Running Title:AM Fungi for Salinity Stress

Arbuscular Mycorrhizal Fungi---alleviator for salinity stress: A review

Muzafar H. DAR1*, Syed M. RAZVI2, Narender SINGH1, Ahmad MUSHTAQ2 and Shahnawaz DAR3
1
Department of Botany, Kurukshetra University Kurukshetra, Haryana, 136119 (India)
2
Department of Plant Breeding and Genetics Sher-e KashmirUniversity of Agricultural Sciences and Technology of
Kashmir 190025(India)
3
KVK Kargil 11 and High Altitude Research and Extension Station Zanskar, Science Sher-e Kashmir University of
Agricultural Sciences and Technology of Kashmir 190025(India)

ABSTRACT
Salinity stress is considered one of the most harmful environmental stresses as it decreases over 20% irrigated
land crop production globally. Hence, it is imperative to develop salt-tolerant crops in addition to understanding various
mechanisms enabling the plant growth under saline stress conditions. Recently, a novel biological approach, “plant-
microbe interaction” (PMI) such as arbuscular mycorrhizal (AM) fungi, gained momentum as it aimed at addressing the
salinity stress. Arbuscular mycorrhizal fungi colonize the plant root systems and modulate the plant growth in multiple
ways. It has been observed that most land plant roots are colonized by AM fungi. During this process AM fungi obtain
their main nutrients from the involved plants while mineral nutrients including N, P, K, Ca, and S are provided to the
host plant. During the past few decades, broader understanding has advanced towards multifunctional role of AM fungi,
particularly, in the mediation of mineral nutrients and alleviation of stress, especially salt stress, in most crop plants. In
soil-plant systems these can increase uptake of root phosphorus as well as confer augmented tolerance to salinity with a
consequent enhanced growth and yield. Despite the evident anti-stress role and mechanisms described separately, need
arises to discuss and analyze these together. Therefore, the present review addresses the major role of AM fungi in
mitigating salt stress and their beneficial effects on plant growth and productivity. In addition, the mechanisms AM
fungi employ to amplify the salt tolerance of host plants by increased nutrient accession (phosphorus, nitrogen, calcium)
physiological changes (efficiency of photosynthesis, permeability of cell membranes, water status, and nitrogen
fixation), and biochemical changes (inducing the accumulation of different osmolytes like proline, soluble sugars and
antioxidants) will be discussed. Furthermore, the review highlights the role of AM fungi on main antiporter Na +/H+).
The AM fungi inoculation improves osmotic adjustment by accumulation of compatible solutes such as proline, soluble
sugars and antioxidants. In plants, this inoculation increases the activity of multiple antioxidant enzymes including
superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase stress. In addition, the AM alleviates the salt-
induced APX), and peroxidase (POD), thereby scavenging the reactive oxygen species (ROS) generated under salt
deleterious effects by regulating the osmotic balance of the Na +/K+ ratio through maintaining the lesser Na+ and K+
under salt stress conditions. Further research is necessary to gather in-depth knowledge on arbuscular AM fungi-
associated mechanisms to pave a way for large-scale application of these fungal associations under saline stress
conditions, with the main aim of building a healthy, eco-friendly, cost-effective, and sustainable agricultural system.
Key Words: arbuscular mycorrhiza, biochemical and physiological changes, osmolytes,plant-microbe interaction,
sodium accumulation, salt stress

Citation：Muzafar H. DAR, Syed M. RAZVI, Narender SINGH, Ahmad MUSHTAQ, and Shahnawaz DAR .2022.
Arbuscular mycorrhizal fungi---alleviator for salinity stress: A Review. Pedosphere. 32.

INTRODUCTION

An increase in the concentration of salts in the soil, soil salinity, is becoming a significant problem
worldwide, as it is prevailing in all the climates. Among the various salts present in the soil, sodium chloride
(NaCl) is the most prevalent one. Almost 7% of the earth’s land surface has become saline prone (Ruiz-
Lozano et al., 2001) and increased salinization of arable land will result in 50 % land loss within the next 25
years, and up to 50 % by the middle of the twenty-first century (Porcel et al., 2012). It is estimated that about
one billion hectares (ha) traversing more than 100 countries encounter soil salinity problems Food and
Agriculture Organization (FAO, 2015). Likewise, from 1.5 billion ha of cultivated land present around the
world, approximately 77 million hectares (5%) are affected by excess salt content (Sheng et al., 2008).

*
Corresponding author. E-mail: mhussaunidar@gmail.com.
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Current literature sources clearly describe the severe impacts of soil salinization on plant growth,
productivity, and on the crop yield. Recently it has been reported that soil salinization caused a total loss of
US$27.3 billion, with a direct impact on the global economy (Meena et al., 2017). The main causal factors
contributing to increasing soil salinization of cultivable land are excessive use of synthetic chemical
fertilizers, use of groundwater for irrigation purposes and flood irrigation practices which finally transform
fertile soil into saline soil and decrease about 20% of crop productivity (Munns and Gilliham, 2015).
High salt deposition (salinity) shows adverse effects on germination, growth, and reproduction of plants
which subsequently leads to huge losses in productivity (Giri et al., 2003;Chinnusamy et al., 2005;Mathur et
al., 2007). Salinity has become major abiotic stress and has been reported to cause the following severe
impacts: (a) decrease plant growth including seed germination, vegetative development, and reproductive
development (Hasanuzzaman et al., 2013), (b) impair photosynthetic process by decreasing leaf expansion,
leaf area index and raise the production of reactive oxygen species (ROS), ROS-mediated damage to cell
organelles, plasma membrane proteins and lipids (Hashem et al., 2014; Ahmad et al., 2018), (c) detrimental
impact of salinity stress is the accumulation of Na+ and Cl- ions in the cells of plants and causes severe ion
imbalance and physiological drought (Feng et al., 2002). Disturbed ion homeostasis impairs various
physiological and biochemical processes in plants (Munns, 2002).
Plants in their native environment are colonized by a wide range of microorganisms that influence their
morphological, physiological, biochemical, and molecular mechanisms to survive the changing environment
(Ruiz-Lozan et al., 2012; Auge et al, 2014). However, these adaptive strategies become inefficient to cope
with the soil salinity. Arbuscular mycorrhizal (AM) fungi are pervasive among a wide array of soil
microorganisms colonizing the root and can improve plant performance under stress environments and,
consequently, increase the yield of plants (Creus et al., 1998; Smith and Red, 2008). The AM fungi form a
symbiotic association with both terrestrial as well as aquatic plants, and nearly 80% of all terrestrial plants
including most crop species can develop this mutualistic association (Willis et al., 2013). In this respect,
biological processes such as mycorrhizal application to mitigate negative salt stress impact would be a more
favorable choice. The AM fungi have been shown to promote the growth of plant (Fig. 1) and salinity
tolerance by employing numerous mechanisms such as amplifying nutrient accession, modulating the
physiological and biochemical properties of the host plant (Al-Karaki and Al-Raddad, 1997) (Table I).
Extensive research reports that AM leads to enhanced plant growth and yield under salinity stress conditions
(Kapoor et al., 2013; Abdel Latef and Chaoxing, 2014). These advantages of AM have prompted it to be a
suitable successor for bio-amelioration of saline soils. Applied research utilizing these improved AM fungi
and associated microorganisms to improve plant- fungi symbiosis of modern crop production systems has the
potential to increase the yield and crop quality of a wide range of economically valuable plant species
(Martino and Crawford, 2021).

