Plant Soil

DOI 10.1007/s11104-016-3007-x

REGULAR ARTICLE

Mechanisms of plant response to salt and drought stress

and their alteration by rhizobacteria
Cinzia Forni & Daiana Duca & Bernard R. Glick

Received: 15 January 2016 / Accepted: 2 August 2016

# Springer International Publishing Switzerland 2016

Abstract Keywords Drought stress . Plant growth-promoting

Background Soil salinity and drought are an enormous bacteria . PGPB . Salt stress
worldwide problem for agriculture, horticulture and sil-
viculture. The initial responses of plants to drought and
salinity are similar; both are attributed to water deficit
Introduction
which inhibits plant growth and development.
Scope In this review, an overview of the major physio-
During their lifetime, plants may face a wide range of
logical and biochemical changes that occur in plants as a
environmental stress conditions, including temperature ex-
consequence of salt and drought stress is presented. In
tremes, drought, salinity, flooding, pollutant toxicity and
addition, the role of beneficial plant growth-promoting
various oxidative stresses, all of which may negatively
bacteria in ameliorating many of the deleterious conse-
affect growth and limit plants from reaching their full
quences of salt and drought stress is discussed. Mecha-
growth potential. Worldwide, these abiotic stresses affect
nisms used by plant growth-promoting bacteria to ame-
both natural settings and yields of many major crops
liorate the effects of these stresses include the produc-
(Mahajan and Tuteja 2005). More recently, climate change
tion of cytokinin, indoleacetic acid, ACC deaminase,
has shown a trend that leads to differences in rainfall
abscisic acid, trehalose, volatile organic compounds,
patterns, temperature extremes, and soil composition chang-
and exopolysaccharides.
Conclusion Given the fundamental understanding of es, including salinization (Verslues et al. 2006). Given the
many of the mechanisms operating in plant-bacterial many environmental challenges facing the agriculture in-
interactions, it is expected that the practical use of ben- dustry, significant genetic improvement of crops (Araus
eficial bacteria in agriculture, horticulture and silvicul- et al. 2008) or the use of plant growth-promoting bacteria
ture will grow dramatically in the coming years. that interact with those crops (Glick 2012) are needed to
maintain or increase crop yields, in the presence of sub-
optimal conditions including drought and high salinity
Responsible Editor: Ian Dodd.
A. The problem of salt and drought stress
C. Forni (*)
Dipartimento di Biologia, Università degli Studi di Roma BTor Drought and soil salinity threaten the sustainability of
Vergata^, Via della Ricerca Scientifica, 00133 Rome, Italy agriculture by negatively impacting plant growth and
e-mail: forni@uniroma2.it crop production (Bray et al. 2000). Therefore, a better
D. Duca : B. R. Glick understanding of the physiological variations in plants
Department of Biology, University of Waterloo, Waterloo, ON caused by stress is required to facilitate the identification
N2L 3G1, Canada of effective tolerance mechanisms.
 Plant Soil

In arid and semi-arid areas, even though irrigation to osmotic stress than root growth, e.g. mild osmotic
helps to increase productivity, the over-exploitation of stress can inhibits the growth of stems and leaves
irrigation schemes, land clearing and some ill-conceived (Nonami and Boyer 1990; Bartels and Sunkar 2005).
agricultural practices often leads to soil salinization. At Reduced leaf size is generally considered to be benefi-
the present time, nearly 20 % of all cultivated and irrigat- cial to plants under water deficit conditions because of a
ed lands (equivalent to 62 million ha) are negatively salt concomitant reduced rate of transpiration, even though
affected with some estimates being as high as 50 % it may impact on the photosynthetic rate. In moderately
(Khan et al. 2015). Soils are classified as saline when dry climates such a strategy is not always as successful
the electrical conductivity of a saturated paste soil extract as expected, due to the direct evaporation from the soil
(ECe) is 4 dS/m or more. This is equivalent to approxi- when it remains partially wet (Tardieu 2005). Many
mately 40 mM NaCl and generates an osmotic pressure mature plants subjected to drought respond by acceler-
of approximately 0.2 MPa (Munns and Tester 2008). ating senescence and abscission of the older leaves
Such an ECe significantly reduces the yield of most (Gepstein and Glick 2013). This process is also known
crops. In saline soils, NaCl is the most prevalent soluble as leaf area adjustment, while the roots continue to
salt, but a range of other dissolved salts, such as Na2SO4, elongate (Sharp et al. 1988). During drought stress,
MgSO4, CaSO4, MgCl2, KCl, and Na2CO3, can also continued root elongation can be explained by the
contribute to salinity stress (Munns and Tester 2008). plant’s need to reach groundwater (Brunner et al.
Besides salinity, frequent occurrences of drought and 2015). In salt stress, heavier roots can accumulate higher
abnormal weather events have lately been observed all amounts of chloride. Moya et al. (1999) determined the
over the world (McNutt 2014). Almost every year, some rate of chloride uptake by detecting this ion depletion in
region of the earth is hit by drought, damaging crops and the media and reported that in Citrus species under
disrupting agricultural production. saline conditions the root chloride uptake is a passive
process. According to the authors the shoot to root ratio
B. Differences and similarities between drought and has a role in modulating chloride uptake in sensitive or
salt stress tolerant species. The authors found differences in the
amount of chloride uptake based on the growth of shoot/
In principle, plants can be divided into those sensitive root ratio that tended to increase (in sensitive species) or
and those tolerant towards abiotic stresses (Dolferus 2014). decrease (in tolerant species) chloride uptake. Root
Unfortunately, the difference between sensitivity and toler- pruning and defoliation showed a dependence of the
ance of a species to these stresses is often difficult to define, uptake on root system size. Leaf biomass was responsi-
however, for crop plants it is usually related to yield. ble of leaf chloride accumulation.
Water deficit induces different responses in plants de- At a cellular level the osmotic stress, caused by salt
pending on three distinct stage of soil dehydration as and drought, leads to different degrees of effects de-
reported by Serraj and Sinclair (2002). Most of the research pending on the severity of the stress applied. Under
on stress tolerance has been performed in laboratory ex- severe stress, cell dehydration is a consequence of water
periments applying severe stress conditions, while the removal from the cytoplasm into the extracellular space,
effect of milder stress has been less comprehensively thereby decreasing cytosolic and vacuolar volumes
studied. In field conditions, plants may be exposed to a (Bartels and Sunkar 2005). These osmotic stresses limit
wide natural variation in stresses that need to be considered plant growth due to photosynthetic decline and result in
to optimize crop performance (Collins et al. 2008). The the production of reactive oxygen species (ROS) that
more severe conditions that have been studied in some lab may damage cell components as described below. An-
experiments have pointed the way towards successful other consequence of osmotic stress involves autopha-
(although still somewhat limited) field experiments (for gy, an intracellular degradation process that delivers
example Saravanakumar and Samiyappan 2007). cytoplasmic constituents to the vacuole (Han et al.
The plant phenological stage, the severity and the 2011); this is considered to be a central component in
length of exposure to the stress play an important role the integrated stress response (Kroemer et al. 2010).
in the growth arrest or in determining the damage caused Under osmotic stress, cytosolic and organelle proteins
by stress. Osmotic stress can be a consequence of either may have reduced activity or even undergo complete
salt or drought. Leaf growth is generally more sensitive denaturation. The ability of autophagy to scavenge
Plant Soil

