Biotechnology Advances 32 (2014) 429–448
Contents lists available at ScienceDirect
Biotechnology Advances
journal homepage: www.elsevier.com/locate/biotechadv
Research review paper
The role of mycorrhizae and plant growth promoting rhizobacteria
(PGPR) in improving crop productivity under stressful environments
Sajid Mahmood Nadeem a, Maqshoof Ahmad b, Zahir Ahmad Zahir c,⁎, Arshad Javaid d, Muhammad Ashraf e
a
Burewala Sub-campus of University of Agriculture Faisalabad, Burewala, Pakistan
University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan
Institute of Soil & Environmental Sciences, University of Agriculture, Faisalabad 38040, Pakistan
d
Institute of Agricultural Sciences, University of the Punjab, Lahore, Pakistan
e
University College of Agriculture, University of Sargodha, Sargodha, Pakistan
b
c
a r t i c l e
i n f o
Article history:
Received 15 April 2013
Received in revised form 17 December 2013
Accepted 19 December 2013
Available online 28 December 2013
Keywords:
Mycorrhizae
PGPR
Interactions
Stress
Plant
Growth
a b s t r a c t
Both biotic and abiotic stresses are major constrains to agricultural production. Under stress conditions, plant
growth is affected by a number of factors such as hormonal and nutritional imbalance, ion toxicity, physiological
disorders, susceptibility to diseases, etc. Plant growth under stress conditions may be enhanced by the application of microbial inoculation including plant growth promoting rhizobacteria (PGPR) and mycorrhizal fungi.
These microbes can promote plant growth by regulating nutritional and hormonal balance, producing plant
growth regulators, solubilizing nutrients and inducing resistance against plant pathogens. In addition to their interactions with plants, these microbes also show synergistic as well as antagonistic interactions with other microbes in the soil environment. These interactions may be vital for sustainable agriculture because they mainly
depend on biological processes rather than on agrochemicals to maintain plant growth and development as
well as proper soil health under stress conditions. A number of research articles can be deciphered from the literature, which shows the role of rhizobacteria and mycorrhizae alone and/or in combination in enhancing plant
growth under stress conditions. However, in contrast, a few review papers are available which discuss the synergistic interactions between rhizobacteria and mycorrhizae for enhancing plant growth under normal (nonstress) or stressful environments. Biological interactions between PGPR and mycorrhizal fungi are believed to
cause a cumulative effect on all rhizosphere components, and these interactions are also affected by environmental factors such as soil type, nutrition, moisture and temperature. The present review comprehensively discusses
recent developments on the effectiveness of PGPR and mycorrhizal fungi for enhancing plant growth under
stressful environments. The key mechanisms involved in plant stress tolerance and the effectiveness of microbial
inoculation for enhancing plant growth under stress conditions have been discussed at length in this review.
Growth promotion by single and dual inoculation of PGPR and mycorrhizal fungi under stress conditions have
also been discussed and reviewed comprehensively.
© 2014 Elsevier Inc. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Plant growth under stress conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Nitrogen fixation under stress conditions . . . . . . . . . . . . . . . . . . . . . . .
Strategies to mitigate the adverse effects of stresses . . . . . . . . . . . . . . . . . . . . . .
3.1.
Plant adaptations/defense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Plant growth promoting rhizobacteria (PGPR) . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Beneficial aspects of PGPR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Harmful aspects of PGPR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3.
Mechanisms employed by PGPR to mitigate stress-induced adverse effects on plants . . .
Mycorrhizae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1.
Mechanisms used by mycorrhizae to mitigate stress-induced adverse effects on plant growth
⁎ Corresponding author. Tel.: +92 41 9201092; fax: +92 412409585.
E-mail address: [email protected] (Z.A. Zahir).
0734-9750/$ – see front matter © 2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.biotechadv.2013.12.005
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S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
6.
Inducing stress tolerance through microbial inoculation . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.1.
Stress tolerance through PGPR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.2.
Stress tolerance through mycorrhizae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.2.1.
Mycorrhizae and nitrogen fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.
Synergistic role of PGPR and mycorrhizal fungi in stress tolerance . . . . . . . . . . . . . . . . . . . . . . .
8.
Inducing stress tolerance through combined inoculation of PGPR and mycorrhizae (PGPR–mycorrhizae interactions)
9.
Mycorrhizae–PGPR application and constraints under natural environmental conditions . . . . . . . . . . . .
10.
Conclusion and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
The rhizosphere is a soil volume that is under the influence of plant
root. Hiltner (1904) described the term ‘rhizosphere’ for the first time as
a zone of maximum microbial activity. The microbial population present
in this environment is relatively different from that of its surroundings
due to the presence of root exudates that serve as a source of nutrition
for microbial growth (Burdman et al., 2000). The microorganisms may
be present in the rhizosphere, rhizoplane, root tissue and/or in a specialized root structure called a nodule. Very important and significant interactions were reported among plant, soil, and microorganisms present in
the soil environment (Antoun and Prevost, 2005). These interactions
may be beneficial, harmful and/or neutral, and can significantly influence plant growth and development (Adesemoye and Kloepper, 2009;
Ahmad et al., 2011a; Lau and Lennon, 2011).
The microorganisms colonizing plant roots generally include bacteria, algae, fungi, protozoa and actinomycetes. Enhancement of plant
growth and development by application of these microbial populations
is well evident (Bhattacharyya and Jha, 2012; Gray and Smith, 2005;
Hayat et al., 2010; Saharan and Nehra, 2011; Zahir and Arshad, 1996).
Of different microbial populations present in the rhizosphere, bacteria
are the most abundant microorganisms (Kaymak, 2010). Various genera
of bacteria, Pseudomonas, Enterobacter, Bacillus, Variovorax, Klebsiella,
Burkholderia, Azospirillum, Serratia and Azotobacter, cause a pronounced
Environmental
Stresses
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effect on plant growth and are termed as plant growth promoting
rhizobacteria (PGPR). PGPR play a significant role in enhancing plant
growth and development both under non-stress and stress conditions
by a number of direct and indirect mechanisms (Glick et al., 2007;
Nadeem et al., 2010b; Zahir et al., 2004). The mechanisms that promote
plant growth include: nitrogen fixation, phosphorus solubilization, production of siderophores, plant growth regulators and organic acids as
well as protection by enzymes like ACC-deaminase, chitinase and
glucanase (Berg, 2009; Glick et al., 2007; Hayat et al., 2010).
In addition to bacterial population, fungi also represent a significant
portion of soil rhizosphere microflora and influence plant growth. The
symbiotic association generated by fungi with plant roots (mycorrhizae) increases the root surface area, and therefore enables the plant to
absorb water and nutrients more efficiently from large soil volume.
Two types of mycorrhizae i.e. ecto- and endo-myccorrhizae have been
reported in a number of plant species. The mycorrhizal association not
only increases the nutrient and water availability, but also protects the
plant from a variety of abiotic stresses (Evelin et al., 2009; Miransari,
2010). Mycorrhizae and PGPR play an important role in improving
plant growth through various mechanisms (Fig. 1).
Although microbial-inoculants are being widely used to improve
plant growth under controlled as well as natural field conditions, the results obtained from these studies did not attain a reasonable degree of
efficacy and consistency that is required for their commercialization
Negative impact on
growth
Salinity
Drought
Hormonal Imbalance
Heavy metals
Nutritional imbalance
Flooding
Ion toxicity
Pathogens
Desiccation
Temperature
Disease susceptibility
PGPR + AM
Mechanisms used by PGPR
Lowering of ethylene
Phytohormones Production
Exopolyscaccharides production
Induced systematic resistance
Siderophores production
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Mechanisms used by AM
Dualinoculation/
Interactive effect
Improved nutrition
Enhanced antioxidant system
Modification of root architecture
Enzyme production
Water use efficiency
Fig. 1. Mechanisms used by plant growth promoting rhizobacteria and mycorrhizae for enhancing plant growth under stress.
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
on a large scale. This might be due to the soil environment and microbial
populations that interact with one another and these interactions could
be vital for plant growth. Exploring the mechanisms of growth promotion by PGPR and mycorrhizae could be very useful for enhancing
plant growth by using these microbial populations together, particularly
under stressful environments. Although a number of studies have
shown that combined application of PGPR and fungi could be a meaningful approach for sustainable agriculture (Denton, 2007; Najafi et al.,
2012; Ordookhani et al., 2010), there are still certain aspects which
need further investigations for obtaining maximum benefits in terms
of improved plant growth from this naturally occurring population particularly under stress conditions.
Thus, the present review highlights and discusses the present
knowledge on the role of PGPR and mycorrhizal fungi in enhancing
plant growth under stressful environments. The major emphasis is
given to the basic mechanisms used by PGPR and fungi for promoting
plant growth as well as the interactions among these beneficial microbial communities. The effectiveness of inoculation with PGPR and mycorrhizal fungi alone as well as their combined inoculation on plant growth
under stress conditions has been reviewed and discussed in detail.
2. Plant growth under stress conditions
Soil is a complex and dynamic system that supports plant growth. In
the soil environment, plant growth and development is influenced by a
variety of stresses that are major constraints for sustainable agricultural
production. These stresses are biotic such as plant pathogens and pests
(viruses, bacteria, fungi, insects, nematodes, etc.) and abiotic including
salinity, drought, flooding, heavy metals, temperature, gases and nutrient deficiency or excess. Abiotic stresses are considered to be the main
source of yield reduction; however, the intensity of these stresses varies
with a number of soil and plant factors. Some of the general impacts of
these stresses on plant growth include hormonal and nutritional imbalance, and physiological disorders such as epinasty, abscission and senescence, and susceptibility to diseases (Ashraf, 1994; El-Iklil et al.,
2000; Nadeem et al., 2010b; Niu et al., 1995; Zhu et al., 1997).
Some stresses cause a particular direct or indirect negative impact
on plant growth and development. For example, under salinity, drought
and waterlogging stress, elevated levels of ethylene are produced (Glick
et al., 2007; Zapata et al., 2003) that are inhibitory to root growth and
therefore affect a number of plant processes (Belimov et al., 2002; Sun
et al., 2007). In addition, under salinity stress, ion toxicity occurs particularly due to excessive amounts of Na+ and Cl− that causes injurious effects on plant growth and development (Ashraf, 1994; Ashraf and
Khanum, 1997). Similarly, drought stress apart from increasing ethylene concentration also inhibits photosynthesis, causes changes in chlorophyll contents and damages the photosynthetic apparatus (IturbeOrmaetxe et al., 1998). Due to limited supply of water, root growth is
severely affected. Similarly, other stresses like salinity, heavy metals,
nutrient deficiency/excess, pathogen attack, etc. also cause negative
impact on plant growth and development in a number of ways like
disturbing hormone balance, susceptibility to diseases and causing
metal toxicity (Ashraf, 2003; Glick et al., 2007; Saleem et al., 2007).
2.1. Nitrogen fixation under stress conditions
As discussed earlier that environmental stresses like salinity,
drought and heavy metals cause detrimental effect on plant growth
and development. Most of the plant growth and yield parameters
are affected under stress conditions. These stresses affect the number of plant physiological and biochemical processes. Among these
processes, nitrogen fixation is one of the most important processes
that are severely affected under stress conditions. Saline conditions
induce adverse effects on nitrogen fixation thereby causing considerable reduction in crop yield. Salt stress not only inhibits the process of nodulation and nitrogen fixation (Elsheikh and Wood, 1995;
431
Zahran, 1999), but it also induces premature senescence of already
formed nodules (Swaraj and Bishnoi, 1999). For example, in soybean
it was observed that process of nodule initiation was extremely sensitive to 26 mM NaCl leading to a 50% decrease in nodulation and
total nodule weight per plant (Singleton and Bohlool, 1984). As salinity affects rhizobium colonization of root and early infection
events (Singleton and Bohlool, 1984; Zahran, 1999) therefore, reduced nodule formation in mungbean (Vigna radiata) plants at low
levels of salinity could be due to adverse effects on the process of
nodule initiation (Ahmad et al., 2011b, Ahmad et al., 2012).