Table I
Role of AM fungi under salinity stress conditions
Plant AM Fungal species Salinity levels Effect of AM fungi References
species
Cucumis Funneliformis mosseae 0-100 mM NaCl Enhanced nutrient uptake, stand establishment rate, and Sallakua et al., 2019
sativus photosynthetic rate
Glomus versiforme 0 mmol/L and 100 Elevated levels of antioxidant enzymes (SOD, POD, Ahmad et al., 2018
mmol/L NaCl CAT) and lower uptake of Na+

Trigonella Glomus monosporum 0, 75 and 150 mM Enhanced growth, proline, and antioxidant enzymes and Metwally and
foenum- NaCl phosphatase Abdelhameed, 2018
graecum
Triticum Rhizophagus irregularis NaCl levels (0, 1 Increased leaf area, stomatal density, stomatal Zhu et al., 2018
Aestivum and 2 g kg−1 dry conductance (gs) and maximum rate of gs to water
soil) vapour (gsmax), and leaf water potential
Glomus mosseae 0 and 150 mM Increased total phenol, proline content, leaf area, shoot Tofighi et al.,
NaCl and root dry weights, and lengths 2017
Rhizophagus irregularis 0, 9.5 and Increased plant dry weight; stomatal conductance, Zhu et al., 2016
19.0 dS m−1 NaCl density, size, and aperture; higher soluble sugar
concentration; and K+:Na+ ratio, C assimilation, and N
uptake
Medicago Funneliformis mosseae 1.4, 7 and 12 Increased K+, K+:Na+, and Ca+2:Na+ Namdari et al., 2018
sativa dS/m Nacl
Capsicum Glomus irradicans 0, 25 and 50 mM Increased total fresh and dry weight, chlorophyll a and Hegazi et al., 2017
annuum NaCl b concentrations, antioxidant content expressed as total
soluble phenols and proline concentrations, relative
water content, and decreased membrane permeability
Cajanus Funneliformis mosseae and 0-100 nM NaCl Improved plant biomass and reduced oxidative burst by Pandey and Garg, 2017
cajan Rhizophagus irregularis strengthening antioxidant enzymatic activities

Plant species AM Fungal species Salinity levels Effect of AM fungi References

Ocimum Glomus deserticola 0.64 dS m−1 5 dS m−1 Increased chlorophyll content and water use Elhindi et al.,

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 basilicum 10 dS m−1 efficiency K, P and Ca, K/Na, and Ca/Na 2017
Solanum Rhizophagus 0 mM NaCl Increased K+ concentration, K+:Na+ ratio Khalloufia et al.,
Lycoper- irregularis 100 mM NaCl cytokinins, indoleacetic acid and abscisic acid 2017
sicum concentrations
Oscimum Glomus mosseae, 0 mM NaCl, 75 mM Increased in proline accumulation Shekoofeh et al., 2012
basilium Glomus NaCl and 100 mM
intraradices NaCl
Cucurbita Glomus 1 and 35 mM NaCl Enhanced relative water content Colla et al., 2008
pepo intraradices
Lupinus Glomus etunicatum, 250 nM NaCl Increased proline, glycine betaine, sugars and
termis Glomus increased the activities of key antioxidant Hashem et al.,
intraradices and enzymes like superoxide dismutase (SOD), 2016
Glomus mosseae catalase (CAT), ascorbate peroxidase (APX),
and peroxidase (POD)
Cicer Funneliformis 0-100 mM NaCl Enhanced nodulation and nitrogen fixation Garg and Singla,
arietinum mosseae 2016

Different research studies on various plant species have shown that AM fungi inoculation promotes
plant salinity tolerance by enhancing multiple processes including photosynthesis, nutrient absorption,
antioxidant defense, and osmolyte accumulation, which eventually leads to improved growth performance
and enhanced plant salinity tolerance. The present review paper will cover various mechanisms (nutrient
uptake, biochemical and physiological mechanisms) employed by AM symbiosis in host plants for
alleviating salt stress which is discussed in the following sections.

