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REGULAR ARTICLE
Alleviation of salinity stress in plants by
endophyticplant-fungal symbiosis: Current knowledge,
perspectivesand future directions
Sneha Gupta & Martino Schillaci & Robert Walker
&Penelope M. C. Smith & Michelle Watt & Ute
Roessner
Received: 11 February 2020 /Accepted: 22 June 2020# The
Author(s) 2020
Abstract Salinization of soil with sodium chloride ionsinhibits
plant functions, causing reduction of yield ofcrops. Salt tolerant
microorganisms have been studied toenhance crop growth under
salinity. This review de-scribes the performance of endophytic
fungi applied tocrops as a supplement to plant genetics or soil
manage-ment to alleviate salt stress in crops. This is achieved
viainducing systemic resistance, increasing the levels ofbeneficial
metabolites, activating antioxidant systemsto scavenge ROS, and
modulating plant growth phyto-hormones. Colonization by endophytic
fungi improvesnutrient uptake and maintains ionic homeostasis
bymodulating ion accumulation, thereby restricting thetransport of
Na+ to leaves and ensuring a low cytosolicNa+:K+ ratio in plants.
Participating endophytic fungienhance transcripts of genes encoding
the high AffinityPotassium Transporter 1 (HKT1) and the
inward-rectifying K+ channels KAT1 and KAT2, which playkey roles in
regulating Na+ and K+ homeostasis.Endophytic-induced interplay of
strigolactones playregulatory roles in salt tolerance by
interacting with
phytohormones. Future research requires further atten-tion on
the biochemical, molecular and genetic mecha-nisms crucial for salt
stress resistance requires furtherattention for future research.
Furthermore, to designstrategies for sustained plant health with
endophyticfungi, a new wave of exploration of
plant-endophyteresponses to combinations of stresses is
mandatory.
Keywords Endophytic fungi . Biochemical changes .
Ionic homeostasis . Osmoregulation . Hormones .
Salinity . Roots . Soil . Inoculants .Microorganisms
Soil salinity affects agriculture globally
The beginning of the 21st century has been marked byglobal
scarcity of water resources, increased environ-mental pollution and
salinization of soil and fresh water.Two major threats for
agricultural sustainability areincreased human population and
reduction in arableland available for crop cultivation (Shahbaz
andAshraf 2013). Several environmental stresses such ashigh winds,
extreme temperatures, drought, salinity andflood have impacted on
the production and cultivationof agricultural crops. Among these,
soil salinity is one ofthe most significant environmental stresses
resulting inmajor reductions in cultivatable land area, and
decreasedcrop productivity and quality. It is estimated that 50%
ofall arable land will be impacted by salinity by 2050(Shrivastava
and Kumar 2015) and that globally, soilsalinity results in more
than US$12 billion in annuallosses due to reduced crop productivity
(Jägermeyr and
https://doi.org/10.1007/s11104-020-04618-w
Responsible Editor: Boris Rewald
S. Gupta (*) :M. Schillaci :R. Walker :M. Watt :U.
RoessnerSchool of BioSciences, University of Melbourne, Parkville,
VIC,Australiae-mail: [email protected]
P. M. C. SmithCentre for AgriBiosciences, Department of Animal,
Plant and SoilSciences, School of Life Sciences, La Trobe
University,Bundoora, VIC, Australia
/ Published online: 9 July 2020
Plant Soil (2021) 461:219–244
http://crossmark.crossref.org/dialog/?doi=10.1007/s11104-020-04618-w&domain=pdf
-
Frieler 2018). Salinity is recognized as the main threat
toenvironmental resources in several countries, affectingalmost 1
billion ha worldwide, which represents about7% of the earth’s
continental area (Shrivastava andKumar 2015). Consequently, it is
important to under-stand the crop responses to this major soil and
plantstress to minimize economic loss and improve foodsecurity.
Soil is defined as being saline when the electricalconductivity
(EC) of the saturation extract (ECe) in theroot zone exceeds 4 dSm−
1 at 25oC and has an ex-changeable sodium of 15% (w/v).
Salinization also in-cludes excessive accumulation of ions such as
calcium(Ca2+), magnesium (Mg2+), sodium (Na+), sulphates(SO4
2−), and chlorides (Cl−) in the soil, inhibiting plantgrowth and
cellular functions. The most abundant ion inmost salt-affected
soils is Na+ and hence the exchangephase is dominated by Na+. A
secondary process oftenassociated with saline soils is
alkalinisation, creating acondition known as sodicity. This results
in the degra-dation of soil physical properties and porosity,
leadingto reduced water and air flow and increased soil hard-ness
and crusting.
Apart from affecting soil physical properties, highsoil salinity
directly and adversely affects plants- bothnative vegetation and
introduced crops, severely affect-ing seed germination, root
growth, and the physiologicalfunctions of crops (Oster and
Jayawardane 1998). It hasbeen estimated that worldwide 20% of total
cultivatedand 33% of irrigated agricultural land is affected by
highsalinity. This is mainly due to the toxicity of the salt
ionsdirectly on the plant cells but also through generalosmotic
effects of the soil around the roots of the plant.High osmotic
potentials at the soil-root interface reducethe ability of the
plant to absorb water from the soil(Machado and Serralheiro
2017).
Native plants have evolved mechanisms to toleratelow rainfall
and high salinity over hundreds of thou-sands of years (Steffen et
al. 2009). However, in the past200 years, human activities have
intensely disrupted thenatural hydrological balance in many regions
of theglobe. This has resulted in significant consequencesfor the
distribution of salt in all landscapes leading tosevere degradation
of both natural and agricultural en-vironments. It is predicted
that the total area of landaffected by salinity will increase
drastically over thenext few decades if effective solutions are not
imple-mented. These solutions would involve significantchanges to
our present systems of management
including research and development of strategies toimprove salt
tolerance in crops and improve mecha-nisms to mitigate its
consequences (Rengasamy 2002,2006).
Effects of salt stress on above-groundand below-ground organs of
plants
Plants have two major systems, the above-ground or-gans (shoots)
and below-ground organs (roots). Eachsystem has morphological,
physiological and anatomi-cal differences that affect plant
performance differently(Gregory 2007). However, while these two
systemsgrow and function as a separate site for the uptake
ofnutrients and other resources, they are coupled, and
theirfunctions need to form an integrated system. The above-ground
system is highly dependent on the developmentof below-ground organs
and without a sufficiently de-veloped root system, the above-ground
system cannotfully mature (de Willigen and van Noordwijk 1987).
Salinity limits vegetative and reproductive develop-ment by
inducing physiological dysfunctions, and thishas profound
implications on different harvested organssuch as leaf, stem, root,
shoot, fruit or grain. The com-plex phenomenon of tolerance and
response to salt stressinvolves dynamic changes in growth,
physiology, met-abolic pathways and gene expressions (Atkinson
andUrwin 2012; Munns and Tester 2008). Strategies usedto mitigate
against salt stress include proline accumula-tion within cells
(Matysik et al. 2002), modulation ofhormones and accumulation of
glycine betaine andpolyols (Gupta and Huang 2014). They also
involvegeneration of nitric oxide (NO) and compounds to com-bat
formation of reactive oxygen species (ROS). NOdirectly or
indirectly triggers expression of severalredox-regulated genes. NO
also reacts with lipid radicalsthus preventing lipid oxidation,
exerting a protectiveeffect by scavenging superoxide radicals and
formationof peroxynitrite that can be neutralised by other
cellularprocesses. NO also helps in the activation of
manyantioxidant enzymes including catalase (CAT), ascor-bate or
thiol-dependent peroxidases (APX), glutathionereductases (GR) and
superoxide dismutase (SOD).
The effect of salinity on leaf growth, biomass pro-duction and
grain yield on several crops are well docu-mented (Hasanuzzaman et
al. 2013; Munns et al. 2011;Munns and Tester 2008; Sun et al.
2014). The extent towhich plants are damaged by salinity depends on
several
220 Plant Soil (2021) 461:219–244
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factors including species, genotype, plant growth phase,ionic
strength, duration of salinity exposure, composi-tion of salinizing
solution and, most importantly, whichplant organ is exposed (Robin
et al. 2016).
Munns (2005) hypothesized that salinity damage inplants occurs
in two temporal phases. The first phase ofgrowth reduction occurs
rapidly after exposure and isdue to an osmotic effect, while the
second phase, whichis a slower process, is due to the accumulation
of saltions, mainly in older leaves. Early symptoms of thesecond
phase of growth reduction include damage toold leaves and a reduced
photosynthetic capacity(Munns et al. 2006). At the plant organ
level, shootshave been demonstrated to be more sensitive to
salinitythan roots (Munns and Tester 2008). However, roots
areexposed to salinity stress before leaves and can respondrapidly
through changes in elongation (Rahnama et al.2011) and function
(Shelden et al. 2016). The roots arecrucial for a myriad of
physiological processes includ-ing water and nutrient uptake,
preventing toxic sub-stances from reaching photosynthetic tissue,
signal ex-change with shoots, anchoring of plants, and
providingmechanical support to the above-ground organs.
The root-soil interface/ The rhizosphere
Roots and their growing substrate are intrinsically con-nected,
and they mutually influence each other at allstages of plant life
(Gregory 2006). The interface be-tween roots and the soil is a
complex and often ill-defined zone. Compounds are released from
roots intothe surrounding soil matrix resulting in changes to
itschemical and physical properties. The narrow zone ofsoil that
surrounds and is influenced by plant roots isknown as the
rhizosphere. The term rhizosphere wasfirst defined over a century
ago by Hiltner (1904) andrecently, redefined by Pinton et al.
(2007) as the mostdynamic interface on earth that includes soil
influencedby the root, along with the root tissues. The
rhizosphereis home to a vast number of microorganisms (Morganet al.
2005; Pinton et al. 2007), and consists of threedistinct zones: (a)
the endorhizosphere, which includespart of the cortex and
endodermis in which microbesoccupy the apoplastic space; (b) the
rhizoplane, which isthe medial zone immediately next to the root
consistingof the root surface and mucilages; and (c)
theectorhizosphere, which extends from the rhizoplaneout into the
bulk soil (Lynch 1990).
The root system architecture is greatly influenced bysoil
conditions (Rich andWatt 2013), including nutrientgradients and
concentrations of nitrate and phosphorus(Ho et al. 2005; Paterson
et al. 2006). Roots also affectthe surrounding nutrient composition
by the release oforganic compounds that play a vital role in
mineralizingnutrients. The compounds released from the roots
intothe surrounding soil are generally part of rhizodeposits(Jones
et al. 2009), which include a range of substancesfrom sloughed-off
root cells and tissues, mucilages,volatiles, and soluble lysates
and exudates from dam-aged and intact cells (Curl and Truelove
1986; Dakoraand Phillips 2002; Watt 2009). Abiotic factors
influencethe root system (Bekkara et al. 1998; Brimecombe et
al.2000; Groleau-Renaud et al. 1998; Watt and Evans1999) with roots
responding by secreting a differentcombination of compounds to
protect against negativeeffects and encourage positive microbial
interactions(Badri and Vivanco 2009). These secreted
compoundsusually induce an interactive metabolic cross-talk
in-volving diverse biosynthetic networks and pathways.