Nabizadeh et al. (2011) observed a significant decrease in number
of active nodules and nitrogen content, relative water content and
leaf chlorophyll content in alfalfa (Medicago sativa) under salinity
stress. The adverse effects of salt stress on nitrogen fixation may be
due to salt-induced effect on the activity of rhizobia for infection of
legumes, effect on the growth and development of nodules and, finally direct effect on the activity of nodules for nitrogen fixation
(Bouhmouch et al., 2005). Although rhizobium is more tolerant to
salinity than a host plant, a great magnitude of variability among rhizobial strains with respect to salinity tolerance has been observed.
Nitrogenase enzyme is a major component in the process of nitrogen
fixation. Salinity stress is believed to significantly reduce the nitrogenase activity in microbes (Rai and Tiwari, 1999). Jofre et al. (1998) observed that high salt concentration decreased the biosynthesis of
nitrogenase. However, it is also generally known that the biosynthesis
of nitrogenase is inhibited more than nitrogenase activity (Tripathi
et al., 2002). Although low level of sodium (Na) is required for optimum
nitrogenase activity, sodium concentration up to 60 mM NaCl was
found to decrease the nitrogenase activity up to 50%, whereas complete
inhibition of nitrogenase activity occurred at 90 mM NaCl (Bhargava
et al., 2003).
Similar to salinity, drought is one of the major factors that affect nitrogen fixation and is one of the commonest stress factors affecting legume yields worldwide (Serraj, 2009). A number of grain legumes
show significant reduction in nitrogen fixation under water limited
conditions (Sinclair et al., 1987). Water stress not only affects nitrogen
fixation at earlier stage, but also causes a negative impact on already
formed nodules. When nodules are subjected to dry conditions, they
show retarded growth resulting in a partially developed root cortexembedded organ.
It is evident from the literature as discussed above that environmental stresses including both biotic and abiotic are detrimental for plant
growth. These stresses affect the plant growth and development by
causing adverse effects on morphological, physiological and biochemical processes. Many such processes are affected directly while a number
of others are indirectly affected under stress conditions.
3. Strategies to mitigate the adverse effects of stresses
A number of strategies to alleviate the stress-induced adverse effects
on plant growth have been described in many comprehensive reviews
(Evelin et al., 2009; Glick et al., 2007; Saharan and Nehra, 2011). For example, elevated levels of ethylene produced under stressful environments can be reduced by the application of ethylene inhibitor like
amino ethoxy vinyl glycine (AVG), cobalt ion (Co2 +) and silver ion
(Ag+), and plant growth can be enhanced by alleviating the adverse effects of high ethylene (Coupland and Jackson, 1991; Kim and Mulkey,
1997; Mckeon et al., 1995). However, these agrochemicals are expensive as well as toxic for human and soil health (Dodd et al., 2004). Furthermore, despite increasing crop yield, the use of such chemicals
results in lowering the net cash return for the farmers. There are also environmental concerns about the persistence of these chemicals in the
soil environment (Ahmadi et al., 2009). The other negative impacts of
stresses such as specific ion toxicity caused by salinity or root desiccation under drought stress may not be overcome by the use of these
chemicals.
432
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
Although plants employ some specific mechanisms to combat these
stresses, beneficial microbial populations in the rhizosphere also play a
significant role in reducing the intensity of a stress.
3.1. Plant adaptations/defense
Certain abnormalities may occur in plants under stress and their
intensity increases under such conditions. Plants adopt specific strategies to overcome the negative impact of a stress. In most of the
stress environments, reactive oxygen species (ROS) such as superoxide, hydrogen peroxide and hydroxyl radical are produced that are
detrimental for normal plant growth and development (Ashraf,
2009; Hajiboland and Joudmand, 2009; Mittler, 2002; RomeroPuertas et al., 2004). The presence of ROS can cause cellular damage
through oxidation of lipids and proteins, chlorophyll bleaching,
damage to nucleic acids, ultimately leading to cell death (Apel and
Hirt, 2004; Ashraf, 2009; del Rio et al., 2003; Herbinger et al.,
2002). Plants develop self defense mechanisms by producing antioxidant enzymes like superoxide dismutase, ascorbate peroxidase, glutathione reductase and catalase (Abdel Latef, 2011; Abdel Latef and
Chaoxing, 2010; Ashraf, 2009; Ashraf and Ali, 2008; Mittler, 2002).
The antioxidant system plays an important role in plant tolerance
against stress conditions and high concentrations of these antioxidative enzymes have been reported in tolerant species compared to
sensitive ones (Gill and Tuteja, 2010). The efficiency of antioxidant
defense systems is related to the degree of plant tolerance against a
stress (Tunc-Ozdemir et al., 2009). In addition to antioxidant enzymes, non-enzymatic antioxidants also protect the plant from
stress-induced adverse effects (Amirjani, 2012). Non-enzymatic
antioxidants include major cellular redox buffers, carotenoids, flavonoids, tocopherols, ascorbate, glutathione, etc. (Apel and Hirt, 2004).
In a saline environment, in addition to nutritional and hormonal imbalance, plant water uptake decreases due to changes in soil water
potential. Under such conditions, accumulation of compatible solutes like proline, glycine betaine, trehalose, polyols, and many
other such organic solutes, takes place in the plant body that plays
an important role to protect the plant from the stress-induced deleterious effects by osmotic adjustment, limiting water loss and diluting the concentration of toxic ions (Ashraf et al., 2013; Munns and
Termaat, 1986; Slama et al., 2006). Accumulation of compatible
solutes enables the plants to maintain their osmotic potential for enhanced uptake of water. For example, accumulation of proline in the
cell protects the plant by adjusting osmotic pressure as well as by
stabilizing many functional units like complex II of the electron
transport system, proteins and enzymes (Ashraf and Foolad, 2007;
Makela et al., 2000).
Plants also protect themselves from pathogens by the synthesis of
antimicrobial phytoalexins, hypersensitive reactions, induction of
hydrolytic enzymes and construction of defense barriers through gelatinous materials like lignin and suberin (González-Teuber, 2010; Luhova
et al., 2006). The enzymes like peroxidases have also been reported to
play an important role in lignification and suberization (Gaspar et al.,
1991; Hiraga et al., 2001). Plants also develop certain other selfdefense mechanisms to protect themselves from pathogen attack.
These include accumulation of secondary metabolites and synthesis of
defense proteins (Ashry and Mohamed, 2012; Castro and Fontes,
2005). Recently, Spaepen and Vanderleyden (2011) also reported that
the phytohormone auxin acts as a plant defense system against phytopathogenic bacteria.
The above discussion shows that under stress conditions plants
adopt certain strategies to reduce the negative impact of stress. Some
of these strategies include production of antioxidant enzymes, organic
solutes, induction of hydrolytic enzymes and the construction of defense barriers. These strategies help the plant to maintain its growth
under stress environment by mitigating the negative impact of stress
on plant growth and development.
4. Plant growth promoting rhizobacteria (PGPR)
An important group of microbial communities that exerts beneficial
effects on plant growth and development is called as PGPR (Kloepper
and Schroth, 1978). Rhizosphere is influenced by the physical, chemical
and biological processes of root, which is an ideal place for the proliferation of these microbes (Sorensen, 1997). These microorganisms generally exist more or less near the roots due to the presence of root
exudates, which are used as a source of nutrients for microbial growth
(Doornbos et al., 2012; Phillips et al., 2011; Whipps, 1990). Many of
these microorganisms depend on plant root exudates for their survival
(Glick et al., 1998).
4.1. Beneficial aspects of PGPR
The microorganisms termed as PGPR residing in the soil environment can cause dramatic changes in plant growth by the production
of growth regulators and/or improving plant nutrition by supplying
and facilitating nutrient uptake from soil (Zahir et al., 2004). In addition,
many of these rhizobacterial strains can also improve plant tolerance
against salinity, drought, flooding, and heavy metal toxicity and, therefore, enable plants to survive under unfavorable environmental conditions (Belimov et al., 2001; Glick, 2010; Ma et al., 2011; Mayak et al.,
2004b; Nadeem et al., 2007; Sandhya et al., 2009; Zahir et al., 2008). Although various free-living soil bacteria are considered as plant growth
promoting rhizobacteria, all bacterial strains of a particular genus do
not have identical metabolic capabilities for improving plant growth
to the same extent (Gamalero et al., 2009). A number of workers have
reported beneficial effects of these rhizobacteria for improving plant
growth under normal as well as stressful environment (Belimov et al.,
2009; Heidari and Golpayegani, 2012; Nadeem et al., 2010a,b;
Saravanakumar and Samiyapan, 2007; Tank and Saraf, 2010; Zahir
et al., 2004).
These rhizobacteria can be used in different ways when plant
growth promotion is required (Lucy et al., 2004). The two major ways
through which PGPR can facilitate plant growth and development include direct and indirect mechanisms (Glick et al., 1995). Indirect
growth promotion occurs when PGPR prevent or reduce some of the
harmful effects of plant pathogens by one or more of the several different mechanisms (Glick and Bashan, 1997). These include inhibition of
pathogens by the production of substances or by increasing the resistance of the host plant against pathogenic organisms (Cartieaux et al.,
2003; Nehl et al., 1997). For example, PGPR produce metabolites
which reduce pathogen population and/or produce siderophores that
reduce the iron availability for certain pathogens thereby causing reduced plant growth (Arora et al., 2001; Bhattacharyya and Jha, 2012;
Kloepper, 1996). Similarly, PGPR can also increase plant resistance
against diseases by changing host-plant vulnerability, through a mechanism called induced systemic resistance and therefore, provide protection against pathogen attack (Saravanakumar et al., 2007).
Direct growth promotion takes place in different ways like providing
beneficial compounds to the host plant synthesized by the bacterium
and/or facilitating the uptake of nutrients from the soil environment
(Kloepper et al., 1987). They also facilitate the growth of their host
plant by fixing atmospheric nitrogen, and synthesizing and secreting
siderophores which may solubilize and sequester iron thereby increasing its availability for plant uptake, producing phytohormones, and solubilizing minerals such as phosphorus so as to increase its availability
(Glick, 1995; Kloepper et al., 1989; Patten and Glick, 2002).
Despite these mechanisms, PGPR may also enhance plant growth
and development by the virtue of their key enzymes (ACC-deaminase,
chitinase) and also by the production of substances such as
exopolysaccharides, rhizobitoxine, etc. that help plants to withstand
stress conditions (Ashraf et al., 2004; Glick et al., 2007; Sandhya
et al., 2009). Rhizobitoxine is an inhibitor of ethylene synthesis
that enhances nodulation by diluting the negative impact of high
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
ethylene concentration (Vijavan et al., 2013). Moreover, many
rhizobacterial strains may have several traits and affect plant growth
by any one or more of these mechanisms. The effectiveness of these
strains also depends upon the host plant and soil characteristics
(Gamalero et al., 2010).
