agronomy

Review
Plant Growth Stimulation by Microbial Consortia
Gustavo Santoyo 1, * , Paulina Guzmán-Guzmán 1 , Fannie Isela Parra-Cota 2 , Sergio de los Santos-Villalobos 3 ,
Ma. del Carmen Orozco-Mosqueda 4 and Bernard R. Glick 5

1 Instituto de Investigaciones Químico Biológicas, Universidad Michoacana de San Nicolás de Hidalgo,

Morelia 58030, Michoacán, Mexico; paulina_gzmn2@yahoo.com
2 Campo Experimental Norman E. Borlaug, INIFAP, Norman E. Borlaug km. 12,
Ciudad Obregón 85000, Sonora, Mexico; parra.fannie@inifap.gob.mx
3 Instituto Tecnológico de Sonora, 5 de febrero 818 sur, Ciudad Obregón 85000, Sonora, Mexico;
sergio.delossantos@itson.edu.mx
4 Facultad de Agrobiología “Presidente Juárez”, Universidad Michoacana de San Nicolás de Hidalgo,
Uruapan 60170, Michoacán, Mexico; del.orozco@umich.mx
5 Department of Biology, University of Waterloo, Waterloo, ON N2L 3G1, Canada; glick.bernard@gmail.com
* Correspondence: gsantoyo@umich.mx; Tel.: +52-4433265788

Abstract: Plant-associated microorganisms play an important role in agricultural production. Al-

though various studies have shown that single microorganisms can exert beneficial effects on plants, it
is increasingly evident that when a microbial consortium—two or more interacting microorganisms—
is involved, additive or synergistic results can be expected. This occurs, in part, due to the fact that



multiple species can perform a variety of tasks in an ecosystem like the rhizosphere. Therefore,


the beneficial mechanisms of plant growth stimulation (i.e., enhanced nutrient availability, phyto-
Citation: Santoyo, G.;
hormone modulation, biocontrol, biotic and abiotic stress tolerance) exerted by different microbial
Guzmán-Guzmán, P.; Parra-Cota, F.I.;
players within the rhizosphere, such as plant-growth-promoting bacteria (PGPB) and fungi (such as
Santos-Villalobos, S.d.l.;
Trichoderma and Mycorrhizae), are reviewed. In addition, their interaction and beneficial activity are
Orozco-Mosqueda, M.d.C.; Glick, B.R.
Plant Growth Stimulation by
highlighted when they act as part of a consortium, mainly as mixtures of different species of PGPB,
Microbial Consortia. Agronomy 2021, PGPB–Mycorrhizae, and PGPB–Trichoderma, under normal and diverse stress conditions. Finally, we
11, 219. https://doi.org/10.3390/ propose the expansion of the use of different microbial consortia, as well as an increase in research on
agronomy11020219 different mixtures of microorganisms that facilitate the best and most consistent results in the field.

Academic Editors: José Keywords: biotic and abiotic stress; sustainable agriculture; plant-growth-promoting bacteria;
David Flores-Félix, plant microbiome
Encarna Velazquez and
Fernando González-Andrés
Received: 24 December 2020
Accepted: 21 January 2021
1. Introduction
Published: 24 January 2021
Today, there is a need to produce enough food for the more than 7 billion people
on the planet, and it is expected that by the year 2050, the global population will reach
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
~9.5 billion [1]. Moreover, in 2020, it was estimated that ~900 million people were malnour-
published maps and institutional affil-
ished. For decades, the indiscriminate use of agrochemicals (mainly chemical fertilizers
iations. and pesticides) in agriculture to increase production and/or decrease the constant threat
of infections caused by plant pathogens has led to a loss of plant health. Unfortunately,
the ways in which the production of the various agricultural systems has increased in the
vast majority of countries is not sustainable [2]. Agricultural soils, directly or indirectly,
are continuously losing their quality and physical properties (soil texture, permeability,
Copyright: © 2021 by the authors.
porosity, and drainage), as well as their chemical (imbalance of nutritive elements) and
Licensee MDPI, Basel, Switzerland.
This article is an open access article
biological (beneficial organisms) health [3]. In the case of the soil microbiota, some authors
distributed under the terms and
have shown that pesticides can decrease their abundance and diversity, leading to an
conditions of the Creative Commons impairment of their functioning in agro-systems [2–4]. Pesticides also negatively impact
Attribution (CC BY) license (https:// other beneficial organisms in agriculture, such as pollinating insects, which are important
creativecommons.org/licenses/by/ in improving the production of several crops [5,6]. In certain regions of the world, attempts
4.0/). have been made to reduce or eliminate the use of potentially deleterious agrochemicals,

Agronomy 2021, 11, 219. https://doi.org/10.3390/agronomy11020219 https://www.mdpi.com/journal/agronomy

Agronomy 2021, 11, 219 2 of 24

mainly due to their risk to human health, but in many developing countries, they continue
to be used without any type of regulation [7].
There is a pressing need for approaches that facilitate food production without the
excessive use of agrochemicals and for the use of genetically improved crops, including
selection of plant varieties that are resistant to pests and various adverse environmental
conditions [8]. Much of this may be achieved by the genetic modification of plants [9,10]
and/or the application of plant-growth-promoting microorganisms [11–15]. In some cases,
using a mixture of two or more compatible microorganisms of different species (or strains)
can facilitate beneficial additive or synergistic results, since the lack of activities in one
added microbe can be found through the action of the other [16]. Here, it is important
to define these two concepts in the context of this work. An additive effect is the sum of
activities, while synergy refers to an effect that goes beyond the sum of individual actions,
since there is a stimulation of one action (or microorganism) by another.
These new “plant microbiome engineering” approaches, consisting of adding effec-
tive bioinoculants, induce new structured biological networks in diverse soil types. This
promotes the recovery of functional, beneficial microbial groups that are positively linked
to soil fertility and replenishes the natural microbiome, which has been reduced by crop
domestication practices. The addition of microbial consortia, therefore, can restructure
and stimulate plant-growth-promoting mechanisms in both optimal conditions and under
different types of biotic and abiotic stress [17]. Here, the strategy of designing microbial
consortia between bacteria, Trichoderma, and/or arbuscular mycorrhizae fungi to stimu-
late plant growth is reviewed; this is a strategy that is expected to significantly increase
agricultural productivity.

2. Plant-Growth-Promoting Microorganisms
Plant-growth-promoting microorganism (PGPM) is a term that applies to all microor-
ganisms (e.g., bacteria, actinomycetes, fungi, and algae) that have a beneficial effect on
plant growth through the action of either direct or indirect mechanisms (e.g., mineral
nutrition, ethylene reduction, disease suppression) [18]. PGPMs have a significant role in
sustainable agriculture. They increase the production of various crops, improve soil fertility,
promote diversity and interaction with other beneficial microorganisms, inhibit the growth
and infective action of potential pathogens, and generally maintain the sustainability of
the systems [18,19].
Most studies of PGPMs are based on interactions of single microorganisms with
plants, evaluating different parameters of growth and plant health, such as length or
weight of the plant or its individual tissues, chlorophyll content, or the nutritional content
of its tissues or fruits [18,20–22]. This has led to a better understanding of plant–microbe
interactions, but leaves aside the “real” factor of these interactions in the environment,
where a multiplicity of microbial species can exist. For example, one gram of soil typically
contains a wide range of organisms, including bacteria (∼9 × 107 cells per g), actinomycetes
(∼4 × 106 cells per g), fungi (∼2 × 105 cells per g), algae (3 × 104 cells per g), protozoa
(∼5 × 103 animals per g), and nematodes (∼3 × 101 animals per g) [23]. From this diversity
of organisms, several species can occupy different niches and multiple interactions can take
place. The plant influences the interactions in the rhizosphere, since, through the exudation
of compounds (e.g., sugars, amino acids, and organic acids), new battles for nutrient
acquisition, colonization of spaces, and survival are generated. It has been suggested that,
due to the plethora of interactions that can occur when single species are inoculated in the
field, positive and consistent results in terms of facilitating plant growth are not always
achieved [24]. However, more consistent positive results may be obtained by inoculating
plants with microbial consortia containing two or more beneficial microorganisms [25,26].
Following seed germination, plants continuously interact with microorganisms that
reside both below and aboveground. These interactions are dynamic and change depending
on the microbial structure that is formed during the different stages of plant growth and
development [27,28]. In part, this dynamic is due to the volatile compounds emitted by the
Agronomy 2021, 11, 219 3 of 24

