Microbiological Research 239 (2020) 126569

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Microbiological Research
journal homepage: www.elsevier.com/locate/micres

Productivity and quality of horticultural crops through co-inoculation of T

arbuscular mycorrhizal fungi and plant growth promoting bacteria
Obianuju Chiamaka Emmanuela,b, Olubukola Oluranti Babalolaa,*
a
Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, 2735, Mmabatho, South Africa
b
Farming System Programme, National Horticultural Research Institute, P.M.B. 5432, Jericho Reservation Area, Ibadan, Nigeria

A R T I C LE I N FO A B S T R A C T

Keywords: Associations between plants and microorganisms exist in nature, and they can either be beneficial or detrimental
Antioxidants to host plants. Promoting beneficial plant-microbe interaction for increased crop yield and quality is one
Bio-fertilizer pathway to eco-friendly and sustainable crop production. Arbuscular mycorrhizal fungi (AMF) and plant growth
Crop yield promoting bacteria (PGPB) are microorganisms that are beneficial to horticultural crops. Arbuscular mycorrhizal
Microorganism
fungi establish symbioses with plant roots which help to improve nutrient uptake by the host plant and alter its
phytochemicals and nutrient uptake
physiology to withstand external abiotic factors and pathogens. Plant growth promoting bacteria promote plant
growth either directly by aiding resource acquisition and controlling the levels of plant hormones or indirectly
by reducing the inhibitory effects of phytopathogens. Co-inoculation of both organisms combines the benefits of
each for increased crop productivity. Even though the co-inoculation of PGPB and AMF have been shown to
enhance the yield and quality of crops, its benefits have fully not been exploited for horticultural crops. In this
review, the response of horticultural crops to co-inoculation with PGPB and AMF with particular interest to the
impact on the yield and crop quality was discussed. We explained some of the mechanisms responsible for the
synergy between AMF and PGPB in plant growth promotion. Finally, suggestions on areas that need to be
researched further to exploit and improve the effects of these organisms were highlighted.

1. Introduction management conditions (Ganeshamurthy et al., 2015). This has a lot of

Increased awareness in recent years of the health-promoting and
protecting attributes of phytochemicals and minerals in horticultural
crops has led to increased attention to them as vital constituents of
regular diets. Horticultural crops include vegetables, fruits, spices and
nuts which are directly utilized as food by man, as well as flowers and
ornamental plants, medicinal and aromatic plants (Singh and Prajapati,
2018). Edible horticultural crops, when incorporated into the daily diet,
have strongly been linked with reduced risk of cancer, heart disease,
infections and other chronic diseases (Prior and Cao, 2000). The shift
towards healthier diets and population growth has led to an increased
demand for fruits and vegetables (Mason-D’Croz et al., 2019). To keep
pace, a more sustainable and environmentally friendly approach needs
to be adopted. Duhamel and Vandenkoornhuyse (2013) stated that the
dilemma facing contemporary horticulture is the necessity to cultivate
sufficient nutritious food for the growing global population without
aggravating the existing environmental challenges. These horticultural
crops may absorb between 500 – 1000 kg of nitrogen (N), phosphorus
(P) and potassium (K) per hectare annually or even more under good
cost and environmental implications. In a review, Alori et al. (2017)
reported that the constant use of fertilizers can lead to low agricultural
productivity, unfavourable returns on investment, food poisoning, soil
damage, biodiversity loss and severe environmental hazards.
Consequently, efforts need to be put in place for more sustainable
horticultural practices for greater crop yield and quality. These prac-
tices should maximize the use of methods that improve nutrient uptake
and increase the nutrient pool in soil. To meet these objectives, the
opportunities offered by microorganisms can be a beneficial alternative
(Rouphael et al., 2015). Microbial inoculants such as AMF and PGPB
are used as biofertilizers/biostimulants to improve the availability and
uptake of soil nutrients (Alori et al., 2017) although they are neither
nutrients nor pesticides (du Jardin, 2015). Exploring their mechanisms
can be a valuable tool for the realization of sustainable horticultural
production (Rouphael et al., 2015).
Arbuscular mycorrhizal fungi establish symbioses with plant roots
which help to improve nutrient uptake by the host plant and alter its
physiology to withstand external abiotic factors and pathogens
(Nadeem et al., 2017). They are known to prompt variations in plant

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

https://doi.org/10.1016/j.micres.2020.126569
Received 11 May 2020; Received in revised form 23 July 2020; Accepted 25 July 2020
Available online 31 July 2020
0944-5013/ © 2020 Elsevier GmbH. All rights reserved.
O.C. Emmanuel and O.O. Babalola
secondary metabolism resulting in improved phytonutrients (Rouphael
et al., 2015). Plant growth promoting bacteria promote plant growth
directly by facilitating nutrient uptake through fixing nitrogen, solu-
bilisation of phosphorus, production of hormones (cytokinins, gibber-
ellings, ethylene, auxin and indole acetic acid) and iron uptake (Glick,
2012; Olanrewaju et al., 2017). They also promote plant growth in-
directly by reducing the inhibitory effects of several phytopathogens on
plant growth and development (Glick, 2012). The co-inoculation of
both organisms combines their benefits for increased productivity as
PGPB have been shown to stimulate the beneficial role of AMF and vice
versa (Xie et al., 2018). Arbuscular mycorrhizal fungi interactions with
bacteria have been reported to enhance plant growth through phos-
phate solubilization, nitrogen fixation, increased AMF spore germina-
tion and colonization of plant roots (Selvakumar et al., 2016). The
potential of co-inoculation of these two organisms in promoting the
growth of horticultural crops like tomato (Bona et al., 2018), straw-
berry (Todeschini et al., 2018), lettuce (Kohler et al., 2010) and spinach
(Khalid et al., 2017) have also been reported. These studies prove that
increased nutrient uptake in plants colonized by AMF and PGPB can
lead to a significant reduction of the application rate of fertilizers and
pesticides while at the same time giving equal or even greater crop
yields. However, these benefits have not fully been exploited for most
horticultural crops. This could be due to inconsistent results obtained
from the use of these organisms because of the complexities involved in
their interaction with host plants, inoculation methods and environ-
mental conditions (Baum et al., 2015).