Root exudates include both secretions (includingmucilage) that
are actively released from the root anddiffusates which are
passively released because of os-motic differences between soil
solution and the rootcells (McNear 2013). Inorganic root exudates
includeions, water, ubiquitous H+ and electrons. Although
theconcentration of inorganic compounds make up far lessof the root
exudate composition compared to organiccompounds but their role is
still significant (Khorassani2008; Uren 2000). Organic compounds
can be classifiedinto high molecular weight compounds, such as
com-plex molecules including polysaccharides secreted byroot cap
cells and epidermal cells at the apical zone, andlow molecular
weight compounds that include arabi-nose, fructose, glucose, amino
acids, organic acids,plant hormones and phenolic compounds (Bertin
et al.2003). Due to the richness of inorganic and organiccompounds
in rhizodeposits, the rhizosphere is hometo specialised microbes
that are able to utilise thesecompounds as an energy source.
Several recent and comprehensive reviews have beenwritten
covering the diversity and activity of microor-ganisms at within
roots and in the rhizosphere, as well asthe functions and effects
of microorganisms in nutrientturnover and supply to the plant
(Garcia et al. 2016;Jacoby et al. 2017; Smith and Smith 2011;
Udvardi andPoole 2013). In the following section, the use of
micro-organisms as one of the key approaches used to alleviate
221Plant Soil (2021) 461:219–244
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abiotic stresses, with the focus on using fungi as a
majorbeneficial microbe will be discussed.
Alleviating salt stress by association with endophyticfungi
Diverse metabolic and genetic strategies used by
plant-associated microbes can reduce the impact of salt stressand
other abiotic stresses arising from extreme environ-mental
conditions (Gopalakrishnan et al. 2015; Singh2014). Induced
Systemic Tolerance (IST) is the termused to describe
microbe-mediated induction of abioticstress responses (Meena et al.
2017). In these beneficialsituations, rhizosphere microorganisms
not only per-ceive and respond to signal molecules secreted by
plantroots, they also release diverse signalling molecules
thatinfluence plants, resulting in increased biotic and
abioticstress resistance or tolerance, as well as root develop-ment
and plant growth (Zhang et al. 2017a). Microbialinteractions with
plants induce several local and system-ic responses that improve
the metabolic capacity ofplants to respond to salt stress (Nguyen
et al. 2016).This microorganisms-based plant biotechnology
hasproven to be more efficient in many cases than plantbreeding and
genetic modification approaches (Smith2014).
Beneficial effects due to plant root interactionswith endophytic
fungi
In recent years the ability of mycorrhizal fungi to
inducetolerance against salt stress in crops has been
documented(Gangwar and Singh 2018) (Fig. 1). In a
mycorrhizalassociation, the fungus colonizes the host plant’s
roottissues, either intracellularly as in arbuscular
mycorrhizalfungi (AMF), or forms extracellular
exchangemechanismsoutside of the root cells, as in ectomycorrhizal
fungi. Thus,mycorrhiza fungi can be categorised as endo- inside
planttissue, or ecto- associated with the external rhizosphere
ornot penetrating root cells. For the purpose of clarity,
thisreview will only focus on endomycorrhizal (termed asendophytic
for this review) fungi.
Penetration and colonisation of plant roots appears tobe
essential for some endophytic fungal strains that arereported to
promote plant growth and provide protectionagainst pathogens. For
example, some species belong-ing to the genus Trichoderma can
colonize local sites(Metcalf and Wilson 2001) on roots, mediated
by
hydrophobins- (Viterbo et al. 2004) and expansin-likeproteins
(Brotman et al. 2008) present in the outermostcell wall layer that
coats the fungal cell surface. Otherrhizosphere-competent
Trichoderma spp. colonize en-tire root surfaces for long periods of
time (Harman 2000;Thrane et al. 1997) or penetrate the epidermis
and thecortex (Yedidia et al. 1999). Once hyphae penetrateroots, a
series of fungal bioactive compounds can beproduced inducing plant
biochemical mechanisms(Harman 2006). The callose-enriched wall
appositionsin the root cell limit the growth of the Trichoderma
spp.to a small area (epidermis and cortex), preventing theentry of
Trichoderma spp. into the vascular stele(Hermosa et al. 2012;
Yedidia et al. 1999). Arbuscularmycorrhiza fungi (AMF) are another
group of endo-phytic fungi. Their hyphae penetrate plant cells,
produc-ing structures that are either balloon-like (vesicles)
ordichotomously branching invaginations (arbuscules) asa means of
nutrient exchange. The fungal hyphae do notin fact penetrate the
protoplast (i.e. the interior of thecell), but invaginate the cell
membrane. Dark septateendophytic (DSE) fungi are also root
endophytes, char-acterized by intense dark pigmentation and the
forma-tion of septate and melanized hyphae and
occasionallymicrosclerotia (Knapp et al. 2015; Yuan et al.
2016).They can be found in plant cortical cells inter-
andintracellularly and are present in several environments(Li et
al. 2019; Santos et al. 2017). In contrast to the vastinformation
on AMF, information on the role of DSEfungi in the ecosystem is
limited.
Colonization of several crops with endophytic fungihas been
reported to induce systemic resistance to path-ogens, mitigate
stress by increasing the levels of protec-tive metabolites and
osmoprotectants, activate antioxi-dant systems to prevent damage
caused by ROS, de-creasing salt induced root respiration and
modulate thephytohormone profile tominimize salt effects on
growthof plants (Ghaffari et al. 2016; Jogawat et al. 2013; Liet
al. 2017; Nia et al. 2012; Rewald et al. 2015; Zhanget al. 2019a).
These effects are in coordinated to im-prove plant growth and
resilience to salinity stress.These ameliorative effects can be
evaluated in terms ofimproved plant growth exhibited by endophyte
colo-nized (ENC) plants in comparison to non-endophytic(NENC)
colonized plants.
Salinity triggers a decrease in stomatal conductance,thus
decreasing the CO2:O2 ratio and increasing photo-respiration
(Kangasjärvi et al. 2012). This causes anincrease in stomatal
resistance to transpiration and an
222 Plant Soil (2021) 461:219–244
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increase in the rate of tissue respiration. Under
theseconditions, photosynthetic capacity is limited, and theplant
uses its own photo-assimilates, resulting in de-creased growth.
Rewald et al. (2015) showed that inNENC Ulmus glabra seedlings
there was a significantincrease in fine root respiration under salt
stress ascompared to their ENC counterparts. This suggestedthat
colonization by endophytic fungi can prevent amajor increase of
root respiration under moderate NaClstress, enabling trees to
deploy more assimilated C forgrowth and, theoretically, improve
defence mechanismsagainst other stress factors occurring in
urbanenvironments.
Endophytic fungi are effective against several rootdiseases
(Azcón-Aguilar and Barea 1997; Borowicz2001) and impart stress
tolerance to plants (Duc et al.2018; Evelin et al. 2019; Yasmeen et
al. 2019),but canalso enhance susceptibility to biotrophic leaf
pathogens(Gernns et al. 2001; Waller et al. 2005). These
endo-phytes have been frequently reported to not only
protectagainst plant pathogens and pests but also impart
strongtolerance against several abiotic stresses in crops(Gangwar
and Singh 2018).
In the past decade, significant progress has been madeto
understand several mechanisms of salt toleranceimparted by
endophytic fungi. In the following sections,
Fig. 1 Potential beneficial effects of root colonisation of
plants byendophytic, symbiotic fungi in saline soil conditions,
summarisedfrom the literature. Salinity results in reduced root
biomass due tosalt-induced inhibition of cell division and affect
the total biomassyield (1) (left). Plant colonized with endophytic
fungi improvesbiomass accumulation by modifying root architecture
and in-creased nutrient absorption (1a) (right). Salt accumulation
createscompetition for nutrient uptake and transport. This results
inimbalance of the ionic composition of plant, affecting
plant’sphysiological traits (2) (left). Endophytic fungi improve
expres-sion of genes and upregulate several cation transporters,
resultingin improved nutrient uptake and maintenance of ionic
homeostasis(2a) (right). Increase of salt in soil lowers soil water
potential
resulting in cellular dehydration (3) (left). Endophytic fungi
negatethis effect by mediating accumulation of osmolytes
consequentlyimproving plant’s water status (3a) (right). Increasing
salinitycauses oxidative stress due to imbalance in reactive oxygen
spe-cies generation and quenching activities of antioxidants (4)
(left).Endophytic fungi improve the antioxidant systems of plants
re-ducing oxidative stress under salt stress (4a) (right). Salt
stresshinders photosynthesis by reducing uptake of magnesium
anddecreasing chlorophyll concentration which eventually
reducescarbon dioxide supply to RuBisCo (5) (left). Endophytes have
apositive effect on photosynthesis under salt stress (5a) (right).
Seetext for relevant references and further details
223Plant Soil (2021) 461:219–244
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current understanding of biochemical and physiologicalchanges
that occur in salt stressed plants inoculated withendophytic fungi
will be covered. This will include ad-vances made recently toward
better understanding of themechanisms that contribute to salt
stress alleviation inENC plants. Finally, gaps in our understanding
of themechanisms will be identified and research challenges tobe
met in future studies will be discussed.
Mechanisms of salt tolerance in ENC plants
Increase in total biomass
Total biomass is usually evaluated as an indicator of theplant’s
ability to tolerate salinity. Several studies havehighlighted that
endophytic fungi impart salinity tolerancein host plants by virtue
of higher biomass as compared toNENC plants. Endophytic fungus
colonization has beendemonstrated to increase biomass in Zea mays
L. (Rhoet al. 2018), soybean (Hamayun et al. 2017),
Vochysiadivergens Pohl (Farias et al. 2019), Solanum
lycopersicum(Azad and Kaminskyj 2016), Brassica juncea (Ahmadet al.
2015), Oryza sativa L. (Saddique et al. 2018) and,Triticum aestivum
L. (Zhang et al. 2019b).
The total biomass can also be assessed by measuringplant
relative growth rate (plant weight increment perplant weight unit).
