Eur J Plant Pathol

https://doi.org/10.1007/s10658-021-02393-7

The use of microbial inoculants for biological control, plant

growth promotion, and sustainable agriculture: A review
Ahmed S. M. Elnahal · Mohamed T. El‑Saadony · Ahmed M. Saad ·
El‑Sayed M. Desoky · Amira M. El‑Tahan · Mostafa M. Rady ·
Synan F. AbuQamar · Khaled A. El‑Tarabily

Accepted: 19 September 2021

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2022

Abstract Microbial control agents serve as alterna- the importance of using microorganisms in the agri-
tives to synthetic pesticides for the management of culture sector for their potential role in fulfilling the
insect pests and plant pathogens. Naturally occurring nutritional requirements of plants, food safety, and
microorganisms such as bacteria, fungi, and proto- sustainable crop production. Microorganisms can
zoa may be beneficial, pathogenic, or neutral to host interact with the crop plants to improve their resist-
plants. This review focuses on the potential role of ance to pathogen attack, plant growth, and develop-
useful microorganisms as biofertilizers or biopesti- ment. Their metabolites have been recognized based
cides in sustaining and enhancing crop production, on their precious excellent plant growth promotion,
and protection. It is necessary to highlight the advan- efficient biocontrol capabilities, successful mass
tages of the beneficial microorganisms to encour- production, appropriate formulation and availability
age farmers to use biological control agents and for commercial application. Bio-complexes, includ-
biofertilizers and reduce the excessive use of toxic ing biofertilizers and biopesticides, promote growth
chemical pesticides and fertilizers. Here, we review and provide protection to plants against various biotic

A. S. M. Elnahal M. M. Rady
Department of Plant Pathology, Faculty of Agriculture, Department of Botany, Faculty of Agriculture, Fayoum
Zagazig University, Zagazig, 44511, Egypt University, Fayoum, 63514, Egypt

M. T. El‑Saadony S. F. AbuQamar (*) · K. A. El‑Tarabily (*)

Department of Agricultural Microbiology, Faculty Department of Biology, College of Science, United Arab
of Agriculture, Zagazig University, Zagazig, 44511, Egypt Emirates University, Al‑Ain, 15551, United Arab Emirates
e-mail: sabuqamar@uaeu.ac.ae
A. M. Saad
K. A. El‑Tarabily
Department of Biochemistry, Faculty of Agriculture,
e-mail: ktarabily@uaeu.ac.ae
Zagazig University, Zagazig, 44511, Egypt

E.-S. M. Desoky
Department of Botany, Faculty of Agriculture, Zagazig
University, Zagazig, 44511, Egypt

A. M. El‑Tahan
Department of Plant Production, Arid Lands Cultivation
Research Institute, The City of Scientific Research
and Technological Applications, SRTA-City, Borg El
Arab, Alexandria, Egypt

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and abiotic stress through the production of plant without causing injury to the plant are called endo-
growth regulators and siderophores, enhancement of phytic bacteria, which form ecologically important
nutrient uptake, increasing yield, and production of relationships with the host plant (Alblooshi et al.,
antagonistic compounds such as antibiotics, hydro- 2022; Beattie, 2007; Fanning et al., 2018; Lefort
lytic enzymes, hydrogen cyanide, and volatile organic et al., 2016; Ramakuwela et al., 2020).
compounds. This review sheds the light on the poten- Indeed, a diversity of biochemical signals are trans-
tial of employing microbial agents in agriculture as mitted between microorganisms and their host plants.
biofertilizers, biopesticides, nano-biofertilizers and For example, various plant-associated microorgan-
nano-biopesticides to enhance plant productivity and isms have the ability to promote growth of and/or
sustainable agriculture. control diseases in different plant species (Al Hamad
et al., 2021; Beattie, 2007; Mantzoukas et al., 2020;
Keywords Biological control · Microbial Nihorimbere et al., 2011; Saeed et al., 2017). Bacteria
inoculants · Plant growth-promoting rhizobacteria · residing the rhizosphere and exhibiting plant growth-
Sustainable agriculture promoting activities are designated as plant growth-
promoting rhizobacteria (PGPR). In fact, some PGPR
products have been used for agricultural applications
Introduction because of their growth-enhancing actions and biocon-
trol capabilities. Plants have been demonstrated to ben-
Plants are rich hosts for microbial growth. Various plant efit from their interactions with PGPR (Fig. 1), which
surfaces and tissues, especially those rich in moisture can improve plant health and growth, suppress dis-
and nutrients, are suitable environments for the prolif- ease-causing microorganisms, enhance nutrient avail-
eration of microorganisms (Andrews & Harris, 2000; ability, and accelerate nutrient assimilation. However,
Beattie, 2007; Fanning et al., 2018; Mantzoukas, 2010). the strict regulations and requirements placed upon
Microorganisms can be beneficial, pathogenic, or neu- pesticides may prevent some PGPR products that act
tral to the host plant depending on their type and behav- as biocontrol agents from being registered as biopesti-
ior. This review focuses on beneficial microorganisms cides (Harman et al., 2010). Instead, these PGPR prod-
that can be used as biofertilizers or biopesticides. ucts are often commercialized as plant inoculants.
The diverse structures and components of plants In general, microorganisms related to plants
can provide a suitable medium for the development include prokaryotes and eukaryotes. The bacterial
of microorganisms. Microorganisms can inhabit domain is the most dominant component among
several zones within and around plants: the sper- microflora; bacteria can achieve a density of approx-
mosphere (the area of soil that surrounds a germi- imately ­109 cells per gram of plant root tissue. The
nating seed, which contains nutrients that enhance eukaryotic domain, which includes filamentous fungi,
microbial growth), the phyllosphere, (the zone that yeasts, algae, protozoa, and nematodes, is present at
includes the above-ground plant parts and fluctuates lower densities (e.g. 1­ 05–106 for fungi, 1­ 03 for algae,
according to external factors such as rain, tempera- and ­102–103 for protozoan cells per gram of root tis-
ture, and radiation), and the rhizosphere, (the region sue) (Beattie, 2007; Vega, 2018). In additionally,
that consists of plant roots and the surrounding soil viruses and bacteriophages have been reported at a
or substrate). Within the rhizosphere, intense interac- density of ­108–109 cells per gram of soil (Ashelford
tions may occur among plants, soil, and microfauna et al., 2003; Lefort et al., 2016).
owing to the high carbon content and energy in this Three different categories have been established to
zone. Plant roots secrete organic compounds derived determine the interactions between beneficial microor-
from photosynthesis and other plant processes into ganisms and plants. The first is comprisesd of micro-
the rhizosphere (Pinton et al., 2007). Microorganisms organisms responsible for plant nutrition that interact
can also colonize other zones such as endophytic sites directly or indirectly with the plant, such as nitrogen
and vascular tissues. These vascular tissues (xylem N-fixing bacteria. The second category is the bio-
and phloem) constitute rich environments for bacte- control agents, which includes microorganisms that
rial growth. Bacteria that can colonize plant tissues indirectly stimulate plant growth by preventing the

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Fig. 1  Mechanisms of plant growth-promoting rhizobacteria (PGPR) during the plant-microbe interaction. ACC​ 1-aminocyclopro-
pane-1-carboxylic acid, HCN hydrogen cyanide, ISR induced systemic resistance

growth of plant pathogens. The third category is those increasing iron uptake, and/or producing volatile
microorganisms that act directly on plant growth by substances (Fanning et al., 2018; Nihorimbere et al.,
producing plant hormones, solubilizing phosphates, 2011; Podile et al., 2007). Many plant-associated

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microorganisms provide enormous benefits to the eco- controlling plant pathogens (Jaber & Enkerli, 2016;
system and agricultural production by providing sus- Vessey, 2003). Alternatively, chemical-based agricul-
tainable and clean alternatives compared to chemical tural fertilizers stimulate plant growth by providing
fertilizers/pesticides (Al Raish et al., 2021; Beattie, essential nutrients such as nitrogen, phosphorous, and
2007; Gathage et al., 2016). potassium.
The nature of pesticides can also vary, but most
importantly is that naturally- derived pesticides
The use of microbial inoculants as biopesticides pose no risk to human health and environment. In
and biofertilizers contrast, numerous negative impacts are associated
with chemical-based pesticides (EPA, 2001). Biope-
In response to the global issue of misuse and overuse sticides include naturally- occurring substances,
of pesticides and chemical fertilizers, biofertilizers microorganisms, and pesticide compounds produced
and microbial inoculants have gained particular rel- by plants. Microorganisms that are widely used and
evance in agricultural industries. Biopesticides and available in the market are fungi, algae, and bacteria.
biofertilizers have great potential for the application in Such biocontrol agents are applied to protect agricul-
organic and conventional farming practices (Gardener tural products from insects, ;;;pathogens, and weeds
& Fravel, 2002; Jaber & Enkerli, 2016; Rady et al., (Butt & Copping, 2000; Lefort et al., 2016; Russo
2019; Ramakuwela et al., 2020). According to Berg et al., 2019a, 2019b). The control of plant patho-
(2009), the market for microbial inoculants is grow- gens by microorganisms involves the suppression of
ing worldwide at an annual rate of approximately pathogens to favor plants, for which this approach has
10%. Compared to chemical pesticides and fertilizers, gained popularity as an alternative to chemical pes-
microbial inoculants are considered much safer (Berg, ticides and fungicides, especially in organic farms
2009). The two main factors determining the useful- (Fravel, 2005; Klieber & Reineke, 2016). Bacterial
ness of microbial inoculants for agricultural purposes biocontrol agents can stimulate resistance in plants
are their ability to stimulate growth as well as to sup- by activating host defense mechanisms. This phe-
press diseases on plants (Kamil et al., 2018). Table 1 nomenon can occur without direct contact between
summarizes selected studies that investigated biope- the pathogen and the biocontrol agent. For instance,
sticides and biofertilizers, and describes their benefi- when a biocontrol agent is applied to plant roots, it
cial effects on plant growth and resistance to various induces systemic resistance, resulting in suppressing
pathogens. disease throughout the plant (Dash et al., 2018; Gnan-
The efficiency of microbial inoculants in stimulat- amanickam, 2002).
ing plant growth and suppressing diseases plays a key Factors such as the increasing costs of soil fumi-
role in agriculture. Farmers rely on the proper selec- gation, concerns about exposure to fungicides, and
tion of fertilizers and pesticides to improve yield and the development of pathogen resistance to fungicides
control pests. Farmers can select products according have contributed to the need to reduce dependence
to the materials they are derived from, i.e. nature- on chemicals. As a result, ecologically-based pest
based materials such as animals, plants, bacteria, min- management practices such as biocontrol have been
erals, or chemical-based products. Nature-based prod- adopted. In addition, the environmental conscious and
ucts, such as PGPR, have shown promising results as sustainable shift in agricultural and agri-food sectors
biofertilizers and biopesticides, indicating that they have led to the development of organic farming (Dash
can be implemented in sustainable agricultural prac- et al., 2018; Fravel, 2005; Rigby & Cáceres, 2001).
tices. Accordingly, bioproducts sold to improve plant In fact, organic farming systems prohibit synthetic
performance are referred to by various terms, includ- chemicals in crop production and thus rely on bio-
ing inoculants, plant-strengthening agents, biofer- control for pest management. The United States (US)
tilizers, and plant growth-promoting microorgan- Department of Agriculture estimates that organic
isms (Harman et al., 2010). The term “biofertilizer” farming has been one of the fastest-growing segments
describes soil microorganisms that increase the avail- in the past decade, with a 15% increase in the num-
ability and uptake of mineral nutrients into plants. ber of organic farmers. In Ohio, the total area under
Such biofertilizers may also stimulate plant growth by organic agricultural farming increased from 37,710

