Plant growth promoting rhizobacteria for ameliorating abiotic stresses triggered due to climatic variability

Abstract

The world is gifted with varied landforms and diversity of climatic conditions such as the lofty mountains, the riverine deltas, high altitude forests, peninsular plateaus, variety of geological formations endowed with varying temperature and rainfall. Physical features like temperature, pH, salinity, water content constitute abiotic factors of the ecosystem and if these factors exceed beyond the threshold limit then, they might result in abiotic stresses. Economy of different countries relies on agriculture and abiotic stresses are the major constraints that limit crop productivity around the globe. The development of stress tolerant crops is not an easy and economical approach for sustainable agriculture; however microbial inoculation to alleviate stress tolerance is a better option because it minimizes production costs and environmental hazards.

Full text

RESEARCH ARTICLE
Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
DOI:
Plant growth promoting rhizobacteria for ameliorating abiotic
stresses triggered due to climatic variability
Sakshi Tewari ••
••
• Naveen Kumar Arora*
Abstract The world is gifted with varied landforms and
diversity of climatic conditions such as the lofty mountains,
the riverine deltas, high altitude forests, peninsular plateaus,
variety of geological formations endowed with varying
temperature and rainfall. Physical features like temperature,
pH, salinity, water content constitute abiotic factors of the
ecosystem and if these factors exceed beyond the threshold
limit then, they might result in abiotic stresses. Economy of
different countries relies on agriculture and abiotic stresses
are the major constraints that limit crop productivity around
the globe. The development of stress tolerant crops is not an
easy and economical approach for sustainable agriculture;
however microbial inoculation to alleviate stress tolerance
is a better option because it minimizes production costs and
environmental hazards.
Keywords Abiotic stress, drought stress, pseudomonas,
PGPR, salinity stress
Introduction
Agriculture is considered to be the most vulnerable
sector that is often exposed to the plethora of climate-change.
Abrupt change in climatic conditions increases the incidence
of abiotic and biotic stresses that become major cause for
stagnation of productivity in principal crops (Grover et al.,
2010). Amongst abiotic factors, interseasonal climatic
variability is a concern, which is usually reflected from year-
to-year fluctuations in crop yields. The probability of
occurrence of extreme climatic events such as drought,
salinity, extreme high/low temperatures, flooding stress,
heavy metals stress has increased in the last couple of
decades, and farmers lack the management options to sustain
the agricultural productivity (Kalra et al., 2013).
When farmers see their agricultural crops declining in
yield and production due to abiotic stresses, they often expect
a dramatic and magical treatment to make them lush, green,
Department of Environmental Microbiology, Babasaheb Bhimrao Ambedkar University, Lucknow, India
*Corresponding author E-mail id: nkarora_net@rediffmail.com
and healthy again so that productivity increases. As a result,
they start using chemicals and fertilizers disregarding their
future effects. The extensive use of certain synthetic organic
chemicals in the past decades has led to a number of long-
term environmental problems (Arora et al., 2012).
One of the focuses of the present research involves
implication of plant associated microbes (PAMs) including
plant growth promoting rhizobacteria (PGPR) to combat the
harmful effects of these ecological stresses and enhance plant
growth and productivity by direct and indirect mechanisms
(Kloepper and Schroth, 1978; Arora et al., 2013). PAMs can
play important role in conferring resistance to abiotic
stresses. These organisms basically include close residents
of rhizosphere, rhizoplane, phyllosphere, phylloplane,
endophytes and symbiotic fungi that operate through a
variety of mechanisms, like triggering stress response that
alleviates stress tolerance and induction of novel genes in
plants. The development of stress tolerant crop varieties
through genetic engineering and plant breeding is essential
but a long drawn and costly process, whereas microbial
inoculation to alleviate stresses in plants could be a more
cost effective, environmental friendly option which is
available in a shorter time frame (Grover et al., 2010). The
main aim of the present review is to highlight the impact of
climatic variations that cause abiotic stresses and to
apprehend the role of microorganisms in helping crops to
cope with various abiotic pressures.
