2

Impact of Biofertilizers on
Horticultural Crops
Clement Kiing Fook Wong1* and Chui-Yao Teh2

Department of Agricultural and Food Science, Faculty of Science,

1

Universiti Tunku Abdul Rahman, Jalan Universiti, Perak, Malaysia

2
School of Biological Sciences, Faculty of Science and Technology,
Quest International University Perak, Perak, Malaysia

Abstract
The ever-increasing global population, climate change, as well as pest and disease
outbreak remains as challenges to the horticultural crop production. There is an
urgent need to intensify crop production using sustainable methods. Plants are
associated with rhizospheric microbes, which have the ability to promote crop
growth and stress tolerance, enhance plant nutrition, and improve vegetation
propagation. Thus, the formulation and application of biofertilizers containing
these beneficial microbes is a promising approach to improve horticultural crops.
In this chapter, the impact of applying biofertilizers will be discussed comprehen-
sively which will include the possible mechanisms of biofertilizers in conferring
plant growth promoting and stress tolerance traits in crops. This chapter will also
look at the possible challenges that will arise from biofertilizer application and
recommend solutions to ensure the most efficient use of biofertilizer in the horti-
culture industry.

Keywords: Abiotic stress, biofertilizer, biotic stress, crop tolerance, horticulture,

yield

*Corresponding author: kfwong@utar.edu.my

Inamuddin, Mohd Imran Ahamed, Rajender Boddula, and Mashallah Rezakazemi (eds.)
Biofertilizers: Study and Impact, (39–104) © 2021 Scrivener Publishing LLC

39
40 Biofertilizers

2.1 Introduction
The horticulture industry is one of the fastest growing sector to fulfill the
increasing demand as the dietary intake from the low- and middle-income
countries has begun to shift toward a higher consumption of vegetables
and fruits due to increased purchasing power [1]. In addition, the esti-
mated world population coming to 2025 will be nearly 8.5 × 109 which
means substantial amount of agricultural produce is needed [2]. Such high
demand often requires the exhaustive use of chemical fertilizers and pesti-
cides to boost yield but these practices have caused potential health issues
among farmers and consumers, soil pollution and infertility, eutrophica-
tion of water sources, pesticide resistance of insects and plant pathogens, as
well as compromised food safety and quality [3]. An estimated of demand
for nitrogenous fertilizer exceeds 130 million tons per year and the depen-
dence on these resources does not only damage the natural environment
but it is also economically infeasible since the production of synthetic
N fertilizer depends heavily on the use of fossil fuels [4, 5]. To achieve
the goal of sustainable horticulture farming, the use of microbial-based
fertilizers or biofertilizers is an alternative that is not only user- and
environmental-friendly but also ensures continuous food production
under variable environmental conditions [6].
A biofertilizer is defined as a formulated product containing one or a
mixture of microorganisms that can improve the nutrient content, growth,
and yield by making nutrients available for plants [7]. These beneficial
microbes are often developed into dry and liquid formulations to prolong
microbial viability under variable conditions and to ensure their efficiency
will not be compromised when exposed to biotic and abiotic stresses [8].
Commonly used beneficial microbes, including the plant growth pro-
moting (PGP) microbes and mycorrhizae fungi, are derived from natural
resources such as the nutrient-rich root rhizosphere and phyllosphere of
the plant. The PGP properties of these microbes are usually characterized
by their ability to fix nitrogen, to solubilize phosphate and potassium, to
produce plant growth regulators and to biodegrade organic soil matter
resulting in enhanced crop growth and yield. Generally, more than 60%
to 90% of applied chemical fertilizer is lost through soil-leaching and only
10% to 40% is taken up by plants [5]. Therefore, the application of biofer-
tilizers has a great potential in integrated nutrient management to ensure
nutrient use efficiency and to improve nutrient availability for crop growth
and yield. Besides improving crop yield, biofertilizers were found to allevi-
ate biotic and abiotic stresses in crops. In the face of climate change, abiotic
 Biofertilizers on Horticultural Crops 41

factors including flooding, increased temperature, soil salinity and drought

has severely hampered crop production [9]. Similarly, biotic stress such as
the invasion of plant pathogens, nematodes, insect pests, and weeds is one
of the major contributors to crop loss [10]. Certain beneficial microbes also
possess dual function of increasing crop tolerance toward biotic and abi-
otic stresses and promoting crop growth and yield under stress conditions
[11]. This chapter will emphasize on the impact of biofertilizers in promot-
ing growth and yield, enhancing tolerance to biotic and abiotic stress and
improving vegetative propagation of horticultural crops. Furthermore, this
chapter will cover the future challenges on the application of biofertilizer
that horticulturists and researchers should be aware of and also the possi-
ble solutions to address these challenges.

2.2 Microbial Strains Used in Biofertilizers

Considering the major drawbacks of using chemical fertilizers and pesti-
cides, the use of biofertilizers is an alternative to reduce the harmful effects
of these chemicals on crop production, environment, and humans. By har-
nessing the microbial diversity in the plant root rhizosphere region, var-
ious microbial strains were incorporated into formulations that, through
their interactions with the inoculated hosts, could benefit plant intake of
nutrients and enhance plant tolerance against biotic and abiotic stresses.
Important microbial strains typically used in the formulation of biofertil-
izers are summarized in Table 2.1.

2.3 Impact of Biofertilizer Application

on Horticultural Crops
2.3.1 Increased Yield and Quality of Crops
One of the obvious impact of applying biofertilizer on horticultural crops is
the improvement of yield count and quality of crops. The overall improved
crop growth performance begins at the root rhizosphere. The complex
interaction between microbial inoculants and the rhizospheric region plays
an important role in shaping the plant’s overall ability to uptake nutrient
(Figure 2.1). Beneficial microorganisms tend to have a symbiotic relation-
ship with plants whereby they derived most of their carbon sources from
the root exudates and in exchange, they make nutrients available for plants
to uptake [5].
42 Biofertilizers

Table 2.1 Microbial strains used in biofertilizers.

Types of Examples of common microbial
biofertilizers Group genera used in biofertilizers
Nitrogen-fixing a
Free-living Azotobacter, Clostridium,
(non-symbiotic) Cyanobacteria (Anabaena),
Klebsiella, Rhodopseudomonas,
Rhodospirillum, Bacillus
b
Symbiotic Rhizobia (Allorhizobium,
Azorhizobium, Bradyrhizobium,
Mesorhizobium, Rhizobium,
Sinorhizobium), Actinomycete
(Frankia)
c
Associative Azospirillum, Herbaspirillum,
Alcaligenes, Bacillus,
Pseudomonas, Enterobacter,
Klebsiella, Acetobacter
Phosphorus Phosphate Bacillus, Pseudomonas, Penicillum,
solubilizers Aspergillus, Trichoderma,
Rhizobium, Burkholderia,
Flabobacterium, Pantoea
Phosphate Arbuscular mycorrhiza
mobilizers (Acaulospora, Glomus,
Gigaspora, Sclerocystis,
Scutellaspora), ectomycorrhizal
(Amanita, Boletus, Laccaria,
Pisolithus)
Micronutrients Potassium Bacillus, Paenibacillus
solubilizers
Silicate and zinc Bacillus, Thiobacillus,
solubilizers Saccharomyces
(Continued)
 Biofertilizers on Horticultural Crops 43

Table 2.1 Microbial strains used in biofertilizers. (Continued)

Types of Examples of common microbial
biofertilizers Group genera used in biofertilizers
Growth Plant growth Alcaligenes, Azotobacter,
promotion promotion Actinomycetes, Rhizobium,
Bradyrhizobium, Bacillus,
Pseudomonas, Enterobacter,
Pantoea, Xanthomonas,
Flavobacterium
Adapted from Singh et al. (2014).
a
Free living nitrogen fixers do not form symbiotic interaction with host plants for nitrogen
fixation.
b
Symbiotic nitrogen fixers form symbiotic interaction with host plants for nitrogen fixation.
Symbiosis is usually characterized by bacterial nodules formed in plant roots.
c
Associative nitrogen fixers form symbiotic interaction with host plants from graminaceous
plants without the formation of nodules.

Improved crop growth and yield due to:

• Increased N levels
• Increased soluble mineral ions
• Regulation of phytohormones

Attract N2
Attract N fixation via free
Root living and associative
Root
exudates N fixing microbes
exudates
NH+
Root Attr
ac
exudates t Insoluble P, K
N2 Mineral ion
N fixation via root
Attract

nodulating bacteria solubilization by PGP

NH+ microbes and AMF
Soluble P, K ions
Root nodulation

Production of
phytohormones by PGP
 microbes and AMF

Figure 2.1 Mechanism of crop growth and yield enhancement induced by beneficial
microbes present in biofertilizers.

Some microbes such as those from the Trichoderma, Pseudomonas, or

Bacillus genus produced organic acids or low molecular weight siderophores
to solubilize essential minerals such as phosphorus (P), iron (Fe), and zinc
(Zn) for plants to uptake. The Rhizobia genus are symbiotic N fixers that col-
onize roots of legumes, through the formation nodules, in order to absorb
nutrients from the root exudates while providing N sources for the plants
[12]. Other microbes including the free-living (Azotobacter, Beijerinckia,
44 Biofertilizers

Klebsiella, and Cyanobacteria) or associative N fixers (Azospirillum) are able

to fix atmospheric N as plants commonly take up N in the form of nitrate
or ammonia ions [13]. Plant hormones are also produced exogenously
by microbes that could cause significant changes to the play physiology.
Auxins (indole acetic acid, IAA), cytokinins, gibberellins, and abscisic acid
are synthesized by microbes and these phytohormones regulate the growth
of plants via the stimulation of cell division [3]. Improved root growth is
often observed as a result of hormonal-induced enhancement [14]. As there
is greater mineral nutrient availability due to microbial solubilization and N
fixation, extensive root networks are beneficial for efficient nutrient uptake
which translates into better growth and yield in crops [15]. The following
sections emphasize on the use of biofertilizer in improving the yield and
quality of vegetables, fruits, and ornamental plants.