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Table 1  Some of the selected studies investigating the effects of biocontrol agents on plant growth and resistance to pathogens
Biocontrol agent Pathogen Host plant Reference

Pseudomonas syringae Penicillium italicum citrus Smilanick et al. (1996)

Rhodotorula glutinis Penicillium expansum Pear Sugar & Spotts (1999)
Candida saitoana Penicillium digitatum, Botrytis Pome and citrus Droby et al. (2009)
cinerea
Bacillus spp. Rhizocotonia solani Wheat Ryder et al. (1998)
Candida oleophila B. cinerea Apple Mercier & Wilson (1995)
R. glutinis, Cryptococcus P. expansum, Alternaria alter- Cherry Qin et al. (2003)
laurentii nata
Candida famata P. digitatum Citrus Arras et al. (1996)
Flavobacterium Phytophthora cactorum Apple Alexander & Stewart (2001)
Trichoderma harzianum, Tricho- Phytophthora cactorum Apple Alexander & Stewart (2001)
derma koningii
Bacillus subtilis B106 Pseudocercospora musae Banana Fu et al. (2010)
B. subtilis Plasmodiophora brassica Chinese cabbage Peng et al. (2011)
Gliocladium catenulatum P. brassica Chinese cabbage Peng et al. (2011)
Alcaligenes sp. EIL-2 Phytophthora meadii Hevea brasiliensis RRII 105 Abraham et al. (2013)
Alcaligenes sp. EIL-2 P. meadii Hevea brasiliensis RRIM 600 Abraham et al. (2013)
Bacillus amyloliquefaciens P. digitatum Mandarin fruit Hao et al. (2011)
HF-01
B. subtilis R33, B. subtilis R13 Phytophthora capsici Pepper Lee et al. (2008)
Serratia plymuthica 5–6 Fusarium sambucinum Potato Gould et al. (2008)
Aspergillius versicolor lm6–50 Spongospora subterranea Potato Nakayama & Sayama (2013)
Aspergillius versicolor S. subterranea Potato Nakayama & Sayama (2013)
lm6–50 + fluazinam
Trichoderma atroviridae LU132 B. cinerea LU829 Strawberry cv. Yolo Card et al. (2009)
T. atroviridae LU132 + fenhexa- B. cinerea LU829 Strawberry cv. Pajero Card et al. (2009)
mide
Phage PhiRSL1 Ralstonia solanacearum Tomato Fujiwara et al. (2011)
B. subtilis Peronophythora sp. Lychee Jiang et al. (2001)
Trichoderma spp. B. cinerea, Colletotrichum Strawberry Freeman et al. (1998)
acutatum
Cryptococcus laurenti, C. P. expansum Apple Vero et al. (2002, 2009)
candida
Heat-tolerant yeast P. expansum, Monilinia fruc- Apple Leverentz et al. (2003)
ticola
Cryptococcus infirmo-miniatus Rhizopus stolonifer Cherry Spotts et al. (1998)
Pantoea agglomerans P. digitatum Citrus Plaza et al. (2004)
P. agglomerans Monilinia laxa, R. stolonifer Nectarine Bonaterra et al. (2003)
P. agglomerans P. expansum, B. cinerea, R. Pear Poppe et al. (2003)
stolonifer
Muscodor albus Colletotrichum sp., P. digitatum Apple and peach Mercier & Jimenez (2004)
B. subtilis P. italicum, P. digitatum Citrus Obagwu & Korsten (2003)
Lactobacillus plantarum L292 Xanthomonas campestris, Plant surfaces and plant-associ- Visser et al. (1986)
Erwinia carotovora, Pseu- ated products
domonas syringae
Enterococcus mundtii MC6, L. X. campestris, E. carotovora, M. Fresh fruits and vegetables Trias et al. (2008)
plantarum TC110, Leuconos- laxa B. cinerea
toc, Mesenteroides XM360

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Table 1  (continued)
Biocontrol agent Pathogen Host plant Reference

Lactobacillus spp. KLF01 Ralstonia solanacearum, Xan- Rhizosphere of tomato Shrestha et al. (2014)
thomonas axonopodis pv. citri
L. plantarum IMAU10014 B. cinerea, Alternaria solani, Fermented milk (koumiss) Wang et al. (2011)
Phytophthora drechsleri,
Fusarium oxysporum, Glom-
erella cingulata
Weissella confuse, Lactococ- Pseudomonas savastanoi Rhizosphere of olive trees and Fhoula et al. (2013)
cus lactis, L. plantarum, desert truffle
Lactococcus mesenteroides
Enterococcus durans, Entero-
coccus faecium
Enterococcus spp. B. cinerea, Verticillium dahliae Rhizosphere of olive trees and Fhoula et al. (2013)
desert truffle
L. plantarum TC92 PM411 Erwinia amylovora, P. syringae Pear and tomato Roselló et al. (2013, 2017)
L. plantarum SLG17 Fusarium culmorum, Fusarium Silage Baffoni et al. (2015)
graminearum
Streptomyces sp. PGPA 39 Sclerotinia sclerotiorum Chickpea Sathya et al. (2017)
B. amyloliquefaciens FZB42 F. graminearum Wheat Gu et al. (2017)
Trichoderma harzianum M-10 R. solani Tomato Manganiello et al. (2018)
Entoleuca sp. Rosellinia necatrix Prill Avocado Ghorbanpour et al. (2018)
Rhizophagus irregularis MUCL Phytophthora infestans Potato Alaux et al. (2018)
41833
Trichoderma virens JSB100 F. oxysporum f. sp. lycopersici Tomato Jogaiah et al. (2018)
Sphingomonas spp., Pantoea P. syringae pv. tabaci Tobacco Qin et al. (2019)
spp.
B. subtilis Cryphonectria parasitica Chestnut Murolo et al. (2019)
Sarocladium strictum C113L, F. graminearum Wheat Rojas et al. (2020)
Anthracocystis floculossa
P1P1 and F63P, Penicillium
olsonii ML37
Bacillus sp., Pseudomonas sp. F. solani and F. kuroshium Three Lauraceae spp. Báez-Vallejo et al. (2020)
P. syringae and Pseudomonas R. solanacearum Tomato Mohammed et al. (2020)
fluorescens
Trichoderma sp.SANA20 B. cinerea Cucumber Aoki et al. (2020)
B. subtilis MK-252 F. oxysporum f. sp. cepae Onion Bektas & Kusek (2021)
T. harzianum, T. gamsii Fusarium proliferatum, F. Garlic Mondani et al. (2021)
oxysporum
Aureobasidium pullulans P. cactorum B. cinerea Strawberry Iqbal et al. (2021)
Induratia coffeana CML 4009 Colletotrichum lindemuthianum Common bean Mota et al. (2021)
T. harzianum R. solanacearum Tomato Yan & Khan (2021)
Trichoderma longibrachiatum Magnaporthiopsis maydis Maize Degani & Dor (2021)
and Trichoderma asperel-
loides

to 52,949 acres between 2006 and 2008 (USDA, Diversity of microorganisms used as inoculants
2009). The growing need for eco-friendly practices
in sustainable agriculture has resulted in significant Although many plant-microbe interactions have been
increases in the use of microbial biocontrol agents described, agricultural biotechnology research has
over the past 40 years (Fravel, 2005). focused on developing of commercial products that