oxidized proteins and to regulate ROS levels suggests its According to Tavakkoli et al. (2010), plants grown in
probable role in salt and drought stress. Some of the the presence of high NaCl concentrations accumulate
ATG genes (termed AuTophaGy-related genes), in- both Na+ and Cl− simultaneously, although the effects of
volved in the autophagocytosis, such as AtATG8 in the two ions may differ. High Cl− concentrations reduce
Arabidopsis have been reported to function in response the photosynthetic capacity and quantum yield due to
to salt stress (Slavikova et al. 2008). Under normal chlorophyll degradation and impaired photosystem II
growth conditions AtATG8 encoded proteins are assem- efficiency. High Na+ interferes with K+ and Ca2+ nutri-
bled within autophagosome-resembling structure in the tion, affecting stomatal regulation and decreasing pho-
vacuoles, they modulate the effect of cytokinin on root tosynthesis and growth. Significantly, the other major
architecture. Under salt stress the expression of recom- detrimental impacts of drought and salinity on the cel-
binant protein AtAtg8 prevents the inhibition of primary lular energy supply and redox homeostasis are balanced
root growth, the mechanism behind this effect is still by global re-programming of plant primary metabolism
unknown (Slavikova et al. 2008). and altered cellular architecture. Therefore, the physio-
The major factor affecting plant water relations is the logical responses of plants to salinity are often similar to
large difference in the concentration of water vapor other environmental stresses, such as drought (Munns
between the plant’s substomatal pore and the atmo- and Tester 2008) and may share common stress-
sphere, i.e. the driving force for the movement of water tolerance pathways.
through the soil–plant–atmosphere continuum. The flux Severe drought stress removes water from cellular
of water through the plant carries essential nutrients to membranes, disrupting their normal bilayer structure. A
the shoots, but in a saline environment, within the tran- further contribution to the loss of membrane integrity is
spiration stream, any dissolved solutes can also be car- due to the displacement of membrane proteins causing
ried from the soil to the leaves, where they must be changes in selectivity, disruption of cellular compart-
either re-circulated or excreted in order to prevent the mentalization and a loss of activity of membrane pro-
toxicity of some ions. All plants have the ability to teins (Mahajan and Tuteja 2005). Regulation of water
acquire ions that are then compartmentalized in the movement across cellular membranes is controlled by a
vacuoles. Under high salinity, excessive accumulation family of water channel proteins called aquaporins, a
of Na+ and Cl− ions occurs and is detrimental to bio- highly conserved protein family called major intrinsic
chemical processes (Munns and Tester 2008) and inter- protein (MIP) with several homologues in different
feres with nutrient availability as the soil dries. Na+ plants. These proteins facilitate the efficient transport
uptake, transport and compartmentation are crucial for of water molecules, as well as small solutes across the
plant survival in environments with a high NaCl con- plasma membrane and tonoplast (Chrispeels and Maurel
tent, and salt tolerance is also based on appropriate 1994; Khan et al. 2015).
osmotic adjustment that maintains cellular homeostasis.
Two important strategies have been adopted by
plants exposed to the cytotoxicity of Na+, e.g. improv- How do salt and drought stress affect the physiology
ing ion compartmentation via use of a tonoplast Na+/H+ of plants
antiporter and/or increasing active Na + extrusion
through Na+/H+ antiporters located in the plasma mem- Perception of stress, signaling and defense response
brane, and vacuolar ion sequestration (Sun et al. 2009).
The efficiency of these mechanisms confers different To cope with salt and drought stress, as well as other
degrees of salt tolerance in various plant species, from stresses, and to guarantee success in the adaptation to
glycophytes (salt sensitive plants) like rice (Oryza and survival of limiting growth conditions, plants have
sativa), maize (Zea mays), soybean (Glycine max) and developed diverse stress-responsive signaling pathways
beans (Phaseolus vulgaris) to halophytes which can and sophisticated defense mechanisms (Huang et al.
tolerate high salt concentrations (Mahajan and Tuteja 2012). Plants have multiple stress perception and signal
2005). Plant salt tolerance can also be achieved by transduction pathways, which may interact with one
specific regulation of gene expression involving both another at various steps in the pathways. Plants are also
universal and unique changes to the transcriptome as able to display strategic defense responses when two
indicated below. stressors occur at the same time, and this response can
 Plant Soil

be, in some cases, distinctive from the response to either 2013; Sakuraba et al. 2015). TFs and cis-elements func-
individual stress (Koussevitzky et al. 2008). tion in the promoter regions of different stress-related
To economize their molecular resources plants share genes, and the over-expression or suppression of these
stress protective responses, that require tight coordina- genes may improve a plant’s tolerance to both biotic and
tion of multiple signals. abiotic stress. Therefore, TFs and cis-elements are con-
The master regulators of transcription involved in the sidered important targets for the improvement of stress
stress response and their key roles in plant adaptation tolerance in crop species through genetic engineering.
during adverse environmental conditions have been de- During plant development and stress responses another
scribed and reviewed (Balderas-Hernández et al. 2013). significant role is played by the DEAD-box RNA
A small note of caution is relevant here: most of the helicases that in plants are differentially regulated during
studies on stress perception and response have been development and in response to environmental stresses
conducted using Arabidopsis thaliana and these results (Tuteja et al. 2014a, b).
are not always applicable to other plant species, since A class of small non-coding micro RNAs (miRNAs)
the responses also depend on the genotype and devel- regulates gene expression at the post-transcriptional lev-
opmental stage of the plant (for example Moya et al. el; they play important roles in plant growth and devel-
1999; Pandolfi et al. 2010). opment as well as abiotic stress responses in diverse
The stress response depends on both genotypes and species (Jeong and Green 2013; Ferdous et al. 2015).
developmental stages and may exert positive and nega- During abiotic stress, miRNAs may modulate the ex-
tive effects over plants status and growth. The response pression of genes involved in the stress response, as
mechanisms confer different degrees of stress tolerance, demonstrated by the phenotypic analysis of transgenic
which are largely determined by genetic plasticity in plants or mutants, in which the expression of either
tolerant species. A gradual adaptation is required by stress-responsive miRNAs or their target genes was
non-tolerant species for expression of genes responsible modified (Jeong and Green 2013).
for the acquisition of some degree of tolerance (Zhu In plants, osmotic stress-responsive (OR) genes are
2001; Bartels and Sunkar 2005), demonstrating to some normally silent and are activated under stress conditions.
extent the presence of a genetic program for tolerance in Microarray experiments helped to identify several OR
non-tolerant plants. Hundreds of genes have been asso- genes (Kreps et al. 2002; Seki et al. 2002), including
ciated with the abiotic stress response. The latter in- TFs and regulatory sequences in stress-inducible pro-
volves the activation of mechanisms that prepare the moters. The role of OR genes involves the protection of
plant for adaptation via transcriptional modulation that cells from stress by the production of important meta-
is crucial for the plant’s genetic and biochemical net- bolic proteins and the regulation of the downstream
works. It is a multilevel reorganization that often in- genes for signal transduction.
volves massive changes depending on the severity and The majority of salt- and drought-induced genes
duration of one or more stresses (Atkinson and Urwin appear to function in damage limitation or repair, e.g.
2012). Usually the manipulation of such complex mech- late embryogenesis abundant (LEA) protein, osmotin,
anisms are performed mainly considering the agronomic antifreeze proteins, chaperones and ubiquitination-
point of view and trying to avoid other strategies that related enzymes. LEA/dehydrin-type genes help in
might imply a toll in the production. protecting the partner protein from degradation by pro-
The proper regulation of stress-responsive genes is teinases that function to remove denatured and damaged
important for both recognition and response to stress proteins. Protein kinases (such as mitogen activated
conditions. The gene network involved in the signaling, protein kinase, MAPK; calcium dependent protein ki-
responses and governing of diverse physiological func- nase, CDPK; and receptor protein kinase), protein phos-
tions, include various transcription factors (TFs) phatases (phosphoesterases and phospholipase C) and
(Fig. 1). Recent advances in systems biology have fa- proteinases are also involved in the response (Fig. 1)
cilitated the identification of a number of TFs that par- (Yamaguchi-Shinozaki and Shinozaki 2006).
ticipate in regulating defense and modulate adaptive Downstream transduction of the stress signal, detect-
responses (Balderas-Hernández et al. 2013; Deinlein ed by plasma membrane receptors, generates different
et al. 2014; Elfving et al. 2011; Golldack et al. 2011; second messengers including inositol phosphates and
Li et al. 2015; Nakashima et al. 2009; Nuruzzaman et al. oxidative bursts due to over-production of ROS and
Plant Soil

