VESICULAR ARBUSCULAR MYCORRHIZA AS

BIOFERTILIZER : REVIEW

A DISSERTATION SUBMITTED IN PARTIAL FULFILLMENT OF

REQUIREMENTS FOR THE AWARD OF DEGREE OF

MASTER OF SCIENCE
IN
BOTANY

SUBMITTED BY
AKASH CHAUDHARY
M.Sc. Final
ROLL No. - 1902041

Dr. Vijay kumar Dalal Prof. G.P. Satsangi

( Supervisor ) (Head, Department of
Botany )

Department of Botany, Faculty of Science

Dayalbagh Educational Institute
(Deemed University)
Dayalbagh, Agra- 282005
CERTIFICATE

This is to certify that the present dissertation entitled “VESICULAR ARBUSCULAR

MYCORRHIZA AS BIOFERTILIZER : REVIEW” is submitted by Akash Chaudhary, in partial
fulfillment of the requirements of the award of degree of Master of science in Botany, is a bonafide
presented work carried out by him under my supervision in the faculty of science, Dayalbagh
Educational Institute (Deemed University), Dayalbagh Agra. Further, the matter embodied in this
study has not been submitted for the award of any other degree.

Dr. Vijay Kumar Dalal Prof. G.P. Satsangi

( Supervisor , Department of botany ) ( Head, Department of Botany )

Prof. Sant Prakash

( Dean , Faculty of Science )

ACKNOWLEDGEMENT
Grand gestures on significant occasions mark the passage of time. This acknowledgement is my
gesture of gratitude towards the people who were elemental in making this work a success .

1
I express my deepest gratitude and sincere regards to Dr. Vijay Kumar Dalal, my supervisor for
suggesting an interesting topic to work on for my dissertation, constant guidance in achieving the goal,
valuable suggestions and encouragement throughout the tenure of study .

I express my heartfelt gratitude and sincere thanks to Prof. G.P. Satsangi, Head, Department of botany,
Faculty of science for his kind help and encouragement during the project.

Words fail to express my humble gratitude and profound regards to my family for their affectionate
encouragement and blessings which has always been a source of inspiration for me and without which
it would not have been possible to achieve my objectives.

It is my privilege to take this opportunity to thank all who have directly or indirectly helped in
completion of the present work.

AKASH CHAUDHARY

TABLE OF CONTENTS

Page Numbers

1. ABSTRACT 4-5
2. INTRODUCTION 4-6
3. OBJECTIVES 6
4. REVIEW OF LITERATURE 6-32
5. SIGNIFICANCE 33
6. CONCLUSION AND FUTURE PROSPECTS 33-34
7. REFERENCES 34-46

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 1. Abstract
A wide variety of associations exist in nature of which Vesicular arbuscular mycorrhiza (VAM) is the
most common association that exists between plant roots and fungi. Arbuscular mycorrhizal fungi
(AM fungi or AMF) establish symbiotic associations with more than 80% of terrestrial plants.
Vesicular arbuscular mycorrhizal associations imply a remarkable reprogramming of functions in both
plant and fungal symbionts. As a result, altered plant physiology has an explicit impact on plant yield,
nutritional status (especially phosphorus), resistance to both abiotic and biotic stresses, etc. Hence, due
to their immense benefits to plant in exchange for carbon products for fungi nutrition they are
considered as natural biofertilizers. Apart from the benefits VAM provide to plants, they also
contribute to improve soil texture and structure, soil fertility, and bioremediation of contaminated
soils. The importance of these fungi to agriculture and forestry resides in their role in plant growth and
nutrition, so they can be served as the best replacement to harmful chemical fertilizers, pesticides,
fungicides, etc. In this review, the beneficial services of mycorrhiza to plants have been taken into
account, and have shown how the use of these fungi as biofertilizers can diminish the use of harmful
fertilizers both in agriculture and forestry.