Climatic variability govern abiotic stress
Global warming and changes in precipitation patterns,
lead to several abiotic stresses such as extremes temperatures,
drought, flooding, salinity, metal stress, nutrient stress that
are bound to have adverse effects on food production
(Pandey et al., 2007; Barrios et al., 2008; Selvakumar et al.,
2012). Climate change models have predicted that warmer
temperatures and increase in the frequency and duration of

2Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
drought during the twenty-first century will have net negative
effects on agricultural productivity (St Clair and Lynch,
2010).
In the developing countries, it has been estimated that
on an average, nearly two thirds of the soils are prone to
climatic constraints that significantly reduce crop yields (Lal,
2000). Change in climatic factors result in abiotic stresses
for the crops. Abiotic stress hamper growth and production
of crop, causing land degradation by making soil nutrient
deficient and more stress prone. In one way or another abiotic
stresses are intermingled and correlated with one another.
For example climatic variability such as increase or decrease
in rainfall, rise or fall in temperature brings drought stress.
Drought stress ultimately gives rise to salinity stress (Munns,
2002). Salinity stress causes alkalization of soil. In alkaline
- saline soil the nutrients remain unavailable to the plant
and it leads to nutrient deprived situation or nutrient stress
(Maheshwari, 2012). Humidity is other climatic variability;
in humid areas rate of precipitation is high, soil leaching
decreases soil pH due to the reduction of basic cations. The
adverse effects of soil pH results in acidification stress, the
acidification stress makes nutrient unavailable to plants and
further leads to nutrient stress platform. The abiotic stresses
thus are intermingled and interconnected with one another
and function as a chain, that too very much due to climatic
variations (Grover et al., 2010).
It should be highlighted that the subsequent demand
for food is expected to rise by 3–5 times, the current food
production has to increase by 60% in order to meet the
demands of the future (Wild, 2003). According to the Food
and Agricultural Organization (FAO), if corrective measures
are not taken then these abiotic stressors may result in 30%
land loss in the next 25 years and up to 50% loss by the year
2050 (Munns, 2002). Abiotic stressors are the principal cause
of crop failure worldwide, dipping average yields for major
crops by more than 50% (Mahajan and Tuteja, 2006). Abiotic
stresses cause losses worth hundreds of million dollars each
year due to reduction in crop productivity and crop failure.
In fact these stresses, threaten the sustainability of
agricultural industry. So it is necessary that these stress
affected regions should be reclaimed immediately for the
better future and food security. Ultimately food security can
only be achieved by more production in ever reducing
cultivable land, reclaiming stressed soils and shunning the
harmful chemicals.
PGPRs conflicting and ameliorating abiotic stress
Any living organisms under stressful condition opt for
either of the two strategies: fight or flight. Since plants are
sessile, they cannot run away from adverse conditions, so
they fight back; their tolerance capacity, growth, and
production can be increased with the help of several
mechanistic actions of PGPRs. One of the recent focuses of
research involves implication of PGPRs to combat stress.
The development of biological products based on beneficial
microorganisms can extend the range of options for
maintaining the healthy yield of crops in stressed habitats.
In recent years, this approach to utilize PGPRs for alleviating
salt stress in plants has been developed. PGPRs like
Achromobacter, Azotobacter, Azospirillum, Acetobacter,
Bacillus, Chryseobacterium, Flavobacterium, Enterococcus,
Klebsiella, Pseudomonas, Rhizobium, Serratia,
Paenibacillus are being used currently for conflicting and
ameliorating varied stresses in diverse habitats (Zahran,
1999; Arora et al., 2012; Egamberdieva, 2012; Mishra et
al., 2012; Turan et al., 2012). This section includes different
types of stresses that occur in nature due to natural calamities
and how PGPRs can combat them (Table 1). As stated earlier
in nature one stress generally leads to other stresses and there
can be a sequential phenomenon however, here we discuss
them in isolation just as to determine the impact and solution
for each stress.
Drought stress
Drought stress is one of the major abiotic stresses that
limit crop yields, both at cellular and molecular levels
(Ingram and Bartels, 1996; Vinocur and Altman, 2005;
Saleem et al., 2007). It has been estimated that about one-
half of the earth is vulnerable to drought every year (Kogan,
1997). Climatic variability like decreased land precipitation
and increased temperature, enhances evapotranspiration and
reduces soil moisture that results in droughts. Drought
contributes to estimated 30% reduction in gross primary
production of terrestrial ecosystems over Europe (Ciais et
al., 2005).