This includes measurement of the netassimilation rate (NAR) (the
increase in plant weight perleaf area unit), the leaf area ratio
(LAR) and root relativegrowth rate (RGRplant). Balliu et al. (2015)
investigatedthe effects of commercially available AMF
inoculant(Glomus sp. mixture) on growth and nutrient acquisitionin
tomato (Solanum lycopersicum L.) plants grown inmedia with
different levels of salinity. Salinity stressimmediately and
significantly reduced the LAR, NARand RGRplant in NENC as compared
to ENC plants.Similarly, Sallaku et al. (2019) showed that AMF
alle-viates the salinity stress in cucumber plants by
extendingtheir root length and root surface area and even
morethrough enhancing their photosynthetic rate (NAR) ascompared to
NENC plants.
Alteration of root architecture
Root branching and root system architecture play asignificant
role in determining the composition of exu-dates (Badri and Vivanco
2009). Changes in the rootsystem architecture for regulating salt
acquisition and
translocation are crucial for enhancing plant resistanceto salt
stress (Jung and McCouch 2013). Barley plantsexperienced a decline
in primary root growth undersaline conditions due to salt-induced
inhibition of celldivision and elongation of root epidermal cells,
whilesimultaneously stimulating lateral root development(Rahnama et
al. 2011). Endophytic fungi can modulatethe plant’s ability to
modify root architecture (Salope-Sondi et al. 2015; Vahabi et al.
2016). Yun et al. (2018)observed that the length and volume of
roots weregreater in ENC than in NENC maize plants under
salineconditions and similar observations have been reportedin
Hordeum vulgare (Waller et al. 2005) and Oryzasativa L. (Kord et
al. 2019). Improved root systemsenable the plant to utilize water
and minerals fromnon-saline areas until exploitation of areas
affected bysalt cannot be avoided (Jogawat et al. 2013). Thoughfew
studies have shown the ability of endophytic fungito alter root
architecture under saline conditions forbeneficial purposes, much
remains to be investigatedon endophytic fungi influenced root
architecture forbetter water and nutrient uptake in saline
conditions.
Osmoregulation
Upon exposure to saline environments, plants undergo areduction
in water absorbing capacity from the soil,disrupting cell water
relations and inhibiting cell expan-sion. In order to negate these
effects, plants employosmoregulation as a mechanism to tolerate
salt stress(Munns and Tester 2008). This is achieved by
accumu-lation of osmolytes in the form of proline, glycine
beta-ine, sugars, organic acids, polyamines and amino
acidscontributing to osmotic adjustment (Hasegawa et al.2000).
These osmolytes, often termed as compatiblesolutes, are organic
compounds of lowmolecular weightthat are water soluble and
non-toxic at high concentra-tions (Chen and Murata 2011).
Under salt stress, ENC plants have been shown topossess higher
osmotic potential than NENC plants(Contreras-Cornejo et al. 2014)
due to accumulation ofosmolytes (Ahmad et al. 2015; Song et al.
2015) (Fig.2). Osmolytes are also involved in quenching
reactiveoxygen species (ROS), maintaining membrane integri-ty, and
stabilizing enzymes. Osmolytes are also de-scribed as
osmoprotectants (Azad and Kaminskyj2016; Li et al. 2017).
Endophytic symbiosis can influ-ence the concentration and profile
of polyamines andorganic acids in plants (Chen et al. 2019; Zhao et
al.
224 Plant Soil (2021) 461:219–244
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2014). Polyamines help retain ion homeostasis in plantcells by
enhancing the uptake of nutrients and water(Pang et al. 2007).
Organic acids may increase theavailability of nitrogen, phosphorus
and potassium (N,P and K) in soil (Samolski et al. 2012). The role
ofspecific osmolytes in improving salt tolerance is ENCplants are
discussed below.
Proline
Proline is one of the most common osmoprotectants
thataccumulates in plants during salt stress, thereby
ameliorating the negative effects of salinity. Prolinehas been
observed to protect cell walls under osmoticstress, protect protein
integrity and to increase enzymat-ic activity by acting as a
molecular chaperone. Prolinealso has a role in scavenging ROS and
shows singletoxygen quenching ability (Kaur and Asthir 2015).
De-spite these benefits, there are conflicting reports on therole
of endophytic fungi in proline accumulation in saltstressed plants.
Several studies reported increases inproline contents in ENC plants
compared to NENCplants, while others have reported lower proline
contentsin ENC plants (Table 1). Higher proline content in ENC
Fig. 2 Salinity stress induced osmotic stress tolerance
mecha-nisms in plants. Increase in salt in soil lowers the soil
waterpotential of plant cells. This reduces water uptake by plants
andconsequently causes cellular dehydration (1) (left). To combat
thisissue, plants accumulate osmolytes, such as proline, sugars
andpolyamines in higher concentration. Osmolyte accumulation
re-sults in lowering of cellular water potential and maintains
afavourable gradient for water uptake from soil to roots.
Endophytic
fungi alleviate osmotic stress by influencing the expression
ofspecific genes, P5CS, pyroline-5-carboxylate synthase (1a)
(right),involved in the biosynthesis of the osmolyte proline,
activation ofstarch degrading enzyme, glucan-water dikinase (1b)
(right) andforming tripartite symbiosis with roots and rhizobia
(1c) (right) toelevate the accumulation of sugars and by increasing
the biosyn-thesis of polyamines such as spermidine and spermine
(1D) (right).See text for relevant references and further
details
225Plant Soil (2021) 461:219–244
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Tab
le1
Examples
ofstudieson
effectsof
saltstress
andendophyticfungio
nosmoticregulatio
nin
plants
S.N
o.Saltlevel
(mM
NaC
l)Plant
Fungus
Parametersassessed
Effectsof
References
Salin
ityEndophytic
fungio
nsalt
stressed
plants
10,100
Zeamays
Yarrow
ialip
olytica
Shootp
rolin
econtent,total
flavonoid,totalp
henolics,
phytohormoneanalysis
Increased
Controlledtheproductio
nof
proline
Janetal.(2019)
20,100,
200,300
Hordeum
vulgare
Epichloë
brom
icola
Free,solubleconjugated
and
insolubleboundform
sof
polyam
ine(prolin
e),
putrescine,sperm
idineand
sperminecontent
Increasedproline
Proline,Sp
ermidine,total
spermine-
increasedunder
higher
stress
conditions,
Putrescine,freeform
ofspermine-
significantly
decreasedathigher
salt
treatm
ents
Chenetal.(2019)
30,50
Solanum
lycopersicum
Pirifo
rmospora
indica
Shootp
rolin
econtent
Highlyincreased
Significantly
reduced
Abdelazizetal.(2019)
440,100,
175,250
Medicago
truncatula
Pirifo
rmospora
indica
Shootp
rolin
econtent
Contin
ually
enhanced
inlin
ewith
theincreased
saltconcentration
Significantly
increasedthan
un-colonized
plants
Lietal.(2017)
50,100,200
Brassicajuncea
Trichoderm
aharzianum
Oilandprolinecontent,
pigm
ents,enzym
aticassay
Increasedwith
maxim
umaccumulationof
59.12%
at200mM
NaC
l
Furtherincrease
to70.37%
(Ahm
adetal.2015)
60,150
Triticumaestivum
Trichoderm
alongibrachiatu-
m
Water
contentinleaves
and
roots,chlorophyllcontent,
shootp
rolin
econtent
Increased
Highestincrease
win
plants
pretreated
with
fungus
under150mM
NaC
lstress
Zhang
etal.(2016)
70,70,
150,240
Oryza
sativa
Fiveisolates
ofTrichoderm
asp.
Leafwater
content,
chlorophyllcontent,prolin
econtent,mem
brane
stability,lipid
peroxidatio
nandexpression
ofstress
relatedgenes
Increased
Furtherincreased
Raw
atetal.(2016)
80,100,200,
300,400,
500
Triticumaestivum
Pirifo
rmospora
indica
Totalbiom
ass,photosynthetic
pigm
ents,com
patib
lesolutes
Increased
Furtherincreased
Zarea
etal.(2012)
226 Plant Soil (2021) 461:219–244
-
plants has been attributed to – (i) favouring a decline inionic
influx inside cellular masses thus helping plants tomaintain their
osmotic balance; (ii) increasing the ex-pression of the gene
encoding Pyrroline-5-carboxylatesynthase (P5CS) enzyme which is
involved in prolinebiosynthesis; and (iii) increasing activity of
the P5CSenzyme (Rawat et al. 2016). Besides its role as anosmolyte
proline can act as a stress marker. In ENCtomato plants, proline
accumulation was reduced whenthe toxic effects of salinity were
reduced followingcolonization of an endophytic fungus,
Piriformosporaindica (Abdelaziz et al. 2019).
Sugars
In salt stressed plants, the accumulation of total
solublesugars, such as glucose, sucrose, dextrins and
maltose,serves as an osmoprotection as they can stabilize the
cellmembrane and protoplast. These sugars also protectwater soluble
enzymes from high intracellular concen-trations of inorganic ions
(Liang et al. 2018). The syn-thesis of soluble sugars from starch
and sucrose in plantsis upregulated by the activities of sucrose
anabolizingenzymes such as α- and β-amylase, which convertstarch
into dextrins and maltose, respectively (Preiss2018). Sucrose
phosphate synthase and sucrose syn-thase catalyse the synthesis of
sucrose, while β-fructofuranosidase catalyses the breakdown of
sucroseto glucose and fructose (Peng et al. 2016). In plantsgrown
under saline conditions, sucrose undergoes de-composition in order
to meet the requirements for glu-cose (Munns and Tester 2008).
There have been reports that show the role of endo-phytic fungi
in enhancing accumulation of solublesugars in salt stressed plants
(Qi and Zhao 2013; UmaShaanker 2014; Zhang et al. 2019b). These
sugars act aschemoattractant signals to soil rhizobia (el
ZaharHaichar et al. 2014). These chemoattractants can
directmovement to microorganisms in response to chemicalgradients-
a behaviour known as chemotaxis. This che-motactic response of
microorganisms to root exudatesplay key role in initiating
communication between plantroots and microbes. Yang et al. (2015)
reported that thecolonization by Phomopsis liquidambari could
stimu-late sugar secretion from the rhizodeposition ofsloughed off
cells and root debris of rice, thereby pro-viding carbon to the
endophytic fungi. Another study ofP. liquidambari on peanut showed
increased solublesugar contents in leaves. This was due to the
ability of
the fungus to form tripartite symbiotic associations withpeanut
roots and rhizobia. This tripartite associationsignificantly
enhanced peanut nodulation (Zhang et al.2017b). Here, sucrose
derived from photosynthesis wastransported to bacterial inoculated
root nodules and washydrolysed by sucrose synthase into UDP-glucose
andfructose. This was due to the allocation of more carbonby the
endophyte toward peanut and rhizobia symbiontsby increased soluble
sugar content, leading to moreactive nodule carbon metabolism in
ENC plants.
