Resources, Environment and Sustainability 5 (2021) 100032

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Resources, Environment and Sustainability

journal homepage: www.elsevier.com/locate/resenv

A review on drought stress in plants: Implications, mitigation and the role of

plant growth promoting rhizobacteria
Ojasvini Ahluwalia a , Poonam C. Singh b , Ranjana Bhatia a ,∗
a Department of Biotechnology, University Institute of Engineering and Technology, Panjab University, Chandigarh 160014, India
b
Division of Plant-Microbe Interactions, CSIR-National Botanical Research Institute, Rana Pratap Marg, Lucknow 226 001, India

ARTICLE INFO ABSTRACT

Keywords: Increasing population and subsequent food requirement puts a lot of onus on agriculture worldwide. However,
Abiotic stress agricultural output is constantly influenced by several factors such as small land holdings, lack of proper
Drought mechanization, and occurrence of several abiotic and biotic stresses. Drought stress is one such abiotic
Plant growth-promoting rhizobacteria
stress which causes major setbacks to agricultural productivity every year. Water scarcity due to decline in
Drought tolerance
rainfall and increased frequency of dry spells give rise to drought conditions. Often drought is accompanied
Plant responses
by other detrimental effects like salinity, heat and attack of pathogens. In response plants undergo several
physiological and morphological modifications like reduced transpiration and photosynthesis rate, osmotic
adjustments, repressed root and shoot growth, overproduction of reactive oxygen species (ROS), modified
stress signalling pathways, and senescence. These modifications can cause permanent injury to the plant
and hence there is a need to develop mitigation strategies. Employment of nanoparticles, film farming, use
of drought resistant plant varieties, super-absorbent hydrogels, and biochar are some techniques used to
ameliorate drought stress. Though, most of these practices are labour-intensive and expensive with limited
benefits. Application of plant-growth-promoting rhizobacteria (PGPR), however, is proving to be a preferential
strategy that encompasses many direct and indirect benefits. PGPRs impart induced systemic tolerance (IST)
to plants towards drought stress through a variety of mechanisms like improvement of antioxidant system,
production of ACC-deaminase and phytohormones, nitrogen fixation, phosphate solubilization, siderophore and
exopolysaccharides production, enhanced root and shoot system, amplified photosynthesis rates and carotenoid
production. The commercial applicability of PGPRs as biostimulants will still be dependent on the selection
and performance of robust strains in various environmental conditions.

Contents

1. Introduction ...................................................................................................................................................................................................... 2
2. Plant responses to drought stress......................................................................................................................................................................... 2
3. Stress concurrence ............................................................................................................................................................................................. 2
3.1. Drought and salinity ............................................................................................................................................................................... 2
3.2. Drought and heat stress .......................................................................................................................................................................... 3
3.3. Drought and pathogens ........................................................................................................................................................................... 4
4. Methods to overcome drought stress.................................................................................................................................................................... 5
4.1. Film farming, soilless farming technique .................................................................................................................................................. 5
4.2. Drought-resistant plant varieties .............................................................................................................................................................. 5
4.3. Drought tolerance via nanoparticles ......................................................................................................................................................... 5
4.4. Superabsorbent hydrogel as soil alteration strategy for drought tolerance ................................................................................................... 6
4.5. Drought regulation by the application of biochar ...................................................................................................................................... 6
4.6. Plant growth promoting rhizobacteria mediated drought tolerance ............................................................................................................. 7
5. Impact of PGPRs on physiological processes of a plant.......................................................................................................................................... 7
5.1. Root system ........................................................................................................................................................................................... 7
5.2. Shoot system.......................................................................................................................................................................................... 7
5.3. Relative water content ............................................................................................................................................................................ 7

∗ Corresponding author.
E-mail address: ranjanabhatia20@gmail.com (R. Bhatia).

https://doi.org/10.1016/j.resenv.2021.100032
Received 30 December 2020; Received in revised form 2 July 2021; Accepted 26 July 2021
Available online 11 August 2021
2666-9161/© 2021 The Author(s). Published by Elsevier B.V. on behalf of Lishui Institute of Ecology and Environment, Nanjing University. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
O. Ahluwalia, P.C. Singh and R. Bhatia Resources, Environment and Sustainability 5 (2021) 100032

5.4. Antioxidant metabolism .......................................................................................................................................................................... 8

5.5. Osmotic adjustment ................................................................................................................................................................................ 9
5.6. Exopolysaccharide production ................................................................................................................................................................. 9
5.7. Ethylene and ACC deaminase .................................................................................................................................................................. 9
5.8. Rate of photosynthesis ............................................................................................................................................................................ 9
5.9. Carotenoid production ............................................................................................................................................................................ 10
6. Future prospects and challenges .......................................................................................................................................................................... 10
7. Conclusion ........................................................................................................................................................................................................ 10
Declaration of competing interest ........................................................................................................................................................................ 11
References......................................................................................................................................................................................................... 11

River Basin, Spain, led to a financial impact of approximately 0.57

1. Introduction
It is speculated that by the year 2050 world population will be more
than 9.7 billion, with more than 65% individuals depending solely on
agriculture for their livelihood. This percentage is likely to go up to
90% in developing countries (Castañeda et al., 2016). As a result, not
only is a nation’s economy but also the food supply going to largely
depend on agriculture. However, agricultural practices encounter many
problems such as inaccessibility of an adequate irrigation system, small
and fragmented landholdings, unavailability of good quality seeds,
lack of proper mechanization and over usage of chemical fertilizers
and pesticides. All these lead to unfit soils, soil erosion and natural
calamities (Dev, 2012).
Besides the above hurdles, different crops face different kinds of
biotic and abiotic stress. Biotic stress is any stress caused by living
organisms like insects, viruses, bacteria, fungi, and arachnids. The
plant never develops an adaptive immunity against biotic stress even
on repeated exposures. It is due to this reason that biotic stress is
the major factor of pre-and post-harvest losses (Singla and Krattinger,
2016). Abiotic stress includes conditions such as drought, temperature
fluctuations, high soil salinity, metal toxicity, and oxidative stresses.
These stresses can cause permanent damage to a plant such as stunted
growth, hampered metabolism, reduced yield, and change in genetic
behaviour, leading to mutations in the progeny (Zaidi et al., 2014; Bhat
et al., 2020).
Drought is a major problem faced by farmers every year. It is a
natural phenomenon that is triggered and sustained over an extended
period by the inadequate availability of freshwater for the needs of
humans and the ecosystem (Balint et al., 2013). Drought is difficult to
monitor, recurring in nature and is usually not limited to a specific re-
gion or time period (Salehi-Lisar and Bakhshayeshan-Agdam, 2016). It
is a multidimensional stress which occurs mainly due to depreciation in
rainfall and a consequent dry spell (Gogoi and Tripathi, 2019). Drought
is classified into four distinct categories: meteorological drought that
occurs in areas of dry weather; hydrological drought happens in situa-
tions of low and scarce water supply, especially in surface and ground
water levels and is encountered after several months of meteorological
drought; agricultural drought is often associated with decreased soil
water levels and consequent crop failures, severely affecting food pro-
duction all over the world; and the socio-economic drought that relates
to failure of supply and demand of various commodities due to drought
(Heim, 2002).
Besides affecting food production, drought reduces the underground
water levels, deteriorates water quality, increases soil erosion, and can
eventually result in other calamities like fire, floods and spread of
diseases. According to the United Nations World Water Development
report 2018, an estimated 55 million people are affected worldwide
due to drought and about 700 million people are at risk of being
displaced by 2030 because of it (WWAP, 2018). The socio-economic
impact of drought also leads to massive monetary losses. For example,
agricultural losses in the long California drought were approximately
3.8 billion dollars, with 1.7 billion dollars as crop revenue losses in
2014–2016 (Howitt et al., 2015). Similarly, the 2005 drought of Ebro
billion dollars (Juana et al., 2014).
The effect of drought and the losses incurred are long term. The
expense of groundwater pumping keeps increasing (Lund et al., 2018),
there is decreasing rainfall every year affecting the rain fed agricultural
areas, occurrence of inter-seasonal dry spells and moisture scarcity as
a result of which formation of drought-like conditions is inevitable
(Kaushik, 2015). In India alone, out of the 159.7 million hectares of
agricultural land (Himani, 2014), 42% is under drought (Gogoi and
Tripathi, 2019). Therefore, it becomes vital to make a paradigm shift
towards sustainable agriculture and find solutions to issues related to
water scarcity and its impact on food security (Kaushal, 2019). It is
imperative to devise methods that can enhance the endurance levels of
a plant to drought stress, allowing improved growth and production
of crops in order to satisfy the ever-increasing food requirement in
conditions of limited water availability.
2. Plant responses to drought stress
To withstand drought, plants use different stress coping mecha-
nisms such as synthesis of reactive oxygen species, production of stress
hormones like ethylene and abscisic acid and changes in root and
shoot morphology (Etesami et al., 2015; Chiappero et al., 2019; Bhat
et al., 2021). These mechanisms result in short-term and long-term
responses in plants. Short term responses usually occur when the period
of stress is very small. Some short-term responses include decreased
carbon assimilation, stomatal closure, osmotic adjustment, inhibition of
growth, hydraulic changes, signal transport and cell-drought signalling.
These responses usually do not cause much damage to plants, provided
that normal conditions return soon. Long periods of stress lead to more
dangerous and permanent injuries and even the death of plants. Long
term responses include repressed shoot growth, metabolic adaptations,
limited transpiration area, kernel abortion and senescence (Kaur and
Asthir, 2017). Table 1 illustrates various plant responses to drought
stress and their consequent effects.
3. Stress concurrence
Drought usually occurs concurrently with other stresses like salin-
ity, metal toxicity, unfavourable temperatures, pathogens, or nutrient
deficiency in the environment. Such concurrences are more deleterious
than drought occurring alone and may lead to great agricultural dam-
age. For example, between 1980 to 2012, simultaneous occurrence of
drought and heat stress caused a loss of approximately 200 billion dol-
lars, whereas drought individually caused a damage of 50 billion dollars
to agriculture in the USA for the same period (Suzuki et al., 2014).
Fig. 1 depicts various abiotic stresses which can occur simultaneously
with drought and their effects are detailed below:
3.1. Drought and salinity
Salinity and drought exhibit a great degree of similarity in their
physiological, biochemical, molecular, and genetic effects (Attia et al.,
2020). In regions of high salinity, occurrence of drought is fairly
frequent because as the soluble solute levels increase, water uptake