Drought stress make plant unavailable to utilize water;
water deficiency leads to an enhanced level of ethylene,
leading to abnormal growth and loss in crop production
(Mattoo and Suttle, 1991; Mayak et al., 2004). The elevated
levels of ethylene could be responsible for inhibiting root
and shoot growth, abscission, and premature senescence of
plants parts (Sharp, 2002).
The constraint of drought stress can be healed by
utilizing drought tolerant PGPRs including Azotobacter,
Azospirillum, Bacillus, Rhizobium, Serratia etc (Sandhya et
al., 2009). Under transient water stress, the ACC deaminase
producing PGPR Achromobacter piechaudii significantly
increased the fresh and dry weights of tomato and pepper
seedlings and reduced the ethylene production (Mayak et
al., 2004). Rhizobium meliloti was found to be symbiotically
effective under drought stress and enhanced the production
of alfalfa (Athar and Johnson, 1996). The ability of the
rhizobacterial strain Pseudomonas putida to improve the
plant biomass, relative water content, leaf water potential,

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Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
Table 1 Amelioration of plant health by PGPRs under diverse stress conditions
Abiotic stresses Constraints of abiotic PGPRs for Metabolites/ References
stress in plants amelioration Mechanism
Salinity stress Osmotic stress, Na+ and Cl–Azotobacter, Synthesis of compatible Arora et al., 2012
toxicity, ethylene production, Azospirillum, solutes, ACC deaminase,
plasmolysis, nutrient imbalance Bacillus, Pseudomonas, phosphate solubilization,
and interference with Serratia, Rhizobium biological nitrogen
photosynthesis, decrease of fixation, EPS,
photosynthetic capacity due antioxidative activity
to the osmotic stress, and
partial closure of stomata
leads to hampered plant
growth.
Drought stress Reduces the amount of AMF, Bacillus, Synthesis of heat shock Egamberdieva, 2012
available water for plant use Azospirillum, proteins, siderophore
and effects plant growth. Rhizobium, production, nitrogen
Pseudomonas fixation, phosphate
solubilization for
nutrient uptake and
EPS production
Cold stress Chilling injury causes Exiguobacterium, Synthesis and Mishra et al., 2012
reduction or cessation of Pseudomonas, accumulation of low
growth and photosynthesis, Pantoea, Serratia, and high molecular
tissue water content is Streptomyces weight cryoprotectants,
reduced, solutes accumulate synthesis of antifreezing
and diminish plant growth. proteins
Alkalization/ Excessive leaching of soil Bacillus, Rhizobium, Phosphate solubilization, Zahran, 1999
Acidification stress leads to mineral nutrient Bradyrhizobium, nitrogen fixation,
deficiency (N,P, Fe), that Azotobacter, siderophore production
makes plants weak, short, Azospirillum, to ameliorate nutrient
stunted in growth Pseudomonas, loss
Bacillus Mycorrhiza
Flooding stress Reduced root permeability, Bacillus, ACC deaminase Grichko and Glick,
closure of stomata, decreased Enterobacter, containing bacteria 2001
photosynthesis, alteration in Pseudomonas degrade ACC and
hormone level, inhibition of establish their niche in
stem and root growth and root zone.Lowers the
premature fruit drop level of endogenous
ethylene in plant.