SALINITY TOLERANCE BY AM THROUGH NUTRIENT UPTAKE AND IONIC BALANCE

Phosphorus

Under salt stress conditions, plant growth and development suffer grossly, because of the non-
availability of mineral nutrients and expenditure of most energy adenosine tri phosphate (ATP) in
counteracting the toxic effects of accumulated salts. However, AM symbiosis under these conditions has
been found to increase the strength of the host plant by improving its growth and related traits. More
attention has been paid to the role of mycorrhizal fungi in releasing essential macronutrients such as growth-
limiting nutrients like N and P from organic compounds (Read, 1991). The extent to which AM fungi
colonization benefits the uptake of plant nutrients is also influenced by traits of root physiology and
morphology (Navarro-Fernandez et al., 2016). Several research studies have revealed that plants inoculated
with AM grow better as compared to non-inoculated plants under salt stress environments (Sannazzaro et al.,
2007, Zuccarini and Okurowska, 2008). It has been observed that mycorrhizal Acacia nilotica seedlings had
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higher root as well as shoot dry weight as compared to non-mycorrhizal seedlings (Hajiboland et al., 2010).
Al-Karaki (2000) reported that mycorrhizal tomato plants had a higher shoot and root dry weight, fruit
weight, and fresh fruit yield than a non-mycorrhizal tomato plants. Improved growth, yield, water status,
nutrient content, and fruit quality were reported in Cucurbita pepo plants colonized by Glomus
intraradices under salinity stress conditions (Colla et al. 2008). The enhanced growth of AM plants under
saline stress conditions is mainly related to the mycorrhiza-mediated enhancement of plant host nutrient
acquisition, especially of P nutrition (Plenchette and Duponnis, 2005). Garg and Chandal, (2011) observed
that chickpea plants inoculated with Glomus mossease accumulated higher shoot and root biomasses when
compared to non-inoculated chickpea plants.
AM has been shown to have a positive impact on the mineral nutrient composition, especially for the
poor mobility nutrients like P of plants under salt stress conditions by increasing selective uptake of those
nutrients (Al-Karaki and Clark, 1998). This whole process is regulated by the supply of nutrients to the root
system and enhanced absorption by AM (Sharifi et al., 2007). Soil nutrient absorption, especially phosphorus
absorption, gets reduced because of the formation of phosphate ions with Ca 2+, Mg2+, and Zn2+ and finally
becomes unavailable to plants under a saline stressed environment (Azcon et al., 1979), thereby creating salt-
induced P deficiency in plants. So solubilisation of P is essential for plant growth which in turn may be
helpful in salt stress mitigation by overcoming the binding capacity of P to the soil (Cantrell and Lindermann,
2001).
The increased phosphorus acquisition in AM plants is facilitated by an extensive hyphal network of
fungal partners which allows greater soil volume exploration than non-mycorrhizal plants (Ruiz-Lozano and
Azcon, 2000). A research study has revealed that mycorrhizal Acacia nilotica plants have higher P content (1.
2, 1.2, 0.9, and 0.6%) than non-mycorrhizal Acacia nilotica plants (0.6, 0.5, 0.2, and 0.1%) at different levels
of salinity (1.2, 4, 6.5 and 9.5 dSm-1) in saline soils (Giri et al., 2007). It has been observed that phosphorus
concentration in shoots of mycorrhizal Trifoliumalexandrium plants was higher (0.68, 0.62, and 0.47 mgg-1)
than shoots of nonmycorrhizal Trifoliumalexandrium plants under different soil salinity levels (2.2, 5, and 10
dSm-1) (Shokri and Maadi, 2009). The higher concentration of P in all mycorrhizal plants at various levels of
salinity suggests that AM enhanced uptake of P under saline conditions. This increased P nutrition in AM-
inoculated plants in saline conditions may positively increase their growth rate, antioxidant production in
legume plants (Feng et al., 2002; Alguacil et al., 2003; Garg and Manchanda, 2008). Enhanced P uptake in
mycorrhizal plants, grown under saline conditions, may decrease the negative impact of Na+ and Cl- ions by
maintaining the integrity of the vacuolar membrane, which promotes compartmentalization within vacuoles
and selective uptake of ions, as a result preventing ions from interfering in metabolic pathways of growth
(Rinaldelli and Mancuso, 1996). Thus, keeping these facts in consideration, it is evident that AM fungi
reduce the adverse effects of salinity by preserving the integrity of cell membrane; reducing leakage of ions;
by selective ion uptake.

Nitrogen

Nitrogen is among the abundantly utilized plant nutrients that is absorbed by plants in the form of
nitrate NO32- and ammonium (NH4+) ions. However, soil salinity negatively influences nitrogen acquisition
and utilization by influencing various stages of N metabolism (Frechill et al., 2001). Plant growth is affected
by a limited supply of soil nitrogen, this is confirmed by research studies that used 15N-labeled substrates.
These observations indicated that AM colonization increases the nitrogen uptake of host plants (Crawford
and Glass, 1998 and Hawkins et al., 2000). An increase in nitrogen content among the shoots of AM
associated plants can be explained by (i) improvement in symbiotic nitrogen fixation (ii) direct nitrogen
uptake by mycorrhizal fungi and nitrogen transfer facilitation from nodulated to non-nodulated plants (iii)
increased activities of enzymes like pectinase, xyloglucanase, and cellulase which are mainly involved in the
metabolism of nitrogen and can decompose organic matter of soil (Barea, 2000).
It has been observed that more than 50% of plant nitrogen requirement is accomplished by the
mycorrhizal symbiosis in addition to increasing enzyme activities in roots and shoots of maize plants
(McFarland et al., 2010). Researchers have shown that shoots of mycorrhizal Sesbania grandiflora and S.
aegyptiaca accumulate more N than non-mycorrhizal control plants (Giri and Mukerji, 2004). However, little
is known about the nitrogen transfer from the fungal partner to the roots of the host plant and most authors
proposed the involvement of ammonium transporters in nitrogen transfer during AM symbiosis
(Govindarajulu et al., 2005). Nitrate reductase (NR) enzyme, involved in the NO3- assimilation pathway, is a
substrate induced enzyme and its level sharply drops under saline stress conditions because of low influx
NO3- from soil to plant roots. It has been observed that the activity of nitrate reductase (NR) enzyme
increases in AM inoculated plants and this was correlated with improved tolerance of AM plants under saline
stress conditions (Azcon et al., 2013). In 2012, Talaat and Shawky revealed that activity of NR was higher in