Furthermore, Sherameti et al. (2005) also suggestedthat one of
the major starch-degrading enzymes, glucan-water dikinase,
activated by the fungus in colonizedroots, is responsible for the
increase in soluble sugarsin ENC plants. Similar results were
obtained byGhabooli (2014) with Piriformospora indica increasingthe
level of soluble sugars, including glucose, fructose,and sucrose,
in inoculated plants under salt stressconditions. Recently, Zhang
et al. (2019a) demonstratedthat T. harzianum improved salt
tolerance of cucumberseedlings by enhancing accumulation of sugars.
Thisresults in adjustment of the osmotic potential for
cellularwater retention and turgor maintenance, thereby mini-mizing
the adverse effects of salt stress by balancing thesolute potential
(Bai et al. 2019).
Organic acids
Other important osmolytes in plants are organic acidssuch as
citric acid and malic acid. They are found inplant vacuoles and the
regulation of their metabolismplays a crucial role in providing
tolerance to salt stress(Guo et al. 2010). Fungal endophytes have
been report-ed to induce the release of organic compounds by
theroots (Yang et al. 2015; Zhang et al. 2014), thusinfluencing the
concentrations and profile of organicacids in plants. One of the
major plant nutritional disor-ders associated with increased
salinity in soil is iron (Fe)deficiency. Endophytes can enhance Fe
acquisition bytheir host through their ability to secrete organic
acidswhich chelate and solubilise iron in the soil (Chen et
al.1998; Khan et al. 2006). A study by Zhao et al.
(2014)demonstrated that the release of organic acids
fromendophytes, resulted in ferric solubilization to formorganic
ferric salts that can be assimilated directly byplants under saline
conditions. It has also been shownthat ENC plants have better
nutrient uptake capacity anddistribution within plant tissues due
to modulation of theroot architecture and nutrient availability in
the soil.
227Plant Soil (2021) 461:219–244
-
These benefits are imparted by increases in organicacids
produced by ENC plants (Samolski et al. 2012;Zhao et al. 2014).
Limited research has been done onunderstanding the mechanisms
underlying the changesin organic acids in ENC plants, thus this
topic calls forfurther investigation.
Polyamines
Polyamines (PA) are low molecular weight nitrogenousaliphatic
molecules that participate in physiological pro-cesses such as
activation of antioxidant systems, cellgrowth and development, and
in cellular osmoregula-tion in plants under salt stress (Singh et
al. 2018). PAalso regulate ion channels, either by direct binding
or viaPA-induced signalling molecules (ROS and NO). PAsalso
regulate the activity of ion channels indirectly bymembrane
depolarization. The hyperpolarization-activated Ca2+ influx and the
NO-induced release ofintracellular Ca2+ result in a higher
cytoplasmic Ca2+
concentration, which is a major component in generalstress
responses such as stomatal movements (Wani2018; Williams 1997).
They are either present in free,soluble conjugated (covalently
conjugated with smallmolecules such as phenolic acids) or insoluble
(boundwith macromolecules such as proteins, DNA and RNA)forms.
These compatible solutes accumulate under saltstress and include
putrescine (Put, diamine), spermidine(Spd, triamine) and spermine
(Spm, tetramine)(Minocha et al. 2014; Todorova et al. 2013).
Differences in PA (Put, Spd, Spm) responses undersalt-stress
have been reported in several species (Singhet al. 2018) and it
remains unclear which polyamineplays the major role in imparting
salt tolerance. Chenet al. (2019) demonstrated that the putrescine
contentwas significantly reduced in ENC plants compared toNENC
plants in high stress conditions whereasspermidine and spermine
content showed the oppositepattern. It was suggested that salinity
stress toleranceinduced by endophytic fungus Epichloë bromicola
cor-related with enhanced conversion of putrescine tospermidine and
spermine. The fungus also convertedthe free forms and soluble
conjugated forms of poly-amines to insoluble bound forms of
polyamines.
Modulation of the polyamine pool to help toleratesalt stress by
arbuscular mycorrhizal fungi (AMF) iswell explored (Evelin et al.
2009). However, researchon polyamine metabolism during the
interactions be-tween endophytic fungi and plants under salt stress
is
underrepresented and many questions remain unan-swered. For
example, most plant polyamine researchrelates to changes in free
polyamines, and where poly-amine conjugates have been measured,
substantialchanges have been detected. The precise role of
poly-amines, free or conjugated, in ENC plants remains un-clear.
Further investigations, focusing on
understandingendophyte-facilitated modulation of polyamines,
in-cluding the intracellular localization of free polyaminesand
conjugates associatedwith salt tolerance in plants, isneeded.
Already some of the key genes involved in thebiosynthetic pathways
have been cloned making it pos-sible to manipulate polyamine
metabolism using molec-ular genetic approaches (Malmberg et al.
1998). Hence,genetic manipulation of polyamine levels in ENC
plantsmay allow valuable insights into the role of these com-pounds
especially in studies of plant tolerance to saltstress.
Nutrient acquisition and ionic homeostasis
High salt (Na+ and Cl−) in the soil disturbs
nutrientavailability by imposing competition during
uptake,translocation or distribution within the plant. This
maysuppress nutrient associated activities resulting in unde-sired
ratios of Na+:K+, Na+:Ca2+, and Ca2+:Mg2+
(Munns et al. 2011). This in turn results in imbalanceamong
ionic composition of the plant subsequentlyaffecting plants
physiological traits (Hasegawa et al.2000; Munns et al. 2006).
However, endophytic symbi-osis has been shown to improve
assimilation of nutrientsand assist in maintenance of ionic
homeostasis in hostplants grown in saline conditions (Table 2).
Although the effects of AM fungi on plant nutrientacquisition
are commonly discussed based on the dif-ferences of nutrient
concentration in plant tissues, therelative uptake rate of nutrient
elements (RUR) hasrecently been suggested as a better tool to
distinguishthe differences among treatments over a short period,
asthe nutrient concentration could be largely influencedby the
dilution effect of fast growth in young plants.Balliu et al. (2015)
found that RUR values of ENCtomato plants grown in both non-saline
and moderatesaline conditions were higher than in
non-inoculatedseedlings. Similarly, another study showed the
en-hancement effect of AMF inoculation on the nutrientuptake
capacity of cucumber seedlings after salt stress(Sallaku et al.
2019).
228 Plant Soil (2021) 461:219–244
-
Tab
le2
Examples
ofstudieson
theeffectsof
salinity
andendophyticfungio
nnutrient
concentrationandionicratio
sin
plants
S.
No.
Saltlevel(m
MNaC
l)Plant
Fungus
Parametersassessed
Effectsof
References
Salin
ityEndophytic
fungio
nsalt
stressed
plants
10,140
Cucum
issativus
Phomaglom
erata
LWL2
and
Penicilliumsp.
LWL3
Na+,K
+,C
a2+,M
gcontent
Significantincreases
inNa+
and
decreasesin
K+,M
g2+and
Ca2
+levels
Significantly
higher
levelsof
K+,M
g2+andCa2
+ions,
particularly
incase
ofPenicillium
sp.and
P.g
lomerataandinhibitthe
uptake
ofNa+
Waqas
etal.(2012)
20,100,200
Zeamays
Pirifo
rmospora
indica
Na+,K
+content
IncreasedNa+
inrootsand
shoots,K
+in
shootsand
decreasedK+in
roots
Significantd
ecreased
levelsof
Na+
andK+in
rootsand
increase
inshoots
Yun
etal.(2018)
30,75,100
Arabidopsis
thaliana
Pirifo
rmospora
indica
Transcriptlevelsof
several
genesknow
nto
encode
proteins
involved
inNa+
and
K+homeostasisandthe
abiotic
stress
markergene
relativ
eto
DesiccationA
(RD29a)
Increased-
expression
ofthe
stress
markergene,R
D29a,
expression
levelo
fAtHKT1,
K+contentinrootsand
shoots,D
ecreased
Na+
contentinrootsandshoots
Decreased-expression
ofthe
stress
markergene,R
D29a,
furtherdecrease
inNa+
content,Fu
rtherincreased
expression
levelo
fAtHKT1,
andK+content
Abdelazizetal.
(2017)
40,100
Arabidopsis
thaliana
Trichoderm
avirens
andTrichoderm
aatroviride
Na+
content
Decreased
Na+
contentinroots
FurtherdecreasedNA+content
inroots
Contreras-Cornejo
etal.(2014)
50,150,300,450,
600
Hordeum
vulgare
Epichloe
Na+,C
,P,N
,K+content,C:N,
C:P,N
a+:K
+,N
:Pratio
sIncreasedNa+,N
,PandK+
contents,ionicratios,no
significanteffectonCcontent
FurtherincreasedN,P
andK+
contents,N
:Pratios;
Decreased
C:N,C
:P,N
a+:K
+
ratio
s
Song
etal.(2015)
60,100,300
Hordeum
vulgare
Pirifo
rmospora
indica
Na+,K
+,C
a2+,ionicratio
sIncreasedNa+,C
a2+,D
ecreased
K+:Na+,C
a2+:Na+
ratio
sIncreasedK+,K
+:Na+,
Ca2
+:Na+,D
ecreased
Na+
content
Ghabooli(2014)
70,50,100,150
Loliu
marundinaceum
Neotyphodium
coenophialum
Na+,K
+,C
a2+,and
Mg2
+
contentinleaves,rootsand
sheath
Atlow
ersaltconcentration-
inleaves,decreased
K+,sim
ilar
Na+,C
a2+unaffected;in
sheath,decreased
K+,similar
Na+andCa2
+
Ath
ighersaltconcentration-
inleaves,decreased
Na+,sim
ilar
K+,M
g2+unaffected
Atlow
ersaltconcentration-
inleaves,increased
K+,sim
ilar
Na+,C
a2+unaffected;in
sheath,increased
K+,similar
Na+andCa2
+
Ath
ighersaltconcentration-
inleaves,increased
Na+,sim
ilar
K+,
Mg2
+increasedatall
concentrations
Yin
etal.(2014)
229Plant Soil (2021) 461:219–244
-
Phosphorus
Phosphorus (P) and nitrogen (N) are two of the mostimportant and
essential elements for plant growth withcrucial roles in cell
function and metabolism (Uchida2000). Increased salt in soil
occludes P to plants due toits precipitation with other cations (de
Aguilar et al.1979), thereby creating soil-induced P deficiency
inplants. This affects the normal growth of the plant andcauses
older leaves to die prematurely (Niu et al. 2012).Increased P
acquisition in ENC plants under salineconditions is attributed to
(i) increased availability ofphosphates in soil due to the
conversion of insolublephosphates into soluble forms through the
process ofacidification, chelation and exchange reactions; (ii)
abil-ity of endophytic fungi to absorb P at lower thresholdsowing
to the expression of a high affinity Pi transporter,PiPT, and (iii)
ability of endophytic fungi to interactwith diverse rhizobacteria
which have inorganicphosphate-solubilizing capabilities by virtue
of produc-tion of a variety of organic acids and acid
phosphatases(Johri et al. 2015; Meena et al. 2010; Ngwene et
al.2016; Singh et al. 2009; Srividya et al. 2009; Swethaand
Padmavathi 2016). This effective P uptake in ENCplants aids in
transporting absorbed phosphorus toleaves, prompting plant growth;
increasing absorptionof nutrients and biomass accumulation (Wu et
al. 2019),consequently alleviating the adverse effects of
salinity.
