Applied Soil Ecology 121 (2017) 102–117

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Applied Soil Ecology

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

Review

Bottlenecks in commercialisation and future prospects of PGPR MARK

a,⁎ b a c
Bushra Tabassum , Anwar Khan , Muhammad Tariq , Memoona Ramzan ,
Muhammad Saleem Iqbal Khana, Naila Shahida, Khadija Aaliyaa
a
Centre of Excellence in Molecular Biology, 87-West Canal Bank Road, University of Punjab, Lahore, Pakistan
b
Department of Genetics, Hazara University, Mansehra, KPK, Pakistan
c
School of Biological Sciences, University of the Punjab, Lahore, Pakistan

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

Keywords: During the entire developmental phase of plants, there exists an alliance among the soil, plant and micro-
Plant growth promoting rhizobacteria organisms. This association is developed when the microbial community in the rhizosphere is stimulated by the
biological control release of rhizodeposits from plants. Diverse groups of microorganisms rely on these rhizodeposits, thus es-
commercialization of PGPR tablishing a gradient of interactions from plant growth promotion to parasitism. One of the clearly beneficial
limitation to advertise PGPR
effects of plant growth-promoting rhizobacteria (PGPR) includes the suppression of deleterious microorganisms
PGPR specificity
PGPR field performance
along with the promotion of plant growth attributes. PGPR may produce antibiotics, compete for nutrients with
PGPR formulation pathogens or induce systemic resistance in the host plant to defend it against pathogens. For growth promotion,
PGPR employ the production of phyto hormones, fix nitrogen and solubilize phosphorus that directly affects
plant growth. Many PGPR have been effectively tested for their performance in biological control as well as plant
growth promotion such as Bacillus, Pseudomonas, Serratia and Burkholderia. The use of these strains has sig-
nificantly promoted plant growth and reduced disease occurrence in various economically important crop plants.
Based on these lucrative reports and eco-friendly behaviour, strains of Bacillus, Pseudomonas, Serratia,
Azospirillum and Streptomyces have been advertised. Microbial inoculants for the biological control of plant
diseases combined with plant growth promoters have great potential for a huge market share worldwide with an
annual growth rate of 15%. Successful commercialization of these strains is dependent on improvements and
advancements in interdisciplinary research, large-scale production, formulation methods, product marketing
and education of farmers.

1. PGPR: potential microbes for sustainable agriculture from various pathogens, including fungi, insects and viruses, thus
acting as biocontrol agents (Myresiotis et al., 2015; Mishra et al., 2015;
Rhizosphere is the nutrient-rich part of the soil surrounding plant Jha and Saraf, 2015). PGPR create stress tolerance (Tiwari et al., 2016),
roots and is a habitat for millions of microbes that thrive on root exu- enhance the efficiency of fertilizers, can act as biocontrol agents for
dates, termed rhizodeposits (García-Salamanca et al., 2013). Rhizode- disease control (Pieterse and Wees, 2015; Lecomte et al., 2016) and
posits comprise various compounds that aid the lubrication and nu- bioremediation (Patel et al., 2016; Zameer et al., 2016).
trient acquisition to plants (Baptist et al., 2015). These root exudates act PGPR promote plant growth and there are numerous reports of plant
as chemo attractants that welcome large and diverse microbial com- growth and yield stimulation by PGPR (Bergottini et al., 2015). Plant
munities living in the rhizosphere (el Zahar Haichar et al., 2014; Huang growth-promoting rhizobacteria produce various compounds, including
et al., 2014) to multiply the roots or adjacent rhizospheric soil growth regulators (phytohormones), siderophores, and organic acids,
(Shrivastava et al., 2014). A specific category of microbes bringing fix atmospheric nitrogen, solubilize phosphorus and produce antibiotics
benefits to the plant or involved in some positive root-microbe inter- to suppress harmful rhizobacteria. These substances either directly af-
actions are termed plant growth-promoting rhizobacteria (PGPR) (Zhou fect the metabolism of plants or improve the adaptive capacity of plants
et al., 2015). PGPR can enhance plant growth by employing multiple to absorb other nutrients from the soil (Santoro et al., 2015; Grobelak
mechanisms and assuring the availability and uptake of certain mac- et al., 2015; Gupta et al., 2015). Phytohormones, including auxins,
ronutrients as well as micronutrients to the plant (Jaisingh et al., 2016; cytokinins, gibberellins, ethylene and abscisic acid, help plants in
Khan and Bano, 2016). Simultaneously, PGPR facilitate plant protection growth processes such as cell enlargement, cell division and root

⁎
Corresponding author.
E-mail address: [email protected] (B. Tabassum).

http://dx.doi.org/10.1016/j.apsoil.2017.09.030
Received 7 November 2016; Received in revised form 19 September 2017; Accepted 20 September 2017
Available online 06 October 2017
0929-1393/ © 2017 Elsevier B.V. All rights reserved.
B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

extension (Kudoyarova et al., 2015). Conclusively, the rhizobacteria are

the leading deriving forces in recovering the soil nutrients and are
important for soil fertility (Babalola and Glick, 2012; Ahemad and
Kibret, 2014).
Burkholderia, Bacillus, Pseudomonas, Serratia, and Streptomyces are
few bacterial genera and Ampelomyces, Coniothyrium, and Trichoderma
are fungal representatives that are well characterized for their role in
the suppression of plant pathogens along with plant growth promotion
(Fishal et al., 2010; Bhattacharyya and Jha, 2012; Loganathan et al.,
2014; Sundaramoorthy et al., 2013; Bonaldi et al., 2015; Chen et al.,
2016). Although processes that determine the success of microbial
agents in disease control are quite complex, they can exert their ben-
eficial effect on plants by inhibiting the growth of pathogenic organisms
through various mechanisms.
Numerous PGPR-based biocontrol and plant growth-promoting
products are available on the market, and more are in the process of
development. Most of these products are based on Gram-positive mi-
crobes such as Bacillus (Ding et al., 2014) because they are easy to
formulate and can survive longer because they produce spores and can
tolerate the desiccation step in formulation. Although Gram-negatives Fig. 1. PGPR in the rhizosphere. Rhizosphere is activated by the production of various
strains, including Pseudomonas and Burkholderia, are also included in rhizodeposits by the plant. PGPR after being established in the rhizosphere not only
promote plant growth attributes but at the same time they provide competing circum-
commercial PGPR formulations because of their persistence, they are
stances for pathogens. Hence, PGPR utilize both direct and indirect mechanics to address
not easy to handle (Loganathan et al., 2014; Yuan et al., 2012). In- growth promotion and biological control. Production of phytohormones, nitrogen fixation
tegration of microorganisms for disease control/plant growth promo- and phosphate solubilization are included in direct mechanics, PGPR employ to enhance
tion in cropping systems and the elimination of chemical applications is plant growth. They may limit the success of deleterious plant pathogens by the con-
dependent on effective selection, screening and safety analysis of po- sumption of macro and micronutrients, production of antibiotics or toxins or by triggering
tential PGPR strains. Furthermore, knowledge of marketing and target plant’s own immune system. PGPR are isolated from their niche and screened for their
beneficial role in improving plant health. After passing through safety analysis PGPR are
diseases, cost of mass-scale production and registration procedures also
integrated in the cropping system to protect plant against harmful organisms.
need to be revised to raise the market status of these biocontrol entities.
This review is focused on the role of bacterial genera in plant growth
promotion and biological control of plant pathogens and their su- produced by various bacteria in the rhizosphere and is required by the
premacy over synthetic applications in this context. Moreover, hurdles plants for cell elongation, division and differentiation processes. Dif-
and benefits of the commercialization and future prospects of research ferent rhizobacteria utilize different pathways to produce IAA. Most of
on the use of microbes in the agriculture sector are also included in this the pathways are L-tryptophan dependent, and some are L-tryptophan
discussion. independent. To date, three L-tryptophan-dependent pathways are
known for the production of IAA, while the tryptophan-independent
2. Mechanisms employed by PGPR pathways are not well studied yet (Jha and Saraf, 2015). PGPR that can
produce IAA include Rhizobium, Pantoea agglomerans, Brady rhizobium,
PGPR employ different direct and indirect mechanics to stimulate Agrobacterium tumefaciens, Pseudomonas syringae, Bacillus subtilis, Ba-
plant growth and act as biocontrol agents. For plant growth promotion, cillus megaterium and Bacillus licheniformis (Hao et al., 2012; Mohite,
direct mechanisms are employed by PGPR, including the production of 2013; Xin and He, 2013; Méndez-Gómez et al., 2016; Ali et al., 2009).
growth regulators, nitrogen fixation and phosphate solubilization. In Similarly, plants treated with cytokinin-producing rhizobacteria
the direct mechanisms, PGPR residing in the plant body (Siddikee et al., showed an increased growth rate compared non-treated plants (Amara
2010) release growth regulators and other substances that directly af- et al., 2015). Cytokinin belongs to a group of growth regulators that are
fect the metabolism of plants to stimulate its growth (Glick, 2014; responsible for shoot formation, root elongation inhibition, improved
Vacheron et al., 2014). While biocontrol mechanisms are considered cell division and root development (Porcel et al., 2014; Jha and Saraf,
indirect PGP mechanisms, including antibiosis, competition, and pro- 2015). Several types of cytokines are produced by rhizobacteria in
duction of lytic enzymes, the bacteria indirectly improve plant growth which zeatin and kinetin are the most abundant. Rhizobacteria syn-
through the suppression of pathogens and enhancement of the plant’s thesize zeatin through two different pathways: direct and indirect. The
innate immunity against pathogens as outlined in Fig. 1. Although direct one involves the synthesis of dimethylallyldiphosphate (DMAPP)
bacteria and fungi, both of which are important in creating resistance and N6-isopentenyladenosine monophosphate (i6 AMP), while indirect
against plant pathogens, our focus is only on the extensively studied pathway involves cis-zeatin containing tRNA to release cytokinins.
bacterial communities implicated in plant growth stimulation and Different species of Pseudomonas, Proteus, Azospirillum, Bacillus, Es-
biocontrol. cherichia, Klebsiella and Xanthomonas have been reported to have the
potential to produce cytokinin (Castillo et al., 2015; Maheshwari et al.,
2.1. Production of growth regulators 2015; Frankenberger and Arshad, 1995).
Another crucial class of phyto hormones released by rhizobacteria is
Rhizobacteria can produce different types of phytohormones, in- gibberellins, which are responsible for different developmental pro-
cluding auxins, cytokinins, gibberellins, ethylene and abcisic acid, cesses such as seed germination, flowering process, stem elongation,
which facilitate different growth processes in plants, including cell and fruit setting in higher plants (Saleem et al., 2015). Studies have
enlargement and cell and root extension (Glick, 2014; Kaur et al., shown that plants with gibberellin-producing bacteria in their rhizo-
2016). sphere have better growth rates (Poupin et al., 2013; Vacheron et al.,
Studies have shown that the growth rate of plants treated with IAA- 2014). Only seven bacterial species from growth-promoting rhizo-
producing rhizobacteria was significantly increased compared with that bacteria have been reported for gibberellin-producing PGPR and in-
of non-treated plants (Kaymak et al., 2008; Amara et al., 2015). This is clude Bacillus amyloliquefaciens (Shahzad et al., 2016) and Sphingo-
because of the release of indole-3-acetic acid, which is an auxin monas sp (Khan et al., 2014).