aerial parts of the plant as well as root exudates that are secreted into the soil, attracting
and structuring a particular rhizospheric microbiome [28]. Other abiotic factors can also
influence the interactions that occur between the soil microbiome and plants, including
temperature, water availability, pH, and the availability of nutrients [29]. Under natural
conditions, where the environment is continuously changing, plants communicate with
multiple microbial species, and in turn, these microbes communicate with each other to
give rise to networks that can have beneficial (or harmful) repercussions for plant growth,
thus shaping a plant microbiome [30,31].
Various studies have suggested that microbial consortia can generally perform tasks
better than individual strains. This includes metabolizing complex compounds, carrying
out reactions with two or more steps, degrading plant polymers such as cellulose, and
remaining stable in a fluctuating environment. Some of these activities are not resident in a
single microorganism; therefore, the use of microbial consortia is necessary [32].
The first commercialized bioinoculants included single biological agents [33], such
as rhizobial bacteria, which can form nodules on the roots of legume plants and therein
fix atmospheric nitrogen, facilitating plant growth and development. Unfortunately, the
effectiveness of this type of bioinoculant is limited in that it can only benefit legumes.
In some instances, legumes, such as Phaseolus vulgaris (bean), are co-cultivated with
non-legumes, such as Cucurbita pepo (zucchini) or Zea mays (maize). In these instances, the
application of a bacterial consortium, such as Rhizobium plus Pseudomonas or Bacillus, or a
bacterial-fungal consortium, such as Rhizobium plus Trichoderma or a mycorrhizae strain,
could benefit the three above-mentioned vegetable crops. This increase in plant growth
might occur through provision of a better supply of assimilable nutrients (such as P, Fe,
and N) [34,35].
Bioinoculants based on microbial consortia may include bacteria of different species,
while others may include both beneficial bacteria and fungi. The application of different
PGPM species with diverse mechanisms of action should provide a wide spectrum of
benefits for the plant, including direct stimulation of its growth and health, as well as
increases in production. In addition, a decrease in diseases caused by pathogens would be
expected [36,37].

3. Bacterial Consortia
Currently, synthetic fertilizers are applied to crops on a large scale to meet the growing
global food demand, leading to high health, economic, and environmental costs [38]. A
well-studied and sustainable alternative for improving plant growth and soil fertility is the
application of plant-growth-promoting bacteria (PGPB), which possess functional traits
that regulate the growth, development, and productivity of crops. These growth-promoting
effects are due to the improvement of the availability and biosynthesis of several limiting
macro- and micronutrients, as well as crop protection against stressful environmental
conditions [15,39].
In recent years, the impact of numerous PGPB strains on plants has been well explored,
leading to the commercialization of a large number of microbial inoculants [40,41]. To
enhance the beneficial functions displayed by these bacteria, the design of bacterial consor-
tia has gained interest as a suitable strategy for sustainable food production. A bacterial
consortium generally constitutes two or more compatible bacteria of different species in
a synergistic or additive interaction [42–44]. In some cases, a mixture of different strains
of the same species can exhibit enhanced activities and also be considered a consortium.
Bacterial consortia have been reported to improve beneficial traits in plants in comparison
to individual strains due to the coverage of a diverse set of plant growth promotion and
biological control mechanisms [45]. The use of these consortia is a feasible strategy for
ameliorating drought [46], salinity [47], nutrient uptake [48], pests, and phytopathogenic
infections [49] of agricultural crops. In addition, some bacterial consortia can fix nitrogen,
transform some unavailable nutrients into an assimilable form, produce phytohormones,
nomy 2021, 11, x FOR PEER REVIEW 4 of 26

strategy for ameliorating drought [46], salinity [47], nutrient uptake [48], pests, and phy-
Agronomy 2021, 11, 219 4 of 24
topathogenic infections [49] of agricultural crops. In addition, some bacterial consortia can
fix nitrogen, transform some unavailable nutrients into an assimilable form, produce phy-
tohormones, and chelate iron, which is important in maintaining soil quality and health;
these can alsoandreduce
chelatetheiron,
negative
whicheffects of someinconventional
is important maintaining non-sustainable agricul-these can also
soil quality and health;
tural practices [50]. the negative effects of some conventional non-sustainable agricultural practices [50].
reduce
There are twoThere
typesareof two
bacterial
typesconsortia
of bacterialknown—simple and complex. The
consortia known—simple and differ-
complex. The dif-
ences are theferences
fermentation
are thestrategy or protocol
fermentation (production
strategy of a (production
or protocol large population of bac-
of a large population of
teria to be later formulated
bacteria into formulated
to be later an inoculant), intowhere strains are
an inoculant), grown
where individually
strains are grown or individually
in or
combination in with other species/strains in a suitable medium for all PGPB species
combination with other species/strains in a suitable medium for all PGPB species [51]. [51].
This is an important
This is anstage, since astage,
important highersince
number of species
a higher number generally
of species results in a higher
generally results in a higher
number of interactions
number of among the strains,
interactions amongtherefore generating
the strains, thereforedifferences
generatingindifferences
metabolitein metabolite
secretions. On secretions.
the other On thethe
hand, other hand,ofthe
success successconsortia
bacterial of bacterial consortia
under under fieldisconditions is
field conditions
dependent ondependent
the type and on the type and
function function
of strains of strains
used, where used,
some where
aspectssome
requireaspects require special
special
attention,
attention, including includingto
adaptation adaptation to adverse
adverse climatic climatic conditions,
conditions, survival, and survival, and persistence in
persistence
theinoculation
in the soil after soil after inoculation
[50,52]. [50,52].
The selectionThe selection
of these of these
strains strains isupon
is dependent dependent uponofthe
the source thesource
strain of the strain isolation,
isolation,
sincemembers
since consortium consortium needmembers need to
to proliferate inproliferate in the environmental
the environmental conditions (soil conditions
type, (soil type,
climate, and climate,
host) whereand they
host) will
wherebe they will In
applied. beaddition,
applied. itInisaddition,
important it is
to important
note that, to note that,
when two or when two or are
more strains more strains
part are part of
of a bacterial a bacterial each
consortium, consortium,
strain noteach
onlystrain not only competes
competes
functionally with the others for plant growth promotion, but also complements the others the others
functionally with the others for plant growth promotion, but also complements
for soil and/orforplant
soil and/or plant establishment
establishment [53–55]. Figure [53–55]. Figure 1 the
1 summarizes summarizes
different the different
types of types of
microbial consortia discussed
microbial consortia discussed in this manuscript. in this manuscript.

