Plant beneficial
microorganisms
Types of
PBM
PBM are known as microorganisms that can increase plant establishment,
growth and development, and defend plants across disease and abiotic
stresses. PBM mainly include PGPB, arbuscular mycorrhizal fungi (AMF),
and rhizobia.
Plant growth-promoting
bacteria
The most PBM present in soils are PGPB such as Azospirillum ,Azotobacter , Pseudomonas , and Bacillus , which are
bacteria capable of inducing growth and development of plants and
protecting plants against phytopathogens
(Rocha et al. 2019b). PGPB increase
plant tolerance to environmental stresses and facilitate plant growth
through direct and indirect mechanisms. Direct mechanisms by PGPB
include expanding root growth, fixation of atmospheric nitrogen
(Bloch et al. 2020), solubilization of
mineral nutrients (e.g., phosphate, potassium)
(Adnan et al. 2020), and production of
phytohormones (e.g., auxins, cytokinins, and gibberellins)
(Sudewi et al. 2020), iron-chelating
siderophores (Kramer et al. 2020), and
organic acids. Indirect mechanisms can be neutralized or modify the
harmful effects of plant pathogens by producing various antagonistic
compounds, such as extracellular lytic enzymes, hyperparasitism,
antibiotics, siderophores, and hydrogen cyanide
(Emmanuel and Babalola 2020).Bacillus sp. such as B. amyloliquefaciens , B.
subtilis , and B. sphaericus can breed resistance in plants
against viral diseases (e.g., cucumber mosaic virus on tomato)
(Kloepper et al. 2004).
Arbuscular mycorrhizal
fungi
In agricultural and natural ecosystems, as biologically beneficial
fungi, AMF can create an interaction of physical between plant roots and
soils, which represent an essential part of agricultural ecosystems
(Khan 2005). Nearly 90% of AMF can form
symbioses with plant roots (Ortas and
Bykova 2018, Paravar et al. 2022),
contributing significantly to increasing plant uptake of macro and
microelements in soils under environmental stress
(Ghanbarzadeh et al. 2020) and to
improving soil density to create a protective barrier from pathogens and
enhance water acquisition (Rocha et al.
2019a). AMF can also protect crops against environmental stresses
(Langeroodi et al. 2020). For instance,
under drought stress, AMF may increase plant water uptake and turgor
maintenance associated with osmotic balancing, and root hydraulic
conductivity (Langeroodi et al. 2020,
Zou et al. 2020). Overall, AMF play a
beneficial role in producing metabolites such as essential oil
(Pirzad and Mohammadzadeh 2018), fatty
acids (Rahimzadeh and Pirzad 2019),
phytohormones (Kadam et al. 2020), amino
acids (Zhang et al. 2020), antioxidant
enzymes (Piri et al. 2019,
Zou et al. 2020), and adjusting plant
physiological statuses such as carbon dioxide exchange amount
(Thirkell et al. 2020), stomatal
conductance (Boutasknit et al. 2020),
photosynthetic
pigments, proline content (Alam et al.
2019), and phenolic content (Bencherif et
al. 2019). It has been demonstrated that AMF can enhance photosynthesis
activities and stomatal movement by developing the root systems
(Gholinezhad and Darvishzadeh 2021).
Indeed, root colonization by mycorrhizal mycelium not only bolsters the
root systems but also facilities the absorption of water and nutrient
from larger soil volumes against drought stress
(Paravar et al. 2021). Additionally, a
raised nutrients uptake especially phosphorous by developing root system
can provide the essential ATP and NADPH, which support oil and fatty
acids biosynthesis (Rezaei-Chiyaneh et
al. 2021). Some researchers reported that AMF can decrease the
accumulation of ROS by increasing flavonoids, carotenoids, anthocyanins,
and phenols under water deficit (Jerbi et
al. 2022).
Other beneficial microorganisms are Trichoderma(Coninck et al. 2020) which can be
applied as biological control generalists of plant diseases and
pathogenic fungi with a well-shielded cropping system
(Yang et al. 2017). They can control
pathogens by absorption of released nutrients (known as mycoparasitism)
(Kim et al. 2021), production of
antibiotics (e.g., aldehydes, alcohols, ketones, hydrogen cyanide, and
heterocyclic nitrogen) (Daryaei et al.
2016), and generation of degrading enzymes (e.g., crystalline
cellulose-hydrolyzing enzyme and b-glucosidase) in the cell wall
(Kthiri et al. 2020). Trichodermaspecies can colonize the rhizosphere at the critical “early
germination” stage, contributing significantly to improving nutrient
uptake and plant resistance to various stresses (e.g., heavy metal,
salt, and drought stresses) (Lutts et al.
2016) and they can serve as usual fungi of soil and rhizosphere to
replace chemical seed treatment (Kthiri et
al. 2020).