2.3.1.1 Vegetable Crops

The use of native Rhizobium isolates improved the seed yield of climb-
ing beans (Phaseolus vulgaris) by 89% increase (4,397.75 kg/ha over non-
inoculated control (2,334.81 kg/ha) and 30% increase over commercial
Rhizobia-based biofertilizer (3,698.79 kg/ha) [16]. Native strains are adapted
to local agro-climatic conditions which allows them to have a compatible
interaction with other resident microbial populations resulting in improved
soil health, nutrient availability and better yields [17]. In the same study, dif-
ferent agroecosystems showed varied seed yield of 4,691.26 kg/ha at lower
midland compared to upper midland at 2,644.05 kg/ha indicating that dif-
ferent soil properties and nutrient levels might affect nodulation of rhizobia
[16]. For instance, P deficient soil affects the biological nitrogen fixation
(BNF) activity despite high abundance of native rhizobia strains and replen-
ishing the soil with P helps to improve the BNF activity in plant roots [18].
The seed yield of Faba and runner bean was also improved via the applica-
tion of Rhizobia biofertilizer [19, 20]. The possible mechanism of Rhizobia
in improving seed yield of legumes was suggested [21]. The detection of
GFP-tagged Azospirillum brasilense in developing seeds demonstrated that
Rhizobia strains not only colonize roots and also actively migrate and form
an intercellular colonization in the developing seeds. Such colonization
behavior could have impacted the number of beans in pods and the pod
size [21]. Additional study is therefore needed to unravel the how bacterial
seed colonization could improve seed yield in leguminous plants.
In an agriculture land rich with native Bradyrhizobia, the seed yield of
cowpea was surprisingly lower (1,280 kg/ha) compared to exogenous appli-
cation of new strains of Bradyrhizobia (1,600 kg/ha) [22]. Feasibility study
 Biofertilizers on Horticultural Crops 45

also showed an increase of net returns by $104–163/ha in inoculated plants

compared to uninoculated control. Naturally, large indigenous Rhizobia
population in soil affects the effectiveness of introduced strains due to com-
petition for nutrients and space but this is not the case in this study. The
ineffectiveness of Rhizobia could be due to strain-specific factor in which
native strains exhibited poor colonization pattern under unfavorable soil
chemical properties when compared to introduced strains [23]. The seed
yield of other legumes such as soybean and mung bean was also improved
after the application of peat-based formulation of Bradyrhizobium under
both N-deficient and supplemented conditions [24]. Other environmental
factors such as the type of soil and amount of rain were also found to impact
the colonization behavior of beneficial microbes. The use of commercial
Rhizotech biofertilizer (consisting of four types of AMF) increased tuber
yields of sweet potato from 12.8 to 20.1 t/ha in sandy clay soil compared to
sandy loam soil which only showed improvement of yield from 7.6 to 14.9
t/ha during the short rain season. The colonization of AMF was also found
to be higher during short rain season due to extended fungal hyphae on
the rhizosphere, thereby improving nutrient availability for plant growth
[25]. In order to exert the positive effects of biofertilizers on the yield of
horticultural crops, environmental factors should be taken into account in
future studies and methods to rectify the poor colonization behavior in the
rhizosphere region should be included as well.
Besides improving yield, the excessive use of fertilizers were also reduced
after the application of biofertilizers on some vegetable crops. The yield of
mustard and tomato was improved up to 108% and 203%, respectively, after
applying Trichoderma-based fertilizers which, in turn, reduce the use of N
fertilizer by 50% [26]. In the same way, the application of a consortium of
Bacillus and Pantoea shortened the initiation and maturity of curd (compact
white head) by up to 20 days, produced quality cauliflowers (enriched with
amino acid, micronutrient, and macronutrient) and also reduced the use of
chemical fertilizers by 25% [27]. In addition to reducing the dependency
on chemical fertilizers, the application of biofertilizers also enhanced the
quality of yield in vegetable crops such as broccoli and tomato. By applying
individual inoculants of Bacillus, Brevibacillus, and Rhizobium, the macro-
and micronutrient content in the broccoli was improved [28]. Tomato
plants inoculated with the commercial biofertilizers Baikal EM1 contain-
ing a consortium of Lactobacillus, Phodopseudomonas, and Saccharomyces
produced larger fruit biomass by 14.30 g per fruit and also and improved
yield by 19%–21% through soil application and 13%–14% through foliar
application [29]. Cabrini et al. [30] also discovered that lettuce inoculated
with rhizospheric yeast, Torulaspora globosa produced better yield quality
46 Biofertilizers

in terms of size and number of leaves. On the other hand, the inocula-
tion of Bacillus and Pseudomonas did not improve the quality and yield
of lettuce when transplanted to the field although these strains improved
the biomass of seedlings [31]. The inability of these strains to survive in
harsh field environment could be the reason behind of such inconsistency.
In another example, unequal size of broccoli was found after the inocula-
tion with Bacillus amyloquefaciens although yield is greatly enhanced [32].
Considering that uniformity in crops strongly influences consumer prefer-
ences, the overall quality of the product should be standardized even if the
yield is increased. Gange and Gadhave [32] reported that inconsistencies
found in the microbial colonization behavior in plants, as a result of incom-
patibility toward indigenous strains, has led to various sizes of broccoli.
Future commercial PGPR products should be tailored to specific crops and
soil types so as to achieve consistent yield and quality in crops.

2.3.1.2 Fruit Crops

Among fruit crops, the effect of applying biofertilizers on the yield and
quality of strawberries is widely studied. Crop maturation days of straw-
berry plants were reduced to about 2 weeks after treated with Pedobacter
and Bacillus strains compared to uninoculated control [33]. Pedobacter
sp. specifically improved the quality of strawberry by increasing the fruit
length and shape index (sphericity) by 28% and 36%, respectively. Applying
Azospirillum and commercial effective microbes (EMs) has improved the
average fruit weight of strawberry by 14.3% although there was no sig-
nificant increase in the fruit number [34]. The berries produced by the
Azospirillum treatment showed intense red color compared to other micro-
bial treatments. Regardless of biofertilizer treatment, the overall sweetness
index was improved in inoculated plants with a significant decrease in total
titratable acidity [34]. When P. fluorescens strain Pf4 was paired with AMFs
from the genus of Septoglomus, Funneliformis, and Rhizophagus, the induc-
tion of strawberry flowers were increased by 35% resulting in increased
number of fruit by 22% and increased fruit weight per plant by 14% to
20% [35]. Nevertheless, when the AMFs were paired with Pseudomonas,
the total fruit fresh weight was reduced by up to 17% and the number of
flowers decreased tremendously. Incompatibility between strains has com-
promised colonization ability of AMF on strawberry plants which conse-
quently imparted negative effects on the overall physiology of the strawberry
plants [35, 36]. In a similar study, the inoculation of commercial products
Rhizocell C containing B. amyloliquefaciens improved the photosynthetic
capacity of strawberry plants leading to greater fruit yield and biomass
 Biofertilizers on Horticultural Crops 47

in two seasons of planting compared to other commercialized product

including MYC 800 (contains Rhizophagus) and Mykoflor (a consortium
of AMFs such as Rhizophagus, Funneliformis, and Claroideoglomus) [37].
In other words, selecting biofertilizers with compatible microbial strains is
essential in order to improve the yield and quality of strawberry.
The yield, quality, and shelf life of mango were also enhanced after apply-
ing biofertilizer. Half dosage of inorganic fertilizer coupled with the applica-
tion of Azotobacter increased yield (57.20 kg/plant) and average fruit weight
(285.15 g) compared to control (48 kg/plant and 240.40 g, respectively). The
shelf life of the mango fruit was increased from 5 to 10 days [38]. This study
was also in congruent with previous studies that have utilized a consor-
tium of AMF (Glosum) and PGPR strains (Azospirillum and Azotobacter to
improve the same physiological parameters [39, 40]. The postharvest qual-
ity of mango was improved when a commercial biofertilizer, Maya Magic
was applied to the fruits during the bagging process. Average fruit weight
and penetration resistance were significantly improved compared to control
treatment though the microbial strains in the biofertilizer were not stated
in the study [41]. Seasonal variation was found to reduce the efficiency of
biofertilizer in improving fruit yield. Guava trees treated with Azotobacter
and farmyard manure gave better fruit yield during rainy season (38.2 kg/
tree) compared to winter season (19.0 kg/tree) [42]. Seasonal variation such
as the low temperature during winter might have induced changes in the
population of the introduced strains, thereby causing variation in yield [43].
Improved plant growth are associated with higher quantities of photo-
synthates such as starch and carbohydrates which are then utilized as energy
to produce flowers and fruits [44]. At the same time, the photosynthates
will be translocated to the fruits, thereby improving the postharvest qual-
ity [44]. The number of papaya fruits was increased to an average of 19.72
per tree after the application of a consortium of Azotobacter, Azospirillum,
and versicular-arbuscular mycorrhiza (VAM) [45]. The overall postharvest
quality was also improved with higher total soluble sugar, beta-carotene,
and minimal acidity. A steady increase of fruit yield in pomegranate from
18 kg/plant to 38 kg/plant within 5 years was observed after continuous
application of AMF and Azotobacter. The productivity of the tree was
correlated with the enhanced vegetative growth parameters such as plant
height and plant canopy [46].
Some PGPR strains have disease suppression properties that enable
plants to retain their productivity even under disease infection. Wang et al.
[47] observed that the inoculation of a biofertilizer containing B. amyloliq-
uefaciens improved the yield of banana from 32.91 t/ha to 41.39 t/ha under
field conditions naturally infested with the fungal disease, Fusarium wilt.
48 Biofertilizers

Further transcriptome analysis revealed that bananas inoculated with rhi-

zobacteria such Pseudomonas and Bacillus showed differential expression
of genes that corresponded to growth promotion and regulation of spe-
cific functions such as flowering, photosynthesis, glucose catabolism, root
growth, and plant defense genes against biotic and abiotic stress. Therefore,
banana plants can still produce yield even though severe disease infesta-
tion [48].

2.3.1.3 Ornamental Plants

The application of AMF biofertilizer was also found to have brought signif-
icant impact to the floriculture industry. AMF inoculation usually resulted
in increased number of flowers, number of flowering plants or early flow-
ering in ornamental plants [36, 49, 50]. However, AMF was also reported
to delay flowering onset and reduce number of flowers [51–53]. Such dif-
ferential response of host plants toward AMF could depend on the com-
petition for nutrients and photosynthates between AMF and flowers, the
preference of AMF in colonizing host plants and also, the ability of AMF in
overcoming nutrient deficiency or other forms of environmental stress [53,
54]. Hence, the use of AMF in the floriculture industry is heavily depen-
dent on the fertilizer regime, soil fertility, and the species or cultivars that
are being produced.
The positive effects of biofertilizer containing PGPR, phosphate solu-
bilizing, and nitrogen fixing bacteria were reported to improve the over-
all growth and flowering characteristics of several ornamental plants such
as petunia, geranium, carnation, gladiolus, chrysanthemum, dahlia, and
poinsettia [55–58]. Important flowering characteristics such as the onset of
flowering was significantly reduced in petunia by up to 20 days when NPK
fertilizers was used in combination with phosphate solubilizing and nitro-
gen fixing bacteria [57]. Saini et al. [59] also successfully reduced the flow-
ering time and increase the flower head size of treasure flower (Gazania
rigens) after treated with AMF or Pseudomonas. The vase-life gladiolus
floral spike was increased from 11 to 16 days whereas the total number
of florets doubled from 8 to 16 when Azotobacter or phosphate solubiliz-
ing bacteria were applied [56]. These flowering characteristics are essen-
tial to fulfill the industry demands through the production of long-lasting
flowers. However, wilting of the basal florets hastened when Azotobacter
was applied but the mechanism behind remains unclear [56]. Similarly,
poinsettia treated with P. putida showed reduced anthocyanin content
which could affect the pigmentation of the bracts [58]. These observations
could be due to poor microbial colonization as a result of production of
 Biofertilizers on Horticultural Crops 49

antimicrobial metabolites from its host as a defense response. Additional

study on the colonization behavior of these beneficial microbes on orna-
mental plants is therefore needed. Perhaps, future research could also be
directed toward the use of biofertilizer in producing ornamental plants
that cater to the needs of consumers such as enhanced petal or bract colors
and larger flowers. More research should also emphasize on the economic
feasibility of using biofertilizer in the floriculture industry so that indus-
trial players could adopt this eco-friendly method to reduce fertilization
costs and to fulfill consumers’ demands.

2.3.2 Enhanced Nutritional Content of Produce

Besides improving crop yield and quality, the nutritional content of crops
could be enhanced through biofortification using biofertilizers. Other
biofortification methods such as breeding or transgenic technology are
time-consuming, technically demanding and may subject to various gov-
ernment regulatory issues before commercialization takes place [60].
Generally, microbial biofortification of crops can be achieved through var-
ious types of mechanism as summarized in Figure 2.2 [61].

2.3.2.1 Mineral-Biofortified Crops

Certain microbes are able to solubilize minerals or micronutrients such
as iron (Fe) and zinc (Zn) by excreting small molecules (siderophores)
or organic acids. In Fe-deficient soil, the accumulation of root phenolics
attracts rhizobia strains to promote nodulation in leguminous plants.