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B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

2.2. Biological nitrogen fixation and Stenotrophomonas spp (Prasanna et al., 2012) (Stefan et al., 2012).
Some bacteria produce a single antibiotic while others may secrete
Nitrogen is, by far, the most limiting nutrient for plants. Although multiple substances; for example, strain UW85 of Bacillus cereus not
plentiful, nitrogen reserves are available, but plants cannot uptake or- only produces zwittermicin (Reimer and Bode, 2014) but can also
ganic nitrogen while bacteria have the potential to fix that organic produce kanosamine (Majed et al., 2016). The availability of nutrients
nitrogen for plants. Nitrogen-fixing bacteria are classified into two ca- and surrounding environmental stimuli strongly define the synthesis of
tegories: root/legume-associated nitrogen-fixing bacteria and free- antibiotics (Chowdhury et al., 2015). Similarly, the presence of major
living nitrogen-fixing bacteria. Root/legume-associated bacteria, such and minor minerals, including zinc, a carbon source, pH, temperature
Rhizobium, form nodules in the roots of plants. Free-living bacteria do and some miscellaneous parameters have a direct impact on antibiotic
not physically interact with the roots; rather, they live close to the roots synthesis (Bhatia et al., 2016; Mutturi et al., 2016; Compant et al.,
such that nitrogen fixed by these bacteria can easily be taken up by the 2010). The quantity of in situ-produced antibiotics by various biocontrol
plants. Examples are Azotobacter, Azospirillum, Herbaspirillum, agents can be measured, but the effective dose cannot be measured
Burkholderia, Bacillus, and Paenibacillus (Goswami et al., 2016; Geddes because antibiotics are produced in minor quantities at first; second,
et al., 2015; Habibi et al., 2014; Angus et al., 2013; Anand et al., 2013; several other less toxic organic compounds are also present in the rhi-
Huang et al., 2012). zosphere that belong to some other microbes. The mode of action of
many antimicrobial metabolites is poorly understood. However, some,
2.3. Phosphate solubilization such as phenazine and pyrroluitrin, are known to affect the electron
transport chain (ETC) in fungi: HCN adversely affects the activity of Cu-
Similar to nitrogen, the available form of phosphorus is not appro- containing cytochrome c oxidase; DAPG and biosurfactants disrupt the
priate for plants to absorb; rather, plants can only uptake the soluble membrane integrity as well as zoospores of pathogenic fungi (Haas and
form of phosphate that includes mono-basic and di-basic phosphate Défago, 2005; Raaijmakers et al., 2006, 2009).
(Jha and Saraf, 2015). Rhizobacteria utilize different mechanisms to
solubilize organic phosphate. The most common and prevalent one is 3.2. Competition
through organic acid such as acetic acid, malic acid, lactic acid, succinic
acid, oxalic acid, tartaric acid, 2-ketogluconic acid and citric acid (Patel Competition is the indirect interaction in which pathogens present
and Desai, 2015; Ahemad and Kibret, 2014). These acids are secreted in the rhizosphere compete with each other for food and/or essential
by PGPR as the end product of sugar metabolism. These organic acids, nutrients and physical site occupation (Philippot et al., 2013). From a
resultantly, lower the pH of the soil, making it acidic and triggering microbial perspective, the rhizosphere environment is frequently nu-
Ca2+ chelation to release the soluble form of phosphate from insoluble trient limited, and, for microbes to successfully colonize and survive,
compounds. Many species of Pseudomonas and Bacilli, including Bacillus they occupy the sites where water and carbon-containing nutrients are
megaterium, P. striata, B. coagulans, B. circulans, B. subtilis, P. polymyxa, more readily available. Mostly, the microbes occupy secondary root exit
B. sircalmous, P. florescens, Erwinia herbicola, P. cepacia, and Burkholderia points, damaged cells of epidermis and nectaries. The bacterial com-
cepacia, are considered important strains for phosphate solubilization munity in the rhizosphere competes for essential nutrients such as iron
(Liu et al., 2015; Goswami et al., 2013, 2014; Zhao et al., 2014; Stephen whose availability depends very much on soil pH, carbon, nitrogen and
et al., 2015). phosphorus levels and the levels and form of iron (Sivasakthi et al.,
2014). Generally, microbes need iron in concentrations of 10−6 M;
3. Indirect mechanism however, while in the rhizosphere, its quantity is hardly approximately
10−8 M. Thus, for microbes to survive in such an environment, they
In contrast to the direct mechanisms of PGPR, indirect mechanisms secrete low-molecular-weight iron-binding ligands termed siderophores
occur outside the plant body in which PGPR reduce or halt the harmful that have a high affinity to sequester iron from iron-limited surround-
effects of phytopathogens by producing different signals. The plant’s ings compared with fungal ones (Scavino and Pedraza, 2013). Thus,
defensive metabolic process responds to the signals sent from the bac- microbes make less iron available to pathogens and inhibit their growth
teria either by producing antagonistic substances or inducing resistance in the rhizosphere. For example, P. fluorescens and Serratia secrete
to pathogens. For biotic stress, rhizobacteria play their role to induce siderophores that have been proven to play role in the suppression of
systemic resistance; for abiotic stress, they provide protection against fungal pathogens by depleting iron (Trapet et al., 2016; Khilyas et al.,
unfavourable environmental conditions (Glick, 2014; Jha et al., 2011; 2016).
Nadeem et al., 2014; Gururani et al., 2013; Vacheron et al., 2014).
3.3. Lytic enzymes
3.1. Antibiosis
Microbes secreting cell wall-degrading enzymes lyse the cell walls of
The antagonistic activity of PGPR refers to the synthesis of anti- living organisms, and their general purpose is to obtain a carbon source
biotics or biosurfactants (secondary metabolites) (Doornbos et al., for nutrition. Lytic enzymes use different modes to kill or suppress
2012). Antibiotics are low-molecular-weight toxins produced by the harmful microorganisms in the rhizosphere. They may degrade the cell
bacterial community that can kill and/or poison other microbes. wall of pathogens by producing enzymes such as cellulases, chitinases
However, biosurfactants are ampiphilic compounds that can cause cy- and proteases (Patel, 2015; Naing et al., 2014; Charulatha et al., 2013).
tolysis and leakage while interacting with the membranes of harmful For example, S. plymuthica secretes chitinase enzyme (Vaaje-Kolstad
microorganisms (Banat et al., 2014; Bakker et al., 2013). Plant roots et al., 2013), while Paenibacillus strain and B. cepacia produce glucanase
inoculated with antibiotics-producing bacteria exhibit better and heal- (Li et al., 2015) to hydrolyse chitin and cellulose, respectively. Thus,
thier roots than non-treated roots (Philippot et al., 2013). Several an- they are also documented as effective suppressors of potential plant
tibiotics and toxins have been identified from the bacterial population pathogens (Pliego et al., 2011). Some other lytic enzymes target viru-
living in the rhizosphere. These include amphisin, 2,4-diacetylphlor- lence factors of pathogens such as phytotoxic fusaric acid produced by
oglucinol (DAPG), pyrrolnitrin, hydrogen cyanide (HCN), oomycin A, Fusarium oxysporum (Kumar et al., 2012).
phenazine, tensin, pyoluteorin, tropolone, and cyclic lipopeptides
(Sherathia et al., 2016; Nakkeeran et al., 2013; Wani and Khan, 2014; 3.4. Induced systemic resistance (ISR)
Pandya and Saraf, 2014), while oligomycin A, kanosamine, zwitter-
micin A, and xanthobaccinare are produced by Bacillus, Streptomyces, Induced systemic resistance (ISR) is a state of active resistance that