There is, therefore, the need to understand not only the mechanisms
by which they function, but also how they can be exploited and scaled
for extensive and sustainable horticultural crop production. This re-
view, therefore, highlights the recent advances on the response of
horticultural crops to co-inoculation of AMF and PGPB, particularly on
yield and quality. The quality of horticultural crops in this review refers
to all aspects of the horticultural crop that ensure consumers satisfac-
tion (nutritional value, taste, appearance, shelf life etc.). The nutritional
quality is closely related to the chemical composition of the plant which
comprises of high concentrations of essential minerals, carbohydrates,
bioactive compounds and secondary metabolites (Wiesler et al., 2003).
The quality of horticultural crops can be improved by conventional
breeding, tissue culture, application of micronutrients as well as the
inoculation of PGPB and AMF. We also discuss the effectiveness of these
microbes as a sole inoculant and look at the factors that enhance/limit
the performance of their combined application. We equally gave insight
on how these microbes boost the yield and production of plant sec-
ondary metabolites and how their co-inoculation can be beneficial for
Table 1
Plant secondary metabolites influenced by AMF.
Crop AMF species
Sweet basil Glomus fasciculatum
Rhizophagus intraradices
Tomato Rhizophagus irregularis, Funneliformis mosseae and
Rhizoglomus irregulare
Lettuce Funneliformis mosseae, Rhizoglomus irregularis Glomus
fasciculatum
Strawberry G. intraradices
Garlic G. fasciculatum
Pomegranates G. mosseae, Acaulospora laevis and G. manihotis
Onion Rhizophagus irregularis
Citrus G. versiforme
Grapevine G. mosseae, G.
fasciculatum, G. intraradices
Pepino G. etunicatum and G. versiforme
(Solanum muricatum)
Apple Rhizophagus irregularis
Sour orange G. mosseae, G. intraradices and G. hoi
Trifoliate orange G. versiforme
Microbiological Research 239 (2020) 126569
the enhancement of plant quality.
2. Benefits of arbuscular mycorrhizal fungi inoculants for
horticultural crop production
The AMF are obligate symbionts of the phylum Glomeromycota
(Schüßler and Walker, 2010). They form symbiotic associations with
roots of vascular plants and are widely distributed in a variety of eco-
systems including stressed environments (Sadhana, 2014). This sym-
biosis enhances nutrients like phosphorus (P), nitrogen (N), sulfur (S),
potassium (K), calcium (Ca), copper (Cu) and zinc (Zn) in the soil
(Nadeem et al., 2014; Turrini et al., 2018) especially in nutrient-defi-
cient conditions, thereby having the potential to reduce external ferti-
lizer application (Zouari et al., 2014). The colonized plants reciprocate
by supplying the AMF with plant sugars for its nutrition (Verbruggen
et al., 2013). The AMF are estimated to colonize the roots of up to 80%
of terrestrial plant species (Tarkka et al., 2018) and are beneficial for
many horticultural plants, such as citrus, apple, peach, strawberry,
lettuce, pineapple, onions, melon and pepper (Thamsurakul et al.,
2000; Wu et al., 2013).
Improved phosphorus nutrition is one of the paramount benefits of
AMF to crop production (Hart and Forsythe, 2012). Tawaraya et al.
(2012) reported that AMF increased P availability for welsh onion by
solubilizing the insoluble fractions of inorganic P leading to increased P
uptake and concentration in the plant tissue. Similarly, Aliasgharzad
et al. (2009) reported improved P and K uptake of onions grown under
drought stress due to AMF inoculation. Arbuscular mycorrhizal fungi
colonization of plant roots increases the ability of the roots to absorb
nutrients (Sadhana, 2014). They also grow a web of outer hyphae that
significantly extends the soil surface area for nutrient uptake (Tawaraya
et al., 2012). The rhizosphere zone that is directly influenced by AMF is
referred to as mycorrhizosphere (Azcón-Aguilar and Barea, 2015).
Some of the mechanisms used by AMF include improved plant nutrient
uptake, increased antioxidant system, modification of root architecture
and enzyme production (Nadeem et al., 2014). Similarly, increased
plant tolerance to stress, out-competing the pathogen for food and
space (Schouteden et al., 2015) and activation of defence mechanisms
due to phytochemical accumulation (Olowe et al., 2018) are some of
the beneficial mechanisms of AMF.
Beyond improving the yield of horticultural crops, mycorrhizal in-
oculation has also been shown to improve their nutritional quality
(Baum et al., 2015; Rouphael et al., 2017). It modifies primary and
secondary metabolisms of the host plant, thus stimulating the produc-
tion of phytochemicals in the plant parts (Sbrana et al., 2014). These
AMF enhanced plant secondary metabolites Reference
Essential oil, phenolics Rasouli-Sadaghiani et al. (2010)
Anthocyanins and organic acids Scagel and Lee (2012)
Carotenoids, lycopene, polyphenols Hart et al. (2015)
Giovannetti et al. (2012)
Phenolics, anthocyanins, Carotenoids, Ascorbate Avio et al. (2017)
Baslam et al. (2011)
Flavonoid and phenol Castellanos‐Morales et al. (2010)
Enzyme alliinase Borde et al. (2009)
Phenol, enzymes Catecholase and Cresolase Singh et al. (2012)
carbohydrates, protein and phenolics Lone et al. (2015)
vitamin C, flavonoids, and minerals Zeng et al. (2014)
Sugars, phenol Eftekhari et al. (2012)
vitamin C, total soluble solid content, and dry matter Javanmardi et al. (2014)
percentage
Total sugar, proline, and chlorophyll concentrations Huang et al. (2020)
Chlorophyll, proline and carbohydrate concentrations, Hadian-Deljou et al. (2020)
sugar, and abscisic acid
Phenolics compounds Li et al. (2015)
2
O.C. Emmanuel and O.O. Babalola
secondary metabolites (phenolics, alkaloids, saponins, terpenes, lipids,
carbohydrates) are known to enhance both the taste and health-pro-
moting properties of crops (Schreiner et al., 2012) (Table 1).
