Article Type : Review Article
Authors : Rehman F , Kalsoom M, Adnan M, Toor MD and Zulfiqar A
Keywords : PGPR; Phytohormones; Phosphate solubilizing bacteria; Induced systemic resistance; Siderophore
On the basis of phenotypic and genetic diversity, it
is very difficult to characterize the soil microbial communities. Bacteria that
are associated with the plant roots and have ability to promote the growth of
plant are called Plant Growth Promoting Rhizobacteria (PGPR). Firstly, these
plant growth promoting rhizobacteria inhance the growth of the plant. Secondly,
they have antagonistic activities as biocontrol agents. The growth of the plant
is enhanced through plant growth promoting rhizobacteria directly by fixing the
atmospheric nitrogen, solubilization of insoluble phosphate and secretions of
hormones including IAA, kinetics and GAs. They also facilitate the plant growth
indirectly by production of induced systemic resistance, production of
siderophore, production of antibiotics and lytic enzymes, HCN production and
regulation of stress conditions. This review article thoroughly explains the
direct and indirect mechanisms of action of PGPR.
Bacteria that have ability to colonize plant roots and promote the growth of plant are categorised as plant growth-promoting rhizobacteria (PGPR) [1,2]. Soil microbial communities are so complex and very difficult to characterize because of their immense phenotypic and genotypic diversity [3]. In recent years, a number of PGPR have been identified have a great impact of plants growth mainly because of their role as an ecological unit as in rhizospheric zone has gained importance in the functional activities of the biosphere. PGPR directly influence the growth promotion of plants by Solubilizing insoluble phosphates, fixing atmospheric nitrogen, secreting hormones which helps in regulation of plant growth [4]. PGPR indirectly benefits plant growth by Induced systemic resistance (ISR), competition for nutrients, antibiosis, parasitism and production of metabolites suppressive to deleterious rhizobacteria [5]. PGPR is highly diverse community and their effects can occur through local antagonistic action against the soil-borne pathogens and through induction of systemic resistance against pathogens in the entire plant [6]. Several substances are produced by antagonistic rhizobacteria which have ability to control the pathogen and also have indirect promotion of growth in many plants. The Induced systemic resistance (ISR) in plants resembles pathogen-induced systemic acquired resistance (SAR) under conditions where the inducing bacteria and the challenging pathogen remain spatially separated [7]. Both types of induced resistance make the uninfected plant parts more resistant to pathogen attack in several plant species. Resistance is induced by Rhizobacteria through the salicylic acid-dependent SAR pathway or through require jasmonic acid and ethylene perception from plant for ISR. Rhizobacteria belongs to the genera of Pseudomonas and Bacillus and are well known for their antagonistic effects and their ability to trigger ISR [8]. In few last years, considerable attention has been made to replace agrochemicals (fertilizers and pesticides) with to PGPR for the plant growth promotion through various mechanisms [9] that involved in formation of soil structure, recycling of essential elements, decomposition of organic matter, solubilization of mineral nutrients, degrading organic pollutants, stimulation of root growth, producing numerous plant growth regulators, crucial for soil fertility, promoting changes in vegetation and biocontrol of soil and seed borne plant pathogens. An understanding of both plant growth promoting rhizobacteria and their interactions with biotic and abiotic factors is very important in bioremediation techniques, energy generation processes and in biotechnological industries including pharmaceuticals, chemical and food [10]. Plant growth promoting rhizobacteria also reduce the application of chemical fertilizers and that is economically and environmentally beneficial for lower production cost as well as recognize the best management practices of soil and crop to achieve more sustainable agriculture as well as fertility of soil [11].