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B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

is dependent on the host plant’s chemical or physical barriers and is Saravanakumar et al., 2007b; Karthiba et al., 2010; Sivasundaram et al.,
triggered by specific abiotic or biotic stimuli (Tuzun, 2001; Senthilraja 2008), and some are available in the markets for routine use. PGPR
et al., 2013). It is not easy to distinguish ISR from systemic acquired consisting of a single rhizobacterial strain or in consortia have suc-
resistance (SAR) because both use similar compounds to suppress pa- cessfully been employed previously to control plant pathogens where
thogens. Considerable advancements have been made to reveal the multiple modes of applications were tested to screen the potentially
mechanisms involved in plant-PGPR-pathogen interactions. However, effective one. Zhang and Xue (2010) used a single rhizobacteria strain,
there is an absence of an overall elucidation for ISR signalling by bac- Bacillus subtilis SB24, as PGPR for the suppression of Sclerotinia stem rot
teria. It has been reported that certain structural components of bac- (SSR) in soybean. In the laboratory and greenhouse trials, they em-
teria such as flagella, lipopolysaccharides (LPS) and siderophore and ployed a cell suspension, cell-free culture filtrates and broth cultures of
antibiotic production are the determinants of ISR (Pieterse et al., 2014; B. subtilis strain SB24 on plants and observed 50 to 75% reduced my-
Naureen et al., 2015; García-Gutiérrez et al., 2012). Recently, certain celial growth of the pathogenic fungus Sclerotinia sclerotiorum, and the
other biochemicals produced by PGPR have been proposed to trigger suppression of sclerotial formation was up to 90%. The most effective
ISR. For instance, an N-alkylated benzylamine derivative produced by concentration of PGPR in that study was found to be
P. putida, BTP1 (Kumar et al., 2015), volatile organic compounds 5 × 108 CFU mL−1. Furthermore, Suprapta et al. (2016) used a bac-
(VOCs) produced by B. subtilis and B. amyloliquefaciens (Yuan et al., terial consortium to treat rice blast caused by Pyricularia oryzae. This
2012; Pérez-García et al., 2011), dimethyl disulphide produced by B. consortium comprised Bacillus, Pseudomonas and Achromobacter strains.
cereus C1L (Meldau et al., 2013) and DAPG produced by P. fluorescence The roots of the subjected plants were treated with a bacterial soil
CHA0 (Hernández-León et al., 2015). PGPR use the salicylic acid (SA)- suspension, and up to 100% disease reduction was reported in both
independent pathway to trigger ISR that involves jasmonate or ethylene greenhouse and field trials. Most of the PGPR were used against fungal
signalling (García-Gutiérrez et al., 2013; Elsharkawy et al., 2015). The pathogens, while few were reported for bacterial and viral disease
production of these hormones activate a set of defence genes, leading to control. Shen et al. (2015) treated fungal disease (Fusarium wilt dis-
disease resistance against plant pathogens (Shoresh et al., 2010). The ease) of banana caused by Fusarium through soil application of PGPR,
few ISR inducing defence mechanisms in plants are as follows: cell wall the Bacillus amyloliquefaciens strain, in a field study and reported sig-
reinforcement (Ahn et al., 2007), production of secondary metabolites nificant disease reduction. However, Hahm et al. (2012) reported the
(Choudhary et al., 2007) and accumulation of defence-related enzymes control of bacterial spot disease in pepper by treatment with a cell
(chitinases, glucanase, peroxidase, phenylalanine ammonia lyase and suspension of consortium comprising Ochrobactru and Novosphingobium.
polyphenol oxidase) (Bhattacharyya and Jha, 2012). We suggest that They reported 100% seed germination with a 7–15% weight increase in
the biopriming of plants with beneficial rhizobacteria can provide greenhouse and field trials. Additionally, Harish et al. (2009) effectively
systemic resistance against a wide range of plant pathogens, including controlled the Banana bunchy top virus in bananas by treating the
fungi, bacteria and viruses. Furthermore, evidence from various fields virus-affected plants with a talc-based formulation of P. fluorescens and
and pot trials have confirmed PGPR as ISR mediators against some endophytic Bacillus spp.; 80% disease reduction was reported in
insects and nematodes (Pineda et al., 2010; Singh et al., 2016); hence, greenhouse and 52% in field trials. Table 1 shows the effective man-
they can be applied for potential control. PGPR that are ISR mediators agement of numerous plant diseases using a suspension and other for-
include B. subtilis, B. cereus, B. pasteurii, B. amyloliquefaciens, B. my- mulations of PGPR strains isolated from the rhizosphere and phyllo-
coides, B. pumilus, B. sphaericus, P. fluorescence, Rhizobium legumino- sphere.
sarum, P. putida, Serratia marcescens (Bhattacharyya and Jha, 2012) and PGPR are applied in various ways to control plant pathogens. These
endophytic Actinobacteria (Jacob and Sudini, 2016). may include inundate application, augmentative application and oc-
casional application. Inundate application is the direct inoculation of
4. Application of PGPR in agriculture for disease control and plant bacteria with a dense population to an infection court so that the pa-
growth promotion thogen is eliminated (Heydari and Misaghi, 2003; Heydari et al., 2010).
It involves seed or soil treatment (Heydari et al., 2004; Heydari et al.,
Every year, plant pathogens cause cumbersome losses to food and 2010) or application of biocontrol microorganisms on fruit for protec-
cash crops worldwide. These losses need to be addressed in an effective tion against pathogens (Heydari et al., 2010). Similarly, augmentative
manner to ensure the quality as well as quantity of agricultural products application is the inoculation of a low population of BCAs at one place.
(Ekundayo et al., 2011; Heydari et al., 2010). In addition to appropriate They multiply and spread to other parts of the plant and provide de-
agronomic practices, farmers rely heavily on chemical fertilizers, pes- fence against pathogens (Islam et al., 2005; Heydari et al., 2010). Oc-
ticides and insecticides for biocontrol and plant growth promotion casional or one-time application is applied once on a crop per year and
(Ekundayo et al., 2011; Daayf et al., 2003). The development of insect- is used to maintain the pathogen population below threshold levels
and weed-resistant varieties, human and animal health concerns and (Heydari et al., 2010).
environmental safety concerns have brought PGPR under remarkable PGPR have a significant role in plant growth promotion, which they
consideration (Ekundayo et al., 2011; Zongzheng et al., 2010; Houdart execute through the production of phytohormones, associative nitrogen
et al., 2009; Shi et al., 2006). Moreover, the use of synthetic chemicals fixation, phosphate solubilization and/or siderophore production
in fields has created the problems of eutrophication, Zn deficiency (Richardson et al., 2009). Wu et al. (2015) promoted the growth of the
(Cardoso and Kuyper, 2006; Babalola and Glick, 2012), reduction in the pepper plant by treating them with B. amyloliquefaciens and B. subtilis,
activity and diversity of indigenous rhizosphere microflora (Ferreira which are IAA producers and phosphate solubilizers, respectively. The
et al., 2000; Babalola and Glick, 2012) and non-biodegradable chemical survival rate was reported to be increased by 58.42% in both pot and
residues in soil (Dar et al., 2011). Conclusively, the use of biocontrol field experiments. The reported growth promotion was attributed to
microorganisms in place of chemicals is a better paradigm for sustain- phytohormones that play a critical role in plant architecture such as the
able plant production (Babalola and Glick, 2012). PGPR have several balance between auxin and cytokinin regulating organogenesis and
advantages over chemical pesticides: (i) PGPR are safe for the en- defining root architecture (Aloni et al., 2006). The auxin to cytokinin
vironment, human health; (ii) PGPR-based formulations degrade more ratio can be changed by root-colonizing PGPR because they release IAA,
readily in soil, and (iii) PGPR have a reduced ability to create resistance cytokinin, gibberellin and ABA (Dodd et al., 2010; Overvoorde et al.,
against plants (Berg and Smalla, 2009). Seed treatment and foliar spray 2010).
of different microbial biocontrol agents have reduced the disease in- Several studies have demonstrated that PGPR-based formulations
cidence in major crops such as wheat, rice, corn, sugar beet and cotton improve the growth attributes of the subjected plant such as shoot
(Heydari et al., 2007; Heydari et al., 2010; Senthilraja et al., 2013; elongation, yield, plant biomass, seed germination, seedling vigor, plant