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serve as biofertilizers and biopesticides. A microbial producing plant hormones and other compounds to
inoculant is a formulation of one or more beneficial stimulate plant growth. This group has also shown
bacterial strains within a carrier (Bashan, 1998). The potential as biocontrol agents for root rot and damp-
desired effects of inoculants may include biocontrol ing-off diseases caused by Pythium sp. (Antoun &
of pathogens, N fixation, enhancement of mineral Prévost, 2005; Jaber & Enkerli, 2016). PGPR inocu-
uptake, weathering of soil minerals, and nutritional or lants have several mechanisms of action and they can
hormonal effects. also induce systemic resistance.
The promotion of plant growth by beneficial micro- PGPR such as Azospirillum brasilense, Agrobac-
organisms, especially bacteria, can be traced back terium spp., Bradyrihizobium spp., Enterobacter
for centuries. The first patented microbial product spp., and Rhizobium legominosarum can produce
was registered nearly 100 years ago and used Rhizo- indole-3-acetic acid (IAA), an auxin that promotes
bium sp. as an active ingredient. In addition, inocula- plant growth. Other mechanisms include synergistic
tion with non-symbiotic rhizosphere bacteria such as relationships and stimulation of root growth and bio-
Azotobacter began in the 1930s and 1940s and was control (Al-Anazi et al., 2015; Gathage et al., 2016;
revived in the late 1970s (Antoun & Prévost, 2005). Vessey, 2003). Bacterial genera such as Bacillus,
The use of microorganisms in disease control was Azospirillum, and Pseudomonas can enhance legume
developed later; the first product to be used as a bio- symbioses (Podile & Kishore, 2007). In many cases,
control agent was registered by the US Environmen- various mechanisms are involved in the synergis-
tal Protection Agency (EPA) in 1979 (Fravel, 2005). tic interactions between plants and microorganisms
According to the most updated EPA list, a total of 35 (Nihorimbere et al., 2011; Ramakuwela et al., 2020).
bacterial strains, most of which belong to the genus Thus, identifying the mechanisms responsible for
Bacillus, have been registered as biopesticides and plant growth is a major challenge due to the diversity
are coomercially sold (EPA, 2001). Several PGPR and difficulty in measuring plant growth under differ-
genera and other microorganisms have been used in ent biotic or abiotic conditions (Lefort et al., 2016;
commercial products after showing a potential as Podile & Kishore, 2007).
biofertilizers or biocontrol agents; and the first com- In general, PGPR are comprised of a group of
mercial formulations appeared in 1990 (Bashan, genera including Azospirillum, Azotobacter, Bacil-
1998; Lefort et al., 2016). Other genera include Pseu- lus, Burkholderia, Enterobacter, Klebsiella, and
domonas, Agrobacterium, Streptomyces, Burkholde- Pseudomonas as well as endophytes such as Axo-
ria, and Paecilomyces. The fact that relatively few arcus spp., Gluconacetobacter diazotrophicus, and
bacterial species are marketed as microbial pesticides Herbaspirillum seropedicae (Jan et al., 2015). Azos-
despite the growing body of research on microorgan- pirillum spp., which are isolated from grasses and
isms suppressing pathogen growth, can be attributed cereals, as well as Azoarcus spp., Burkholderia spp.,
to the lack of comprehensive testing protocols and Gluconacetobacter diazotrophicus, Herbaspiril-
information about their EPA registry. lum spp., Azotobacter, and Paenibacillus polymyxa,
PGPR, which are nonpathogenic microorganisms can fix atmospheric N. Bacillus spp. have also been
present in the rhizosphere, possess abilities to enhance reported to promote plant growth and control micro-
plant development. PGPR inoculants promote plant bial diseases in a wide range of plants because of their
growth by improving mineral and water absorption, capacity to inhibit volatile substances (Vessey, 2003).
producing plant growth-stimulating compounds, and Moreover, the beneficial effects of Pseudomonas spp.
suppressing growth of pathogens (de Weert & Bloem- on plant yield and biocontrol of some plant diseases
berg, 2007; Jaber & Enkerli, 2016). Rhizobium spp. have been reported. For example, Pseudomonas spp.
are known for their agricultural benefits. These Gram- is an effective bioagent for controlling Fusarium wilt,
negative bacteria can establish symbiotic relationships a common soil-borne fungal disease.
with leguminous plants, allowing them to fix N. As According to Lucy et al. (2004), Azospirillum spp. are
such, Rhizobium spp. have been used as inoculants best characterized free-living PGPR, that have become
for biofertilization purposes (Mantzoukas & Gram- extremely important in the fields of agriculture and eco-
matikopoulos, 2020; Sessitsch et al., 2002). Moreover, logical sciences (Bashan, 1998; Gathage et al., 2016;
rhizobia are known as “microbial symbiotic partners”, Someya et al., 2011). Production of phyto hormones

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(e.g. IAA), fixation of atmospheric N, and reduction of disease resistance (Dash et al., 2018; Mobarak, 2008).
nitrates are among the mechanisms by which Azospiril- Dry green algae contain high levels of macro- and
lum spp. promote plant growth. Moreover, greenhouse micro-nutrients in addition to amino acids. A prelimi-
and field experiments have revealed improved mineral nary study reported improved growth of lettuce plant
absorption and increases in root elongation in Azospiril- seedlings after inoculation with green microalgae,
lum-inoculated plants (Someya et al., 2011; Vega, 2018). resulting in higher fresh weight than that in control
Interestingly, the genus Azospirillum also can be associ- plants (Faheed & Abd-El Fattah, 2008; Klieber &
ated with Pseudomonas to rapidly colonize plant roots, Reineke, 2016). Macroalgae, such as kelps, have also
providing evidence that these genera can work together been used as biofertilizers as well as biocontrol agent.
as bacterial inoculants to promote plant growth (Someya For example, the application of Ecklonia maxima as
et al., 2011). a soil drench for tomatoes stimulated plant growth
and reduced nematode infestation. Compared with the
uninoculated control, plants inoculated with E. max-
Opportunities for new microbial inoculants ima had higher fresh weight (Crouch & Van Staden,
1993; Dash et al., 2018; Gathage et al., 2016). Hence,
Despite the vast diversity of PGPR, the dominant microorganisms can offer different types of inoculants
bacteria in this group belong to the genera Pseu- depending on their activities. Additional research is,
domonas and Bacillus. Research on these bacteria however, required to investigate the efficacy of dif-
has led to a better understanding of the mechanisms ferent microorganisms as potential biofertilizers and
involved in promoting plant growth and biocontrol. biocontrol agents.
However, other PGPR genera that have been shown to Nanotechnology is the study of science, engineer-
effectively prevent soil-borne pathogens in crops have ing, and technology at the nanoscale (approximately
not been studied in depth (e.g. Mitsuaria and Burk- 1–100 nm) (Abd El‐Hack et al., 2021; El-Saadony
holderia) (Baysal et al., 2008; Gathage et al., 2016). et al., 2021a; Reda et al., 2020). Converting the origi-
Some studies have demonstrated that Burkholderia nal materials into a nano-form imparts many valu-
works as a biocontrol agent in tomatoes by producing able qualities, which are observed in increasing their
siderophores; in addition to evidences of N fixation bio availability (El-Saadony et al., 2020; Reda et al.,
have been found. Therefore, it is essential to identify 2021).
the mechanisms involved in their activity and their Nano-technology is a versatile tool to exploit the
interactions with other biocontrol agents (Caballero- great potential of PGPRs to facilitate its reproducible
Mellado et al., 2007; Jaber & Enkerli, 2016; Russo implementation in the field and sustain agricultural
et al., 2019a, 2019b). One group within this genus, productivity worldwide (El-Saadony et al., 2021b,
Burkholderia cepacia complex (Bcc), has been used 2021c; Timmusk et al., 2018; Vejan et al., 2016).
in biocontrol and bioremediation to degrade xenobi- Nano-biofertilizers have dual benefits of nano-nutri-
otic pollutants (Jaber & Enkerli, 2016; O’Sullivan & ent and bio inoculant applications, including various
Mahenthiralingam, 2005; Parke, 2000). However, Bcc beneficial microbes, for augmenting nutrient use effi-
can cause serious infections in humans, particularly ciency and sustainable crop productivity associated
in patients with cystic fibrosis (Harman et al., 2010). with safer environment (Boddupalli et al., 2017; Kalia
This demonstrates the importance of investigating & Kaur, 2019). These nano-biofertilizer can ensure
the versatility of bacteria, specifically Burkholderia targeted- and timed- delivery of nutrients to the crop
spp., to avoid using potential human pathogens when besides increasing the benefits of the bio-fertilizer
developing biocontrol agents (Gathage et al., 2016; components of the formulation (Gouda et al., 2018).
Parke & Gurian-Sherman, 2001). However, the efficient implementation and develop-
Nonbacterial microorganisms have also proven ment of such formulations are hindered because of
their potential as biofertilizers and biocontrol agents. the scarcity of the basic understanding of various
Marine algae (e.g. seaweed) are a rich source of bio- interactions and exchanges among nano-particles
active compounds used as biofertilizers to improve (NPs), rhizospheric microflora and plant systems
seed germination, increase yields, and enhance (Boddupalli et al., 2017; Razzaghifard et al., 2017).

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The direct nano-material–microbe cell interactions Mechanisms of microbial biocontrol agents