Heavy metal stress Causes metal toxicity by Azotobacter, Bacillus, Stimulated plant growth Turan et al., 2012
accumulation of heavy Pseudomonas, and reduces metal
metal Ni, Cd, Zn, Cu, that Rhodococcus, toxicity by
leads to stunted plant growth flavobacterium phytoremediation
through, siderophore
production, phosphate
solubilization
proline sugars, and free amino acids of maize plants exposed
to drought stress was recently reported by Sandhya et al.,
(2010).The alleviating effects of Arbuscular Mycorrhizae
(AM) fungi on plant growth under drought stress has been
reviewed by Auge (2001) and Evelin et al., (2009). The
extensive hyphal network of AM, significantly increase water
and nutrient uptake by the host plant, which is among the
most important reasons for the enhanced plant tolerance to
the drought stress. Arzanesh et al. (2011) indicated that
efficient strains of Azospirillum spp., significantly alleviated

4Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
the stress of drought on wheat growth. These strains had the
ability to fix N non-symbiotically, and produce plant
hormones such as auxins. They were also able to produce
ACC deaminase, solubilize phosphorous, and produce
siderophores under drought stress. The production of
polysaccharides by PGPRs such as Bacillus, Rhizobium and
Pseudomonas is also another effective mechanism that can
improve soil structure by binding soil particles and hence
alleviates the drought stress (Sandhya et al., 2009; Belimov
et al., 2009). Under drought stress, co-inoculation of bean
(Phaseolus vulgaris L.) with Rhizobium tropici and two
strains of Paenibacillus polymyxa resulted in augmented
plant height, shoot dry weight, and nodule number. Co-
inoculation of lettuce (Lactuca sativa L.) with PGPR
Pseudomonas mendocina and AM fungi (Glomus
intraradices or G. mosseae) augmented an antioxidant
catalase under severe drought conditions, suggesting that
they can be used in inoculants to alleviate the oxidative
damage elicited by drought (Yang et al., 2009;
Egamberdieva, 2012). Another interesting feature of drought
stress alleviation by microbes is the improvement in the Root
Adhering Soil/Root Tissue (RAS/RT) ratio as a result of
inoculation with exopolysaccharides (EPS) producing
PGPR, to counteract the negative effects of drought stress
(Miller and Wood, 1996; Munns, 2002).
Salinity stress
Drought stress and salinity stress are interconnected and
intermingled with one another in fact it may be stated that
climatic variability that causes drought stress gives rise to
salinity stress also (Serrano et al., 1999). Most of the salty
land has arisen due to the presence of salts (like Na+, Cl-,
SO4
2-,Ca2+,Mg2+) in irrigation water over long period of time
that gives rise to arid and semiarid zones (Rengasam, 2002).
As the temperature rises, water evaporates and transpires
the Ca2+, and Mg2+ tend to precipitate as carbonates, leaving
Na+ cation dominant in soil (Ashraf, 1994). At present more
than 900 million hectares land worldwide is suffering from
the problem of salinity (Flower, 2004; Khan and Panda,
2008) and further, salinity gives rise to ionic and osmotic
stress that hamper growth and production of plant (Serrano
et al., 1999).
Soil salinity prevents plant growth and development
with adverse effects such as osmotic stress, Na+ and Cl–
toxicity, ethylene production, plasmolysis, nutrient
imbalance and interference with photosynthesis, decrease
of photosynthetic capacity due to the osmotic stress, and
partial closure of stomata (Drew et al., 1990). Plants suffering
from saline stress present alterations in their homeostasis,
mainly because of a reduction in the osmotic potential and
an inadequate ionic distribution, which causes a nutritional
imbalance.
The problem of salinization can be overcome by utilizing
salinity tolerant PGPRs that synthesize compatible solutes,
osmoprotectants, osmolytes, antioxidants, EPS and maintain
PGP properties like siderophore, phosphate solubilization,
nitrogen fixation, IAA production etc under saline conditions
as reviewed by Arora et al. (2012). PGPR strains, especially
EPS-producing Bacillus, Pseudomonas and Rhizobium, have
been reported to induce soil salinity tolerance and growth
promotion in soybean (Bezzate et al., 2000; Ashraf et al.,
2004). Ryu et al. (2004) showed that Bacillus subtilis induces
systemic tolerance against salinity stress in Arabidopsis
plants.