Figure 1.
Figure 1. Microbial MicrobialRhizosphere
consortia. consortia. Rhizosphere microorganisms
microorganisms like plant-growth-promoting
like plant-growth-promoting bacteriaarbuscular
bacteria (PGPB),
(PGPB),
mycorrhizal fungi arbuscular
(AMF), mycorrhizal
and fungi from thefungi (AMF),
genus and fungi
Trichoderma spp.from
canthe genus Trichoderma
establish spp. can es-with plants,
beneficial interactions
tablish
promoting plant beneficial
growth interactions with
and development, plants, promoting
increasing plant growth
the plant defense systemand development,
against pathogens, increasing
promoting nutrient
the plant defense system against pathogens, promoting nutrient uptake, and enhancing tolerance
uptake, and enhancing tolerance to different environmental stresses. Rhizosphere microorganisms can influence one another,
to different environmental stresses. Rhizosphere microorganisms can influence one another, and
and the resulting consortia of PGPB + PGPB (e.g., a nitrogen-fixing bacterium such as Rhizobium spp. and Pseudomonas
the resulting consortia of PGPB + PGPB (e.g., a nitrogen-fixing bacterium such as Rhizobium spp.
fluorescens), AMF
and Pseudomonas Trichoderma +AMF
+ PGPB, andfluorescens), PGPB may have
+ PGPB, andsynergetic
Trichodermaeffects on plant
+ PGPB may growth and fitness,
have synergetic providing the
effects
plant with enhanced benefits to overcome biotic and abiotic stress. Dashed arrows indicate beneficial
on plant growth and fitness, providing the plant with enhanced benefits to overcome biotic and interactions between
AMF and Trichoderma.
abiotic stress. Dashed arrows indicate beneficial interactions between AMF and Trichoderma.
Agronomy 2021, 11, 219 5 of 24

4. Bacteria–Bacteria Interactions
There is a great diversity of bacteria that are part of the plant microbiota and that
have traits that promote the growth and development of plants in both optimal and stress
environments [56,57]. A key factor influencing the beneficial effects of bacterial consortia is
the interaction between their members to guarantee a stable long-term co-existence [58].
Bacterial interactions within a consortium can be classified into three types based on
the effects they have on each other: (i) stimulatory or positive, (ii) inhibitory or negative,
or (iii) neutral [58]. Positive interactions generally create a network to support individual
members through cross-feeding, where one bacterium utilizes the metabolic products pro-
duced by another consortium member. Mutualism, protocooperation, and commensalism
are examples of positive associations. In mutualism, each of the members need the others to
survive since they mutually exchange required substances or mutually remove toxins [59].
In protocooperation, the interaction between species is beneficial to the growth rate of
both populations, but is not required for either to persist [58]. Commensalism is a positive
one-way interaction, in which one member benefits while the other is unaffected [60].
Negative interactions lead to the suppression of bacterial members in a consortium,
destroying the community structure and its functioning [60]; they include amensalism,
predation, parasitism, and competition. Amensalism is a type of unidirectional interaction
where the growth of one of the members is affected by the production of toxic compounds
by its partner [59]. Predation and parasitism describe interactions where the growth of
one species depends on consuming another species so that the population dynamics often
show continuous oscillations. Competition occurs when members of a consortium need the
same resource, be it nutrients, water, or even space; therefore, the faster-growing species
dominates over time [59,60]. In neutral interactions, members of the consortium do not
influence or affect one another. Neutralism occurs when two species consume different
substances (nutritional divergence) and neither produces compounds inhibitory to other
members of the consortium [58].
In agriculture, consortia members should positively interact, where mutualistic growth
is desirable for stable performance over prolonged cultivation to obtain the expected posi-
tive effect when applied to a crop [61,62]. In this regard, bacterial communication is only
superficially understood at the present time. This communication relies on the production,
detection, and response to extracellular signaling molecules that regulate and shape the
bacterial population in the consortium, where only compatible microbes are involved in
altering the plant defense response affecting overall plant health and growth [63]. Con-
sortium communication is highly dependent on molecular signals; among them, quorum
sensing plays a significant role in bacterial compatibility in consortium formulations [61].
Among several signal molecules, the acyl homoserine lactone (AHL) signal molecules are
the most well known in bacteria [63]. Pure AHLs have shown induction of intracellular
Ca2+ levels and primary root growth [61,64], while AHLs produced by PGPB, such as
Serratia liquefaciens and S. phymuthica, have stimulated root development and total plant
biomass; other bacteria, like Sinorhizobium fredii and Pantoea ananatis, stimulated the forma-
tion of biofilm in the roots of Oryza sativa (rice) and Phaseolus vulgaris (bean) plants [65].
Other species of nitrogen-fixing bacteria, such as Sinorhizobium meliloti, producers of AHLs,
promoted nodulation in Medicago truncatula [62,66] (Figure 2).
Quorum sensing allows bacteria to switch between two distinct gene expression
programs: (i) one at low cell density for individual and asocial behavior, and (ii) another at
high cell density for social and group behaviors, which are preferential for consortia [67].
Williams et al. [68] indicated that the response to fluctuations in cell number in quorum-
sensing systems occurs as follows. Low-molecular-weight molecules called auto-inducers
are synthesized intracellularly; then, these molecules are passively released or actively
secreted outside of cells. As the number of cells in a population increases, the extracellular
concentration of auto-inducers increases. Finally, the auto-inducers are accumulated above
the minimum threshold level required for detection, and the cognate receptors bind the
auto-inducers and trigger signal transduction cascades that result in population-wide
 Agronomy 2021, 11, 219 6 of 24

my 2021, 11, x FOR PEER REVIEW changes in gene expression. Thus, quorum sensing enables cells in a population
6 of 26 to function
in unison and, in so doing, they carry out behavior as a collective, not altering the desired
effects of compatible PGPB in consortia [69,70].

Figure 2. Plant responses to N-acyl homoserine lactones (AHLs) produced by plant-growth-promoting bacteria in the
rhizosphere.Figure
Single 2. Plant responses
members to N-acyl
of a bacterial homoserine
consortium could lactones (AHLs) produced
interact/communicate by plant-growth-pro-
to perceive certain population densities
and respondmoting bacteria in
as a collective to the rhizosphere.
induce Single membersactivities,
several plant-beneficial of a bacterial
suchconsortium could
as stimulation of interact/com-
root hair formation, root
municate to perceive certain population densities and respond
growth and development, and general plant growth and self-defense mechanisms. as a collective to induce several
plant-beneficial activities, such as stimulation of root hair formation, root growth and develop-
ment, and general plant growth
Other and self-defense
important signalingmechanisms.
compounds reported in bacterial consortia are volatile
organic compounds (VOCs), which are implicated in both bacteria–bacteria and plant–
Quorum sensing
bacteriaallows bacteria to [71].
communication switchThese
between two distinct
compounds gene expression
include terpenoids,pro- alkanes, alkenes,
grams: (i) one ketones,
at low cell density for individual and asocial
sulfur-containing compounds, and alcohols that actbehavior, and (ii)asanother at
low-molecular-weight
high cell density for social and group behaviors, which are preferential for consortia
(<300 Da), low-boiling-point, high-vapor-pressure, and lipophilic signal molecules [72]. [67].
Williams et al.These
[68] indicated
properties that the response
facilitate to fluctuations
evaporation in cellthrough
and diffusion numbergas- in quorum-
and water-filled pores
sensing systems occurs as follows. Low-molecular-weight molecules called auto-inducers
in soil and rhizosphere environments [73]. VOCs produced by bacteria can have posi-
are synthesized intracellularly;
tive effects on thethen,growth these molecules
of other nearby areorpassively releasedmodifying
distant bacteria, or activelytheir behavior
secreted outsideandof modulating
cells. As the number
bacterialofresistance
cells in a population
to antibiotics.increases,
Bacterial theVOCs
extracellular
can also have direct
concentration antagonistic
of auto-inducerseffectsincreases. Finally,
against other the auto-inducers
bacteria; for this reason,are manyaccumulated
species of Pseudomonas
above the minimum threshold
and Bacillus thatlevel required
produce VOCs forwith
detection, and theactivity
antibacterial cognateare receptors
used asbindbiocontrol agents
the auto-inducers and trigger signal transduction cascades that result in population-wide
against plant pathogens [74,75]. Furthermore, VOCs influence gene expression involved in
changes in gene expression.
hormonal Thus, quorum
signaling, defensive sensing
pathways,enablesandcells in a population
microbial to func-virulence, and
stress tolerance,
tion in unisonbiofilm
and, information
so doing, [76].
they carry out behavior as a collective, not altering the
desired effects of compatible
The success PGPB in consortia
of bacterial [69,70].
interaction in a consortium depends on (i) a proper description
Other important signaling compounds
of the consortium, the taxonomic reported in bacterial
affiliation consortia
of the strains, and are volatile or-protocols, (ii) a
identification
ganic compounds (VOCs),
detailed which are
explanation ofimplicated in both bacteria–bacteria
how the consortium was made, (iii)and plant–bac-
a full statement of sensitive
parameters,
teria communication [71].such
These as soil physicochemical
compounds includeparameters,
terpenoids,and the exact
alkanes, dosageke-
alkenes, applied, and (iv)
appropriatecompounds,
tones, sulfur-containing living populations of each species
and alcohols that actco-existing, which impacts the inoculated
as low-molecular-weight
consortium’s success
(<300 Da), low-boiling-point, [51,77].
high-vapor-pressure, and lipophilic signal molecules [72].
These properties facilitate evaporation and diffusion through gas- and water-filled pores
5. Plant Growth
in soil and rhizosphere Stimulation
environments by PGPB
[73]. VOCs Consortia
produced Under can
by bacteria Non-Stress Conditions
have positive
effects on the growth There are several
of other nearbystudies in which
or distant bacteria,the modifying
potential of bacterial
their behavior consortia
and to improve
modulating bacterial resistance to antibiotics. Bacterial VOCs can also have direct antag- For example,
plant growth has been demonstrated in greenhouse and/or field conditions.
onistic effects against other bacteria; for this reason, many species of Pseudomonas and Ba-
cillus that produce VOCs with antibacterial activity are used as biocontrol agents against
Agronomy 2021, 11, 219 7 of 24