Plant growth promotion is well-known and an important phenomenon done plant growth promoting rhizobacteriaand amd this growth enhancement is because of the certain traits of rhizobacteria [12]. There are a lot of mechanisms through which PGPR can enhance plant growth and development in diverse environmental conditions. Plant growth promoting rhizobacteria alter the whole microbial community in rhizospheric zone through the production of various substances [13]. Commonly, PGPR promotes plant growth directly on the bases of their ability for supply of nutrient (nitrogen, phosphorus, potassium and essential minerals) or through production of plant hormone levels. PGPR can also bring the plant growth by indirectly through decreasing the inhibitory effects of various pathogens on growth and development in the forms of biocontrol agents, environmental protectors and root colonizers [14]. Phytopathogenic microorganisms have a major and chronic threat to sustainable agriculture and ecosystem stability because they subvert the soil ecology, degrade soil fertility, disrupt environment and consequently show harmful effects on human health and contaminating ground water [15]. PGPR having direct mechanisms facilitate the plant in nutrient uptake or increase nutrient availability through the process of nitrogen fixation, mineralize organic compounds, solubilization of mineral nutrients and production of phytohormones [16]. PGPR is very important in sustainable and environmentally friendly approach to obtain sustainable fertility of the soil and plant growth indirectly. This approach results in wide range of exploitation of PGPR to decrease the need for agrochemicals including fertilizers and pesticides for improve soil fertility through a variety of mechanisms including production of antibiotics, HCN, siderophores and hydrolytic enzymes.
Biological fixation of
nitrogen
Nitrogen is an
important element for life. It is present in the structures of essential
biochemicals like nucleotides and proteins [17]. Although there is a high
concentration of N2 in air in gaseous form but plant cannot use nitrogen in
this form [18]. Biological nitrogen fixation is the main process by N?fixing
bacteria convert N2 into ammonia which can be used by plants as a nitrogen
source. As there is the small quantity of fixed nitrogen that is available for
plant [19]. Therefore, farmers have to apply nitrogen containing fertilizers to
sustain their agriculture. This utilisation of huge amount of chemicals is not
affordable for the farmers and it also have negative impacts on the environment
[20]. These deficiencies can be fulfilled by using PGPR and providing needed
nitrogen by the BNF. This can be an alternative way for farmers to increase
agricultural yield [21].
The production of
biological fixed nitrogen is not limited to the PGPR forms symbiotic nodules
with legumes; it can also be produced by non-symbiotic free living nitrogen
fixing bacteria such as Azospirillum, Azotobacter, Azoarcus, Bacillus polymyxa,
Gluconoacetobacter, Burkholderia and Herbaspirillum [22].
Production of
phytohormones
Phytohormones are the
one of the most important plant growth substances. They are plant hormones that
have a great influence on the responses of plant against its environment [23]. The
production of these hormones occur at one location in the plant and then is
transferred to the other location where they work to enhance the plant growth.
The physical responses due to these hormones results in the growth of roots and
leaves [24].
There are several most
important types of phytohormones. These are auxins, gibberellins, ethylene,
cytokinins and abscisic acid [25]. Plant growth promoting rhizobacteria usually
produces these phytohormones.
Cytokinins production: Cytokinins (CK) are a class of
phytohormones that have vital role in promoting the cell division in plant
roots and shoots [26]. They are mainly involved in cell growth, cell
differentiation, apical dominance, axillary bud growth and leaf senescence
[27]. Actually this hormone is synthesized by the plant but some of PGPR and
yeast strains can also prepare this hormone. Some phytopathogens can also
synthesize cytokinins. Various bacteria including Azotobacter spp., Pantoea
agglomerans, Rhizobium spp., Rhodospirillum rubrum, Bacillus subtilis,
Pseudomonas fluorescens and Paenibacillus polymyxa are reported to produce
cytokinins hormone [28].
Gibberellin production: Gibberellins (GAs) are hormones produced in plants
that regulate various process of development in plant. They play vital role in
stem elongation, dormancy, germination, flowering, flower development and leaf
and fruit senescence. GAs are one of the most important class of plant hormone.
Gibberellins are involved in the process of breaking dormancy and other aspects
of germination. Gibberellin is most important phytohormone that is synthesized
by some cytokinin-producing PGPR [29]. The gibberellin and cytokinin mechanisms
for bacterial production and regulations are of the great importance.