Fig. 1 Overview of salt- and

drought-stress responses in plants.
Salt and drought affect cell
physiology and metabolism and
as consequence reduce plant
growth. Stress signaling is
perceived by the cell and elicits
stress-signaling pathways that
involve transcriptional
remodeling, metabolic changes
and altered hormonal activity.
Bacterial activity may affect the
latter. A positive stress response
leads to plant tolerance of the
stress while a negative response
leads to growth inhibition

calcium (Mahajan and Tuteja 2005). For example, the these genes contribute to plant adaptation and survival
presence of NaCl induces a rapid and transient (Mahajan and Tuteja 2005).
increase of cytosolic calcium, which triggers signal The oxidative bursts, caused by over-production of
transduction pathways that result in diverse cellular ROS, depend on the imbalance between ROS produc-
responses (Bartels and Sunkar 2005). Calcium is tion and ROS scavenging that occurs during stress
an important signaling molecule acting as a second (Miller et al. 2010). Powerful oxidants can react with
messenger, whose intracellular concentration is most cellular components, producing severe damage to
sensed by calcium binding proteins (Tuteja and proteins, lipids and nucleic acids (oxidative stress situ-
Mahajan 2007). These proteins are calmodulin, ations) (Del Rio 2015). Plant cells try to overcome the
CDPKs (calcium-dependent protein kinase) and detrimental effects of increased ROS concentrations
CBLs (calcineurin B-like proteins). These proteins, either by eliciting the production of antioxidant com-
by interacting with their partners, start a phosphor- pounds or by enhancing the activity of enzymes in-
ylation cascade. volved in ROS scavenging or both. Secondary metabo-
The discovery of SOS (Salt Overly Sensitive) genes lites, like phenolics, may play a protective role as anti-
paved the way for elucidation of a pathway linking Ca2+ oxidant molecules in salt and drought stress. Thus,
signaling in response to salt stress (Zhu et al. 1998; Zhu increasing phenolic concentrations has been reported
2002), clearly indicating the fundamental role played by in white clover and an interspecific hybrid of Trifolium
this ion in plant abiotic stress response. The SOS path- exposed to drought (Ballizany et al. 2012; Nichols et al.
way results in the exclusion of excess Na+ ions out of the 2015), and wild genotypes of barley exposed to either
cell via the plasma membrane Na+/H+ antiporter and salt or drought or both stresses (Ahmed et al. 2015).
helps in reinstating cellular ion homeostasis. This path- Anthocyanins are also reported to increase in re-
way has three key components: SOS3, acting as a Ca2+ sponse to salt stress (Parida and Das 2005), while
sensor; SOS2, a serine/threonine protein kinase and their concentration decreases in salt sensitive spe-
SOS1, a plasma membrane Na+/H+ antiporter (Türkan cies (Daneshmand et al. 2010). Moreover, plant
and Demiral 2009). The stress responsive genes repre- tissues containing anthocyanins are more resistant
sent the major target of this reaction. The products of to drought (Chalker-Scott 1999).
 Plant Soil

The enhancement of the activity of enzymes involved et al. 1998; Nawaz and Ashraf 2010), in other cases no
in ROS-scavenging, such as guaiacol peroxidase (G- significant changes in osmolyte concentration was de-
POD), superoxide dismutase (SOD), catalase (CAT), as tected (Di Cori et al. 2013). Therefore, the protective
well as enzymes of the ascorbate-glutathione cycle, such role of osmolytes seems to be species specific and
as ascorbate peroxidase (APX), monodehydroascorbate depends on a number of factors, such as growth
reductase (MDHAR), dehydroascorbate reductase conditions and the plant developmental stage.
(DHAR) and glutathione reductase (GR) has also been Controversy exists about the role of osmolyte
reported (Noctor and Foyer 1998). Under stressful con- accumulation as a selection criterion in crop breeding
ditions, the enhanced activities of these enzymes appear programs to improve yield in dry environments;
to function as important components of the antioxidative according to Serraj and Sinclair (2002) little evidence
defense system (Di Cori et al. 2013; Sharma and Dubey for a strong benefit of such accumulation on crop yield
2005). The coordinated activity of the multiple forms of has been provided. These authors reported that in the
these enzymes in different cell compartments allows a literature a positive correlation between osmotic adjust-
balance between the rate of formation and removal of ment and yield is significant under severe drought stress,
ROS, and maintains hydrogen peroxide (H2O2) at levels when the yields are very low.
required for cell signaling (Munns and Tester 2008). In
fact, the role of ROS as important signal transduction Roles of hormones in plant stress response
molecules of the plant response to abiotic stresses has
been acknowledged and widely accepted (Miller et al. Plant hormones play important roles in regulating the
2010; Del Rio 2015). The key role of ROS as signal responses to a wide variety of internal and external
transduction molecules involves mediating responses to stimuli. They can have direct and/or indirect effects on
stresses, programmed cell death and different develop- multiple plant functions. Hormones also play substantial
mental stimuli (Miller et al. 2010). During ABA- roles in the response of plants to abiotic stress, in par-
mediated stress responses, ROS act to sustain plant sur- ticular, abscisic acid (ABA), salicylic acid (SA), ethyl-
vival under stress conditions. ene, jasmonates (JAs), and cytokinins (Fig. 1).
Since both salt and drought ultimately result in de- Two signal transduction pathways are triggered by
hydration and osmotic imbalance of the cell, the com- salt and drought stresses based on their dependence on
ponents of both stresses interact (cross talk) with each ABA (Takahashi et al. 2004; Golldack et al. 2014; Fujita
other, and the pathways act cooperatively to alleviate et al. 2005; Yoshida et al. 2014). ABA, the most studied
stress. Plant cells need to repair the stress damage plant stress-signaling hormone, is the endogenous signal
through detoxification signals, and to then re-establish molecule enabling plants to survive severe adverse en-
the homeostasis. The production of osmolytes mediates vironmental conditions, such as salt and drought stress.
the osmotic adjustment by overcoming osmotic stress In fact, the synthesis and accumulation of ABA, pro-
and re-establishing cellular homeostasis (Shinozaki and vides a fast response to abiotic stress, in particular water
Yamaguchi-Shinozaki 1997; Zhu 2002). They also help stress (Nakashima et al. 2009; Peleg and Blumwald
the cells to maintain their hydrated state providing re- 2011). In Arabidopsis thaliana, a large number of genes
sistance against drought and cellular dehydration. These are associated with ABA de novo biosynthesis and the
molecules are proline, glutamate, glycine-betaine, car- genes encoding ABA receptors and downstream signal-
nitine, mannitol, sorbitol, fructans, polyols, trehalose ing relays have been characterized (Cutler et al. 2010).
(Petrusa and Winicov 1997; Nawaz and Ashraf 2010; However, the stress response may also involve ABA-
Redillas et al. 2012), sucrose, oligosaccharides and in- independent signaling response pathways (Yamaguchi-
organic ions like K+ (Mahajan and Tuteja 2005). The Shinozaki and Shinozaki 2006). For example, osmotic
maintenance of hydrophilic interactions with membrane stress-responsive gene expression is regulated by both
lipids and proteins, e.g. the preservation of membrane ABA-dependent and -independent pathways (Yoshida
structural integrity, is based on the hydroxyl group of et al. 2014).
sugar alcohols that can substitute for the OH group of ABA-responsive TFs (AREB/ABF) have a pivotal
water. However, the tolerance towards stress is not role in ABA-dependent gene activation, e.g. increased
always related to the presence of osmolytes. In some AREB1/ABF2, AREB2/ABF4 and ABF3 expression is
cases it has been reported that they play a vital role (Aziz induced by drought, high salinity and ABA in
Plant Soil