Jha and Saraf [78] found that the inoculation of a multispecies consortium made up of
Micrococcus sp., Acinetobacter calcoaceticus, Brevibacillus brevis, and Bacillus licheniformis
with the ability to produce indole-3-acetic acid (IAA), 1-aminocyclopropane-1-carboxylate
(ACC) deaminase, and siderophores and to solubilize inorganic phosphorus improved the
yield of the plant Jatropha curcas. Similarly, a bacterial consortium including Azospirillum,
Pseudomonas striata, Pseudomonas sp. B15, and Leuconostoc mesenteroides improved the
plant height and biomass of seedlings of tomato, brinjal, and chili [79]. In another study,
Molina-Romero et al. [80] showed that a consortium consisting of desiccation-tolerant
bacteria (Pseudomonas putida KT2440, Acinetobacter sp. EMM02, Sphingomonas sp. OF178,
and Azospirillum brasilense Sp7) was able to adhere to seeds and colonize the rhizosphere of
maize plants. This latter experiment showed that these bacteria can coexist in association
with plants without antagonistic effects, and that inoculation with this consortium increased
maize plant height, diameter, and shoot–root dry weight (compared to the un-inoculated
control). Dary et al. [81] and Malboobi et al. [82] observed that the inoculation of Solanum
tuberosum and Lupinus luteus plants with a consortium composed of P. putida, P. agglomerans,
Bradyrhizobium sp., and Pseudomonas sp. showed higher plant growth promotion in root
dry weight, aerial dry weight, nitrogen content, and final yield.
Rojas Padilla et al. [83], using a native Bacillus consortium with Triticum turgidum L.
subsp. Durum (wheat) under non-stress conditions, reported an increase in plant length
and weight, as well as the biovolume index, compared to inoculations of a single bacterial
strain at a time. Similarly, Robles Montoya et al. [84] reported that the use of a Bacillus
consortium composed of B. paralicheniformis, B. subtilis, B. megaterium, and B. cabrialesii with
wheat showed a significant increase (compared to un-inoculated seedlings) in the length
of the aerial part of the plant, root length, total length, stem diameter, circumference, dry
weight of the aerial part of the plant, and the biovolume index.
Rhizobia have been widely studied for their ability to form nodules and fix atmo-
spheric nitrogen; they are a diverse group of bacteria that form a symbiotic relationship with
leguminous plants. This group is composed of bacteria belonging to Proteobacteria classes,
primarily Alphaproteobacteria (e.g., Rhizobium, Sinorhizobium, Ensifer, Bradyrhizobium,
Mesorhizobium) and Betaproteobacteria (e.g., Paraburkholderia, Cupriavidus, Trinickia) [85].
Rhizobia induce the leguminous plant’s symbiotic response and the development of nod-
ules in which the nitrogen fixation process occurs. On the other hand, leguminous plants
create a niche and increase chances of survival for symbiotic bacteria by providing carbon
sources for the rhizobia within the nodules.
The symbiotic process starts with the perception of plant-secreted flavonoids (present
in root exudates) by rhizobia, which, in turn, produce lipochitooligosaccharides, termed
nodulation (Nod) factors (NFs), which are sensed by the plant and lead to the activation
of the nodule organogenesis programs [86]. Subsequently, the rhizobia present in the
rhizosphere enter the plant root hairs via root cracks and then migrate and colonize the
nodule structure via infection threads [87]. When present inside the nodule, rhizobia
differentiate into a bacteroid state, a specialized symbiotic organelle-like form that po-
tentiates the nitrogen fixation process [88]. As bacteroids, rhizobia fix atmospheric N2
through the action of the nitrogenase enzyme, providing NH4 to the plant host in exchange
for photosynthetically fixed carbon [89] (Figure 3). It is estimated that legume–rhizobial
biological nitrogen fixation (BNF) globally accounts for ~200 million tons of fixed nitrogen
per year [90], playing a vital role in soil N cycles and overall agricultural productivity.
Rhizobia are common soil and rhizosphere inhabitants and, as a consequence, have
evolved in direct competition and/or synergism with other soil and rhizospheric microbes,
including rhizobial and non-rhizobial bacteria (NRB; free-living rhizospheric and endo-
phytic bacteria). In fact, under natural conditions, leguminous plant roots and root nodules
contain a wide range of rhizospheric and endophytic bacteria, as well as rhizobia [91–95].
Importantly, some of these bacteria may potentiate rhizobial nodule formation and pro-
mote plant growth in both optimal and stressful conditions [91,94]. Hence, obtaining and
exploring the synergistic effects between rhizobia and NRB consortia may be the key for
 Rhizobia are common soil and rhizosphere inhabitants and, as a consequence, have
evolved in direct competition and/or synergism with other soil and rhizospheric microbes,
including rhizobial and non-rhizobial bacteria (NRB; free-living rhizospheric and endo-
phytic bacteria). In fact, under natural conditions, leguminous plant roots and root nod-
ules contain a wide range of rhizospheric and endophytic bacteria, as well as rhizobia [91–
Agronomy 2021, 11, 219 8 of 24
95]. Importantly, some of these bacteria may potentiate rhizobial nodule formation and
promote plant growth in both optimal and stressful conditions [91,94]. Hence, obtaining
and exploring the synergistic effects between rhizobia and NRB consortia may be the key
the development
for the development of inoculants
of inoculants with increased
with increased performance
performance and plant-growth-promoting
and plant-growth-promot-
properties
ing properties (Figure 3).
(Figure 3).

Figure 3. The Figure

formation of N-fixing
3. The formationnodules induced
of N-fixing by rhizobia.
nodules inducedFree-living
by rhizobia.plant-growth-promoting rhizobacteria and
Free-living plant-growth-pro-
moting rhizobacteria
bacterial endophytes may induce theandnodulation
bacterial endophytes may
process and inducethe
increase thenitrogen
nodulation process
fixation, and increase
general plant growth, and
the nitrogen fixation, general plant growth, and nutrimental state.
nutrimental state.