In general, PGPR may promote plant growth and development by
different ways. Some strains possess more than one mechanism and
can withstand not only the normal but also stressful environment. The
effectiveness of PGPR for promoting plant growth also depends upon
the interaction with host plant and soil environment besides their inherent capabilities.
4.2. Harmful aspects of PGPR
No doubt, rhizobacteria play an important role in maintaining soil
fertility and improving plant growth and development. This growth enhancement takes place by a number of mechanisms as discussed earlier,
although the reverse is true in some other studies (Alstorm and Burns,
1989; Saharan and Nehra, 2011; Suslow and Schroth, 1982). For example, the production of cyanide is a well known characteristic of certain
Pseudomonas species. The cyanide production by the bacteria is considered as growth promotion as well as growth inhibition characteristic.
On one hand, cyanide acts as a biocontrol agent against certain plant
pathogens (Martínez-Viveros et al., 2010) while on the other hand, it
can also cause adverse effects on plant growth (Bakker and Shippers,
1987). The auxin production by the PGPR can also cause positive as
well as negative effect on plant growth (Eliasson et al., 1989;
Vacheron et al., 2013; Young and Mulkey, 1997). The effectiveness of
auxin depends upon its concentration. For example, at low concentration, it enhances plant growth (Patten and Glick, 2002), whereas at
high level it inhibits root growth (Xie et al., 1996).
Similarly, rhizobitoxine produced by Bradyrhizobium elkanii has dual
effect. Since, it is an inhibitor of ethylene synthesis, so it can alleviate the
negative effect of stress-induced ethylene production on nodulation
(Vijayan et al., 2013). On the other hand, rhizobitoxine is also considered as plant toxin because it induces foliar chlorosis in soybeans
(Xiong and Fuhrmann, 1996). In addition to having plant growth
promoting traits, certain bacterial strains are also very important in
plants exposed to environmental stresses. Biosurfactant production by
Pseudomonas spp. is an effective environmental trait which has a great
potential for biotechnological and biomedical applications (Banat
et al., 2010). However, certain species having the ability to produce
biosurfactants are opportunistic pathogens (Pamp and Tolker-Nielsen,
2007). In certain cases, the application of PGPR and fungi triggers the
pathogenic activity of the co-inoculated partner although the PGPR itself is non-pathogenic (Dewey et al., 1999).
The above discussion shows that although PGPR are very effective
for promoting plant growth and development, certain bacterial species
may be growth inhibitory. However, such a negative role may occur
under certain specific conditions and also by some particular traits. So
the selection of a particular strain is critical for obtaining maximum
benefits in terms of improved plant growth and development.
4.3. Mechanisms employed by PGPR to mitigate stress-induced adverse
effects on plants
In a non-stress natural environment, most of the mechanisms used
by PGPR for growth enhancement are common, while under stress conditions some strains may not be able to perform efficiently due to their
inability to survive and compete in the harsh environment. However,
certain PGPR strains not only tolerate stress conditions, but also have
the ability to promote plant growth under such stressful environment.
This enhanced growth by PGPR takes place by a multitude of mechanisms such as lowering of stress-induced ethylene level, production of
exopolysaccharides, induced systemic resistance, etc. (Glick et al.,
433
2007; Saharan and Nehra, 2011; Sandhya et al., 2009; Saravanakumar
et al., 2007; Upadhyay et al., 2011).
Lowering of ethylene level is one of the major mechanisms elicited
by PGPR for promoting plant growth under stress conditions. Ethylene
is a phytohormone that enhances plant growth at its low concentration
(Glick et al., 2007; Mattoo and Suttle, 1991). The levels of ethylene are
usually elevated under stress conditions due to enhanced production
of 1-aminocyclopropane-1-carboxylic acid (ACC), an immediate precursor of ethylene biosynthetic pathway (Zapata et al., 2007). ACC is believed to cause an adverse effect on plant growth particularly on root
elongation that ultimately affects overall plant processes including
both nutritional and physiological functions (Alarcon et al., 2012;
Belimov et al., 2002; Visser and Ronald, 2007).
For maintaining normal growth of plants, it is necessary that ethylene concentration remains at a level that is favorable for normal growth.
It can be achieved by certain PGPR containing ACC-deaminase, which
can degrade ACC into ammonia and α-ketobutyrate (Glick et al.,
2007). This decrease in ACC level results in lowering of ethylene concentration in root vicinity, that is helpful for promoting root growth. According to the model described by Glick et al. (1998) PGPR bind to the
root surface due to the presence of root exudates (Whipps, 1990). The
level of ACC in plant roots increases due to the activity of indole acetic
acid (IAA) synthesized by PGPR, as well as endogenous plant IAA that
induces the activity of ACC synthase to convert S-adenosylmethionine
to ACC (Patten and Glick, 1996). The ACC is then taken up by the PGPR
upon its exudation by the plant roots. Due to their activity of ACCdeaminase enzyme, these rhizobacteria convert it into ammonia and
α-ketobutyrate, and therefore protect the plant from deleterious concentrations of ethylene. As the concentration of ACC outside the root decreases due to its degradation, more ACC is exuded by the plant roots
thereby bringing the ethylene concentration down in the plant roots.
This mechanism suppresses the inhibitory effect of ethylene on root
elongation (Pattan and Glick, 1996). This model efficiently explains improved plant growth under stress conditions by maintaining ethylene
concentration. The work of a number of scientists further proved the effectiveness of this phenomenon for promoting plant growth (Barnawal
et al., 2012; Chen et al., 2013; Cheng et al., 2007; Nadeem et al., 2006a;
Siddikee et al., 2012; Tank and Saraf, 2010).
Under stress conditions, plant growth is also affected by nutritional
imbalances. For example, in saline conditions, elevated level of sodium
(Na+) not only disturbs the uptake of other nutrients but also causes
specific ion toxicity (Ashraf, 1994). For salinity tolerance and maintenance of osmotic potential in a plant, a high K+/Na+ ratio is very essential (Hamdia et al., 2004). Certain PGPR strains also have the ability to
protect the plants from the harmful effects of high Na+ concentration
in the saline soil environment. They do this by their ability to produce
exopolysaccharides. The exopolysaccharides so produced reduce Na+
uptake in the plant by binding it and also by biofilm formation
(Geddie and Sutherland, 1993; Khodair et al., 2008; Qurashi and Sabri,
2012). The reduced availability of Na+ results in lowering the uptake
of Na+ thereby maintaining high K+/Na+ ratio that enables the plant
to survive better in salt stressed conditions (Ashraf et al., 2004; Han
and Lee, 2005; Khodair et al., 2008). The exopolysaccharides also play
an important role in plants exposed to water deficit conditions. As
drought conditions cause a negative influence on plants as well as on
microbial population, these exopolysaccharides also protect the bacteria
and plants from desiccation, and enable them to continue their growth
under water deficit conditions (Sandhya et al., 2009).
In soil environment, plant growth is also affected by soil-borne pathogens. The PGPR also protect plants from pathogens and enhance plant
resistance against diseases. This is achieved by a number of mechanisms
including antibiosis, competition and parasitism (Beneduzi et al., 2012;
Cassells and Rafferty-McArdle, 2012; Deshwal et al., 2003; Gula et al.,
2013; Heydari and Pessarakli, 2010; Khokhar et al., 2012; Perneel
et al., 2008; Ping and Boland, 2004). The PGPR protect the plant by
one or more of these biocontrol mechanisms. For example, PGPR inhibit
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the growth of pathogens through the antibiosis mechanism in which
antimicrobial compounds that inhibit pathogen growth are produced
by bacteria (Glick, 1995). Similarly, PGPR reduce the availability of
iron required for pathogens, which ultimately hampers their growth
(Subba Rao, 1993). Another important mechanism used by PGPR is induced systemic resistance (ISR). In this mechanism PGPR bring a change
in host-plant vulnerability and increase the resistance of plants against
diseases (Alizadeh et al., 2013; Khokhar et al., 2012; Saravanakumar
et al., 2007).
From the above discussion it is evident that PGPR promote plant
growth by employing certain mechanisms and protect the plant from
some deleterious conditions by monitoring the availability of some specific biomolecules/agents that directly or indirectly affect plant growth.
These agents can increase plant tolerance against stress conditions.
Furthermore, some of these mechanisms may be present in one
particular strain of bacteria while absent in others. For example, some
Pseudomonas species have the ability to lower stress-induced ethylene
concentration by ACC-deaminase enzyme and also decrease the availability of Na+ by producing exopolysaccharides.
5. Mycorrhizae
Mycorrhiza is a symbiotic association between plant roots and fungi.
The two common types of fungi involved in such association are
arbuscular mycorrhizae (AM) and ectomycorrhizae (ECM). AM are
probably the most abundant fungi that are commonly present in agricultural soils. They form symbiotic association with terrestrial as well
as aquatic plants (Christie et al., 2004; Khan and Belik, 1995; Liu and
Chen, 2007; Willis et al., 2013). About 80% of all terrestrial plants, including most agricultural, horticultural, and hardwood crop species
are able to establish this mutualistic association (Giovannetti et al.,
2006). These fungi penetrate into root cortical cells and form a particular haustoria-like structure called arbuscule that serves as a mediator for
the exchange of metabolites between fungus and host cytoplasm
(Oueslati, 2003). The AM fungal hyphae also proliferate into the soil
(Bethlenfalvay and Linderman, 1992) which helps plants to acquire
mineral nutrients and water from the soil and also contribute to improving soil structure (Javaid, 2009; Rillig and Mummey, 2006).
AM fungi play a very important role in ecosystems through nutrient
cycling (Barea and Jeffries, 1995; Shokri and Maadi, 2009; Wu et al.,
2011; Yaseen et al., 2012). Growth and productivity of several field
crops have been observed by root colonization of mycorrhizal fungi
(Cavagnaro et al., 2006; Nunes et al., 2010). Mycorrhizal roots can explore more soil volume due to their extramatrical hyphae that facilitate
them for absorption and translocation of more nutrients than by nonmycorrhizal plants (Guo et al., 2010; Joner and Jakobsen, 1995). Mycorrhizae can also increase the availability and supply of slowly diffusing
ions, such as phosphate to the plant (McArther and Knowles, 1993;
Sharda and Koide, 2010). It has been estimated that about 80% of the
phosphorus taken up by a mycorrhizal plant is supplied by the fungus
(Marschner and Dell, 1994). In addition to their significant role in P acquisition, AM fungi can also provide other macro- and micro-nutrients
such as N, K, Mg, Cu and Zn, particularly in soils where they are present
in less soluble forms (Clark and Zeto, 1996; Marschner and Dell, 1994;
Meding and Zasoski, 2008; Smith and Read, 2008). In Mediterranean
soils with high phosphate fixing capacity, N fixation by rhizobia is
weak due to limited supply of phosphorus and other minor nutrients.
The AM fungi are commonly associated with legumes in these soils
and, therefore, can increase plant nutrient uptake (Antunes et al.,
2006; Javaid, 2010). For example, improved legume nutrition has been
observed with AM fungi and Rhizobium (Guo et al., 2010; Requena
et al., 2001; Tavasolee et al., 2011). Mycorrhizae also play an important
role in improving soil physical properties. The external mycorrhizal mycelium along with other soil organisms forms stable aggregates thereby
improving soil aggregation (Bethlenfalvay and Schuepp, 1994; Borie
et al., 2008; Rillig et al., 2010; Singh, 2012; Wilson et al., 2009; Wu
et al., 2008). This improvement in soil aggregation might be due to production of an insoluble glycoprotein glomalin (Gadkar and Rillig, 2006)
that plays an important role in soil stability (Rilling et al., 2003). Gohre
and Paszkowski (2006) also found a correlation between the amount of
glomalin in the soil and the amount of heavy metals bound.