Nitrogen
Nitrogen plays a crucial role in cell function and metab-olism
(Chokshi et al. 2017). Plants absorb N as nitrate(NO3
−), ammonium (NH4+) ions, and also as organic
compounds such as amino acids and peptides (Rentschet al. 2007;
Tegeder and Rentsch 2010) but absorption iscompromised by salinity
due to N immobilisation. Ni-trate reductase (NR, E.C.1.6.6.1)
catalyses reduction ofNO3
− to NO2− and its activity is nitrate-inducible. The
NR activity is the limiting step in the conversion ofNO3
− to amino acids (Campbell 1999). Nitrate reductaseactivity in
leaves is largely dependent on nitrate fluxfrom roots
(Ferrario-Méry et al. 1998) and is severelyaffected by osmotic
stress induced by NaCl (Baki et al.2000). A number of reports have
shown that endophyticfungal colonization assists in N uptake under
stressconditions (Khan et al. 2011a; Sherameti et al. 2005;Song et
al. 2015). Recruitment of N in endophyticinteractions differs from
mycorrhizal interactions in
which the fungus preferentially recruits ammoniumrather than
nitrate from the soil (Boukcim and Plassard2003; Gage 2004). Song
et al. (2015) showed that inENC plants, N content increased in both
the shoots androots with increasing salt concentrations. The
funguswas suggested to be involved in the cell’s antioxidantand
ROS-scavenging enzymes where N is an essentialcomponent (Cabot et
al. 2014; Khan et al. 2014). An-other study by Sherameti et al.
(2005) showed a signif-icant increase in growth of ENC plants that
was pro-posed to be associated with a stimulation of the
NADH-dependent NR, the key enzyme of nitrate assimilation
inplants.
Na+:K+ ratio
Increased levels of Na+ in cells impairs important bio-chemical
mechanisms required for plant growth andsurvival. Sodium
accumulation alters cellular Na+:K+
ratios thereby reducing the availability of K+ that isrequired
for activity of various enzymes and for theregulation of osmotic
pressure and stomatal closure.Increased Na+ also competes with K+,
disrupting cellu-lar metabolism in roots and leaf tissues
(Abdelaziz et al.2017). This eventually increases the Na+:K+ ratios
in thecytosol, and subsequently disrupts enzyme activity, pro-tein
synthesis, turgor maintenance, photosynthesis andstomatal movement
(Evelin et al. 2019).
High Na+:K+ ratios in plants indicate higher levels ofstress.
Hence, plants must maintain low levels of Na+ tobe able to resist
the deleterious effects of salinity. ENCplants consistently have
lower Na+:K+ ratios thanNENC plants under saline conditions. Reza
Sabzalianand Mirlohi (2010) demonstrated that the toxic effect
ofNa+ was mitigated in grasses inoculated with endophyt-ic fungi by
increasing K+ concentration and thus main-taining the Na+:K+ ratio
in plants. Similar results werefound by Song et al. (2015) and
Alikhani et al. (2013)where endophytic fungi modulated ion
accumulation incolonized barley plants by decreasing the foliar
Na+:K+
ratio. Restricting the transport of Na+ to leaves andensuring a
low cytosolic Na+:K+ ratio are importantways plants can increase
their tolerance to high saltlevels (Berthomieu et al. 2003; Cuin et
al. 2003). In-crease of K+ concentration is also related to
mechanismsthat control turgor pressure (Beckett and Hoddinott1997).
Song et al. (2015) also showed that the lowerNa+:K+ ratios observed
in ENC plants decreased thelevel of toxic ions and osmotic
influence on plants under
230 Plant Soil (2021) 461:219–244
-
salt stress. Another study on barley plants inoculatedwith
endophytic fungi showed a decreased Na+:K+ ratiocompared to
uninoculated plants, indicating that thisratio is a reliable
indicator of the severity of salt stress,or for screening plant
genotypes for high Na+ tolerance(Ghabooli 2014) (Table 2).
Plants control Na+ homeostasis through a variety ofmembrane
proteins, antiporters, nonspecific cationchannels, Na+ and K+
transporters, vacuolar ATPasesand aquaporins, and the plasma
membrane (PM)(Grabov 2007). Recently, Abdelaziz et al. (2017)
pos-tulated a molecular basis of establishing a balanced
ionhomeostasis of Na+:K+ ratio in ENC plants. InoculatedArabidopsis
plants had enhanced transcript levels of thegenes encoding the high
Affinity Potassium Transporter1 (HKT1) and the inward-rectifying K+
channels KAT1and KAT2, which play key roles in regulating Na+ andK+
homeostasis. Subsequently, lower Na+:K+ ratioswere confirmed in the
Arabidopsis line gl1-HKT:AtHKT1;1 that expresses an
additionalAtHKT1;1 copy driven by the native promoter. Thisstudy
demonstrated that endophytic colonization pro-motes plant growth
under saline conditions by modulat-ing the expression level of the
major Na+ and K+ ionchannels, which helps in the establishment of a
balancedion homeostasis of Na+ and K+ under salt stress condi-tions
(Abdelaziz et al. 2017).
Oxidative stress
Salt stress (osmotic and ionic stress) also interferes
withproper cellular functions of plants due to enhancedproduction
of ROS, which can lead to oxidative damagein several cellular
components such as lipids, proteinsand DNA (Gupta and Huang 2014).
ROS consist of agroup of chemically reactive oxygen molecules such
ashydroxyl radical (OH-), H2O2, O2
− and O2− and areproduced as a result of interrupted pathways in
plantmetabolism that cause transfer of high energy electronsto
molecular oxygen (Gill and Tuteja 2010). Broad hostrange endophytic
fungi can confer effective tolerance toROS under abiotic stress
conditions such as salinity(Mastouri et al. 2010; Rodriguez et al.
2008). (Redmanet al. 2011); Singh et al. (2011) reported that
exposure tohigh salt conditions caused ROS accumulation in toma-to,
rice, panic grass, and dunegrass without endophyticassociations,
whereas the ENC plants had decreasedROS accumulation through
various pathways (Fig. 3).
Plants have two ways to counteract the adverse con-sequences of
ROS, mainly enzymatic and non-enzymatic antioxidative systems. The
enzymatic systemincludes catalase (CAT), ascorbate peroxidase
(APX),superoxide dismutase (SOD), glutathione reductase(GR),
dehydroascorbate reductases (DHAR) andmonodehydroascorbate
reductases (MDHAR). Thenon-enzymatic antioxidant system consists of
ascorbicacid (AsA), glutathione (GSH), carotenoids
andosmoprotectants that play roles in quenching toxic by-products
of ROS.
Baltruschat et al. (2008) reported increased activityof CAT,
APX, GR and DHAR in the root tissues ofbarley under saline
conditions. Increased activity ofDHAR was seen in P. indica
colonized barley leadingto detoxification of ROS and an enhanced
ratio ofascorbic acid to neutralize oxygen free radicals (Foryerand
Noctor 2000). Azad and Kaminskyj (2016) usedH2O2 localization as a
proxy to assess accumulation ofROS and showed that ENC plants had
lower H2O2levels in their leaves following NaCl-stress,
confirmingthe role of endophytes to reduce stress-induced
ROSgeneration.
Also, Zhang et al. (2016) reported that ENC plantshad higher
SOD, peroxidase (POD) and CAT activitysuggesting that the
coordination of POD and CAT ac-tivity along with SOD activity
played a central protec-tive role in the O2
− and H2O2 scavenging process inENC plants (Ahmad et al. 2015).
Increased activity wasa result of increased expression of the genes
encodingthe enzymes (Zhang et al. 2016). Under saline condi-tions,
endophytic colonization also increases the con-centrations of
non-enzymatic antioxidant moleculessuch as AsA, GSH and carotenoids
in plants as shownby several studies (Jan et al. 2019; Jogawat et
al. 2013;Prasad et al. 2013; Waller et al. 2005).
Salinity increases the level of lipid peroxidation(Hernández
2019; Yu et al. 2020) which results inhigher membrane permeability
and loss of ions fromthe cells (Gupta and Huang 2014). NaCl
treatment ofENC plants resulted in higher rates of lipid
peroxidationin salt-sensitive plants than in salt-tolerant plants
sug-gesting that the rate of lipid peroxidation can be used asan
indicator to measure how effectively ENC plantscope with salt
stress (Baltruschat et al. 2008). Anotherstudy showed that ENC
plants contained higher ascor-bate concentrations in roots compared
with NENCplants, while the ratio of ascorbate to
dehydroascorbatewas not significantly altered and CAT, APX, GR,
231Plant Soil (2021) 461:219–244
-
DHAR and MDHAR activities were increased. Thesechanges were
consistent with the decrease of leaf lipidperoxidation observed in
these experiments (Walleret al. 2005). Similar results were shown
by Mastouriet al. (2010) and Zhang et al. (2001) where ENC
plantshad significantly reduced accumulation of lipid perox-ides
than cont rol p lan ts under sa l t s t ress .Malondialdehyde
(MDA), a product of lipid peroxida-tion, is generally regarded as
an indicator of free radicaldamage to cell membranes caused by
oxidative stress.
Zhang et al. (2016) reported that salt stressed ENCplants had a
15% reduction in MDA compared to saltstressed NENC plants. Table 3
lists some of the studiesreporting changes in lipid compositions
due to endo-phytic symbiosis in salt stressed plants.