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mycorrhizal wheat plants under saline stress conditions, compared to non-mycorrhizal wheat plants, which
was attributed to the enhanced tolerance of AM plants to saline stress.
Several hypotheses have been proposed to explain the transfer of ammonia from fungal partners to plant
cells in AM symbiosis including (i) Nitrogen is taken in inorganic form from the soil and then incorporated
and stored as arginine, the main form of nitrogen transported from ERM (Extra-radical mycelium) to IRM
(Intraradical mycelium) (Govindarajulu et al., 2005), (ii) Absorbed nitrogen is assimilated by AM symbiosis
with the help of GS/GOGAT, asparagine synthase and the urea cycle (iii) Transportation of the stored
arginine can be done together with PolyP or bidirectionally to the IRM, and nitrogen is released from the
stored arginine and finally transferred to the cells of plants as NH4+ and is then incorporated in plant root
cells as free amino acids (Jin et al., 2005 and Chalot et al., 2006). It has been found that main Ammonium
Transporters (AMT) reported in Glomus intradices (presently named as Rhizophagusirregularis) like
GintAMT1, GintAMT2, and GintAMT3 are involved in AM symbiosis (Perez-Tienda et al., 2011;
Calabrese et al., 2016). More recently Veronica et al., (2017) revealed that higher nitrogen uptake in
mycorrhizal plants under salt stress is due to higher expression of nitrate and ammonium transporters in
wheat (TriticumaestivumL.) plants colonized with a mixture
of Rhizophagusirregularis and Funneliformismosseae.

Calcium

Calcium (Ca), an important macronutrient required for plant growth and development, represents 0.1– 5%
of all plant dry biomass (White and Broadley 2003). Calcium’s signalling role in plant cells is in response to
a wide array of environmental cues and, among the inorganic nutrients, Ca may be highly involved in the
molecular communications and the transmission of metabolic signals in eukaryotic cells (Thor, 2019).
Calcium plays a significant role by acting as a second messenger and its concentration increases to transduce
signals during salinity stress conditions. Several studies have supported the view that AM fungi association
strongly increased the uptake and concentration of Ca2+ in different plants including lettuce and banana as
compared to non-inoculated AM fungi plants (Linderman, 2001; Yano-Meloet al., 2003). Additionally, it
improves selective absorption of Ca2+ over Na+ deleterious and also helps in sustaining lower Na/K ratio
(Ahmad et al., 2014). Furthermore, Elhindi et al., (2017) observed that inoculation of AM fungi to the
Ocimumbasilicum increased the content of Ca and Ca/Na. More recently, Cui et al., (2019), while working
on peanut (Arachishypogaea L.), reported that Calcium acts as an essential modulator in mycorrhizal
colonization, and the AM increases the absorption of Ca2+ for host plants in Ca deficient soils.

IONIC BALANCE

K+/Na+ Ratio

Another mechanism used by AM fungi to promote the growth of plants under salinity stress is the
regulation of plant nutrition. Under salinity stress, a high concentration of sodium (Na+) is deleterious for
normal plant growth and a low K+/Na+ ratio has been found in plants under salt stress conditions (Ashraf et
al., 2004). A good balance of K+: Na+ is important for maintaining ion balance in the plant leave cytoplasm
and is, hence, a potential indicator of salt tolerance in the plants (Abdelhamid et al., 2010). The optimal
potassium (K+) level plays an important role in various metabolic processes like activation of enzymes,
stomatal movements, and synthesis of protein (Blaha et al., 2000; Tomar and Agarwal, 2013). Under salinity
stress, a higher Na+: K+ creates the ionic imbalance in the cytoplasm and Na+ ions compete with K+ for
binding sites essential for various cellular functions, finally disrupts different metabolic processes (Giri et al.,
2007). A significant role is being played by AM fungi in sustaining a high K +/Na+ ratio in plants that are
exposed to saline stress conditions (Selvakumar and Thamizhiniyan, 2011, Zhang et al., 2011). The AM
fungi inoculation under salinity stress conditions reduces the Na+ uptake and enhances the uptake of K+ ions
compared to non-AM fungi plants, suggesting higher loading of K+ than Na+ in the roots of AM fungi
inoculated plants (Hammer et al., 2011). It has been observed that AM fungi inoculation increases the plant’s
K+ uptake resulting in a higher K+: Na+ ratio (Kadian et al., 2013).
Recently Namdari et al., (2018) observed that concentration of K+, K+: Na+, and Ca2+: Na+ increased in
AM fungi inoculated Medicagosativa plants compared to non-inoculated AM fungi plants. The AM fungi
inoculated plants under salinity stress conditions demonstrated selective absorption of K + and Ca2+ over
deleterious Na+ results in sustaining a lower Na+/K+ ratio (Ahmad et al., 2014). Maintaining a higher K+/Na+
ratio in AM fungi inoculated plants is an excellent strategy to alleviate stress-induced harmful changes
(Wu et al., 2010). It has been revealed that the concentration of K+, Ca2+, and NO3 reduces in irrigated land

5
under salinity stress while as the concentration of inorganic phosphate (PO43-) and Na+ and Cl- ions decreases
to a level that creates osmatic and nutrient imbalance (Bothe, 2012).

Na+/H+ antiporters

Sodium intake and its distribution within plants is the main determinant for the salt sensitiveness of
plants under salinity stress conditions. The principal strategies by which plants cope with high salt stress
conditions include prevention of Na+ entry into the root, allocation within the leaf and sequestration into the
vacuole. The Na+/H+ antiporters facilitate the transfer of Na+ out of the cytoplasm into either vacuole or
apoplast. It has been reported that transgenic plants (Arabidopsis) with overexpressed Na+/H+ antiporters are
more salt tolerant compared to the controls (Gaxiola et al., 1999; Sottosanto et al., 2004). Actually in
Arabidopsis, transporters contribute to Na+ homeostasis include vacuolar Na+/H+ antiporters and the plasma
membrane uniporter (HKT1) (Zhu, 2003).
Ouziad et al., (2006) analysed the expression of two Na+/H+ antiporters-LeNHX1 and LeNHX2-
independently on the salt and mycorrhizal colonization and reported that under these employed conditions,
no significant alterations by mycorrhization were detected in the expression of LeNHX1 and LeNHX2.

SALINITY TOLERANCE THROUGH PHYSIOLOGICAL CHANGES

Salt stress negatively affects majority of the crop plants by disrupting various physiological
mechanisms like decreasing efficiency of photosynthesis, membrane disruption water status, abscisic acid
(ABA) level and nitrogen fixation. However, AM symbiosis can overcome such physiological changes to a
greater extent, which is discussed in the following section.