Indole-3-Acetic Acid Production: IAA is one of the most important
phytohormone produced by plants and PGPR. It has vital role in plant cellular
responses including cell division, gene expression, organogenesis, pigment
formation, root development, seed germination, stress resistance of plants,
tropic responses and photosynthesis [30]. IAA can work both as inhibitors and
stimulators. The required amount of IAA for the plant growth promotion is
greatly influenced by plant species and bacterial species. Since
Indole-3-Acetic Acid is responsible for root formation and lengthening. IAA is
widely produced by the activity of PGPR [31].
Ethylene production: Ethylene is a plant growth hormone produced by
almost all plants and plays a vital role in many of physiological changes in
plants at molecular level. The production of ethylene is stimulated by plant
responses to biotic and abiotic stresses that have adverse effects of on root
growth and as a result on the whole plant growth [32]. PGPR have certain enzyme
such as 1-aminocyclopropane-1-carboxylate (ACC) deaminase, that have ability to
regulates ethylene production. PGPR Inoculation is very helpful to maintain the
plant growth and development under stress conditions.
Abscisic acid production: Abscisic acid is the plant growth
hormone that is synthesized by plants when it is under abiotic stresses like
stresses due to drought, salt stress, cold or soil pollution etc. It activates
the stress resistance genes. Several strains of PGPR synthesize Abscisic acid
[33]. When plants are inoculated with Abscisic acid-producing strains i.e.
Bacillus licheniformis Rt4M10, Azospirillum brasilense Sp 245, Pseudomonas
fluorescens Rt6M10, the internal content of ABA is increased. Thus the plant
becomes more resistant to drought. Thus PGPR helps the plant to regulate the
growth.
Phosphate solubilizing
bacteria
Nitrogen is not the only important element for
life of which unavailability can limit the plant growth. Phosphorus is also an
important for the plants. Soil has large amounts of phosphate, but it is found
in insoluble form that can not be utilized by the plants for growth. Some PGPR
have ability to solubilize the phosphate in the soil by the mechanism of
acidification, chelation, or enzymatically [34]. For example, Gluconacetobacter
diazotrophicus is a PGPR present in sugarcane and can solubilize phosphate
through acidification.
Antibiotics and lytic
enzymes production for biocontrol
It is well known that
there is a great compitition between microorganisms for nutrients and
colonization sites in their natural environments. Many PGPR species have
ability and have evolved various mechanism to reduce competition by releasing
of antibiotics, lytic enzymes or weak organic acids to their environment [35].
Due to this, PGPR is a valuable tool and can be used against plant pathogens.
The increased use of antibiotic producing bacteria can result in development of
resistant strain of pathogens. The enzymes secreted by PGPR are utilized to
eliminate pathogens [36] like Botrytis cinerea, Fusarium oxysporum, Sclerotium
rolfsii, Phytophthora spp., Pythium ultimum and Rhizoctonia solani. These
secreted enzymes are cellulates, chitinases, lipases and proteases.
Production of induced
systemic resistance (ISR)
Systemic acquired
resistances and Induced systemic resistance are evolved mechanisms of response
in plants against pathogens. Systemic acquired resistance is a resistance that
is triggered when a pathogen infects a plant and Induced systemic resistance is
a resistance that is triggered by the PGPR. ISR appears to be same as of
systemic acquired resistance (SAR) [7]. When the inoculum of PGPR is applied to
the plant, the PGPR induce a resistance in that plant against many of the bacterial
pathogens. It results in induced systemic resistance.
Siderophore production
Iron is another
important nutrient for plants. In aerobic conditions, iron is present as Fe3+
form which is not soluble to be used by microorganisms and plants. Some
microbes produce and secrete low mass iron chelators. These chelators are known
as siderophores. They have high affinity for iron. They work as solubilizing
agents for Fe3+ in limiting conditions. Fe3+ becomes Fe2+
which is then unbind from the siderophores inside the cell [37]. Siderophore
production works as a biocontrol mechanism, since with this process, plant
growth promoting rhizobacteria derives other microorganisms from iron [38].