Photosynthesis
Salt stress hinders photosynthesis resulting in an enor-mous
loss in crop productivity (Sudhir and Murthy
Fig. 3 Oxidative stress tolerance mechanisms in salt
stressedplants. Increase in salinity causes oxidative stress in
plants due toredox imbalance between ROS (reactive oxygen species)
andantioxidants. This results in molecular and cellular damage
andmembrane peroxidation eventually disturbing the normal
function-ing of the cell. Several antioxidant enzymes are induced
to combatsalt stress including catalyse (CAT), ascorbate peroxidase
(APX),superoxide dismutase (SOD), peroxidase (POX), glutathione
reductase (GR), dehydroascorbate reductase (DHAR)
andmonodehydroascorbate reductase (MDHAR). Ascorbate
(AsA),glutathione (GSH) and carotenoids are non-enzymatic
antioxi-dants that are produced to counteract the adverse
consequencesof salt stress. In endophyte colonized (ENC) plants,
the tolerancemechanism in reinforced by activating an efficient
antioxidantsystem that abates the oxidative damage caused due to
salt stress
232 Plant Soil (2021) 461:219–244
-
Tab
le3
Examples
ofstudieson
theeffectsof
salin
ityandendophyticfungio
nlip
idperoxidatio
nin
plants
S.N
o.Saltlevel
(mM
NaC
l)Plant
(Fam
ily)
Fungus
Param
etersassessed
Effectsof
References
Salin
ityEndophytic
fungio
nsalt
stressed
plants
10,100,
200,300
Oryza
sativa
Pirifo
rmospora
indica
Totalsolubleproteins,lipid
peroxidatio
n(m
easuredthiobarbitu
ricacid
reactiv
esubstances
inshootsandroots),free
prolinecontent,andenzyme
antio
xidants(catalase(CAT:
EC1.11.1.6),glutathionereductase(GR:
EC1.6.4.2),superoxide
dism
utase(SO
D:E
C1.15.1.1),
ascorbateperoxidase(A
PX:E
C1.11.1.11))activ
ity
Increasedlip
idperoxidatio
n,SO
D,A
PX,C
AT,G
R;
Decreased
totalsoluble
proteins,freeproline
content
Increasedtotalsoluble
proteins,prolin
e,further
increase
inSOD,A
PX,
CAT,G
R;D
ecreaseinlip
idperoxidatio
n
Bagherietal.
(2013)
20,100
Glycine
max
Fusarium
verticillioides
Lipid
peroxidatio
n,antio
xidant
enzyme
analysis,gibberellins,A
BA,salicylic
acid
IncreasedABA,S
A,lipid
peroxidatio
n;Decreased
CAT,S
OD,P
OD,S
A,
ABA
IncreasedCAT,S
OD,P
OD;
Decreased
lipid
peroxidatio
n,ABA,S
Asignificantly
Radhakrishnan
etal.(2013)
30,100
Glycine
max
Fusarium
verticillioides
andHum
icola
sp
Protein
content,catalase
activ
ity,A
BA
content,SA
content,lip
idperoxidatio
n(m
easuredin
term
sof
malondialdehyde-M
DAcontent)
IncreasedABA,S
A,lipid
peroxidatio
n;Decreased
CAT,S
OD,P
OD,S
A,
ABA,lipid
peroxidatio
n
Significant
three-fold
reductionin
MDAlevel,
ABA,S
A;Increased
CAT,
SOD,P
OD
Radhakrishnan
etal.(2015)
40,100,
175,250
Medicago
truncatula
Pirifo
rmospora
indica
Proline,MDA,S
odium
ion,
antio
xidant
enzymes
IncreasedMDA,N
A+in
shoots,slig
htincrease
inprolinecontent;Decreased
POD,S
OD,C
AT
Highestincreasedin
proline
contentw
ithincrease
inPOD,S
OD,C
AT;
decreasedMDA,N
A+in
shoots
Lietal.(2017)
50,200
Cucum
issativus
Trichoderm
aharzianum
Antioxidant
enzymes,K
+content,
K+/Na+
ratio
,Na+
content,ethylene
levels,M
DAlevelsas
ameasure
oflip
idperoxidatio
n
IncreasedMDAlevels,N
a+
content,ethylene
levels;
Decreased
antio
xidant
enzymes,K
+content,
K+/Na+
ratio
Improved
activ
ities
ofantio
xidant
enzymes,
increasedK+content,
K+/Na+
ratio
;decreased
Na+
content,ethylene
levels,M
DAlevels
Zhang
etal.
(2019a)
233Plant Soil (2021) 461:219–244
-
2004). Salt stress has been shown to degrade D1 and D2proteins
of the photosystem II reaction centre. Theseproteins play crucial
roles in protein phosphorylationcoupled with the flow of electrons
(Jansen et al. 1996).Salt stress also results in decreased
photosynthetic pig-ments by reducing the activity of enzymes that
synthe-size them. Osmotic shock resulting from salt stress leadsto
reduced leaf area and decrease in stomatal and meso-phyll
conductance (Chaves et al. 2009). This limits CO2availability and
assimilation which consequently affectsRuBisCO (Seemann and
Critchley 1985). DecreasingCO2 assimilation also increases the risk
of the accumu-lation of electrons in thylakoid membranes and
predis-poses the photosynthetic apparatus to increased
energydissipation. Thus, to dissipate this energy, photosystemII
loses excess electrons causing injury to photosynthet-ic tissues
and affecting the net photosynthetic rate(Redondo-Gómez et al.
2010).
Plants can protect the photosystems from light in-duced
inhibition and damage in several ways such asminimizing harvesting
of light and dispersion of excessenergy by non-photochemical
quenching (NPQ) (LimaNeto et al. 2015). An increase in NPQ can
limit quantumyield (Baker 2008) but ENC plants are reported to
havelower NPQ, therefore symbiosis enhances photosynthet-ic
efficiency by proficient conversion of harvested lightinto chemical
energy and minimizing NPQ (Pehlivanet al. 2017). Endophytic fungi
are also known to rein-force these mechanisms and reduce the
negative effectsof salinity on plant photosynthetic capacity
(Jogawatet al. 2013; Molina-Montenegro et al. 2018). Table 4lists
some of the studies in the last decade on effect ofsalinity and
endophytes on photosynthesis in plants.Endophytic symbiosis combats
the negative effects ofsalt stress on photosynthesis in several
ways. ENCplants have shown improved water status resulting inlarger
leaf area and higher stomatal conductance andeventually better
assimilation of carbon dioxide (Zareaet al. 2012).
Magnesium (Mg) is one of the essential macronutri-ents for plant
growth and is involved in numerousphysiological and biochemical
processes such as photo-synthesis, enzyme activation and synthesis
of nucleicacids ad proteins (Chen et al. 2018). It is the central
atomof the tetrapyrrole ring of chlorophyll a and bmolecules,which
are the major pigments for photosynthetic lightabsorption
(Wilkinson et al. 1990). Salt reduces uptakeof Mg2+ thus also
reducing the concentration of chloro-phyll in leaves (Sudhir and
Murthy 2004). ENC plants
maintain higher chlorophyll concentration by improvingthe uptake
ofMg2+ (Jogawat et al. 2013; Yin et al. 2014)and this leads to
maintenance of plastid integrity andenhanced photosynthetic
efficiency (Johnson et al.2014).
Another way in which endophytes induce defencesystems in plants
under saline conditions is by upregu-lating the
ascorbate-glutathione (ASH-GSH) cycle; forexample Kumar et al.
(2012) described that during saltstress, the endophytic fungus P.
indicamaintains a highantioxidative environment by defence system
priming,especially the ascorbate–glutathione (ASH–GSH) cycleleading
to maintenance of plastid integrity and thereforeenhanced
photosynthetic efficiency in colonised plantsduring abiotic stress
(Johnson et al. 2014). ENC plantsalso confer the benefit of
maintaining the integrity ofphotosystem II by repairing
salt-induced degradation ofD1/D2/Cytb 559 complex by the
accumulation of gly-cine betaine in ENC plants (Rivero et al.
2014). Glycinebetaine is also known to stabilise PSII
pigment-proteincomplexes and protect the activities of RuBisCO
andrubisco activase enzymes responsible for fixing CO2 inAM fungi
(Talaat and Shawky 2014).
Hormonal regulation
Induction of phytohormones is also one of the strategiesplants
use to mitigate abiotic stresses that ultimatelyenhance plant
growth and productivity in stressful envi-ronments (Ryu and Cho
2015). Phytohormones, oftenregarded as plant growth regulators, are
compounds thatare derived from plant biosynthetic pathways
actingeither locally or via transport to other sites within
theplant to mediate growth, development and nutrient allo-cation
(Peleg and Blumwald 2011). These includeabscisic acid (ABA),
gibberellins (GA), ethylene(ETHY), cytokinins (CKs),
brassinosteroids (BRs) andauxins, particularly indole acetic acid
(IAA). To initiatesuitable plant responses to environmental
stimuli, thereis interplay between these hormones to modulate
bio-chemical and physiological processes (Saeed et al.2017).
It is known that some strains of endophytic fungi canproduce
plant hormones, especially gibberellins (GAs),to help the plant to
tolerate or avoid abiotic stress(Contreras-Cornejo et al. 2009;
Khan et al. 2011b; Wal-ler et al. 2005). Hamayun et al. (2010)
reported thatinoculation with the endophytic fungi Phoma
herbarumshowed increased plant biomass and elevated
234 Plant Soil (2021) 461:219–244
-
Tab
le4
Examples
ofstudieson
theeffectsof
salin
ityandendophyticfungio
nphotosynthesisin
plants
S.No.
Saltlevel(m
MNaC
l)Plant
Fungus
Param
etersassessed
Effectsof
References
Salin
ityEndophytic
fungionsalt
stressed
plants
10,200,300
Oryza
sativa
Pirifo
rmospora
indica
Photosyntheticpigm
ent
content[chlorophyll
(Chl)a,Chl
b]
Decreased
Increased
Jogawatetal.
(2013)
20,50,150
Lactucasativa(lettu
cevar.Rom
aine)
andSolanum
lycopersicum
(tomato
var.Moneymaker)
Colobanthus
quitensis
(AFE001)
and
Descham
psia
antarctica(AFE002)
The
netp
hotosynthesis
rate(A
),and
transpirationrate
(EC),water
use
efficiency
(WUE)for
photosynthesisas
the
ratio
between
photosyntheticrate
andtranspiration
(A/EC)
Decreased
Amax,
WUE
Significantly
increased
Amax,W
UE
Molina-Montenegro
etal.(2018)
30,100,200,300,400,
500
Triticumaestivum
Pirifo
rmospora
indica
andAzospirillum
spp.
Photosynthetic
pigm
ents(Chl
a,b,
ab)
Decreased
Significantly
increased
with
inoculationof
both
organism
s
Zarea
etal.(2012)
40,300,500
Solanumlycopersicum
Fusariumculmorum
Photosystem
II(PsII)
efficiency
Decreased
Increased
Azadand
Kam
inskyj
(2016)
235Plant Soil (2021) 461:219–244
-
production of active GAs including GA1, GA3, GA4,and GA7 in
salt-stressed soybean. Similar results wereshown by Waqas et al.
(2012), where salt-stressed cu-cumber plants inoculated with
Penicillium sp. had largershoot growth and plant biomass that was
attributed tothe secretion of bioactive GAs. A study on
salt-stressedcucumber plants inoculated with Trichodermaasperellum
Q1 alleviated the suppression effects of saltstress by altering the
phytohormone levels (IAA, GAand ABA) and the phosphate
solubilization ability (Leiand Zhang 2015). Three bioactive GAs,
i.e. GA4, GA9and GA12 were more abundant in ENC plants grownunder
salt stress compared to NENC plants (Khan et al.2011c), and this
mitigated the adverse effects of salinityand improved growth.