vegetative tissues (Fujita et al. 2005), and based on microarray expression analyses have determined that
overexpression data, these three AREB/ABFs are posi- numerous genes encoding proteins with cytokinin sig-
tive regulators of ABA signaling under drought stress naling pathways are affected differently by various abi-
conditions (Fujita et al. 2005; Yoshida et al. 2010, otic stresses. Javid et al. (2011) reported that the exog-
2014). In Arabidopsis many drought-regulated genes enous application of a synthetic cytokinin, kinetin, is
are ABA-responsive genes; while, about a third of iden- capable of breaking stress-induced seed dormancy in
tified drought-regulated genes are not significantly reg- crop plants such as tomato, barley and cotton. This
ulated by ABA or ABA analogues, thus belonging to positive effect of kinetin treatment may be due to the
ABA-independent pathway (Huang et al. 2008). It is cytokinin activity as a direct free radical scavenger or it
noteworthy to mention that promoter motif analyses of may be involved in antioxidant activity related to the
the latter genes revealed a significant over- protection of purine breakdown (Javid et al. 2011).
representation of ABA-responsive promoter motifs Moreover, by enhancing root cytokinin synthesis it is
(e.g. ABRE-like, ACGTABREMOTIFA2OSEM, and possible to modify both shoot hormonal and ion status,
GADOWNAT) in the promoters of these genes. There- thus ameliorating the salinity induced decreases in
fore the expression of many of these genes could be at growth and yield (Ghanem et al. 2011). However, the
least partially linked to the ABA-dependent stress signal positive role played by this hormone in ameliorating
pathway (Huang et al. 2008). stress is still controversial based on the analyses of genes
The crucial role of DREBs (dehydration-responsive involved in stress response and regulated by cytokinin.
element binding) also referred to as CBF (C-repeat Improved salt and drought stress tolerance in cytokinin
binding factor) proteins in drought, high salinity and deficient mutants has been reported by Nishiyama and
heat stress have been pointed out in Arabidopsis coworkers (Nishiyama et al. 2011; Nishiyama et al.
(Sakuma et al. 2006a, b; Kim et al. 2012). DREB2A 2012). Tran et al. (2010) reported that the three cytoki-
and DREB2B have been reported to function mainly in nin receptors AHK2, AHK3 and AHK4 act as negative
ABA-independent manner under osmotic, drought,high regulators in both ABA-dependent and ABA-
salinity and heat stress (Yoshida et al. 2014). DREB2A independent pathways.
seems to function mainly in ABA-independent water JAs are involved in drought tolerance and in the
stress–inducible gene expression, since its expression response to salt stress, acting as positive regulators of
is strongly induced by drought and high-salinity stresses salt tolerance (Dong et al. 2013; Qiu et al. 2014; Zhao
but not by ABA treatment (Liu et al. 1998). A better et al. 2014). There is growing evidence that jasmonic
elucidation of the role of DREB2A under water stress acid and biologically active derivatives alleviate salt
has been made by Sakuma et al. (2006b), who reported stress in plants. After methyl jasmonate application,
that DREB2A regulates the drought-stress responsive enhanced amount of different antioxidants have been
genes expression, thus enhancing the stress tolerance. reported (Ahmad et al. 2016). However, it seems that the
Cytokinins are produced in the root tips and then response to the jasmonate application is depending on
translocated to the shoot through xylem. The effects of the concentration and is species specific (Ahmad et al.
the cytokinins on stress tolerance are rather complex. 2016). The defensive effects of treatment with
Several studies have provided strong evidence of the jasmonates have been mainly ascribed to the induction
existence of crosstalk among cytokinin, ABA, and stress of antioxidant activity (Dar et al. 2015). Jasmonic acid
signaling pathways (Tran et al. 2010; Nishiyama et al. enhances the activities of the enzyme cationic peroxi-
2011; Nishiyama et al. 2012). According to some au- dase, pathogenesis related proteins, like PR-1 and PR-
thors, cytokinin and ABA may exert antagonistic activ- 10, and salt stress responsive proteins in roots of rice
ities during a number of growth and physiological pro- plants (Moons et al. 1997) and antioxidant enzymes in
cesses, including stomatal opening, cotyledon expan- wheat (Qiu et al. 2014).
sion and seed germination (Javid et al. 2011). Much progress has been made to elucidate the role of
The exposure of plants to water limiting conditions jasmonates in signaling, cross-talking, jasmonate recep-
decreases cytokinin levels while excessive overproduc- tors etc., but not all the mechanisms behind the stress
tion of cytokinins above a certain threshold causes ab- response have been clarified (Ahmad et al. 2016).
normal organ and tissue development, but not drought Salicylic acid (SA) and ethylene may be generated
tolerance (Gepstein and Glick 2013). In Arabidospis, during stress responses (Mahajan and Tuteja 2005).
 Plant Soil

These molecules may amplify the initial signal, gener- In contrast to JAs, which promotes stomatal closure,
ating a second round of signaling that may follow either ethylene has been implicated in stomatal movement
the same pathway or use other components of the sig- (Daszkowska-Golec and Szarejko 2013), either by
naling pathway. It is well known that SA plays an inhibiting ABA-induced stomatal closure, or promoting
important role in plant responses to pathogens, but it is stomatal closure by promoting NADPH oxidase-
also involved in the regulation of plant growth, devel- mediated ROS production in guard cells (Kazan 2015).
opment, ripening, flowering, and responses to abiotic Overall, these results are contradictory and the possible
stresses (Miura and Tada 2014). The involvement of SA effects of ethylene-mediated stomatal movement on
in the regulation of drought responses is based on the drought avoidance require further investigation.
results obtained in different species (Munne-Bosch and Jung and Park (2011) reported that in transgenic
Penuelas 2003; Bandurska and Stroìnski 2005). SA- plants the overexpression of the gene YUCCA3
inducible genes PR1 and PR2 are induced by drought (YUC3), which encodes an auxin biosynthetic enzyme,
stress (Miura and Tada 2014). Controversy still exists caused sensitivity to salt in germinating seeds of
about the effect of SA on drought tolerance because Arabidopsis. High salt stress greatly remodels root ar-
some investigators have reported enhancement of chitecture by altering auxin accumulation and redistri-
drought tolerance by SA application, while others have bution. This means that the redistribution of auxin max-
reported a reduction (Miura and Tada 2014; Kang et al. ima formation in plant tissues is correlated with reduced
2012). An increase in endogenous hormone levels pro- growth, and therefore the reduction observed under
motes stomatal closure; probably caused by the genera- stress conditions could also be the outcome of such
tion of ROS induced by SA (Melotto et al. 2006). altered auxin accumulation and redistribution (Ryu and
Stomatal closure may also be caused by the exogenous Cho 2015; Dodd and Pérez-Alfocea 2012). Decreases in
application of SA leading to ROS, H2O2, and Ca2+ root branching in Arabidopsis are associated with
accumulation (Dong et al. 2001; Liu et al. 2003). changes in indole-3-acetic acid (IAA) response follow-
Low levels of ethylene have been reported to be ing the addition of 150 mM salt (Ulmasov et al. 1997;
involved in the defense against abiotic stress (Forni Dubrovsky et al. 2008; Contreras-Cornejo et al. 2014).
et al. 2012; Kazan 2015). However, when ethylene is Results showed that salinity inhibits auxin-inducible gene
produced above a threshold level, it is considered to be expression in primary root tips (Contreras-Cornejo et al.
Bstress ethylene^ which is unfavorable in terms of root/ 2014). In another study, the accumulation of IAA in grey
shoot proliferation and other growth parameters and, poplar trees exposed to 150 mM NaCl was compared to
thus hinders plant growth and development. The syn- the non-treated controls. The concentration of IAA in
thesis of stress ethylene occurs in two peaks of ethylene poplar trees exposed to salt was decreased by 65–85 %
that are observed after stress exposure to plants. The first (Luo et al. 2009; Dodd and Pérez-Alfocea 2012). More-
small peak of ethylene is believed to be responsible for over, Arabidopsis mutants with defects in auxin transport
transcription of genes that encode plant defensive/ were more sensitive to salt stress, suggesting that the
protective proteins. The second much larger ethylene transport of IAA between plant cells affects plant re-
peak, termed as Bstress ethylene^, is detrimental to plant sponse to saline conditions (Wang et al. 2009;
growth and initiates processes like senescence, chlorosis Contreras-Cornejo et al. 2014). Plant mutants with de-
and leaf abscission (Glick et al. 2007). Increased foliar fects in transcription factors/receptors involved in the
ethylene evolution as a consequence of salinization has auxin response were dramatically affected by salt, show-
been detected as reviewed by Dodd and Pérez-Alfocea ing up to 50 % inhibition in shoot fresh weight. Based on
(2012). Ethylene production as a consequence of observations that high salt levels decreased the level of
drought depends on the plant species. Thus, rapid IAA in various plant tissues, researchers have shown that
drought stress elicits production of this hormone in the addition of exogenous IAA could alleviate some of
wheat (Narayana et al. 1991), but not in common bean, the adverse effects of salt stress (Afzal et al. 2005; Abd
cotton, or miniature rose (Morgan et al. 1990). Plant El-Samad 2013; Liu et al. 2015).
growth inhibition caused by stress ethylene may be Polyamines are a group of ubiquitous aliphatic amine
reduced by PGPB that possess the enzyme 1- compounds, involved in plant development and physi-
aminocyclopropane-1-carboxylate deaminase (ACCD), ology as well as in modulating the defense response to
as described below. stress, such as salt and drought (Gill and Tuteja 2010).
Plant Soil