Tomato is one of the health-promoting horticultural crops that is
widely consumed. It contains antioxidants like lycopene, β-carotene
ascorbic acid, vitamin E, etc., that neutralize dangerous free radicals in
the blood, reduce cholesterol and lower blood pressure (Bhowmik et al.,
2012). Tomato inoculated with AMF showed higher concentrations of
glucose, fructose, nitrate and malate (Copetta et al., 2011). Similarly,
AMF inoculation increased tomato fruit P, Zn and lycopene content up
to 60%, 28% and 18.5% respectively (Giovannetti et al., 2012).
Another beneficial effect of AMF is increased seedling survival and
establishment (Delian et al., 2011) since most horticultural crops are
raised in the nursery where AMF inoculation is carried out before
transplanting to the field. Increased uptake of nutrients facilitated by
AMF supports the seedling survival and establishment. Quality seedling
is a prerequisite for a healthy crop and good yield. Bettoni et al. (2014)
reported increased build-up of proteins, proline and soluble sugars on
onion leaves in plants inoculated with AMF, which also enhanced the
onion seedlings’ tolerance of environmental stresses and increased
growth. Inoculation of cucumber with Glomus mosseae and G. etuni-
catum stimulated seedling survival and growth with or without P2O5.
Inoculated cucumber plants had higher seedling survival rate, fruit
yield, P and Zn shoot concentration (Ortas, 2010). Arbuscular mycor-
rhizal fungi were also reported by Gavito et al. (2008) and Kumari et al.
(2017) to help in fruit seedling development and establishment. Fur-
thermore, they enhanced the fruit yield and quality, uniformity of fruit
crops, early and better flowering (Kumari et al., 2017). Early flowering
and maturing ensure early harvest which commands a higher market
price as reported in tomato production (Ortas et al., 2013).
Apart from the advantages mentioned above, AMF are needed to
lengthen the surface area around the roots for horticultural crops like
carrots that possess small root hairs (Dechassa et al., 2003). For in-
stance, heirloom carrot varieties inoculated with AMF in organic field
conditions grew heavier and longer carrots due to enhanced nutrient
uptake from the surface area (Keller-Pearson et al., 2020). Citrus plants
are also known to be highly dependent on AMF because they have few
root hairs (Wu et al., 2013). Verbruggen et al. (2013) pointed out that
inoculation with AMF is a viable option to increase AMF root coloni-
zation where it is not achieved with native AMF species. It may also be
more beneficial to develop indigenous mycorrhizal strains for improved
crop production than using exotic inoculants since some native strains
are sometimes as effective as exotic isolates (Pellegrino et al., 2011).
This can also forestall the antagonistic relationship between the in-
digenous strain and the introduced exotic strains. Ananthakrishnan
et al. (2004) selected three species of AMF associated with cashew for
inoculation. Out of these species, only one significantly increased
cashew growth indicators under greenhouse condition. This, therefore,
implies the need to screen and select suitable AMF for each crop for
optimal crop production where exotic strains are required. This agrees
with the report of Heneghan et al. (2008) that the use of AMF requires
an understanding of the complex ecological processes involving rhizo-
sphere organisms, plant growth and site‐specific environmental condi-
tions.
Arbuscular mycorrhizal fungi inoculation may not always be asso-
ciated with positive outcomes. Ibiremo et al. (2012) reported that the
inoculation of cashew with introduced AMF species may not be needed
since the native AMF species readily colonize the root cashew in the
investigated soil. The AMF inoculation did not have a significant effect
on biomass yield and uptake of N, P, K, Ca and Mg in cashew seedlings.
In fact, they were reported to have even suppressed N and P uptake in
one of the studied soil (Ibiremo et al., 2012). The success of mycorrhizal
inoculation is determined by the quality of the inoculums with high
numbers of infective AMF propagules and also significant nutrient
supply to the host plant (Baum et al., 2015). Thus far, the existing re-
sults on the use of AMF for perennial fruit trees are promising
3
Microbiological Research 239 (2020) 126569
(Ananthakrishnan et al., 2004) but require further and long term stu-
dies to identify additional influences.
Arbuscular mycorrhizal fungi also indirectly contribute to the nu-
tritional quality of crops by reducing the need for pesticide applications
since they enhance plant tolerance to pathogens and diseases (Wang
et al., 2011; Rouphael et al., 2015). Wang et al. (2011) further provided
evidence that AMF increased the yield of carrot and green onion and
decreased the concentration of organophosphorus pesticides in both
vegetables and soil. The health risks posed by residual effects of pes-
ticides in horticultural crops are eliminated or at least reduced to the
barest minimum. Arbuscular mycorrhizal fungi inoculation enhanced
physical quality by extending the shelf life of onions (Makus, 2020) and
produced firmer onion bulbs (Charron et al., 2001). The increased
firmness of the onions by AMF was probably induced by the formation
of calcium pectate which favours cells cementing action. Previously,
inoculant production was mainly for PGPB; however, in recent years
there has been commercial mycorrhizae inoculant production
(Rouphael et al., 2015).