In general, mycorrhizae promote plant growth not only by providing
nutrients necessary for plant growth, but also help the plant to tolerate
stress environment. Different mechanisms may justify this growth
promotion.
5.1. Mechanisms used by mycorrhizae to mitigate stress-induced adverse
effects on plant growth
The growth promotion due to mycorrhizal association can be explained by several mechanisms used by fungi under certain conditions.
These include production of metabolites like amino acids, vitamins,
phytohormones, and/or solubilization and mineralization processes
(Azcon-Aguilar et al., 2002; Bharadwaj et al., 2008; Khan et al., 2009;
Meddad-Hamza et al., 2010; Smith and Read, 1997; Turnau and
Haselwandter, 2002).
In addition to providing nutritional and structural benefits to plants,
they also impart other benefits to them including production/accumulation of secondary metabolites, osmotic adjustment under osmotic
stress, improved nitrogen fixation, enhanced photosynthesis rate, and
increased resistance against biotic and abiotic stresses (Khaosaad
et al., 2007; Ruiz-Lozano, 2003; Schliemann et al., 2008; Selvakumar
and Thamizhiniyan, 2011; Sheng et al., 2009; Shinde et al., 2013; Takeda
et al., 2007; Wu and Xia, 2006). Many researchers have reported that
AM fungi can improve plant tolerance to heavy metals, drought, and salinity, and also protect plants from pathogens (Azcon-Aguilar et al.,
2002; Bartolome-Esteban and Schenck, 1994; Gamalero et al., 2009;
Gosling, et al., 2006; Hildebrandt et al., 1999; Marulanda et al., 2006,
2009; Vivas et al., 2003; Zhang et al., 2010). They can also improve
crop growth and yield by alleviating the negative influence of
allelochemicals (Bajwa et al., 2003; Javaid, 2008).
These ameliorative effects can be explained by a number of mechanisms that may vary depending on AM–plant association as well as
stress conditions. For example, a number of studies have shown that improved P nutrition under salinity and water deficit environment is a primary mechanism for promoting stress tolerance in plants (Cantrell and
Linderman, 2001; Colla et al., 2008; Feng et al., 2002; Ruiz-Lozano et al.,
1996; Subramanian et al., 1997). There are many reports which show
that AM fungi can increase soil enzyme activities, such as phosphatase
(Kothari et al., 1990; Mar Vazquez et al., 2000).
Some studies have also demonstrated that AM association not only
influences P nutrition but also affects the physiological processes of
plants by increasing proline contents (Ruiz-Lozano et al., 1995). Proline
is known to act as an osmoregulator under stress conditions (Ashraf and
Foolad, 2007; Irigoyen et al., 1992). Similarly, the mechanisms used by
AM to alleviate stress-induced adverse effects of salinity on plant
growth include: improvement of plant nutrition, variation in Na+ and
K+ uptake, modification in physiological and enzymatic activities and
alteration of the root architecture to facilitate water uptake (Evelin
et al., 2009; Gamalero et al., 2010; Zhang et al., 2011; Zolfaghari et al.,
2013).
Physiological processes involved in osmoregulation like enhanced
carbon dioxide exchange rate, water use efficiency, and stomatal conductance are also influenced by the activities of AM fungi (Birhane
et al., 2012; Ruiz-Lozano and Aroca, 2010). Mycorrhizae also increase
the nitrogen availability of host plant under drought conditions
(Subramanian and Charest, 1999). It has been shown that mycorrhizal
plants absorb water more efficiently under water deficit environment
(Khalvati et al., 2005) that might be due to modification in root architecture which results in better root growth due to numerous branched
roots (Berta et al., 2005). As abscisic acid regulates the stomatal conductance by closing stomata under water limited environment, the positive
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
effect of AM fungi on plant growth and development under drought
stress might be due to its influence on abscisic acid concentration in
plants (Jahromi et al., 2008). They reported more abscisic acid content
in mycorrhizal lettuce plants compared to non-mycorrhizal ones. It
has also been observed that AM fungi increase salinity tolerance of
host plants by improving water status of the inoculated plants by facilitating water transport in plants (Ouziad et al., 2006).
Mycorrhizae also enhance soluble sugars and electrolyte concentrations in host plants. For example, improved osmoregulation capacity in
AM inoculated maize was related to higher soluble sugar and electrolyte
concentrations (Feng et al., 2002). Porcel and Ruiz-Lozano (2004) and
Al-Garni (2006) also reported increased sugar concentrations in mycorrhizal plants of soybean and Phragmites australis. This increase in sugar
concentration could be explained by a previously reported hypothesis
of Nemec (1981) who demonstrated that high sugar level in mycorrhizal plants may be due to hydrolysis of starch to sugars.
It is also well documented that AM fungi affect the expression of a
number of antioxidant enzymes (Gamalero et al., 2009), which protect
the plants from reactive oxygen species produced under stress conditions. Similarly, improved nodulation due to increased activities of
these enzymes under salinity stress has been observed along with
other factors such as leghemoglobin content, nitrogenase activity and
polyamine contents (Gamalero et al., 2009; Garg and Manchanda,
2008; Matamoros et al., 2010; Sannazzaro et al., 2007; Yaseen et al.,
2012).
Another mechanism used by AM fungi to facilitate plant growth
under salinity stress is the regulation of plant nutrition. High Na+ concentration under salinity stress is detrimental for normal plant growth
and low K+/Na+ ratio has been observed generally in salt sensitive
plants (Ashraf et al., 2004). Therefore, improved K+/Na+ ratio is believed to be a potential indicator of salinity tolerance in most plants.
The AM fungi also play an important role in maintaining a high K+/
Na+ ratio in host plants exposed to saline conditions (Giri et al., 2007;
Sannazzaro et al., 2006; Selvakumar and Thamizhiniyan, 2011; Zhang
et al., 2011).
In general, mycorrhizae enhance plant growth under stressful environments by a number of mechanisms such as regulation of plant nutrition, production of hormones and antioxidant enzymes, and regulation
of a multitude of physiological processes. However, it is also evident
from the above discussion that the effectiveness of these mechanisms
also depends on the extent of AM and host plant association as well as
a number of soil and plant factors.
6. Inducing stress tolerance through microbial inoculation
A number of studies conducted by different workers have shown the
effectiveness of microbial inoculation for enhancing plant growth under
normal as well stress conditions, which has been reviewed and
discussed in the following sections.
6.1. Stress tolerance through PGPR
It is now well established that PGPR strains are equally effective for
improving growth of cereals, legumes and vegetables grown under
stress conditions (Han and Lee, 2005; Mayak et al., 2004a,b; Nadeem
et al., 2010b; Zahir et al., 2009). Several researchers have demonstrated
the positive effect of rhizobacteria in terms of alleviating the negative
impact of salinity on crop growth under laboratory as well as field conditions (Jalili et al., 2009; Nadeem et al., 2007, 2010a; Saravanakumar
and Samiyapan, 2007). Some selected examples of growth promotion
with inoculation of these rhizobacteria under stressful environments
are included in Table 1.
Among various biotic and abiotic stresses, salinity is one of the major
limiting factors for crop production in arid and semiarid regions of the
world. One of the common hypotheses employed in most of the studies
conducted under salinity stress was the lowering of ethylene level by
435
the ACC-deaminase activities of PGPR. These studies conducted under
both controlled and natural environments in greenhouse showed that
inoculation with PGPR containing ACC-deaminase significantly increased plant growth and yield compared to that of un-inoculated
control.
In addition to regulating plant nutrition by enhancing K+ uptake
over Na+ in plants under salt stress conditions (Nadeem et al., 2007) inoculation with PGPR also enhances the uptake of other major nutrients
as well as improves the water content of stressed plants (Mayak et al.,
2004a; Nadeem et al., 2006b). Yue et al. (2007) have also shown that inoculation with Klebsiella oxytoca (Rs-5) containing ACC-deaminase enhanced the absorption of major nutrients such as N, P, K and Ca, and
promoted plant growth by mitigating the negative effects of salt stress.
The inoculation with Pseudomonas spp. improved the eggplant growth
by depressing the uptake of Na+ and increasing the activities of antioxidant enzymes under salinity stress conditions (Fu et al., 2010). According to them, regulation of mineral uptake and increase in the
antioxidant enzyme activities may be the two key mechanisms involved
in alleviation of salt stress.
The PGPR strains are effective not only for improving plant growth
under salinity stress but are also helpful for enhancing plant growth
and development under heavy metals, flooding and drought stress
(Glick et al., 2007). The ajmalicine (antihypertension alkaloid) content
of drought stressed Catharranthus roseus plants increased with the inoculation of Pseudomonas fluorescens (Jaleel et al., 2007). Similarly, PGPR
containing ACC-deaminase alleviated the adverse effects of drought
stress on the growth of pea plants (Zahir et al., 2008). Sandhya et al.
(2009) demonstrated that rhizobacteria having the ability to produce
exopolysaccharides can be used effectively for enhancing drought resistance in sunflower plants. Similarly, lowering of ethylene concentration
under heavy metal stress is also one of the mechanisms used by PGPR
for promoting plant growth in contaminated soil (Belimov et al., 2005;
Dell' Amico et al., 2008). The growth promotion under heavy metal
stress may also be due to the reason that certain PGPR strains can accumulate metals in their cells and reduce their availability to the plant.
Another important aspect of PGPR is to increase resistance against
pathogens and provide protection to plants from diseases. Plant growth
promoting rhizobacteria have been shown as effective biocontrol agents
against a number of plant pathogens (Kotan et al., 2009; Ramos-Solano
et al., 2008b). This increase in disease tolerance may be due to several
mechanisms such as improved nutrient availability, production of cell
wall lytic enzymes, competition for nutrients, and prevention of growth
of pathogens or induction of systemic resistance (Bhattacharyya and
Jha, 2012; Nihorimbere et al., 2011; O'Sullivan and O'Gara, 1992;
Ramos-Solano et al., 2008a; Singh et al., 1999; Soltani et al., 2012). The
biocontrol ability of these PGPR strains against diseases had also been
demonstrated previously by Domenech et al. (2006) in tomato and pepper. In addition, PGPR strains are also helpful to alleviate the negative influence of temperature stress, parasitic weeds and increase the shelf life
of flowers (Ait Barka et al., 2006; Babalola et al., 2003; Bensalim et al.,
1998; Grichko and Glick, 2001; Nayani et al., 1998).
Although PGPR can enhance plant growth under normal as well as
stress conditions however, they have differential potential for improving plant growth and development. For example, Zahir et al. (2009)
found that Pseudomonas putida had better ability to mitigate the adverse
effect of salinity than that of Serratia proteamaculans. Similarly,
Pseudomonas fluorescens and Pseudomonas stutzeri performed better in
enhancing growth of canola and tomato plants, respectively (Jalili
et al., 2009; Tank and Saraf, 2010). These variable effects of PGPR strains
might be due to difference in their specific characteristics such as ACCdeaminase activity, indole acetic acid production, root colonization ability, phosphorus solubilization ability, etc. (Gamalero et al., 2009;
Saravanakumar and Samiyapan, 2007; Zahir et al., 2009).
PGPR strains have been reported to be equally effective when
applied with other microbial populations. For example, Figueiredo
et al. (2008) evaluated the effect of co-inoculation with Paenibacillus
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S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
Table 1
Effectiveness of PGPR for promoting plant growth under stress conditions.