Several
Several studies havestudies have demonstrated
demonstrated that range
that a diverse a diverse range of free-living
of free-living rhizospheric and
rhizospheric
endophytic
and endophytic bacteriabacteria
are ableare
to able to potentiate
potentiate the nodulation
the nodulation and nitrogen
and nitrogen fixation
fixation pro- processes of
several
cesses of several rhizobial
rhizobial strains,
strains, leading
leading totoincreased
increasedleguminous
leguminousplant
plantgrowth
growth (Table 1). The NRB
1). The NRB partners include bacteria belonging to the Firmicutes (e.g., Bacillus,Paenibacillus),
include bacteria belonging to the Firmicutes (e.g., Bacillus, Paenibacil- Proteobac-
teria (e.g., Pseudomonas, Azospirillum, Pantoea) Actinobacteria (e.g., Streptomyces, Nocardia),
Flavobacteria, and some cyanobacteria. Moreover, the beneficial effects of co-inoculations
have been observed in diverse systems (e.g., forming determinate or indeterminate nodules)
between several leguminous plants (e.g., Phaseolus vulgaris, Glycine max, Cicer arietinum)
and their respective compatible alpha and beta-rhizobial symbionts (e.g., Rhizobium, Neorhi-
zobium, Bradyrhizobium, Ensifer/Sinorhizobium, Mesorhizobium, Cupriavidus). This indicates
that the co-inoculation process can be a generally beneficial practice that benefits most
legume–rhizobia symbioses [96].
Agronomy 2021, 11, 219 9 of 24

Table 1. Studies reporting the beneficial interactions between consortia of rhizobia and non-rhizobial bacteria and their
positive effects in the symbiosis with leguminous plants.

Rhizobia Co-Inoculant Plant Host Reference

R. tropici CIAT899 Bacillus megaterium Phaseolus vulgaris [97]
R. tropici CIAT899 Paenibacillus polymyxa (DSM 36) Phaseolus vulgaris [98]
R. tropici CIAT899 Serratia grimesii BXF1 Phaseolus vulgaris [99]
R. tropici CIAT899 Pseudomonas fluorescens YsS6 Phaseolus vulgaris [100]
Bacillus aryabhattai Sb
Rhizobium spp. Trifolium repens [101]
Azotobacter vinelandii G31
Pseudomonas fluorescens P-93
Rhizobium Phaseolus vulgaris [102]
Azospirillum lipoferum S-21
Bacillus insolutis,
Rhizobium leguminosarum bv.
Bacillus brevis Trifolium pratense [94]
trifolii
Agrobacterium rhizogenes
Pisum sativum;
Rhizobium leguminosarum PR1 Bacillus thuringiensis KR1 [103]
Lens culinaris
Bacillus subtilis OSU-142
Rhizobium Phaseolus vulgaris [104]
Bacillus megaterium M-3
Rhizobium spp. IC3123 Bacillus megaterium NR4 and NR6 Cajanus cajan [105]
Pseudomonas putida;
Rhizobium sp. AR-2–2 P. fluorescens Cajanus cajan [106]
Bacillus cereus
Rhizobium etli Paenibacillus polymyxa Phaseolus vulgaris [107]
(Neo)Rhizobium galega bv. Pseudomonas trivalis 3Re27
Galega orientalis [108]
orientalis Pseudomonas extremorientalis TSAU20
Serratia proteamaculans 1–102
Bradyrhizobium japonicum 532C Aeromonas hydrophila P73 Glycine max [109]
Serratia liquefaciens 2–68
B. japonicum E109 Bacillus amyloliquefaciens LL2012 Glycine max [110]
B. diazoefficiens USDA110 Bacillus velezensis S141 Glycine max [111]
B. japonicum SB1 Bacillus thuringiensis KR1 Glycine max [112]
B. japonicum B. subtilis Glycine max [113]
B. subtilis NEB4 and NEB5
Bradyrhizobium japonicum Glycine max [114]
B. thuringiensis NEB17
B. japonicum spp. Streptomyces griseoflavus P4 Glycine max [115,116]
B. elkanii BLY3–8 Streptomyces griseoflavus P4 Glycine max [117]
Nocardia alba
B. japonicum Nonomuraea rubra Glycine max [118]
Actinomadura glauciflava
Bradyrhizobium sp. BR1602 Pantoea phytobeneficialis MSR2 Calopogonium muconoides [119]
Sinorhizobium meliloti Exiguobacterium sp. M2N2c and B1N2b Trigonella foenum-graecum [96]
Bacillus anthracis Ml
E. adhaerens Paenibacillus taichungensis M10 Paenibacillus Vigna radiata [120]
xylanilyticus M15
Sinorhizobium meliloti B399 Bacillus sp. M7c Medicago sativa [121]
Ensifer (Sinorhizobium) medicae
Pseudomonas fluorescens WSM3457 Medicago truncatula [122]
WSM419
Mesorhizobium sp. BHURC02 Pseudomonas fluorescens BHUPSB06 Cicer arietinum [123]
Mesohizobium spp. Ca181 and
Pseudomonas sp. CRP55b and CRS68 Cicer arietinum [124]
Ca313
Mesohizobium spp. Ca181 Pseudomonas spp. Cicer arietinum [125]
M. ciceri TAL-1148 Ochrobactrum ciceri Ca-34 Cicer arietinum [126]
Mesorhizobium ciceri Anabaena Cicer arietinum [127]
Cupriavidus taiwanensis Pseudomonas fluorescens YsS6 Mimosa pudica [100]

The study of the interactions between rhizobia–NRB consortia has revealed some of
the mechanisms that are involved in the NRB abilities to promote nodulation and nitro-
gen fixation by rhizobia. These include (i) the direct increase in the number of rhizobial
populations in the soil, (ii) the production of siderophores that promote rhizobial growth
Agronomy 2021, 11, 219 10 of 24

under iron-limiting conditions [105,128,129], (iii) the direct effect on plant root growth and
nutrient uptake (i.e., N, P, K), which positively impacts the symbiotic efficiency, (iv) lytic en-
zyme activities (e.g., cellulase) [108] that play a role in rhizobial colonization, (v) induction
of plant flavonoid biosynthesis that leads to the expression of rhizobial nod genes [124,130];
(v) biosynthesis of plant hormones such as IAA, cytokinins, gibberellins [108,110,111] that
facilitate plant growth and development and the regulation of the nodulation process, and
vi) expression of ACC deaminase [99,131] and the modulation of plant ethylene levels,
which are involved in the regulation of the nodulation process [131,132].
Interestingly, recent studies have demonstrated that the consortia benefit not only the
rhizobial partner, but also the NRB partner. For example, Zgadzaj and colleagues [133]
have shown that Mesorhizobium loti induces infection threads that can selectively guide
non-rhizobial endophytic bacteria towards nodule primordia. These endophytes are then
able to migrate and colonize the root nodule together with rhizobia, benefiting from the
increased carbon concentrations found within the nodule.

6. Plant Growth Stimulation by PGPB Consortia Under Stress Conditions

Along with the increase in agrochemicals, climate change and modifications in land use
can create unfavorable stress conditions for microbial interaction in agro-ecosystems [134].
Stress conditions can impair plant morphology, physiology, biochemistry, and gene regula-
tion, as well as soil microbial and physicochemical properties, resulting in considerable yield
loss [38]. The different types of stress may be classified as biotic and abiotic, where biotic
stress is caused by living organisms, including viruses, bacteria, fungi, nematodes, insects,
arachnids, and weeds, while abiotic stresses include extremes of temperature, drought,
environmental contaminants, and salinity [56].
Beneficial bacteria can contribute to sustaining the intrinsic resistance of the plant to
these challenges; therefore, the inoculation of plants with bacterial consortia can reduce the
negative influence of biotic or abiotic stress conditions on crops [134] (Table 2). However,
novel approaches are needed to explore bacteria–bacteria and plant–bacteria interactions
under abiotic and biotic stress conditions to identify potential stress-tolerant or resistant
bacteria to improve plant growth and disease resistance [56].

Table 2. Examples of bacterial consortia and their beneficial effects on crop plants under biotic and abiotic stresses.