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 2. Introduction
Bio-fertilizers are organic substances which are used to increase the fertility of soil. They are not
harmful to crops or other plants like the chemical fertilizers. In modern days the use of chemical
fertilizers has been increased in agriculture that cause toxicity and other harmful effects to crop plants.
Fertilizers increase the cost of energy, and currency that have been rising exceedingly and will
continue to rise in future. The use of bio-fertilizer is the best option to get rid of the problems caused
by chemical fertilizers, as they are environment friendly.
Vesicular-arbuscular mycorrhiza (VAM)/Arbuscular Mycorrhizal Fungi (AM fungi or AMF) are one of
the best biofertilizers that we can add to plants to improve their quality and yield. Vesicular Arbuscular
Mycorrhizas are formed by aseptate mycelial fungi and are named because of the two characteristics
attributes they form inside the host plants that are - vesicles and arbuscules- present in plant roots with
type of infection. AMF are symbiotic fungi that form association and live in mutualistic relationships
with plant roots. VAM fungi invade the roots of a host plant through hyphae going in the cortex region
of roots to establish their symbiotic relationship with plant, this established filamentous network
encourage bi-directional movement of nutrients where carbon flows to the fungus and inorganic
nutrients move to the plant, thereby forming a critical linkage established between the plant root and
rhizosphere.
The most limiting nutrients for plant growth and development are P and N. Although soil may contain
vast amounts of either nutrients, they are not easily available for plants to use. The application of VAM
helps plants to capture nutrients such as phosphorus and micronutrients from the soil. VAM colonized
plants have significantly increased root absorption surface area in soil that enhances its nutritional
quality like providing the plant with an additional supply of phosphorus (as phosphate) in the soil. The
importance of VAM fungi to agricultural and forest plant species resides in their role in plant growth
and nutrition uptake. In agriculture by the expanded take-up of soil minerals by VAM colonized plants,
it is possible to consider significantly decreasing applications of fertilizers and pesticides and
simultaneously get equivalent or considerably higher crop yields (Abbott and Robson, 1991a). Apart
from an improved nutritional supply, VAM interaction offers other benefits to plants, such as improved
drought and salinity tolerance (Augé et al., 2015) and disease resistance (Pozo and AzcónAguilar,
2007). VAM fungi are also known to lessen heavy metal toxicity in the host plants and to tolerate high
metal concentrations in the soil. Furthermore, VAM can also have a direct effect on the ecosystem, as

4
they can improve the structure and texture of soil. VAM fungi have the ability to expedite the
decomposition process of soil organic matter (Paterson et al., 2016).
The impact of VAM symbiosis on greenhouse gas emission has recently been investigated (Bender et
al., 2014; Lazcano et al., 2014). Bender et al. (2014) had determined that AM fungi can reduce the
emissions of N2O gas, which is an important greenhouse gas that causes harm to the ozone layer, thus
indicating that they could play a role in the alleviation of climatic change.
Arbuscular mycorrhizal fungi are widely distributed and can form symbiosis with more than 80% of the
plant families in the world. It is alleged that the event of the VAM symbiosis played a significant part
in the initial colonization of the land by plants and in advancement of the vascular plants (Brundrett,
2004).
The aim of this review is to provide the knowledge about VAM fungi and role of VAM fungi as
biofertilizers in the regulation of plant growth and development, hence the productivity of plants with
enhanced nutrient uptake. Other beneficial services provided by VAM fungi to host plants and the
ecosystem are also considered like the role of VAM fungi in mitigating the biotic and abiotic stress,
bioremediation, etc. The indirect contribution of VAM fungi in soil aggregation and stability have also
been taken into account.

3. Objectives
The overall objective of this review is to undertake the comprehensive knowledge on VAM and their
influence on host plants, their advantages and applications. The specific objectives of this review are
as follows:
1) Literature review to explore capabilities of VAM as biofertilizer, in terms of cost effectiveness,
environment friendly, and energy saving.
2) To review the suppressing abilities of VAM against soil pathogens (root feeding nematodes,
fungi, etc) infecting various crops.
3) Review to increase the productivity of cereal crops, fruits, and vegetable crops and highlight
the future research directions in mycorrhizal technology.