Crop
Type of
stress
Tomato (Solanum
lycopersicum)
Salinity
Cotton (Gossypium hirsutum)
Groundnut (Arachis
hypogaea)
Maize (Zea mays)
Wheat (Triticum aestivum)
Canola (Brassica napus L.)
Tomato (Solanum
lycopersicum) and pepper
(Capsicum annuum)
Indian mustard (Brassica
juncea)
Pea (Pisum sativum)
Bacterial strain
Response
Reference
Achromobacter piechaudii ARV8 Inoculation increased fresh and dry weight as well as water use efficiency of tomato
by decreasing the ethylene production under stress.
Pseudomonas fluorescens,
All PGPR strains enhanced the root and shoot growth of tomato. Sodium contents
P. aeruginosa, P. stutzeri
(Na) were low in plants inoculated with P. Stutzeri and showed relatively better
grwoth compared to other two strains.
Klebsiella oxytoca
In addition to significant increase in height and dry weight of cotton plants,
inoculation with PGPR uptake of major nutrients like N, P, K, and Ca increased while
Na deceased.
P. fluorescens TDK1,
Bacterial strains proved useful for increasing salt tolerance of groundnut. The impact
P. fluorescens PF2 and
of strains was variable and P. fluorescens TDK1 proved most effective than other ones.
P. fluorescens RMD1
Pseudomonas spp., Enterobacter PGPR enhanced the growth of maize under salinity but with variable efficacy. Overall,
aerogenes, Flavobactrium
high chlorophyll content, relative water content and K+/Na+ ratio was observed in
inoculated plant than uninoculated control.
ferrugineum
Pseudomonas putida,
Pseudomonas putidawas was more effective and a signifiacnt increase in plant height,
P. aeruginosa, S. Proteamaculans root length and chlorophyll content was observed compared to control.
Pseudomonas spp., Enterobacter Inoculation not only reduced the negative impact of salinity stress on wheat but also
cloacae, S. ficaria.
dilute the impact of ethylene on etiolated pea seedlings.
Bacillus spp. Enterobacter spp.
Inoculating wheat seedlings produced more biomass compared to control.
Paenibacillus spp.
Exopolysaccharides producing PGPR protect the plant from Na toxicity by decreasing
its uptake.
Pseudomonas spp.
Rate of seed germination and seedling growth was significantly higher. ACCdeaminase producing Pseudomonas spp. enhanced canola tolerance against salinity
stress.
Drought P. putida GR12-2,
Inoculating plants were able to maintain their growth under water limited
Achromobacter piechaudii ARV8 conditions. The PGPR dilute the negative impact of stress induced ethylene on root
growth by the activity of their ACC-deaminase enzyme.
Heavy
Rhodococcus spp.,
Cadmium (Cd) tolerant PGPR strain protected the plant metal from toxicity. A sigmetals
Variovorax paradoxus spp.
nificant improvement in plant growth was observed at toxic Cd concentration.
P. brassicacearum AM3,
Inoculating plants produced longer roots, greater root density and improved nutrient
P. marginalis Dp1
uptake. Bacteria counteracted the Cd-induced inhibition of nutrient uptake by plants.
polymyxa and Rhizobium tropici on growth, nitrogen content and nodulation of common bean (Phaseolus vulgaris L.) under water deficit environment in a greenhouse. The study was conducted with two strains of
P. polymyxa singly or in mixture at three levels of drought. The results
showed that co-inoculation enhanced the plant growth, nitrogen content and nodulation of bean under drought stress compared to uninoculated control.
To commercialize the PGPR inocula, the effectiveness of PGPR has
also been evaluated in the field. In a field trial, under water stress conditions, PGPR inoculation enhanced the proline, chlorophyll and water
content of basil (Ociumum basilicum L.) under stress conditions
(Heidari et al., 2011). The PGPR were not only effective under water
stress conditions but also proved helpful for enhancing plant growth
under salinity stress. The growth and yield of groundnut was significantly higher under salt stress conditions when inoculated with PGPR
strains. However, the strains were variable regarding their potential
(Saravanakumar and Samiyapan, 2007). Similar results were also observed when maize seed was inoculated with rhizobacteria containing
ACC-deaminase (Nadeem et al., 2009). The mechanisms used by PGPR
under field condition are almost similar as discussed earlier.
The above discussion clearly indicates that PGPR strains are very
helpful to enhance plant growth under stressful environments, such as
drought, flooding, salinity, heavy metals, pathogen attack, etc. This
growth promotion may take place by lowering the ethylene concentration due to their enhanced ACC-deaminase activity or by production of
exopolysaccharides or through induced systemic resistance. Although a
few studies have been conducted in the field however, results are inconsistent with those of laboratory or greenhouse studies.
6.2. Stress tolerance through mycorrhizae
There are a number of reports available in the literature, which indicate the potential of mycorrhizal fungi for improving growth and development of plants under stressful environments (Adewole et al., 2010;
Mayak et al.
(2004a)
Tank and Saraf
(2010)
Yue et al. (2007)
Saravanakumar
and Samiyappan
(2007)
Nadeem et al.
(2007)
Zahir et al. (2009)
Nadeem et al.
(2010a)
Upadhyay et al.
(2011)
Jalili et al. (2009)
Mayak et al.
(2004b)
Belimov et al.
(2005)
Safronova et al.
(2006)
Bhosale and Shinde, 2011; Sannazzaro et al., 2006; Selvakumar and
Thamizhiniyan, 2011; Shinde et al., 2013). Some of the selected examples have been mentioned in Table 2. Although increased nutrition status of a plant through mycorrhizal association enables it to tolerate
stress environment (Azcon-Aguilar and Barea, 1996), the association
of AM with the plant also improves plant health by providing specific
protection against biotic and abiotic stresses (Barea and Jeffries, 1995).
As discussed earlier, drought is one of the major factors limiting plant
growth and development, particularly in arid and semiarid regions
(Ashraf and Mehmood, 1990). Drought-induced hormonal imbalance
such as increase in ethylene concentration causing inhibition of root
growth (Mayak et al., 2004a), and reduced nutrient and water uptake
under drought stress are also major factors which cause negative influence on plant growth and development (Agnew and Warren, 1996;
Ashraf et al., 2013). The AM fungi can affect the water relations of
many plants (Auge, 2001) and have great potential to increase plant resistance to maintain its growth under adverse conditions (Allen and
Allen, 1980). The mechanisms used by AM fungi to enhance the water
relations of host plants are not amply clear, however, this may occur
by increasing water absorption by external hyphae, regulation of stomatal apparatus, increase in activity of antioxidant enzymes and absorption of nutrients particularly phosphorus (Birhane et al., 2012; RuizLozano, 2003; Wu et al., 2008; Habibzadeh et al., 2012; Younesi et al.,
2013).
Under drought stress, due to the generation of reactive oxygen species, an efficient antioxidant system is needed in the plant. It has been
observed that AM fungi increase the activity of antioxidant enzymes of
host plants (Ruiz-Lozano, 2003; Wu et al., 2008). A study conducted
on wheat under water stress environment showed that mycorrhizal inoculation enhanced the activities of antioxidant enzymes such as peroxidase and catalase compared to those in un-inoculated control plants
(Khalafallah and Abo-Ghalia, 2008). Mycorrhizal inoculation significantly increased the contents of proline, free amino acids, total soluble
and crude proteins, total carbohydrates, and total soluble and insoluble
Table 2
Effectiveness of mycorrhizae for promoting plant growth under stress conditions.
Type of
stress
Mycorrizal species
Maize (Zea mays)
Diesel stress
Compaction
Glomus constrictum
Trappe
Glomus spp.
Semi-arid
wasteland
Heavy metal
Glomus fasciculatum and
G. macrocarpum
Glomus spp.
Legume (Cassia
siamea)
Maize (Zea mays)
Sunflower
(Helianthus
annuus)
Soybean (Glycine
max)
Tomato (Solanum
lycopersicum)
Wheat (Triticum
aestivum)
Maize (Zea mays)
Sorghum (Sorghum
bicolor)
Mung bean (Vigna
radiata)
Tomato (Solanum
lycopersicum)
Glomus mosseae and
Acaulospora laevis
Glomus mosseae, Glomus
intraradices
Water stress
G. intraradices
Glomus intraradices
Glomus spp.
Glomus intraradices
Glumos intraradices
Salinity
stress
Glomus mosseae,
G. intraradices
Glomus mosseae
Glomus mosseae
Maize (Zea mays)
Glomus mosseae
Wheat (Triticum
aestivum)
Soybean (Glycine
max)
Glomus spp.
Glomus etunicatum
Reference
The heights and basal diameters of the inoculated seedlings significantly increased and malondialdehyde and free proline content decreased. High activities
of superoxide dismutase and catalase at low diesel stress while peroxidase showed high activities at high diesel stress.
Nutrient uptake decreased in compacted soil while inoculation significantly enhanced uptake of nutrient and alleviate the impact of compaction on corn
growth.
Mycorrhizae decreased the alkalinity of rhizosphere and high concentration of P, K, Cu and Zn was observed in inoculated plants. Growth was better in
inoculated plants and G. macrocarpum was more effective than G. fasciculatum
Plant height, basal diameter, seedling biomass and superoxide dismutase activity was more in mycorrhizal plants. Significant high lead concentration was
observed in mycorrhizal plants roots.
Mycorrhizal root colonization rate and sporulation ability enhanced in the presence of heavy metals. More shoot length, root biomass and shoot recorded in
inoculated plants. A. laevis was more effective than G. mosseae
AM fungus increased enhanced the infection of sunflower root and also increased the pollution tolerance and yield of sunflower in a degraded soil.
Tang et al. (2009)
Miransari et al.
(2009)
Giri et al. (2005)
Zhang et al. (2010)
Abdelmoneim and
Almaghrabi (2013)
Adewole et al.
(2010)
Porcel and RuizLozano (2004)
Subramanian et al.
(2006)
Khalafallah and
Abo-Ghalia (2008)
Celebi et al. (2010)
Alizadeh et al.
(2011)
Habibzadeh et al.
(2012)
Plant salt tolerance increased in mycorrhizal plants mainly due to elevated levels of superoxide-dismutase, catalase, ascorbate peroxidase and peroxidase He et al. (2007)
which degraded reactive oxygen species and alleviated membrane damage.
Mycorrizae minimize the negative impact of low temperature on plant growth and enhanced growth, photosynthesis and antioxidant activities.
Abdul Latef and
Chaoxing (2010)
Larger root diameter and root volume of mycorrhizal plants showed a significant shift towards a thicker root system. Improved root activity and the coarse Sheng et al. (2009)
root system enable the mycorrizal maize to withstand under salinity stress.
Glomus spp. showed variable efficacy for improving wheat growth. Glomus etunicatum performed more efficiently that indicates the importance of right
Daei et al. (2009)
selection of AM fungus.
Mycorrhizal inoculated plants grow better in saline conditions than uninoculated plants. Fresh and dry weight, root colonization and proline contents were Sharifi et al. (2007)
more in salt pre-treated fungus that than non salt pretreated fungus.
Mycorrhizae protected the plant from drought. Higher leaf water potentail was recorded in inoculated plants and kept the plant protected against oxidative
stress.
High concentration of N and P was observed in mycorrhizal plants. Significant increase in dry matter and number of flowers and fruits were observed. Effect
was more pronounced as the drought intensity increased.
Mycorrhizae significantly increased the content of proline, free amino acids, total soluble and crude protein and also enhanced activities of antioxidant
enzymes
Inoculation increased the silage yield. Significant increase in green and dry matter yield as well as leaf and stem ratio was observed.