Increased secondary metabolite

production

Increased
micronutrients content Increased vitamin C
(Fe, Zn) and B content

Microbes Microbes

At t
tra
ct Root exudates – Root exudates– rac
Production of Att
organic acids, sugars, organic acids, sugars,
• Siderophores Fe and Zn complex
amino acids, amino acids,
• Organic acids
secondary metabolites secondary metabolites
• Chelating agents Signaling
Soluble cations Synthesis of molecules?
vitamin B
Readily absorbed by roots Readily absorbed
by roots

To induce the production of vitamin C and secondary

metabolites

Figure 2.2 Mechanism of biofortification of crops induced by beneficial microbes present

in biofertilizers.
50 Biofertilizers

These strains produced siderophores under Fe-deficient condition to

solubilize Fe which then promotes the binding of Fe to transporter pro-
teins produced from host plants [62]. So far, most studies on legumes and
tomato emphasized on the estimation of Fe content in the vegetative parts
instead of the beans or fruit in which human consume [63–65]. In fact, the
only successful iron biofortified Phaseolus vulgaris beans was developed by
HarvestPlus through selection breeding and not microbial biofortification
method [66]. Tomato plants treated with Trichoderma biofertilizer showed
an increase in Fe content (245.73 mg/kg) in fruits compared to control
treatment (195.85 mg/kg) and conventional NPK fertilization (202.94 mg/
kg) [67]. As iron deficiency is still prevalent and it is the greatest contrib-
utor to anemia disease, further research on utilizing biofertilizer in pro-
ducing iron-biofortified horticultural crops is necessary. On the other
hand, Zn solubilization could be achieved when bacteria or AMF secrete
organic acids to lower soil pH as slightly acidic soil was found to increase
Zn bioavailability to plants [68]. The production of chelating agents such
ethylenediamine-tetraacetic acid (EDTA) by bacterial strains such as
Agrobacterium Ca-18, Azospirillum lipoferum, and Pseudomonas sp. was
also able to chelate Zn ions which increased the bioavailability of Zn to
plants [69, 70]. Several reports indicated that inoculation of liquid formu-
lation containing Pseudomonas sp. showed accumulation of 26.12% of zinc
in chickpea seeds compared to control while AMF inoculation showed an
increase of zinc content from 12.61 to 16.09 ppm in tomato fruits [71, 72].

2.3.2.2 Enhanced Secondary Metabolites

Flavonoids, polyphenols, anthocyanin, and antioxidants are naturally pro-
duced in plants as secondary metabolites and these beneficial compounds
are widely studied for their anti-inflammatory, anticancer, anti-aging, and
anti-microbial properties [73]. Biofortification of crops through biofer-
tilizer application could be a method for humans to obtain these health
supplements without having to purchase costly over-the-counter supple-
mentary pills. Strawberries, which were treated with AMF or PGPRs (such
as Azotobacter, Azospirillum, Bacillus, Klebsiella, and Pseudomonas), pro-
duced fruits with overall higher flavonoids, polyphenols, anthocyanin, and
antioxidants compared to control treatments [35, 74, 75]. Interestingly,
Todeschini et al. [35] described that AMF inoculation improved the growth
of strawberry, whereas Pseudomonas inoculation improved the yield and
anthocyanin content of the fruit under sterile soil condition. Thus, it is
possible for future study to choose a potential consortium of beneficial
microbes to enhance growth, yield, and secondary metabolite production
 Biofertilizers on Horticultural Crops 51

at the same time. In spite of that, more research have to be carried in a nat-
ural field environment to validate the observations [35].
Economically important crops such as tomatoes were also enriched with
antioxidants (lycopenes), flavonoids, and polyphenols after the application
of biofertilizers containing Bacillus or Trichoderma [67, 76, 77]. Similarly,
other crops such as spinach and flax also exhibited increased amount of all
three metabolites as mentioned after treated with Azotobacter, Bacillus, or
AMF [78, 79]. It would be interesting if clinical trials could be performed
to ascertain the potential of consuming these nutritionally enhanced crops
on a long-term basis.

2.3.2.3 Improved Vitamin Content

Vitamins are sought-after targets of biofortification in crops. The transgenic
golden rice and orange-fleshed sweet potato loaded with provitamin A
are good examples of biofortification via genetic engineering and conven-
tional breeding, respectively [80, 81]. Nonetheless, the tedious government
approval of transgenic crops and lengthy breeding process warrants a much-
needed research on the application of biofertilizers in the improvement of
vitamin A content in crops. The vitamin B group is another topic of interest
lately as deficiency is reported in many poor nations with less diversified
diet [82]. In nature, plants could take up vitamins B1 (thiamine) and B12
(cobalamin) from soil but plants could only synthesize minimal amount of
B1 and B9 (folate). Attempts to utilize biofertilizer in vitamin B fortifica-
tion of horticultural crops are extremely limited. Co-inoculation of AMF
and Pseudomonas were found to increase vitamin B9 content in strawber-
ries [36]. Microbial-rich organic wastes such as cow dung were utilized to
improve the B1 and B12 vitamins content in mung bean sprouts and spinach
[83, 84]. Identification of microbes with the ability to synthesize the B vita-
mins from the cow dung is needed so that these potential microbes could be
formulated into biofertilizers for biofortification of vitamin B in crops.
Vitamin C are mostly found in fruits. The majority of research dis-
covered that application of biofertilizers usually result in higher vita-
min C content in fruits. The utilization of microbes from the genus
Phyllobacterium, Paenibacillus, Pseudomonas, and Glomus have success-
fully increase the vitamin C content in strawberries, lettuce, and tomatoes
[36, 85–87]. In particular, the vitamin C content in strawberries treated
with Pyllobacterium endophyticum was 79% higher that the uninoculated
control. In some cases, the vitamin C content in fruits was reduced after the
inoculation of microbes. For instance, the co-inoculation of Pseudomonas
and Bacillus reduced the vitamin C level of strawberries [88]. Further
52 Biofertilizers

investigation underlying the mechanisms of vitamin C synthesis in plants

during plant-microbe interaction is required in order to facilitate the selec-
tion of potential microbes in vitamin C fortification.

2.3.3 Improved Tolerance Against Biotic Stress

Plants are sessile organisms that are susceptible to different biotic stresses
ranging from plant pathogens infection, nematode infestation, weed, and
insect pest invasion. Sustainable disease management is desirable compared
to conventional chemical methods as it protects both users and the environ-
ment from being exposed to hazardous chemicals [89]. Utilizing biofertiliz-
ers as a potential means of improving tolerance of plants against biotic stress
is gaining popularity among growers due to its positive long-term effect on
soil health and crop productivity [90, 91]. Generally, crop tolerance against
biotic stress is generally as a result of the interaction between beneficial
microbes and host plants which is usually followed by host defense response
(Figures 2.3 and 2.4). The following section reviews comprehensively on the
use of biofertilizer in improving growth and yield of horticultural crops as
well as in building crop tolerance against biotic stress.

2.3.3.1 Fungal and Bacterial Pathogens

Generally, crop loss due to plant pathogens amount to 25% of the global
crop production annually [92]. By harnessing the microbiome in soil
and plants, plant pathogens can be sustainably managed using soil or

Foliar application
of biofertilizer Microbial-induced viral pathogen
Improved crop growth and yield due to: tolerance:
• Microbial release of PGP • SA increase, JA decrease
hormones • Microbial interference of viral
• Enhanced root growth and coat protein and particles
Viral infection
nutrient uptake assembly.
• Improved photosynthesis • Degradation of viral coat protein
activity by microbial proteasome

Fungal
Microbial induced fungal and
infection Microbial-induced nematode invasion
bacterial pathogens tolerance:
Nematode tolerance:
• JA increase, SA decrease
invasion • Competition for space
• Microbial biofilm formation
Bacterial • Root cell wall lignification
• Microbial Secondary
infection • Egg masses colonization and
antimicrobial metabolites
feeding by nematophagous fungi
production
• JA increase to suppress nematode
• Microbial antibiotic production
invasion.
• Competition for nutrient and
• SA increase when nematode-
space
induced root gall is detected by
• Shift in microbiome to enhance
Soil application of microbes.
diversity of beneficial microbes
biofertilizer

Figure 2.3 Mechanism of crop tolerance against plant pathogens (bacterial, fungal,
and viral pathogens) and nematodes as induced by beneficial microbes present in
biofertilizers.
 Biofertilizers on Horticultural Crops 53

Microbial control of weeds::

• Microbial HCN production–interfere
with host metabolism.
Attracts
HIPV release • Microbial secondary metabolite
Natural predators production-interfere host metabolism
• Microbial ALA production - disruption
of chloroplast organelles
Foliar application • Microbial IAA production-inhibit root
Foliar feeding of biofertilizers and shoot growth.
insect larvae

Microbial-induced insect pests tolerance:

• JA increase, SA decrease
• ROS scavenging activity decrease Soil application of
• Volatile (HIPV) production after biofertilizers
microbial inoculation to attract
natural enemies Root-feeding
• Protease release to degrade insect insect larvae
• Microbial production of insecticidal
toxins
• Microbial production of proteinase-
inhibitors to interfere insect digestive
system.

Figure 2.4 Mechanism of crop tolerance against insect pests and weeds as induced by
beneficial microbes present in biofertilizers.

plant-­derived beneficial microbes, by a method known as biological con-

trol (biocontrol), instead of using conventional and harmful chemical
methods [93]. Most of these microbes were known to have both PGP and
biocontrol properties which has garnered attention from researchers to
formulate them into biofertilizers. Several successful instances of applying
biofertilizers to sustain the production of horticultural crops even the inva-
sion of fungal and bacterial plant pathogens were highlighted.
Pre-treating tomato plants by foliar application of B. methylotrophicus
bacterial suspension inhibited the growth of fungal pathogen Botrytis
cinerea by up to 60% while improving plant biomass and fruit diameter
under glasshouse and field trials [94]. The common bean seeds soaked
in B. subtilis suspension also improved the overall vegetative growth and
increased disease control of Curtobacterium flaccumfaciens pv. flaccumfa-
ciens from 42% to 76% [95]. The pre-treatment of seed could have induced
induced systemic response (ISR) response in the bean seedlings by trig-
gering the jasmonic acid (JA)–dependent defense response as evidenced
in the increase of phenylalanine (PAL) activity, phenolics, and lignin accu-
mulation [95, 96]. The application of B. subtilis also improved the ger-
mination of mung beans when inoculated with three different Fusarium
pathogens–Fusarium verticillioides, F. oyxsporum, and Fusarium sp. [97].
Although B. subtilis were not found to produce chitinase (an important
enzyme for degrading fungal chitin cell wall), this strain produced a lipo-
peptide biosurfactant known as surfactin [97]. Yan et al. [98] described
that surfactin helps in biofilm formation that protects microbial cells from
harsh environments, improves microbial swarming motility to nutrient
54 Biofertilizers