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O. Ahluwalia, P.C. Singh and R. Bhatia Resources, Environment and Sustainability 5 (2021) 100032

Table 1
Drought tolerance mechanisms of plants, their effects, and responses.
Secondary Primary mechanism Positive effects Negative effects References
mechanism
Oxidative Production of Reactive oxygen species act as ∙ Decreased rate of photosynthesis Sharma et al. (2012);
adjustment reactive oxygen secondary messengers during stresses ∙ Lipid peroxidation Chiappero et al. (2019)
species like drought, salinity, pathogenic ∙ Protein mutations, peptide chain
attack fragmentation
∙ DNA oxidation, strand breakage, mismatch
mutations
∙ Cell death
Decreased Stomatal closure Prevention of water loss due to ∙ Reduced CO2 and nutrient uptake, Ngumbi and Kloepper
transpiration and transpiration from stomata of stems decreased photosynthesis (2016); Liu et al. (2019)
stomatal and leaves ∙ Adaptations like leaf shedding, permanent
conductance wilting of leaves
∙ Sclerophylly — hardening of leaves
∙ Permanent changes in chlorophyll and
mesophyll content of germinating seeds

Modified root and Increased uptake of Thinning of roots, short shoot growth ∙ Stunted shoot growth Etesami et al. (2015);
shoot system water through roots, for prevention of water loss through ∙ Cell damage, degradation of amyloplasts in Barnawal et al. (2019)
decreased transpiration columella cells of plant roots, hydrotropism
transpiration rate ∙ Decreased plant yield
through shoots
Osmotic adjustment Accumulation of ∙ Protection of plants by cellular ∙ Ineffective osmotic adjustment under Etesami et al. (2015);
inorganic cations osmotic adjustment conditions of rapid desiccation Vurukonda et al. (2016)
and anions, organic ∙ Detoxification of reactive oxygen ∙ Water loss
acids, species ∙ Genotype dependent solute accumulation
carbohydrates, ∙ Protection of cell membrane
amino acids, and integrity
sugars ∙ Enzymes or proteins stabilization
Production of stress Produced by the Abscisic acid: ∙ Seed dormancy Daszkowska-Golec (2016)
hormones, abscisic plant’s stress ∙ Altered root architecture to prevent ∙ Inhibition of stimulatory activity of some
acid and ethylene signalling system water loss through transpiration, phytohormones
increased water influx into roots ∙ Inhibition of shoot growth by inhibition of
∙ Increased root to shoot ratio cell division in the vascular cambium
∙ Leaf senescence
∙ Stomatal closing to prevent water
loss
∙ Increased adaptivity of the plants
Ethylene: ∙ Over accumulation of ethylene in leaves, Iqbal et al. (2017);
∙ Reduced water loss due to increased leaf abscission, decreased stomatal Ngumbi and Kloepper
transpiration conductance (2016);
∙ Stimulation of fruit ripening, ∙ Decreased growth of the root and shoot Danish et al. (2020)
regulation of nodulation system
∙ Altered leaf senescence behaviour ∙ Increased epinasty
∙ Inhibition of germination
∙ Long-term hypoxia in root system
∙ Cell damage, cell death
∙ Decreased plant yield

becomes limited owing to a decrease in water potential, initiating
drought conditions (Lee et al., 2004). Prompting of the antioxidant de-
fence system, phytohormone production, osmotic adjustment, decline
in transpiration, growth and photosynthesis rates, carbon assimilation,
leaf wilting, and siderophore production are some plant responses to
combat drought and salinity stress (de Oliveira et al., 2013).
These responses have deleterious effects on plant growth and de-
velopment. For example, under severe drought conditions, a plant’s
response is root elongation in order to reach deeper levels of ground-
water (Sahin et al., 2018). However, under simultaneous conditions of
salinity, thicker roots accumulate more ions like Na+ and Cl− which in
turn affects photosynthesis and chlorophyll synthesis (Lee et al., 2004).
Drought and salinity also often lead to cellular dehydration, decrease
in water potential resulting in reduced cell growth, shoot growth,
hampered cell expansion and cell wall synthesis, and salt deposition
around stomatal openings causing their malfunction (Ahmed et al.,
2015b). Barley plants when subjected to salinity and drought stress
combination showed decreased root and shoot length, and fresh and
dry weight (Ahmed et al., 2013). Vysotskaya et al. (2010) postulated
that while encountering high salt concentrations, plants sequester more
NaCl in the leaf, lowering its osmotic potential and reducing the root
hydraulic conductance, therefore triggering drought conditions in the
leaf tissue. Overproduction of reactive oxygen species (ROS), caused
by decrease in CO2 assimilation rates and excessive light absorption
is another common occurrence under these conditions, causing lipid
peroxidation, DNA mutation, and cell damage (Flexas et al., 2007;
Kumar et al., 2019).
Hence, drought and salinity conditions can severely affect the over-
all growth and yield of plants, increase leaf and flower abscission,
and frequent senescence and cell necrosis (Ahmed et al., 2015b; Sahin
et al., 2018). Climate models and soil-based studies have shown highly
frequent occurrences of such abiotic stress combinations in the future.
Therefore, it becomes imperative to understand these stresses, mimic
field conditions in laboratories and device techniques to mitigate their
effects.
3.2. Drought and heat stress
Drought and heat stress are simultaneously prevalent in semi-arid
or drought-stricken areas and have been extensively studied. Still, very
little is known about their combined effect on plants (Zhao et al., 2017;
Lamaoui et al., 2018). Rate of photosynthesis is a physiological re-
sponse of a plant under stress conditions that is influenced by stomatal