Drought caused negative impact on sorghum length, shoot dry mater, 1000 kernel weight and yield. Mycorrhizae inoculation dilute the negative impact of
stress and enhanced yield. Grain yield increased 17.5% due to inoculation compared to drought.
Seed yield, leaf P, leaf N, proteins and water use efficiency improved in mycorrhizal plants.
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
Crop
437
438
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
sugars in wheat plants. They suggested that mycorrhizal association
could improve the osmotic adjustment, enhance its defense system,
and alleviate oxidative damage caused by drought stress. The improved
plant growth under drought stress was also observed in coriander
(Coriandrum sativum L.) by inoculation of AM and application of phosphorus (Farahani et al., 2008), which was found to be associated with
enhanced water use efficiency in field grown drought-stressed coriander plants.
As it was mentioned earlier that the effectiveness of AM fungi depends upon a number of soil as well as plant factors, Porcel and RuizLozano (2004) studied the effect of AM fungi both on root and shoot
parts of plants under drought stress conditions. The aim was to reveal
the preferred target tissues for effects of AM fungi against drought
stress. Their work showed that the plants associating AM fungi showed
more drought tolerance in terms of higher shoot biomass production
and leaf water potential than that by non-AM plants. High proline contents in the root and low in the shoot were observed in droughtstressed AM plants, whereas low activity of lipid peroxidase was observed in the shoots of drought-stressed AM plants. They demonstrated
that AM symbiosis enhanced osmotic adjustment in roots that helped to
maintain favorable water potential gradient for water movement from
soil to roots. It results in high water potential under drought stress
and, therefore, protects plants from the drastic effects of drought.
Although some workers have reported inhibition of AM growth under
salt stress conditions (Asghari, 2008; Juniper and Abbott, 2006; McMillen
et al., 1998), a number of other researchers have demonstrated the tolerance of AM in the presence of salt (Cantrell and Linderman, 2001; Evelin
et al., 2009; Gonsalves et al., 2012; Langenfeld-Heyser et al., 2007; Nayak
et al., 2012; Sharifi et al., 2007; Tang et al., 2009). This alleviating effect
may take place due to single or mixed AM culture. For example,
Langenfeld-Heyser et al. (2007) found a positive symbiosis between the
fungus Paxillus involutus and poplar hybrid Populus canescens, which
was found to be associated with increased plant biomass and reduced
Na+ uptake. Giri et al. (2003) found that mixed inoculation of six
arbuscular mycorrhizal fungal species enhanced the root colonization,
chlorophyll content, biomass production, and K and P contents in Acacia
auriculiformis under salinity stress. Since salinity and drought are often
linked together in dry soils, Cho et al. (2006) studied the response of mycorrhizae to sorghum under combined drought and salinity stresses. In
two greenhouse experiments, several water relation characteristics
were measured in sorghum plants colonized by Glomus intraradices and
Gigaspora margarita during drought and salinity stress. They observed
that upregulation of stomatal conductance by G. margarita which occurred with exposure to NaCl/drought stress, but not due to drought
alone. They concluded that AM fungi could alter host response to drought.
AM fungi also play an important role in heavy metal tolerance (Gaur
and Adholeya, 2004; Glassman and Casper, 2012; Vahedi, 2013), therefore, they can be used for achieving enhanced plant growth on metal
contaminated soils. It has been observed that heavy metals can cause
positive, negative and/or neutral effects on mycorrhizae (Chen et al.,
2005). For example, it has been observed that AM inoculation enhanced
the growth of a number of plant species grown in metal contaminated
soils. The work of Chen et al. (2007) showed enhanced growth of
M. sativa through AM inoculation in heavy metal contaminated soils.
Similarly, Liang et al. (2009) and Zhang et al. (2010) demonstrated better performance of Glomus mosseae for enhancing growth of maize and
rice in heavy metal contaminated soils.
The AM fungus promotes plant growth in contaminated conditions
in two ways i.e. by reducing the uptake of toxic metals and by enhancing
the metal uptake. For example, AM fungi reduced the uptake of cesium
(Cs) in contaminated soil (Berreck and Haselwandter, 2001). The toxic
effects of heavy metals on plant growth reduced due to their binding
with fungi. The fungi produce an insoluble glycoprotein glomalin that
has the ability to bind heavy metals (Bedini et al., 2009; Gohre and
Paszkowski, 2006). Fungal cell wall due to presence of chitin also
has good capacity to bind metals (Zhou, 1999). On the other hand
mycorrhizae also enhance the metal uptake and reduce their concentration in contaminated soils. Khan et al. (2000) demonstrated that polluted soils can be rehabilitated by the presence of mycorrhizal plants that
enhance the uptake of metals by increasing their bioavailability through
their effect on rhizosphere.
The work of Zhang et al. (2010) conducted in greenhouse to study the
effect of AM on Pb uptake, demonstrated that location and stress attenuation in maize showed better performance of mycorrhizal plants. The performance of mycorrhizal and non-mycorrhizal plants was compared at
varying Pb levels. It was observed that higher plant height, basal diameter
and biomass of seedlings were found in the seedlings inoculated with AM.
Moreover, higher activity of antioxidant enzyme superoxide dismutase
was observed in AM inoculated plants compared to that in nonmycorrhizal ones. They observed that Pb was higher in the roots of
mycorrhizal plants where it was mainly deposited in the hyphal wall,
the hyphal inner chambers, the hyphal inner-chamber membranes and
the vacuolar inner-chamber membrane. The previous work of other researchers also indicated better performance of AM under Pb contaminated soil environment which was believed to be due to alterations in
antioxidant enzymes, lipid peroxidation and soluble amino acid profile
(Andrade et al., 2009; Karagiannidis and Nikolaou, 2000). Similarly,
there are reports that indicate the role of AM fungi for enhancing plant
growth under heavy metal stress (Abdelmoneim and Almaghrabi, 2013;
Asif and Bhabatosh, 2013; Glassman and Casper, 2012; Miransari, 2010;
Vahedi, 2013; Vivas et al., 2003).
By obtaining positive results from laboratory/greenhouse experiments, the scientists used this microbial population under natural conditions so that maximum benefits can be obtained. In an earlier work,
Kothari et al. (1990) observed enhanced drought tolerance in fieldgrown maize plants as a result of improved P status by inoculation
with Glomus fasciculatum. A significant increase in plant biomass and
grain yield of wheat inoculated with G. mosseae or Glomus etunicatum
was observed under water stress (Al-Karaki et al., 2004). The plants inoculated with G. etunicatum showed high colonization than plant inoculated with G. mosseae. This shows the variable potential of mycorrhizae
for improving plant growth. The effectiveness of AMF under field conditions has also been demonstrated in sorghum (Mehraban et al., 2009).
The authors found that mycorrhizal colonization improved growth,
water status, nutrient contents and yield of sorghum plants under
drought stress. Celebi et al. (2010) appraised the effectiveness of mycorrhizae in a field at five different irrigation regimes on silage maize (Zea
mays L.). The mycorrhizal inoculation increased the silage yield of maize
at all irrigation regimes when compared with non-mycorrhizal plants.
AM inoculation resulted in a significant increase in green and dry matter
yield even in low irrigation regimes, indicating the effectiveness of AMF
under water stress environment. They demonstrated that the positive
response of AM inoculation could be due to several mechanisms including water uptake by fungal hyphae, increased turgor by lowering leaf
osmotic potential, and improved nutrition. Mycorrhizal colonization is
not only effective for enhancing plant growth but also proves helpful
for improving efficiency of other microbial population. It is evident
from the work of Giri et al. (2004) that AM fungi promoted the rhizobial
symbiosis efficiency of Sesbania aegyptiaca and Sesbania grandiflora in
saline soil. The AM inoculated plants showed high shoot and root dry
biomass as well as increased chlorophyll, N, P and Mg contents.
The above-discussion clearly indicates the effectiveness of mycorrhizae for improving plant growth under stressful environments. The
mycorrhizae are equally effective under controlled as well as natural
field condition. It is also evident that different traits of AM fungi have
variable potential for enhancing growth under a particular stress environment. That could be one of the reasons for inconsistent performance
of this microbial population.
6.2.1. Mycorrhizae and nitrogen fixation
A number of studies have demonstrated that inoculation with AM
fungi improves growth of plants under various environmental stresses
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
(Abdelmoneim and Almaghrabi, 2013; Alizadeh et al., 2011; Porcel and
Ruiz-Lozano, 2004; Tang et al., 2009; Zhang et al., 2010). In addition to
non-leguminous plants, the AM fungus has great potential to improve
nodulation, and hence nitrogen fixation in legumes. Increased phosphorus and other nutrients as well as synergistic interactions with other
rhizospheric microorganisms could be very effective for enhancing nitrogen fixation under stressful environments for achieving maximum
grain yield of legumes. Some studies conducted under laboratory and
field conditions have shown that dual inoculation AM fungus with nitrogen fixer bacteria was very effective for enhancing nitrogen fixation
in legumes (Bagyraj et al., 1979; Lesueur and Sarr, 2008; Rabie et al.,
2005). As AM fungi exist naturally in stressful environments like salinity
(Evelin et al., 2009) so their association with plants could be very effective for improving growth and vigor of plants under stress conditions
(Farahani et al., 2008; Kumar et al., 2010). Most of the legumes are
known to be salt sensitive (Munns, 2002), however, nitrogen fixation
of such crops can be improved under stress conditions by inoculation
with particular microorganisms. For example, Garg and Chandel
(2011a) observed that symbiotic association of pigeon pea (Cajanus
cajan) with G. mosseae led to a significant improvement in plant dry
mass and nitrogen-fixing potential of nodules under salt stress. Similar
results were also obtained in case of chickpea (Cicer arietinum L.)
where AM plants exhibited better growth and nitrogen fixation under
stress as well as normal conditions compared to un-inoculated ones
(Garg and Chandel, 2011b).
As mycorrhizal effects on plant water relations are well documented
(also discussed in one of the earlier sections), so inoculation with mycorrhizae is also effective for improving growth of legume crops under
water stress conditions. AM symbiosis enhances osmotic adjustment
in roots, which could contribute to maintaining a water potential gradient favorable to water absorption by the roots from soil (Porcel and
Ruiz-Lozano, 2004).
Many legumes form symbiotic association with AM fungi. Root colonization by AM-fungi favors nodulation by rhizobia (Smith et al., 1979).
The combination of Rhizobium and AM fungi could be very effective for
enhancing nitrogen fixation under stress conditions (Chalk et al., 2006;
Franzini et al., 2009). For example, AM-fungi protected mungbean
(V. radiata) plants from the deleterious effects of salts (Rabie and
Almadini, 2005). Shokri and Maadi (2009) demonstrated an increase
in total dry weight, root length and phosphorus uptake in Trifolium
alexandrinum under salinity stress.
The application of AM fungus with PGPR is also found to enhance nitrogen fixation ability of plants. For example, application of P. putida
strain R-20 enhanced growth and nodulation of subclover when applied
with AM fungus (Meyer and Linderman, 1986). However, Bisht et al.
(2009) observed that although AM fungus showed a positive response
with Rhizobium leguminosarum, a similar response was observed in
case of P. fluorescens. This study suggested that enhanced plant growth
with AM and PGPR depended on type of bacteria.
Overall, it can be concluded that although stressful conditions are a
limiting factor for nitrogen fixation, this stress-induced effect can be diluted by incorporating AM fungus into the soil. AM fungus alone or in
association with other microbial populations could be very effective
under stressful environments. However, selection of a suitable partner
is a critical step that will determine the success of this approach.