rich rhizosphere, enhances root colonization efficiency, and causes perfo-

ration of the pathogens’ membrane resulting in cell electrolyte leakage and,
ultimately, cell death. The use of lactic acid bacteria, Lactobacillus planta-
rum has also successfully reduced the disease severity of three bacterial
pathogens–Pseudomonas syringae pv. actinidiae in kiwifruit, Xanthomonas
arboricola pv. pruni in Prunus, and Xanthomonas fragrariae in strawberry
[99]. Metabolite analysis of the culture filtrate revealed that the presence of
bactericidal metabolites such as lactic acid, plantaricin, and organic acids
could be involved in disease suppression [100, 101]. However, the involve-
ment of these metabolites produced by lactic acid bacteria in biocontrol of
plant pathogens have yet to be elucidated in detail.
Fungal biocontrol strains from the Trichoderma genus are also well
known for their biocontrol and PGP characteristics. Trichoderma asperel-
lum was reported to improve growth and effectively control the fungal
pathogen Macrophomina phaseolina in melon, eggplant, and chickpea
[102] and Fusarium solani in beans, chilli, and peanuts [103]. Bacterial
wilt of tomato, caused by Ralstonia solanacearum, was reduced to an aver-
age of 50% in the first and second year of planting after the inoculation
of T. asperellum [104]. Maximum tomato yield of 6.93 t/ha was achieved
for the first year but the yield slightly dropped to 5.82 t/ha in the second
year which could mean that the biocontrol efficiency was reduced. Rather
than applying the biofertilizer once, continuous and long-term application
could be more beneficial to sustain the population of biocontrol agents
and to maintain the biocontrol efficiency [105]. Enhanced seedling growth
and tolerance of tomato seedlings against the fungus Sclerotia sclerotium
was achieved by the inoculation of T. harzianum [106]. The production of
harzianolide by T. harzianum was discovered to induce expression of genes
involved in the salicylic acid (SA) and JA-ethylene (JA/ET) pathways in pre-
treated tomato seedlings. ISR in tomato seedlings was first initiated with
the activation of PAL enzyme activity through JA/ET signaling pathway
which is also a key regulator enzyme in the synthesis of SA. Subsequently,
the antioxidant activity was triggered via the SA-signaling pathway as a
response of the accumulation of reactive oxygen species (ROS) due to oxi-
dative stress induced by the fungal pathogen [106, 107].
Applying multiple mixture of bacterial strains has been reported to exert
better biocontrol efficiency compared to the use of a single strain. A mixture
of two different strains of B. velezensis improved plant growth and reduced
disease severity of Xanthomonas axonopodis pv. vesicatoria on tomato,
Pseudomonas syringae pv. tomato on tomato, Rhizoctonia solani on pepper,
and Phytium ultimum on cucumber [108]. The synergistic production of
antimicrobial metabolites or enzymes by each strains in the mixture might
 Biofertilizers on Horticultural Crops 55

have resulted in the synergistic effect on disease suppression. Based on

previous study conducted [109], individual B. velenzensis strains produced
specific antimicrobial metabolite such as haloduracin α and bacillomycin,
respectively, worked synergistically in disease suppression. Istifadah et al.
[110] also used a combination of Lysinibacillus, Bacillus, Azotobacter, and
Pseudomonas to decrease the disease incidence of Ralstonia solanacearum
wilt in chilli plants by up to 80% and plant growth promotion was also
observed in this study. The application of a consortium of P. aeruginosa
and T. harzianum formulated into pesta granules has also reduced disease
severity of Fusarium wilt in banana by 66.67% compared to conventional
benomyl fungicide (37.50%) besides promoting the vegetation growth of
banana plants [89].
Changes in the soil microbiome after introduction of new microbial
strains also play an essential role in disease suppression and plant growth
promotion. B. amyloliquefaciens, formulated with pig manure and neem
cake as carriers, increased banana yield, and reduced disease incidences
of Fusarium wilt while at the same time, stabilized the overall bacte-
rial metabolic potential in carbohydrate, carboxylic, acid and phenolics
metabolism in soil [105]. Microbial degradation of these compounds in
soil could lead to lower disease incidence since they could serve as alle-
lopathic agents against plant pathogens [111]. The long-term application
of B. amyloliquefaciens has also caused higher richness and diversity of
soil culturable rhizobacteria in which a healthy and stable soil microbial
population is necessary to maintain continuous cropping and sustainable
high crop productivity [112]. In a follow up study, the use of the same
strain has also improved the rhizospheric soil bacterial population and
improved disease suppression for over 3 years of field trial through bac-
terial taxa specific suppression mechanisms, which has yet to be fully
understood at the current state [91]. A consortium of B. cereus and B.
subtilis were also proposed to influence the soil microbiome of pepper
plants. This has caused the degradation of organic and inorganic materials
in soil which, in turn, provide nutrients for both biocontrol microbes and
plants to thrive [90, 113]. The Bacillus microbial mixture applied together
with mushroom composts significantly enhanced the yield and posthar-
vest quality of pepper fruit and the control efficacy against Ralstonia wilt
and Phytophthora blight in naturally infested field was 76% and 81%,
respectively [113]. Furthermore, the ability of Bacillus strains in solubi-
lizing mineral nutrients into freely available potassium (K) and phosphate
(P) has helped to retain the soil fertility after one growing season [113].
In a recent study, two bacterial strains B. velenzis and P. fluorescens dras-
tically reduced the wilt disease of tomato by reducing R. solanacearum
56 Biofertilizers

population while promoting crop growth [114]. Shifts in the soil microbi-
ome were also observed whereby the enriched Actinobacteria population
in soil was suggested to be involved in the suppression of Ralstonia wilt
[115]. Elsayed et al. [114] also utilized confocal laser microscopy to show
that these strains actively colonized the roots and within xylem vessels.
Efficient root colonizers would often compete with plant pathogens result-
ing in unsuccessful establishment of crop diseases [116]. In addition, the
genome sequencing of the B. velenzis and P. fluorescens has identified anti-
biotic biosynthesis genes that produced diacetyl-phlorolglucinol (DAPG)
and phenazine which have been widely reported for their broad spectrum
antimicrobial activity against plant pathogens [114]. To put it simply, the
interaction of beneficial microbes, host plants and plant pathogens is
complex and dynamic. Such interaction is often interconnected in order
to achieve the biocontrol and PGP effects desired for the development of
sustainable disease management.

2.3.3.2 Viral Pathogens

Viruses are obligate parasites that infect most cultivated crops with at least
450 different species and most of them are RNA viruses [117]. An esti-
mated of 40% of total crop losses are due to viral infestation [118]. Plant
viruses are commonly transmitted through insect vectors and the current
method is to use insecticides which could cause long-term hazards to
the environment and human health [119]. The increasing costs of pesti-
cides and consumers’ demand for pesticide-free food have resulted in the
replacement of chemicals with sustainable alternative such as the use of
biofertilizers [120]. The use of PGP microbes contained in biofertilizers
has been successful in managing plant viruses as well as in improving the
vegetative growth and yield of various horticultural crops.
Tissue-cultured bananas bacterized with Pseudomonas and Bacillus
under in vitro condition reduced banana bunchy top virus (BBTV) by up
to 60% after transplantation [121]. Foliar spray of tissue-cultured bananas
with the same bacterial strains during the hardening and acclimatiza-
tion stage also reduced BBTV infection with pronounced accumulation
of defense related enzymes and pathogenesis-related (PR) proteins which
suggested the priming effect of these strains in activating the host defense
response against viral infection [122, 123]. Under glasshouse and field
conditions, a biofertilizer containing the same microbial strains reduced
BBTV infection at 80% and 52%, respectively, and also, reduced the virus
titer and increased the yield by 53.33% [124]. The high population of the
PGP microbes in the rhizosphere region throughout the growing period
 Biofertilizers on Horticultural Crops 57

could have triggered a cascade of host defense response and improved

the growth of bananas by promoting nutrient uptake [124]. Other similar
studies also demonstrated that banana plants inoculated with a single or
a consortium of Pseudomonas, Rhizobacteria, and Bacillus also increased
tolerance against BBTV, yield and postharvest quality of banana under
field conditions [125–127].
Mild cucumber mosaic virus (CMV) was found to control virulent
CMV infecting tomato plants but causes side effects such as mild stunting,
vigor reduction and 20% yield loss [128]. Hence, a combined application
of Pseudomonas, Stenotrophomonas, Azospirillum, or Anabena with mild
CMV reduced the replication of virulent CMV with decreased disease
severity up to 91.3% [128] while fruit yield of tomato was also improved
by 48% and 40% in glasshouse and field conditions [129]. Beris et al.
[130] concluded that triple soil drench, foliar spray, and seed imbibition
of tomato with B. amyloliquefaciens reduced the severity of tomato spot-
ted wilt virus (TSWV) from 50% to 80%. Moreover, the accumulation of
potato virus Y (PVY) in tomato was also reduced as there was delayed
detection in the apical leaves. SA-induced PR proteins were upregulated in
TSWV and PVY infected tomato plants after inoculation with B. amyloliq-
uefaciens whereas the expression of JA-induced genes were not significant
[30]. Plant defense against viruses is primarily based on SA and second-
arily on JA signaling. SA is crucial for systemic resistance through the acti-
vation of mitogen activated kinase cascade that leads to the upregulation of
NPR1 gene which, in turn, triggers the transcription of PR genes and RNA
silencing antiviral mechanism [131].
Foliar spray with phyllosphere-derived bacteria, B. amyloliquefaciens
prior to virus infection, reduced the relative contents of CMV coat pro-
tein RNA over a 3-year field trial. Viral tolerance of pepper plants was also
associated to the upregulation of PR genes indicating that SA defense sig-
naling was induced [132]. Naturally occurring virus such as broad bean
wilt virus and pepper mottle virus was reduced [132]. The seed transmis-
sion rates of cucumber green mottle mosaic virus (CGMMV) and pep-
per mild mottle virus (PMMoV) in pepper and watermelon seeds were
reduced after the application of P. oleovorans [133]. The subcellular local-
ization of movement protein (MP) of PMMoV was also abolished since
the culture filtrate of P. oleovorans remodeled the aggregation of the viral
protein necessary for seed-to-seed transmission [133]. The study also pro-
posed that the use of PGP microbes could result in several antiviral mech-
anisms including the interference of the production and translation of
subgenomic RNA (sgRNA) in encoding the viral coat protein (CP), affect-
ing the assembly and disassembly of viral particles and the degradation of
58 Biofertilizers

free CP by microbial proteasome [133]. In one study, cucumber plants pre-

treated with Stenotrophomonas maltophilia delayed virus replication for
more than 3 days and repressed the viral protein genes (CP, MP, and Rep)
expression in cucumber leaves [134]. Maksimov et al. [118] described that
most PGP microbes displayed several other antiviral mechanisms includ-
ing the production of extracellular RNases that disintegrate virus particles,
the synthesis of bacterial barnases that possess antiviral activity, and the
production of microbial surfactants that trigger the SA defense signaling
pathway during viral infection. Till now, these proposed antiviral mecha-
nisms induced by PGP microbes have yet to be fully elucidated and such
information would help in developing biofertilizers that contain desirable
antiviral properties in future.