3
O. Ahluwalia, P.C. Singh and R. Bhatia
Fig. 1. Combined effects of different stress conditions on plants.
restrictions such as insufficient CO2 availability, as well as non-stomatal
restrictions like decreased electron transport capacity and RuBisCO
activity. However, concurrence of drought and heat stress can lead
to impairment of Photosystem II, reduced RuBisCO activity, increased
leaf temperature, reduced stomatal conductance and diminished con-
centrations of photosynthetic pigments. Raja et al. (2020) reported
that the chlorophyll and carotenoid concentrations decreased by 80%
and 57% respectively in tomato plants under the influence of both
drought and heat stress. Drought and heat stress together also affect
pistil and pollen development, ovule functions and grain weight (Prasad
et al., 2011). Apart from this, there is overproduction of ROS resulting
in denaturation of proteins and lipid peroxidation, reduced nutrient
uptake, impairment of membrane structure and hampered plant growth
and yield. Drought and heat stressed maize plants showed significantly
increased levels of ROS and malondialdehyde, declined activities of
antioxidant enzymes like catalase and ascorbate peroxidase, reduced
nutrient uptake, shortened root and shoot length and decreased grain
and kernel yield (Hussain et al., 2019).
A plant’s response to co-occurrence of drought and heat stress is
further complexed by its prioritization for the more serious stress. For
example, under drought conditions, stomata are closed prematurely
by the plant to prevent water loss, while under heat stress there
is increased stomatal conductance to cool down the temperature of
leaves through transpiration (Rizhsky et al., 2004). Rizhsky et al.
(2002) demonstrated that tobacco plants when subjected concurrently
to drought and heat stress, exhibited higher leaf temperature in com-
parison to plants subjected to heat stress alone due to the precedence of
stomatal closure to reduce water loss over the need to cool the leaves
by keeping them open. Similarly, accumulation of osmo-protectants
is different under drought stress where proline is one of the major
osmoprotectants that aggregates in plants, whereas no accumulation
of proline is reported under heat stress conditions. Moreover, under
conditions of combined stress, proline accumulation is found to be
toxic and sucrose is the main osmoprotectant that accumulates (Mittler,
2006; Cohen et al., 2020).
Therefore, drought and heat stress impact the plants adversely in
several ways. However, there is still a need to fully understand their
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Resources, Environment and Sustainability 5 (2021) 100032
combined impact. Studies on the plant’s assimilate partitioning and
phenotypic plasticity would improve the understanding to subsequently
achieve improved yield and grain quality of the crop and overall
tolerance of the plant under prolonged stress conditions (Lamaoui et al.,
2018; Cohen et al., 2020).
3.3. Drought and pathogens
Plant’s response to the co-occurrence of drought and pathogen
stress has been widely studied. These responses depend on plant type,
developmental stage, severity, duration of each stress and the effect of
both stresses at the cellular level (Mittler, 2006).
Effects of drought and pathogen infection may result as a conse-
quence of each other and can either be additive or antagonistic (Carter
et al., 2009; Ramegowda et al., 2013). Their combinatorial effects on
roots are extensive. Reduced length of roots, root rot disease develop-
ment, reduced fresh weight of roots, number of root hair and magnitude
of branching, hormonal imbalance, impaired cell division and root
decay are some of the effects of drought and pathogen stress seen on
plants (Sharma and Pande, 2013; Zhan et al., 2015). Water potential of
plants is usually an indicator of soil moisture levels and its maintenance
is very important for proper functioning of the plant vascular system.
During drought stress, the plant’s primary response is the closure of
stomata to prevent water loss due to transpiration. However, in cases
of pathogen infection, this response is interrupted (Pandey et al., 2015;
Choudhary et al., 2016). Leaf rust-causing Uromyces phaseoli releases
toxins that cause malfunctioning of stomata in plants like Phaseolus
vulgaris resulting in compromised drought tolerance (Duniway and
Durbin, 1971). Under mild drought conditions, the basal defence of
a plant is activated which defends it against pathogenic infection.
Although, under severe drought conditions the pathogenic infection
can be aggravated due to release of cellular nutrients into the apoplast
(Mayek-Perez et al., 2002; Ramegowda et al., 2014; Gupta et al., 2020).
Susceptibility of plants to drought and pathogen infection may be
due to their incapability to modify tolerance mechanisms and inten-
sification of the damage caused by any of the stresses. Lastochkina
et al. (2020) reported that exposure of wheat to drought stress and
O. Ahluwalia, P.C. Singh and R. Bhatia
fungal pathogen, Fusarium culmorum, the causal agent of common root
rot and seedling blight, resulted in higher malondialdehyde content,
increased leaf yellowing, decreased root and shoot growth, and decline
of biomass accumulation in comparison to individual stress. In other
cases, drought-stressed plants showed resistance to certain pathogens
that required consistently moist or humid environmental conditions.
Under drought stress conditions, N. benthamiana plants showed fewer
disease symptoms upon infection with the fungal pathogen, Sclerotinia
sclerotiorum (causal agent of white mould) as opposed to pathogen-
infected well-watered plants (Ramegowda et al., 2013).
Present-day studies largely reflect limited plant responses to both
drought and pathogen infection, whether they are concurrent or occur
singly. However, combined stress responses are complex, therefore, fur-
ther studies like simulation modelling and transcriptomic investigations
will be able to make intricate predictions about the onset of pathogen
infection during drought stress conditions and understand the impact
of both drought and pathogen stress over a large spectrum of soil types
and pathogens, so as to develop techniques to mitigate their effects
(Jones et al., 2019; Vemanna et al., 2019).
4. Methods to overcome drought stress
Periodic recurrence of drought has made it important to devise
techniques that can be employed to ameliorate its stress. Over the years,
research has focused on areas of sustainable agriculture to combat plant
stress and convert wastelands to arable grounds. Some recent meth-
ods to ameliorate drought stress include film farming (Mori, 2013),
development of drought-resistant crops (Nuccio et al., 2018), drought
tolerance by the use of nanoparticles (Saxena et al., 2016), use of super-
absorbent hydrogels and biochar (Saha et al., 2020; Zhang et al., 2020),
and employment of plant growth-promoting rhizobacteria (Chiappero
et al., 2019).
4.1. Film farming, soilless farming technique
Film farming is a technique that involves the use of hydrogel films
to grow plants. The hydrogel is a 3-dimensional polymer, a thin layer
of film with 60 cm width, and 0.06 mm thickness that can entrap
large volumes of water in its intermolecular spaces (Batista et al.,
2019). This technique involves the use of a drip irrigation system and
a greenhouse setup. The drip system is laid above and beneath the
hydro-membrane to evenly supply nutrients and water to plants above
the hydro-membrane. The system is equipped with a control device to
keep a check on the amount of water dispersed through the tubes (Mori,
2015; Zhang et al., 2021). It is reported that the roots of plants become
extremely thin to penetrate through the minute pores of the hydrogel
to reach the drip system under the film. As the plants take up water
under high pressure, they can absorb nutrients of high quality (Zhang
et al., 2021).
Film farming requires negligible amounts of soil, water, fertilizers,
and energy. Yields are high and crops are rich in nutrients. A large num-
ber of crops can be grown even in deserts and concrete by implementing
this method (Mori, 2013). Still, this technique is not used popularly
because it is very time consuming, labour-intensive, uneconomical,
requires huge hectares of land, cannot be practised by small farmers,
and requires a greenhouse set up (Sardare and Admane, 2013).
4.2. Drought-resistant plant varieties
Plants employ various physiological and morphological strategies
such as osmotic adjustment, phytohormone production, reduction in
transpiration rates, exopolysaccharide production to combat drought
stress (Sahoo et al., 2013). Through gene discovery and manipula-
tion, hundreds of quantitative trait loci (QTLs) have been identi-
fied and mapped as a result of which functions of many proteins
and transcriptional factors or precursors of enzymes involved in sig-
nalling/regulatory pathways can be modified so that they can aid in
5
Resources, Environment and Sustainability 5 (2021) 100032
drought tolerance. Through modifications of such proteins, drought
tolerance outputs like increased production of phytohormones, osmotic
adjustments can be enhanced to a great extent (Hu and Xiong, 2014).
Transgenic plants have reported better productivity and adapta-
tion to abiotic stress (Rastogi Verma, 2013; Fita et al., 2015; Nuccio
et al., 2018). For example, Liang (2016) created a transgenic plant
variety with a controlled expression of abscisic acid (ABA), a plant
stress hormone. The gene NCED3, belonging to the cytochrome P450
CYP707 A family and having a regulatory function towards ABA was
identified and inserted into Arabidopsis thaliana. Insertion of this gene
facilitated the control of over-expression of ABA, hence, regulating
its deleterious effects on plants under drought stress. Lawlor (2012)
developed transgenic tobacco for the production of osmoprotectant