105
 Table 1
A summary of PGPR strains effective against deleterious viruses, bacteria, fungi, insects and nematodes along with modes of application and level of disease reduction in green house, pot or field trials.

Crop Plant Pathogens PGPR strain Mode of Application Trial Reduction in Disease Reference
B. Tabassum et al.

Rice (Oryza sativa) Rhizoctonia solani (sheath blight) P. fluorescens Seed, soil and root Field trial 49.71% Nandakumar et al. (2001)
treatment
Sheath rot caused by Pseudomonas flourescens Pf1, TDK1, TV5 and Bacillus subtilis bioformulation Glass house and field Significant Sundaramoorthy et al.
Sarocladium oryzae isolate TH10 trials (2013)
Rice blast caused by Pyricularia Bacillus methylotrophicus KDDA, Bacillus amyloliquefaciens O38, Root treatment and soil Green house and field 100% Suprapta et al. (2016)
oryzae Pseudomonas aeruginosa OR3 and Achromobacter xylosoxidans suspension trials
Al7Kla
Pearl millet (Pennisetum Sclerospora graminicola (Downy Bacillus pumilusT4, B. pumilus INR7, B. amyloliquefaciens IN937a, Liquid suspension and talc Green house and field significant Raj et al. (2003)
glaucum) mildew) Bacillus subtilis IN937b, B. pumilus SE34, Brevibacillus brevis formulation trials
IPC11, and B. subtilis GB03
Soybean Sclerotinia sclerotiorum SSR B. subtilis SB24 Bacterial suspension and Green house trials 60–90% Zhang and Xue (2010)
filtrate
Macrophomina phaseolina Bacillus megaterium, B. cereus and P. fluorescens Liquid formulation Pot and field trial 35.5%–87.5% Attia et al. (2011)
Peas (Pisum sativum) Fusarium wilt caused by Trichoderma and Pseudomonas Seed treatment Pot trials 50% Sharma (2011)
Fusarium
Tomato (Lycopersicum Fusarium Bacillus subtilis S499 Seed treatment with spore Field trial 65–70% Nihorimbere et al. (2010)
esculentum) suspension
Phytophthora infestans Bacillus sp. AB11, Bacillus subtilis AB10, AB12, AB14, AB17, Soil suspension Green house trials 60–70% Lamsal et al. (2013)
Bacillus amyloliquefaciens AB05, Paenibacillus polymyxa AB15
Fusarium wilt caused by Bacillus subtilis (BS2) Talc bio-formulation Field trials 58.4% M et al. (2014)
Fusarium oxysporum f.sp.
lycopersici
Tomato yellow leaf curl virus Enterobacter asburiae BQ9 suspension Green house trial 58.7% Li et al. (2016)
(TYLCV)
Peanut Apergillus niger (Crown rot) Paenibacillus polymyxa Seed treatment Field trial 99% Haggag (2007)

106
Chick Pea Helicoverpa armigera B.thuringiensis. var. kurstaki Liquid formulation Field trial Significant Ahmed et al. (2012)
pepper (Capsicum annuum) Phytophthora blight Bacillus subtilis Cell suspension Green house trial 86.8 and 71% Lee et al. (2007)
Bacterial spot disease Ochrobactrum lupini KUDC1013 and Novosphingobium Cell suspension Green house and field significant Loganathan et al. (2014)
pentaromativorans KUDC1065 trials
Bitter Almond Agrobacterium tumefaciens P. fluorescens Agrobacterium Root treatment Field trial 97.89% Rhouma et al. (2008)
(Crown gall) radiobacter B. subtilis
Agrobacetrium rhizogenes
Egg plant (Solanum Fungal disease B. subtilis SY1 Liquid formulation Field trial significant Zongzheng et al. (2010)
melongena)
Oilseed rape (Brassica Sclerotinia sclerotiorum P. fluorescens P13 Liquid spray and seed Field trial 59% Li et al. (2011)
napus) (Sclerotinia stem rot treatment
Olive groves Pseudomonas savastanoi pv. B. subtilis F1 and F-4 Seed treatment Green house 50% Krid et al. (2012)
Savastanoi. (olive knot) experiment
French bean (Phaseolus Rhizoctonia solani Glomus sinuosum, Gigaspora albida, P. fluorescens Soil treatment Field trial Significant Neeraj and Singh (2011)
vulgaris)
Banana Banana bunchy top virus (BBTV) P. fluorescens strains CHA0 Talc- based formulation Green house and Field 72–80% Kavino et al. (2008)
trials
Banana bunchy top virus (BBTV) P. fluorescens (Pf1) and endophytic Bacillus spp. (EPB22) Talc-based formulation Green house and Field 52–80% Harish et al. (2009)
trials
Fusarium oxysporum Pseudomonas sp. (UPMP3) and Burkholderia sp. (UPMB3) Liquid inoculation Pot trial 51% Fishal et al. (2010)
Fusarium wilt disease Bacillus amyloliquefaciens NJN-6 Soil application Field trial Significant Shen et al. (2015)
Tea (Camellia sinensis) Exobasidium vexans (blister Pseudomonas and Bacillus Talc-based formulation Field 85% Saravanakumar et al.
blight) foliar spray (2007a)
Sunflower Sunflower necrosis virus B. licheniformis, Bacillus sp. P. aeruginosa, Streptomyces Foliar spray, seed and soil Field trials 34.8–40% Srinivasan and Mathivanan
(Sunflower necrosis disease) treatment (2009)
Cotton Verticillium wilt Paenibacillus xylanilyticus YUPP-1, Paenibacillus polymyxa YUPP- Liquid suspension Pot experiment/ 38.1% Yang et al. (2013)
8 and Bacillus subtilis YUPP-2 greenhouse trial
Cotton leaf curl virus disease P. aeruginosa, Burkholderia sp. and Bacillus spp. Foliar spray Green house trial 73.6% Ramzan et al. (2016)
(continued on next page)
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B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

height, fresh and dry weight, and leaf area (Prasanna et al., 2012;

Selva Kumar et al. (2013)

Hungria et al., 2010; Wang et al., 2016) of economically important
crops, including rice, tomato, soya bean, and wheat (Almaghrabi et al.,
Meng et al. (2013)
Ding et al. (2013)

2013; Imran et al., 2015; Shahzad et al., 2013) as outlined in Table 2.

However, the impact of PGPR on plant roots and the whole plant in
quantifiable terms remains challenging. One strategy to reveal this is to
Reference

inoculate the plant roots with PGPR in vitro and monitor the outcome on
the plant by evaluating the change in the growth rate of the primary
root, increase or decrease in the lateral roots and effect on root hair
development (Contesto et al., 2008; Chamam et al., 2013).
Reduction in Disease

28.50–40.25%

5. Commercialization of PGPR
stem canker:
black scurf:
30–41.45%
17–57%
84.6 %

PGPR production from laboratory to farmer requires careful and

extensive study and market survey; it has to pass through different
stages before appearing on the farmer’s shelf. The process to select a
specific strain or consortia for commercial availability depends on the
Green house trial

Greenhouse trial
Greenhouse trial

crop requirement (Bhardwaj et al., 2014). For example, if a crop is

vulnerable to fungi, as in case of potato and other sugar-rich crops, the
consortia of PGPR may contain a strain with antagonistic activity for
fungi. The climate in a certain geographic region has an impact on
Trial

PGPR performance (Compant et al., 2010). Thus, climate change may

substantially impact the diversity and activities of plant-associated
microbial communities (Drigo et al., 2008). According to Rashid et al.
Mode of Application

(1997), in different ecological zones of Punjab wheat performance is

quite variable in response to bacterial inoculation. In Pakistan, increase
Seed treatment
Soil treatment