2.3.3.3 Insect Pests

Annually, the total economic losses in agriculture caused by insect pests
reached US$17.7 billion [135]. The use of insecticides is still widely
adopted because of their effectiveness. However, the detrimental effects of
insecticides on users, environment, natural predators, and the rise of resis-
tant insects have prompted the use of beneficial microbes with insecticidal
properties to manage pests in a sustainable manner [136]. The application
of biofertilizers containing individual or a consortium of microbial strains,
which possess dual functions of promoting crop growth and enhancing
crop tolerance against various insect infestation, has also begun to receive
attention [137].
Cucumber seeds imbibed in bacterial suspension of P. fluorescens strain
PF169 showed increased yield of cucumber by 58%, promoted early mat-
uration of plant by reducing the flowering time and most importantly,
reduced the population growth rate of aphids by delaying on the repro-
duction rate of female cotton aphids, Aphis gossypii [138]. Imbibition of
tomato seeds in P. putida also decreased the infestation of cotton leafworm
(Spodoptera litura) and increased the plant biomass as well as yield by 60%
and 40%, respectively [139]. Biochemical analysis of the tomato plants
revealed that antioxidant activity was enhanced and protease activity was
promoted which might indicate the accumulation of proteinase inhibi-
tors that are detrimental against the larvae of S. litura during leaf feeding
[139]. Biofertilizers containing a mixture of Glomus, Rhizobacterium, and
Pseudomonas significantly increased the biomass and yield of Faba beans
and reduced the aphid (Aphis fabae) population by 71.3% compared to
inoculation of single microbial strain (64.0%) [140]. On the contrary, the
inoculation of both Glomus mosseae and G. fasciculatum did not reduced
 Biofertilizers on Horticultural Crops 59

the larval survival of the root-feeding black vine weevil Otiorynchus sulca-
tus resulting in poor strawberry plant performance such as reduced plant,
root biomass and runner production [141]. Colonization with individual
strains could otherwise revert this negative effect by preventing about
88% of eggs from developing into full grown larvae. Gadhave et al. [142]
explained that incompatibility and competition between different strains
could have led to poor root colonization and eventually reduced the host
defense response against insect infestation.
In order to induce the host defense response against silverleaf white-
fly (Bemisia tabaci), the colonization of B. subtilis strain BsDN of tomato
plants triggered a long-term ISR via JA signaling process [143]. The resis-
tance response is a combination of JA-dependent and JA-independent
defense pathways. In JA-dependent pathways, host anti-nutritive proteins
such as proteases and proteinase inhibitors were produced during insect
feeding while the SA-signaling is suppressed to increase host tolerance.
Proteinase inhibitors act to block insect midgut proteinases, thus imprai-
rng protein digestion which delays the release of peptides and amino acids
from dietary protein. This leads to weak and stunted growth and eventually
death [144]. In the same study, mutant tomato plants, which were unable
to produce JA, were used to delineate if plants could achieve similar level
of tolerance against B. tabaci. Interestingly, genes involved in photosyn-
thesis, phenylpropanoid and terpenoid biosynthetic pathways as well as a
Hsp90 chaperonin were upregulated which possibly mediated pest resis-
tance response while also down-regulated pathogenensis and hypersensi-
tivity response in tomato plants [143]. More studies are therefore required
to understand JA-independent pathway in a tripartite relationship of plant,
PGP microbes and insect pests.
All three different strains of Bacillus efficiently suppressed the infestation
of cabbage aphid (Brevicoryne brassicae) infestation and increased the pop-
ulation and parasitism of braconid endoparasitoid (Diaeretiella rapae) but
the bacterial inoculation did not significantly affect the growth of broccoli
[145]. Pare et al. [146] suggested that bacterial volatiles might have facil-
itated plant cellular defences and thus primed plants against the cabbage
aphids. D’Alessandro et al. [147] suggested that rhizobacteria increases her-
bivore-induced plant volatiles (HIPV) production from plants that could
attract and trigger natural enemy responses against herbivorous insects.
The application of AMF Glomus mosseae together with the predatory mite
Pytoseiulus persimilis reduced the population of two-spotted spider mites
(Tetranychus urticae) in common bean plants [148, 149]. It was also sug-
gested that AMF colonized roots may change plant aboveground attributes
such as biomass and the production of HIPV compounds that might have
60 Biofertilizers

attracted predators and parasitoids [151]. The major HIPV compounds

produced by AMF-colonized plants was later discovered to consist of
β-ocimene and β-caryophyllene and terpenoids [151, 152]. Moreover, the
predatory mites were also specifically attracted to AMF-colonized bean
plants by sensing prey-related cues such as egg masses produced by spider
mite and webbing bearing faecal pellets [150].
Soil amendment with two Bacillus strains did not reduce aphid infesta-
tions of pepper in two field seasons but there were reduced population of
green peach aphids (Myzus persicae) colonizing plants compared to con-
trol treatments [153]. Though so, the fruit weight and number of pepper
fruits was higher than control plants consecutively for two harvests. In
other words, plants grown in the presence of Bacillus tolerated the dam-
ages caused by aphids without a reduction in yield. Perhaps, the utilization
of PGP microbes can be combined with natural enemies to control aphid
populations and to conserve naturally occurring biocontrol predators in
field. Soil amendment with PGPR formulation containing Paenibacillus
macerans and B. amyloliquefaciens did not reduce aphid (M. persicae) den-
sities in tomato plants within two years of field study. The yield of tomato
was 1.7- to 2.3-fold greater in PGPR treatments than in untreated plots for
the first harvest but in the subsequent years, no significant improvement
in yield was observed [154]. Tomato plants inoculated with P. fluorescens
strain WCS417r increased the susceptibility toward B. tabaci making the
PGPR strain unsuitable for insect pest management [155]. The ineffective-
ness of some strain of PGPR could be due to the ability of P. fluorescens to
reduce the JA signaling pathway needed for ISR and improved plant nutri-
tion and quality which leads to greater infestation [156, 157]. Megali et al.
[158] also reported that the use of biofertilizers containing a consortium
of lactic acid bacteria, phototrophic bacteria and actinomycetes improved
the yield of tomato but failed to suppress the population rate of African
cotton leafworm (S. littoralis) with a possible reason that the PGPR sup-
pressed the insecticidal glycoalkaloid molecule tomatine production and
JA-dependent defense pathway.
As an alternative, fungal entomopathogens were found to have PGP
and insecticidal traits. A consortium of compatible Beauveria bassiana
and Metarhizium brunneum enhanced the growth of sweet pepper without
affecting the population of aphid endoparasitoids Aphidius colemani [159].
The population of green peach aphid, M. persicae was greatly reduced
by prolonging the larvae development time, delaying the onset of repro-
duction and decreasing the egg production by female aphids. The ento-
mopathogenic fungi are known to be endophytes that colonize roots and
 Biofertilizers on Horticultural Crops 61

increase root hairs during germination. The fungus produces an adhesion

gene (MAD2) that contributes to plant adhesion whereas the other MAD1
gene functions for the fungi to attach to insect cuticles [160]. These bene-
ficial fungi are also able to transfer nitrogen (N) to plants once they have
obtained N by digesting the insect tissue. In return, the carbon derived
from plant photosynthesis is moved to the fungus for nutrition and growth
[137]. To exert their insecticidal activity, these fungi attach on the insect
cuticle, release proteases to degrade the cuticle for penetration, form blas-
tospores to absorb nutrients in the insect hemocoel, and produce insecti-
cidal toxins such as beavericin causing insect death within a few days [137].

2.3.3.4 Nematodes
Plant-parasitc nematodes (PPNs) including root-knot nematodes and cyst
nematodes are causing global crop loss of more than US$157 billion per
year [161]. These nematodes not only damage plant roots but also, they
facilitate infections from plant pathogens such as fungi, bacteria and
viruses. Chemical nematicides are commonly used, but as concern for
environmental problems and human health increase, biological methods
using nematophagous microbes have attracted attention of researchers and
growers.
There are numerous successful instances of nematode management
using biofertilizers containing beneficial microbes. PGP bacterial strains
B. penetrans reduced the Meloidogyne igconita infestation to about 80%
under field condition followed by enhanced plant biomass and postharvest
quality of sugar beet [162]. The utilization of B. velezensis alone consis-
tently decreased the incidence of Heterodera glycines (soybean cyst nem-
atodes) in glasshouse, microplot, and field trials, whereas a combination
of the same strain with B. altitudinis and abamectin (anthelmintic pesti-
cide) increased early plant growth in microplot trials and also, enhanced
soybean yield in field trials [163]. Seed treatment and soil application of
B. subtilis together with vermicompost recorded the highest carrot yield
by up to 28.85 and a drastic decrease of M. incognita population of up to
69.3% [164]. The application of Paenibacillus and Bacillus strains has also
reduced the number of galls and egg mass of M. incognita and improved
the plant biomass as well as nutrient uptake of tomato plants [165, 166].
Crop rotation of tomato with maize and the inclusion of a nematophagous
fungi, Ponchonia chlamydosporia increased yield of tomato by up to 63% in
the first season but dropped slightly to 41.67% on the second season within
a year [167]. The reduction of yield could be due rainy seasons and warm
62 Biofertilizers

weather conditions that result in drop of flowers and constant wet leaves
causing other pathogens to thrive under such condition [168]. Weather
changes might also cause the sporulation of P. chlamnydosporia to decrease,
thereby reducing the nematicide activity [167]. In other words, the study
could be extended to a few seasons to better understand the duration of
protective effect exerted by biocontrol agents.
Increased root branching in banana plants as a result of AMF Glomus
sp. inoculation reduced the root infection by migratory endoparasitic
nematodes, Radophilus similis and Pratylenchus coffeae [169, 170]. The
suppressive effect of AMF could be due to competition for space since
AMF symbiosis promotes increased root branching in which a denser
and extensive root system is less favorable for nematodes because their
infection sites are commonly on primary roots [171]. The application of
another AMF Rhizophagus irregularis also showed efficient root coloni-
zation and reduced root necrosis caused by R. similis by up to 56% which
suggested that AMF competes with nematode for space during root colo-
nization [172]. Vos et al. [173] proposed that nematode suppressing effect
of Glomus sp. against juvenile R. similis in tomato plants was because of the
lignification of root cell and a water soluble compound from the mycor-
rhizal root extract. No further identification and characterization of that
compound was conducted. Coffee plants inoculated with Glomus also
indicated lignification of cell wall, thereby impeding the penetration of M.
exigua into plant roots [174]. Vos et al. [175] found that the priming effect
of Glomus in banana plants primarily triggered the phenylpropanoid path-
way which is responsible for production of lignins resulting in enhanced
banana defense against M. incognita infection.
Nematophagous fungi such as Pasteuria penetrans and Paecilomyces
lilacinus were equally effective in causing maximum reduction in M. incog-
nita infection of okra which leads to the increase in plant growth [176].
These fungi function to reduce root penetration by enveloping the nema-
tode juveniles with endospores, to interfere with the development of repro-
ductive systems in female nematodes causing failure in forming egg masses
and to extend their hyphal in the eggs for colonization which ultimately
leads to egg rupture [177]. A peptidase S8 superfamily protein known as
Sep1, which has serine protease activity found in B. firmus, exhibited the
potential of degrading the intestinal tissues of nematodes [178]. In contrast,
the PGP P. fluorescens produced the antibiotic DAPG that provides mod-
erate protection against M. incognita at 41% but not against M. arenaria,
P. minor, or H. glycines [179]. The production of DAPG was reported to be
not effective against migratory ectoparasites such as P. minor whereas host
 Biofertilizers on Horticultural Crops 63

ISR was found to be effective in the management of sedentary (Meloidogyne

sp.) and migratory endoparasites (Radophilus sp. or Pratylenchus sp.)
[180]. Therefore, nematode suppressing activity could be microbial strain
specific. Combining decomposed organic materials as soil amendments
with biocontrol agents is also one method to enhance nematode control.
Luambano et al. [167] recommended that carbon to nitrogen (C:N) in
organic materials should be moderate as higher C:N ratio could release
toxic phenols that reduce the colonization degree of nematophagous fungi
such as P. chlamydosporia. The organic materials were also decomposed
for 30 days so that immediate nutrient is provided for P. chlamydosporia to
proliferate and parasitize nematodes [167].
Suppressing nematode infestation in horticultural crops is also
largely dependent on host SA and JA signaling pathway induced by PGP
microbes. Martínez-medina et al. [181] explained in detail the regulation of
SA/JA systemic defense response induced by Trichoderma during the inva-
sion of M. incognita in tomato plants. During the invasion stage, Trichoderma
boosts SA-dependent defences in roots which enhance host resistance
against nematode attack. During the feeding stage, Trichoderma interferes
the suppression of JA signaling by nematode for invasion by increasing host
JA levels and thus, reducing nematode development and reproduction. If
nematode parasitim is established, Trichoderma then boosts the activation
of SA-dependent defense which is activated in the gall which then serves as
a defence against invasion by new juveniles. de Medeiros et al. [182] con-
firmed that defense response of tomato against M. javanica to be systemic
whereby the first generation of Trichoderma-primed tomato inherited PGP
and nematode resistant traits. Additionally, Trichoderma-primed tomato
plants also triggered SA-dependent defense response in the early inocula-
tion stage as evidenced by the increase of NAPDH oxidase activity (involves
in ROS production due to hypersensitivity response) and flavonoid biosyn-
thesis. As nematodes utilize ROS depletion and suppresses flavonoid pro-
duction in hosts, inoculation of Trichoderma could be beneficial to crops
in order to block nematode root penetration by boosting the SA-signaling
pathway. In a recent study, the use of biofertilizers containing a consortium
of Glomus, Trichoderma, Pochonia, Agrobacterium, Bacillus, Streptomyces,
and Pichia might not be efficient in protecting plants from nematode infesta-
tion in the long run since antioxidants activity was upregulated which could
rapidly deplete ROS in host and favors nematode infection [183]. Perhaps,
future research should look into the effect of a single and a consortium of
microbial strains in the SA/JA signaling pathways and whether these strains
could provide long-term protective effect against nematodes.
64 Biofertilizers