The most common polyamines i.e., putrescine, decreasing the inhibitory effects of various pathogenic
spermidine and spermine, can be found in free, soluble agents on plant growth.
conjugated and insoluble bound forms. A connection Plant growth is readily facilitated when plants are
among polyamine metabolism, abiotic stress and ABA provided with optimal levels of various plant hormones
has been postulated (Jiménez-Bremont et al. 2007; Al- including cytokinins, gibberellins, indoleacetic acid
cázar et al. 2010). (IAA) and ethylene. However, a detailed understanding
Under salt stress conditions, enhanced polyamine of the role of bacterially produced phytohormones is
titre has been correlated with improved salinity toler- complicated by the fact that plants simultaneously pro-
ance (Zapata et al. 2004; Alcázar et al. 2010). Several duce precisely the same molecules. Some PGPB can
authors suggested a possible beneficial activity of exog- synthesize either cytokinins or gibberellins or both
enous application of polyamines for the improvement of (Salamone et al. 2001; Joo et al. 2005). Notwithstanding
plant tolerance to abiotic stress (Gill and Tuteja 2010), the demonstration that cytokinin producing bacteria
but this is still an unresolved issue. For example, the may enhance plant growth in drying soil (Arkhipova
response may depend on the organ developmental stage, et al. 2007), scientists have not yet elaborated a detailed
since Pandolfi et al. (2010) reported that in the mature understanding of the functioning of bacterial cytokinins
root zone of maize and Arabidopsis pre-treatment with or gibberellins in plant growth and development. In this
1 mM spermine, spermidine or putrescine prevented case, the putative roles played by these two phytohor-
salt-induced K+ leak, while in the distal elongation zone mones is largely based on studies where purified hor-
opposite effect was observed. The authors suggested the mones have been added to individual plants. While the
existence of complex mechanism that involves poly- scientific literature contains descriptions of a number of
amine transport, cyplasmic accumulation, different naturally occurring auxins, by far the most
metabolization and functional expression. common and the most studied auxin is IAA. This hor-
mone affects plant cell division, extension and differen-
tiation; stimulates seed and tuber germination; increases
xylem and root development; initiates lateral and adven-
Plant growth-promoting bacteria titious root formation; mediates responses to light, grav-
ity and fluorescence; affects pigment formation; and can
In healthy soils there are typically around 108 to 109 help to mediate resistance to various stresses (Spaepen
bacteria per gram of soil, with this number dropping and Vanderleyden 2011). Plant roots and shoots are both
down to as low as 104 in environmentally stressed soils affected by IAA although at very different concentra-
(Schoenborn et al. 2004). Moreover, bacteria are not tions, with the optimal IAA level for roots being ap-
evenly distributed in soils, with the concentration of proximately five orders of magnitude lower than for
bacteria around the roots of plants, i.e., in the rhizo- shoots. The plant hormone ethylene is also active in
sphere, generally being much higher than in the rest of modulating plant growth and development in a very
the soil. This is a direct consequence of the many small wide range of concentrations, i.e. from about 0.05 μL/
molecules including sugars, amino acids and organic L to around 200 μL/L (Abeles et al. 1992). Ethylene in
acids that are exuded from the roots of most plants and plants can promote root initiation, inhibit root elonga-
serve as a food source for many soil bacteria (Badri and tion, promote fruit ripening and flower wilting, stimulate
Vivanco 2009). Soil bacteria may affect plants in their seed germination, promote leaf abscission, inhibit
vicinity in several different ways. The interaction be- Rhizobia spp. and mycorrhizae plant interaction, and
tween soil bacteria and plants may be beneficial, harm- be produced as a response to various environmental
ful or neutral for the plant. Here, the focus is on bene- stresses (Abeles et al. 1992). The enzyme 1-
ficial soil bacteria, i.e. plant growth-promoting bacteria aminocyclopropane-1-carboxylate (ACC) deaminase
(PGPB). These bacteria employ a wide range of mech- can cleave plant-derived ACC (the immediate biosyn-
anisms to facilitate plant growth (Glick 2012). For ex- thetic precursor of ethylene) and thereby lower ethylene
ample, they may promote plant growth directly, gener- levels in plants (Glick et al. 1998). In practice, this
ally by either facilitating resource acquisition (e.g. Fe, P means that PGPB that express ACC deaminase can
and N) or by modulating plant hormone levels. On the modulate all of the above mentioned effects of ethylene
other hand, they may promote plant growth indirectly by on plants (Glick et al. 2007). Finally, it is necessary to
 Plant Soil