proline and observed enhanced root biomass under water stress. All
such advancements are contributing to the future of transgenic plants.
However, there are several disadvantages to the use of transgenic
plants for combating drought stress. This approach is time consuming,
laborious, and may result in the loss of other beneficial characteristics
of the host’s gene pool. Genetically modified plants also encourage
the use of additional herbicides, can create superweeds, trigger uncon-
trolled population growth of insects and may lead to antibiotic resis-
tance (Key et al., 2008). Moreover, as the biochemical and molecular
basis for drought perception, signal transduction, and stress adaptation
remains unknown to a great extent, genetic manipulation for drought
resistance becomes difficult (Hu and Xiong, 2014). Cross-contamination
is another disadvantage. These plants have similar features as normal
plants and usually follow the same pollination patterns. Under a condi-
tion where the seeds of genetically modified plants are cross-pollinated
with normal plants, the outcome for both fields may become uncertain
(Mathews and Campbell, 2000). Therefore, despite its benefits, this
approach is also not practised extensively.
4.3. Drought tolerance via nanoparticles
Nanoparticles (NPs) possess very specific and diverse physicochem-
ical properties such as high surface area, high reactivity, adjustable
pore size and diverse particle morphology (Saxena et al., 2016). The
use of nanoparticles to combat drought stress is novel and successful.
Nanoparticles of silicon, silver, zinc, titanium dioxide and iron help to
improve photosynthetic rates, decrease malondialdehyde content (an
indicator of lipid damage), increase relative water content, enhance the
root and shoot system, and aid in the overall development and growth
of plants (Ashkavand et al., 2018).
The mechanism of action of nanoparticles to induce drought tol-
erance is complex and remains largely unknown. However, different
studies have reported that nanoparticles regulate aquaporins, the water
channel proteins responsible for water permeability and seed germi-
nation, ensuring improved water and nutrient supply to the germinat-
ing seeds, thus boosting germination rates even under drought stress
conditions (Khodakovskaya et al., 2011; Li et al., 2020).
TiO2 are the most studied nanoparticles. They have the ability
to improve photosynthesis rate by their characteristic photo-catalytic
activity through which a charge transfer occurs between the light-
harvesting complex II and TiO2 NP. Ze et al. (2013) noted that the
ability of TiO2 NPs to improve photosynthesis rate is because the
nanoparticles play an important role in many key processes of pho-
tosynthesis like promotion of light absorption ability of chloroplasts,
regulation of light distribution between photosystems I and II, acceler-
ation of light energy transfer to electric energy, and water and oxygen
generation.
The association between ROS and nanoparticles can also have vary-
ing outcomes. Some studies have found nanoparticles to aggravate the
concentrations of ROS in plants under abiotic stress leading to cytotoxic
effects (Khan et al., 2017). However, when non-toxic concentrations of
nanoparticles are used, they prime the plant to combat abiotic stresses
like drought. NPs also amplify the levels of antioxidant systems by aid-
ing the production of enzymatic and non-enzymatic antioxidants, and
O. Ahluwalia, P.C. Singh and R. Bhatia
in some cases even mimic the role of ROS scavengers (Ashkavand et al.,
2018; Sun et al., 2021; Zaimenko et al., 2014) observed that analcite
NPs improved drought resistance in wheat and corn by significantly
enhancing the accumulation of scavenging enzymes.
Sun et al. (2021) found that application of ZnO NPs in drought-
affected maize plants improved net photosynthesis rate, aided stomatal
movement, increased the water and chlorophyll content, and also
enhanced the activities of enzymes involved in starch and sucrose
biosynthesis and glucose metabolism in the leaves of maize plants.
Jaberzadeh et al. (2013) observed increased photosynthetic rates, ger-
mination rates, better chlorophyll formation, improved regulation of
the activity of enzymes involved in nitrogen metabolism, and an overall
enhancement in the growth and yield of wheat plants under drought
stress after treatment with TiO2 nanoparticles. Zaimenko et al. (2014)
also reported that at low concentrations the analcite nanoparticles
supplement germination and growth of seedlings along with enhanced
activity of key enzymes. Hence, by the treatment of nanoparticles
drought mitigation can be achieved.
Despite these advantages, there are many drawbacks associated
with the use of nanoparticles as a component in sustainable agriculture.
NPs can cause cytotoxic effects on plants they are interacting with.
Martínez-Fernández et al. (2016) reported that NPs adhere to the root
cells causing hydraulic imbalance and dehydration of plants by block-
ing the pores. They also cause a nutrient imbalance and overproduction
of ROS. Different parts of the same plant when exposed to a specific
concentration of NP may exhibit contrasting effects (Rawat et al.,
2018). This proves that the use of nanoparticles is still at a juvenile
stage and to fully comprehend and utilize the advantages and potential
of nanoparticles in the agriculture sector, their interactions with plants
has to be clearly understood at both the cellular and molecular levels
(Ahmad et al., 2020). Moreover, the exact impact of nanoparticles
on the environment is not yet recognized. It may be possible that
their continued usage could lead to long-term adverse effects that
are not identified immediately (Moulick et al., 2020). Therefore, risk
assessment of the application of nanoparticles in agriculture is still
imperative.
4.4. Superabsorbent hydrogel as soil alteration strategy for drought toler-
ance
Apart from depreciation in rainfall and consequent dry spells, fac-
tors like stunted water retention capacity, nutrient and water percola-
tion to deeper layers, and excessive surface runoff are also responsible
for drought conditions to prevail (Geng et al., 2015). Super absorbent
hydrogels (SAHs) are an upcoming strategy that aims to induce drought
tolerance by bringing about modifications in the soil. Hydrogels are
a category of polymers having highly crosslinked 3-D structures that
have the ability to absorb and retain substantial quantities of water and
solute molecules. The materials used to create these hydrogels are non-
toxic, biodegradable, biocompatible and cost effective (Ahmed, 2015;
Saha et al., 2020). Various hydrophilic groups like carboxyl, hydroxyl,
sulphonates, sulphates, and phosphates are joined to the polymeric
backbone and grant the ability to the hydrogel to swell up and retain
extensive amounts of water. SAHs present in the soil absorb water
during periods of rainfall and release it in the consequent dry spell to be
taken up by the plants to survive under drought conditions (Feng et al.,
2014; Tomášková et al., 2020). SAHs when applied to various soils are
found to improve water use efficiency, soil permeability, and reduce the
surface runoff rates and soil erosion frequency. SAHs are also found to
improve the plant’s available water content (Narjary et al., 2012; Yang
et al., 2014).
Ahmed et al. (2015a) reported that the snap bean plants subjected to
drought treatment showed significant enhancement in plant growth and
total yield with the application of SAHs to the soil. Higher chlorophyll
content and soil water potential, and lower dehydration levels were
reported in plants that were grown in treated soil in comparison to
6
Resources, Environment and Sustainability 5 (2021) 100032
control. Overall, SAHs improved the growth and productivity of bean
plants by bringing about positive physiological changes to the soil and
plant.
Regardless of all the advantages of this technique, its commercial-
ization is still in its nascent stages and the technique is limited to the
laboratory. These hydrogels also lose their retention capacity over time
due to multiple drying and wetting cycles as a result of the ageing cost-
effectiveness of the polymer. Some studies also suggest that polymer
networks may bind the absorbed water so firmly that the plant roots
are unable to extract the required amount of water (Yang et al., 2015;
Saha et al., 2020; Tomášková et al., 2020).
4.5. Drought regulation by the application of biochar
Biochar is a carbon-rich substance that is formed by the oxygen-
limited pyrolysis of biomass. The importance of biochar as a plant stress
alleviator has been significantly increased in the past few years because
of its ability to enhance soil fertility, nutrient uptake and growth, and
improve water retention capacity in plants under stress (Semida et al.,
2019; Haider et al., 2020).
Biochar’s application as a soil amendment technique depends on
its physical and chemical composition including the type of feedstock
used, pyrolysis conditions, specific surface area and porosity (Afshar
et al., 2016; Zhang et al., 2020). When incorporated in the soil, biochar
because of its negatively charged surface, high surface area and carbon
sequestration property, significantly impact the soil’s surface area,
porosity, pore-size distribution and water holding capacity, as well as
many other chemical and biological aspects (Durukan et al., 2020;
Zhang et al., 2020). Improved soil fertility greatly enhances plant
growth and establishment in drought conditions. Biochar absorbs and
retains nutrients directly in the soil and plant roots subsequently take
them up, without having to grow deeper into the ground for water
absorption. Studies have reported a notable improvement in the plant’s
photosynthetic rates, xylem water potential, chlorophyll content, phy-
tohormone production, uptake of essential nutrients like N, Si, P, K
and, overall biomass and growth upon the application of biochar (Ali