Under saline conditions, generation of reactive oxygen
species (ROS) causes oxidative damage to biomolecules such
as lipids and proteins that eventually leads to plant death
(Del Rio et al., 2003). PGPR such as Sinorhizobium
proteamaculans and Rhizobium leguminosarum produce
antioxidant enzymes such as superoxide dismutase (SOD),
peroxidase (POX), and catalase (CAT) and nonenzymatic
antioxidants such as ascorbate, glutathione, and tocopherol
that protect plant under saline conditions (Han and Lee,
2005). Synthesis of many compatible solutes (glutamate,
proline, glycine, betaine, carnitine, sucrose, trehalose,
tetrahydropyrimidines (ectoines) by PGPRs proved to be
effective stabilizers of enzymes, providing protection not
only against high salt but also against high temperature,
freeze–thawing, and drying (Yancey et al., 1982; Galinski
and Truper, 1994). Large number of PGPRs like Alcaligens,
Arthobacter, Azotobacter, Azospirillum, Bacillus, Klebsiella,
Pseudomonas, Paenibacillus, Rhizobium, Rhodococcus,
Serratia, Thiobacillus, Xanthomonas etc. are being used for
enhancing plant growth parameters under saline conditions
(Arora et al., 2012). Khare et al. (2011) reported the
suppression of charcoal rot of chickpea by fluorescent
pseudomonas under saline stress condition
Alkalization and acidification stress
Soil acidity/alkalinity are the significant problems faced
by agriculture in many areas of the world that limits crop
productivity (Zahran, 1999). Distinctions between acidic and
alkaline soils are usually associated with differences in
amount of precipitation compared to evapotranspiration
(Clark and Baligar, 2000). If precipitation exceeds
evapotranspiration for some time, soils usually are leached,
which leads to formation of acidic soils. If evapotranspiration
exceeds precipitation, soils are usually neutral to alkaline.
Alkaline soils are also well distributed throughout the world,
and various mineral deficiency and toxicity problems are
commonly associated with them (Wilkinson, 1999). Both
acidic and alkaline soils can impose relatively severe mineral
nutritional problems on plants making them weak and fragile.
Approaches for overcoming mineral nutrient deficiency/

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Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
toxicity constraints under alkaline or acidic conditions might
be to take advantage of soil microorganisms such as
mycorrhiza and beneficial phosphate solubilizing bacteria/
fungi (Paul and Clark, 1988). Widada et al. (2007) reported,
effects of AM fungi and rhizobacteria inoculation
(phosphate-solubilizing bacteria, N2-fixing bacteria and
siderophore-producing bacteria) on the growth and nutrients
uptake of Sorghum in acidic and low-availability phosphate
soil. Inoculation of either AMF or rhizobacterium improved
the plant dry weight and uptake of nutrients such as N, P,
Fe, and Zn. Dual inoculation of AMF and rhizobacterium
yielded higher plant dry weight and nutrients’ uptake
compared to single inoculation (Clark and Baligar, 1999).
Occurrence of PGPRs such as Rhizobium, Bradyrhizobium,
Azotobacter, Azospirillum, Pseudomonas and Bacillus has
been reported from desert ecosystems, acid soils, alkaline
areas and highly eroded hill slopes of India (Selvakumar et
al., 2009).These PGPR offer protection of plant health under
stressed conditions. Zahran (1999) reviewed that the
selection of acid-tolerant strains of rhizobia will ensure the
establishment of legume symbiosis that leads to increase crop
production. Rhizobium loti and R. tropici are repoted to
multiply at pH 4.5 and have the ability to nodulate legume
at acidic pH (Cunningham et al., 1984; Zahran, 1999).
Temperature stress
Plants are sensitive to temperature changes and respond
to seasonal variations and diurnal changes in the season.
Change in temperature, due to global warming posse serious
threat to world agriculture. Fluctuation in temperature leads
to hormonal imbalances in plants and, thus, their growth is
significantly influenced. Increase in ethylene production
under high and chilling temperatures has been reported by
several researchers, both in plant tissues and microbial
species in the rhizosphere (Wang, 1987; Strzelczyk et al.,
1994). Thus, an introduction of rhizobacteria containing
ACC deaminase into the plant ecosystem could ease
unfavorable conditions caused due to temperature variations.
For example, a rhizobacterium possessing ACC deaminase
activity, Burkholderia phytofirmans inoculated in potato
was able to maintain stem length, shoot and root biomass
under temperature stress (Bensalim et al., 1998).