are also quite complex. They may elicit some unique against plant pathogens
variability in the cell physiology and level gene
expression of microorganisms, leading to either pro- The term “biocontrol” refers to the intentional use of
liferation (Pallavi et al. 2016) or reduction of micro- introduced or resident microorganisms to suppress
bial diversity of specific groups of soil microbiota one or more plant pathogens (Heydari & Pessarakli,
(Simonin et al., 2016). Consequently, nanomateri- 2010). PGPR are common biocontrol agents that sup-
als should be sequestered in nano-vehicles to reduce press plant pathogens by producing various types of
their mobility and toxicity to soil-beneficial microbes. inhibitors, increasing the natural resistance of the host
Similarly, these negative impacts on soil microorgan- plant, or displacing and out-competing pathogens
isms may be reduced by adding nano-primed benefi- (Gheorghe et al., 2008). PGPR can rapidly colonize
cial PGPRs in the tested plants instead of the direct the rhizosphere, competing with harmful microor-
use of nano-materials (Nasr, 2019; Timmusk et al., ganisms and soil-borne pathogens on the root surface
2018). (Stockwell et al., 2002). PGPR that co-grow with a
Several studies considering the effect of NPs plant host can stimulate its growth through direct and
on the plant–microbe system suggests two possi- indirect mechanisms (Fig. 2). Direct mechanisms
ble mechanisms for promoting plant growth; direct include the production of plant hormones, solubiliza-
mode by improving nutrient bio-availability and an tion of phosphates, and increased uptake of iron. Indi-
indirect mode by initiating a stimulating effect on rect effects include antibiotics production, nutritional
PGPRs before seed inoculation. In summary, the competition, parasitism, pathogen toxin inhibition,
nano-biofertilizers can: (1) increase the nutrient use and induced resistance (Klieber & Reineke, 2016;
efficiency through reduced application rates, enhanc- Vessey, 2003).
ing bioavailability and reducing environmental The main biocontrol mechanism of bacterial
losses; and (2) improve the plant-growth-promoting antagonists is antibiosis. Antibiosis involves the pro-
(PGP) conditions and properties such as bioinocu- duction of volatile and nonvolatile compounds, which
lant protection from desiccation, better cell viability, act as antibiotics or antifungal agents (Rao et al.,
reduction of cell sedimentation percent in the formu- 2016). Antibiotics are toxins produced by micro-
lation, increase shelf life and enhance the synthesis of organisms that can poison or kill other microorgan-
PGP substances/secondary metabolites (Duhan et al., isms at a low concentration. Antagonistic bacteria
2017; Rangaraj et al., 2014; Sadeghi et al., 2017; may also produce other metabolites that interpose the
Timmusk et al., 2018; Vejan et al., 2016). Therefore, pathogen’s growth and activities (Ghorai et al., 2021).
several studies on various plants have been under- Among these metabolites are lytic enzymes, which
taken to identify the likely role of increased nano- break down polymeric compounds such as chitin,
biofertilizer-based formulations in achieving the protein, DNA, hemicelluloses, and cellulose (Hey-
objective of sustainable crop production as shown in dari & Pessarakli, 2010; Rao et al., 2016); volatile
Table 2. Furthermore, decoding the probable interac- compounds such as hydrogen cyanide; and antifungal
tions occurring among the NPs, beneficial microbes metabolites (a class of cyclic lipo-peptides). The sec-
and plant systems and optimizing these mutual inter- ondary metabolites of different bacterial species and
actions for further regulation of the delivery and their role in plant growth and stress management are
release of formulations at the desired site and time shown in Table 3.
will improve efficient use of nano-biofertilizers and Beyond bacterial volatiles, most volatiles have
can be considered a step closer to the Green Revolu- shown a positive effect on plant health. Such vola-
tion (Kalia & Kaur, 2019; Sadeghi et al., 2017; Tim- tiles are diverse in their chemical structures, with a
musk et al., 2018; Vejan et al., 2016). range from small aliphatic (e.g., dimethyl disulfide
(DMDS), produced by a myriad of bacteria) or aro-
matic molecules (e.g., indole, produced by Escheri-
chia coli), to large ketones, alkenes, or alkanes (e.g.,
the 1-undecene, produced by certain species of Pseu-
domonas). Terpenes (e.g., geosmin, produced by

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Table 2  Application of nano-biofertilizer-based formulations in agriculture. NPs nano-particles, PGPRs plant growth promoting rhizobacteria, IAA indole-3-acetic acid, EPS
exopolysaccharide
Nano-biofertilizer Impact / mode of action References

ZnO-NPs + PGPRs Enhances siderophore production Haris & Ahmad (2017)

CuNPs + Pseudomonas sp. Enhances the IAA production levels Dimkpa et al. (2012)
(Biozar + Zn, Fe, Mn-(NPs) Enhances the performance of wheat crop in terms of Mardalipour et al. (2014)
growth and yield
ZnO-NPs, ­Fe2O3-NPs, CuO-NPs and ­TiO2-NPs + suitable Boosts the plant growth promoting action of the bioferti- Anderson et al., 2017; Babaei et al., 2017; Ghooshchi,
bio-fertilizers lizers, improves plant photosynthetic ability, enhances 2017; Kheirizadeh Arough et al., 2016; Timmusk et al.,
antioxidant enzyme activities, plant growth, and yield 2018
components
SiO2- NPs and nano-Agand calcium phosphate (CaP)- Increases seed germination, root proliferation, growth Karunakaran et al., 2013; Khan & Bano, 2016; Rane et al.,
NPs + different PGPRs promotion, improves propagation of beneficial 2015; Rangaraj et al., 2014
microbes, bio control activity, soil nutrient contents,
phytohormones production and the bioavailability of
essential nutrients e.g. Mg, K, Na, etc
ZnO-NPs, ­Fe2O3-NPs, Mo-NPs and K-NPs + various Improves yield parameters, quality, nodule weight, and Farnia & Ghorbani, 2014; Ghalamboran, 2011; Jacobson
bio-fertilizers number, pod production, nitrogen fixation, symbiotic et al., 2018; Khati et al., 2018; Kumar et al., 2015; Morsy
systems, antioxidant activities, germination, plant et al., 2017; Shcherbakova et al., 2017; Taran et al., 2014
growth, and overall physiological state
CuNPs, ZnO-NPs, ­Fe2O3-NPs and CuO-NPs + Rhizobium Increases the production of EPS and stimulates the IAA Oves et al. (2014)
sp. production upon CuO-NPs exposure
ZnO-NPs + algea (Chaetomorpha antennina & Sargas- Improves seed germination, shows antibacterial activity Roy & Anantharaman (2017; 2018)
sum ilicifolium)
Eur J Plant Pathol
Eur J Plant Pathol

Fig. 2  Indirect mechanisms used by plant growth-promoting rhizobacteria (PGPR) as biocontrol agents for pest/diseasemanage-
ment. HCN hydrogen cyanide

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 Table 3  Microbial secondary metabolites produced by different bacterial species and their role in plant growth and stress management. ISR induced systemic resistance, ROS
reactive oxygen species, IAA indole-3-acetic acid, EPS, exopolysaccharide, HCN hydrogen cyanide, ACC​1-aminocyclopropane-1-carboxylic acid, IBA indole-3-butyric acid
Bacterial species Metabolites Biotic or abiotic stress Mechanism of action References

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Secondary metabolites of Pseudomona spp.
P. putida GAP-P45 Exopolysaccharides Drought tolerance in sunflower Biofilm formation, better soil Sandhya et al. (2009)
aggregation and water content
P. putida NH-50 Pyoleuteorin Colletotrichum falcatum, the ISR Hassan et al. (2011)
causal agent of red rot on
sugarcane
P. putida AKMP7 Catalase Heat stress in wheat Scavenges ROS Shaik et al. (2011)
P. fluorescens Gibberellic acid Raddish grown under saline Increases fresh weight of shoots Mohamed & Gomaa (2012)
conditions and roots
Proline Salinity stress on faba bean Decreases the ROS level Metwali et al. (2015)
P. flurescens Mk25 Auxin Salinity stress on mung bean Enhances root growth Ahmad et al. (2013)
P. fluorescens strain CHA0, 2,4-Diacetyl fluroglucinol, Root rot and damping off in ISR, Biofilm formation Weller, (2007)
2–79 and 30–84 HCN, pyoveridine, pyoleute- cucumber, tomato and tobacco;
orin, salicylate, pyrrolnitrin and Gaeumannomyces graminis
phenazine-1-carboxylic acid var. tritici, the causal agent of
and anthranilic acid take all disease on wheat
P. aeruginosa PF23 EPS Drought stress in sunflower; and Activates antioxidant machinery, Sandhya et al. (2009); Tewari &
charcoal rot of sunflower caused antifungal activity Arora (2014a, 2014b)
by Macrophomina phaseolina
P. aeruginosa PM389, ZNP1 Cytokinin, IAA and EPS Osmotic stress on Arabidopsis Ameliorates the osmotic stress Ghosh et al. (2019)
thaliana
P. chlororaphis PA23 Pyrrolnitrin Sclerotinia sclerotiorum stem rot Shows antifungal action Nandi et al. (2015)
of canola
Pyrrolnitrin and HCN The nematode Caenorhabditis Lessens egg laying rates due to
elegans lethal paralysis (repellant)
P. stutzeri MBE05 Ascorbate peroxidise Saline conditions in peanut Reduces ROS levels Sharma et al. (2016)
Secondary metabolites of Bacillus spp.
Bacillus sp. SC2b IAA, ACC deaminase, and Metal toxicity in Sedum plumbi- Enhances accumulation of Zn and Ma et al. (2015)
siderophores zincicola Cd in roots and leaves
Bacillus sp. Nitrogenase Low nitrogen stress on maize Increases nitogen supply and Kuan et al. (2016)
fixation
Bacillus sp. PZ-1 Hydroxamate-type siderophore High Pb contaminated soils in Shows phytoremediation poten- Yu et al. (2017)
Brassica juncea tial by improving Pb assimila-
tion
B. subtilis CAS15 Trilactone siderophore 2,3-dihy- Pepper wilt caused by Fusarium Shows ISR and reduces chla- Yu et al. (2011)
droxybenzoate-glycinethreonine oxysporum f.sp. capsici mydospore germination
Eur J Plant Pathol

(DHB-Gly-Thr)3
 Table 3  (continued)
Bacterial species Metabolites Biotic or abiotic stress Mechanism of action References

B. subtilis FZB24 and GB03 Surfactin Fusarium wilt caused by F. Shows ISR, antifungal action Kong et al. (2010)
oxysporum; potato black scurf through cytoplasmic membrane
Eur J Plant Pathol

caused by Rhizoctonia solani; disruption

root rot and damping off Fusar-
ium sp., Pythium, Phytophthora
sp., Rhizoctonia sp. of Brassica
family
B. subtilis V26 Chitosanase Botrytis cinerea, causal agent of Shows antifungal action Kilani-Feki et al. (2016)
tomato fruit rot
B. megaterium Bm4C Siderophores and auxin produc- Ni toxicity in soil cultivated with Enhances minerals uptake and Mani & Helena (2008)
tion Indian mustard Fe, increases dry weight and
shoot length
B. amyloliquefaciens FZB42 Fengimycin, bacillomycin (lipo- Fusarium wilt caused by F. Shows ISR, and causes deforma- Chowdhury et al. (2015); Gu et al.
peptide) oxysporum tion of conidia and the hyphal (2017)
cytoplasmic membrane
B. amyloliquefaciens SYBC Fengycin, bacillomycin L and Gummosis in peach caused by Inhibits germination of conidi- Li et al. (2016)
H47 surfactin (lipopeptides) Botryosphaeria dothidea ospores
B. drentensis P16 EPS Saline stress in mung bean Promotes biofilm formation and Mahmood et al. (2016)
maintains nutrient and water
availability to plants
B. tequilensis J12, B. endophyti- IAA, cytokinin, and EPS Osmotic stress in A. thaliana Ameliorates osmotic stress Ghosh et al. (2019)
cus J13
Secondary metabolites of Azos-
pirillum spp.
Azospirillum sp. IBA/IAA Nutrient deficiency of C, N and P Promotes plant growth and root Malhotra & Srivastava (2009)
development
Exopolysaccharide Rrice blast caused by Pyricularia Promotes ISR Sankari et al. (2011)
oryzae
IAA Drought stress in canola Increases shoot length and weight Fukami et al. (2018)
A. brasilense Phenylacetic acid P. syringae pv. tomato, the causal Shows antibacterial activity Bashan & DeBashan (2002); Som-
agent of bacterial speck disease; ers et al. (2005)
crown gall caused by Agrobac-
erium tumefaciens; and Leaf
blight of mulberry
Gibberellic acid Dormancy of soybean and wheat Decreases hydrolytic enzymes, Mehnaz (2015)
such as protease and amylases