Photosynthesis

Salt stress hinders photosynthesis, hence enormously declining the productivity of crops (Pitman and
Läuchli, 2002; Sheng et al., 2008). Salt stress-induced osmotic tension leads to decreasing leaf area, coupled
with a decrease in conductance of stomata and mesophyll, which restricts CO2 availability and assimilation
(Chaves et al., 2009). AM symbiosis curtails the negative impacts of salt stress on photosynthesis. This is
achieved by enhanced water status in mycorrhizal plants resulting in retaining larger leaf area and higher
stomatal conductance, therefore, enhancing CO2 assimilation (Wu et al., 2015; Chen et al., 2017).
It has been observed that reduction in chlorophyll content occurs under high salinity stress environment
because of suppression of enzymes that are mainly responsible for the synthesis of photosynthetic pigments
(Murkute et al., 2006). Reduced photosynthetic pigment content under saline stress conditions in different
crop plants like Zea mays, Triticumaestivum, Viciafaba and Phaseolus vulgaris, have previously been
confirmed by various independent researches (Bargaz et al., 2016; Awad et al., 2012; El-Lethy et al., 2013
and Dawood et al., 2014). The research findings of Aroca et al., 2013 for tomato (Solanum lycopersicum)
and lettuce (Lactucasativa) reveal that AM inoculation improved chlorophyll content in these plants
compared to non-inoculated under saline conditions. Likewise, increased salinity levels are positively related
with the chlorophyll content in Ephedra alata (Alqarawi et al., 2014). The decreased chlorophyll content
under salinity stress is associated with the increased chlorophllase activity resulting in the degradation of
photosynthetic pigments, eventually leading to reduced photosynthesis and plant growth. In addition,
multiple studies have documented that reduced photosynthetic pigments, mostly chlorophyll pigments, are
due to salinity stress (Sudhir et al., 2005; Neelam and Subramanyam, 2013, Khan et al., 2014, Yang et al.,
2015) and a number of researchers believe that the AMF-triggered synthesis of chlorophyll pigment is due to
significant Mg+ uptake, which forms the central part of the head of chlorophyll pigment (Sheng et al., 2008).
Recently, AM fungi were shown to increase the activity of rubisco and other associated carbon-metabolizing
enzymes, which positively impact the plant growth under salinity stress conditions (Hashem et al., 2015).
Increasing salinity stress reduces the mineral uptake, particularly magnesium, needed for biosynthesis
of chlorophyll in addition to diminishing the leaf chlorophyll content in the leaf chloroplasts (Giri and
Mukerji, 2004; Ibrahim et al., 2011). Moreover, studies have demonstrated that mycorrhizal plant leaves
under saline stress have higher chlorophyll content, suggesting that salt stress interferes to a lesser extent
with chlorophyll biosynthetic process in mycorrhizal plants than non-mycorrhizal plants (Sannazzaro et al.,
2006;Zuccarini, 2007 and Colla et al., 2008). The antagonistic effect of Na+ on the uptake of Mg2+ is
counterbalanced and suppressed in mycorrhizal plants, and under stress these plants reach greater
photosynthetic capacity to non-stressed plants (Zuccarini and Okurowska, 2008). The photosystem II (PSII)
reaction centre along with electron transport system in the photosynthetic apparatus in majority of the plants
could be deteriorated under salt stress conditions. The toxic effect of salinity on the PSII reaction centre

6
complex could be mitigated under AM symbiosis (Sheng et al., 2008). Higher non-photochemical quenching
is reported in inoculated mycorrhizal plants than non-mycorrhizal plants because it protects the plant leaves
from light-induced damage (Maxwell and Johnson, 2000).

Cell Membrane Permeability

Uptake regulation and transport of ions in cells are controlled by cell membranes and are the initial sites
of salt stress injury and damage. Under saline stress conditions, cell membrane permeability changes causing
cell membranes to take up and retain solute changes negatively (Khatkar and Kuhad, 2000). It has been
observed that the electrical conductivity of roots of mycorrhizal plants was higher than the non-mycorrhizal
plants, and roots of inoculated pigeon pea (Cajanuscajan) roots demonstrated relatively higher permeability
at different soil salinity levels (4, 6, and 8 dSm1-, ECe) than the non-inoculated plants (Garg and Manchanda,
2008). Kaya et al., (2009) reported that the leakage of electrolyte in the leaves of Capsicum
annum inoculated with AM at two different concentrations of NaCl (50 Mm and 100Mm) were relatively
lower as compared to non-inoculated plants. Therefore, it is evident that mycorrhizal plants have lower
plasma membrane electrolyte leakage and higher membrane stability than non-mycorrhizal plants because of
increased P uptake and increased production of antioxidants (Feng et al., 2002).

WATER STATUS IMPROVEMENT

Water stress is also a major constraint faced by many crops under saline stress conditions. The crop
plants face physiological drought as Na+ and Cl- mineral ions bind to water, making it immobile for the
plants, thus hindering vital physiological processes (Fuzy et al., 2008). Yang et al., (2014) reported that
mycorrhizal inoculated Malus hupehensis seedlings maintained higher leaf turgidity and reduced osmotic
potential compared to non-mycorrhizal plants when subjected to a saline stress environment. Several studies
have indicated that AM inoculated plants maintain higher water content than un-inoculated plants
(Jahromi et al., 2008; Colla et al., 2008). This enhanced water status of inoculated plants under salt stress
conditions could be due to the direct uptake and transport of water by AM fungal hyphae (Jiang et al., 2017).
In addition, AM inoculated plants have higher stomatal conductance leading to increased transpiration
demand (Dell et al., 2002). Furthermore, studies have revealed that lower osmotic potential in mycorrhizal
plants is actually maintained by fungal accumulation in solutes, consequently, improving osmotic adjustment
under saline conditions. The water status of most AM fungi inoculated plants improved by lowering water
saturation deficit and higher turgor potential (Al-Garni, 2006). All these improved facilities in host plants
mediated by AM colonization, enabling them to use water efficiently under stress conditions and maintaining
a lower concentration of intercellular carbon dioxide. As a result, the gas exchange capacity increases in the
inoculated plants (Graham and Syversten, 1984).