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4. Review of Literature
What is Vesicular-arbuscular mycorrhiza / Arbuscular Mycorrhizal
Fungi?
Vesicular-arbuscular mycorrhiza (VAM) is a symbiotic association formed by a group of root obligate
biotrophs that form mutualistic relationships with the roots of plants. Plants in contact with VAM
show more yield and growth as compared to the plants which lack such association. Arbuscular
mycorrhizal (AM) fungi can be seen in a variety of ecosystems including agricultural lands, forests,
grasslands and many stressed environments, and form symbiotic association with the roots of most
plants, including bryophyte, pteridophyte, gymnosperms and angiosperms. AM fungi are the most
common variety of mycorrhizal fungi; these are microscopic and branched forms found in the cortical
cells of the root. VAM fungi go deep in the soil or other substrata with an extensive extraradical
mycelium where roots of the plant cannot invade and absorb essential elements for the plant in
exchange of photosynthetic products made by the plant . Outside the host the fungal hyphae produce
the very large spores often described as chlamydospores. Formation of the mycorrhizal symbiotic
association is an infection process. Spores germinate near a plant root and the germinating hyphae
penetrate the root in response to root exudates. Hyphae grow through the root tissues, cross epidermis
then hypodermis and finally reach to the root cortex where they form arbuscules (site for exchange
between fungus and plant). All AM fungi are obligately biotrophic, as they are entirely dependent on
plants for their survival. This does not pose any problem for AM fungi, as they show little or no host
specificity and can establish symbiotic association with the majority of plants. Since AM fungi are
obligately biotrophic, attempts made to grow them on their own in culture medium have so far failed.
However, since the majority of commercially grown plants form AM associations, interest in
developing ways of inoculating crops with the best fungus continues to intensify.

What fungi and plants are involved in VAM?

Mainly six genera of fungi belonging to Endogonaceae i.e. Glomus, Gigaspora, Acaulospora,
Entrophospora, Sclerocystis and Scutellospora, have been shown to form mycorrhizal associations.
Many species of plants have been seen to form mycorrhizal association with VAM fungi including
some relevant crops such as Solanum lycopersicum, Sorghum bicolor, Withania somnifera,

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Cucurbita maxima, Piper longum, Phaseolus vulgaris, Panicum hemitomon Schult, and some free
fruits such as Citrullus lanatus, Musa acuminata, Prunus cerasifera, etc.

VAM Structure and functions

Vesicular-arbuscular mycorrhizal fungi form lipid rich vesicles, arbuscules, spores in the roots of
plants by hyphae that grow outside as well as inside of roots. Hyphae grow in the direction of roots,
then penetrate the root cell by forming a swelling called appressoria. Once the hyphae and root cells
form contact with each other their mutualistic relationship starts.

Hyphae
Hyphae of AM fungi present in soil are known as extraradical or external hyphae. They are
filamentous fungal structures which develop and divide in the soil. They are accountable for nutrient
acquisition, propagation of the association, spore formation, etc. Generally, different soil hyphae of
various morphologies and functions are produced by AM fungi which include thick "distributed" or
"infective" hyphae to thin "absorptive" hyphae as well as "fertile" (spore-bearing) hyphae. “Branched
absorptive structures” (BAS) can be produced by finer hyphae, where fine hyphae proliferate (Bago et
al. 1998). BAS are also known as arbuscular like structure (ALS).
Hyphae are initially aseptate (without cross walls) after the entry into the roots, but septation may
occur in the older roots. The absorptive ability of VAM fungal hyphae is more than that of plant roots
because they have a high surface to volume ratio. The hyphae of VAM are also finer as compared to
roots and can easily enter into pores of the soil that are unreachable to roots and thus upgrade plant
access to nutrients, particularly those whose ionic forms have a poor mobility rate or those which are
present in low concentration in the soil solution.