3. Plant growth promoting bacteria and horticultural crop
production
Plant growth promoting bacteria are important to agricultural
production due to their ability to improve plant growth and increase
plant protection from diseases and abiotic stress like drought and sali-
nity (Glick, 2012; Numan et al., 2018). Plant growth promoting bac-
teria can either be found on the root surface (rhizosphere), leaf/stem
surfaces (phyllosphere) or interior parts of the plant (endophytic)
(Glick, 2014). In the soil, most species are found close to plant roots and
are collectively called plant growth promoting rhizobacteria (PGPR). As
a biostimulant, PGPB stimulate natural processes that increase plant
nutrient uptake and efficiency, abiotic stress tolerance and quality of
crops (Calvo et al., 2014). Plant growth promoting bacteria have also
been identified as a potential bioorganic component of nano-bio-
fertilizers which can increase plant growth and inhibit the growth of
parasitic fungi (Gouda et al., 2018).
3.1. Mechanism of action of plant growth promoting bacteria
Mechanisms of action through which PGPB facilitate plant growth
can either be direct or indirect. Direct mechanisms refer to the traits
that result in the direct promotion of plant growth. This could be by
providing beneficial compounds to host plants and facilitating nutrient
uptake from the soil. Indirect mechanisms refer to those traits that in-
hibit the functioning of one or more plant pathogenic organisms.
Different PGPB possess either or both traits and can differ in activities
under different environmental and soil conditions (Olanrewaju et al.,
2017). The various mechanisms utilized by PGPB for plant growth
promotion are illustrated in Fig. 1. These mechanisms may act in-
dependently or together to be beneficial to the plant (Zaidi et al., 2015).
Through these mechanisms, PGPB offer some benefits to horti-
cultural crops and assist in the uptake of both micronutrients and
macronutrients (Ramakrishna et al., 2019). Potassium is a key nutrient
that enhances the quality of horticultural crops. Some groups of PGPB
known as Potassium-solubilizing bacteria (KSB) can increase soil nu-
trient availability and plant growth by discharging K from insoluble
minerals into the soil (Meena et al., 2013). These bacteria release or-
ganic such as oxalic acid, gluconic acid, tartaric acids, citric acid, 2-
ketogluconic acid, succinic acid and malic acid, (Meena et al., 2014),
that either dissolve rock K or chelate silicon ions releasing K into soil
solution thereby making it available to plants (Parmar and Sindhu,
2013). It was shown that inoculating tomato with KSB increased the
available potassium in soils, leading to increased biomass accumulation
and nutrient uptake.
Phosphate solubilization is an indirect mechanism for plant growth
promotion by bacterial species. Phosphate solubilizing bacteria (PSB)
O.C. Emmanuel and O.O. Babalola
Fig. 1. Mechanism of action of plant growth promoting bacteria.
convert P that is insoluble to plant-available forms (Olanrewaju et al.,
2017). Phosphate solubilization is achieved through the secretion of
organic acids that leads to acidification of microbial cells and their
immediate environment leading to release of phosphate ions. Bacillus
subtilis showed significant prospects in phosphate solubilization, ACC
deaminase and acid phosphate activity (Latif Khan et al., 2016). It also
showed higher Indole Acetic Acid (IAA) production which led to in-
creased shoot and root biomass of tomato. The carotenoid and chlor-
ophyll contents of plants inoculated with B. subtilis were also more than
that of the control plants as reported by Latif Khan et al. (2016).
The co-inoculation of B. pumilus and B. subtilis by Pandey et al.
(2018) significantly increased various proximate constituents and es-
sential amino-acids of Amaranth grains. The percentage increase over
the control was crude protein (22.13%), dry matter (32.25%), fat
(30.77%), dry matter (32.25 %), fat (30.77%), and carbohydrate
(49.08%). The increase recorded for essential amino acids were me-
thionine (47.68%), lysine (59.41%) and tryptophan (38.05%). In-
creased protein and carbohydrate levels of Amaranthus hypochon-
driacus may be related to the fact that the Bacillus isolates facilitated
resource acquisition by plants. Enhanced N uptake aids protein synth-
esis while increased carbohydrate content is because solubilized nu-
trients are accumulated in the plants.
Furthermore, Heidari and Golpayegani (2012) inoculated basil
(Ocimum basilicum) with 3 PGPB (Pseudomonades sp., Bacillus lentus and
Azospirillum brasilens) species singly and in combination under water
stress. The antioxidant enzymes monitored are ascorbate peroxidase,
guaiacol peroxidase and catalase. The results revealed that inoculation
with all the bacteria species increased the antioxidant activity of basil
and photosynthetic pigments; however, the highest value (up to 50%
increase) was obtained from the combination of the three bacterial
species. Similarly, de Andrade et al. (2019) reported increased biomass
of strawberry following co-inoculation with 3 bacterial strains (Azos-
pirillum brasilense, Burkholderia cepacia and Enterobacter cloacae). The
authors attributed the positive result to the IAA produced by the bac-
terial strains. These results support the submission of Souza et al.
(2015) that inoculation with a consortium of bacteria is a promising
alternative to using single organisms due to the combined mechanisms
of each strain. On fruit quality, Pešaković et al. (2013) reported sweeter
strawberry fruit in PGPB inoculated plants. The increase in sweetness
index is attributed to the higher total sugar concentration which is fa-
cilitated by the modulation of photosynthesis and sugar (sucrose)
concentration of the fruit by PGPB through the control of the abscisic
acid level of the plant (Bona et al., 2015). Abscisic acid signalling path
is connected to sugar sensing levels in the plant. Sugars synthesized
through photosynthesis serve as signalling compounds in the growth
4
Microbiological Research 239 (2020) 126569
and development of plants, hence improving photosynthesis can be a
motivating factor for PGPB inoculation (Bailly and Weisskopf, 2012).
Berger et al. (2017) investigated how the PGPB Kosakonia radi-
cincitans affect tomato fruits and found that they increased the amino
acid, sugar, and volatile organic composition of ripened fruits. They
also accelerated ripening and contributed to a more pleasant-tasting
fruit without compromising the quality. Regulation of ethylene levels
by K. radicincitans could be responsible for the accelerated ripening. The
pleasant taste is associated with the interaction between sugar, acids
and volatile compounds of the tomato as affected by the PGPB. This is a
promising result as good quality tomato fruits command a higher
market price. PGPB has also been used during the post-harvest storage
of tomato fruits to ensure wholesomeness and extended shelf life.