et al., 2017; Semida et al., 2019). Application of 0.75% biochar on
Phragmites karka, a biofuel plant under drought stress, significantly
enhanced its fresh and dry biomass, root and shoot length, chlorophyll
content and net photosynthesis rate and soil water retention capacity.
Plants under biochar treatment also encountered less oxidative stress
due to increased production of scavenging enzymes and photosystem
II efficiency (Abideen et al., 2019). Haider et al. (2020) reported
improved transpiration rates, relative water content, root and shoot
length, plant biomass and osmotic defence system in water-stressed
maize as compared to control.
Although the application of biochar as a tool to ameliorate drought
stress might seem favourable, the hazards and risks of this technology
are still largely unknown. Some of the known major disadvantages
include unavailability of feedstock, inefficient energy utilization during
the production of biochar, binding and deactivation of nutrients, pres-
ence of herbicides and insecticides, increased pH of the soil, release of
toxic substances and heavy metals into the soil, and destruction of the
natural microbial flora of soil (Hussain et al., 2017; Kuppusamy et al.,
2016; Oni et al., 2019). Also, biochar may not have any significant
benefits on some plants as it has on others. For example, biochar did
not show any significant improvement in leaf weight, photosynthetic
rate, leaf area and plant height in milk thistle, Silybum marianum L.
Gaertn under drought stress (Afshar et al., 2016). Biochar production
is a tedious and expensive process for farmers using crop residues as
feedstock. The technology of biochar requires extensive research to
fully comprehend its effects on the environment.
O. Ahluwalia, P.C. Singh and R. Bhatia
4.6. Plant growth promoting rhizobacteria mediated drought tolerance
Plant growth promoting rhizobacteria (PGPR) are microorganisms
found in the rhizosphere wherein their metabolic activity is fuelled by
the presence of root exudates (Wozńiak and Gałaz˛ka, 2019; Xiong et al.,
2020). The large diversity of PGPRs in the rhizosphere depends on the
physiological conditions of soil and nutrient availability. These PGPRs
confer various growth-promoting benefits to the plant by colonizing
the roots. Chemotaxis, motility, presence of membrane proteins like
lipopolysaccharides and exopolysaccharide, existence appendages like
pili and fimbriae and ability to utilize root exudates are some of
the characteristics that enable root colonization (Kabiraj et al., 2020;
Pathania et al., 2020). PGPRs thrive symbiotically or non-symbiotically
in the rhizosphere. Several of them can enter roots and develop en-
dophytic associations in the stem, leaves and other parts of the plant
(Wozńiak and Gałaz˛ka, 2019; Kabiraj et al., 2020). These bacteria
are mostly beneficial and act as biostimulants by getting directly or
indirectly involved in promoting plant growth and production. Some
examples of PGPRs include Pseudomonas, Bacillus, Rhizobium, Bradyrhi-
zobium, Pantoea, Azospirillum, Acetobacter, Burkholderia (Timmusk et al.,
2014; Chiappero et al., 2019; Pathania et al., 2020).
The most prominent functions of PGPRs involve nitrogen fixation,
phosphate solubilization, acclimation of micronutrients, release of phy-
tohormones, maintenance of soil composition, bioremediation of pol-
luted soil, induced systemic resistance against pests, insects and fungal
pathogens, and mitigation of abiotic stresses like salinity and drought
(Novo et al., 2018; Pathania et al., 2020). The presence of the nitroge-
nase enzyme allows the PGPRs to fix atmospheric nitrogen and make
it available to plants as ammonia and nitrate (Hakim et al., 2021).
Similarly, PGPRs carry out phosphate solubilization via the production
of organic acids which form complexes with phosphate enhancing
its availability to the plant (Kabiraj et al., 2020; Pathania et al.,
2020). PGPRs also boost the availability of micronutrients like iron
by the production of siderophores, which are low molecular weight,
and high-affinity iron chelators (Singh, 2020). Availability of plant
growth hormones such as auxins and gibberellins, control of pathogens
by production of antibiotics, hydrogen cyanide and lytic enzymes, and
bioremediation of soil via production of various degradative enzymes
are also key attractions of PGPRs (Pathania et al., 2020). The impact of
PGPRs on different plants is reviewed in more detail in Pathania et al.
(2020).
Bacteria are known to survive abiotic stress conditions by employ-
ing a variety of physiological mechanisms, including the amassing of
compatible solutes, exopolysaccharide synthesis, antibiotic production,
and spore formation. PGPRs employ similar physical, chemical, and
biological modifications in plants to help them survive and flourish
under stress conditions like drought. Besides, their application is cost-
effective and less laborious (Vurukonda et al., 2016; Etesami and
Maheshwari, 2018). PGPRs, therefore, are capable of providing added
benefits of drought tolerance along with improved plant performance.
Drought sometimes completely changes the morphology of a plant.
With the help of PGPRs, drought tolerance of plants can be improved
to a great extent. PGPRs impact not just one part of the plant, but help
to mitigate drought effects from the plant as a whole. They improve
root and shoot morphology, employ antioxidant mechanisms, increase
water sustainability, produce biofilms to improve water availability to
the plant and produce secondary metabolites to benefit the plants (Lim
and Kim, 2013; Carmen et al., 2016; Kumar et al., 2019; Li et al., 2020).
Fig. 2 depicts the various effects of drought and its mitigation by the
application of PGPRs. Table 2 enumerates some examples of PGPRs
employed in the mitigation of drought stress.
5. Impact of PGPRs on physiological processes of a plant
PGPRs impact a plant experiencing drought conditions in several
ways as elaborated below.
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Resources, Environment and Sustainability 5 (2021) 100032
5.1. Root system
Roots are the first to perceive the upcoming drought conditions
and enact the plant’s primary response by adapting to maximize water
and nutrient uptake. Plants produce phytohormones like gibberellins,
cytokinins, auxins and abscisic acid for their growth and development.
Abiotic stresses like drought cause decrease in the levels of these
phytohormones thereby reducing their impact on plants (Kaushal and
Wani, 2016; Ngumbi and Kloepper, 2016).
PGPRs can balance the levels of plant hormones by synthesizing
and secreting phytohormones thus facilitating an increase in the total
surface area and length of roots, number of root hairs, and the overall
growth of the root system (Vacheron et al., 2013). Plant hormone
indole acetic acid (IAA), is known to assist plant cell growth and tissue
elongation, thus providing a greater root surface area for absorption of
nutrients and water, and coordinates a cellular defence against drought
stress (Etesami et al., 2015). About 80% of the PGPRs can synthe-
size IAA. Armada et al. (2014) reported the effect of B. thuringiensis
on Lavandula dentate plants to ameliorate drought stress conditions
by the production of IAA which enhanced nutrition, physiology, and
metabolic activities of the plant. Like IAA, gibberellins also assist
drought tolerance, seed germination, starch metabolism and cell sig-
nalling. Gibberellins producing P. putida H-2-3 significantly improved
the growth and yield of the drought-stressed soybean plant (Kang et al.,
2014).
Hence, by the production of phytohormones, PGPRs can improve
the architecture of plant root systems, aiding the plant to survive
drought stress.
5.2. Shoot system
Under conditions of moderate drought, the plant maintains its
above-ground growth. But as the drought conditions worsen, gradual
water depletion causes a decrease in shoot growth, whereas the roots
continue to grow. This increases the root/shoot ratio. Although the
decline in shoot growth aids in restricting transpiration rates and
preventing dehydration, it reduces the overall productivity and growth
of the plant (Skirycz and Inzé, 2010; Ngumbi and Kloepper, 2016).
PGPRs release hormones and enzymes such as cytokines, auxins,
gibberellins, ACC deaminase which help the plant to support near-
normal shoot growth rates by carrying out mechanisms like tissue and
cell elongation and by mitigating the detrimental effects of ethylene.
For example, drought-stressed wheat plants when inoculated with plant
growth-promoting Pseudomonas spp. showed remarkably better shoot
length and dry biomass in contrast to uninoculated plants (Tariq et al.,
2020). PGPRs can therefore effectively aid in getting near normal plant
shoot length.
5.3. Relative water content
Relative water content (RWC) is an indicator of the water status
in plants. Leaf relative water content is the relationship between water
supply to leaf tissue and transpiration rates (Lugojan and Ciulca, 2011).
Water plays a major role in all the metabolic processes in a plant cell.
The ability of a plant to recover from stress and its consequent yield
depends on relative water content. A fall in water levels causes the
plant cells to experience decreased turgor pressure, which leads to cell
damage, and overall wilting, and a decrease in the growth of plants.
The high relative water content helps the plant to thwart the reactive
oxygen species and osmotic stresses caused by droughts and potentially
contribute to greater output (Ngumbi and Kloepper, 2016; García et al.,
2017). The hydraulic conductivity of a plant is the rate of water uptake
by the roots and its movement through the stem. Plants under stress
conditions usually experience a decrease in the hydraulic conductivity
which in turn affects the relative water content.
O. Ahluwalia, P.C. Singh and R. Bhatia Resources, Environment and Sustainability 5 (2021) 100032