Endophytic symbiosis under saline conditions has apositive
influence on the endogenous concentration ofauxins
(Contreras-Cornejo et al. 2009). Contreras-Cornejo et al. (2014)
evaluated the expression of theauxin-responsive marker gene
DR5:uidA which wasupregulated in ENC plants compared to their
counter-parts under saline conditions speculating that, by
pro-viding auxins, Trichoderma spp. could restore auxinhomeostasis
and, consequently growth and develop-ment could be normalized when
grown under salt stress.
Perspectives and future directions
Evolution has led to complex interactions between awide
diversity of microorganisms and plants; many ofthem resulting in
the establishment of a symbiotic rela-tionship between them
(Hassani et al. 2018). Theseinteractions beneficially impact plant
survival, biodiver-sity, fitness and ecosystem function (Bai et al.
2018;Rosier et al. 2016; Sasse et al. 2018). Growing
evidenceindicates that endophytic associations can also be
im-portant for plant fitness, development of the immunesystem,
tolerance to abiotic stresses, nutrient acquisitionand disease
suppression (Hiruma et al. 2016; Khan et al.2015; Khare et al.
2018; Soliman et al. 2015; Terhonenet al. 2016; Zuccaro et al.
2014). This review highlightssome of the numerous mechanisms by
which endophyt-ic symbiosis promotes salt tolerance in plants.
However,there are several challenges and issues that future
re-search should address for comprehensive understandingof these
mechanisms. It is well established how osmoticadjustment in plants
under salt stress via enhanced ac-cumulation of osmolytes is
achieved using endophyticsymbiosis. However, the biochemical,
molecular and
genetic mechanisms are largely unexplored. Therefore,there is a
need to understand these phenomena by in-vestigating genes encoding
enzymes used for the syn-thesis of molecules that are crucial for
salt stress resis-tance. Therefore, dedicated research into
unravelling themolecular basis of osmolyte accumulation in
ENCplants will broaden our understanding of the mecha-nisms
involved.
In recent years, new compounds, such as polyamines,and
strigolactones have been implicated in improvingplant tolerance to
salt stress (Fahad et al. 2015).Strigolactones (SL) play regulatory
roles to combatabiotic stress, including salinity, and in order to
be fullyeffective, they need to modulate and interact with
otherphytohormones, especially auxin and ABA. SLs arealso involved
in several aspects of plant development;suppression of secondary
branches in shoots, regulationof leaf senescence, stimulation of
internode length andinduction of endophytic symbiosis (de Saint
Germainet al. 2013; Lopez-Raez et al. 2017; Yamada et al.2014).
This group of sesquiterpene lactones is responsi-ble for hyphal
branching and successful colonisationwithin roots by producing
5-deoxy-strigol, followed bythe formation of a pre-penetration
apparatus (Genreet al. 2005). Recently, SL secreted by roots
ofArabidopsis thaliana was found to act as a signal mol-ecule for
colonization of endophytic Mucor sp.(Rozpądek et al. 2018). Studies
on auxin and ABAinvolvement with endophytes under salt stress has
beenexplored, but further research is required to investigatethe
role of strigolactones secreted by ENC plants inameliorating salt
stress.
The root is the primary location in plants that sensessalt
stress. The PM constitutes the interface between acell and its
surroundings and plays an important role incell wall biosynthesis,
ion transport, endocytosis, sens-ing of environmental stimuli, and
cellular signal trans-duction (Mansour et al. 2015). PM lipids and
proteins insalt tolerant plants are protected from oxidative
attackthrough enhanced antioxidant systems, a mechanismthat
minimizes lipid and protein oxidation whileretaining PM integrity
(Mansour 2013). Though lipidperoxidation has been elucidated in ENC
plants undersalt stress, lipid metabolism in the PM in root tissues
isyet to be investigated. Hence future research that eval-uates how
endophytic symbiosis influences thesechanges under saline
conditions is warranted.
Limited studies are available to understand the role
ofendophytic fungi in modifying the photosynthetic
236 Plant Soil (2021) 461:219–244
-
capacity of plants to alleviate the negative effects ofsalinity
as described in previous sections. Salt stresshas been shown to
degrade proteins of the PSII reactioncentre. These proteins play
fundamental roles in phos-phorylation of proteins (Jansen et al.
1996). Studies inthe past have focused on understanding how
AMFsymbiosis acts to maintain the integrity of PSII showingthe
upregulation of the genes encoding these proteinsunder salt stress
(Chen et al. 2017). However, researchon maintenance of these
proteins by endophytic fungiunder salt stress is a field to
explore.
Metabolomics is increasingly being utilized for gen-erating deep
insights into abiotic stress responses. Sev-eral studies have
focused on exploring and discoveringcompounds that stimulate ENC
plant growth by allevi-ating stress using various technologies
(Chetia et al.2019; Kusari and Spiteller 2012; Mazlan et al.
2019;Tawfike et al. 2018). However, molecular signallingmechanisms
employed by endophytic fungi under salineconditions are yet to be
explored. The high-throughputmass spectrometric profiling of
cellular metabolites ofplant-associated endophytes under the
influence of saltstress could help to reveal the level of
interference by thestressor in overall cellular homeostasis. Thus,
future‘omics-based research is required to generate compre-hensive
information on specific plant-endophytic fungi-salt stress systems
to resolve facts behind precise mech-anisms of stress tolerance in
crop plants.
Although this review covers mechanisms and strate-gies employed
by plants under salt stress, in nature plantsoften face multiple
biotic and abiotic stresses instead of asingle stress. These
combinations of stresses exert morecomplex effects on plant fitness
which eventually resultsin potential differences from the responses
elicited undersingle stresses. (Bai et al. 2018) demonstrated that
tomatodeveloped integrated responses via genetic componentsand
cross-talk of signalling pathways under combinedsalinity and
pathogen stresses. This shows that plantsmust have evolved to
mitigate a combination of stresses.Addressing specific questions
related to multiple stressessuch as how beneficial microorganisms
and pathogens orcombined abiotic stresses interact would facilitate
thedesign of strategies for sustained plant health under di-verse
environmental stresses.
In conclusion, directing future research on endophyt-ic
symbiosis under salinity in order to understand theabove-mentioned
challenges will help improve ourknowledge and understanding of the
mechanisms ofendophyte facilitated salinity tolerance in host
plants.
Acknowledgements SG thanks the University ofMelbourne
forproviding the Melbourne Research Scholarship for
financialassistance.
Open Access This article is licensed under a Creative
CommonsAttribution 4.0 International License, which permits use,
sharing,adaptation, distribution and reproduction in anymedium or
format,as long as you give appropriate credit to the original
author(s) andthe source, provide a link to the Creative Commons
licence, andindicate if changes were made. The images or other
third partymaterial in this article are included in the article's
Creative Com-mons licence, unless indicated otherwise in a credit
line to thematerial. If material is not included in the article's
Creative Com-mons licence and your intended use is not permitted by
statutoryregulation or exceeds the permitted use, you will need to
obtainpermission directly from the copyright holder. To view a copy
ofthis licence, visit
http://creativecommons.org/licenses/by/4.0/.
References
Abdelaziz ME, Kim D, Ali S, Fedoroff NV, Al-Babili S (2017)The
endophytic fungus Piriformospora indica enhancesArabidopsis
thaliana growth and modulates Na+/K+ homeo-stasis under salt stress
conditions. Plant Sci 263:107–115
Abdelaziz ME, Abdelsattar M, Abdeldaym EA, Atia MA,Mahmoud AWM,
Saad MM, Hirt H (2019) Piriformosporaindica alters Na+/K+
homeostasis, antioxidant enzymes andLeNHX1 expression of greenhouse
tomato grown under saltstress. Sci Hort 256:108532
Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John
R,Egamberdieva D, Gucel S (2015) Role of Trichodermaharzianum in
mitigating NaCl stress in Indian mustard(Brassica juncea L.)
through antioxidative defense system.Front Plant Sci 6:868
Alikhani M, Khatabi B, Sepehri M, Nekouei MK, Mardi M,Salekdeh
GH (2013) A proteomics approach to study themolecular basis of
enhanced salt tolerance in barley(Hordeum vulgare L.) conferred by
the root mutualisticfungus Piriformospora indica. Mol Biosyst
9:1498–1510
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic
andabiotic stresses: fromgenes to the field. J ExpBot
63:3523–3543
Azad K, Kaminskyj S (2016) A fungal endophyte strategy
formitigating the effect of salt and drought stress on plantgrowth.
Symbiosis 68:73–78
Azcón-Aguilar C, Barea J (1997) Arbuscular mycorrhizas
andbiological control of soil-borne plant pathogens–an overviewof
the mechanisms involved. Mycorrhiza 6:457–464
Badri DV, Vivanco JM (2009) Regulation and function of
rootexudates. Plant Cell Environ 32:666–681
Bagheri AA, Saadatmand S, Niknam V, Nejadsatari T, BabaeizadV
(2013) Effect of endophytic fungus, Piriformosporaindica, on growth
and activity of antioxidant enzymes of rice(Oryza sativa L.) under
salinity stress. Int J Adv Biol BiomedRes 1:1337–1350
Bai Y, Kissoudis C, Yan Z, Visser RG, van der Linden G
(2018)Plant behaviour under combined stress: tomato responses
tocombined salinity and pathogen stress. Plant J 93:781–793
237Plant Soil (2021) 461:219–244
https://doi.org/
-
Bai X, Dai L, Sun H, Chen M, Sun Y (2019) Effects of
moderatesoil salinity on osmotic adjustment and energy strategy
insoybean under drought stress. Plant Physiol Biochem
139:307–313
Baker NR (2008) Chlorophyll fluorescence: a probe of
photosyn-thesis in vivo. Annu Rev Plant Biol 59:89–113
Baki GAE, Siefritz F, Man HM, Weiner H, Kaldenhoff R, KaiserW
(2000) Nitrate reductase in Zea mays L. under salinity.Plant Cell
Environ 23:515–521
Balliu A, Sallaku G, Rewald B (2015) AMF inoculation
enhancesgrowth and improves the nutrient uptake rates
oftransplanted, salt-stressed tomato seedlings.
