PGPRs Multi-metal contaminated soil
Ochrobactrumsp. Enterobacter cloacae stenotrophomonas Phenanthrene
maltophilia (Consortium) Pyrene
Benzo-pyrene
hydrolases, hydratases, aldolases, etc. (Reddy et al., 2019). Bacterial
strains that degrade POPs through aerobic oxidation include various
genera like Pseudomonas, Bacillus, Achromobacter, Rhodococcus, Ral­
stonia, Corynebacterium, to mention but a few (Vergani et al., 2017).
In anaerobic degradation, anaerobic bacterial species breakdown
chemical compounds in the soil to release energy required for their
metabolic processes. Anaerobic bacterial respiration takes place by
means of electron acceptors such as sulphate and nitrates in unpolluted
soils. When soils are contaminated with PCB, they switch to reductive
dehalorespiration (Field and Sierra-Alvarez, 2008). Dehalorespiration is
a process in which bacterial species attack chlorine substituent in the
para and meta positions, thus replacing them with hydrogen atoms
(Furukawa and Fujihara, 2008). Bacteria involved in the process of
dechlorination, transforms higher chlorinated compounds to less chlo­
rinated compounds, thus decreasing their toxicity levels and further
making them available to aerobic degradation (Yim et al., 2008).
The intense and frequent use of pesticides has led to a persistence in
soil due to a lack of their in-time degradation (Rangasamy et al., 2018).
These pesticides loaded in the soil rhizosphere are responsible for
causing negative consequences on the microbial community and plants
as well (Rangasamy et al., 2018). Because of their long shelf life and
nonbiodegradable nature, these toxic chemicals persist in the environ­
ment and enter into the food chain causing serious health hazards (Singh
et al., 2008). These increased amounts of pesticides deteriorate the
whole ecosphere through biomagnifications (Morillo and Villaverde,
2017). Decomposition of pesticides can be carried out by biotransfor­
mation, biomineralization, bioaccumulation, biodegradation, bioreme­
diation, and cometabolism (Liu et al., 2019b). Bacterial degradation is
defined as bacterial mediated decomposition of pesticides into simple
inorganic compounds on the contaminated sites, soil rhizosphere,
ground water, and industrial systems (Subbanna et al., 2018). Therefore,
the PGPR which play their substantial role in pesticide removal from the
environment, are of special significance for improving soil health and
plant promotion.
6. Conclusions and perspectives
Unlocking the potential mechanisms of action in PGPR and its
beneficial interactions with plants is highly important to increase plant
growth and production. This must be done because of the prevailing
need to feed a continuously growing world population, which is ex­
pected to reach 10 billion by 2050 and peak in approximately
2070–2080 (Lutz et al., 1997). Therefore, one of the objectives of this
work is to emphasize the different mechanisms of PGPR, as well as their
enormous potential to generate optimal conditions for sustainable
agricultural production, which includes a reduction on the environ­
mental impact. Therefore, understanding of rhizobacterial ecological
roles in a microecosystem like the rhizosphere is an essential first step to
obtain better results in the field when inoculating PGPR (Santoyo et al.,
2019). There are several important aspects to determine the efficiency of
a bioinoculant with stimulatory or protective effects, including
12
Journal of Environmental Management 273 (2020) 111118
Source of isolation (Country) References
Qu et al. (2015)
– Yim et al. (2008)
– Fang et al. (2010)
Pan et al. (2017)
Soil (ïn situ work) Spain Dary et al. (2010)
– Arulazhagan and Vasudevan (2009)
regulation at the molecular level of genes involved in the production of
diffusible and volatile compounds as well as enzymes in the rhizosphere;
also the colonizing capacity of PGPR, interaction with other beneficial
soil microorganisms, tolerance and adaptive mechanisms to abiotic and
biotic stresses, among others. All these aspects have been extensively
studied and a broad knowledge has been generated; however, the dis­
covery of new bacterial strains (or even species) with plant growth
promoting activities emerge, which keeps unveiling the dark side of
known and unstudied ecosystems with potential applications in agri­
culture. In addition, novel molecular and genomic strategies are high­
lighting the specific but important roles of bacterial consortia in direct
and indirect activities of plant growth promotion (Carrio �n et al., 2019).
Despite all this knowledge, there is still an enormous gap in the transi­
tion from the laboratory and field, which is usually the bottleneck that
reduces the possibilities of expanding the use of PGPR in the agriculture.
In this phase, not only scientists, but other business and political actors
are required to create optimal and legal conditions to generate a bene­
ficial impact on agricultural and economic production among all,
without neglecting the aspect of sustainable agriculture and an envi­
ronment healthy for the population, particularly in those developing
countries.
Author contributions
Zobia Kathoon: Conceptualization, Investigation, Writing - Review­
ing and Editing. Suiliang Huang, Mazhar Rafique, Ali Fakhar, Muham­
mad Aqeel Kamran: Writing - Original Draft. Gustavo Santoyo:
Conceptualization, Investigation, Visualization, Writing- Reviewing and
Editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
G.S. thanks the CONACYT-M�exico (Proyecto No. 169346) and
Coordinacio�n de la Investigacio
�n Científica-UMSNH (2020) for financial
support to research projects.
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