7. Synergistic role of PGPR and mycorrhizal fungi in stress tolerance
Rhizosphere is a dynamic environment that differs from bulk soil
both in physical and chemical properties. Some of the important interactions include plant–plant interactions, root–microorganism interactions and microbe–microbe interactions (Adesemoye and Kloepper,
2009; Bais et al., 2008; Lau and Lennon, 2011). The synergistic and antagonistic response of these interactions depends upon the nature of
microbial strains involved in these interactions as well as plant species.
The management of such interactions is a promising approach and a key
439
factor for sustainable agriculture. The interactions may take place between plant and fungus/bacteria in which both partners get benefits
as mutualistic association (Beattie, 2007; Finlay, 2007) and ultimately
plant growth enhances due to growth promotion mechanisms used by
microbes such as production of phytohormones, suppressing of pathogens, nitrogen fixation and solubilization of minerals (Ahmad et al.,
2008; Bootkotr and Mongkolthanaruk, 2012; Franche et al., 2009;
Hayat et al., 2010; Saharan and Nehra, 2011).
In mycorrhizal association, the plant–fungus interactions occur in
the soil zone surrounding the roots and fungal hyphae, termed as
mycorrhizosphere (Johansson et al., 2004). In this zone, fungus also interacts with other microorganisms like bacteria and synergistic interaction between them not only promotes plant growth but also enhances
the population of each other (Artursson et al., 2006; Yusran et al.,
2009). Bacteria can produce compounds to increase cell permeability
so as to enhance the rate of root exudation that stimulates the hyphal
growth and facilitates root penetration by the fungus (Jeffries et al.,
2003). On one hand, mycorrhizae help the plant to resist against biotic
and abiotic stresses by increasing surface area of roots for nutrient acquisition or through more specific mechanisms (Artursson et al., 2006;
Asif and Bhabatosh, 2013; Miransari, 2010; Sikes, 2010). Furthermore,
PGPR improve the development of the mycosymbionts and facilitate
the colonization of plant roots by AMF (Hildebrandt et al., 2002;
Jaderlund et al., 2008). The presence of PGPR supports the establishment of mycorrhizae and improves their ability to perform various functions adequately. For example, inoculation with bacterial strain
Paenibacillus brasilensis has been shown to increase the extent of root
colonization by the AM fungus G. mosseae on clover (Artursson, 2005).
Long ago, Linderman (1992) reported that AM fungi enhance the activity of nitrogen fixing and phosphorus solubilizing bacteria and thus promote plant growth.
As a result of synergistic interactions, dual inoculation of G. mosseae
and Trichoderma spp. increased the yield, seed quality and seed composition of soybean and also the growth of tomato by co-inoculation of P.
fluorescens and G. mosseae BEG12 (Egberongbe et al., 2010; Gamalero
et al., 2004). However, antagonistic interactions may also occur due to
nutrient competition and production of some secondary metabolites
(Antoun and Prevost, 2005; Long et al., 2000; Trivedi et al., 2012).
It has also been observed that these interactions also vary among
species and a same bacterium may react differently with different fungal
species. In a study conducted on wheat, Jaderlund et al. (2008) used two
bacterial strains (P. fluorescens SBW25 and P. brasilensis PB177), two AM
fungi (G. mosseae and G. intraradices) and one pathogenic fungus
(Microdochium nivale) to study their effect on plants in a greenhouse
trial. They observed that both bacteria affected the colonization levels of
the AM fungi in different ways. The fungus G. intraradices increased the
plant dry weight of M. nivale (pathogenic fungus)-infested wheat plants
when applied singly or in dual inoculation with P. fluorescens, however,
P. brasilensis nullified this positive effect. They suggested the testing of
the most suitable combination of plant, bacteria and fungi so as to achieve
satisfactory results in terms of improved growth. This argument is also
supported by the previous work of Requena et al. (1997) where coinoculation of native G. coronatum with bacterial strain was more effective
than that by exotic G. intraradices.
From above discussion, it is evident that positive interactions exist
between PGPR and mycorrhizae. The presence of PGPR and mycorrhizae
in the rhizosphere is helpful for promoting the activities of both populations. These synergistic interactions among PGPR and mycorrhizae
could be very helpful for enhancing plant growth and development in
soil environment.
8. Inducing stress tolerance through combined inoculation of PGPR
and mycorrhizae (PGPR–mycorrhizae interactions)
Although the combined inoculation of PGPR and mycorrhizae is reported to be helpful to enhance plant growth under normal conditions
440
Table 3
Examples of PGPR and mycorrhizae inoculation for promoting plant growth under normal conditions.
Crop
Bacteria/mycorrhizae
Response
Reference
Tomato (Lycopersicon esculentum)
a
Synergistic effect on root weight and root architecture and improved mineral nutrition by increasing Pcontent
Dual inoculation caused significant effect on lycopene, antioxidant activity and potassium content of
tomato
Gamalero et al. (2004)
a
Alfalfa (Medicago sativa)
Subterranean clover (Trifolium
subterraneum L.)
Mung bean (Vigna radiata)
Chick pea (Cicer arietinum)
Apple (Malus domestica)
a
Ordookhani et al. (2010)
Dual inoculation of PGPR and AM fungus provide great control of root-knot nematode on tomato than
single inocualtion
The effect was variable with respect to different combination of bacteria and AM.
Liu et al. (2012)
A significant increase in shoot and root dry weight, was observed when both the PGPR and AM fungi were
present.
Positive response of AM to EM was observed. Nodulation also enhanced significantly with co-inoculation
Dual inoculation enhanced nutrition and growth of chick pea
Meyer and Linderman
(1986)
Javaid et al. (2000)
Tavasolee et al. (2011)
The severity of root rot diseases of fungus decreased by mixture of AM fungus and bacteria
Dohroo and Sharma
(2012)
Medina et al. (2003)
PGPR.
Fungi.
b
Table 4
Examples of PGPR and mycorrhizae inoculation for promoting plant growth under stress conditions.
Crops
Type of stress
Bacterial strains/AM species
Effect
Reference
Retama (Retama sphaerocarpa)
Drought
*
Enhanced root development, reduced water required to produce shoot biomass
Marulanda et al. (2006)
Plant inoculated with mycorrhiza and Sinorhizobium strains are less affected by water stress.
Mycorrhizal plants modulated by genetically modified Sinorhizobium proved better.
Vazquez et al. (2001)
Paenibacillus brasilensis strongly inhibited the growth of pathogenic fungus M. nivale in dual
culture plate assays.
In a greenhouse experiment positive response was observed through co-inoculation but variable
Inoculation enhanced lycopene and antioxidant activity, shoot and fruit potassium content
Jaderlund et al. (2008)
Single as well as dual inoculation caused positive effect under lead contamination
Vivas et al. (2003)
Enhanced plant biomass. However, aggregate stability decreased under salinity even with inoculation
Kohler et al. (2010)
Medicago spp. (M. nolana, M.
rigidula, M. rotata)
Wheat (Triticum aestivum)
Pathogenic
Tomato (Lycopersicon esculentum)
P-deficient environment
Red clover (Trifolium pratense L.)
Heavy metal
Lettuce (Lactuca sativa)
Salinity
*
**
PGPR.
AM fungus.
Bacillus thuringiensis
**
Glomus intraradices
*
Sinorhizobium meliloti (wild type and
genetically modified derivative)
**
Glomus deserticola, Glomus intraradices
*
Pseudomonas fluorescens SBW25 and
Paenibacillus brasilensis PB177
**
Glomus mosseae and G. intraradices
*
Pseudomonas putida, Azotobacter
chroococcum and Azosprillum lipoferum
**
Glomus spp.
*
Brevibacillus spp.
**
AM fungus spp.
**
Pseudomonas mendocina
*
Glomus mosseae
Ordookhani et al. (2010)
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
Pseudomonas spp.
Glomus mosseae
Pseudomonas putida, Azotobacter chroococcum and Azosprillum
lipoferum,
b
Glomus intaradics, Glomus mossea and Glomus etunicatum.
a
Bacillus spp.
b
Glomus spp.
a
Bacillus pumillus and B. licheniformis
b
Glomus deserticola
a
Pseudomonas putida
b
Glomus fasciculatum
Effective microorganisms (EM) and AM
a
Mesorhizobium spp.
b
Glomus sp.
a
Bacillus and Pseudomonas spp.
Glomus spp.
b
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
(Table 3), the interactions between PGPR and mycorrhizae could be
very useful to reduce the negative impact of a stress on plant growth
and development (Table 4). Stress conditions not only disturb the normal plant physiology, but also cause adverse effects on microbial functions. The negative influence of a stress on microbial efficiency can be
reduced by combined inoculations. For example, root colonization of
lettuce by AM fungus was reduced under drought stress, but dual
application of fungus and bacteria improved it (Vivas et al. (2003).
The bacterium (Bacillus spp.) caused a significant stimulatory effect on
G. intraradices development by enhancing the mycelium growth.
This stimulatory effect of Bacillus spp. was further evaluated by coinoculating it with drought tolerant and drought sensitive species of
AM fungus under water stress environment (Marulanda et al., 2006).
Under drought stress, reduction in plant water uptake occurs. This
reduced water uptake decreased nitrogen and carbon metabolism and
ultimately changed the plant physiology (Ruiz-Lozano and Azcon,
2000). Microbial inoculation, as indicated in the earlier section, could
be more useful under such conditions. However, dual inoculation of
PGPR and mycorrhizae proved more useful for enhancing water and nutrient content. It is evident from the work of Benabdellah et al. (2011)
who reported improved water content of drought stressed Trifolium
repens inoculated with PGPR and mycorrhizal fungi. They demonstrated
that PGPR and AM inoculation decreased stomatal conductance and increased the relative water content; both are important for plants growing in water limited environment.
Similarly, maintenance of proper antioxidant system enables plants
to protect themselves from the deleterious effects of reactive oxygen
species. Although PGPR and AMF individually promoted the tomato
growth, however, maximum antioxidant activities were observed in
plants co-inoculated with both PGPR and AMF that enabled the plants
to combat harsh environment (Ordookhani et al., 2010). Under stress
environment, the non-availability of nutrients also becomes a limiting
factor for plant growth. This deficiency may be due to non-availability
of major nutrients like phosphorus even if it is present in the soil environment or due to antagonistic effect of one nutrient with others. In saline environment, high concentration of sodium caused a negative
impact on uptake of essential nutrients and dual inoculation of PGPR
and mycorrhizae proved helpful for providing nutrients to plants subjected to stress conditions. For example, a pot study carried out by
Shirmardi et al. (2010) on sunflower (Helianthus annuus L.) under salinity stress is an evidence of this claim. They found that inoculation with
PGPR and mycorrhizal fungus significantly enhanced the uptake of essential nutrients. Although they observed that mycorrhizae enhanced
the uptake of phosphorus however, they demonstrated that due to
small soil volume in pots, hyphae could not work properly and hence
did not show their full potential.
The co-inoculation was also effective in metal contaminated soils
where bacteria enhanced plant growth, N and P accumulation, as well
as nodule number and mycorrhizal colonization (Vivas et al., 2006).
This enhancement occurred due to stimulation of symbiotic structures
(nodules and AMF colonization) and a decreased Zn concentration in
plant tissues. Similarly, in a previous study, bacterial strains isolated
from lead polluted soil, enhanced plant growth, nitrogen and phosphorus accumulations, nodule formation, and mycorrhizal infection of
Trifolium pratense in the presence of Pb toxicity (Vivas et al., 2003).