2.3.3.5 Weeds
Weeds are a major problem in the agricultural system as they are associated
with reduction of about 37% of crop yield [184]. The common weed man-
agement involves herbicide treatment which have caused many health and
environmental hazards while at the same time, producing herbicide resis-
tant weed biotypes [185]. Biological control of weeds using rhizospheric
microorganisms is a promising alternative for reducing chemical usage.
Bacterial or fungal strains isolated from the rhizospheric region were
found to be effective in not only reducing common weeds found in the
horticultural setting but also retain or increase crop yield [186]. Therefore,
the following sections emphasizes on some bacterial and fungal strains
that have been utilized in suppressing weed growth and/or in improving or
maintaining the yield of some horticultural crops.
P. aeruginosa strain KC1 reduced the biomass of two weeds, spiny ama-
ranth, and common purslanes under glasshouse condition [187]. This
strain produced hydrogen cyanide (HCN) that inhibits root growth. The
presence of cyanide causes the formation of metal complexes with func-
tional groups of plant enzymes involved in several major metabolic pro-
cesses such as respiration, nitrate, and carbon dioxide assimilation as well
as carbohydrate metabolism. Cyanide also interacts with a specific protein
plastocyanin which could inhibit the electron transport during photo-
synthesis [188]. P. fluorescens strain WSM3455 also produced HCN that
reduced the biomass of wild radish by 53.2%. The application of this strain
did not pose any significant negative effect on the grapevine plants [189].
Another P. fluorescens strain G2-11 also suppressed the growth of green
foxtail weeds by more than 77.0% and barnyard grass by up to 62.0% while
enhancing the growth of soybean under field conditions. Growth reduc-
tion of soybean was only reported to be 6.5% for root and 1.2% for shoot
[190]. Two species of broomrape weeds were also suppressed by P. fluo-
rescens strain G2-11 as observed by the reduction of shoot emergence from
seeds by 64% and 76%, respectively. The same strain also decreases the
flowering time of Faba bean by up to 11 days and the number of flowers
also increased by five-fold which has proven the dual function of this par-
ticular strain [191].
Certain chemical compounds are released by microbes to inhibit weed
growth. For instance, P. fluorescens strain WH6 produced a compound
known as Germination Arrest Factor (GAF) that arrested germination of
seeds from grassy weeds after the emergence of plumule and coleorhiza
[192]. The compound was later identified chemically as 4-formylaminooxy-
L-vinylgylcine and it was shown to interfere with enzymes that utilize
 Biofertilizers on Horticultural Crops 65

pyridoxal phosphate as a cofactor which include enzymes associated with

nitrogen metabolism and ethylene biosynthesis [193]. However, some
grass species planted for seed and food were reported to be sensitive to
GAF compared to dicot species [192]. Instead of applying to graminaceous
crops, this microbial strain could be applied to dicots to manage the emer-
gence of grassy weeds. P. fluorescens strain BRG100 formulated into pesta
granules also suppressed the activity of green foxtail weed through the pro-
duction of two herbicidal compounds known as pseudophomin A and B
[194, 195]. The biosynthesis pathway of the compounds and their mecha-
nism of growth inhibition of weed remain unknown.
The biosynthesis of 5-aminoleveulinic acid (ALA) produced by B. flexus
strain JMM24 improved the biomass of Indian mustard and decreased the
plant biomass of the yellow vetchling weed [196]. ALA, in high concen-
trations, was found to cause disruption and disintegration of important
cellular organelles such as mitochondria, thylakoid, and chloroplast and
also reducing cellular antioxidant activity leading to cell death [197]. High
concentration of IAA at 64 mM produced by Bradyrhizobium japonicum
strain GD3 also led to inhibition of root growth of morning glory seed-
lings [198]. Transmission electron microscopy (TEM) revealed that dam-
aged root cells were due to vesiculation, cytoplasm disorganization, and
cell wall degradation [198]. IAA, at toxic concentrations, could result in the
inhibition of root and shoot growth, decreased elongation of internodes
and leaf growth, intensified green pigmentation on leaves, stomatal clo-
sure, and increase of ROS accumulation [199]. A phytotoxic compound
known as viridiol was produced by Trichoderma virens which inhibited the
growth of broadleaf and grassy weeds without causing significant loss of
crop vigor and yield of vegetables such as pumpkins and tomatoes [200].
However, the exact mechanism of suppression of viridiol against invasive
weed has yet to be elucidated.

2.3.4 Improved Tolerance Against Abiotic Stress

Due to climate change, agricultural land is facing threats arising from
temperature changes, salinization of land, inconsistent rainfall, and heavy-
metal contaminated soil [201]. Consequently, crops suffer from these
unfavorable abiotic stresses such as drought, salinity, heavy metal toxicity,
cold, and heat stress that could severely plant growth and development
and ultimately reduce yield to about 70% [202]. The use of microbes in the
form of biofertilizer have shown promising results in helping horticultural
crops to gain an upper hand against abiotic stress via various mechanisms
66 Biofertilizers

Heat stress
Microbial-induced plant growth Microbial-induced heat tolerance:
and yield under abiotic stress: • Regulation of stress-related
• Improved nutrient uptake phytohormones (ABA)
• Regulation of growth-related
phytohormones (GA) Microbial-induced cold tolerance:
• Improved photosynthetic • Thickening of xylem cell wall
activity • Enhanced antioxidant activity
• Increased plant biomass (root • Upregulation of cold acclimation
and shoot) Cold stress and stress-responsive genes
• Enhanced yield under stress • Accumulation of secondary
metabolites

Heavy metal +
Cu2+ + Microbial-induced salinity and
Pb Na Cl-
(HM) stress
+
Zn+ drought tolerance:
Cd
+ Ni+ Na+ Cl- • Enhanced antioxidant activity
As • Osmolytes accumulation
Salinity stress
• Regulation of stress-related
Microbial-induced HM phytohormones (ABA, SA, JA)
tolerance: • Regulation of stress-responsive
• Detoxification of HM. genes
• Biosorption and • Production of biofilm as host
Application of microbes
bioaccumulation of barrier
for stress alleviation Drought stress
HM • Production of ACC-deaminase
• Methylation of HM
• Chelation of HM.

Figure 2.5 Mechanism of crop tolerance against abiotic stress as induced by beneficial
microbes present in biofertilizers.

(Figure 2.5). The following sections described the potential use of various
PGP microbes in enhancing abiotic stress tolerance while at the same time,
improving overall vegetative growth and crop yield.

2.3.4.1 Drought
Drought is a water deficit environmental condition that affects agricultural
productivity across the globe and it is linked to global warming. Insufficient
water reduces crop growth and yield which is detrimental to the global
food security, particularly in the developing world [203]. Drought is
expected to hamper crop production for more than 50% of the arable farm-
ing lands by the year 2050 [204, 205]. Currently, beneficial microbes with
PGP and drought tolerant traits are exploited for their ability to improve
growth and yield of horticultural crops under water deficit condition. As
these microbes are abundantly found in different soil conditions including
the dry and arid regions, apply them as biofertilizers could a promising
alternative to help crops cope with drought stress [203].
Under polyethylene glycol induced drought stress, seed germination
of chickpea was improved after seed bacterization with P. putida [206].
P. putida induced drought tolerance in chickpea was characterized by
improved root growth, increased number of nodules, and enhanced anti-
oxidant activity to relieve oxidative stress [206]. The endophytic fungus
Phoma glomerata and Penicillum sp. also produced phytohormones such
as gibberellic acid (GA) and IAA that functioned to enhance cucumber
 Biofertilizers on Horticultural Crops 67

growth in both shoot and root under drought condition while also, improve
nutrient uptake of essential nutrients such as potassium, calcium, and mag-
nesium [207]. Cucumber plants inoculated with a consortium of Bacillus
and Serratia showed darker green leaves and lesser wilt symptoms since
the rubisco enzymatic activity involved in photosynthesis was maintained
after 13 days of withholding water [208]. The negative impact of ethylene
accumulation as a result drought stress in pea and potato plants was allevi-
ated by microbial 1-aminocyclopropane-1-carboxylic acid (ACC) deami-
nase produced by Variovorax, Achromobacter, and Pseudomonas which, in
turn, produced plants with better plant vigor and root growth as compared
to uninoculated plants [209, 210].
Bacterization of grapevine plantlets by B. licheniformis and P. fluorescens
exhibited an increase in abscisic acid (ABA) levels by 76-fold and 40-fold,
respectively, compared to un-inoculated control under drought stress
[211]. Higher levels of ABA during drought are commonly observed which
lead to stomato closure, thereby reducing transpiration rate [212]. After 20
to 30 days of post bacterization, the production of secondary metabolite
such as terpenes increased in grapevines. Terpenes are suggested to have
antioxidant properties that sequestrate free radicals and protective role in
cellular membrane integrity [213, 214]. Nonetheless, more study has to be
conducted to understand the role of terpenes in abiotic stress alleviation
using molecular tools. Drought tolerance in ornamental plants such as lav-
ender was also improved after the application of B. thuringiensis in arid
environment [215]. The potassium, K, content was significantly improved
in lavender in which the K+ ion is an important osmolyte that regulate
water homeostasis, stomatal opening, osmotic potential, and transpiration
under drought stress [215].
The phytohormone, cytokinin (CK), also plays an important role in
drought stress tolerance. During drought stress, the endogenous cytoki-
nin levels in plants decrease to favor root growth and promote stomatal
closure to limit the transpiration process [216]. The use of CK-producing
microbes could replace the loss of endogenous CK in plants, thereby
improving drought tolerance. Improved CK levels in lentil during drought
due to inoculation of CK-producing Methylobacterium stimulated early
growth of shoots and roots, increased photosynthetic rates and improved
harvest by at least 4-fold [217]. In a similar study, lettuce seedlings treated
with CK-producing Bacillus increased the shoot biomass by 50% under
water deficit condition [218]. The ornamental Oriental Thuja plants also
displayed higher levels of CK after inoculation of B. subtilis with the leaves
of seedlings showing higher relative water content under drought condi-
tion [219].
68 Biofertilizers

The production of microbial extracellular polymeric substances (EPS)

is an essential trait that allows bacterial to form biofilm as a protective bar-
rier against drying and fluctuations in water potential. Sadhya et al. [220]
described that the application of P. putida improved the drought tolerance
of sunflower plants because the microbe produced EPS that aggregates
soil around the root which has improved plants’ ability to uptake water
and nutrients from soil. With the advent of high-throughput sequencing,
the whole genome sequence of rhizobacterial strains has made discov-
ery of genes related to symbiotic establishment, nitrogen fixation, and
drought tolerance possible [221]. These two strains (Rhizobium sp. and
Rhizobium cellulosilyticum) has successfully improved seed germination
of soybean under drought condition imposed by 4% PEG [221]. The
sequence information can be further exploited in future to better under-
stand the interaction between microbe and host under drought condition
so that agricultural production could be extended to semi-arid and arid
regions.