Masmoudi et al. (2019) isolated 6 strains of halotolerant bacteria from
saline habitats belonging to the Bacillus genus with PGP properties. The
halotolerant bacterial species exhibited biocontrol activities against
grey mold disease of tomato fruits caused by Botrytis cinerea more than
2 commercial biofungicide tested. The inoculation of broccoli with
Bacillus cereus, Brevibacillus reuszeri and Rhizobium rubi led to an in-
crease in chlorophyll, N, K, Ca, S, P, magnesium (Mg), iron (Fe),
manganese (Mn), Zn and Cu contents (Yildirim et al., 2011). The
chlorophyll content correlated with total N concentration of broccoli.
This could be attributed to the promotion of N uptake by PGPB. The
crop yield also increased by 17.0%, 20.2% and 24.3% while the
chlorophyll content increased by 14.7%, 14.0% and 13.7% in treat-
ments inoculated with B. cereus, R. rubi and B. reuszeri, respectively.
They further showed that there could be a 50% reduction in the
quantity of chemical fertilizer used when PGPB were used together with
manure.
Unlike annual horticultural crops, fruit trees and grapes are per-
ennial crops with massive root systems. This makes inoculation with
PGPB difficult, especially in mature plants. The root inoculation with
PGPB is normally done at the seedling stage before or at transplanting.
However, most of these perennial fruit crops are propagated vegeta-
tively, hence the use of foliar application of PGPB. Studies have shown
that bacteria genera like Agrobacterium, Pseudomonas, Bacillus,
Alcaligenes and Streptomyces might induce root formation in stem cut-
tings for vegetative propagation (Köse et al., 2003; Pırlak and Köse,
2009). Production of auxin, ethylene, and cytokinin by PGPB induce
and promote root hair elongation (Zhang et al., 2016b).
Plant growth promoting bacteria produce growth factors that inhibit
competitors and antagonists. In soil, they accomplish this through an-
tagonism, competition, and antibiotics production. They also induce
disease resistance and promote plant growth by improving nutrient
uptake by altering plant hormone levels (Anith et al., 2004). These
O.C. Emmanuel and O.O. Babalola
Fig. 2. Schematic drawing representing the interactions of Arbuscular mycor-
rhizal fungi and plant growth promoting bacteria in the rhizosphere.
microorganisms modify the plant microbiome and also alter the entire
activities of microbes found in the rhizosphere and within plant tissues
(del Carmen Orozco-Mosqueda et al., 2018), which together favour the
germination of AMF propagules. The success of PGPB inoculants,
however, depends on their ability to colonize plant root, plant root
exudates and the capacity of the soil sustain organisms (Souza et al.,
2015).
4. Interactions between arbuscular mycorrhizal fungi and plant
growth promoting bacteria
Interactions between AMF and PGPB in the rhizosphere can result in
synergistic effects which enhance plant growth and quality as shown by
Khalid et al. (2017) and Bona et al. (2017) (Fig. 2). Though the parti-
cular mechanism by which AMF and PGBP interact and stimulate the
beneficial effects of each other is still largely unknown, recent studies
have tried to explain some possible mechanisms. Artursson et al. (2006)
rightly pointed out that both organisms promote plant growth through
enhanced plant nutrition and inhibition of fungal plant pathogens.
Some PGPB are sometimes called “mycorrhiza helper bacteria”
(MHB) due to their ability to stimulate the growth of AMF hyphae
thereby facilitating root penetration (Xie et al., 2018). Selvakumar et al.
(2016) observed that Gram-positive bacteria are linked to AMF (Fun-
neliformis caledonium, Racocetra alborosea and F. mosseae) spores more
than Gram-negative bacteria, hence the name spore associated bacteria
(SAB). For example, Mohandas et al. (2013) isolated actinomycetes
(Gram-positive) with plant growth promoting (PGP) potentials from G.
mossae cohabiting the guava rhizosphere. Battini et al. (2017) however
isolated a mixture of Gram-positive and Gram-negative bacterial strains
from R. irregularis spores amongst which Actinobacteria, Bacillaceae
and Sinorhizobium meliloti strains that exhibited some PGP activities like
P mineralization from phytate and P solubilization. Ortaş et al. (2017)
also identified some Gram-negative bacterial genera that have been
noted for their interaction with AMF for instance Proteobacteria
(Agrobacterium, Azotobacter, Azospirillum, Bradyrhizobium, Burkholderia,
Enterobacter, Pseudomonas and Rhizobium). It can be deduced that AMF
hyphae associates with both Gram-positive and Gram-negative PGPB
that are compatible.