Soil treatment

in the yield was observed from 10 to 35% as compared to the control. A

country could have various ecological zones as the ecological zone is a
combination of climate, soil properties and temperature of the region.
The ecological zone is defined in terms of climate, temperature and soil
properties; thus, a country may have different ecological zones. To
provide PGPR and BCAs for different ecological zones of a country, it is
very difficult for any company to develop and supply different micro-
bial consortia for different zones of a single province/state.
Considerable climate change induces increased temperature, re-
Bacillus amyloliquefaciens and Bacillus subtilis

sulting in severe drought that not only affects the plant but also affects
the performance of PGPR (Heidari and Golpayegani, 2012). Environ-
mental stresses may also result in inadequate biological activity such as
salt and drought in certain areas, which means low soil nutrients. The
functions of dwelling soil microbes have not been properly discovered
yet, for that very reason commercial inoculants may not be effective
Bacillus and Pseudomonas
Bacillus amyloliquefaciens

when used, as they are usually not derivative of locally isolated mi-
crobes. Climate changes are likely to induce changes in plant phy-
siology and root exudation. As L-tryptophan is a precursor for indole
PGPR strain

acetic acid, and this amino acid present in root exudates, the decrease
in tryptophan due to climate change means the PGPR will produce a
low quantity of IAA, affecting the vegetative growth and root pro-
liferation of the plant. The root Exo metabolite tryptophan can regulate
the synthesis of auxins in soil microflora, including introduced rhizo-
Potato bacterial wilt (Ralstonia

bacteria. The rhizosphere micro flora possesses plant growth-promoting

black scurf and stem canker
disease (Rhizoctonia solani)

activity when the concentration of tryptophan in the rhizosphere is

Scab (Streptomyces spp)

sufficiently high (Kravchenko et al., 2004). An elevated temperature

might induce changes in plant physiology; together, they likely lead to
Plant Pathogens

changes in the composition, abundance or activity of plant-associated

solanacearum)

microbial communities. Consequently, microorganisms known for their

valuable effects on plant health or growth might also be impaired, in
terms of exhibiting their desirable properties and colonization capacity
under certain conditions (Compant et al., 2010).
The success of application of PGPR in various climate zones and for
a particular variety of cultivated crop can be well predicted by under-
standing the plant growth stimulation mechanism, disease control by
Table 1 (continued)

rhizobacteria and effect of abiotic factors on PGPR interaction. Hence,

for maximum effectiveness of the employed PGPR strain, region-spe-
cific microbial strains need to be identified to achieve higher yields
Potato
Crop

with better biological control under specific climatic conditions

(Fischer et al., 2007). Similarly, plant cultivar is another important

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 B. Tabassum et al.

Table 2
Summarized PGPR strains reported to be effective for plant growth promotion. Various modes of application and the specific plant growth attribute affected are described in green house, pot or field trials.

Crop PGPR strain Growth parameter Trial Response References

Rice (Oryza sativa) Pseudomonas culture Nitrogen and Phosphorus uptake Pot trial +++ Yadav et al. (2014)
Providencia sp., Brevundimonas sp., Ochrobacterium sp., Anabaena sp., Calothrix sp., nitrogen fixing potential Pot ++++ Prasanna et al. (2012)
Anabaena sp.
P. putida, P. fluorescens, A. lipoferum Yield Enhancement and Higher Zn Content Field trial ++ Sharma et al. (2014)
Pearl millet (Pennisetum Bacillus subtilis strain GBO3 and B. pumilus strain SE34 IAA production, phosphate solubilization Green house ++++ Raj et al. (2003)
glaucum)
Soybean Azospirillum brasilense and Bradyrhizobium japonicum Nitrogen fixation Field trial +++++ Hungria et al. (2013)
Peas (Pisum sativum) Variovorax paradoxus ACC deaminase Green house +++ Wang et al. (2016)
Tomato Pseudomonas putida, Pseudomonas fluorescens, Serratia marcescens, Bacillus Nitrogen fixation Green house +++ Almaghrabi et al. (2013)
amyloliquefaciens, Bacillus subtilis and Bacillus cereus
Peanut (Arachis hypogaea) Rhizobium, Pseudomonas and Bacillus Nitrogen fixation, Pot +++ Mathivanan et al. (2014)
Chick pea (Cicer arietinum) Ochrobactrum ciceri and Mesorhizobium ciceri IAA-production, nitrogen fixation Field trial ++++ Imran et al. (2015)
Pseudomonas aeruginosa and Mesorhizobium nitrogen and phosphorus uptake pot and field trial +++ Verma et al. (2013)
Pepper (Capsicum annuum) Bacillus amyloliquefaciens and Bacillus subtilis IAA-production, phosphate solubilizer Pot and field +++ Wu et al. (2015)

108
Egg plant (Solanum melongena) Brevibacillus sp B65 IAA, ARA, anti-fungal activity and ammonia Green house ++++ Ratón et al. (2014)
production
Oil seed rape (Brassica napus Bacillus megaterium A6 solubilizing phosphorus Green house pot +++++ Hu et al. (2013)
L.)
French beans (Phaseolus Bacillus sp phosphate solubilization pot +++ Saxena et al. (2013)
vulgaris) Paenibacillus polymyxa (Pp) and Pantoea agglomerans Nitrogen fixation pot culture ++++ Chauhan and Bagyaraj (2015)
Banana Bacillus amyloliquefaciens Phosphate solubilizer and IAA producer pot and field +++ Wang et al. (2013)
Tea (Camellia sinensis) Pseudomonas putida, Bacillus megaterium, Bacillus subtilis, Bacillus subtilis and IAA, nitrogenase activity, phosphorus solubilization Field ++++ Çakmakçı (2016)
Pseudomonas fluorescens and ACC deaminase activity
Maize (Zea mays) Pseudomonas thivervalensis and Serratia marcesens ACC deaminase activity field +++ Shahzad et al. (2013)
Achromobacter sp., Burkholderia sp., Pseudomonas sp. and Arthrobacter sp Nitrogen and Phosphorus content Pot +++ Arruda et al. (2013)
Potato (Solanum tuberosum) Achromobacter xylosoxidans, Pseudomonas oryzihabitans and Variovorax paradoxus auxins and ACC deaminase Pot and field trial ++++ Belimov et al., (2015)
Strawberry Alcaligenes, Staphylococcus, Agrobacterium, Pantoea and Bacillus phosphate solubilization, nitrogen fixation, ACC Field trial ++++ Ipek et al. (2014)
deaminase
Cherry (Prunus cerasus) Bacillus mycoides and Bacillus subtilis IAA production, phosphate solubilization, nitrogen Field trial ++++ Arikan and Pirlak (2016)
fixation
Marigold (Tagetes minuta) Pseudomonas fluorescens, Azospirillum brasilense Nitrogen fixation Greenhouse ++++ del Rosario Cappellari et al.
(2013)
Cotton Bacillus sp. phosphate solubilization field +++ Qureshi et al. (2012)
Applied Soil Ecology 121 (2017) 102–117
B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

Fig. 2. A generalized scheme of the bio pesticide formulation by in-

dustry where PGPRs are preserved in an appropriate carrier molecule
and packaged for commercial application at farmer’s end. Several
PGPR formulations are commercially available in market by different
commercial producer and different Government institution.