2.3.4.2 Salinity
About 50% of a total of 5.2 billion hectare of agriculture land is affected by
salinity [222]. Salinity or salt stress is caused by sodium chloride (NaCl)
which is the major constituent and the Na+ and Cl− ions are toxic for plants
at high concentrations. Reclamation of saline soil using conventional
methods such as scraping, leaching, flushing, or amending with additives
(gypsum or CaCl2) showed limited success. This calls for sustainable meth-
ods including the use of salt-tolerant microbes in enhancing the tolerance
of horticultural crops against salt stress [223]. PGP microbes utilize a vari-
ety of mechanisms to ameliorate salinity stress in crop plants including the
production of an array of phytohormones such as IAA, gibberellins, and
cytokinins, synthesizing of ACC deaminase to reduce the deleterious effect
of ethylene due to oxidative stress, production of exopolysaccharides (EPS)
or biofilm as a barrier for host plants, regulation of host cellular sodium
and potassium levels to achieve homeostasis in osmotic potential, regula-
tion of stress related genes, accumulation of osmolytes (proline) to regulate
cellular osmotic potential and activation of antioxidant systems to scav-
enge ROS during salinity stress [224, 225].
Pantoea dispersa not only improved salt stress tolerance but also yield
of chickpea by improving biomass (32%–34%), pod number (31%–34.%),
pods weight (30%–32.6%), and seeds weight (27%–35%) [226]. The inoc-
ulation of B. subtilis also decreased ROS concentrations while increas-
ing proline content and improved uptake of essential mineral nutrients
 Biofertilizers on Horticultural Crops 69

(N, P, K, and Mg) in chickpea under field salinity stress [227]. The produc-
tion of EPS by salinity tolerant Halomonas variabilis and Planococcus rifi-
etoensis facilitated the formation of biofilm in chickpea roots that served
as a barrier to retain moisture for root growth and to aggregate soil to the
roots so that plants can continuously uptake water and nutrient during salt
stress [228]. Pea plants inoculated with the same bacterial strain showed
reduction in Na+ uptake, reduced membrane damage, improved chloro-
phyll content, and enhanced K+ uptake [228]. In lettuce seedlings, both
AMF strains of Glomus sp. stimulated growth of the seedlings under mod-
erately saline conditions while inoculation with P. mendocina increased
plant biomass even under severely saline conditions which means that
selected microbes can differentially alleviate salinity stress [229]. Besides
that, microbial-treated lettuce seedlings increased root biomass which
helps plants to enhance water and nutrient uptake during salt stress [229,
230]. P. medocina also produced EPS that chelate the harmful Na+ ions and
reduced the Na+ bioavailability for plant uptake [229]. After inoculating
pea plants with Variovorax paradoxus, the growth of pea plants were also
improved by 54% due to increased photosynthetic activity, enhanced root
growth and improved uptake of Ca, Mg, and K [231].
The ability of microbes in regulating host endogenous hormone levels
also play an important role in salinity tolerance. Cucumber plants treated
with Bukholderia and Promicromonospora showed an increase in SA and
GA but lower ABA content [232]. Higher SA level in plants was reported
to suppress ABA signaling, regulate Na+ and K+ vacuolar sequestration in
roots, and reduce Na+ accumulation in shoots by reducing the host activity
of Na+ ion transporters [233, 234]. Lower ABA level in plants increased
leaf conductance and photosynthetic rate due to stomatal opening while
high GA level in cucumber seedlings is desirable since it is involved in
plant growth and development [232]. On the other hand, the application
of P. putida on soybean plants indicated lower endogenous ABA and SA
but higher level of JA during saline condition [235]. Lower level of SA is
associated with less ROS generated during salt stress. The upregulation of
JA and downregulation of SA is similar to ISR against biotic stress. In other
words, ISR could have been signaled in soybean plants since they were
pre-treated with P. putida 7 days before NaCl was applied. Nevertheless,
the exact role of JA in salinity tolerance is still unknown [236]. From these
studies, the changes of SA, JA, GA, and ABA in plants during salinity could
be dependent on microbial strains. Khan et al. [237] described Aspergillus
fumigatus lowered the endogenous ABA but elevated both SA and JA con-
tents in soybean plants which contradicted with previous studies. The SA
and JA signaling in plants are known to be antagonistic which warrants
70 Biofertilizers

further investigation to understand the signaling mechanism of both phy-

tohormones in plant-microbe interaction during salinity stress.
The co-inoculation of Azospirillum and Rhizobium also promoted root
branching in common bean seedlings and increased secretion of nod gene
inducing flavonoids which promoted root nodulation under saline con-
dition [238]. In particular, Azospirillum allows a longer, more persistent
exudation of flavonoids from root which functions to activate nod genes
leading to nodulation in bean roots. Inoculation with PGP microbe from
Azopirillum, Enterobacter, or Pseudomonas genus were found to improved
plant biomass, increased K+ cellular content, enhanced root growth for
nutrient absorption, and yield in various horticultural crops during
salinity stress including tomato, cucumber, pepper, and okra [239–242].
Intriguingly, these studies also demonstrated the ability of PGP microbes
in improving chlorophyll and photosynthesis rate of inoculated plants
during salinity stress. Yan et al. [243] explained that the expression levels
of the Toc (Translocon complexes) GTPases or chloroplast protein import
apparatus were upregulated in tomato plants inoculated with P. putida. This
might facilitate the import of nucleus-encoded proteins from the cytosol
for chloroplast development, thereby indicating that photosynthesis-
related pathways were not affected during salinity stress [244].

2.3.4.3 Heavy Metal

Soil contaminated with high concentrations of heavy metal is often asso-
ciated with excessive use of chemical fertilizers, mining activities, sewage
sludge application, and disposal of heavy-metal waste. Plants absorb and
accumulate heavy metals which could ultimately pass to humans through
food chain [245]. Furthermore, plants also suffer from heavy metal stress,
whereby the negative effects include damage of cellular structures and
metabolism [245]. Applying biofertilizers containing heavy metal-tolerant
PGP microbes is an attractive approach to improve crop tolerance toward
heavy metal stress. In general, microbial bioremediation of heavy metal
includes the transportation of metals across the cytoplasmic membrane,
biosorption and bioaccumulation on the microbial cell walls, metal entrap-
ment in cellular structures such as vacuoles, precipitation of heavy metal,
and metal detoxification via cellular oxidation-reduction [246].
Grapevine plantlets bacterized with a consortium of Micrococcus
luteus and B. licheniformis improved the biomass and also protected the
plants from oxidative stress due to high concentration of cadmium (Cd)
by increasing the host antioxidant activity [247]. Heavy metal tolerant
Bradyrhizobium japonicum increased shoot and root lengths of lettuce
 Biofertilizers on Horticultural Crops 71

seedlings under nickel (Ni), copper (Cu), or lead (Pb) stress. Further FTIR
spectrum of the bacterium indicated that the presence of amine and nitro
functional groups on the membrane were discovered to be responsible for
metal biosorption, thereby reducing the heavy metal bioavailability for
plant uptake [248]. Soybean plants inoculated with Bradyrhizobium sp.
also indicated improved photosynthetic pigments and increased carot-
enoid content to reduce photo-oxidation of chlorophyll pigments under
Cd stress. Inoculated plants also showed reduced Cd content in both root
and shoot. Increased magnesium and iron contents in soybean plants were
also observed which suggested that this microbial strain produce sidero-
phores to sequester essential minerals for host uptake [249].
The plant biomass of spinach was also significantly increased with
decreased accumulation of Cd, Pb, and zinc (Zn) due to the ability of a
consortium of Pseudomonas and Bacillus to produce the growth hormone
IAA [250]. Tomato cultivated under Cd stress did not accumulate high lev-
els of Cd in roots and shoots after applying P. aeruginosa and Burkholderia
gladioli. Metal transporter gene in tomato was also not highly expressed
when inoculated with both PGP bacteria. Metal chelating compound such
as total thiols and non-protein bound thiols in tomato plants was also
enhanced under Cd stress after bacterial inoculation [251]. However, the
mechanism behind the microbial regulation of metal transporter gene
and the production of metal chelators in plants has yet to be investigated.
AMF such as R. intraradices colonizes pepper better than F. mosseae
under Cu stress. The AMF strains prevented metal translocation to shoots
through metal chelators and retained heavy metals on the cell walls of the
mycelia [252]. Reduced arsenic (As) in chickpea seeds and tolerance of
host against As stress were observed after host inoculation of Trichoderma
[253]. Trichoderma was reported to induce methylation of heavy metal in
soil and methylated metals in soil are reduced via volatilization into the
air [254].

2.3.4.4 Cold Stress

Many horticultural crops, including tomato, soybean, and legumes, lack
the ability to tolerate cold temperatures since they are cultivated in tropical
and subtropical regions [255]. Cold or chilling stress severely affects plant
growth and development, limits planting of plant species in cold regions,
and causes loss of crop yield [256]. In terms of plant physiology, cold stress
reduces cellular metabolism, accumulates ROS, decreases cellular osmotic
potential, solidifies plasma membrane, and destabilizes protein complexes
for metabolism [202]. To enable crops to withstand cold stress, microbial
72 Biofertilizers

inoculants or biofertilizers have been successfully applied to enhance crop’s

tolerance against low temperatures.
In vitro grapevine plantlets bacterized with the endophyte Burkholderia
phytofirmans were able to survive at low temperatures of 4°C [257]. The
bacterization of plants showed improved biomass, reduced electrolyte
leakage as a result of thickening of xylem cell wall, elevated levels of sec-
ondary metabolites such as phenolics and proline, and enhanced rate of
photosynthesis and deposition of starch [257, 258]. The bacterial priming
effect of the grapevine plantlets also contributed to cold tolerance through
the upregulation of stress-related genes and metabolites indicating that
the endophyte plays an essential role in the cold acclimation of the plant-
lets [259]. Furthermore, B. phytofirmans was found to induce cell wall
strengthening which prevented cell collapse due to the formation of inter-
cellular ice crystals [260].
Tomato seeds bacterized with cold-tolerant Pseudomonas of Flavobacterium
were successfully germinated at 15°C. Cold tolerance was also achieved
in bacterized plants as observed in the reduction of membrane dam-
age (reduced malondialdehyde levels and electrolyte leakage), activa-
tion of antioxidant activities, and accumulation of proline in the plants
[261]. Similarly, chilling resistance in tomato plants bacterized with cold-
tolerant Pseudomonas was evident with the reduced membrane disrup-
tion, decreased ROS levels, and upregulated expression of cold acclima-
tion genes [262]. The inoculation of AM fungi, Funneliformis mosseae and
Glomus mosseae of cucumber and tomato plants, respectively, reduced
mortality rate, increased plant biomass, increased secondary metabolite
production (proline, phenols, flavonoids, and lignin), enhanced ROS scav-
enging activity and elevated the expression of stress-related genes during
chilling stress [263, 264]. The root water uptake of the common bean inoc-
ulated with Glomus sp. was also not affected under 4°C which suggest that
AMF fungi could protect the root cell membrane from being damaged
under cold stress condition [265]. Cold tolerance was also achieved by
reducing the accumulation of endogenous ethylene in stressed plants. In a
study conducted, a cold tolerant P. putida promoted the growth of canola
under cold stress by producing ACC deaminase which is an enzyme that
reduces the production of ethylene [266]. The accumulation of ethylene
during chilling stress is not desirable as it could increase the senescence
rate of plants. To date, most biofertilizer studies on enhancing crop toler-
ance to cold stress is still at its preliminary stage. More research should be
conducted to understand the role of host defense signaling and metabolic
 Biofertilizers on Horticultural Crops 73

pathways in conferring cold tolerance in crops especially when they are

treated with biofertilizer.