keep in mind that the functioning in plants of bacterial mechanism(s) employed by a PGPB strain in conferring
phytohormones is complicated by the interaction be- salt or drought tolerance to a plant is completely un-
tween these exogenous hormones and the endogenous known (see Table 1). While these bacterial strains may
plant mechanisms that regulate plant hormone be useful to the lab that reported the work, they do not
homeostasis. provide other researchers with any clear mechanistic
guidelines for selecting additional PGPB that are able
to confer salt or drought tolerance to treated plants.
How do PGPB protect plants against stress Another problem with some of the literature reports on
the use of PGPB to ameliorate the effects of drought or
Using PGPB to protect plants from salt and drought salt stress is that sometimes the work reported in these
stress manuscripts does not include the characterization of the
PGPB strain(s) to the genus and species level. Again,
Many of the mechanisms that PGPB utilize to protect this makes it almost impossible for others to reproduce
plants from salt and drought stress are interconnected and build upon this published work.
and affect one another. Moreover, a detailed description Numerous bacterial traits have been suggested to be
of the nature of these interconnections remains, for the involved in conferring salt or drought tolerance to treated
most part, to be elaborated. In addition, while PGPB can plants. These include the production of cytokinin,
provide some protection against the inhibitory effects of indoleacetic acid, ACC deaminase, abscisic acid,
salt or drought stress (e.g. by promoting plant growth), trehalose, volatile organic compounds, and
they may also alter plant gene expression so that the exopolysaccharides. Some scientists have also reported
plant is less likely to succumb to these stresses. For that beneficial PGPB may synthesize siderophores and
example, various PGPB have been shown to increase have the ability to solubilize phosphate, traits that are
plant production of the metabolites betaine, proline and unlikely to contribute directly to conferring salt or
trehalose as well as the synthesis of enzymes such as drought tolerance to treated plants but nevertheless can
SOD and CAT that can detoxify reactive oxygen species contribute to a plant’s overall health.
(for example, Nautiyal et al. 2013).
Occasionally, conferring salt or drought tolerance Cytokinin
upon plants can be unequivocally attributed to one or
another specific PGPB mechanism. However, generally Arkhipova et al. (2007) tested the hypothesis that the
speaking, to prove that a particular bacterial mechanism lowered levels of cytokinin in drought stressed plants
is operative it is necessary to either inactivate a key help the plant to adapt to the decreased amount of water
gene, so that less (or none) of the gene product is made, by (i) favoring carbon allocation to root growth and (ii)
or to overproduce the product of a key gene so that more promoting stomatal closure. These workers added a
of the gene product is made. cytokinin-producing Bacillus sp. strain to the soil where
The involvement in plant biochemistry/physiology of lettuce seedlings were grown. Inoculation of plants with
a PGPB that either overproduces or underproduces a this bacterium significantly increased both shoot/leaf
key metabolite or enzyme can then be demonstrated cytokinin content and biomass (measured 20 days after
directly by comparing the behavior of the mutant to seedling inoculation) of 12-day-old seedlings that were
the wild-type strain. While this may seem obvious, it subjected to various levels of drought. In addition the
is nevertheless only very rarely done. Thus, many labs bacterial treatment resulted in no or only a small in-
purport to understand the mechanisms that are operative crease in root biomass while the root length was de-
in a specific plant-microbe interaction based solely on creased. From the results of this study, it was concluded
the presence of a certain biological activity within the that (i) the added bacterial strain elevated plant cytokinin
PGPB that they have utilized. In fact, all that these levels slightly increasing root biomass and increased
workers have done is to show that there is a correlation root sink strength thereby compensating for decreased
between a certain trait and a specific behavior. This root length and (ii) the increase in plant cytokinin did
approach does not prove the involvement of the trait in not result in the protective closure of stomata. This latter
question with the observed behavior. In addition, the effect is attributed to the rise in plant ABA levels that
literature contains a number of reports where the accompanied the rise in cytokinin levels. The
Table 1 Amelioration of salt and/or drought stress in various plants by PGPB. The entries in this table are grouped according to the mechanisms used by the PGPB with the oldest paper
listed first within each mechanism category
Plant Soil

Plant Microorganism Conditions Suggested mechanism(s) Conditions Reference

Lettuce Bacillus sp. Growth chamber Cytokinin Drought, 20 days of 30 % of soil Arkhipova et al. 2007
water capacity
Alfalfa Sinorhizobium meliloti Greenhouse Cytokinin Drought; 3–4 days of no water Xu et al. 2012
Wheat Pseudomonas aureantiaca, Growth chamber IAA Salt, 100 mM NaCl Egamberdieva 2009
P. extremorientalis
Medicago truncatula Sinorhizobium meliloti Greenhouse, hydroponics IAA Salt, 150–300 mM NaCl Bianco and Defez 2009
Silybum marianum P. extremorientalis Growth chamber IAA Salt, 25–100 mM NaCl Egamberdieva et al. 2013
Cotton P. putida, P. chlororaphis Growth chamber IAA Salt, 100 mM NaCl and Egamberdieva et al. 2015
100 mM Mg2SO4
Wheat Hallobacillus sp., Bacillus Laboratory IAA, P solubilization, siderophores Salt, 80–320 mM NaCl Ramadoss et al. 2013
halodenitrificans
Rice Serratia sp., P. sp. Greenhouse IAA, N-fixation, P solubilization Salt, Electrical conductivity =0–16 dS/m Nakbanpote et al. 2014
Sunflower P. aeruginosa Growth chamber IAA, siderophores, exopolysaccharides Salt, 125 mM NaCl Tewari and Arora 2014
Arabidopsis thaliana Micrococcus yunnanensis, Growth chamber IAA, P solubilization, siderophores Salt, 200 mM NaCl; drought, Sukweenadhi et al. 2015
Paenibacillus barengoltzii 5 days of no water
Groundnut P. aeruginosa Greenhouse IAA, P solubilization Salt, Electrical conductivity =0–6 dS/m Ghorai et al. 2015
Beans Rhizobium etli Greenhouse Trehalose Drought, 3 weeks of no water Suarez et al. 2008
Maize Azospirillum brasilense Greenhouse Trehalose Drought, 10 days with no water Rodriguez-Salazar et al. 2009
Beans Rhizobium etli Growth chamber Trehalose Drought, 5 or 10 days with no water Reina-Bueno et al. 2012
Wheat Bacillus thuringiensis Growth chamber Volatile organic compounds Drought, 10 or 14 days with no water Timmusk et al. 2014
Tomato, pepper Achromobacter piechaudii Growth chamber ACC deaminase Drought, 7 or 12 days with no water Mayak et al. 2004a, 2004b
Tomato Achromobacter piechaudii Growth chamber ACC deaminase Salt, 0–172 mM NaCl Mayak et al. 2004a
Groundnut P. fluorescens Laboratory, field ACC deaminase Salt, 120 mM NaCl Saravanakumar and Samiyappan 2007
Canola P. putida Growth chamber ACC deaminase Salt, 1 M NaCl at 10 °C and Cheng et al. 2007
1 mM NaCl at 20 °C
Cucumber P. putida Growth chamber ACC deaminase Salt, 0–200 mM NaCl Gamalero et al. 2010
Cucumber P. fluorescens Greenhouse ACC deaminase, Salt, 659 mS m−1 Egamberdieva et al. 2011; Cho et al. 2015
siderophore
Red pepper Brevibacterium iodinum, Greenhouse ACC deaminase Salt, 100–200 mM NaCl Siddikee et al. 2011
Bacillus licheniformis,
Zhihengliuela alba
Barley Paenibacillus polymyxa, Field ACC deaminase Drought, naturally occurring Timmusk et al. 2011
Bacillus megaterium,
Bacillus cereus,
bacillus pumilus
Tomato P. mendocina Growth chamber, greenhouse ACC deaminase Salt, 172–207 mM NaCl Sadrnia et al. 2011
Soybean P. sp. Growth chamber ACC deaminase, IAA Salt, 200 mM NaCl Kasotia et al. 2012
Chickpea Mesorhizobium ciceri Growth chamber ACC deaminase Salt, 0.15 % NaCl Brígido et al. 2013
Spring wheat Variovorax paradoxus Greenhouse ACC deaminase Drought, No water until soil matric Chen et al. 2013
potential was −30 kPa
Mung bean, bean, peanut Bradyrhizobium sp., Growth chamber ACC deaminase, IAA Salt, 50 mM NaCl; drought, no water Tittabutr et al. 2013
Enterobacter sp., until plants showed visible
Chryseobacterium sp. signs of stress
Table 1 (continued)
Plant Microorganism Conditions Suggested mechanism(s) Conditions Reference