Antagonistic interactions have been reported where the positive
effect on one is suppressed by the other (Johansson et al., 2004;
Svenningsen et al., 2018). Arbuscular mycorrhizal fungi sometimes
alter the PGPB community in the rhizosphere through competition for
food (Miransari, 2011). In certain circumstances, the PGPB may not act
as a MHB, however, they will not inhibit the role played by AMF in
5
Microbiological Research 239 (2020) 126569
plant growth promotion (Todeschini et al., 2018). Alongside these ef-
fects of PGPB on AMF, AMF also are involved in structuring the com-
position of bacterial communities due to their carbon-rich exudates in
the rhizosphere, which are a nutrient source to PGPB (Priyadharsini
et al., 2016). Zhang et al. (2016a) stated that when AMF releases the
carbon obtained from a plant, the bacteria (mostly PSB), reciprocate by
mineralizing organic P into the rhizosphere, which is utilized by the
AMF. Working on Medicago sativa, Zhang et al. (2014) reported that
Pseudomonas alcaligenes, a PSB associated with Rhizophagus irregularis
hyphae, was instrumental in phytate P mineralization, while R. irregu-
laris applied priming effects on the mineralization and turnover of
phytate in the soil. R. irregularis cannot utilize phytate directly due to its
inability to secrete phytases (Tisserant et al., 2013). It rather depends
on the PGPB. Additionally, sole inoculation of P. alcaligenes (Zhang
et al., 2014) increased the concentration of microbial P but not when
co-inoculated with R. irregularis. This may be facilitated by the AMF
hyphal exudates such as sugars and carboxylates that can be used by
bacteria as a source of carbon resulting in the alteration of the bacterial
composition in the rhizosphere (Zhang et al., 2016a). These sugars and
carboxylates are released at different concentrations into the soil,
however, each bacterial isolate has a preference for some sugars more
than others (Zhang et al., 2019). Zhang et al. (2018) further demon-
strated that fructose released by R. irregularis was not just a carbon
nutrient source for the bacteria; it also prompted the expression of
phosphatase genes of the R. aquatilis, thereby encouraging synergic
interaction between the two microorganisms.
Arbuscular mycorrhizal fungi also improve efficient phosphatase
secretion to the rhizosphere via regulation of protein secretory systems
in the bacteria. Similarly, the presence of the bacteria improves the
process of phosphate transfer in the hyphae of the AMF. Further re-
search is required to determine if other compounds apart from sugar,
such as carboxylates and amino acids found in AMF hyphal exudates
help in the release of inorganic P by PGPB. Zhang et al. (2019) also
showed that R. irregularis encourages the expression of gene-encoding
citrate synthase, an enzyme important in the tricarboxylic acid (TCA)
cycle, hence the level of Adenosine Triphosphate (ATP) production in
Rahnella aquatilis. This was beneficial to R. aquatilis as its activity de-
pends on ATP produced during the TCA cycle and the increase in ATP
encourages the activity of the bacteria.
In some cases, AMF have also been reported to work synergistically
with symbiotic and asymbiotic N fixing bacteria. With symbiotic N
fixers, there is improved nodulation and AMF root colonization, with
significant benefit to plant growth (Xavier and Germida, 2002). Ar-
buscular mycorrhizal fungi enhance P availability which is crucial for
nodulation and also supply photosynthates (Desai et al., 2016). Ar-
buscular mycorrhizal fungi interactions with free-living bacteria have
been documented. Khalid et al. (2017) reported that the synergy be-
tween AMF (Glomus fasciculatum, G. mosseae) and PGPB (Azotobacter
chroococcum, Bacillus mucilaginous and B. megaterium) increased root
colonization of spinach by AMF.
The presence of these beneficial bacteria stimulated the germination
of the fungal spores thereby giving it a better chance to colonize plant
roots. This could be explained by the ability of the bacteria to decom-
pose insoluble biopolymers like chitin and chitosan, the two major
components of AMF spore walls, thus enhancing germination (Turrini
et al., 2018). To further understand this tripartite relationship that
exists between AMF, PGPB and plants, there is a need to understand the
extent to which mycorrhizae associated with bacteria participate in
plant nutrition and nutrient flows.
5. Co-inoculation of arbuscular mycorrhizal fungi and plant
growth promoting bacteria for horticultural crops
Many studies have identified co-inoculation of AMF and other
beneficial microorganisms like fungi (e.g. Trichoderma sp.) and bacteria
as a promising tool and a viable method for sustainable crop production
O.C. Emmanuel and O.O. Babalola
(Baum et al., 2015). The cooperation of plant roots, bacteria and my-
corrhizae in the rhizosphere for plant growth promotion, nutrient up-
take and plant protection, is referred to as tripartite association (Ortaş
et al., 2017; Kothe and Turnau, 2018).
The Co-inoculation of AMF and PGPB was reported to have in-
creased the growth and yield of alfalfa more than the sole inoculation of
each organism and provided the plants with better nutrition and im-
proved nutrient uptake (Zhu et al., 2016).
Todeschini et al. (2018) differentiated the role played by AMF and
PGPB in promoting the yield and fruit quality of strawberry. The AMF
enhanced the vegetative growth parameters while the PGPB increased
the fruit yield and quality. Bona et al. (2017) assessed the effects of two
Pseudomonas strains and AMF on tomato fruits in the field which re-
ceived less fertilizer and got positive results. Both organisms worked
synergistically to improve fruit production, fruit sugar and vitamin
concentration in comparison to the control treatment. Arbuscular my-
corrhizal fungi improved the concentration of citric acid, while PGPB
positively regulated sugar production and the sweet taste of the toma-
toes. According to Bona et al. (2017), PGPB could control photo-
synthesis and sugar concentration, regulating the plant abscisic acid. In
an earlier work by Bona et al. (2015) on another tomato variety, the
inoculation with AMF and PGPB significantly increased fruit size (both
length and diameter) and weight, making it more marketable with high
economic returns. This could be due to the influence of AMF and PGPB
on plant nutrient balance and hormone production, as pointed out by
Torelli et al. (2000) and Boldt et al. (2011). The inoculation of straw-
berry plants with a group of AMF (Rhizophagus intraradices, Glomus
aggregatum, G. viscosum, Claroideoglomus etunicatum, and C. claroideum)
and Pseudomonas sp, under reduced fertilization, resulted in early
flowering and fruiting, increased yield, and nutritional content. The
fruits of inoculated plants were also heavier and longer. Pseudomonas
sp. could have produced auxins and gibberellins which favour flowering
and fruiting (de Jong et al., 2010).