factor with an impact on the field performance of a given PGPR strain Although PGPR have the potential scope in commercialization,
(Egamberdieva, 2011). Inoculation of defined consortia of PGPR strains there are some safety issues associated with environment and humans.
may have a different response on plant growth that varies depending on For a successful PGPR inoculum, the selected strain should be able to
the plant cultivar used. Therefore, PGPR inoculants should be plant colonize the plant roots, can persist in the rhizosphere and should not
cultivar specific to develop the successful association trait with those represent a potential sanitary risk for the environment and human
bacteria. Additionally, if the soil is of alkaline nature, then a good health. Certain bacterial strains exhibit promising effects in promoting
phosphate solubilizer must be provided. Additionally, if farmer needs plant growth in controlled conditions of the laboratory but fail in field
vegetative growth for a crop, then hormone-producing PGPR may be experiments due to their ineffectiveness in colonizing the rhizosphere
included. To market a PGPR-based product, the crop requirements are and plant roots (Benizri et al., 2001). These strains cannot adapt to the
preferred. Thus, there is no unique PGPR strain that may perform well plant microenvironment and, hence, cannot compete with the existing
for all crops, cultivars and environment, implying more effort for native bacterial community for establishment and persistence in soil.
companies. Certain PGPR strains such as P. aeruginosa, P. cepacia and B. cereus
The process of commercialization (Fig. 2) is outlined as follows: pose a threat to infect human beings as opportunistic pathogens
(Nakkeeran et al., 2005). For example, Stenotrophomonas maltophilia is
1 The field survey is an important aspect of commercialization. Unless found in the rhizosphere associated with the roots of cultivated plants,
companies or institutes do not know about the properties of the soil including potato, wheat and maize (Garbeva et al., 2001; Sturz et al.,
or crop for which PGPR is used, climatic conditions of the area and 2001) and produce high amounts of IAA that promote plant growth.
farmer adaptability to biological products, PGPR product may not However, this bacterium is associated with bacteremia, cystic fibrosis
perform as expected. and urinary tract infections in humans (Friedman et al., 2002). The
2 The isolation and screening of PGPR, if the type of soil and crop is commercial companies should therefore prefer the microbial consortia
known, occur in the laboratory. The screening of region-specific, with zero impact on human/environment health. The government
local PGPR strains is needed as emphasized by Adesemoye et al. should also regulate the screening procedure and laws for selecting
(2009) because no microbial inoculant can be universal for all PGPR strains for commercial purpose. Another environmental safety
ecosystems. Furthermore, in screening, nutritional optimization is issue associated with PGPR strains is they may have neglected non-
an important aspect. The best strain is selected for each trait—e.g., targeted effects on the native microbial community such as: (i) re-
phosphate solubilization, hormone production, nitrogen fixation, placement of the native non-target species through temporal struggle
biocontrol activity and accdeaminase activity—and preference is for nutrients (competitive displacement); (ii) hypo-virulent PGPR
given to strains with multiple properties. If consortia are provided, strains might gain virulence through gene transfer (pathogenicity); (iii)
then the compatibility of strains must also be analysed—e.g., the release of toxins/allergens that remove native non-targeted species
biocontrol bacteria Bacillus amyloliquefaciens inhibits the growth of (toxicity/allergenicity) (Gullino et al., 1995; Cook et al., 1996). The
other bacteria such as Pseudomonas spp. abovementioned safety concerns need to be clarified before the large-
3 The selection of the carrier material and method required for in- scale acceptance, registration and adoption of PGPR for pest and dis-
oculation must be selected based on of the microorganism’s viabi- ease management.
lity, availability to plant roots and feasible application. Liquid for-
mulations are not preferred for survivability and propagation of
microorganism; rather, solid carrier materials are considered best 6. Limitations to advertise PGPR
for field applications. pH, organic matter and the nutritional content
are considered as the selection of carrier. According to careful estimation, crops are attacked by approxi-
4 The selected bacteria are first evaluated in pots in a control en- mately 67,000 different pest species, including phytopathogens, weeds,
vironment with subsequent application in farmer fields. Extensive many invertebrates and few vertebrate species, causing approximately
trials are done before the product is to be market. 40 percent loss of crop yield worldwide (Chandler et al., 2011). The
potential of PGPR in biological control has increased gradually because
they offer the best substitute to chemical pesticides and other

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B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

supplements (Droby et al., 2009). However, compared with chemical on a cotton crop because they may not be compatible with the crop on
pesticides, few biocontrol agents are registered for commercial avail- which they are inoculated. The growth condition of different crops
ability. In a productive PGPR formulation, the rhizobacterial strains might hinder the adaptability of PGPR to survive. This compels the
should exhibit high competitive saprophytic ability, high rhizosphere commercial vendors of PGPR to provide separate consortia for different
competence, feasible mass multiplication, a broad spectrum of action, crops, making it difficult for companies to introduce different products
enhanced plant growth, compatibility with other rhizobacteria, and for different crops.
environmental safety. Additionally, the strains should tolerate abiotic Many biopesticides are highly selective. Usually, a biological control
stresses such as heat, desiccation, UV radiation and oxidizing agents targets only a single major pathogen. For example, bioinsecticides
(Nakkeeran et al., 2005). based on baculoviruses are selective for single or a limited number of
The selection of carrier is a key step for the survival and efficiency of species of insects, and BT targets major pests but only those of the
PGPR. The value addition of various compounds as active agents to Lepidoptera order. Thus, these are safe for non-target species, including
enhance the stability of product, application efficacy, safety and per- humans and other mammals, beneficial microbes and insects but have
sistence in the field is another important step for the success of the very low profit potential, which is a large disadvantage of biopesticides
product and leads to commercialization. Generally, these products are (Chitrampalam et al., 2011; Jackson, 2007; Cummings, 2009). Biolo-
formulated as wet-able powders, dusts, granules and oil-based liquids. gical control agents differ in host specificity, which is a highly variable
The formulations are in two forms—dry powder (solid) and liquid biological trait; hence, a narrow host specificity is a limiting factor in
suspensions. Dust, granules and oil-based liquids with mineral and or- the commercialization of PGPR. The cause may be that PGPR have a
ganic carriers (Ardakani et al., 2009; Heydari et al., 2010) are being dedicated plant microenvironment to colonize either plant roots (en-
used for the preparation of formulations. Powder preparations can be dorhiza), shoots, leaves (phyllosphere), or fruits or seeds (Laca et al.,
either a wettable dry powder or moist powder culture or both. Various 2006). There are soil-borne and foliar pathogens, and BCAs are required
carrier materials being used are turf, peat, kaolinite talc, pyrophyllite, to target both types of pathogens. PGPR can survive both in the rhi-
lignite, zeolite, alginate, montmorillonite, sawdust, press mud and zosphere and phylloplane. For the best performance, a specific pa-
vermiculite (Rabindran and Vidhyasekaran, 1996; Nakkeeran et al., thogen-targeted PGPR strain for a particular crop is needed that can
2005). Carriers not only protect bacteria from desiccation, resulting in successfully colonize the plant part in that particular microenviron-
the increase in the survival rate and shelf life but also provide a fa- ment. This is also a problem for companies providing biocontrol agents
vourable microenvironment for the fast growth of bacteria after their for soil-borne and foliar pathogens because not all types of bacteria
release. survive on phylloplane. Recently, Liu et al. (2017) studied that 28 elite
The commercialization and success of strains for biocontrol is based PGPR strains with a variable response to six fungal plant pathogens and
on market demand, broad spectrum action, consistent activity, ex- other characteristics of plant growth. Thus, a single isolate cannot in-
tended shelf life, low capital costs, environmental safety, quality control hibit different fungal pathogens. Companies marketing biofertilizer
and affable associations between scientific organizations and industries containing BCAs should have an efficient method to obtain the data
(Bhattacharyya and Jha, 2012). from their consumers and know the requirement of the farmer with
Factors that limit the commercialization of PGPR formulation in- respect to plant pathogens—e.g., B. velezenis may be an efficient bio-
clude the following: control strain against Rhizoctonia solani, but this strain is not efficient
against Pythium ultimum in crops such as potato, where both the fungal
6.1. Farmer psychology pathogen mentioned above is a problem regarding how a single bio-
control agent will meet the need of the farmer. For a problem such as
Chemical fertilizer and pesticides have been the mainstay of crop this, companies should have survey teams and previous data and divide
protection for more than 50 years; hence, a wealth of experience is the territory among the survey team that comprises the technical and
available regarding their effectiveness that provides confidence to marketing personnel that provide robust feedback to the companies
farmers and growers. They have an immediate effect on nutritional where they must have different BCAs that target respective fungi. Ad-
availability and crop pathogens, producing result in a short time frame. ditionally, the mode of application of PGPR must be specific towards
Additionally, with agro chemicals, a small dose provides higher benefit. the pathogen. For example, for sheath blight control in potato triggered
In comparison, the PGPR-relevant products lack practical evidence for by Rhizoctonia solani (a soil borne fungus), seed treatment of the seed
their instant effectiveness, creating uncertainty in farmers about their with such a PGPR strain is needed so that it can colonize the potato
performance (Pannell, 2003; Moser et al., 2008). The knowledge roots and have significant biocontrol activity against R. solani. The
needed by farmers to obtain effective control with pesticides is lower environmental conditions, soil properties and ecological habitat do also
than that with tactics such as biocontrol (Cowan, 1991; Cowan and have an impact on the performance of the biological control agent
Gunby, 1996). Large fixed costs of biopesticides pose a disadvantage for (Benhamou et al., 1996).
early adopters because the cost will only decrease once the technology
is used more widely. Furthermore, to make a handsome profit for ve- 6.3. Microbial preference for PGPR formulation
getable and fruit crops, along with the yield, the cosmetic appearance is
mandatory. The risk associated with an unmarketable crop turns high, Commercially available PGPR formulations prefer Gram–positive
forcing the growers to rely on chemical pesticides rather than on bacteria such as Bacillus and Paenibacillus spp because they confer
choosing the untested, new crop protection technique of biopesticides. higher population stability during formulation and storage of inoculant
This risk-averse preference of farmers creates hindrance in the com- products (Kokalis-Burelle et al., 2005). Although several Gram-negative
mercialization of many bio pesticides. bacterial strains (like Azospirillum, Pseudomonas) are potential PGPR
strains with efficient biocontrol ability as well but are difficult to for-
6.2. Specificity of PGPR strains mulate because they do not produce spores. Thus, a commercial for-
mulation based on Gram-negative PGPR has a short shelf life, and
The crop specificity of PGPR is independent of root colonization. bacteria are easily killed upon desiccation of the formulation (Perez-
Some PGPR show less specificity, whereas others may display much Garcia et al., 2011; Kamilova et al., 2015). Although it is much more
broader specificity. After colonization, the metabolites produced by difficult to handle Gram negatives, their effect should be preferred over
PGPR induce defences in plant either by inhibiting the pathogen or Gram positives due to their persistence. To overcome the short shelf life
interacting with the host. Thus, the combination of bacterial strains of Gram-negative-based formulations, maintaining sufficient viable
used on a sugarcane crop as PGPR may not perform well when applied bacterial inoculum for an acceptable period of time is a valid option.