Mung bean P. syringae, P. fluorescens Growth chamber ACC deaminase, IAA Salt, Electrical conductivity Ahmad et al. 2013
=4–12 dS/m
Cotton Klebsiella oxytoca Greenhouse ACC deaminase, IAA Salt, 1.3–3.5 g NaCl kg−1 soil Yue et al. 2007; Liu et al. 2013
Pepper Bacillus licheniformis Growth chamber ACC deaminase, IAA Drought, 10–15 days of no water Lim and Kim 2013
Wheat Serratia spp., Aerococcus spp. Jars with soil ACC deaminase Drought, 15–60 % of water Bangash et al. 2013
holding capacity
Mung bean Rhizobium sp., PGPB Field ACC deaminase Salt, Electrical conductivity =5.6 dS/m Aamir et al. 2013
Maize P. syringae, P. fluorescens Field ACC deaminase Drought, water to 50 % of field capacity Zafar-ul-Hye et al. 2014
Barley, oats P. putida, P. sp., P. corrugata Greenhouse, field ACC deaminase Salt, Electrical conductivity Chang et al. 2014
=9.4 dS/m
Limonium sinense Bacillus, Arthrobacter, Streptomyces, Greenhouse ACC deaminase Salt, 0–250 mMNaCl Qin et al. 2014
(Girard) Kuntze Isoptericola
Tomato, Arabidopsis Enterobacter sp. Growth chamber ACC deaminase, IAA Salt, 200 mM NaCl Kim et al. 2014
Tomato P. putida Greenhouse ACC deaminase Salt, 0–190 mM NaCl Yan et al. 2014
Tomato P. fluorescens, P. migulae Greenhouse ACC deaminase Salt, 0–185 mM NaCl Ali et al. 2014
Rice P. stutzeri Growth chamber ACC deaminase Salt, 120 and 2000 mM NaCl Han et al. 2015
Potato Achromobacter xylosoxidans, Greenhouse ACC deaminase Drought, 40 % of soil water Belimov et al. 2015
Pseudomonas oxyzihabitans, holding capacity
Variovorax paradoxus
Velvet bean Rhizobacteria Growth chamber ACC deaminase Drought, 45 % of water Saleem et al. 2015
holding capacity
Barley Hartmannibacter diazotrophicus Greenhouse ACC deaminase Salt, 200 and 400 mM NaCl Suarez et al. 2015
Sunflower PGPB Greenhouse ACC deaminase Salt, Electrical conductivity Kiani et al. 2015
=8–12 dS/m
Canola Brevibacterium epidermidis, Laboratory ACC deaminase Salt, 120 mM Siddikee et al. 2015
Bacillus aryabhattai
Chinese cabbage Herbaspirillum sp. Growth chamber ACC deaminase, Salt, 0 and 150 mM NaCl Lee et al. 2015
IAA, siderophores
Chickpea Bacillus amyloliquefaciens, Greenhouse ACC deaminase, IAA, Drought, 14 days of no water Kumar et al. 2015
P. putida P solubilization
Pea Variovorax paradoxus Greenhouse ACC deaminase Salt, 70 and 130 mM NaCl Wang et al. 2016
Maize Azospirillum spp. Greenhouse Unknown Salt, 0 to −1.6 MPa osmotic potential Abd El-Samad Hamdia et al. 2004
Rice Bacillus Pumilus, P. pseudoalcaligenes Greenhouse Unknown Salt, 0.5–2.5 g NaCl/ kg of soil Jha and Subramanian 2013
Wheat Azosprillium lipoferum, Greenhouse Unknown Salt, Electrical conductivity =14 dS/m Saghafi et al. 2013
P. fluorescens
Rice Bacillus amyloliquefaciens Greenhouse Unknown Salt, Nautiyal et al. 2013
Plant Soil
Plant Soil

conclusion from these experiments is that in the field, (Egamberdieva et al. 2013). Since this bacterium
the decreased cytokinin levels that are induced by mod- doesn’t produce ACC deaminase (see below), it was
erate drought contribute to drought tolerance; however, assumed that the tolerance to salt stress was a conse-
inoculation with a cytokinin-synthesizing bacterium quence of bacterially synthesized IAA. These workers
may also have a beneficial effect. Some of the apparent- did not detail the nature of the changes within the plant
ly paradoxical effects of changes in plant cytokinin other than size and biomass.
levels as compared to the effect of adding a cytokinin Microbial IAA not only serves to mediate the plant-
producing bacterium may relate to the fact that many microbe relationship but may also be a mechanism for
PGPB affect plants in a variety of different ways and it is the bacteria to protect themselves from environmental
often difficult to ascribe every change to a particular stress. For example, after osmotic stress about 50 % of
bacterial mechanism. untreated bacterial cells died as opposed to only 30 % of
Recently, a strain of Sinorhizobium meliloti was IAA-treated cells (Bianco et al. 2006).
engineered to overproduce cytokinin and then tested
for the ability to protect alfalfa plants against the senes-
cence that results from drought stress (Xu et al. 2012). ACC deaminase
The S. meliloti transformant expressed an
Agrobacterium ipt gene under the control of the trp As mentioned above, abiotic stress such as high salt or
promoter and produced ~5 times the level of cytokinin drought induces the synthesis of stress ethylene in plants
synthesized by the non-transformed strain. After a peri- and this ethylene generally inhibits plant growth (Abeles
od of severe drought stress, alfalfa plants inoculated et al. 1992). Thus, it was predicted that a PGPB that
with the engineered strain were significantly larger than possessed the enzyme ACC deaminase would lower the
plants inoculated with the non-transformed strain. When level of stress ethylene, thereby allowing greater plant
the plants subjected to drought were rewatered, plants growth under various abiotic stresses. To test this hy-
inoculated with the transformed strain grew to a level pothesis, Mayak et al. (2004a and b) isolated and char-
similar to plants that had not been drought stressed at all. acterized an ACC deaminase-containing PGPB from a
This experiment clearly demonstrates the ability of rhi- hot, dry and salty environment and tested its ability to
zobial strains synthesizing higher than normal levels of promote the growth of tomato plants at high levels of
cytokinin to improve the tolerance of alfalfa (and possi- salt or following a period of drought. As predicted, the
bly other crops) to severe drought stress. bacterium significantly increased the biomass of treated
plants both in the presence of high salt or following
IAA drought conditions. In addition, the bacterium dramati-
cally lowered the amount of ethylene produced by salt
To create a PGPB strain to better protect plants against treated plants. Subsequent experiments showed that on-
inhibition by high salt, a strain of Sinorhizobium meliloti ly wild-type PGPB (ACC deaminase-containing), and
was engineered with an additional pathway for IAA not mutant PGPB (that lacked ACC deaminase)
biosynthesis (Bianco and Defez 2009). When the trans- protected plants from ethylene-mediated growth inhibi-
formed S. meliloti strain was used to nodulate Medicago tion, regardless of whether the bacteria were
truncatula plants, the plants became more resistant to rhizospheric or endophytic in nature (Cheng et al.
the effects of high salt (0.3 M) and to several other 2007; Ali et al. 2014; Han et al. 2015). Subsequent to
stresses. The bacterially treated plants had a higher the pioneering experiments of Mayak et al. (2004a),
proline content and an increase of activity of several many additional laboratories have successfully utilized
antioxidant enzymes including superoxide dismutase, ACC deaminase-containing PGPB to ameliorate salt
peroxidase, glutathione reductase and ascorbate stress with a wide variety of different plants, both in
peroxidase. the laboratory and in the field (Table 1).
When the medicinal plant Silybum marianum (milk Based on some of the above-mentioned experiments,
thistle), inoculated with Pseudomonas extremorientalis, many researchers tacitly assume that for PGPB that
was grown in the presence of high salt concentrations, synthesize IAA and/or produce the enzyme ACC deam-
the plant’s root and shoot lengths and fresh weight were inase, the mechanism of drought or salt protection has
increased in the presence of the bacterium already been established so that it is not necessary to
 Plant Soil