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actinobacteria) that have been frequently studied as

secondary metabolites (Chen et al., 2011; Riedlmeier
et al., 2017), are a further essential class of bacterial
volatiles. Bacterial volatiles have direct and indirect

Figueiredo et al. (2008)

Bano & Fatima (2009)

Adediran et al. (2015)

effects on plant health. Regarding the direct effects,
Cassa´n et al. (2009)

Tortora et al. (2011)

Alami et al. (2000)

some studies have suggested a strong phytotoxicity

Wani et al. (2008)

effect for the inorganic volatiles HCN and ammonia,
References

leading to the potential use in the biological control of

weeds (Flores-Vargas & O’Hara, 2006; Zeller et al.,
2007). However, only few organic bacterial volatiles
Shows growth promotion, N fixa- might have phytotoxic activities (Tyagi et al., 2018).
tion, and redcues metal toxicity

Promotes growth and reduces Zn

Promotes root growth and mini-

The indirect beneficial effects of bacterial volatiles

Promotes the formation of soil

can be achieved by either helping plants cope with

Shows antifungal activity

biotic and abiotic stresses, through induced systemic

mizes osmotic stress
Mechanism of action

resistance (ISR) or inhibiting plant pests and patho-

toxicity in roots
gens, through hindering various developmental stages
Promotes growth
Promotes growth

of multiple-fungal, and bacterial pathogens (Garbeva

aggregates

& Weisskopf, 2020).

Some the bacterial volatiles can confer tolerance to
abiotic stress; such as (1) tolerance to salinity and drought
mediated by 2,3-butanediol (2,3 BD) due to internal
berry caused by Colletotrichum

Metal- contaminated soil with Ni

bean grown in greenhousecon-

decrease in sodium levels and increase in proline accu-

Zn-contaminated media grown
Anthracnose disease of straw-

Stress conditions on common

mulation (Cho et al., 2008, 2013; Desoky et al., 2020a;

Drought stress in sunflower

Ledger et al., 2016; Vaishnav et al., 2015). (2) tolerance

Salinity stress on maize
Biotic or abiotic stress

with brown mustard

Abiotic stress on rice

to low and high temperatures, and heavy metal contami-

nation (Desoky et al., 2020b; Esmaeel et al., 2018). (3)
and Zn in Pea

mitigation of nutrient deficiency through complex vola-

acutatum

tile blends, which has been shown to initiate from acidi-

ditions

fication and lead to increased iron uptake (Zhang et al.,

2009). In addition, DMDS can increase plant growth
under sulfur-limited conditions (Meldau et al., 2013). (4)
the secretion of disease-suppressive bacterial volatiles
A. brasilense REC 2 and REC 3 Siderophores (catechol type)

such as 2-methyl furan, benzaldehyde, 2-furaldehyde,

IAA, cysteine rich peptide
Polyamines (cadaverine)

benzothiazole, N,N-dimethyloctylamine, trimethylamine,

and sulfur-containing volatiles (Hol et al., 2015; Pie-
IAA and cytokinin
Phytohormones

phytohormones

chulla et al., 2017; Tahir et al., 2017).

On the other hand, some bacterial volatiles confer
Metabolites

tolerance to biotic stress (1) the ISR can be triggered

by many volatiles such as 2,3-butanediol, benzalde-
EPS

hyde, indole, 1,3-butanediene and 1,2-benzisothiazol-

3(2H)-one (Chuankun et al., 2004; Hol et al., 2015;
Secondary metabolites of Rhizo-

Piechulla et al., 2017). (2) sulfur-containing volatiles,

1-undecene, or the terpene caryolan-1-ol display
Rhizobium sp. YAS34

direct inhibitory impacts on and fungal pathogens

R. tropici CIAT 899
Table 3  (continued)

Rhizobium sp. RP5

R. leguminosarum

(Chen et al., 2011; Piechulla et al., 2017; Riedlmeier

Bacterial species

Rhizobium sp.

et al., 2017; Weisskopf, 2013). (3) DMDS was uti-

bium spp.

lized as a soil fumigant against pests and soil-borne

diseases (Gómez-Tenorio et al., 2018; Pecchia et al.,
2017). Besides (4) other volatiles, such as nonanal,

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the sesquiterpenes albaflavenone, or acetophenone Van Elsas et al., 1998). Figure 3 shows the various
and pentalenolactone, have been reported to show roles of PGPR in biocontrol and plant growth pro-
direct of inhibition towards bacterial pathogens (Rajer motion. Two recently discovered strains, Burkholde-
et al., 2017; Tetzlaff et al., 2006; Zhao et al., 2008). ria sp. R4F2 and Mitusaria sp. H24L5A, have been
However, the outstanding mechanism is competi- identified from disease-suppressive soils by termi-
tive exclusion; bacterial antagonists compete vig- nal restriction fragment (TRF) length polymorphism
orously with the pathogen for nutrients and space. (T-RFLP) of bacterial 16S rRNA genes associated
Antagonists are often better acclimatized to adverse with damping-off disease suppression (Benítez &
environmental conditions, providing them with a Gardener, 2009; Klieber & Reineke, 2016; Zaynab
competitive advantage over pathogens (Köhl et al., et al., 2018). These two strains, which belong to the
2019; Rao et al., 2016). In addition, antagonistic β-subclass of Proteobacteria, have undergone the
bacteria may produce siderophores, which are iron- early processes of testing and formulation as biocon-
binding proteins with low molecular mass that allow trol agents.
microorganisms to sequester nutrients. Because The genus Burkholderia belongs to the Burk-
antagonists can effectively utilize nutrients at low holderiaceae family in the order Burkholderiales
concentrations, they exhibit rapid growth and can sur- and was separated from Pseudomonas as a new
vive under conditions unfavorable to the growth of genus by Yabuuchi et al. (1992). The genus is
pathogens. Thus, antagonists may stop or slow down known for its ability to adapt to different habitats,
pathogen growth without killing the pathogen directly ranging from freshwater sediments to plant tis-
(Garbeva & Van-Elsas, 2004). sues. The sequencing of more than 35 genomes of
Although PGPR are the most common agricul- Burkholderia has provided very useful information
tural biocontrol agents, several other taxa also employ on the pathogenicity and biotechnological poten-
similar mechanisms. For example, the antagonistic tial of this genus (Patterson & Burkholder, 2003).
activities of Pseudomonads on Fusarium oxysporum In general, Burkholderia can be divided into two
(the causative agent of fire blight in orchards) are also major groups. The first includes pathogens such
attributed to antibiosis (Stockwell et al., 2002). Hey- as Bcc, and the second includes nonpathogenic
dari and Pessarakli (2010) provided a comprehensive species that are typically associated with plants.
list of antibiotics with antifungal potential, includ- Several interesting properties have been reported
ing 2,4-dacetylphloroglucinol, pyrrolnitrin, pyolu- among the second group, including rhizosphere or
teorin, and several derivatives of phenazine. Lytic intercellular colonization, plant growth promotion,
enzymes that interfere with the pathogen’s growth increase of nutrient availability through N fixation
and activities are also produced by many active or phosphate solubilization, aromatic compound
microorganisms. For example, control of the south- decomposition, and the ability to form symbiotic
ern blight-causing fungus Sclerotium spp. by Serra- relationships with plants (Suárez-Moreno et al.,
tia mascescens appears to be mediated by chitinase 2010). For example, a strain of Burkholderia trop-
expression. Similarly, Myxobacter, which produces ica isolated from the tomato rhizosphere in Mexico
lytic enzymes, is effective against some plant patho- demonstrated the ability to promote plant growth by
gens (Heydari & Pessarakli, 2010). dissolving mineral phosphate (Caballero-Mellado
et al., 2007). Bcc, a group of closely related Burk-
holderia species, contains different strains, includ-
Examples of microbial biocontrol mechanisms ing human and plant pathogens. The presence of
that promote plant growth and suppress pathogen human pathogens in Bcc is a major concern regard-
growth ing its use as a biocontrol agent; therefore, the use
of Bcc has been banned (Parke, 2000). The genus
The use of microbial inoculants with beneficial prop- Mitsuaria was discovered in 1999 when a strain
erties is likely to increase. Microbial inoculants can formerly known as Matsuebacter chitosanotabidus
be considered safe, low-cost, and convenient additives was isolated from Matsue soils in Japan (Park et al.,
that are a nature-based option for promoting plant 1999). A new name for the species was later pro-
growth and disease control (Al-Taweil et al., 2010; posed by Park and Amakata’s group, who named

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Fig. 3  The role of plant growth-promoting rhizobacteria (PGPR) in disease suppression (biocontrol) and plant growth promotion
(biofertilization). ISR induced systemic resistance

his chitosanase-producing bacteria as Mitsuaria chi- Benítez and Gardener (2009) isolated two strains
tosanitabida (Amakata et al., 2005). The genus is of Mitsuaria and Burkholderia from soils and identi-
characterized by its chitinolytic capacity, potential fied them as soil-borne disease-suppressing microor-
antagonistic activity against phytopathogenic fungi, ganisms. They isolated these two strains using a pop-
and its ability to colonize the rhizosphere of cab- ulation-based approach to correlate the presence of
bage, soybean, and petunia (Someya et al., 2011). microbial populations with disease suppression using