110
B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

Increasing the number of microbes in the inoculant can confer a longer 6.6. Variability in the field performance of PGPR
shelf life to the formulation. Even upon the decline in the population
over time, sufficient cells remain alive at seeding time. For PGPR, they must colonize the roots to be effective. The in-
Most of the available PGPR formulations comprise a single micro- oculated bacteria must sufficiently establish and propagate in an eco-
bial strain that may not perform well in the field. However, if a higher logical environment (Schroth and Becker, 1990). Therefore, the com-
diversity is preferred over a single strain in a PGPR formulation, a more petitive process of root colonization is affected not only by the
symbiotic relationship with plants will be obtained because some will characteristics of PGPR but also the host. Additionally, for an effective
help in plant growth promotion and others will help suppress disease response, a specific population density of PGPR strains is required.
through their independent mechanisms of action. Diverse microbial Several different PGPR strains can colonize a single host at various
populations act together as a community and are pivotal for nutrient population densities—for instance, maize. The strain that colonizes the
uptake and suppression of a particular disease. maize hybrid at the highest level may not be the best colonist of a
different maize hybrid.
PGPR developers face many problems, including crop or even the
6.4. PGPR survival and stability inside formulations cultivar specificity of PGPR. The field performance of a given for-
mulation varies with the multiplicity of climatic and environmental
Formulation into products with a longer shelf life regarding Gram- conditions of the crop, including the soil type, temperature, and rain-
negative bacteria (non-spore formers) is quite a problematic task (Berg, fall. These attributes change from field to field, thus causing a disparity
2009). The commercialization of PGPR can be faster with formulations in the potentiality of PGPR-based formulations. Compared with the
with a broad spectrum of action with consistent performance and in- controlled environment of a laboratory, it is difficult to predict how an
creased shelf life under field conditions. Several critical elements are organism will react when placed in the field, another challenge of using
involved in the development of a successful inoculant such as the for- PGPR.
mulation of the inoculant, mass multiplication, selection of the strain, For the efficient performance of PGPR in the field, an appropriate
carrier selection, packaging and marketing. The formulations play a mode of application is mandatory that depends on the pathogen and/or
role in stabilizing the microorganism, protecting the microbe at the plant trait being targeted. Farmers, if not educated properly, may not
target zone, aiding its delivery and increasing the efficacy of the mi- obtain the desired benefit from PGPR formulations. For example, to
croorganisms against the target. Furthermore, details of the production control a seed-borne disease, seed application with PGPR is re-
and formulations of biocontrol products are trade secrets that seriously commended; if the farmer applies the said formulation on aerial plant
hamper scientific advancement in these areas, consequently lessening parts, the field performance will be badly affected. Regardless, no such
the promotion of these products. specific application is required in the case of chemical use.
The compatibility of bacterial consortia in bioformulations is also a
problem. Many bacterial species are not compatible with other strains, 6.7. Regulatory issues
causing problems for the selection of bacterial species. The formulation
should not be toxic to plants, must release the bacteria and should be Regulatory issues are additional challenges of PGPR. In every
easily dissolvable in water. Its cost effectiveness, consistent control of country, there are different risk assessments and efficacy testing po-
plant diseases, and compatibility with other agrochemicals are also very licies present to avoid unregulated release of potentially damaging
important factors to be considered. Furthermore, the carriers must be biological organisms, but the procedure should simpler for organic and
economical and readily available for formulation development sustainable growers. Although numerous biological control products for
(Nakkeeran et al., 2005). common pathogens are commercially available, due to the complex
regulatory policies, only few of them are registered. Furthermore, the
development of appropriate and cost-effective delivery systems serve as
6.5. PGPR handling and re-inoculation an added obstacle to produce commercially successful microbes
(Ravensberg, 2011; Glare et al., 2012). Time-consuming and expensive
As bioformulations are a living product, special considerations are registration procedures for new products are also a huge obstruction for
required for strain selection, preparation and packaging. Because the the market expansion of bacterial biocontrol products (Berg, 2009).
inoculants have to be produced, stored, delivered, and ultimately used Because of the challenges faced in formulation, screening and ap-
by the grower, the proper concentrations of inoculants in a carrier have plication, PGPR need to be improved in their potential as commercial
to be maintained over a significant period of time. To maintain the inoculants. The development of PGPR as reliable components for the
microbial load and robustness in field application, they must have the management of sustainable agricultural systems must be facilitated by
ability to be propagated and re-produced. The carrier must have the advanced knowledge of their formulation, mechanisms of action, di-
ability to facilitate the inoculant to self-reproduce and colonize the versity, colonization ability and their application. Although PGPR
target plan upon delivery. Furthermore, the product should be com- performs well under laboratory conditions, there are many limitations
patible with the grower’s work. All these factors must be well con- to be addressed to successfully develop the product. In addition to the
sidered to make the product sufficiently effective to be used by the mentioned limitations, researchers must acquire knowledge regarding
consumer, as well as the efficiency and cost. how to apply and deliver these unique pesticides to ensure maximum
Another constraint that limits the commercialization of PGPR is the performance, which is at present a huge concern for producers and
mishandling of the product by growers, explaining why PGPR perfor- consumers.
mance in field conditions is not very good compared with that under Regardless, despite the discrepancies of the estimated market size
controlled conditions, making the commercialization of these products for microbial biocontrol agents, a considerable annual growth rate of
very challenging. The end user of PGPR might not be technically skilled 15.6% per year in global agrochemical industry has been observed.
to handle PGPR products, and they may mishandle the product with More than 20 different Bacillus-based products have been sold in China
respect to providing appropriate conditions before use that affects the to eliminate soil-borne diseases of plants (Heydari et al., 2010). Like-
efficacy of the product. Additionally, PGPR have to be re-inoculated wise, commercial products of B. subtilis are used in the United States
over time because bacteria will not survive in the soil forever. That’s (US) to treat soil-borne pathogens of peanut, cotton, corn, soya bean,
why naturally occurring bacteria quickly returns to normal levels after small grain crops and vegetables (Nakkeeran et al., 2005; Heydari et al.,
a season, an encouraging factor of PGPR. 2010). B. thuringiensis has gained ample market size due to its broad-
spectrum activity against invertebrate pests (Glare, 2000). Other PGPRs

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 Table 3
Detailed outline of the selected PGPR-based bio formulation available commercially in the market. The country of origin and the specific crop they are recommended for is also outlined.

Product Name Composition Country Benefit/Target pathogen/disease Suitable for

B. Tabassum et al.

Actinovate AG Streptomyces lydicus strain WYEC 108 USA Soil borne diseases like Powdery Mildew, Downy Fruit and vegetable crops
Mildew, Botrytis etc.
Bio-Phospho Bacillus Subtilis India Phosphate solubilization wheat, maize, rice and cotton
Bio Promotor Phosphobacteria Bacillus megaterium India Phosphate solubilization wheat, maize, rice and cotton
Bio Promotor Rhizobium Rhizobium sp. India Nitrogen Fixation Legumes
Azotobacter Bio Fertilizer Azotobacter chroococcum India Nitrogen Fixation Legumes
Paddy Azospirillum Azospirillum India Nitrogen Fixation Paddy crops
Cyanonuticon cyanobacterial strains India carbon status and soil health rice and wheat
NPK Liquid Azotobacter chroocomccum, Pseudomonas India nitrogen fixing, P-solubilizing, k-solubilizing All crops
striata, Bacillus sp.
Potash solubilizing liquid Bacillus species India k-solubilizing Cereals, millets, fibre, vegetables
Azospirillum Inoculant Azospirillum India Nitrogen Fixation Crops, cereals, millets
Quantumr Bacillis subtilis USA
Kodiakr Bacillis subtilis USA Fusarium and Rhizoctonia soil pathogens peanut, soybean, small grain, corn and vegetable
Epicr Bacillis subtilis USA crops
AzoBac Azospirillum CM1404 South Africa Bio remediation, Nitrogen binder,Root stimulator. Maize, Wheat, Sugarcane and grass Pastures
Azospirillum CM1403
Kiwa Microbial Specific Fertilizer For Rice Bacillus China Green planting fast and early tillering. Rice
Nitragin Rhizobium USA Nitrogen Fixation wheat, maize, rice and cotton
Fasloon ka jarasimi teeka Phosphate solubilizing microorganisms (PSM) Pakistan Phosphate solubilization leguminous and non-leguminous crops (wheat, maize,
rice and cotton
Associative Diazotrophs Rhizobium Pakistan Nitrogen Fixation Egyptian clover, alfalfa, lentil
Azolla blue green algae (Azolla Anabaena) Pakistan Nitrogen Fixation wheat, maize, rice and cotton
BioPower Rhizobium Pakistan Nitrogen Fixation Legume, soybean, alfalfa, pea and cowpea, wheat,
maize and rice.