2.3.4.5 Heat Stress

Global climate change is predicted to increase temperatures to about
1.5°C–5.8°C by 2100 [267]. High temperature has caused major impact
on plant growth and development particularly reduction in yield and crop
quality. In order to overcome heat stress in crops, there are several instances
of using biofertilizers to increase plant tolerance to heat stress while sus-
taining or improving the yield. Several studies have discovered the poten-
tial of PGP bacteria from the Pseudomonas, Bacillus, and Orchrobactrum
genus to increase heat tolerance in cereal crops such as wheat while also
improving grain yield under heat stress conditions [268–270]. Surprisingly,
studies on the improvement of thermo-tolerance of horticultural crops
through the biofertilizer application is still lacking. Currently, only a sin-
gle study that utilized B. aryabhattai to improve the tolerance of soybean
plants to thermal stress of up to 38°C. From this study, the PGP bacterium
was found to produce exogenous absisic acid (ABA) which also regulated
the host endogenous ABA. As a result, the bacterial-treated soybean plants
showed elevated concentrations of ABA which led to stomatal closure to
prevent further transpiration during heat stress condition [271]. Since bio-
fertilizer is a promising tool to circumvent heat stress in plants, research
focus should therefore be directed toward horticultural crops to prevent
potential economic loss in the face of climate change.

2.3.5 Improved Vegetative Propagation Efficiency

2.3.5.1 Propagation by Cuttings
Vegetative propagation of horticultural crops uses cuttings as a source of
material to produce clonal planting materials. This method is also an alter-
native to grafting since no rootstocks are needed [272]. There is also no
need for seed germination as certain seeds undergo dormancy. Difficult
to root species often rely on the use of synthetic auxins which act similarly
to natural plant rooting hormones but can be toxic to plants at high con-
centrations [273]. To replace harmful chemicals, applying PGP microbes
to cuttings has begun to receive attention due to their ability to produce
rooting hormones such as IAA to facilitate the rooting process of cuttings.
74 Biofertilizers

Black pepper cuttings dipped in B. tequilensis for 30 minutes produced

cuttings with higher root numbers and plant biomass [274]. Bacillus strains
also improved the kiwifruit semi-hardwoord stem cuttings by 47.5% and
hardwood stem cuttings by 42.5% [272]. The differences in rooting capac-
ity might be due to juvenility of the cuttings. Juvenile cuttings might have
better cellular plasticity than matured cuttings as differentiated cells in the
juvenile cuttings are able to switch and differentiate into adventitious roots
[275]. Grapevine cuttings treated with Azospirillum brasilense also improve
the rooting parameters in terms of the number of roots, root architecture,
and biomass of vines compared to conventional method [276]. It was also
found rooting using PGP microbes is also cultivar dependent whereby not
all grapevine cultivars were responsive to the microbial inoculation [276,
277]. Koyama et al. [278] discovered that when A. brasilense was applied
together with 3 g/L IBA, higher number of adventitious roots was observed
in olive-tree cuttings but the percentage and survival of rooted cuttings
were not significantly different with other treatments. The addition of IBA
might have influenced the production of natural IAA by the rhizobacte-
ria which requires further validation. Certain strains such as Pantoea sp.
produced higher rooting percentages in olive cuttings regardless of inoc-
ulation methods (i.e., dipping or immersing cuttings in bacterial suspen-
sion) and three test cultivars of olive [279]. Interestingly, this strain is not
the best IAA producer compared to Pseudomonas and Bacillus but it syn-
thesizes ACC deaminase that reduces the accumulation of ethylene upon
wounding (i.e., collection of cuttings) and to prevent ethylene from inhib-
iting root development [280].
Most of the vegetative propagation studies of horticultural crops using
PGP microbes are still at its infancy stage. In fact, more in-depth experi-
mental designs should be conducted to study the cultivar/genotype effect
on microbial colonization behavior, factors that affect microbial IAA pro-
duction, the reception and transportation of exogenous auxin in cuttings
exposed to PGP microbes, and the auxin signaling pathways during root-
ing process after inoculation. These information could be proven useful to
accelerate the vegetative propagation process of horticultural crops.

2.3.5.2 Grafting
In modern cropping systems, grafting is commonly used to impart patho-
gen resistance, manipulate plant physiology, confer disease or pest resis-
tance, and tolerate certain soil types [281]. Grafting also increases nutrient
uptake and utilization efficiency in fruits, ornamental, and vegetables.
The rootstocks absorb water and ions more efficiently than rooted plants
 Biofertilizers on Horticultural Crops 75

derived from cuttings, and these water and ions were then transported to
the aboveground scion [282]. Considering the benefits of grafting for farm-
ers, various grafting methods were developed to improve the success rate
of grafting union between rootstocks and scions which include the use of
PGP microbes. Combined application of P. putida and B. simplex (i.e., the
scions were immersed in bacterial suspension for an hour) resulted in 100%
callusing and grafts survival rate compared to single inoculation and con-
trol treatments [283]. Bacterized graft shoots also root faster than control
with better developed and thick shoots which could be due to natural plant
growth regulator, IAA produced by the microbial strains. IAA promotes
active cell division leading to callus formation which then differentiates to
adventitious roots [283, 284]. Köse et al. [285] also submerged the scion for
at least 3 hours in individual strains of Pseudomonas and Bacillus and graft-
ing results showed that the success rate was from 80% to 93.3%. Similarly,
these two strains were known to produce IAA and produce ACC deaminase
which reduced the host ethylene levels in order to facilitate callus formation
[286]. Cacao grafting was improved to 62% as compared to water treatment
(38%) through foliar spray of B. subtilis suspension on the graft unions [287].
Currently, there are still limited research on the effect of these PGP microbes
on other horticultural crops and the mechanism of initiating callus and root
differentiation on the graft union have yet to be studied.

2.4 Future Perspectives and Challenges Ahead

It is evident that the potential of biofertilizers does not confine to growth
and yield enhancement of horticultural crops. Stress tolerance toward var-
ious biotic and abiotic stress of crops was also largely improved through
microbial-mediated defense response. Biofertilizers is also successfully
applied to increase horticulture planting materials through means of veg-
etative propagation. Despite that, there are still a myriad of factors that
affect the efficiency of biofertilizers in delivering consistent results. Factors
that lead to inefficient biofertilization and recommendations to overcome
these issues were summarized comprehensively in Table 2.2. Among them,
non-reproducible results from biofertilizer application are associated with
crop genotypes and physiological age, method and frequency of appli-
cation, and the viability counts or contaminants present in commercial
biofertilizers. Most importantly, academia-industry collaboration on bio-
fertilizer production and knowledge transfer to farmers have also received
less attention in which emphasis are often restrain in lab-scale optimiza-
tion and production of biofertilizers. Social feedbacks from farmers are
76 Biofertilizers

Table 2.2 Challenges and recommendations to improve the efficiency of

biofertilizers.
Challenges Points to consider Recommendations
Manufacturing • Single or a • Ensure the consortia are
process of consortium of compatible to each other [288,
biofertilizer inoculants. 289].
• Shelf life of • Identify suitable carriers and
biofertilizer. additives to protect inoculants
• Types of carrier from harsh soil or phyllosphere
used to contain conditions to increase viability
the inoculants. [290].
Marketing and • Concentration of • Present regulations should
quality control viable cells. be enforced and updated
of biofertilizers • Contaminants regularly so that manufacturers
present in abide by the requirements
biofertilizers. for a quality biofertilizer
before commercialization is
commenced [7, 291].
Biosafety issues • Some inoculants • Use polyphasic approach to
of inoculants may be characterize inoculants to
opportunistic ensure inoculants are not
human human pathogens and to follow
pathogens. Environmental and Human
Safety Index (EHSI) to compare
inoculates with pathogens [292,
293].
Persistence of • Develop • The molecular marker-assisted
microbial methods to track method including T-RFLP,
inoculant in the persistence DGGE, or TGGE could be
soil of inoculants used to qualitatively assess the
that lead to plant persistence of inoculants and
growth and changes in the microbiome
stress tolerance. [294].
• Use of qRT-PCR to specifically
target and quantify the
inoculants present soil and root
[295, 296].
(Continued)
 Biofertilizers on Horticultural Crops 77

Table 2.2 Challenges and recommendations to improve the efficiency of

biofertilizers. (Continued)
Challenges Points to consider Recommendations
Microbial • Competition • Future study on the key genes
inoculant between native involved in the interaction
interaction and introduced process between inoculants and
with biotic and inoculants. native microbes to understand
abiotic stress • Survival of the metabolic potential of soil
inoculants in microbial communities in
harsh conditions response to inoculation which
in soil (e.g., allow the design of biofertilizers
salinity, heavy to specific soil/crops [294].
metal toxicity, • Identify strains that are tolerant
and soil pH). to abiotic stress to increase
survival rate in soil [297].
Fertilization • Viability of • Optimization study of
scheme inoculants suitable dosages in combined
affected by the treatments of fertilizers and
application inoculants to achieve positive
of organic outcomes [298, 299].
or chemical • Choosing suitable organic
fertilizers. fertilizers except for sewage
sludge which reduces soil
microbial community [300].
Cultural practices • Soil disturbance • Conservation tillage enhances
in farm such as tillage the stability of rhizopsheric
reduces microbial microbial community
community (e.g., which directly improve crop
AMF). production [301, 302].
Application • Performance • Automated application of
methods of biofertilizers biofertilizer to ensure equal
affected by distribution [294].
application • Repeat application of biofertilizer
methods. as boosters to improve microbial
colonization [303, 304].
• Further optimization work
needed for biofertilizer applica­
tion in different agriculture
field production setting to meet
farmers’ requirement.
(Continued)
78 Biofertilizers

Table 2.2 Challenges and recommendations to improve the efficiency of

biofertilizers. (Continued)
Challenges Points to consider Recommendations
Crop genotype, • Inoculant • Proper optimization study
physiological performance needed to study the effect
factors, and differs in various of crop genotypes and
plant health crop phenotypes, physiological stages on the
health colonization behavior of
conditions inoculants [305–307].
of plants, • Future study to study the root
physiological exudates of crop of various
stages (i.e., seed, genotypes, physiological stages
seedlings, or and health conditions which
matured plants). could directly affect microbial
colonization [308, 309].
Knowledge • Transfer of • Engaging researchers-industry
transfer to technical collaboration to produce
industrial level knowledge for quality biofertilizers [304].
for optimum industry to
formulation produce quality
biofertilizers.
Awareness of • Farmers’ poor • Engaging stakeholders
farmers perception on in educating farmers in
biofertilizer biofertilization [310, 311].
(i.e., chemical • Monitoring farmers’ and
fertilizers/ stakeholders requirements
pesticides are and feedbacks on the
easily available biofertilization efficiency on
and more crop production for continuous
efficient than improvement [312–314].
biofertilizers).

also essential so that constant improvements could be made to improve

the quality of the biofertilizers. To conclude, successful biofertilization on
horticultural crops require a thorough consideration of numerous factors
so that growers could benefit from the sustainable and consistent use of
biofertilizers instead of relying heavily on chemical fertilizers.
 Biofertilizers on Horticultural Crops 79

2.5 Conclusion
Biofertilizers have indeed brought positive impacts to the horticulture
industry by ensuring that crop productivity is sustained under unpre-
dictable environmental conditions. Yet, inconsistencies still exist in many
of the research as reviewed in this chapter. In order to bridge the gap,
future investigations should be directed toward a holistic understanding
of the mechanisms and factors that affect the efficiency of biofertilizers.
On the other hand, policy makers should enforce tight regulations to ensure
the biofertilizers have met the necessary requirements prior to commer-
cialization. Stakeholders, too, should be actively involved in transferring
knowledge to farmers and to constantly monitor the outcomes from field
trials. Combining these approaches would foster the use of biofertilizers
as a sustainable choice instead of using chemical fertilizers or pesticides.

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