Table 2
Different plant growth promoting rhizobacteria employed for the mitigation of drought stress.
PGPR
Pseudomonas putida
Azospirillum sp.
Bacillus cereus, Bacillus subtilis,
Serratia sp.
Phyllobacterium brassicacearum
Pseudomonas aeruginosa
Achromobacter xylosoxidans,
Pseudomonas oryzihabitans,
Variovorax paradoxus
Pseudomonas spp., Enterobacter
spp., Bacillus sporothernoduran
Azospirillium spp.
Pseudomonas fluorescens
Variovorax paradoxus,
consortia of Pseudomonas spp.
Bacillus spp.
Pseudomonas azotoformans
Plant under drought stress Effects of PGPRs References
Maize Increased concentrations of proline leading to Sandhya et al. (2010)
improved relative water content, biomass, and
decreased reactive oxygen species
Wheat Indole acetic acid (IAA) boosted lateral root formation Arzanesh et al. (2011)
and growth, improved water and nutrient uptake
Cucumber plant Reduced malondialdehyde content and wilting Wang et al. (2012)
resulting from production of scavenging enzymes,
higher chlorophyll content, enhanced root morphology
Oilseed rape Increased abscisic acid content resulting in enhanced Bresson et al. (2013)
antioxidant metabolism
Mung Bean Increased root and shoot length, and relative water Kang et al. (2014)
content, up-regulation of abiotic stress genes
Potato Increased production of ACC-deaminase and auxin, Belimov et al. (2015)
decreased ethylene concentrations and improved root
biomass and tuber yield
Sunflower Siderophore production, improved chlorophyll content, Pourbabaee et al. (2016)
plant biomass and availability of nutrients like
nitrogen, iron
Maize Increased proline content, enhanced shoot dry weight, García et al. (2017)
improved seedling growth and germination rates
Foxtail millet Enhanced seed germination rates, improved root Niu et al. (2018)
adhering soil to root tissue dry mass ratio.
Wheat Improved foliar nutrient concentrations, root and Chandra et al. (2019)
shoot length, antioxidant properties and overall plant
biomass
Maize Decreased ascorbate peroxidase and glutathione Silva et al. (2020)
reductase activities, enhanced proline content,
improved nutrient uptake
Wheat Improved seed germination rate, root length and Ansari et al. (2021)
shoot length