Microbial
consortia
Association between microorganisms and host plants can keep soil
fertility and plant health, especially in low-input agriculture, which
depends on biological prices than agrochemicals
(Sessitsch and Mitter 2015). Indeed, in
the microbial consortium, microbial species can perform synergistic
interaction and give benefit each other. Some strains can maintain the
non-producing strains against drought stress by producing secondary
metabolites, such as exopolysaccharides
(Lau et al. 2022). A study showed that
microorganisms belonging to the roots of grapevine and olive plants can
improve the growth of Orize sative L. This enhancement may be due
to the extensive roots system and increased water uptake ability
(Yoolong et al. 2019). In addition, it
has been found that using humic acid and PGPR (B.megaterium andB. subtilis ) enhanced the plant height and yield compared with
untreated control. Indeed, Humic acid and PGPR enhanced the
photosynthesis process by promoting stomatal conductance and stomatal
density, thereby, improving the yield
(Ansari et al. 2019). Also, it has been
reported that the application of PGPB and N-fixing bacteria caused the
improvement of root growth and resilience of plants against
environmental stresses, as well as decreased N losses
(Dal Cortivo et al. 2017) PGPB can be
used in the formation of ameliorating nodules in legumes when
co-inoculated with rhizobia (Rocha et al.
2019a). It has been found that Bacillus polymyxa andAzospirillum brasilense increased root colonization byGlomus aggregatum , and promoted biomass and phosphorus amount of
palmarosa grass grew under irresoluble inorganic phosphate source
(Oliveira et al. 2017).
PBM inoculation on plant
growth
Nutrients
Mixed or separate microorganisms can be inseminated within leaves,
seeds, seedlings, roots, or soils. These inoculations cause the
colonization of the rhizosphere or the inside of the plant, as well as,
growth and toleration across abiotic stress stimulation
(Lopes et al. 2021). PBM inoculation
directly improves plant growth and productively, tolerance to abiotic
stresses (e.g., drought, salt, and extreme temperatures) by increasing
nutrient uptake, producing exopolysaccharides, osmoregulators, and
antioxidants, regulating phytohormones (e.g., auxin, gibberellin,
cytokinin, abscisic acid, and ethylene)
(Lichtfouse et al. 2009) and/or
indirectly protect plants against abiotic stresses by inducing systemic
resistance, as well as producing siderophore and volatile metabolites
(Abhilash et al. 2016). Due to the
increase in reactive oxygen species (ROS) production, peroxidation of
lipids, free radical accumulation and elevated ethylene production,
plant growth is inhibited during drought stress. Hence, the above events
resulted in cell death and decreasing in photosynthetic rates and
chlorophyll content. Also, PBM inoculation can positively affect
germination indices of seed, seedling and early growth characteristics,
root development and improve crop biomass and productivity
(Moradtalab et al. 2020,
Sharma et al. 2012).
It has been proved that PBM can be used as biofertilizers to increase
the stock of macro and micro-elements, boost plant growth and decrease
the application of chemical fertilization
(Ghanbarzadeh et al. 2020). Since the
essential nutrients for plants mainly include nitrogen, phosphorus, and
iron, among PBM selection tests, nitrogen fixation, phosphate
solubilization, and siderophore production are widely investigated
(Lopes et al. 2021). One of the essential
macro-elements for synthesizing proteins and nucleic acids is nitrogen.
It has been reported that PGPB strains such as Azospirillum ,Azotobacter , Achromobacter , Rhizobium andKlebsiella can fix biological nitrogen via decreasing nitrogen
gas (N2) to ammonia (NH3)
(Souza et al. 2015). Moreover,
phosphorus is an urgent plant nutrient for growth, which participates as
a structural ingredient of nucleic acids, phospholipids, and adenosine
triphosphate (ATP) (Khan et al. 2009,
Maleki Farahani et al. 2019). Some PGPB
strains such as Rhizobium , Bacillus , Pseudomonas ,Azotobacter , and Azospirillium can dissolve phosphate and
convert insoluble organic and inorganic phosphate into available plant
form, which are called phosphate-solubilizing bacteria
(PSB)(dos Santos et al. 2020;. Organic
acids (gluconic or keto-gluconic acids) produced by PSB along with their
carboxyl and hydroxyl ions chelate cations and reduce pH to release
phosphorus (Sharma et al. 2013).
Furthermore, PGPB act a main role in metabolic and biochemical pathways,
especially for biological nitrogen fixation and photosynthesis
(Richardson and Simpson 2011). It is
known that large proportions of soil-phosphorus remain interlocked in
various insoluble forms and are unavailable for plants. PBM can decrease
soil pH through execration of organic acids such as gluconate, citrate,
lactate, and succinate that leads to the acidification of the
surroundings and microbial cells, therefore, phosphorus ions are
released by substitution of H+ for
Ca2+ (Martínez-Viveros
et al. 2010). In addition, iron is one of the essential micro-elements
for the biosynthesis of chlorophyll, photosynthesis, and respiration. As
a chelator, siderophores have a great specificity to bind iron,
continued by the transport and deposit of Fe3+ in
bacterial cells (Dimkpa et al. 2009).Burkholderia , Enterobacter , Grimontella , andPseudomonas can be used as siderophore producers to promote plant
nutrition and inhibit phytopathogens via sequestration of free
environmental iron (Souza et al. 2015).