The levels of total phenolic compounds, flavonoids and phenolic
acid contents of spinach were increased significantly more by co-in-
oculation of AMF and PGPB than the sole inoculation of either (Khalid
et al., 2017) (Table 2). Thilagar et al. (2016) assessed the option of
reducing chemical fertilizer application on chilli using Funneliformis
mosseae and Bacillus sonorensis in a farmer's field. The results indicated
that the recommended NPK fertilizer application rate could be reduced
by half through inoculation with a consortium of microbes without any
detrimental effect on the growth, nutrition, and yield of chilli. The re-
sult further showed that the activities of soil enzymes and soil organic
carbon were also improved in the inoculated plot with half of the fer-
tilizer treatment. Abd-Alla et al. (2014) reported that in alkaline soil,
the dual inoculation of Rhizobium leguminosarum and AMF consortia
(Acaulospora laevis, G. mosseae, G. geosporum and Scutellospora armeniac)
improved the nodulation and N fixation of faba bean. Alkaline soils
inhibit nodulation and consequently plant growth and yield. Increased
nodulation could be due to the ability of AMF to enhance uptake of Fe
and P involved in the biosynthesis of nitrogenase and leghaemoglobin.
The synergetic/antagonistic impact of microbial inoculants is
usually due to the characteristics and compatibility of the microbial
strains involved along with the interactions that occur between the
PGPB, AMF and plant species. Some functions of PGPB like mobilization
of nutrients from soil minerals, N fixation and plant protection against
root pathogens also enhance the synergic relationship between the two
organisms. For example, the co-inoculation of G. mosseae and Bacillus
sp. on tomato provided greater control of root-knot nematode leading
to the better plant growth promotion than single inoculations (Liu et al.,
2012).
5.1. Factors that affect the performance of co-inoculation of arbuscular
mycorrhizal fungi and plant growth promoting bacteria
The efficiency of inoculation depends on soil nutrient content, type/
6
Microbiological Research 239 (2020) 126569
specie of crop and competition with native strains. To get the maximum
benefits of AMF and PGPB associations, these factors must be con-
sidered. Intensive agricultural production has also been found to be
negatively associated with microbial growth. Native forest soils host
more AMF species than cultivated soils (Chiomento et al., 2019). The
decreased species and population of AMF in cultivated soil could be due
to the high input of inorganic fertilizers, pesticides, and herbicides
Rouphael et al. (2015).
Tillage and frequent fallow periods decrease the abundance of vi-
able AMF propagules (Schnoor et al., 2011) due to the disruption of the
mycelial network and reduction of host plant during the fallow period.
Another factor is the ability of the introduced organisms to compete
with the indigenous population of both bacteria and mycorrhizae for
survival (Lesueur et al., 2016). For maximum effectiveness, location-
specific microbial strains need to be identified for the specific climate
(Fischer et al., 2007). Drigo et al. (2008) identified that the diversity
and activities of PGPB are substantially impacted by climate change.
Tabassum et al. (2017) also noted that an increase in temperature might
lead to changes in the physiology of the plant and root exudates. This
may lead to variations in composition, profusion, viability, and activ-
ities of the microbial communities associated with plants since roots
exudates play a major role in the recruitment of rhizosphere organisms.
Abiotic stresses may also lead to the impairment of the beneficial effects
of these microorganisms. Conditions like salinity, drought and soil
pollution are all responsible for the inability of the microorganisms to
exhibit their desirable traits (Tabassum et al., 2017).
5.2. Challenges of Co-inoculation of arbuscular mycorrhizal fungi and plant
growth promoting bacteria
The major constraint for the use of biofertilizers is that their effects
in the field and laboratory conditions often vary. This could be due to
the fact that plant-microbe interactions in the rhizosphere are active,
complex and sometimes difficult to manage (Aeron et al., 2011). The
effect of PGPB on plant growth either directly or indirectly differs from
species to species up to strain level (Aeron et al., 2011). Arbuscular
mycorrhizal fungi have also been reported to differ even at the strain
level (Li et al., 2007). It is, therefore, necessary to identify efficient
strains for real conditions which are well adapted to a particular en-
vironment. It is also important to comprehend the interaction between
PGPB and associated plants and how the beneficial attributes of PGPB
are altered by various biotic and abiotic soil factors. Efforts are also
needed to identify PGPB strains with multiple growth promoting
properties that will be specific for horticultural crops. It is also neces-
sary to understand the ability of PGPB species to persist in the soil and
plant tissue to determine the application rate and frequency for optimal
growth and yield of crops.
Arbuscular mycorrhizal fungi, on the other hand, are sensitive to
physical, chemical and biological changes due to human activities
which impede their establishment (Verzeaux et al., 2017). Liu et al.
(2016) identified that AMF are controlled by soil P status, and root
colonization, therefore, has an inverse relationship with soil available P
and plant P nutrition. Bonneau et al. (2013) rightly pointed out that
high concentrations of N and P can limit mycorrhizal colonization.
Microbial inoculation should be complemented with agronomic prac-
tices that are favourable to their establishment to maximize the bene-
fits. Cover cropping and reduced tillage are reported to increase root
colonization of annual crops by AMF (Lehman et al., 2019).
The Inoculation of plants with AMF can be carried out in the
greenhouse under controlled environment or in the field (Igiehon and
Babalola, 2017). However, the large scale inoculation of AMF in the
field is cumbersome (Alori et al., 2017) and pure AMF strains are not
easily achieved because they are obligate symbionts and cannot be
grown or cultured in the laboratory (Igiehon and Babalola, 2017).
Some plants are colonized by the AMF only when co-inoculated
with PGPB, while some are colonized with sole AMF application but
 O.C. Emmanuel and O.O. Babalola

Table 2
Benefits of co-inoculation of arbuscular mycorrhizal fungi and plant growth promoting bacteria on Horticultural Crops.