Tuberization was also enhanced by as much as 63% in
bacteria-treated potato. The same bacterium enhanced plant
growth and physiological activity of grapevine explants
under in vitro at both ambient (26°C) and low (4°C)
temperatures (Cheng et al., 2007). The study clearly indicates
the potential of ACC deaminase in normalizing plant growth
through lowering stress ethylene induced by extreme
temperature conditions. Protein denaturation and aggregation
are the other major types of cellular damage that result from
higher temperatures. Ali et al. (2009) reported the ability of
a thermo tolerant Pseudomonas strain to alleviate the heat
stress in sorghum seedlings. Srivastava et al. (2008) isolated
thermotolerant P. putida from drought stressed rhizosphere
of chickpea. The thermotolerance of the strain was attributed
to the over expression of stress sigma factor and enhanced
biofilm formation at high temperatures.
Frost injury as a result of cold temperatures is one of
the most commonly encountered problems in temperate
agriculture. Chilling stress is a direct result of low-
temperature effects on cellular macromolecules that cause a
slowdown of metabolism, solidification of cell membranes
and loss of membrane functions. Freezing stress acts
indirectly via extracellular ice crystals that cause freeze
dehydration, concentrate cell sap and have major mechanical
impacts (Mishra et al., 2012). To improve cold stress in
plants, cold-tolerant PGPRs are being used (Ait Barka et
al., 2006; Cheng et al., 2007). Ait Barka et al. (2006)
observed that in vitro inoculation of grapes (Vitisvinifera
cv. chardonnay) explants with a PGPR, B. phytofirmans,
increased grapevine root growth and plantlet biomass, and
physiological activity at a low temperature. A psychrotolerant
ACC deaminase producing bacterium P. putida UW4 was
found to promote canola plant growth at low temperature
under salt stress (Cheng et al., 2007). Pseudomonas spp
strain PPERs23 significantly improved root length, shoot
length, dry root biomass, dry shoot biomass, total
chlorophyll, total phenolics, and amino acid contents of
wheat seedlings. Certain epiphytic bacteria such as Erwinia
herbicola and Pseudomonas syringae with ice-nucleating
activity (ice+ bacteria) prevented supercooling of plants at
subzero temperatures (Lindow and Leveau, 2002).
Increasing population of P. syringae (ice+) bacteria resulted
in increase in ice-nucleation temperature that could be an
effective and practical means to manage cold/low-
temperature stress in plants (Lindow and Leveau, 2002). Ice
nucleating strains of P. syringae are known to increase the
frost susceptibility of tomato and soybean when sprayed on
leaves prior to low temperature stress (Anderson et al., 1982).
The potential of novel cold tolerant plant growth promoting
bacterial species viz., Pantoea dispersa, Serratia
marcescens, Pseudomonas fragi, Exiguobacterium
acetylicum and Pseudomonas lurida in promoting plant
growth at cold temperatures was demonstrated by
Selvakumar et al. (2012).
Flooding stress
Globally, the number of great inland flood catastrophes
during the period 1996–2005 are twice as large, per decade,
as between 1950 and 1980, while related economic losses
have increased by a factor of five (Kron and Berz, 2007).
Floods have been the most reported natural disaster events
in many regions, affecting 140 million people per year on

6Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
average (WDR, 2003). Variety of climatic processes like
intense precipitation, snowmelt due to increase in
temperature, dam break due to heavy rain, ice jams or
landslides, or by storm cause flooding stress (Kron and Berz,
2007). Flood stress leads to water logging; water logging
causes the ACC, which is synthesized in roots, to be
transported to plant shoots, where it is converted to ethylene
by ACC oxidase (Bradford and Yang, 1980). The increased
ethylene levels observed in shoots of waterlogged plants
corresponds with enhanced activities of ACC synthase in
the submerged roots and ACC oxidase in the shoots (Chao
et al., 1997; Olson et al., 1995). Grichko and Glick (2001)
observed significant tolerance to flooding in 55 day old
tomato plants inoculated with ACC deaminase producing
strains of Pseudomonas and Enterobacter. Much more efforts
are required to unravel the potential of rhizobacterial species
in alleviating water logging or flood stress as uptill now the
information regarding this is very less.