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T-RFLP. The Mitsuaria and Burkholderia strains Indeed, induced resistance can act remotely and
were marked by different TRFs that revealed a posi- provide systemic protection to plants. Local infection
tive association with disease suppression (Benítez with bacterial, viral, or fungal strains can stimulate
& Gardener, 2009). On screening, Mitsuaria sp. the synthesis of signal molecules that are systemi-
H24L5A showed a clear distinction from the well- cally spread throughout the plant, leading to induced
known species M. chitosanitabida, with 98%–99% systemic resistance (ISR). ISR is relatively easy to
sequence identity according to the Basic Local Align- identify as rhizobacteria present on roots can protect
ment Search Tool. Moreover, the Burkholderia sp. plants against foliar pathogens (Gnanamanickam,
also was clearly distinguished from Bcc, with only 2002). Local oxidative burst, followed by a hypersen-
96% identity. sitive response leading to programmed cell death and
Several isolates of both genera have been tested necrosis of the infection site are the characteristics of
for their biocontrol ability by conducting pathogen ISR (Heil, 2001; Jaber & Ownley, 2018). Rhizobacte-
growth inhibition tests in vitro and in vivo against sev- ria must trigger specific signals to induce ISR. PGPR
eral plant pathogens, including Pythium aphanider- must produce ISR elicitors, and the plant must have
matum, Phytophthora capscici, Pythium sylvaticum, a matching receptor and catalytic defense pathway
Phytophthora sojae, Rhizoctonia solani, Fusarium downstream that can activate the system after iden-
graminearum, Alternaria solani, and F. oxysporum. tification. Microbial-mediated ISR has been reported
The results showed that Mitsuaria sp. isolates have in various crops, including cucumber, bean, radish,
good biocontrol ability to inhibit the mycelial growth tobacco, and tomato, and protection against fungi,
of these pathogens in vitro. Moreover, all the Mitsu- bacteria, viruses, and insects has been demonstrated
aria sp. isolates showed chitinolytic activity when (Gnanamanickam, 2002; Manoussopoulos et al.,
tested in vitro. Conversely, the Burkholderia sp. iso- 2019).
lates showed variable, less frequent inhibition and Biocontrol has also been applied as a part of
no chitinolytic activity in vitro. In addition, in vivo integrated pest management (IPM) practices. IPM
assays on tomato and soybean seedlings revealed is a system in which the hosts, pathogens, environ-
that Mitsuaria sp. H24L5A reduced the severity of ment, and socioeconomic components interact. For
lesions caused by pathogens on soybean and tomato instance, tomatoes require intensive management and
seedlings by 15% and 20%, respectively, compared high economic inputs; therefore, there is a strong need
with negative control. Burkholderia sp. isolates also to fulfill economic and environmental requirements
reduced lesion severity in vivo (Amakata et al., 2005). through effective pest control methods. Indeed, the
Additional research was conducted on Mitsuaria use of rhizobacteria should be considered in an inten-
sp. H24L5A, and the draft genome sequence was sive management program, considering factors such
obtained by Rondot and Reineke (2018). Their study as N fertilization, mulching, and spraying of fungi-
revealed that strain H24L5A had 53% and 53.7% cides to optimize the management of tomato diseases
DNA sequence identity with Leptothrix cholodnii (Bamisile et al., 2019; Jaber & Salem, 2014; Nava
SP-6 and Methylibium petroleiphilum PM1, respec- Diaz, 2006). Given the importance of tomato crops
tively. In addition, some of the protein-encoding and the significant economic impact that diseases
genes not shared with these species were identified may have on them, it is crucial to provide evidence
as genes encoding chitinases, chitosanases, and cel- of disease control that may help overcome disease
lulases, which correspond to the positive chitinolytic outbreak. Bacterial speck caused by Pseudomonas
activity shown in vitro (Benítez & Gardener, 2009; syringae pv. tomato and bacterial spot caused by a
Kuchár et al., 2019; Rong et al., 2012). The bio- group of species in the genus Xanthomonas are the
control mechanisms employed by these strains may most devastating diseases that impact tomato crops.
include nutrient competition, iron competition, pro- These strains are classified into four pathogen groups
duction of antibiotics, secretion of lytic enzymes, and as separate species: X. euvesicatoria (group A), X.
stimulation of plant resistance (Bamisile et al., 2019; vesicatoria (group B), X. perforans (group C), and X.
Gnanamanickam, 2002). Stimulation of plant resist- gardneri (group D). The strains in groups A, B, and
ance is an important mechanism for biocontrol agents D infect both tomatoes and peppers, whereas group C
that do not directly contact the pathogen. strains can only infect tomatoes (Bangeppagari et al.,

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2014; Jones et al., 2004). X. gardneri is especially be grown in different substrates, environments, and
important in Ohio owing to the extremely hot and edaphic conditions (Gnanamanickam, 2002).
humid summer conditions that favor disease progres- Correct formulation and delivery also play an
sion, leading to substantial crop losses (Patiño‐Vera important role in the successful application of bio-
et al., 2005). In fact, according to the USA Depart- control agents. Recent research has focused on cre-
ment of Agriculture, the US produces approximately ating new carriers with favorable characteristics.
13% of the world’s wheat and exports approximately Although a good carrier need not possess every
25% of the world’s wheat (Sales, 2018). desired property, it is recommended that they pos-
Two diseases are of particular concern for wheat sess as many as possible to ensure the efficiency
crops in Ohio; Septoria tritici blotch and Stagonos- and success of the inoculant (Bashan, 1998; Jaber &
pora nodorum blotch. The latter is a major disease Enkerli, 2016; Russo et al., 2019a, 2019b). Inoculants
worldwide and can lead to low wheat yields (Engle are either formulated (carrier and cells) or unformu-
et al., 2006; Jaber & Salem, 2014). S. nodorum is a lated (only cells), which can form aggregates that are
foliar pathogen that gained importance in the Mid- more resistant to environmental changes (Burdman
west in the late 1980s. Stagonospora leaf blotch can et al., 2000; Klieber & Reineke, 2016). In biocontrol
be managed through crop rotation, fungicidal seed products, the formulations can significantly affect the
treatments, application of foliar fungicides, cultiva- performance of the biocontrol agent; thus, it is neces-
tion of resistant cultivars, and application of biocon- sary to consider these parameters in the development
trol agents (Liu et al., 2017). For example, Nolan process (Fravel, 2005; Jaber & Enkerli, 2016). Deliv-
and Cooke (2000) inoculated wheat flag leaves with ery systems must be developed considering the time
Drechslera teres, resulting in a significant decrease and place and the application method, which are cru-
in disease severity and a significant increase in crop cial for ensuring the establishment, proliferation, and
yield. activity of the biocontrol agent (Bamisile et al., 2019;
Fravel, 2005; Xue et al., 2009).
Finally, to test the specificity of the biocontrol
Development and assessment of microbial agents to a location or pathogen, it is necessary to
inoculants for plant growth promotion and disease conduct tests to assess their potential for exploitation,
suppression followed by greenhouse and field tests. Greenhouse
and field tests have three principal objectives: (1)
Successful biocontrol depends on the screening pro- selection of active biocontrol agents that can control a
cess for the biocontrol agent as well as its ability to wide range of plant pathogens, (2) evaluation of bio-
survive in various environments, the correct formu- control agents under controlled environmental condi-
lation and application to the plant or soil, and most tions, and (3) evaluation of different formulations and
importantly, consistent performance in field and methods of application. Biocontrol agents are tested
greenhouse trials (Fravel, 2005; Lefort et al., 2016). directly in the system in which they are intended
First, as described by Benítez and Gardener (2009), for use because the type of biocontrol agent can be
there are multiple approaches for screening biocontrol affected by, environmental conditions, crop culti-
agents, ranging from genomic comparison studies to vars, formulation, method of application, and time
culture-based screenings. Early methods focused on of disease assessment (Bamisile et al., 2019; Fravel,
recovering cells and then screening them for activity. 2005; Zaynab et al., 2018). Biocontrol agents can be
More recently, an applied culture-independent molec- applied by seed coating, spraying, soil-drenching, and
ular tool was developed to identify and recover bio- root-dipping (Gnanamanickam, 2002). The applica-
control bacteria (Benítez & Gardener, 2009). tion method is selected based on the target pathogen,
To determine the ability of biocontrol agents to crop stage, nature and spread of disease, and climatic
survive in various environments, their activity must condition. Soil applications can protect nurseries until
be tested in vitro and in vivo under controlled condi- after transplanting.
tions and in the field. To investigate the mechanisms After biocontrol activity is confirmed using
and desirable traits of biocontrol agents, they should greenhouse and field experiments, the next step is to