Fig. 2. Effects of drought on plants and its mitigation by PGPRs.

PGPRs have the potential to regulate the water content by altering
the hydraulic conductivity and stomatal openings (Zheng et al., 2018).
The exact mechanism of this process is still unknown. However, it is
speculated that by the exogenic production of osmoprotectants like
proline and phytohormones like indole acetic acid, PGPRs can aid
in increasing the relative water content of the plant. For example,
Pseudomonas azotoformans treated wheat plants, under drought stress
conditions, showed a 16% increase in relative water content in contrast
to untreated plants (Ansari et al., 2021). Therefore, measurements of
relative water content are important to examine the extent of drought
stress. PGPRs positively affect the relative water content of plants.
5.4. Antioxidant metabolism
Reactive oxygen species are the inevitable consequence of a plant’s
response to drought stress. During drought stress, the primary response
of a plant is the closure of stomata to limit the water loss through
transpiration (Sharma et al., 2012; Wang et al., 2012). As a con-
sequence of the premature closure of stomata, photosynthesis rates
decrease because of the low concentration of CO2 in the leaves. These
low levels, in turn, affect the reactions of the Calvin cycle, causing a
lower consumption of NADPH and ATP. Accordingly, the regeneration
of electron acceptors also decreases, prompting excessive production of
ROS (Chiappero et al., 2019).
Reactive oxygen species like hydrogen peroxide (H2 O2 ), singlet
oxygen (1 O2 ), superoxide radicals (O2− ), and the hydroxyl radical
(OH), when present in small quantities in the plant act as secondary
messengers. But when their quantity increases, the effects of ROS be-
come deleterious. Lipid peroxidation, fragmentation of peptide chains,
deoxyribose oxidation, strand breakage, removal of nucleotides, and
cell death, are a few effects of over-accumulation of ROS (de Car-
valho, 2008; Miller et al., 2010; Sharma et al., 2012). Malondialdehyde
(MDA), a hydrocarbon, is the ultimate product of lipid peroxidation
and is often interpreted as a sign of cellular damage. It is also used