Arbuscules
Arbuscules are complicatedly ramified haustoria originating from branches of the intraradical hyphae
that are formed by the VAM fungi within the root cortex cells of the plant. Arbuscules are rich in
numerous nuclei, mitochondria, glycogen particles and lipid globules.
Arbuscules are regarded as the site of extreme alkaline phosphatase and possibly ATPase activity
(Marx et al., 1982). The fungus may take up the phosphate from the soil, stockpile it as granules of

7
polyphosphate, and transfer it in this form along the hyphae through cytoplasmic streaming to the
active arbuscule. Here, the phosphorus is released to the host by degrading the granules (Callow et al.,
1978).
The fungus constricts arbuscules for the exchange of phosphorus, carbon, other nutrients, and water
with the plant. Arbuscules are made by repeated dichotomous branching and reductions in hyphal
width. Gallaud in 1905 named arbuscules because they look like little trees. Arbuscules begin to show
up shortly after root infiltration (Brundrett et al. 1985). They develop inside individual cells of the root
cortex, however stay outside their cytoplasm, because of invagination of the plasma membrane.
Arbuscules are viewed as the significant or main site for trade between the organism and host.
Arbuscules are short lived and die after a few days that is why in nature senescent arbuscules are more
frequently encountered than active arbuscules especially in older roots.

Vesicles
Vesicles are globose bodies formed as intercalary or terminal swellings of hyphae in the root cortex
region of root both inter and intracellularly having a storage function. Vesicles are developed by AM
fungi to stockpile storage products in VAM associations. Vesicles contain lipids and cytoplasm inside.
Vesicles may function as propagules by developing thick walls around themselves in older roots .

Spores
Spores are formed as swellings on one or more subtending hypha in the soil or in roots. spores contain
lipids, cytoplasm and numerous nuclei. Spores can typically work as propagules by developing thick
walls with more than one layer. Spores may be aggregated into groups called sporocarps. Spores
explicitly start to form when nutrients are remobilised from roots where associations are senescing.
They function as storage structures, resting stages and propagules. When AM fungi sporulate, the
number of propagules formed are as many as 14,000 to 38,000 per root have been roughly calculated
in monoxenic cultures (St-Arnaud et al., 1996).

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 Figure 01 Stained root of Hieracium pilosella, colonized by Rhizophagus intraradices (a) with
arbuscules (b) and vesicles (c). Adapted from: Javidnia, Javad. (2013).

AM fungi provide a wide range of benefits to plants like increase the absorption surface area of plant
roots, nutrition availability increases (especially phosphorus), provide protection to stress conditions
like droughts, nematodes, and other agents that cause damage to plants, increase the rate of
photosynthesis, etc. In turn VAM take carbohydrates and fat from plants to survive. Positive effects
were reported in sorghum inoculated with VAM fungi increasing plant height, the number of leaves,
biomass, total nitrogen, phosphorus and potassium uptake ( Nakmee et al., 2016). VAM also play a very
important role in improving the soil structure and texture that ultimately help the plant to develop
better (Thirkell et al., 2017). Fungal hyphae also have a role in decomposition of organic matter
present in the soil (Paterson et al., 2016).

Mechanism of colonization of plant by AM fungi

Formation of symbiotic relationship between AM fungi and roots of plant requires a signaling
pathway, roots of plant secrete a branching factor (BF) that greatly stimulates branching of hyphae
during spore germination of AM fungi. BF initiates mitosis in the hyphae, which is important to frame
new hyphal branches and increment root–parasite contacts. BF first induces expression of genes
related to mitochondrial activity in the fungus, then increases the rate of respiration, and mitochondrial
reorganization prior to stimulating fungal ramification. Later it was found that a strigolactone is the
active molecule in the branching factor. So, first AM fungi activity is stimulated by the hormone
called Strigolactones (root borne signal) which helps in growth of AM fungi in the soil (Besserer et al.,
2006). In response to the chemical secreted by plants, the AM fungi secrete lipochito-oligosaccharides,

9
which are recognized by the plant and initiate the signal transduction pathway that is imparted with the
root nodule symbiosis. Hence, it is called the common signaling pathway. In root cells, a genetically
described signalling pathway gets activated involving calcium spiking in the nucleus as secondary
messenger to accommodate fungus intracellularly (Gutjahr and Parniske, 2013). There are
bidirectional exchanges of symbiosis signals between plant roots and AM fungi that help them to form
a mutualistic relationship.
After these signal pathways, an infectious structure called penetration apparatus starts to form that
allows cellular invasion by the hyphae into the root cell (Genre et al., 2005, 2008), and formation of
arbuscles inside the cell that help in nutrition transport between the partners. The fungal hyphae enter
the cell wall but they don’t cross the membrane of the cell. In plants, nutrients are absorbed at a plant-
derived periarbuscular membrane, which encircle arbuscules of fungal hyphae and has a specific
transporter composition that is required for symbiotic efficiency (Harrison, 2012; Gutjahr and
Parniske, 2013). Once the establishment of AM fungi in the host cells occurs, AM fungi start to
reprogramme the host cells leading to activation of hundred of genes (Hogekamp and Küster, 2013;
Calabrese et al., 2017), some of the genes express primarily in the cell with arbuscles. It is believed
that activation of genes is required to accommodate fungus inside the cells to form the symbiotic
relationship between them.