Sustainability7:15967–15981
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B,Gullner
G, Janeczko A, Kogel K-H, Schäfer P,Schwarczinger I, Zuccaro A,
Skoczowski A (2008) Salttolerance of barley induced by the root
endophytePiriformospora indica is associated with a strong
increasein antioxidants. New Phytol 180:501–510
Beckett R, Hoddinott N (1997) Seasonal variations in tolerance
toion leakage following desiccation in the moss Atrichumandrogynum
from a KwaZulu-Natal afromontane forest. SAfr J Bot 63:276–279
Bekkara F, Jay M, Viricel MR, Rome S (1998) Distribution
ofphenolic compounds within seed and seedlings of two Viciafaba cvs
differing in their seed tannin content, and study oftheir seed and
root phenolic exudations. Plant Soil 203:27–36
Berthomieu P, Conéjéro G, Nublat A, Brackenbury WJ, LambertC,
Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F,Simonneau
T, Essah PA, Tester M, Véry A-A, Sentenac H,Casse F (2003)
Functional analysis of AtHKT1 inArabidopsis shows that Na+
recirculation by the phloem iscrucial for salt tolerance. EMBO J
22:2004–2014
Bertin C, Yang X, Weston LA (2003) The role of root exudatesand
allelochemicals in the rhizosphere. Plant Soil 256:67–83
Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter
plant–pathogen relations? Ecology 82:3057–3068
Boukcim H, Plassard C (2003) Juvenile nitrogen uptake
capacitiesand root architecture of two open-pollinated families of
Piceaabies. Effects of nitrogen source and ectomycorrhizal
sym-biosis. J Plant Physiol 160:1211–1218
BrimecombeMJ, De Leij FA, Lynch JM (2000) The effect of
rootexudates on rhizosphere microbial populations. In: RobertoP,
Zeno V, Paolo N (eds) The Rhizosphere: Biochemistryand Organic
Substance at the Soil-Plant Interface. MarcelDekker, New York, pp
95–141
BrotmanY, Briff E, ViterboA, Chet I (2008) Role of swollenin,
anexpansin-like protein from Trichoderma, in plant root
colo-nization. Plant Physiol 147:779–789
Cabot C, Sibole JV, Barceló J, Poschenrieder C (2014)
Lessonsfrom crop plants struggling with salinity. Plant Sci
226:2–13
Campbell WH (1999) Nitrate reductase structure, function
andregulation: bridging the gap between biochemistry and
phys-iology. Annu Rev Plant Biol 50:277–303
Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis
underdrought and salt stress: regulation mechanisms from wholeplant
to cell. Ann Bot 103:551–560
Chen TH, Murata N (2011) Glycinebetaine protects plants
againstabiotic stress: mechanisms and biotechnological
applications.Plant Cell Environ 34:1–20
Chen L, Dick WA, Streeter JG, Hoitink HA (1998) Fe chelatesfrom
compost microorganisms improve Fe nutrition of soy-bean and oat.
Plant Soil 200:139–147
Chen J, Zhang H, Zhang X, Tang M (2017) Arbuscular mycor-rhizal
symbiosis alleviates salt stress in black locust throughimproved
photosynthesis, water status, and K+/Na+ homeo-stasis. Front Plant
Sci 8:1739
Chen ZC, PengWT, Li J, Liao H (2018) Functional dissection
andtransport mechanism of magnesium in plants. Semin CellDev Biol
74:142–152
Chen T, Li C, White JF, Nan Z (2019) Effect of the
fungalendophyte Epichloë bromicola on polyamines in wild
barley(Hordeum brevisubulatum) under salt stress. Plant Soil
436:29–48
Chetia KD, Bharali B. Ojha S, Barkataki MP, Saikia D, Singh
T,Mosahari PV, Sharma P, Bora U (2019) Exploring the ben-efits of
endophytic fungi via omics. In: Singh BP (ed)Advances in Endophytic
Fungal Research. Springer, NewYork, pp 51–81
Chokshi K, Pancha I, Ghosh A, Mishra S (2017)
Nitrogenstarvation-induced cellular crosstalk of ROS-scavenging
an-tioxidants and phytohormone enhanced the biofuel potentialof
green microalga Acutodesmus dimorphus. BiotechnolBiofuels 10:60
Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos
C,López-Bucio J (2009) Trichoderma virens, a plant
beneficialfungus, enhances biomass production and promotes
lateralroot growth through an auxin-dependent mechanism
inArabidopsis. Plant Physiol 149:1579–1592
Contreras-Cornejo HA, Macías-Rodríguez L, Alfaro-Cuevas
R,López-Bucio J (2014) Trichoderma spp. improve growth
ofArabidopsis seedlings under salt stress through enhanced
rootdevelopment, osmolite production, and Na+ elimination
throughroot exudates. Mol Plant-Microbe Interact 27:503–514
Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003)
Potassiumactivities in cell compartments of salt-grown barley
leaves.J Exp Bot 54:657–661
Curl EA, Truelove B (1986) The Rhizosphere.
Springer-Verlag,Berlin
Dakora FD, Phillips DA (2002) Root exudates as mediators
ofmineral acquisition in low-nutrient environments. Plant
Soil245:35–47
de Aguilar CA-G, Azcón R, Barea J (1979) Endomycorrhizalfungi
and Rhizobium as biological fertilisers for Medicagosativa in
normal cultivation. Nature 279:325
de Saint Germain A, Ligerot Y, Dun EA, Pillot J-P, Ross
JJ,Beveridge CA, Rameau C (2013) Strigolactones stimulateinternode
elongation independently of gibberellins. PlantPhysiol
163:1012–1025
de Willigen P, van Noordwijk M (1987) Roots, plant productionand
nutrient use efficiency. PhD thesis, WageningenUniversity &
Research. Netherlands
dos Santos SG, da Silva PRA, Garcia AC, Zilli J, Berbara
RLL(2017) Dark septate endophyte decreases stress on riceplants.
Braz J Microbiol 48:333–341
Duc NH, Csintalan Z, Posta K (2018) Arbuscular mycorrhizalfungi
mitigate negative effects of combined drought and heatstress on
tomato plants. Plant Physiol Biochem 132:297–307
el Zahar Haichar F, Santaella C, Heulin T, Achouak W (2014)Root
exudates mediated interactions belowground. Soil BiolBiochem
77:69–80
238 Plant Soil (2021) 461:219–244
-
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungiin
alleviation of salt stress: a review. Ann Bot 104:1263–1280
Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation
ofsalinity stress in plants by arbuscular mycorrhizal
symbiosis:current understanding and new challenges. Front Plant
Sci10:470
Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S,Hassan
S, Shan D, Khan F, Ullah N, Faiq M, Khan MR,Tareen AK, Khan A,
Ullah A, Ullah N, Huang J (2015)Phytohormones and plant responses
to salinity stress: a re-view. Plant Growth Regul 75:391–404
Farias GC, Nunes KG, Soares MA, de Siqueira KA, Lima WC,Neves
ALR, de Lacerda CF, Filho EG (2019) Dark septateendophytic fungi
mitigate the effects of salt stress on cowpeaplants. Braz J
Microbiol 51:243–253
Ferrario-Méry S, Valadier M-H, Foyer CH (1998) Overexpressionof
nitrate reductase in tobacco delays drought-induced de-creases in
nitrate reductase activity and mRNA. Plant Physiol117:293–302
Foryer C, Noctor G (2000) Oxygen processing in
photosynthesis:regulation and signaling. New Phytol 146:359–388
Gage DJ (2004) Infection and invasion of roots by
symbiotic,nitrogen-fixing rhizobia during nodulation of temperate
le-gumes. Microbiol Mol Biol Rev 68:280–300
Gangwar O, Singh AP (2018) Trichoderma as an efficaciousbioagent
for combating biotic and abiotic stresses of wheat-A review. Agric
Rev 39:49–54
Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty P-E (2016)Take
a trip through the plant and fungal transportome ofmycorrhiza.
Trends Plant Sci 21:937–950
Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG
(2005)Arbuscular mycorrhizal fungi elicit a novel intracellular
ap-paratus in Medicago truncatula root epidermal cells
beforeinfection. Plant Cell 17:3489–3499
Gernns H, Alten H, Poehling H-M (2001) Arbuscular
mycorrhizaincreased the activity of a biotrophic leaf pathogen–is
acompensation possible? Mycorrhiza 11:237–243
Ghabooli M (2014) Effect of Piriformospora indica inoculationon
some physiological traits of barley (Hordeum vulgare)under salt
stress. Chem Nat Compd 50:1082–1087
Ghaffari MR, Ghabooli M, Khatabi B, Hajirezaei MR, SchweizerP,
Salekdeh GH (2016) Metabolic and transcriptional re-sponse of
central metabolism affected by root endophyticfungus Piriformospora
indica under salinity in barley. PlantMol Biol 90:699–717
Gill SS, Tuteja N (2010) Reactive oxygen species and
antioxidantmachinery in abiotic stress tolerance in crop plants.
PlantPhysiol Biochem 48:909–930
Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney
RK,GowdaCL, Krishnamurthy L (2015) Plant growth promotingrhizobia:
challenges and opportunities. 3 Biotech 5:355–377
Grabov A (2007) Plant KT/KUP/HAK potassium transporters:single
family–multiple functions. Ann Bot 99:1035–1041
Gregory PJ (2006) Roots, rhizosphere and soil: the route to a
betterunderstanding of soil science? Eur J Soil Sci 57:2–12
Gregory PJ (2007) Plant Roots: Growth, Activity and
Interactionswith the Soil. Blackwell, London
Groleau-Renaud V, Plantureux S, Guckert A (1998) Influence
ofplant morphology on root exudation of maize subjected to
mechanical impedance in hydroponic conditions. Plant
Soil201:231–239
Guo L, Shi D, Wang D (2010) The key physiological response
toalkali stress by the alkali-resistant halophyte
Puccinelliatenuiflora is the accumulation of large quantities of
organicacids and into the rhyzosphere. J Agron Crop Sci
196:123–135
Gupta B, Huang B (2014) Mechanism of salinity tolerance
inplants: physiological, biochemical, and molecular
character-ization. Int J Genomics 2014:701596–701596
Hamayun M, Khan SA, Khan AL, Rehman G, Kim Y-H, Iqbal I,Hussain
J, Sohn E-Y, Lee I-J (2010) Gibberellin productionand plant growth
promotion from pure cultures ofCladosporium sp. MH-6 isolated from
cucumber (Cucumissativus L.). Mycologia 102:989–995
Hamayun M, Hussain A, Khan SA, Kim H-Y, Khan AL, WaqasM, Irshad
M, Iqbal A, Rehman G, Jan S, Lee I-J (2017)Gibberellins producing
endophytic fungus PorostereumspadiceumAGH786 rescues growth of salt
affected soybean.Front Microbiol 8:686
Harman GE (2000) Myths and dogmas of biocontrol changes
inperceptions derived from research on Trichoderma harzinumT-22.
Plant Dis 84:377–393
Harman GE (2006) Overview of mechanisms and uses ofTrichoderma
spp. Phytopathology 96:190–194
HasanuzzamanM, Nahar K, Fujita M (2013) Plant response to
saltstress and role of exogenous protectants to mitigate
salt-induced damages. In: Ahmad P, Azooz MM, Prasad MNV(