PGPR also use siderophores to obtain other heavy metals from the soil and prevents
the heavy metal to cause toxicity in plants. It can be used for bioremediation
of the heavy metal toxic soil.
Regulation of stress
conditions
Ethylene is a
phytohormone. It is also secreted in the response of biotic and abiotic
stresses from salt, drought or pathogenic bacteria. Although it promote the
growth of plant and help in ripping of fruits, the high amounts ethylene also
have harmful effects on the plant. Many PGPRs synthesis an enzyme i.e. ACC
deaminase [39]. This enzyme destroys the precursor of ethylene and which is
1-aminocyclopropane-1-carboxylate. It results in decreasing the ethylene levels
that relieve the stress of the plant.
HCN production
The harmful
rhizobacteria can work as biocontrol agents of weeds. They colonize plant root
surfaces and suppress their growth. Cyanide are toxic and are produced by many
of microorganisms including bacteria, algae, fungi and plants. They work as a
means of survival by competing with counterparts. There is no any negative
impact on the host plants by inoculation with cyanide-producing bacterial
strains [40]. The host-specific Rhizobacteria can work as biological weed
control agents. Many of the secondary metabolite are also produced which act as
an effective agent for the biocontrol of weeds. HCN is mostly synthesized by
Pseudomonas and Bacillus species. HCN inhibits electron transport chain and
energy supply to cell [41]. This disturbance results in the death of cells.
Competition
PGPR often compete with
the many of the harmful microbes for the nutrition uptake. These nutrients are
present in trace amount, therefore, they can limit the disease causing agent
[42]. When there are abundant non-pathogenic microbes present in the soil and
rapidly colonize the surfaces of plants and also utilize nutrient available. This
utilization of nutrients will inhibit the growth of pathogenic microbes. These
mechanisms are difficult to study in the system. The competition for the
nutrient between PGPR and pathogens is one of the important interaction that
indirectly supports the growth of the plants by inhibiting the growth of
pathogens [43].
PGPR is one of the most
important and safe means of agriculture to increase the yield. It is a
promising solution to meet the requirements of higher yield [44]. The most
important thing is that it protects plants from chemicals that are applied to
control the pests and also cause harmful impacts on the ecosystem. PGPR can
also improve the yield by controlling various plants diseases and pests as
diseases are responsible for huge losses of plant yield. PGPR have beneficial
effects on laboratory as well as greenhouse experiments [45]. Genetic
engineering is an emerging field to improve and explore the uses of PGPR
strains. Besides all the advancements, there are some environmental barriers
and adverse conditions that greatly influence the activity of PGPR. The
problems of varying efficacy of PGPR can be improved by strain mixing, using
improved inoculation techniques and gene transfer of active genetic source of
antagonists to the host plant. Various diverse conditions can also influence
the PGPR action as biocontrol because biocontrol agents need specific
ecological environment for growth and survival. Hence under diverse ecological
niche, the efficacy of biocontrol agents could be changed by the usage of
compatible mixed inoculum of biocontrol agents. Other then these beneficial
aspacts, there are several challenges faced by PGPR [46]. The natural variation
is a main problem because it is difficult to predict how bacteria will act in
laboratory and what will be it's action when placed in field. These variations
can affect the whole experiment. Another challenge is that the propagation of
PGPR to regain their viability and biological activity e can vary according to
the plant type and season [47].
The use of PGPR has
resulted in significant improvement in growth, health and yield of plants. The
PGPR can stimulate the improvements in growth, health and yield of plants by
direct or indirect mechanism of PGPR action. PGPR can also improve growth of
plant by reducing the activities of phytopathogens which reduce the yield and
growth. The result of PGPR inoculation can vary according to the plant age and
the chemical, physical and biological properties of the soil. There are several
challenges for making their commercial uses. This can be overcomed by using
advance techniques and applying biotechnology to reduce the challenges faced by
PGPR. Hence one day the use of PGPR will replace the use of chemical
fertilizers.