Figure 02 Entry of VAM fungi into the host cells

Adapted from: https://depts.washington.edu/dislc/Soil%20Life/definition.htm

Genomics of AM fungi

Arbuscular mycorrhizae is a type of endomycorrhiza in which fungal hyphae penetrate inside the plant
cells. AM fungi are obligate symbionts, and cannot grow without their host plants except in very rare
cases. One of the reasons behind obligate biotrophy of AM fungi is their dependence on hosts to
receive carbohydrates, and recent studies have shown that AM fungi also drain lipids from their host

10
plants and the transfer is dependent on the transcription factor RAM2 (REQUIRED FOR
ARBUSCULAR MYCORRHIZATION 2) and the ATP binding cassette transporter–mediated plant
lipid export pathway (Jiang et al., 2017). As they are obligate symbionts, AM fungi are quite difficult
to culture in vitro, especially axenically (Declerck et al., 2005). This inability of AM fungi towards
artificial culture prevents improvements derived from basic research as well as effective agricultural
use. Hence, the molecular genomics of AM fungi are not as advanced in comparison to other fungi.
The first mycorrhizal fungus to have its complete genome sequenced was Laccaria bicolor which is an
ectomycorrhizal fungus (Martin et al., 2008). Till now, the genomes of multiple ectomycorrhizal fungi
have been sequenced and loss of plant cell wall-degrading enzymes has been confirmed to be a
common feature of the genomes of ectomycorrhizal fungi.
In 2013, the first genome sequence of an AM fungus was published for the model strain Rhizophagus
irregularis DAOM197198, it presented new tools to investigate the biology of this symbiosis
(Tisserant et al., 2013). The DAOM197198 genome is homokaryotic with a low nucleotide sequence
polymorphism, and one of the largest fungal genomes, with an oddly high content of transposable
elements (TEs) and a strikingly high number of gene duplications (Tisserant et al., 2013).
The loss of genes encoding plant cell wall-degrading enzymes, thiamine synthase and type-I fatty acid
synthase was revealed by the analysis of the genome of Rhizophagus irregularis DAOM197198
(Wewer et al., 2014). The inability of these fungi to synthesize fatty acids on their own is consistent
with the revelation of lipid transport from plants to AM fungi (Jiang et al., 2017). Hence, finding out
of missing genes that govern important biological processes may provide hints about the essential
nutrient requirements of AM fungi. Such information can also be useful for developing culture
conditions for AM fungi. Tang et al., (2016) proposed that these missing genes of AM fungi can be
recognized as “Missing Glomeromycotan Core Genes (MGCG)” in their transcriptome analysis of two
Gigaspora species. The inability of transcriptome analysis to detect genes with no or very low
expression makes it necessary to confirm the absence of MGCGs at the genomic level. In order to
investigate a common genetic basis for obligate biotrophy in AM fungi Kobayashi et al., 2018
estimated the genome size of R. clarus and it came out to be approximately 146.4 Mbp, which is a
little smaller than that of R. irregularis DAOM197198 which has approximately 153 Mbp (Tisserant et
al., 2012) but much larger than the average fungal genome size (42.3 Mbp) (Mohanta and Bae. 2015).
Absence of cytosolic fatty acid synthase genes is a common feature of AM fungi which plays a pivotal
role in the biosynthesis of long-chain fatty acids (Kobayashi et al., 2018). Kobayashi et al., 2018