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improve the efficacy. Different formulations may be between in vitro and in planta results may occur due
tested to obtain the most efficient and effective for- to the influence of the test medium. In addition, the
mula for the biocontrol agent. Reliable data and con- nutrient status, which represents the availability of
firmed protocols are required to isolate and prepare food for biocontrol agents, contributes to its effec-
biocontrol products. An understanding of the mar- tiveness in the field (Fravel, 2005; Gnanamanickam,
ket and in-depth knowledge of registration processes 2002; Jaber & Enkerli, 2016). One approach that
will help new researchers overcome the challenges considers nutrient status is the use of biosensors to
associated with promoting biocontrol agents as reli- provide nutritional information on biocontrol agents.
able pesticide alternatives for growers. The processes For example, studies on Pseudomonas fluorescens
involved in applying biocontrol agents in an agricul- strain A506 identified a direct relationship between
tural setting include screening, production, registra- antibiotic production against fire blight and iron avail-
tion, and distribution of biocontrol agents. These pro- ability (Bamisile et al., 2019; Temple et al., 2004).
cesses represent links in a chain, which will remain This information can provide data that enables more
robust only if each link is properly monitored and accurate predictions of the effectiveness of biocontrol
developed. agents.
Another key factor in biocontrol is community
signaling. Quorum sensing plays a central role in the
Field testing: a challenge for microbial biocontrol regulatory networks of bacterial genes and is involved
agents in controlling gene expression depending on the spe-
cific concentration of the bacterial population produc-
Microbial biocontrol agents are living organisms that ing signal molecules. This system participates in con-
must overcome a series of obstacles to survive and jugation, symbiosis, and virulence processes, which
proliferate in the medium where they have been inoc- lead to systemic resistance and biofilm formation
ulated. Their capacity to overcome these obstacles in bacteria. Thus, approaches used to assess signals
is tested in the transition from the laboratory to the related to quorum sensing mechanisms are useful for
field. This challenge has proven difficult even for suc- predicting the activity of biocontrol agents. Further
cessfully registered biocontrol agents due to the het- analyses targeting the relationship between quorum
erogeneity of soil inhabitants and lack of standardized sensing and regulatory systems related to biocontrol
protocols to scale up laboratory production. Under- capacity, such as the GacS/GacA system, should be
standing the ecology and micro-ecology of biocontrol assessed. This will provide information about signal-
agents facilitates optimization. Creating an inventory ing cascades and regulatory networks that may occur
of rhizosphere or phyllosphere communities can help in plant–microorganism interactions (Jaber & Enkerli,
elucidate the associations among inhabitants. Gen- 2016; Liu et al., 2001; Manoussopoulos et al., 2019;
eral studies of community dynamics can reveal con- Wei & Zhang, 2006).
clusive data regarding the survival and performance
of biocontrol agents. Pineda et al. (2012) used the
dominance index to compare the competitiveness Scaling up and formulation of microbial
of microbial species under particular environmental biocontrol products
conditions.
The interactions between pathogens and isolates Effective methods for commercial-scale systems
are scored under modified conditions such as water must be developed to produce microbial biocon-
activity and temperature. This research identified in trol agents (Cañamás et al., 2008; Mantzoukas &
vitro interactions under conditions that simulate those Grammatikopoulos, 2020). Production process
during flowering (Anderson et al., 2015; Mantzoukas must be scaled up at least to the level of a pilot
et al., 2019). This approach provides an alternative plan to obtain semi-commercial quantities of bio-
to dual cultures, provides a realistic approximation control agents that could be applied at field scales
of natural conditions, and serves as an alternative to (Patiño‐Vera et al., 2005). For successful commer-
other in vitro assays. Moreover, it opens the alter- cial production, the microbial cells must be toler-
native to media manipulation because differences ant to transportation and storage; therefore, the

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selected medium must provide sufficient nutrients comprehensive understanding of the common appli-
to the microorganism and be inexpensive and suit- cation practices and equipment. The ingredients
able for production in large quantities. Published must be safe and in adherence of regulatory guide-
research on the scaling up of fermentation of bio- lines. All ingredients used must be tested first to
control agents is limited. However, pilot-scale pro- ensure that the target crop is not damaged (Leggett
duction has been conducted for the biocontrol agent et al., 2011; Manoussopoulos et al., 2019; Sasan
Rhodotorula minuta. A 100-L pilot fermenter was & Bidochka, 2013). There is no specific approach
developed and two media were tested to select the for formulating biocontrol products because of the
most suitable one (Patiño‐Vera et al., 2005). As a diversity of species/strains, target pathogens, crops,
result, an alternative medium with a lower produc- and environmental conditions.
tion cost and viable cells of the biocontrol agent Variability may occur even within the same spe-
were obtained on a large scale (Mantzoukas et al., cies, making it necessary to develop separate research
2019; Patiño‐Vera et al., 2005). and development processes for each organism, result-
Methods to manipulate or modify biocontrol ing in higher production costs. In fact, the products
agents have been developed to improve the viability already on the market may not have the most optimal
and efficiency of scaling up processes. For exam- formulation due to cost constraints (Burges, 1998;
ple, Cañamás et al. (2008) induced thermotolerance Manoussopoulos et al., 2019). Continuous research
in yeast cells using mild heat treatments, allowing to improve formulations will facilitate the successful
the cells to survive at higher temperatures when incorporation of biocontrol products into agricultural
processed by spray drying for further formulation. production. Therefore, formulations are a key com-
Although the cells could survive, their viability ponent in determining the effectiveness of biocontrol
was insufficient to consider spray drying as a com- agents in addition to other processes involved in bio-
mercial dehydration method (Cañamás et al., 2008; mass discovery, production, and stabilization. If the
Manoussopoulos et al., 2019). Thus, additional biocontrol agent strains do not reach the formulation
research is required to improve cell tolerance and stage in a stable manner, the commercial potential of
survival during the scaling up of production pro- the agent will be affected (Bamisile et al., 2019; Ron-
cesses. Accordingly, from a technical perspective, dot & Reineke, 2018; Schisler et al., 2004).
effective formulations require prior knowledge Nano-biopesticides present a rapidly expanding,
regarding the biology of the biocontrol organism, commercially appealing concept with a positive
pathogen, environment, and community dynamics. trend to green and precision agricultural techniques.
Indeed, biological formulations that contain living These nano-biopesticides are more acceptable than
organisms have a profound impact on manufactur- conventional chemical pesticides because they are
ing processes. Furthermore, ensuring the ability to safer for plants and generate less pollution (Barik
survive and replicate requires consideration of the et al., 2008; Saad et al., 2021). Nano-biopesticides
target and the stage of the biocontrol agent for for- are chemical complexes of biological origin with
mulation (Burges, 1998; Mantzoukas & Eliopoulos, NPs used as pesticides. Their effectiveness or effi-
2020). ciency can be enhanced through polymers, active
Preparation of the correct formulation for com- particles, metal oxides, and micelles. Qualified
mercial products that contain biocontrol agents can nano-biopesticides should have properties such as
be challenging. Time and money must be invested increasing solubility of low-solubility active ingre-
to find the correct amendment, sometimes with dients, slow targeted release of these ingredients,
unsuccessful results. Most commercially marketed and non premature degradation of these ingredients
products undergo a wide range of transitions before (de Oliveira, 2021; Ragaei & Sabry, 2014). In addi-
a suitable formulation is found. For example, prod- tion, increasing the target specificity and outcome is
ucts containing Bacillus thuringiensis underwent possible via the synthesis of nano-pesticides based
various formulation changes, which started from on the knowledge about pest/pathogen behavior.
aqueous suspensions and wettable powders to flow- Nano-formulations have considerable effects on
able, dry granules (Schisler et al., 2004). Develop- the fate and properties of their active ingredients.
ing a commercially viable formulation requires a Consequently, the shape, size range, and surface

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characteristics of the NPs, adjuvants used and char- in the field. However, the ultimate fate of this nano-
acteristic release within realistic conditions should be formulation in insects, plants, soils, animals, and
defined before application (Ragaei & Sabry, 2014). humans must be determined to ensure their safe appli-
Features such as increased spreading, faster degrada- cation and labeling as stable nano-based products on
tion in soil, and slower residue levels in plants can the national and worldwide market (Lade & Gogle,
be achieved by modifying the biocomposite of nano- 2019; Vimala Devi et al., 2019).
biopesticide, or by forming a polymer carrier, which
has properties such as crystallinity, penetrability, stiff-
ness, biodegradability, solubility, and thermal stabil- Storage and distribution of commercial microbial
ity (Bordes et al., 2009; Bouwmeester et al., 2009; biocontrol agents
Jianhui et al., 2005).
Interestingly, nanotechnology can facilitate the In general, after the biocontrol agent is produced, for-
development of nano-biopesticides from active pes- mulated, and packaged, it is stored in the producer’s
ticide composites and biodegradable polymers to warehouse before shipment to retailers. In the first
improve targeted delivery, and cost-effectiveness. storage room, the producer can adjust the storage
The second generation of nano-biopesticides (poly- environment to the optimal conditions to maintain the
protease, bifunctional insect-specific inhibitors) has original concentration of the cells. However, when
tremendous potential in pest management. Plant- the product leaves the warehouse, it will encounter
derived active pesticide compounds are promising different environmental conditions that may affect its
agents in the development of nano-formulations ideal stability. Consequently, it is important to identify the
for future pesticide solutions. Nano-formulations storage factors that may limit the effectiveness of the
based on bio-based NPs have been extensively stud- product. Thus, storage and shipment durability has
ied and synthesized (de Oliveira, 2021; Narayanan been a priority for new research. Approaches such as
& Sakthivel, 2010). For example, microorganisms using of new granule carriers or the adding of pre-
and plant extracts, are used in the biological produc- servatives are being developed, leading to less expen-
tion of silver NPs, which can be performed at room sive technologies with greater efficacy. Furthermore,
temperature with little or no energy (Benelli, 2016). packaging plays an important role in limiting expo-
The method is also economical and, most signifi- sure of the product to environmental changes. Many
cantly, recyclable (Ingale & Chaudhari, 2013). These types of packaging have been developed, most of
natural nano-factories can synthesize stable NPs with which depend on the final composition of the product.
well-defined sizes, morphologies, and compositions For example, tight plastic containers have been used
simply by adjusting reaction conditions and selecting for liquid suspensions, whereas bags with reinforced
the best organisms (El-Saadony et al., 2021d, 2021e; structures have been used for powdered formulations
Iravani, 2014; Sheiha et al., 2020). For instance, a to ensure handling resistance (Fravel, 2005; Leg-
nano-formulation based on bio-based NPs contains gett et al., 2011; Mantzoukas & Grammatikopoulos,
silver NP with the leaf extract of Ocimum sanctum 2020).
under definite conditions and ­AgNO3. This product
has been successful in controlling insect pests such as
Helicoverpa armigera. Transferring the technology of microbial
The controlled release of these nano-biopesticides inoculants to growers
can be achieved via binding the bioagent to a specific
polymer (e.g., proteins or carbohydrates) that binds Researchers, especially plant pathologists, play an
NPs to the active ingredient-complex (Lade & Gogle, important role in the transfer of technology to grow-
2019). This tertiary structure of the active biopes- ers. Researchers design field bioassays to test biocontrol
ticide-based NPs with a polymer helps release the agents alone or in combination with other products such
active ingredient in a controlled manner and exhib- as pesticides, providing information about integrating
its prolonged insecticidal activity (de Oliveira, 2021; biocontrol into production systems, leading to inte-
Ragaei & Sabry, 2014). The efficacy and efficiency of grated disease control programs. This process should
nano-pesticides are ultimately assessed in vitro and be ongoing, especially for growers who are used to