Phytohormones
Phytohormones are organic compounds that are responsible for plant
development. PBM can modulate phytohormones, such as auxins, cytokinins,
gibberellins, abscisic acid, ethylene, salicylic acid, brassinosteroids,
jasmonates, polyamines, and strigolactones
(Santner et al. 2009). A study reported
the increased auxin and gibberellin in leaves of Zea maysinoculated by PGPB (Khan et al. 2016).
The negative effects of drought, chilling, heat, or salinity stress can
be alleviated by PBM inoculation via auxin production, gibberellin,
cytokinin, ACC deaminase, abscisic acid strigolactones, and jasmonates
(Khan et al. 2020). It has been
demonstrated that PBM inoculation increased auxin concentration in
plants and improved the growth of various plant species (e.g., Zea
mays , Brassica juncia , Fagopyrum esculentum , andSaccharum officinarum ) by improving uptake of water and nutrient
(Gouda et al. 2018). The auxin produced
by PBM is a beneficial phytohormone that regulates cell division
(Sarkar et al. 2017). PBM can improve
plant-related parameters (e.g., seed germination, development of leaves,
stem, flower and fruit) by enhancing gibberellin
(Zerrouk et al. 2020). Under saline
conditions, PBM inoculation can increase the concentrations of abscisic
acid, jasmonates, and brassinosteroids in plants
(Arora et al. 2020).
Exopolysaccharides
Microorganisms can form a productive biofilm on the root surface by
producing exopolysaccharides (Banerjee et
al. 2019). In this way, this mechanism causes the increase of water
keeping in soil particles and maintains soil moisture in the
rhizosphere. In addition, Streptococcus epidermidis can protect
the cells of plant roots against osmotic stress and enhance
environmental stress tolerance (Banerjee
et al. 2019). It was suggested that Pseudomonas putida strain
GAP-P45 as an exopolysaccharide producing bacterium can cause the
biofilm formation on the root surface in Helianthus annuusseedlings and increase tolerance of seedlings against drought stress
(Naseem et al. 2018). In addition, other
studies have demonstrated that proline accumulation, sugars and free
amino acids increased in plants inoculation by exopolysaccharides
producing bacterium Pseudomonas aeruginosa andAzospirillum spp. under drought stress
(Bano et al. 2013,
Gusain et al. 2015,
Rana et al. 2020).
Antioxidants
The PBM can enhance antioxidant enzymes activities such as ascorbate
peroxidase (APX), catalase (CAT) and superoxide dismutase (SOD), and
antioxidant non-enzymes such as glutathione (GSH), carotenoids,
tocopherols, and phenolics to alleviate ROS accumulations that are
caused by various stresses (Fazeli-Nasab
et al. 2021, Gouda et al. 2018).
Increased activity of CAT and APX due to inoculation of Cuminum
cyminum seeds with Pseudomonas fluorescens and Trichoderma
harzianum under drought stress conditions has been reported
(Piri et al. 2019). Linum
usitatissimum inoculation with P. fluorescens enhanced
antioxidant enzymes such as CAT, APX, and GSH in storage conditions
(Gafsi et al. 2006).
Osmoregulants
Against drought and salinity stresses, microbial inoculants can produce
osmoregulants such as carbohydrates, proteins, amino acids lipids,
proline, glycine betaine, and trehalose
(Van Oosten et al. 2017). Osmoregulants
induce the stabilization of protein and membrane structure under
dehydration conditions, maintain osmotic balance across the membrane,
and ensure protein correct folding under salinity stress
(Sharma et al. 2012). It has been found
that Burkholderia phytofirmans . can increase plant
tolerance across low temperatures by modifying carbohydrate metabolism
(Fernandez et al. 2012). Also,Pseudomonas fluorescens has been found to promote plant tolerance
against water stress by enhancing catalase and peroxidase enzyme
activities and proline accumulations
(Saravanakumar et al. 2011).
Inoculation methods of
PBM
Different methods of PBM inoculation on host plants can affect the
survival and reproduction of microbes crowded into the rhizosphere and
their ability to promote plant growth
(Strigul and Kravchenko 2006). Due to
the fact that the mobility of microorganisms in the soil is low,
microbial inoculants should be placed in the vicinity of the
rhizosphere. To spread microbial inoculants around the rhizosphere,
nematodes can be used as a vector for their inoculation
(Msimbira and Smith 2020). Except for
inoculant density and methods of inoculation, the response of the plant
to PBM inoculation and their colonization is also important for
microbial functioning (Venturi and Keel
2016). After inoculation, the reduction of microbial population in the
rhizosphere may be due to unadapted microorganisms to their new
environment. However, root exudations play a critical role in microbial
growth. Besides, biotic and abiotic factors can also affect the
functional variety of microbial populations
(Strigul and Kravchenko 2006). Microbial
inoculation can be carried out with a single isolate or microbial
consortia (e.g., co-inoculation). It was found that co-inoculation
improves the efficiency of inoculation and plant development
(Lopes et al. 2021). Different methods
including seed, soil, root, and foliar inoculation are used to inoculate
plants with PBM (Fig. 1; Table 1).
Table 1. Effects of different methods of PBM inoculation on
plant growth