In addition to biotic stress, co-inoculation of PGPR with mycorrhizae
is also helpful for alleviating the negative impact of biotic stress. The inoculation of PGPR and mycorrhizae proved useful for enhancing the
growth parameters and reducing the intensity of disease (Dohroo and
Sharma, 2012). They found that mixture of PGPR, AM fungi and their
helper bacteria decreased the severity of root rot of apple.
Although most of the work regarding co-inoculation of PGPR and
mycorrhizae was conducted in laboratory and greenhouse, however,
the dual inoculation of PGPR and mycorrhizae also proved useful for
improving plant growth under natural conditions. The work of
Constantino et al. (2008) showed that combined application of PGPR
441
and mycorrhizae was effective for improving plant growth and nutrient
content of habanero chili (Capsicum chinense Jacquin). It is also evident
from the field study of Adesemoye et al. (2008) where significantly
higher amount of N, P and K was observed from the plots inoculated
with PGPR, mycorrhizal fungi and/or both. The recent results of Najafi
et al. (2012) have shown the positive effects of PGPR–mycorrhizae
interactions with barley root enhanced the water and nutrition absorption. The major impact of drought on plant growth is the nonavailability of water. The dual inoculation of PGPR and mycorrhizae increased colonization and biological grain yield of barley under field
conditions. This association is also useful for protecting the plant from
deleterious impact of plant pathogens. Jaizme-Vega et al. (2006)
demonstrated that dual application of AM fungus and PGPR could be
very effective for controlling root-knot diseases of papaya caused by
nematodes. The effectiveness of co-inoculation was depending upon
mycorrhizal species.
The above reports show that dual inoculation of PGPR and mycorrhizal fungi is very effective for enhancing plant growth under stress environment. This positive effect might be due to combination of certain
mechanisms and also the synergistic effect of these populations on
one another. These synergistic interactions are effective in both biotic
and abiotic stresses. However, the selection of these combinations and
their effectiveness under natural soil environment still needs further
investigation.
9. Mycorrhizae–PGPR application and constraints under natural
environmental conditions
It is evident from the above sections of the review that application of PGPR and/or mycorrhizae is very effective for promoting
growth and development of most plants. This synergistic effect is
due to positive interactions among PGPR, mycorrhizae as well as
the plant. The application of PGPR with mycorrhizae could be very
beneficial for plant growth for one or the other reason. In coinoculation, each strain not only competes successfully with indigenous rhizosphere population, but also proves helpful for promoting
the growth of each other. For example, PGPR by their effect on root
colonization and nutrient uptake enhance AM fungal development
(Richardson et al., 2009). Similarly, enhancing the amount of root exudates by microbe activates the fungal hyphae and hence increases
the rate of root colonization (Barea et al., 2005). P. fluorescens
C7R12, an effective biocontrol agent against Fusarium spp., is also
helpful for promoting symbiosis between Medicago truncatula and
G. mosseae (Pivato et al., 2009). Before this, in an earlier study,
Barea et al. (1998) also demonstrated that Pseudomonas spp. had the
ability to produce antifungal metabolites but did not cause any negative effect on G. mosseae. On the other hand, the bacterial strain promoted the root colonization by the fungal hyphae. Bianciotto et al.
(2001) observed that exopolysaccharides-producing PGPR enhanced
the bacterial attachment to mycorrhizal roots and fungal structure.
Bacterial strains also stimulate spore germination of AM fungus
(Hildebrandt et al., 2006). Therefore, the co-inoculation of PGPR
with AM fungus can enhance the AM activity during symbiosis
(Artursson et al., 2006).
The presence of PGPR and mycorrhizae in the rhizosphere is not only
helpful for plant growth but it is also beneficial for each other. On one
hand, bacteria stimulate the hyphal growth by enhancing cell permeability so as to facilitate root penetration by the fungus (Jeffries et al.,
2003), while on the other hand, mycorrhizae enhance the activities of
nitrogen fixing and phosphorus solubilizing bacteria (Linderman,
1992).
The above discussed studies indicate that PGPR and mycorrhizae
alone or in combination could be very effective for enhancing plant
growth and development under normal as well as stress conditions.
However, the major bottleneck to the commercial use of microbial inoculants is their inconsistent performance under field conditions. It has
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S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
been observed that under certain cases the results obtained in a field are
not similar to those of laboratory (Smyth et al., 2011; Zhender et al.,
1999). The inoculum efficiency depends upon a number of factors like
soil mineral content, type of crop and competition with indigenous
strains (Jefwa et al., 2009). In certain cases, the inoculum fails to form
association as observed by Corkidi et al. (2004) where half of ten inoculants failed to perform. The inconsistency in results might be due to the
reason that inoculum has less ability to compete with an indigenous
population. It has been observed that microbial performance in the rhizosphere was significantly affected due to competition with an indigenous population for nutrient and niches (Strigul and Kravchenko,
2006). This might also be due to certain edaphic conditions and a number of abiotic factors (Schreiner, 2007). For example, tillage can reduce
the mycorrhizal activity (McGonigle and Millar, 1993). Although tillage
practice is recommended as a key soil management practice, it causes a
negative impact on AM fungus by disrupting mycelial network (Jasper
et al., 1991). Similarly, soil nutrition also affects the activity of mycorrhizae. For example, high phosphorus content in soil reduces the activity of
AM fungus (Mitiku and Aswathanarayan, 1987). Such kind of inconsistent results are more common where a single inoculum is used. However, such variability can be minimized in field conditions where multistrain inoculum or co-inoculation is adopted.
Moreover, in certain cases, detrimental interactions also take place.
Such interactions might be due to incompatibility and/or pathogenicity
of one partner to the other as observed by Dewey et al. (1999). They observed that associated bacteria enhanced the fungal pathogenicity, although the bacterium itself was nonpathogenic. The presence of such
partners which do not have compatibility with each other could be
one of the reasons for their failure in the field.
The synergistic interactions between PGPR and AM were also observed in plants exposed to saline environment (Gamalero et al.,
2010). However, surprisingly, this effect disappeared at high salt concentration. According to their view, this may be due to the reason that
plants exposed to salt stress can release different root exudates that
may decrease or abolish the synergism among the microorganisms. It
may also be due to the non-compatibility of inoculated strains. For example, Kohler et al. (2010) showed that although co-inoculation of
PGPR and/or AM fungi enhanced the biomass of Lactuca sativa in the
presence of salinity, they found that the aggregate stability of soils inoculated with the PGPR and/or G. mosseae significantly decreased with increase in the intensity of saline stress. They demonstrated that suitable
combination of strains should be used for maintaining proper plant and
soil health. It is also evident from an earlier work where PGPR and AM
fungi suppressed the Verticillium wilt of strawberry when applied
alone, however, dual inoculation did not cause a significant effect compared with the single inoculation (Tahmatsidou et al., 2006). Although
they did not give any explanation of this non-additive response of
dual inoculation, they emphasized the need to further investigate this
aspect. Therefore, for obtaining maximum benefit from this naturally
occurring population, it is important to determine the PGPR specificity
for AM fungus as well as for plant. The PGPR–mycorrhizae interactions
are very important from plant growth point of view and the testing of
most suitable combination of plant, bacteria and fungi could be one of
the suitable solutions to obtain satisfactory results in both laboratory
and field conditions.
10. Conclusion and future prospects
It is evident from the above discussion that stressful environments
can cause a negative impact on plant growth and development by causing nutritional and hormonal imbalances. However, the stress-induced
negative impact on plant growth can be alleviated and/or minimized
by naturally occurring microorganisms including bacteria and fungi
whether applied singly or in combination.
Although a number of studies revealed the effectiveness of sole application of PGPR or mycorrhizae for improving plant growth under
stress conditions, however, a number of researchers have reported
more usefulness of dual inoculation compared to that of individual inoculation. In spite of better performance of dual inoculation of PGPR and
mycorrhizae, there are still certain aspects which need critical consideration. One important aspect is the evaluation of this approach under
natural field conditions. Most of the previous studies were conducted
under controlled conditions, and the response of these organisms observed under such conditions may vary significantly in view of variable
ecology of these microorganisms in the natural environment. In soil environment, a number of biotic and abiotic factors also interact with
these organisms that may affect their performance. Additionally, most
of the work has been done on major stresses i.e. drought and salinity.
No doubt, salinity and drought are two major stresses that cause detrimental effect on plant growth all over the world, but in a natural environment, plants also have to face other harsh conditions like toxicity
of heavy metals and pathogen attack. Therefore, the role of combined
inoculation of these microorganisms for providing relief from other
stresses also needs to be researched.
It is also evident from the above discussion that PGPR and AM species show a variable response under different stress environments. It
might be due to their ability to mitigate the impact of stress due to
their specific traits. Such traits enable them to tolerate stress conditions
and also enhance their ability to promote plant growth. The application
of specific strains under a particular stressful environment could be effective for obtaining maximum benefits from microbial inoculation. It
has also been observed that in certain cases dual inoculation does not
yield significant results when compared with single inoculation. It indicates the incompatibility of these strains with one another. Therefore,
utmost care should be taken while selecting strains for dual inoculation.
It is also observed from the above discussion that microbes can enhance
plant growth by a number of mechanisms; however, most of the studies
have been focused on individual mechanisms. It is therefore necessary
to examine the relative contribution of all these mechanisms involved
in growth promotion. Similarly, ecology, colonization time and environment may alter the specific function of PGPR and fungi. Therefore, it is
also necessary to understand which factor limits performance of microbial inoculation and how this limitation can be overcome. Such understanding will be very useful for improving the effectiveness of
microbial inoculums under natural environment.
The role of PGPR and mycorrhizae for nutrient acquisition is well defined in the above discussion; however, the correlation between nutrient solubilization and their uptake by the plant is not yet clear. Future
studies on this issue will help enhance our understanding of how microbial inoculation could be helpful to minimize the environmental impact
of fertilizers by reducing their use.
The use of PGPR and mycorrhizae strains has great potential to protect plants from diseases through their biocontrol mechanism. This offers an alternative environment-friendly strategy by reducing the use
of chemicals. Such microbial populations need systematic strategy so
that their potential can be utilized in an effective way.
Another important aspect is to generate transgenic plants encoding
the genes of particular traits of PGPR or mycorrhizae. The literature
shows that these transgenic plants have the ability to withstand stress
environment. However, such studies were conducted in controlled conditions. Most of these studies are preliminary investigations which require further verification by performing extensive experimentation.
Moreover, information about the molecular mechanisms governing
the process of stress tolerance is limited. Identification of genes controlling stress tolerance traits of PGPR and mycorrhizae would enhance our
knowledge about the molecular basis of the stress tolerance mechanisms. Most of the in vitro studies lack biochemical and physiological
mechanisms involved in stress tolerance. Thus, the work on this aspect
will significantly improve the understating of the mechanism.
Overall, future research should be focused: i) to elucidate the mechanisms of interactions between PGPR and mycorrhizae in natural field
conditions under stressful environments, ii) to explore what strains of
S.M. Nadeem et al. / Biotechnology Advances 32 (2014) 429–448
PGPR and fungus are beneficial for promoting plant growth and also the
combination of these strains that interact synergistically so as to achieve
a maximum benefit (iii) to examine the effectiveness of co-inoculation
in a multi-stressed natural environment for commercialization of
microbial inocula, iv) to identify target genes for promoting growth
under stress, and v) to transfer target genes into plants through
biotechnology.
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