8
O. Ahluwalia, P.C. Singh and R. Bhatia
to estimate a plant’s tolerance to drought stress (Miao et al., 2010;
Chiappero et al., 2019; Kumar et al., 2019).
To reduce this over accumulation, plants possess non-oxidative
and oxidative enzymes called the scavenging enzymes. These include
superoxide dismutase, ascorbate peroxide, catalase, glutathione re-
ductase, and peroxidase. These enzymes mitigate the effects of over-
accumulation of ROS by oxidation, reduction, and dismutation of
O2 to H2 O2 . However, under abiotic stress conditions like drought,
the activity of these enzymes is altered and reduced, thus making
them unable to carry out the ROS regulatory functions (Etesami and
Maheshwari, 2018; Chiappero et al., 2019).
PGPRs increase the concentration and activity of these enzymes,
hence reducing the accumulation of ROS (de Carvalho, 2008; Tim-
musk et al., 2014). For example, a notable increase was reported in
several scavenging enzymes, including ascorbate peroxide, superoxide
dismutase, and catalase, in which the specific activity of catalase was
up to 1.8 times higher under drought-stressed PGPR-treated plants in
comparison to the non-treated plants. It was suggested that because
of the increase in concentration of ROS-scavenging enzymes, PGPR-
treated potato plants were able to tolerate drought stress (Gururani
et al., 2013). Batool et al. (2020) showed that B. subtilis improved
the activity of catalase by 68%, superoxide dismutase by 63%, and
peroxidase by 51% in potato plants under severe drought stress. Hence,
it can be understood that PGPRs can palliate oxidative damage in plants
under drought stress by interfering with the regulation of antioxidant
defence.
5.5. Osmotic adjustment
Osmotic adjustment is an adaptive mechanism used by plant cells
to increase tolerance towards drought stress. It can be carried out in
two ways: osmoregulation and osmo-protection. Osmo-regulation is the
maintenance of cell turgor by decreasing the osmotic potential through
the accumulation of solutes. Osmo-protection works either by strength-
ening the antioxidant defence system or assisting in ion homeostasis
(Zivcak et al., 2016; Barnawal et al., 2019). Ion homeostasis involves
the accumulation of various osmoprotectants like proline, trehalose,
and glycine betaine, sugars and polyamines to help maintain cell turgid-
ity and normal cellular character. Drought affects the inherent ability
of a plant to produce these osmoprotectants, thus interfering with the
osmotic adjustment mechanism.
Proline is one of the major osmoprotectants. It has a variety of
roles like maintaining cell turgor, stabilizing sub-cellular structures like
proteins, enzymes, cell membranes and lipids and acting as a cytosolic
pH buffer. Proline also acts as a source of organic carbon, nitrogen,
and energy during the stress recovery stage, thereby increasing the
overall growth of the plant (Gusain et al., 2015; Zivcak et al., 2016;
Barnawal et al., 2019). Due to drought stress, intake of nitric acid and
its transport to leaves is reduced, as a consequence of which proline
synthesis decreases (Ngumbi and Kloepper, 2016; Iqbal et al., 2017;
Etesami and Maheshwari, 2018).
Plant growth-promoting rhizobacteria also synthesize a significant
number of osmoprotectants. PGPRs increase the concentration of these
osmoprotectants thereby aiding in osmotic adjustment mechanisms.
Streptomyces pactum Act12 was found to improve the growth of PEG-
induced drought-stressed wheat plants. Increased levels of proline in
inoculated plants indicated improved tolerance of a plant towards
water stress (Li et al., 2020). Sandhya et al. (2010) reported that by
the accumulation of proline, Pseudomonas putida GAP-P45 improved the
relative water content, increased the biomass, and aided in maintaining
cellular water levels in maize plants under drought stress. Conse-
quently, it can be perceived that the accumulation of osmoprotectants
enables osmotic adjustment in plants. PGPR aids in the synthesis of such
osmoprotectants, ergo ameliorating drought stress.
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Resources, Environment and Sustainability 5 (2021) 100032
5.6. Exopolysaccharide production
Exopolysaccharides (EPS) are natural polysaccharides secreted by
microorganisms that help the microbes to survive inhospitable condi-
tions like water shortage by retaining large amounts of water. EPS are
involved in various roles such as surface attachment, biofilm formation,
nutrient supply, water retention, plant-microbe interactions, bioreme-
diation, and protection from pathogens and abiotic stresses (Kaushal
and Wani, 2016; Khan and Bano, 2019).
In plants under drought stress, EPS released by PGPRs help in
preventing desiccation by forming hydrophilic biofilms on the root
surface and thus, allowing the water to be released at a slower rate.
They also aid in providing improved soil aggregation, structure and
permeability, and root aggregation. This is possible by the subsequent
release and absorption of EPS on the soil aggregates surface with the
help of mechanisms like cation bridges, Van der Waal forces, anion
adsorption (Sandhya et al., 2009; Vurukonda et al., 2016; Khan and
Bano, 2019).
Inoculation of EPS producing Pseudomonas azotoformans FAP5 con-
tributed towards the production of indole acetic acid, improved growth
and germination rates, enhanced root length, biomass, and drought
tolerance capacity of wheat (Ansari et al., 2021). Seed bacterization of
sunflower with Pseudomonas sp. strain GAP-P45 improved the survival
rates, root adhering soil capacity, germination, and water uptake (Sand-
hya et al., 2010). Therefore, it can be understood that PGPRs produce
polysaccharide chains like exopolysaccharides which play a major role
in drought tolerance thus increasing global food security.
5.7. Ethylene and ACC deaminase
Ethylene is a plant hormone produced under stress conditions like
drought and salinity. Its functions include the ripening of fruit, stress
signalling and gender determination of the plant. However, when
present in high quantities, especially during stress conditions, ethylene
is detrimental to plant growth and survival. Some of the deleterious
effects of ethylene include increased leaf abscission, decreased stomatal
conductance, decreased growth of root and shoot system, epinasty,
long-term hypoxia in the root system, cell damage, and ultimate death
of the plant. 1-aminocyclopropane-1-carboxylic acid (ACC) is the im-
mediate precursor of ethylene (de Poel and Van Der Straeten, 2014;
Saleem et al., 2018; Saikia et al., 2018). ACC is cleaved into ammonia
and alpha-ketobutyrate by the enzyme ACC deaminase to regulate the
endogenous concentrations of ethylene below inhibitory levels (Saikia
et al., 2018; Gupta and Pandey, 2019; Zafar-Ul-Hye et al., 2019).
Drought affected plants inoculated with PGPRs have shown in-
creased root and shoot growth and decreased cell damage due to high
concentrations of IAA and ACC deaminase. For example, inoculation
of drought-stressed maize plants with ACC deaminase producing PGPR
successfully lowered the ethylene levels resulting in improved root
and shoot growth, better nutrient uptake and improved chlorophyll
contents (Danish et al., 2020). ACC deaminase producing PGPRs also
improve nitrogen fixation thereby stimulating nodulation in legume
plants. Belimov et al. (2009) reported that ACC deaminase producing
PGPR strain V. paradoxus 5C-2 increased nitrogen levels in drought-
stricken pea plants and concluded that a decrease in ethylene concen-
tration was responsible for increased nitrogen levels and subsequent
nodulation. Therefore, synthesis of ACC deaminase is a salient strategy
employed by PGPRs to mitigate drought stress in plants and ensure
plant survival and its overall growth and development.
5.8. Rate of photosynthesis
Hindrance to plant growth during drought stress is first brought into
play by decreased growth rate of the assimilatory surfaces followed
by inhibition of photosynthesis. Decreased photosynthesis rates during
drought can be attributed to stomatal as well as non-stomatal factors
O. Ahluwalia, P.C. Singh and R. Bhatia
(Drake et al., 2017; Liu et al., 2019). Stomatal restrictions of photosyn-
thesis may be described as inefficient CO2 assimilation in the leaves
and sub-stomatal cavities due to premature closure of the stomata.
Non-stomatal photosynthesis restrictions arise when there is a decrease
in RuBisCO activity, chloroplast activity, ATP availability, ribulose
1,5-bisphosphate [RuBP] synthesis, leaf nitrogen and impairment of
photosystem I and II (Gaion et al., 2018; Liu et al., 2019). Stomatal
restrictions occur under mild and moderate water stress conditions and
normal photosynthetic rates are achieved by improving the soil water
levels. However, the effect of non-stomatal restrictions is dominant
during conditions of severe drought and the metabolic constraints
imposed by it are not easily relieved, requiring a prolonged recovery
period (Bellasio et al., 2018). Wang et al. (2018) postulated that due to
decreased photosynthesis rates, the light energy absorbed by plants is
not utilized efficiently leading to the overproduction of reactive oxygen
species. ROS hinder the synthesis of D1 protein, which is the core of
photosystem II, downregulating the photosynthetic electron transport
chain and inhibiting CO2 fixation which in turn accelerates the decline
of photosynthesis (Bellasio et al., 2018).
PGPRs improve photosynthesis rates in plants under stress condi-
tions with the production of phytohormone cytokinin. Cytokinin (CK)
influence both the structural and functional characteristics of photo-
synthesis. CKs amplify stomatal conductance and promote cell division
and differentiation in the early stages of leaf development leading to
an increased number of vascular bundles, improved xylem and phloem,
and enhanced number of cells per leaf area (Chernyad’ev, 2000; Hönig
et al., 2018). Okazaki et al. (2009) reported that with the differentiation
of etioplasts and their transformation to chloroplasts, CKs improve
the chloroplast numbers at cellular levels. At the thylakoid membrane
level, increased grana formation, improved synthesis of photosynthetic
pigments such as chlorophyll and carotenoids, regulation of enzymes
of the primary and secondary phase of photosynthesis, and upregula-
tion of genes of photosynthesis are some of the beneficiary effects of
cytokinins (Cortleven and Schmülling, 2015; Talla et al., 2016). Apart
from this CKs implement the regulation of ROS by carrying out their
decomposition, delay the process of senescence by downregulating
the senescence-associated genes and inhibit the activity of senescence
inducing enzymes which hinder the photosynthesis machinery (Hönig
et al., 2018). Cytokinin producing Acinetobacter calcoaceticus X128
when inoculated to Sambucus williamsii Hance plants under drought
stress, showed 11.6% improvement in stomatal conductance, up to 13%
enhancement in photosynthetic rates and also the reversal of degrada-
tion process of chlorophyll (Liu et al., 2019). It can thus be inferred
that PGPRs aid in improving photosynthesis rates by the production of
phytohormones like cytokinin.
5.9. Carotenoid production
Carotenoids are a class of metabolites that are of great importance
to the plant under water deficit conditions. They act as antioxidants
to various forms of ROS and aid the plant in activating its antioxidant
defence mechanism. Carotenoids acts as an antioxidant against singlet
oxygen (1 O2 ) generated by triplet chlorophylls either by carrying out
direct quenching of triplet chlorophyll or through the de-epoxidation
reaction of violaxanthin to zeaxanthin which prevents the formation of
triplet chlorophyll and, in turn, the singlet oxygen species (Ruiz-Sola
and Rodríguez-Concepción, 2012; Uarrota et al., 2018). By acting as
antioxidants, carotenoids strengthen the rigidity of thylakoid and cell
membrane. They are also the precursors of many phytohormones like
abscisic acid and strigolactones. Carotenoids dispel excess energy and
prevent the over-excitation of photosystem II (Brunetti and Guidi, 2015;
Cicevan et al., 2016; Uarrota et al., 2018). Production and regulation of
carotenoids is particularly dependent on the plant species and duration
and intensity of drought stress. For example, rice plants under the
influence of drought stress expressed a 33% decline in the carotenoid
concentration (Nasrin et al., 2020).
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Resources, Environment and Sustainability 5 (2021) 100032
PGPR inoculation to plants under drought stress conditions re-
sulted in increased concentrations of carotenoids. Yasmin et al. (2017)
reported an increase in carotenoid concentration in drought-stressed
maize plants after co-inoculation of Pseudomonas sp. and Bacillus pumilus.
PGPR consortium of Planomicrobium chinense, Bacillus cereus, and sali-
cylic acid also improved the carotenoid contents by 57% in drought
stressed maize plants (Khan et al., 2020).
Notably, carotenoid production is essential for the photosynthetic
machinery of the plant and its concentration is highly affected during
drought stress. However, with the application of PGPRs, the carotenoid
content can be increased tenfold in plants.
6. Future prospects and challenges
In today’s world, as the demand for higher outputs, improved pro-
duction of crops, soil fertility, and sustainable agriculture is increasing,
research is shifting towards rhizo-engineering to fabricate a unique
environment for the interaction of plants and microorganisms. Plant
growth-promoting rhizobacteria are a promising component of rhizo-
engineering and their benefits are numerous and evident (Katiyar et al.,
2016). PGPRs are effective in the mitigation of many abiotic and
biotic stresses. PGPRs are also known to boost the overall growth
and development of plants by employing various mechanisms such
as phytohormone production, antioxidant mechanisms, exopolysaccha-
ride production, ethylene regulation, triggering of induced systemic
resistance.
However, consistency in the performance of PGPRs under field
conditions is still questionable. The basis of this concern is the sub-
standard quality of inocula and the incapability of bacteria to contend
against indigenous populations under disadvantageous conditions. The
inoculated PGPR strains must be rhizosphere adept to compete with in-
digenous populations for the procurement of limited resources, survive
and colonize particular areas of roots. Therefore, high concentrations
of beneficial bacterial strains have to be fed to the soil for agronomical
utility (Nadeem et al., 2016; Kumar et al., 2019). In cases where a
single bacterial strain is not effective in providing stress tolerance,
multi-strain bacterial consortium might be beneficial (Smyth et al.,
2011). Method of inoculation is also important as improper application
can lead to inconsistent and wrong results. Some accurate inoculation
techniques include the use of peat-based inoculants, liquid inoculation,
and seed coating (O’Callaghan, 2016; Katiyar et al., 2016).
The commercial viability of PGPRs depends on the selection and
performance of robust strains in nutritionally deficient soils and chang-
ing weather conditions. It will also depend on the shelf life of PGPRs,
viability of cells, protection against soil environment, convenient use,
and cost-effectiveness. These strains should also be nonpathogenic
and nontoxigenic (Mutturi et al., 2016; Tabassum et al., 2017). Mi-
croencapsulation of PGPRs is a great method to enhance performance,
decrease cost, and improve viability and shelf life (John et al., 2011;
Mutturi et al., 2016). Overall, application of PGPRs is a promising
approach to combat biotic and abiotic stresses and promote sustain-
able agriculture. Its successful commercialization will depend on the
association between agriculturists, microbiologists, biotechnologists,
industrialists, and farmers. Every step taken will be a step towards
sustainable agriculture.
7. Conclusion
Drought severely affects plant productivity and lowers the overall
economic viability of agriculture. Many methodologies have been de-
veloped to challenge drought and each has its advantages as well as
limitations. However, the use of PGPRs is most effective in overcoming
drought conditions besides providing other direct and indirect benefits
to enhance overall plant performance. Application of PGPRs is very eco-
nomical, can be practised on small landholdings, and does not require
huge energy sources. However, the commerciality of PGPRs is highly
O. Ahluwalia, P.C. Singh and R. Bhatia
dependent on the robustness of strain, shelf life of the formulation, and
their economical use. Nonetheless, the promise of the positive impact
of PGPRs on the mitigation of drought cannot be ignored and therefore,
more focus must be given to make them commercially available to
average farmers all around the world.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared to
influence the work reported in this paper.
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