11
checked for the absence of MGCG in the R. clarus genome. Among 39 MGCGs, eight genes involved
in thiamine biosynthesis were all absent from the R. clarus and R. irregularis genomes, suggesting
common loss of genes for thiamine synthesis in AM fungi. Several other enzymes were also found to
be absent from both AM fungi. For example, in the metabolic pathway for vitamin B6, AM fungi lack
genes encoding enzymes that convert pyridoxal 5′-phosphate (the active form of vitamin B6) or
pyridoxal into related derivatives such as pyridoxine and pyridoxamine, in contrast to the presence of
these genes in Saccharomyces and Aspergillus. Although AM fungi can synthesize bioactive forms of
vitamin B6, the lack of derivatives might affect some metabolic processes. These specific losses of
vitamin metabolisms were unique characteristics among fungi. Kobayashi et al., 2018 further
suggested that AM fungi may have a reduced ability to utilize cellulose as a substrate compared to
other fungi because the absence of genes encoding β-glucosidases is specific to AM fungi. Low
glycolysis activity in AM fungi is suggestively due to the absence of a gene encoding a glycogen-
degrading enzyme, glucoamylase (EC 3.2.1.3) specifically from AM fungi.

VAM fungi as biofertilizer

Inorganic fertilizers, fungicides, herbicides have been used for a long time, and their usage has come
out as problems to soil, plants, and the consumer health, through their damaging effect on soil health,
food quality, water system, and air. There is an urgent need to replace these harmful fertilizers with
something natural that has the same effect on plant yield and productivity and at the same time it does
not pose any harm to the environment and the consumer health.
Biofertilizers are organic substances which are used to improve the fertility of land. They enhance the
nutritional quality of soil as well as help the plants to develop and thrive better. They are also called
bioinoculants. One of the present day challenges in agriculture is the use of environmental friendly
processes, and the use of VAM fungi has a great impact on agriculture. Different studies on VAM
fungi have revealed that they provide enormous benefit to plants, soil, and environment. Therefore, it
is believed that VAM fungi should be used as a replacement of inorganic fertilizers in the near future,
because they can be a better option to enrich the soil quality over the use of chemical fertilizers
especially phosphorus (Ortas, 2012).
In tropical forests incidences of mycorrhizas have a great influence on soil fertility and thus have
positive effects on plant growth and development (Bagyaraj, 1989). Bisleski (1973) reported that

12
VAM fungi can increase absorption capability of host roots as much as ten times. There are some ions
in the soil like P, Zn and Cu that are not readily dissolved and absorbed in the soil by the plants. Due
to their poor diffusion capacity, plants show deficiency of these immobile ions. VAM symbiosis with
plant roots shows increased nutrition uptake by the hyphae in the soil (Harley and Smith, 1983), and
hence, increase in the plant growth. Mycorrhizal fungal hyphae can increase the effectiveness of
immobile elements by as much as sixty times by extending deep into the soil. The main benefit
derived from symbiosis is phosphate uptake by the plant, however, in some soils ammonium, copper
and zinc are also important (Stribley, 1987). VAM fungi also play a very important role in indirect
benefits that provide additional support to the plant growth and development as well as improve the
surrounding area. Indirect benefits given include increased soil aggregation, improvement in soil
texture, stabilization of soil associated with hyphae. Species of AM fungi have been reported to
increase plant growth directly or indirectly by improving soil conditions (Kapoor and Mukerji, 1990).
Root colonisation by VAM fungi enables the plant to show defence response to biotic stress, for
instance - protection against parasitic fungus or nematode (Cordier et al., 1998). Mycorrhizal hyphae
can explore soil to greater depth and uptake more N, P, K, Zn, Cu, S, Fe, Ca, Mg and Mn elements as
compared to roots and supply them to the host (Marschner and Dell, 1994). In agriculture, crop plants
which are colonized by the VAM fungi show increased uptake of soil minerals. So, the application of
fertilizers and pesticides artificially into the soil has been reduced to a great extent, and on the other
hand, yields of the crop plants have been increased or remain the same (Abbott and Robson, 1991a).
The association between the VAM fungi and roots of plants is providing plenty of benefits not only to
the plants but also to the soil, environment, water, etc. Hence, it is clear that VAM fungi play a crucial
role in nutrient cycling and in turn to the productivity of crop plants.