Heavy metal stress
Temperature and flood stress can also give rise to heavy
metal stress. High temperature, increased precipitation
intensity, and long periods of low flows are projected to
exacerbate soil pollution that includes sediments, pathogens,
pesticides, heavy metals and thermal waste. Intense rainfall
comprising rainwater and melt water draining from hard
surfaces, such as roads and roofs in urban areas, often contain
heavy metals, in particular Cu, Zn, Cd, and Pb (Morrison,
1989; Pettersson et al., 1999). In addition, more frequent
heavy rainfall events overload the capacity of sewer systems
and water and wastewater treatment plants often release
heavy metals that severely contaminates soil with them
(Leemans and Kleidon, 2002; Bouraoui et al., 2004). Over
recent decades, the annual worldwide release of heavy metals
reached 22,000 MT (metric ton) for cadmium, 939,000 MT
for copper, 783,000 MT for lead and 1,350,000 MT for zinc
that results in heavy loss in yield and production of
agricultural crops (Singh et al., 2003; Turan et al., 2012).
Some PGPR strains are known to have potential for
mitigating the effect of heavy metal contamination in soil as
they reduce the toxic effects of heavy metals on plants by
accumulating those (Belimov et al., 2004). Recently much
attention has been paid in bioremediation of heavy metal
contaminated soils with PGPRs (Narasimhan et al., 2003;
Huang et al., 2005). Under heavy metal contamination
conditions, it has been hypothesized that plant growth is
mainly achieved by introducing PGPRs that display IAA
production (Patten and Glick, 2002), ACC deaminase activity
(Penrose and Glick, 2001), and siderophores (Burd et al.,
2000).
Sheng et al. (2008) observed increases in biomass
production and total lead uptake in Bacillus napus after
inoculation with Microbacterium sp. G16, a bacterial strain
that can produce IAA, ACC deaminase, and siderophores.
Soil microbes such as AM fungi and PGPR can alleviate the
stress of heavy metals by absorbing high rates of heavy
metals in their tissues. There are different mechanisms by
which soil microbes can detoxify the unfavorable effects of
heavy metals in their tissue including intra- and extra-cellular
mechanisms. Production of proteins, which absorb heavy
metals, and detoxification of metal stress by accumulating
them in their vacuoles are among some of the most important
mechanisms by which soil microbes can alleviate this stress
(Gerhardt et al., 2009; Giller et al., 2009; Haferburg and
Kothe, 2010). Kinkle et al. (1987) examined two genera of
soybean-nodulating rhizobia and bradyrhizobia to determine
the level of resistance to different heavy metals.
(Zahran,1999) reviewed the addition of Ni (5 to 8 mM) to
both the nitrate grown and symbiotically grown soybean
plants resulted in a 7-to 10-fold increase in urease activity
in leaves and significantly increased the hydrogenase activity
in isolated nodule bacteroids.
Conclusion
Abiotic stressors are the combined result of
anthropogenic activity and climatic variability that limit
agriculture around the globe. All the stressors occurring in
nature are in turn connected with one another in a series.
For example drought stress gives rise to salinity stress,
temperatures, acidity/alkalinity, low pH and metal toxicity
(Grover et al., 2010). However, nowadays the role of
microbes in management of abiotic stresses is gaining
importance. The subject of PGPR elicited tolerance to abiotic
stresses in agriculture is opening the new and emerging
application of microorganisms in stress agronomy.
Understanding the mechanisms of stress tolerance in PGPR
is expected to contribute to the long-term goal of plant–
microbe interactions for exploitation of stress affected
regions so as to enhance crop productivity. Development of
stress-tolerating microbial bioformulations will be a non-
polluting and cost-effective way to improve production of
crops in a deteriorated environment. In general, PGPRs can
contribute to reduce the burden of soil nutrient loss in arable
lands, to counteract part of the negative effects of saline
stresses on plant growth, and help plants to avoid or minimize
contaminants uptake. PGPRs with stress ameliorating
capabilities can be used for reclamation of wastelands such
as arid, acidic or alkaline soils so as to enhance food
production in an ecofriendly manner leading to food security
for the future.
Acknowledgements
Thanks are due to Council of Science and Technology,
Lucknow, India. Authors are grateful to Vice Chancellor,

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Climate Change and Environmental Sustainability (October 2013) 1(2): 0-0
BBA University, Lucknow, India for their support and
facilities.
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