Crop AMF PGPB Effects on plants Reference

Tomato R. intraradices, R. aggregatum, Eptoglomus viscosum, Pseudomonas sp, P. fluorescens Enhanced flowering and fruiting increased levels of sugars and vitamins in the tomato Bona et al. (2017)
Claroideoglomus etunicatum, C. claroideum fruits. Bona et al. (2018)
Increased fruit β-carotene concentration, reduction of chemical fertilizer, improved
fruit quality
Glomus intraradices Bacillus amyloliquefaciens, Improved nutrient acquisition and healthy plant growth Yusran et al. (2009)
Pseudomonas sp
Strawberry G. aggregatum, G. mosseae, G. intraradices Pseudomonas sp, P. fluorescens Increased concentration of anthocyanins in strawberry fruits and reduced fertilizer Lingua et al. (2013)
application
F. mosseae, Septoglomus Pseudomonas sp Increased concentration of Todeschini et al.
viscosum, and R. irregularis sugar and anthocyanidin, controlled pH, malic acid, volatile compounds, and elements (2018)

7
R. intraradices, G.aggregatum, G. viscosum, Claroideoglomus Pseudomonas sp Increased flowering, fruiting and bigger fruit size, and increased concentrations of Bona et al. (2015)
etunicatum, and C. Sugars, ascorbic and folic acid
claroideum)
Sunflower Haematophilum, R. irregularis Chryseobacterium humi, Ochrobacterium Higher biomass production, increased uptake of K+, Mg2+, Ca2+, N and P, reduced Pereira et al. (2016)
haematophilum Na + contents in tissues and enhanced plant antioxidative response.
Trifoliate orange R. intraradices, P. mucilaginosus Improved plant growth, root morphology. Increased leaf chlorophyll, root activity, Wang et al. (2017)
anti-oxidative enzymes levels. Mitigating the stress of low P levels.
Basil G. intraradices Dietzia natronolimnaea Increased biomass and yield, increased quantity and quality of essential oil, Bharti et al. (2016)
amelioration of salinity stress, increased shoot and root N, P, K and Ca content.
Lettuce G. mosseae P. mendocina Enhanced plant biomass under saline stress. Kohler et al. (2010)
Spinach G. fasciculatum, G. mosseae, Azotobacter chroococcum, B. mucilaginous, Chlorophyll, flavonoid, phenolic acids and total phenolic compounds Khalid et al. (2017)
B. megaterium
Rose Geranium G. aggregatum, G. fasciculatum, G. intraradices and G. Bacillus subtilis Increased biomass production. Alam et al. (2011)
mosseae
Red pepper Acaulospora longula, G. clarum and G. intraradiaces. Methylobacterium oryzae Increased uptake of N, P, K, Ca, Zn, Cu and Fe and chlorophyll content Kim et al. (2010)
Microbiological Research 239 (2020) 126569
O.C. Emmanuel and O.O. Babalola
more efficiently colonized when AMF are co-inoculated with PGPB. In
both cases, PGPB is indispensable in the tripartite relationship as its
presence determines the success or failure of AMF root colonization.
The synergistic and antagonistic response of the interactions of both
organisms is determined by the characteristics of microbial strains and
plant species involved in these interactions. Such negative interactions
could be as a result of the incompatibility and/or pathogenicity of one
organism to the other as identified by Li et al. (2007). It is therefore
vital to pick the best combination of microorganisms to use for co-in-
oculation. The "best combination" should be determined based on the
time and method of inoculation, host plant, pathogen, and ecological
conditions (Liu et al., 2012). It has been established that plants shape
the microbial composition of the rhizosphere, as different crops on the
same piece of land recruit different microbial communities (Jambon
et al., 2018). It is also important to ensure the purity of AMF inoculant
and control the likely presence of pathogens that could be a potential
threat to plants (Berruti et al., 2016). There are many commercially
available bio-fertilizers of AMF and PGPB singly or combined, however,
the survival of the inoculants during storage and their effectiveness still
pose a challenge (Ma, 2019). Agnolucci et al. (2018) explored the
bacterial metagenome in a commercial AMF (Rhizophagus irregularis)
inoculum using Illumina high-throughput sequencing and found diverse
bacterial communities with PGP properties. This affirms earlier reports
that PGP bacterial communities are present in the spores of native AMF
(Agnolucci et al., 2015; Bidondo et al., 2016). Battini et al. (2016) re-
ported that some of the PGP bacterial communities found in commer-
cial AMF inocula still retain their growth promoting properties in their
various life cycles. Since viable PGPB can be obtained in AMF inocula
without inhibiting the activities of the AMF, pure cultures of such
bacterial species could be co-inoculated with the AMF for sustainable
horticultural production, thereby reducing the use of agrochemicals
(Agnolucci et al., 2018). It has also been observed that interactions of
both organisms differ among species and PGPB may react differently
with various AMF species (Nadeem et al., 2014). It is therefore im-
portant to assess and pick the best combination of microorganisms to be
used as an inoculant to promote synergy among the organisms.
6. Conclusions and future perspectives
Current data has suggested some mechanisms used by AMF when
co-inoculated with PGPB. The mechanisms translate to plant growth
promotion evidenced by increased yield and crop quality. There is still a
gap in understanding the exact mechanism and nature of the interaction
between both organisms; how the interactions of both organisms
combine in the enhancement of the health-promoting phytochemicals
of horticultural plants. It is also imperative to identify and use species
that are compatible with each other for specific/suitable host plants.
Both organisms are economical and environmentally friendly, unlike
the continuous application of chemical fertilizers and agro pesticides.
Future research studies should aim at (i) further understanding of the
roles played by AMF and PGPB in this tripartite relationship for plant
growth promotion (ii) identifying compatible organisms that will work
synergically to promote plant growth (iii) scaling-out the use of in-
oculants that contain both organisms in large fields and (iv) under-
standing the way these organisms will work in a mixed cropping system
that characterizes African smallholder farmers.
Declaration of Competing Interest
None.
Acknowledgments
OCE received a postdoctoral fellowship from the North-West
University. OOB is grateful to the National Research Foundation, South
8
Microbiological Research 239 (2020) 126569
Africa for the grant (Unique Grant No: 123634) received.
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