ABSCISSIC ACID

Abscisic acid (ABA) is a well-known plant stress hormone that enables plant growth and survival under
different stress conditions, particularly salinity stress (Basu and Rabara, 2017). Under salinity stress
conditions, ABA accelerates the accumulation of K+, Ca2+, and compatible solutes such as proline and sugars
in root cells, thereby preventing the Na+ andCl- uptake which finally protects the plants from severe impacts
of salinity stress (Atia et al., 2018).
The role of ABA as a positive or negative regulator for plant growth under salinity stress conditions is
still unclear (Tardieu et al., 2010). Abscisic acid is the established endogenous phytohormone and is known
to increase with increasing salinity of the soil (Javid et al., 2011). The endogenous levels of ABA in
mycorrhized plants subjected to salinity stress are also controversial and could be explained by differences in
soil or plant water status. (Hause et al.,2007). Abscisic acid acts as a signal for regulating various plant
activities like opening and closing of stomata, plant growth and development under salt stress conditions
(Wasilewska et al., 2008). The inoculation of the host plants with AM fungi can alter the levels of ABA
(Ludwig-Muller, 2010). Martin-Rodríguez et al., (2016) have reported that in mycorrhized tomato plants,
ABA reduces Gibberellic acid (GA) biosynthetic and enhances the GA-catabolic gene expression leading to
reduction in bioactive GAs. On the contrary, GA activated ABA catabolism in mycorrhized roots.
Increased concentrations of ABA in response to salinity stress have been observed in several plants
including musrard, common bean, maize and rice (He and Cramer, 1996; Cabot et al., 2009, Cramer and
Quarrie, 2002; Kang et al., 2005). Aroca et al., 2013 reported that concentration of ABA increased with the
increasing levels of NaCl in lettuce plant inoculated with Rhizophagusirregularis. It has been documented

7
that Lotus glaber plants inoculated with Glomus intraradices have higher levels of ABA as compared to non-
colonized plants (Sannazzaro et al.,2007). The production of ABA is important for an appropriate
establishment of colonization of AM in plant roots and its impact on the formation and functioning of
arbuscules (Herrera et al., 2007 and Pozo et al., 2015). Under salinity stress conditions, the concentration of
ABA in plants increases and is mostly related to leaf or soil water potential, indicating that the production of
endogenous ABA is resulted by water deficit and not by effects of salt (Zhang et al., 2006 and Javid et al.,
2011).
ABA is an important cellular signal that modulates the expression of various salt and water deficit-
response genes. It has been reported that AM fungi enhance salinity tolerance of host plants by water status
improvement of the host plants by increasing water transport facility (Ouziad et al., 2006). However,
depending on the host plant properties, the impact of AM fungal species on ABA content in the host plant
differ (Evelin et al., 2009; Porcel et al., 2012).

NITROGEN FIXATION IMPROVEMENT

Numbers of research findings have reported that AM inoculation improved plant growth under various
environmental stress conditions (Abdelmoneim and Almaghrabi, 2013; Alizadeh et al., 2011; Tang et al.,
2009 and Zhang et al., 2010). Similarly, AM inoculation has significant potential to enhance nodulation,
nitrogen fixation in leguminous and non-leguminous plants under different stress conditions. Research
studies conducted under field and laboratory environmental conditions have clearly shown that dual
inoculation of AM fungus along with nitrogen-fixing bacteria increased nitrogen fixation in legume plants
(Lesueur and Sarr, 2008). The AM has been known to occur naturally in saline environments, so its
association with host plants could be very important for improving plant growth and vigour under saline
stress conditions (Farahani et al., 2008, Evelin et al., 2009). Legume plants are known to be salt-sensitive
and their nitrogen fixation can be improved under such stress conditions by particular inoculation with a
specific microorganism (Munns, 2002). Garg and Chandel (2011) observed that inoculation of pigeon pea
(Cajanuscajan) with Glomus mosseae improved plant dry mass and nodules nitrogen-fixing potential under
salt stress conditions. Nodules of legume plants, formed by nitrogen-fixing bacteria, are considered as
smooth targets for salinity stress and their number decreases under salt stress condition
Nodules of leguminous plants which are formed through symbiosis with the nitrogen-fixing bacteria are
considered a soft target for salt stress environments and their diversity decreases under salt stress conditions
(Harisnaut et al., 2003; Rabie and Almadini, 2005; Garg and Manchanda, 2008). This occurs due to
premature nodule senescence triggered by salt stress causing green pigment formation from leghaemoglobin
leading to loss of nitrogen fixation (Matamoros et al., 2010). The application of AM can counteract the
harmful effects of salinity stress on nodule formation and nitrogen fixation in leguminous plants. Moreover,
AM symbiosis could mitigate salt stress-induced premature nodule senescence and increase the nodule
number in legumes indicating a positive impact of AM on legume-nitrogen fixing bacteria symbiosis (Rabie
and Almadini, 2005). Plants inoculated with AM have higher nitrogen-fixing activity and nitrogenase
enzyme activity attributing to relief from P stress, which is important for the normal functioning of the
nitrogenase enzyme (Founoune et al., 2002). Therefore it may be suggested that nodule and mycorrhizal
symbiosis acts synergistically on plant nutrition and growth, and increase plant stress tolerance under salt
stress conditions.

BIOCHEMICAL CHANGES

The water potential of soil under salinity stress becomes more negative due to increased salt
accumulation in the soil. To counteract this negative effect, plants must decrease their water potential by
osmoregulation or osmotic adjustment for continuous water flow from the soil into roots. The osmotic
adjustment is gained through active accumulation of organic ions or solutes and the most common include
proline, betaines, soluble sugars and polyamines (Hoekstra et al., 2001; Rabie and Almadini, 2005). This
kind of osmotic adjustment enables plants to maintain cell turgor and related processes like stomatal opening,
cellular expansion, and photosynthesis. Osmolytes (proline, soluble sugars, etc.) are compatible solutes that
help in osmoregulation by maintaining the water content of cells (Ahmad et al., 2008, Ahanger et al., 2014).
The present review paper will discuss proline and soluble sugars only.