Consortium Crop Stress Effect Reference

Reduction of mycelial growth
Pseudomonas spp. Potato Phytophthora infestans [135]
Decreased release of zoospores
induced systemic resistance (ISR)
Xanthomonas sp., activation (reduced the number of
Hyaloperonospora
Stenotrophomonas sp., Arabidopsis thaliana pathogen spores) [136]
arabidopsidis
and Microbacterium sp. Plant growth promotion
(shoot fresh weight)
ISR activation (peroxidase (PO),
polyphenol oxidase (PPO),
phenylalanine ammonia-lyase
Pseudomonas putida
Macrophomina (PAL), β-1,3 glucanase
CRN-09 and Bacillus Mung bean [137]
phaseolina and chitinase)
subtilis CRN-16
Plant growth promotion
(increased shoot and root length,
shoot and root fresh weight)
Pseudomonas aeruginosa ISR activation (increased
PHU094 and phenolic compounds)
Chickpea Sclerotium rolfsii [138]
Mesorhizobium sp. Plant growth promotion (increased
RL091 shoot length and total biomass)
Pseudomonas fluorescens Decreased root rot incidence
Cotton Rhizoctonia bataticola [139]
and Azospirillum Increased seed cotton yield
Agronomy 2021, 11, 219 11 of 24

Table 2. Cont.

Consortium Crop Stress Effect Reference

Increased photosynthetic rate, the
Bacillus cereus Y5,
content of carotenoids and
Bacillus sp. Y14, and Wheat Salinity [140]
crude protein
Bacillus subtilis Y16
Higher grain yield
Increased fermination percentage
Brevibacillus fluminis,
Brinjal, potato, Plant growth promotion (an
Brevibacillus agri, and Salinity [141]
tomato, and chilli increase in shoot length, root
Bacillus paralicheniformis
length, dry and fresh weight)
Pseudomonas sp. PFS1
and BSS3B2, Serratia
proteamaculans Salinity, petroleum Plant growth promotion
saltgrass [142]
S1BD1, Alcaligenes sp. hydrocarbons (increased plant biomass)
PKS1, and
Bacillus sp. PSS2
Reduced Al uptake in plants
B. megaterium CAM12 Plant growth promotion
Aluminum
and P. agglomerans Mung bean (increased plant biomass) [143]
and drought
CAH6 Higher content of
carotenoids, chlorophyll
Increased the leaf proline content
Bacillus cereus AR156,
Significantly enhanced the
Bacillus subtilis SM21, Cucumber Drought [144]
superoxide dismutase
and Serratia sp. XY21
(SOD) activity
Rhodotorula graminis
WP1, Burkholderia
vietnamiensis WPB,
Rhizobium tropici PTD1,
Acinetobacter
Plant growth promotion (increased
calcoaceticus WP19,
root dry weight, shoot dry weight,
Rahnella sp. WP5,
poplar Drought total dry weight, total nitrogen) [145]
Burkholderia sp. WP9,
Reduced damage by reactive
Enterobacter asburiae
oxygen species (ROS)
PDN3, Sphingomonas
yanoikuyae WW5,
Pseudomonas sp. WW6,
and Curtobac-
terium sp. WW7
Plant growth promotion
(increased seed germination
Ochrobactrum
percentage, root length, shoot
pseudogrignonense RJ12,
length, and dry weight)
Pseudomonas sp. RJ15, Black gram and Pea Drought [146]
Elevated production of ROS
and Bacillus
scavenging enzymes and
subtilis RJ46
cellular osmolytes
Higher leaf chlorophyll content

6.1. Biotic Stress

Plant defense can generally be induced more effectively and efficiently by microbial
consortia compared to a single microbial inoculant. Therefore, considering the abilities of
several bacteria in a consortium to activate pathways related to resistance or biocontrol,
there is an ample opportunity to harness these mechanisms for controlling yield and
diminishing diseases in an associated crop [135,137,138].
In this way, Singh et al. [138] evaluated the effectiveness of a microbial consortium that
included three compatible rhizosphere microorganisms, Pseudomonas aeruginosa PHU094,
Trichoderma harzianum THU0816, and Mesorhizobium sp. RL091, in promoting plant growth
and mobilizing phenolic acid in chickpea infected by Sclerotium rolfsii. In this work, several
Agronomy 2021, 11, 219 12 of 24

phenolic compounds, such as myricetin, ferulic acid, syringic acid, and quercetin, were
accumulated in higher levels in the treated plants. Moreover, shikimic acid was maximally
produced in the leaves of consortium-treated chickpea plants after pathogen infection
(compared to untreated control plants or plants treated with a single microbe). However, it
should be noted that using species of opportunistic human pathogens, such as P. aeruginosa,
restricts their use and release in the field, so it is advisable to use other species without any
pathogenic potential.
The synergistic interaction between Pseudomonas putida CRN-09 and Bacillus subtilis
CRN-16 was evaluated in Vigna radiate (mung bean), where the consortium triggered the ex-
pression of induced systemic resistance against the phytopathogenic fungus Macrophomina
phaseolina. This resulted in enhanced plant levels of peroxidase (PO), polyphenol oxidase
(PPO), phenylalanine ammonia-lyase (PAL), β-1,3 glucanase, and chitinase [137]. In ad-
dition, De Vrieze et al. [135] used a leaf disk assay with three different potato cultivars
to compare the activity of nine selected Pseudomonas strains against the phytopathogenic
fungus Phytophthora infestans when the selected strains were applied alone or in various
combinations. The results revealed that the combination of two strains (P. frederiksbergensis
S19 and P. fluorescens S49) was particularly effective at controlling the pathogen; while
strain S49 had a stronger inhibition effect on mycelial growth, strain S19 was a very efficient
inhibitor of zoospores. Similarly, a bacterial consortium (P. aeruginosa and Azospirillum sp.)
was found to have a synergistic effect on the plant yield and suppression of root rot disease
caused by the phytopathogenic fungus Rhizoctonia bataticola in cotton plants at both full
and half levels of synthetic fertilization [139].
The way a consortium is created can have a significant impact on food production
and control of phytopathogens. For example, Berendsen et al. [136] studied the microbiota
of Arabidopsis when it was infected with the phytopathogenic fungus Hyaloperonospora
arabidopsidis and found that three bacterial genera were most abundant, including Xan-
thomonas spp., Stenotrophomonas spp., and Microbacterium spp. They observed that these
bacteria interact synergistically in the formation of biofilms in vitro, and although these
bacteria did not separately affect the plant to any significant extent, together, they induced
systemic resistance against downy mildew and promoted plant growth. Thus, the strains
in this bacterial consortium for controlling phytopathogens are clearly compatible.

6.2. Abiotic Stress

Abiotic stresses can inhibit a plant’s development due to the oxidative damage by
free radicals produced in their cells, which attack vital cellular components like DNA and
cellular membranes [147]. Antioxidant enzymes, such as catalase and peroxidase, can
neutralize these reactive molecules and protect the cells from damage [56]. Several species
of bacteria have the ability to enhance the activity of these and other enzymes, as well as to
produce protective substances, such as trehalose, which also helps to improve the response
of plants to abiotic stress [12].
Heidari and Golpayegani [148] reported that Ocimum basilicum (basil) inoculated
with a bacterial consortium (Pseudomonas sp., Bacillus lentus, and Azospirillum brasilense)
displayed an increased level of chlorophyll content and antioxidant activity in plants under
water stress conditions. Similarly, the effect of a consortium consisting of ten bacterial
strains was investigated on commercial hardwood cuttings of Populus deltoides × P. nigra
clone OP-367. After one month under water stress conditions, there was substantial
growth promotion with improved foliar physiology in response to bacterial endophytic
colonization; furthermore, the inoculated plants showed reduced damage by reactive
oxygen species [145].
On the other hand, plants colonized by specific bacterial strains under abiotic stress
conditions increase the accumulation of abscisic acid and degradation of reactive oxy-
gen species by the microbial production of auxins, gibberellins, cytokinins, and antioxi-
dants [147]. In this regard, a field experiment was conducted to evaluate different carriers
for a bacterial consortium (Bacillus cereus Y5, Bacillus sp. Y14, and Bacillus subtilis Y16) to
Agronomy 2021, 11, 219 13 of 24