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apply biocontrol agents as alternatives to conventional Status of biocontrol agents on the market
methods for plant disease management (Fravel, 2005).
In production, the experience of growers and farmers is According to marketing statistics, global biopesticide
important because the conventional agricultural prac- sales have been increasing since 1997 and continue to
tices must be considered. In this regard, regional differ- increase at an annual rate of 10% (Bailey et al., 2010;
ences are also important. For example, Canadian grow- González-Mas et al., 2019; Lopez & Sword, 2015). In
ers often use peat-based and seed-applied inoculants, 2007, the global biopesticide market reached USA $512
whereas growers in the USA prefer liquid inoculants million, accounting for approximately 2.4% of all pes-
(Mantzoukas & Eliopoulos, 2020). ticide sales. Biopesticide sales were expected to reach
Moreover, the needs and experiences of the grow- over one billion dollars by 2012, accounting for approx-
ers must be taken to account to market the product imately 4.2% of the total market. The USA, Canada,
to them. The challenge is to meet low-cost require- and Mexico account for 44% of all biocontrol products
ments, ease of preparation and application, and good sold worldwide, and 53 microbial biopesticides are reg-
performance. Ease of preparation and application and istered in the USA. The European Union has registered
performance can be improved by altering the formu- 21 microbial biopesticides, accounting for 20% of the
lation to make it more user friendly (Burges, 1998; global biopesticide market. The remaining biopesti-
González-Mas et al., 2019). Cost-efficiency can also cide sales are in the Oceanic countries, Latin America,
be improved by paying attention to the methods of and Asia, accounting for 20%, 10%, and 5%, respec-
formulation, storage, and delivery. For example, pre- tively (Bailey et al., 2010; Chandler et al., 2011; Mar-
paring concentrated biomass in liquid formulations is rone, 2008; Russo et al., 2019a, 2019b). Market analy-
practical and can minimize transportation costs but is sis is essential to estimate the size of the target market
highly dependent on the storage temperature, which and avoid product drop-outs due to the lack of interest
implies that the product should be stored and distrib- from agrochemical companies in developing markets
uted under refrigerated/cooled conditions (Abadias (Burges, 1998; Lopez & Sword, 2015; Russo et al.,
et al., 2003; Mantzoukas et al., 2019). Appropriate 2019a, 2019b). These data provide useful information
storage conditions may not be an obstacle; neverthe- on the global status of biopesticides and the increasing
less, warehousing and distribution should be consid- worldwide demand.
ered to accommodate growers’ and farmers’ practices.
Therefore, studies are needed to understand the
needs and preferences of target consumers. This will Microbial pesticide regulatory systems
allow researchers and industries to design better and
more efficient technologies for production, applica- According to the US EPA, all microbial pesticides
tion, and distribution, as well as encourage national are considered biopesticides and are defined as mass-
and local governments to formulate policies for the produced agents derived from living microorganisms
use of biocontrol agents (González-Mas et al., 2019; or natural products and sold for plant pest control
Moser et al., 2008; Russo et al., 2019a, 2019b). For (Chandler et al., 2011; EPA, 2001; Jaber & Salem,
example, Moser et al. (2008) developed the first com- 2014). All microbial products sold in the USA to
parative study to learn about farmers’ perceptions control plant diseases must be registered with the US
of biocontrol in three different regions as part of an EPA. The EPA regulates the use of pesticides under
integrated strawberry pest management project. The the authority of three federal laws: the Federal Insec-
factors that had the greatest influence on the farm- ticide, Fungicide, and Rodenticide Act; the Federal
ers’ confidence in biocontrol were personal hands-on Food, Drug, and Cosmetic Act; and the Food Quality
experience, positive publicity, and advertising. Con- Protection Act. The EPA also regulates three classes
sequently, their study provided a starting point for of biopesticides: biochemical pesticides, microbial
further research on the topic, allowing researchers pesticides, and plant-incorporated protectants. The
and industry personnel to learn more about farmers’ principal aims of pesticide regulations are to ensure
perceptions. that their use does not cause unreasonable negative
impacts on human health or the environment. The

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regulations also serve to characterize the products in educating their customers and placing their bio-
offered by manufacturers, ensuring that they are reli- control products on the market via experienced part-
able and of good quality (Chandler et al., 2011; EPA, ners. Governments should increase federal funding
2001; Fravel, 2005). With regard to human safety, to develop efficacy trials and demo programs, and
tests are needed to assess the pathogenicity, toxic- researchers should focus on integrating of biopes-
ity, and allergenicity of biopesticides (EPA, 2001; ticides and chemicals (Jaber & Salem, 2014; Jensen
Fravel, 2005; Lopez & Sword, 2015; Jensen et al., et al., 2019; Marrone, 2008; Sasan & Bidochka,
2019). 2013).
Moreover, the need for such control is increases Moreover, the development of new microbial
further, and other countries are considering establish- biopesticides will increase the need for market-
ing regulatory systems for biocontrol agents. Regula- ing teams who can understand the needs of farmers,
tions must be implemented realistically and with the agronomists, plant pathologists who can understand
sole purpose of informing about the safety of biope- plant–pathogen interactions, microbiologists who
sticides (Bueno et al., 2004; Chandler et al., 2011). can understand the physiology of biocontrol agents,
The decision to authorize or use biopesticides for chemists who can understand the physical and chemi-
commercial purposes must be based on expert opin- cal properties of formulations, and statisticians who
ion within a regulatory framework. Professionals such can design experiments and analyze data, which
as plant pathologists, entomologists, and environmen- will ensure the development of accurate approaches
tal experts must participate in regulatory processes and efficient methodologies (Bailey et al., 2010;
because of their competence in this field. When regu- González-Mas et al., 2019).
lators lack expertise in the field of biopesticides, they
may delay decision making or request information
that exceeds what is necessary (Chandler et al., 2011;
Jaber & Salem, 2014; Jensen et al., 2019; Sasan & Conclusions
Bidochka, 2013).
Biological control using microbial inoculants is an
effective and environmentally friendly strategy and
Challenges and future perspectives for microbial should be used extensively to control plant patho-
biocontrol agents gens. Biocontrol agents can promote plant growth
and increase plant resistance to pathogens. Apply-
Biocontroll research has grown in the past decade, ing biocontrol strategies will prevent pollution
helping growers reduce chemical pesticides due to the caused by chemical pesticides, fungicides, and fer-
growing demand for environmentally friendly prod- tilizers, thereby providing a clean and sustainable
ucts. The increasing demand for organic products and solution for maintaining successful agricultural
concern for sustainability in the agricultural sector production. In addition, the preparation and produc-
will contribute to new strategies to control diseases. tion of microbial inoculants is easy and inexpensive
One approach to this challenge is to develop a com- compared with that of chemical pesticides. How-
prehensive pest management system in which plant ever, more research is required to confirm the fea-
pest-resistant crops can be used as a second line of sibility of using these microbial inoculants before
defense. The pest-resistant crops must be managed in being marketed to growers and farmers. Careful
a way that allows pest regulator systems to provide consideration should be given to the type of micro-
natural biocontrol. Within this system, IPM promotes bial inoculant and its compatibility with the crop
the regulation of natural pests using environmentally plant. Microbial inoculants have great potential to
friendly technologies (Chandler et al., 2011; Sasan & increase plant growth and resistance to pathogens
Bidochka, 2013; Speiser et al., 2006). when applied to large-scale field and greenhouse
For the successful integration of biocontrol agents, production. This review provides insight into the
government, research, and industry, efforts should complexities of microbial inoculants, describing
focus on increasing user education about pesticides. the benefits and effects on plant growth and resist-
Specifically, production companies will need to invest ance to pathogens. However, we also highlighted

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the need for more research on the mechanisms of Al-Anazi, M. S., Virk, P., Elobeid, M., & Siddiqui, M. I.
actions of microbial inoculants, community interac- (2015). Ameliorative effects of Rosmarinus officinalis
leaf extract and Vitamin C on cadmium-induced oxida-
tions, formulations, and regulations. tive stress in Nile tilapia Oreochromis niloticus. Journal
of Environmental Biology, 36, 1401.
Acknowledgements Authors would like to thank the Alaux, P. L., César, V., Naveau, F., Cranenbrouck, S., &
library at Murdoch University, Australia, for the valua- Declerck, S. (2018). Impact of Rhizophagus irregularis
ble online resources and comprehensive databases. MUCL 41833 on disease symptoms caused by Phytoph-
thora infestans in potato grown under field conditions.
Funding The project was funded by Khalifa Center for Bio- Crop Protection, 107, 26–33.
technology and Genetic Engineering (Grant#: 12R028) to Alblooshi, A. A., Purayil, G. P. Saeed, E. E., Ramadan, G. A.,
SAQ; and Abu Dhabi Department of Education and Knowl- Tariq, S., Altaee, A. S., El-Tarabily, K. A., & AbuQamar,
edge (Grant#: 21S105) to KE-T. S.F. (2022). Biocontrol potential of endophytic actino-
bacteria against Fusarium solani, the causal agent of sud-
Declarations den decline syndrome on date palm in the UAE. Journal
of Fungi, 8, 8.
Alexander, B. J. R., & Stewart, A. (2001). Glasshouse screen-
Conflict of interest The authors declare no conflict of ing for biological control agents of Phytophthora cacto-
interest. rum on apple (Malus domestica). New Zealand Journal
of Crop and Horticultural Science, 29, 159–169.
Research involving human participants and/or ani‑ Al Hamad, B. M., Al Raish, S. M., Ramadan, G. A., Saeed, E.
mals Not applicable. E., Alameri, S. S. A., Al Senaani, S. S., AbuQamar, S.
F., & El-Tarabily, K. A. (2021). Effectiveness of augmen-
Informed consent Not applicable. tative biological control of Streptomyces griseorubens
UAE2 depends on 1-aminocyclopropane-1 carboxylic
acid deaminase activity against Neoscytalidium dimidi-
atum. Journal of Fungi, 7, 885.
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