Proline

Proline is one of the most important organic solutes produced by plants in response to salinity stress and
plays a significant role in sustaining the osmotic adjustment of a cell to ameliorate the effect of salt stress. It

8
is one of the main osmo-protectants in plant cells under salinity stress and is responsible for preventing
cellular damage by sustaining water potential and integrity of proteins (Mansour and Ali, 2017). Several
plants under salinity stress and low water potential conditions accumulate proline as a protective osmolyte to
maintain osmotic stability (Jain et al., 2001; Ashraf and Foolad, 2007; Sannazzaro et al., 2007).
Number of studies have reported that concentration of proline increases in AM fungi inoculated plants
compared to non-inoculated AM fungi plants under salinity stress (Dodd and Perez-Alfocea, 2012; Garg and
Baher, 2013). It has been observed that accumulation of more proline is found in roots that are primary
salinity stress sites than in shoots under salinity (Borde et al., 2011). Under salinity stress conditions, proline
synthesis is up-regulated with a great decline in its catabolism (Mo et al., 2016; Iqbal et al., 2015). It was
also reported that AM fungi inoculation triggered the proline accumulation, which leads to improved
transport of water and efficiency of metabolic reactions (Shekoofeh et al., 2012; Wu et al., 2016). The
enhancement in proline accumulation caused by AMF symbiosis might be due to the up-regulation of the
delta1-pyrroline-5- carboxylate synthetase (Huang et al., 2013). A recent research analysis by Pan et
al.,(2020) demonstrated that AM fungi in halophytes increased the accumulation of inorganic ions (K and Ca)
and decreased the accumulation of osmolyte proline to increase biomass production under salinity stress
conditions

SOLUBLE SUGARS

The sugar content increase in the host plant is positively correlated with mycorrhization (Thomson et al.,
1990). The sugar content increased by AM symbiosis under salt stress conditions (Talaat and Shawky, 2011,
Liu et al., 2016, Garg and Bharti, 2018, Zhu et al., 2018). Talaat and Sahwky (2012) observed a positive
correlation between concentrations of total soluble sugars and the mycorrhization of wheat plants. A similar
positive response was observed in pigeon pea plants colonized with F. mosseae that protected the plants
against harmful effects of salinity (Garg and Chandel, 2011). Porcel and Ruiz-Lozano (2004) have reported
that colonization of soybean plant roots by G. Intraradices increased sugar concentrations under salinity
stress. This positive correlation between sugar content and mycorrhization is due to the sink effect of the
fungus demanding sugars from the cells of the shoot (Augé, 2000). The higher accumulation of sugars in
mycorrhizal plants is because of- (i) higher photosynthetic efficiency (ii) higher activities of alpha and beta
amylases (iii) higher organic acid content; and (iv) carbon requirement of AM (Garg and Baher, 2013, Yu et
al., 2015, Zhu et al., 2016).
Trehalose (a-D-glucopyranosyl-1,1-a-D-glucopyranoside) is a non-reducing disaccharide that balances
carbohydrate metabolism (Lunn et al., 2014). Generally, it acts as a protective metabolite under stress
conditions by maintaining K+: Na+ ratio, scavenging ROS, and increasing the soluble sugar concentration in
plants (Garg et al., 2002, Redillas et al., 2012, Chang et al., 2014). The mycorrhizal plants under salt stress
conditions accumulate more trehalose compared to non-mycorrhizal plants (Garg and Pandey, 2016).
Ocon et al. (2007) analyzed the effect of salt stress on trehalose content and metabolism in the extra-radical
hyphae of Glomus intraradices and deciphered the possible role of trehalose in plant protection against
salinity stress. More recently (Wengie Qin et al, 2021) reported that AMF-inoculated peanut plants showed
higher net photosynthetic rate, leaf relative water content (RWC), plant height and osmolyte accumulation
but lower leaf relative electrolyte conductivity (REC) compared to non AM fungi-inoculated plants.
Furthermore, authors reported that malondialdehyde (MDA) concentration was reduced while the antioxidant
enzymes such as superoxide dismutase (SOD), guaiacol peroxidase (G-POD), catalase (CAT), and ascorbate
peroxidase (APX) were activated. In addition, transcriptome data indicated that AM fungi potentially
alleviate salt stress by regulating redox processes, cell wall assembly, cell growth, and other similar
processes.

SALT TOLERANCE BY AM THROUGH THE ANTIOXIDANT DEFENCE SYSTEM

Salinity stress-induces a secondary stress in the plants known as the oxidative stress. It results due to the
equilibrium disturbance betweenreactive oxygen species (ROS) generation and its abatement by various
antioxidants (Gill and Tuteja, 2010). The superfluous generation of ROS upsets vital cell functions by
attacking important biomolecules such as nucleic acid, protein, and membrane lipid (Foyer and Noctor,
2005). Under a salinity stress environment, the level of lipid peroxidation and membrane permeability
increases and results in loss of ions from the cells (Evelin et al., 2012, Pedranzani et al., 2016, Zhang et al.,
2018). The AM fungi affect the expression of several different antioxidant enzymes (Table II) which are
involved in the protection of plants from reactive oxygen species (ROS) produced under stress conditions
(Gamalero et al., 2009). Plants manage salt stress by increasing the accumulation of antioxidants that protect
the plant cells from oxidative injury (Rai et al., 2011). It has been observed that activated oxygen species can

9
react with DNA, proteins, lipids, and in the absence of a protective antioxidant system; they can damage cell
structure and function (Alguacil et al., 2003). Thus plants developed protective mechanisms to escape
oxidative damage by involving antioxidant molecules and enzymes (Jiang and Zhang, 2002, Yamane et al.,
2004). The ROS accumulation depends on the balance between production and scavenging of ROS (Miller et
al., 2010), the plants have developed both enzymatic as well as non-enzymatic antioxidant systems to
mitigate the oxidative damage by ROS within the cells (Sharma et al., 2012). The non-enzymatic oxidant
system includes ascorbate, glutathione, phenolics, tocopherols, and ascorbic acid (Alguacil et al., 2003;
Wu et al., 2006), and the enzymatic oxidant system includes catalase (CAT), peroxidize (POD), superoxide
dismutase (SOD), ascorbate peroxidase (APOX), glutathione reductase, dehydroascorbate reductase,
guaiacol peroxidase, oxidized glutathione, and glutathione peroxidize (Yamane et al.,2004; Ghorbanli et al.,
2004).