improve wheat production under salinity stress. The results revealed that the bacterial
inoculation of multiple strains improved the photosynthetic rate, the content of carotenoids,
protein levels, and the yield of the treated wheat crop [140].
PGPB typically enhance the level of the osmoprotectant proline in plants exposed to
abiotic stresses. Proline scavenges reactive oxygen molecules and acts to stabilize proteins
through molecular chaperones in the stressed cells [147]. Wang et al. [144] reported the
effect of a consortium of three bacterial strains (Bacillus cereus AR156, Bacillus subtilis
SM21, and Serratia sp. XY21) on drought tolerance in cucumber plants. After withholding
watering for 13 days, consortium-treated cucumber plants had much darker green leaves
and fewer wilt symptoms than control plants; in addition, the consortium inoculation
increased the leaf proline and chlorophyll content and enhanced the superoxide dismutase
(SOD) activity. These results indicated that the tested bacterial consortium conferred
induced systemic tolerance to drought stress in cucumber plants by protecting the integrity
of plant cells, maintaining photosynthetic efficiency and root vigor, and increasing some
antioxidation activities, all of which led to increased drought tolerance.
Under abiotic stress conditions, increased ethylene levels in plants restrict root and shoot
growth, but bacterial ACC deaminase can degrade excessive ACC produced by the plant
and balance the total ACC content in plants, thereby enhancing plant growth [38,149,150].
For example, Saikia et al. [146] showed that the inoculation of a consortium of three ACC-
deaminase-producing rhizobacteria (Ochrobactrum pseudogrignonense RJ12, Pseudomonas sp.
RJ15, and Bacillus subtilis RJ46) significantly increased the seed germination percentage, root
length, shoot length, and dry weight of the legumes Vigna mungo and Pisum sativum under
drought stress.

7. Plant Growth Stimulation by Fungal–Bacterial Consortia

Plants can establish interactions with several soil-borne microorganisms. Those in-
teractions can take place in the rhizosphere, inside the root cortex, or on the root surface
(rhizoplane), and they can be beneficial, neutral, or harmful. The overall result of plant–
microorganism interactions is determined by the development status of the plant, the soil
structure and chemistry, and the microorganisms present at certain times. Such microor-
ganisms are termed the microbiome. The plant microbiome is formed by many diverse
organisms that respond to the conditions of the rhizosphere, which is influenced by the
root exudates, and its diversity determines the outcome of the interaction with the plant,
as well as the countless interactions that take place within this plant holobiont [151–153].
Plant-growth-promoting organisms, which are part of the plant microbiome, have
been studied to find sustainable alternatives to the use of chemical fertilizers and pesticides.
Among these organisms are PGPB, mycorrhizal fungi, and plant-beneficial fungi. The
majority of studies include interactions between root- and/or rhizosphere-colonizing
bacteria and root-colonizing fungi, pointing towards synergistic effects of these organisms
on plants [154]. PGPB, arbuscular mycorrhizal fungi (AMF), and Trichoderma species are
the most important components of the plant microbiome that are actively being studied;
their interactions that improve plant health and fitness are discussed below.

7.1. Plant Growth Stimulation by AMF–PGPB Consortia

Arbuscular mycorrhizal fungi (AMF) are a monophyletic fungal lineage, Glomeromy-
cota, that can establish a mutualistic relationship with the roots of most of the plants on
the planet. This relationship is known as “the mycorrhizal symbiosis”. Once the AMF is
established inside the root plant, it develops structures called arbuscules inside certain
plant cells. The establishment of the AMF in the root cortex changes many aspects of the
plant physiology, including the composition of root exudates, which can stimulate growth
of other beneficial microbes and the AMF itself [154].
In this relationship, AMF receives carbon compounds from the plant and the plant
receives multiple benefits in exchange, including improved acquisition of nutrients and
water from the soil, facilitating mineral solubilization and uptake. AMF promotes increased
Agronomy 2021, 11, 219 14 of 24

plant biomass and yield, as AMF promotes plant growth, improved plant fitness against
several abiotic stresses, and defense against pathogens stimulating enzymatic activity,
phytohormone synthesis, and lipid peroxidation [154,155].
As part of the plant microbiome, the interaction between PGPB and AMF is useful for
increasing or potentiating the positive effects that each organism can exert on the plant. The
consortia between AMF and PGPB have been of interest mainly due to the impact on plant
growth promotion and defense against phytopathogens. For example, B. subtilis and AMF
present in soil surrounding Acacia gerrardii (Acacia tree) resulted in a significant increase
in shoot and root biomass, as well as in greater root depth, in the absence of abiotic stress
conditions, with the combination of the two organisms being more effective than either
by itself [156].The co-inoculation of either Pseudomonas sp. or Bacillus amyloliquefaciens
with the AMF Rhizophagus irregularis (formerly named Glomus intrarradices) on tomato
plants increased root and shoot dry weight and reduced disease symptoms caused by
the phytopathogen Fusarium oxysporum [157]. In soybean, the co-inoculation of rhizobia
(Bradyrhizobium sp.) and AMF (Glomus mosseae) resulted in an increased resistance and
expression of defense–related genes, such as PR2, PR4, and PR10, in the presence of the
fungal pathogen Cylindrocladium parasiticum compared to the plants inoculated with either
one of the microorganisms [158]. This suggests that, together, AMF and PGPB may provide
a viable biocontrol strategy for some important crop plants (Figure 1).
The increase in plant growth promotion exhibited by a consortium of AMF and PGPB
is due to the enhancement of the benefits that both organisms provide to a plant compared
to the effects that each organism has alone [154,159]. For example, the combination of
AMF and PGPB facilitates soil mineral solubilization, thus improving plant nutrient uptake
(e.g., zinc, magnesium, iron, and phosphorus) and general development. Mineralization
involves the breakdown of complex organic compounds into readily metabolizable forms
by the plants, whose process is catalyzed by microbial phosphatases and phytases. The
production of organic acids by bacteria is another mechanism that results in chelating
mineral ions, along with lowering the pH of the rhizosphere to bring elements into the soil
solution [14]. Thus, the concentration of magnesium, phosphorous, and zinc in tomato
plants increased considerably with the co-inoculation by either Pseudomonas sp. or B.
amyloliquefaciens with R. irregularis in comparison with plants inoculated with just one
of these microorganisms [157]. Accumulation of nitrogen, phosphorous, and potassium
is improved by dual inoculation of Bacillus sp. and G. mosseae in lettuce [160] and the
AMF Pelargonium graveolens [161], yielding better results than either single inoculation.
In addition, the combination of R. irregularis with Sinorhizobium meliloti, Bacillus sp., and
Streptomyces sp. increased biomass and phosphate uptake in maize plants [162]. Thus,
changes in nutrient availability in the rhizosphere can be caused by bacteria and AMF, and
this availability of nutrients might also be a consequence of modulations in the rhizosphere-
beneficial microbiota.
AMF and PGPB consortia also increase plant fitness under environmental stress
conditions, thus promoting plant growth [163]. When drought stress is induced in lettuce,
the co-inoculation of G. mosseae or R. irregularis with Bacillus sp. helped to ameliorate the
effects of this stress by promoting plant growth and nutrient uptake [160]. Under salt stress,
the plant A. gerrardii increased its biomass, improved nutrient uptake, including Na, P,
K, Mg, Ca, and N, and increased the level of photosynthetic pigments and the enzymatic
activity of nitrate/nitrite-reductase and nitrogenase enzymes when co-inoculated with B.
subtilis and AMF, thus promoting overall plant growth and development [156].
The mechanisms that enable AMF–PGPB consortia to have a synergistic effect on the
plant are complex, but one thing is clear: This synergistic effect depends on the nature of
the microorganisms and the interaction that takes place among them [154,163,164]. When
combinations of different species of AMF and/or PGPB have been tested in one plant
species, the effect on plant growth promotion depends on the consortia [157,160,161], plant
genotype [165], and soil nutrient composition [158,165,166]. Further, the presence of PGPB
can enhance AMF mycorrhization and promote its root cortex colonization in the host,
Agronomy 2021, 11, 219 15 of 24

helping AMF to increase its effects on the plant [156–158]. Meanwhile, the presence of AMF
can induce nodule formation in roots, helping Rhizobia to establish the interaction with the
plant, especially under stress conditions [156]. This means that to find suitable AMF–PGPB
consortia, those factors need to be taken into consideration so that the use of plant-growth-
promoting microorganisms may have a positive effect by creating a beneficial rhizosphere.