112
Biozote-p Phosphorus solubilizing bacteria Pakistan P-solubilizing biofertilizer legume crops
Biozote-N Rhizobium-N fixing bacteria Pakistan Nitrogen Fixation Major crops
Biozote-MAX Plant growth promoting rhizo-bacteria Pakistan Phytohormones IAA and GA production Major crops
Rice-Biofert Azolla Faisalabad-Pakistan Microbial metabolite Rice
UniGrow PGPR-enriched organic formulation Faisalabad-Pakistan mineral fertilizer that improve soil health Major crops
Rhizogold plus a mix-culture of Rhizobium and ACC deaminase Faisalabad-Pakistan Reduce salinity stress Cereals
containing PGPR
EM-BIOCONTROL Bacillus subtilis strain LS213 Pakistan Increased plant growth and improved yield crops, vegetables and fruits
Bio-Save 10, 11, 100, 110, 1000 TM P. syringae ESC-100 USA Botrytis cinerea, Penicillium spp, Mucor pyroformis, Pome fruit (Biosave 100) and Citrus (Biosave 1000)
Geotrichum candidum
Blight Ban A506 Pseudomonas fluorescens A 506 USA Erwinia amylovora and russet – inducing bacteria Almond, Apple, Apricot, Blue berry, Cherry, Peach,
Pear, Potato, strawberry, Tomato
Cedomon™ Pseudomonas chloroaphis Sweden leaf stripe, net blotch, Fusarium sp, spot blotch, leaf cereals
spot and others
Campanion Bacillus subtilis GB03 USA Rhizoctonia, Pythium, Fusarium and Phytophthora Horticultural crops and turf
Conquer ™ Pseudomonas fluorescens 276 Australia P. tolassii Mushrooms
Victus™ Pseudomonas fluorescens Australia P. tolassii Mushrooms
BioJect Spot − less Pseudomonas aureofaciens USA P. tolassii Dollar spot, Anthracnose and P. Mushrooms Turf and other crops
aphanidermatum
BioJet ™ Pseudomonas sp + Azospirillum USA Brown batch and Dollar spot disease Turf and other crops
Deny Burkholderia cepacia, Pseudomonas cepacia USA Pythium, Fusarium Alfalfa, Barley, Beans, Clover, Cotton, Peas, Sorghum,
Vegetable crops and Wheat
Intercept ™- Pseudomonas cepacia USA Rhizoctonia solani, Fusarium sp., Pythium sp. Maize, Vegetables, Cotton
Kodiak™, Kodiak HB™, Epic™, Concentrate ™, Quantum Bacillus subtilis GB03 USA Rhizoctonia solani, Fusarium spp, Alternaria spp, and Cotton, Legumes
4000 and System 3 ™ Aspergillus spp
Bio Yield Bacillus subtilis and Bacillus amyloliquefaciens USA Broad spectrum action against greenhouse pathogens Tomato, Cucumber, Pepper and Tobacco
Rhizo-Plus Bacillus subtilis strain FZB24 Germany R. solani,Fusarium spp.,Alternaria spp., Sclerotinia and crops, forest tree seedlings, ornamentals, and shrub.
Verticillium
(continued on next page)
Applied Soil Ecology 121 (2017) 102–117
B. Tabassum et al. Applied Soil Ecology 121 (2017) 102–117

that may capture the lead in agricultural industry are Burkholderia,

Cherries, cucurbits, grapes, leafy vegetables, peppers,

Cucurbits, Grapes, Hops, Vegetables, Peanuts, Pome
Pseudomonas and Streptomyces (Bhattacharyya and Jha, 2012). Table 3

Barley, Beans, Cotton, Peanut, Pea, Rice, Soybean

is dedicated to the commercial PGPR formulations, their country of
origin and specific characteristic they execute when applied onto
plants.

Pome fruit, Citrus, Cherries and Potato

Ornamental and vegetable crops Additionally, the prospects of PGPR for disease protection and
oak trees and green house crops
beneficial enhancement of agricultural crops can never be ignored in
potato, tomatoes and walnuts.

Ornamentals and Vegetables

fruits, stone fruits and other

developing countries. China, India, Australia, Russia and the US are the
main players in the global market for biocontrol products. In Pakistan,
various research institutes and plant protection institutes, Pesticide
Quality Control Laboratory (Lahore, Multan), Nuclear Institute for
Agriculture and Biology (NIAB) Pakistan Agriculture and Pesticide
Suitable for

Association (PAPA), Insecticide Resistance Action Committee (IRAC)

Soybean

Cotton

and International Institute of Biocontrol (IIB) have been actively

playing their role in the development, quality control and market
promotion of biocontrol active microbes in the country. It is not pos-
Botrytis cinerea, Penicillium spp., Geotrichum candidum
Pythium spp., Rhizoctonia solani, Fusarium oxysporum

sible to replace the chemical methods of disease control from the

Powdery mildew, early leaf spot, early blight, late
Powdery mildew, Downy mildew, Cercospora leaf

agricultural practices in a short time, and there is a dire need to com-

Fusariumspp., Rhizoctoniaspp. and Pythiumspp.

municate recent advances with farmers through awareness pro-

grammes, effective use of funds, banning of the import of those pesti-
cides that are not sold in the country of their origin and establishment
of a marketing network for the small- and large-scale producers of
Benefit/Target pathogen/disease

molds, mildews, blights, rusts

biocontrol products.
spot, early blight, late blight

Rhizoctonia and Fusarium,

7. Conclusion and future prospects

Seedling pathogen

growth regulator

The present review indicates that PGPR-based formulations not only

help protect plants from several pathogens by acting as biocontrol
agents but also trigger different biological promotion effects in various
blight

plant growth parameters. Most of the PGPR isolates improve plant

growth characteristics, including plant height, seedling vigor, seed
germination, leaf area, fresh and dry weight and tillering capacity, yield
and nutrient contents, in economically important crops such as rice,
peas, soybean, wheat, tomato, and potato. To replace chemical pesti-
Country

cides with the system of a bio pesticide should be more effective and
USA.
USA

USA

USA
USA
USA
USA
USA

USA

economical. Molecular analysis can result in stabilizing the effects of

PGPR in biological control and possible risk assessment before com-
mercialization. Effective utilization of PGPR for disease reduction or
Bacillus subtilis GB03 and chemical pesticide

crop protection in the future will demand a rational choice of organism

Bacillus cereus BPO1 technical, - Bacillus
pseudomonas chlororaphis strain 63-28

as well as technical improvements in upscaling and formulation tech-

niques. Genetic engineering of PGPR may accentuate the expression of
Bacillus pumilus strain QST 2808
Bacillus subtilis strain QWT713

plant growth and health-promoting genomic products. Therefore, a

Bacillus subtilis strain QST713.

single bacterial strain with multiple characteristics will alleviate the

Bacillus subtilis MB1600

pathogen attack and promote plant growth to facilitate the growers. It

Pseudomonas syringae

has become apparent that PGPR strains employ several mechanisms to

cereus strain UW85

promote plant growth, although studies should be focused on the re-

Bacillus pumilus
Composition

lative contribution of each mechanism responsible for effective plant

growth promotion. However, carefully controlled field trials of crop
plants inoculated with PGPR inoculants is mandatory for maximum
commercial exploitation of these strains. In conclusion, the success of
microbial inoculant-producing industries, particularly those using
PGPRs, will depend on measures including advanced business man-
agement, product marketing, extensive education and research.
Moreover, the optimization of PGPR strains for better fermentation and
formulation processes is still required to introduce them in the agri-
GB 34 Concentrate Biological Fungicide

culture industry.

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