Table II

Effect of AM fungi on antioxidant response in plants under salt stress

Plant species Fungal species Salinity levels Effect of AM fungi on salt stressed plants References

Solanum Glomus mosseae 0, 25, 50 and Increased- enzyme activities Abdel-Latef and
lycopersicum 100 nM NaCl Decreased- MDA content Chaoxing, 2011
(Solanaceae)
Cucumis sativus Glomus etunicatum, 25-200 nM NaCl Increased- total phenol and AsA Hashem et al.,
(Cucurbitaceae) Glomus intraradices, content and activities of SOD, CAT, APX, and 2018
Glomus mosseae GR, decreased- H2O2 and MDA content
Cajanus cajan Funneliformis mosseae 0-100 mM NaCl Increased- GSH:GSS and AsA:DHA ratio, further Pandey and
(Fabaceae) and Rhizophagus increased GR, APX, and Garg, 2017
irregularis SOD activity, decreased- MDA content
Suaeda salsa Glomus mosseae, 0 and 400 mmol Further increased- SOD and CAT activity, Li et al., 2012
(Amaranthaceae) L−1 NaCl decreased- MDA content
Trigonella Glomus intraradices 0, 50, 100 and Increased- AsA, a-tocopherol, GSH, Evelin and
foenum-graecum 200 mM NaCl carotenoid content and SOD, APX, POD, GR, Kapoor, 2014
(Fabaceae) and CAT activity, decreased- leaf and root MDA
and H2O2 content
Sesbania sesban Glomus etunicatum, 0,75 and 150 nM Further increased the activity of enzymatic and Abd-Allah et
(Fabaceae) Glomus intraradices, NaCl non-enzymatic antioxidants al., 2015
Glomus mosseae
Digitaria eriantha Rhizophagus irregularis 200 nM NaCl Increased- shoot MDA content; shoot Pedranzani et
(Poaceae) SOD, CAT, APX activity and root CAT and APX al., 2016
activity, decreased- root and shoot H2O2
content; root SOD; and root and shoot GR
Cicer arietinum Glomus mosseae 0-100 nM NaCl Increased- CAT, GPOX, APX, SOD, MDHAR, Garg and
(Fabaceae) DHAR, GR activity, further increase in GSG, Bhandari, 2016
GSSH, and total glutathione content, decreased-
superoxide radical, H2O2, MDA content, and
lipoxygenase activity
MDA, malondialdehyde; CAT, catalase; SOD, superoxide dismutase; POD, peroxidase; APX, ascorbate peroxidase; GR, glutathione
reductase; GSH, reduced glutathione; GSSG, oxidized glutathione; AsA, ascorbate; H2O2, hydrogen peroxide; DHA,
dehydroascorbate; GPOX, glutathione peroxidase; MDHAR, monodehydroascorbate reductase; DHAR, dehydroascorbate reductase.

Several research findings revealed that AM symbiosis helps plants to mitigate salt stress by enhancing
the activities of antioxidant enzymes (Harisnaut et al., 2003; ZhongQun et al., 2007). Superoxide dismutase
(SOD) is the main enzyme that helps in converting superoxide into oxygen and hydrogen peroxide (H2O2)
(Alscher et al., 2002). The SOD enzyme plays a significant role in the protection of the electron transport
system by mediating the scavenging of toxic superoxide radicals as the increased activity of SOD has been
reported in different plants including cowpea, sorghum and cotton under salinity stress conditions (Freitas et
al., 2011, Wu et al., 2016). The increased SOD activity in AM inoculated plants might be due to higher
uptake of Zn, Cu, Mn, and Fe, which form co-factors for its isozymes (Qun et al., 2007; Kohler et al., 2009).
It has been observed that AM inoculation mediated fast breakdown of H2O2 by enhanced CAT and APX
activity and protected against cellular damage (Foyer et al., 1994; Abd Allah et al., 2018). Alguacil et al.
(2003) also reported enhanced activities of CAT, APOX, and SOD in Olea
europaea and Retamasphaerocarpa. The AM inoculation promoted the accumulation of several essential
polyphenols, contributing to the growth of plants like marjoram, lemon balm, and marigold (Engel et al.,
2016). However, the role of AM on the status of non-enzymatic antioxidants such as carotenoids,
tocopherols, and ascorbic acid of the host plant has not been reported in detail. Therefore, this aspect needs
in-depth research.

10
CONCLUSION AND FUTURE PROSPECTIVE

It is clear from the above discussion that salt stress environment harms growth, mineral nutrition, and
physiological responses. In the present review article, we conclude the prospective of AM symbiosis in
regulating plant growth, nutrient uptake, and various physiological processes under salt stress conditions.
The salt stress induced negative effects on the plant growth can be alleviated or reduced by naturally
occurring mycorrhizae or through AM application exploiting various inoculating methods.
Increase crop production is a major challenge under salt stress conditions and requires a clear
understanding of different mechanisms involved in salt stress response. Crop adaptation to salinity stress
involves changes in water uptake, distribution, and maintenance of photosynthesis to normal levels enables
different plants to live under salt stress conditions. Presently, there is enough evidence about the positive
influence of AM on the regulation of these mechanisms under salt stress conditions. Overall, future research
should be focussed on: (i) to elucidate the mechanisms of interactions between nitrogen-fixing bacteria and
mycorrhizae in natural field conditions under stressful conditions, ii) to explore what strains of fungus and
also the combinations of these beneficial strains are important for promoting plant growth and development
under different stress conditions (iii) to identify target genes for promoting plant growth under stress
conditions and use different biotechnology tools to transfer these target genes.
Identification of genes that are involved in the production of different antioxidants and enzymes
controlling the synthesis of many osmoregulators will, eventually, provide further insights into the molecular
basis of the mechanism. The transporter systems active during the AM symbiosis need to be elucidated and
sophisticated techniques particularly Protoninduced X-ray emission (PIXE) may be employed for studying
the localization of micro- and macro-nutrients in the host plant as well as the fungal partner.

ACKNOWLEDGMENTS

The authors would like to acknowledge SKUAST-K, Srinagar and Kurukshetra University Kurukshetra,
Haryana, India for their support.

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