7.2. Plant Growth Stimulation by Trichoderma–PGPB Consortia

Fungi belonging to the genus Trichoderma are soil-borne filamentous ascomycetes that
can be found in a wide variety of ecosystems, ranging from forests, grasslands, and deserts
to agricultural soils and decaying wood [167]. Moreover, they are effective plant root
colonizers and are present in the rhizosphere [168,169]. As part of the plant microbiome,
Trichoderma spp. can promote plant growth and development by various mechanisms that
have been widely studied and are of interest due to their use in agriculture as an effective
biocontrol agent [170]. The Trichoderma–plant interaction begins with the perception of
plant root exudates that mediate fungal recognition of the host, and then, contact and root
penetration and colonization are initiated [168,171].
Trichoderma have been used as biocontrol agents due to their abilities as effective my-
coparasites of several phytopathogens and their ability to induce plants’ defense systems
and priming [168]. The fungal pathogen biocontrol activity of Trichoderma is a consequence
of competing with the pathogen for nutrients and space, altering the environmental condi-
tions, and promoting inherent plant defensive mechanisms, as well as by the Trichoderma
parasitizing the fungal pathogen. Trichoderma has also been used as a biostimulant because
it can promote plant growth and development through its synthesis of phytohormone-like
molecules and volatile organic compounds, thus improving soil mineral solubilization,
nutrient uptake, and translocation, increasing root system development [168,172,173], and
enhancing plant tolerance to both biotic and abiotic stresses.
On their own, PGPB and Trichoderma spp. can be effective biocontrol agents and
plant-growth-promoting microorganisms. However, combinations of different Trichoderma
species with PGPB have been shown to be more effective than a single microorganism
(Figure 1). For example, co-inoculation of T. harzianum and Serratia proteamaculans had
a positive effect on tomato growth, increasing total biomass [174]. In addition, for co-
inoculation of T. harzianum with different PGPB strains on Mentha arvensis (mint) plants,
in particular, the strain Brevibacterium halotolerans showed a good synergistic effect with
T. harzianum when measuring plant biomass in field experiments compared to single
inoculation [58].
Yield production and pathogen resistance are important traits to consider in biocontrol
and plant-growth-promoting agents. A consortium consisting of B. subtilis and T. harzianum
increased potato yield and conferred resistance against potato common scab induced by
Streptomyces spp. [175]. Co-cultivation of T. atroviride and B. amyloliquefaciens promoted
maize and wheat growth, germination, and vigor, and induced resistance against F. gramin-
earum [176]. In addition, the co-inoculation of Bradyrhizobium sp. and Trichoderma spp. had
positive effects on total shoot and root dry weight of cowpea plants, and it protected the
plants against Rhizoctonia solani infection, especially when the initial co-inoculation was
followed by a re-inoculation of Trichoderma 15 days later [177].
The effect shown by the consortia in conferring plant resistance against different
pathogens may be due to the increase in plant defense systems. Accumulation of reac-
tive oxygen species (ROS) is one sign of plant pathogen invasion; plant defense system
mechanisms include expression of ROS-related enzymes, such as catalases and superoxide
dismutase [178]. The co-inoculation of T. harzianum and S. proteamaculans has also proven
to be effective at activating the enzymatic activity of superoxide dismutases and catalases
in tomato plants in response to R. solani infection [174]. The combination of T. harzianum
Tr6 and Pseudomonas sp. Ps14 enhanced systemic resistance in cucumber and Arabidopsis
when the plants were challenged with the phytopathogens F. oxysporum and Botrytis cinerea,
respectively, compared to single inoculations [179].
Agronomy 2021, 11, 219 16 of 24

As mentioned previously, the beneficial effects of the consortia on plant health and
fitness are the results of the interactions between the microorganisms. When Trichoderma
spp. are inoculated with different strains of Pseudomonas spp. [179] or other PGPB (e.g., B.
subtilis, B. flexus, Stenotrophomonas spp., B. halotolerans) [180], not all the combinations show
an increased beneficial effect compared to single inoculations, meaning that the interaction
with the plant is dependent on the nature of the consortium and on the amount of inoculum
applied [175]. Moreover, the presence of PGPB improves T. harzianum mycelia density,
favoring root colonization [180]. Nevertheless, some strains of T. harzianum showed no
increase in mycelium density in the presence of Pseudomonas sp., although none showed a
negative effect [179].
T. harzianum can change bacterial and fungal diversity in the maize rhizosphere,
which results in plant growth promotion and protection against the phytopathogen F.
graminearum [181]. Moreover, inoculation of T. virens or T. harzianum had a positive influence
on the diversity of prokaryotes and eukaryotes in the lettuce rhizosphere, increasing plant
productivity and N uptake [172]. As effective as Trichoderma spp. or PGPB are in promoting
plant growth and defense, studies point toward a synergistic interaction of this consortium
by combining and potentiating their benefits on plants in order to establish a positive
interaction with their hosts.
The combination of PGPB, mycorrhizal fungi, and biocontrol agents like Trichoderma
spp. provides a strategy that should be commercially exploited in order to endow plants
with a complete “benefits package”: increases in plant biomass and yield production,
resistance to abiotic stresses, biocontrol of phytopathogens, and better nutrient uptake.

8. Conclusions and Perspectives

In any natural or agricultural ecosystem, plants are found to interact with soil microor-
ganisms [182,183]. The vast majority of these interactions, whether pathogenic, neutral,
or beneficial, occur through a complex network of signals, which include metabolites,
volatile and non-volatile compounds [184], physical interactions, and interactions that
regulate gene expression, either by increasing or repressing it [184,185]. It is essential
to take advantage of this intricate network of natural interactions to engineer artificial
microbial consortia that substantially and consistently benefit plant growth and health,
increase crop production, and decrease the use of chemical fertilizers.
Recently, Berg et al. [186] proposed revisiting and redefining the concept of the plant
(and human) microbiome, taking into account the associated microbiota and the “theater
of activity” that involves the production of proteins, lipopolysaccharides, metabolites, and
compounds as environmental factors. This is in agreement with our proposal of using a mi-
crobial consortium as part of the plant microbiome that interacts synergistically to promote
plant growth and health through the production of metabolites with antibiotic activity
and by solubilizing nutrients and making them available to the plant, forming nodules
to fix nitrogen, and producing plant-growth-stimulating phytohormones or enzymes that
degrade ethylene precursors, such as ACC deaminase [12]. The directed use of microbial
consortia will facilitate the production of plants in a more sustainable way that, eventually,
will not depend on agrochemicals.

Author Contributions: Conceptualization, writing—original draft preparation, visualization, writing—

review and editing, G.S. and B.R.G.; writing—original draft preparation, investigation, P.G.-G.; F.I.P.-C.,
S.d.l.S.-V. and M.d.C.O.-M.; supervision, funding acquisition, G.S. All authors have read and agreed to
the published version of the manuscript.
Funding: This research was funded by CONACYT-México, grant number A1-S-15956.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Agronomy 2021, 11, 219 17 of 24

Acknowledgments: P.G.-G. was the recipient of a postdoctoral fellowship under the research pro-
posal number A1-S-15956 supported by CONACYT-México. We thank Francisco N. Nascimento for
the helpful comments and discussions.
Conflicts of Interest: The authors declare no conflict of interest.

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