generate IAA or ACC deaminase minus mutants to example, when the PGPB Azospirillum brasilense
prove the involvement of these mechanisms. Sp245 was grown in the presence of 100 mM NaCl,
Some workers have studied the effects of ethylene on the level of ABA that it produced increased significantly
drought tolerance in considerable detail. For example, (Cohen et al. 2008). Some PGPB strains have also been
Belimov et al. (2009) reported that the ACC deaminase- observed to increase levels of plant secreted ABA fol-
containing PGPB Variovorax paradoxus 5C-2 but not lowing the imposition of water stress (by the addition of
an ACC deaminase minus mutant of this bacterium, polyethylene glycol), however it is difficult to ascertain
improved the growth, yield, and water use efficiency whether the ABA in this case was produced by the
of pea plants subjected to drought. V. paradoxus 5C-2 bacterium or by the plant (Cohen et al. 2008). In addi-
treatment also increased the xylem concentration of tion, it was reported that the wheat aquaporin gene
ABA as well as the ability of Rhizobium leguminosarum (encoding water transport) TaAQP7 was upregulated
bv. viciae to nodulate pea plants in the presence of after drought stress (PEG treatment) and was blocked
drought stress. In addition, Chen et al. (2013) observed by inhibiting ABA biosynthesis (Zhou et al. 2012),
that older more fully expanded wheat leaves partially consistent with the involvement of ABA in the upregu-
lost their ability to close their stomata in response to lating TaAQP7 as a means of enhancing drought toler-
both externally-applied ABA or soil drying (which stim- ance in plants. In other experiments, treating maize
ulates ABA production). On the other hand, the ability plants with fluridone (an inhibitor of ABA synthesis)
to close stomata was partially restored when plants were inhibited plant growth in a manner analogous to drought
pre-treated with either the ethylene receptor inhibitor 1- stress (Cohen et al. 2009). Inoculation of these plants
methylcyclopropene or the ACC deaminase-containing with a PGPB strain of Azospirillum completely reversed
PGPB V. paradoxus 5C-2. These workers have sug- this effect. Moreover, measurement of the relative water
gested that the insensitivity of older leaves to ABA most contents of fluridone-treated or drought stressed plants
likely reflects a decreased sensitivity to ethylene. In was decreased compared to well-watered plants in both
another study, comparing well-watered and water- cases, an effect that was reversed by treatment with the
limited potato plants treated with different PGPB, bacterial strain.
Belimov et al. (2015) suggest that in addition to lower-
ing ethylene levels by ACC deaminase and promoting Trehalose
growth with bacterial auxin, bacteria with these activi-
ties may promote growth by modulating plant phytohor- PGPB can also protect plants from drought and salt
mone balance. Moreover, treating salinized pea plants stress by synthesizing osmoprotectants such as proline
with the ACC deaminase-containing PGPB and/or trehalose (Suarez et al. 2008; Rodriguez-Salazar
V. paradoxus 5C-2 increased K uptake and root to shoot et al. 2009). Trehalose is a highly stable glucoside
K flow, but decreased Na flow (Wang et al. 2016). This consisting of two molecules of α-glucose that forms a
observation is similar to the observation of Mayak et al. gel phase (replacing water) as cells dehydrate, thereby
(2004a) who reported an increase in K uptake in tomato decreasing the damage to cells from drought and salt.
plants treated with a different ACC deaminase- When mutants of a strain of Rhizobium etli that both
containing PGPB strain. Thus, both of these reports overproduce and underproduce trehalose were con-
are consistent with the notion that PGPB that contain structed, the trehalose-overproducing strain increased
both ACC deaminase and auxin ameliorate salt stress in the number of nitrogen fixing nodules per plant while
part by improving plant ion homeostasis and water the trehalose-underproducing strain decreased nodule
relations. number (Suarez et al. 2008). Higher levels of trehalose
had a positive effect on both the survival and yield of
ABA bean plants nodulated by these rhizobial strains, espe-
cially following periods of drought. In addition, when
It is well known that plant ABA levels increase in maize plants were inoculated with a strain of
response to water deficit and that ABA plays a key role Azospirillum brasilense that was transformed with a
in stomatal closure and the induction of several water- plasmid carrying a trehalose biosynthesis gene-fusion
deficit-induced genes (Dodd et al. 2010; Vacheron et al. gene (i.e. otsA and otsB), 85 % of them survived drought
2013). ABA is also produced by several PGPB so, for stress compared to 55 % of plants that survived when
Plant Soil

they were inoculated with the wild-type strain study did not report the numbers of PGPB, either wild-
(Rodriguez-Salazar et al. 2009). Moreover, a 73 % in- type or mutant, bound to plant roots, it is not possible to
crease was observed in the biomass of maize plants know for certain whether the inability of the mutant to
inoculated with transformed A. brasilense compared promote plant growth was a consequence of decreased
with the wild-type strain. These results clearly demon- bacterial numbers on the root.
strate that PGPB that increase the level of trehalose
inside plants can protect those plants against drought Some notes of caution
or salt stress.
As a consequence of a limited number of definitive
Volatile organic compounds experiments (some of which are discussed above), many
scientists have been encouraged to isolate and charac-
In the soil, many bacteria and plants communicate with terize new bacterial strains that are able to help plants to
one another by synthesizing a number of different vol- overcome the potentially debilitating effects of salt and
atile organic compounds. Some of these compounds drought stress. These bacteria have been tested in the
have the ability to turn on the synthesis of plant genes lab, under greenhouse conditions and also in the field
encoding reactive oxygen species scavenging enzymes and have been found to be quite effective. Many of these
such as glutathione reductase, monodehydroascorbate studies are summarized in Table 1. While most of the
reductase, superoxide dismutase and catalase that can, experiments referred to in Table 1 were done either in a
in turn, protect plants against drought or salt stress greenhouse or growth chamber, importantly, a few field
(Timmusk et al. 2014). Notwithstanding the simplicity experiments with similar results have been reported.
and attractiveness of this mechanism, at the present Although it is not always explicitly stated or even
time, this approach has not been extensively studied. tested for by many researchers, most of the PGPB that
have been studied to date are thought to be rhizospheric
Exopolysaccharides while only a few are likely endophytic. However, more
recently, many researchers have specifically focused
Exopolysaccharides (EPS), high-molecular weight car- their efforts on the roles played by endophytic bacteria
bohydrate compounds attached to the outer surface of in promoting plant growth. This is because while both
bacteria, are responsible for the ability of the bacteria to rhizospheric and endophytic bacteria utilize the same
form biofilms and for the attachment of bacterial cells to mechanisms to promote plant growth, only endophytes
surfaces including plant roots and soil particles. In a are protected from both biotic and abiotic environmental
recent study, scientists isolated and characterized a num- challenge.
ber of PGPB (all pseudomonads) from the rhizosphere Notwithstanding the fact that a particular PGPB
of salt contaminated soils, based on the ability of these strain may perform well in growth chamber or green-
bacteria to produce high levels of EPS and to be salt house studies, this strain may not be suitable for use in
tolerant (Tewari and Arora 2014). One particular strain the field. Thus, for example, many strains of
of Pseudomonas aeruginosa was able to grow in up to P. aeruginosa (see Table 1) have been associated with
12 % salt, produce IAA and siderophores, and facilitate human infections so that there is a real question as to
plant growth in the presence of high levels of salt. whether these strains will be acceptable to regulatory
Following chemical mutagenesis of the bacterium, re- authorities for deliberate release into the environment. In
searchers selected a mutant that produced a significantly addition, it was previously observed (Glick et al., un-
decreased level of EPS, while the amount of IAA and published experiments) that upon characterizing a
siderophores was unchanged. With the decrease in EPS, PGPB strain with a very high level of ACC deaminase
the mutant lost its ability to grow and promote plant activity, the strain turned out to be the human pathogen
growth in the presence of high levels of salt suggesting Bacillus anthracis, an organism that is clearly unsuitable
that with the loss of the EPS barrier, salt readily entered for use in the field as a PGPB.
the bacterium thereby inhibiting its functioning. Further- Many of the PGPB that modulate plant cytokinin,
more, these researchers believe that, notwithstanding the IAA, ethylene or ABA levels may also effect the levels
important role played by EPS, the observed stimulation of other plant hormones so that, given the possibility of
of plant growth came from IAA synthesis. Since this cross-talk between these hormones, it is not a simple
 Plant Soil

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