A) Phosphorus uptake and utilization

Phosphorus is quite possibly one of the most important plant nutrients required by the plants in
relatively in high amounts and plays a crucial role in all biological functions like in energy transfer
through the formation of high energy phosphate esters and is also an essential component of
macromolecules such as nucleotides, phospholipids and sugar phosphates. Phosphate is also associated
in signal-transduction pathways via phosphorylation/dephosphorylation, hence managing key
enzymatic reactions in general cellular metabolism, including N fixation in N-fixing plants
(Schachtman et al., 1998). Generally plants acquire P present in the soil solution predominantly as

13
inorganic phosphate (Pi) (H2PO4-/HPO4-2), having maximal absorption rates at pH 5-6 (Holford, 1997;
Mcivor et al., 2011). Different mechanisms have been proposed to account for increased nutrient
(particularly P) uptake by plants including: (i) increased exploration area in soil through hyphae of
VAM fungi; (ii) increased transport of phosphorus into plants via arbuscules; (iii) changes in root
environment; (iv) efficient utilization of P within plants; (v) efficient way of transfering of P to plant
roots; and (vi) increased storage capacity of absorbed P by plants. AM fungi have been proven to be
more productive than plant roots at taking up phosphorus. One of the main reasons behind formation
of phosphorus deficit/depleted zones around the root is absorption rate of phosphate by roots is quite
faster than diffusion of ions to the absorption surfaces of the root (Bhat and Kaveriappa, 2007). The
extensive extramatrical hyphae of VAM fungi expand deep into the soil for several centimeters so that
AM fungi can cross the nutrient depleted zone around the root and take entry into the nutrient rich
zone. Thus, in this way the plant is capable of utilizing microhabitats beyond the nutrient depleted area
where rootlets and root hair cannot flourish (O’keefe and Sylvia, 1992).
The pace of inflow of phosphorus into mycorrhizae is often up to six times higher than that of the root
hairs (Bolan, 1991). In some cases, the job of phosphorus uptake can be totally taken over by the
mycorrhizal network and all the plant’s phosphorus may be of hyphal origin (Smith et al., 2003).
When plants were grown in phosphorus deficient soil, the amount of phosphorus in roots colonized by
VAM fungi was three to five times higher than in non-colonized roots (Smith and Read, 1997).
Increased P uptake through VAM have been observed in tuber crops such as cassava, potatoes,
cocoyam and yam (Duffy and Cassells, 2000). It is important to mention here that species of AM fungi
differ in the abilities to supply phosphorus to the plant.
VAM fungi have an enzyme called alkaline phosphatase that has the ability to mineralize organic P
sources. Alkaline phosphatase activity is linked to phosphate metabolism of fungus as it is present
within the fungal vacuoles where polyphosphate granules were seen. Arbuscules of VAM fungi
accommodate tiny vacuoles with electron-dense granules, inside which are high levels of phosphorus
and calcium, which highlight the conceivable presence of polyphosphates (White & Brown, 1979).
This is why arbuscules are thought to be the site of intense alkaline phosphatase and possibly ATPase
activity (Marx et al., 1982). The fungus may take up the phosphate from the soil, accumulate it as
granules of polyphosphate, and transfer it in this form along the intercellular hyphae by cytoplasmic
streaming to the active arbuscule. Here, the polyphosphate granules present in fine branches of

14
arbuscules are broken down by enzymatic activities releasing inorganic phosphorus in the cytoplasm
(Callow al., 1978).

B) VAM and Plant Nutrient Uptake

In natural environmental conditions there are many significances of mycorrhizal symbiosis in the
nutrition and well-being of an individual plant. VAM fungi are obligate symbionts. They have
restricted saprobic capacity and are reliant on the plant for their nutrition requirement, which is carbon
produced by plants through photosynthesis. Hexoses, fructose and sucrose are the forms in which
VAM fungi take up the plant host’s photosynthetic product as food. The transfer of carbon from the
plant to the fungi may happen through the arbuscules or intraradical hyphae (Pfeffer et al., 1999).
Secondary synthesis from the hexoses taken by VAM fungi occurs within the intraradical mycelium.
Inside the mycelium, hexose is changed over to trehalose and glycogen. Trehalose and glycogen are
carbon stockpiling forms which can quickly be synthesized and degraded and may increase the
intracellular sugar concentrations (Pfeffer et al., 1999). Up to 20% of the host plant’s photosynthate
carbon may be moved to the VAM fungi (Pfeffer et al., 1999) and approximately 25% of the carbon
translocated from the plant to the fungi is captured in the extraradical hyphae (Hamel, 2005). This
shows a high investment of carbon in mycorrhizal network by the host plant and contribution to the
subterranean organic carbon pool. Increase in the amount of carbon provided by the plant to the VAM
fungi increases the uptake of phosphorus and the transfer of phosphorus from VAM fungi to the host
plant (Bucking and Shachar-Hill, 2005). The efficiency of VAM fungi to take up and transfer
phosphorus decreases when the amount of carbon supplied to the fungi decreases. Hence, plants have
to invest a good amount of carbon to take phosphorus from the fungus. Not just the uptake of P is
enhanced by VAM colonized plant roots, the uptake of other macro and micronutrients like N, Ca,
Mg, S, Cu, Fe, Zn and B has also been enhanced (Allen et al., 2003). A few studies have also shown
the transport of inorganic Nitrogen (N) by VAM fungi (Blanke et al., 2005).

15
NITROGEN

AM fungi facilitate the uptake of nitrogen (N) from the soil. The pH is one of the main factors that
influences the form in which nitrogen is available. Generally, in alkaline soils nitrate is the dominating
form of N (Barea et al., 1987). Nitrate is the primary nitrogen source and is more accessible to plants
in dry soil conditions (Tobar et al., 1994). Nitrate ions are readily mobile in dry soil conditions, hence,
the AM-facilitated uptake of nitrate does not happen unless the mass flow and diffusion to the root
surface is hampered by the unfavourable drought conditions (Smith et al., 1985). AM-facilitated
uptake of nitrate can be regarded as critical for N nutrition of plants in arid and semi-arid agricultural
soils.

The N fertilisation as a typical practice in agricultural lands and considering the costs involved, it is
encouraging to learn that N fertilisation seems to be unnecessary in cases of adequate concentrations
of AM fungi in soils. Heavy nitrogen fertilisation may also result in a reduction in AM fungal
concentration and according to some sources may even be more repressing to AM colonisation than P
fertilisation (Hayman, 1970).

POTASSIUM

Some studies have shown a relatively low AM fungi hyphal capacity for K uptake (Karagiannidis et
al., 1995). Different AM fungal species may also differ in K uptake. A decrease in K concentration in
leaves, as observed by Buwalda et al. (1983), might be as a result of a diluting effect caused by an
AM-facilitated increase in vigour.

IRON (FERROUS ION)

AM fungi are known to improve iron uptake. It was found that AM associations, especially with G.
mosseae, increased the concentration of iron in vines (Bavaresco & Fogher, 1992). An increasement in
the chlorophyll levels is usually associated with an increase in iron uptake, thereafter reducing
chlorosis of leaves.

16
Effects of AM fungi on plant yield and quality

Among beneficial microbes, AM fungi are perhaps the most widespread distributed symbiotic fungi
that colonize the majority of agricultural and forest plants and improve their yield and quality.
Beneficial rhizosphere microorganisms not only improve nutrient status but also improve the quality
of crops, for example improved antioxidant property in AMF-colonized strawberry due to increased
levels of secondary metabolites was reported by Castellanos-Morales et al., 2010. The dietary quality
of crops can be enhanced by affecting the production of carotenoids and certain volatile compounds by
AM fungi. Hart et al., 2015 demonstrated that by applying inoculation of AM fungi the nutritional
status of tomato fruits for most nutrients was improved and had higher antioxidant capacity and more
carotenoids. In a study done by Zeng et al. (2014), increased contents of sugars, organic acids,
vitamin C, flavonoids, and minerals due to Glomus versiforme resulting in enhanced citrus fruit quality
was determined. AM fungi can trigger the biosynthesis of valuable phytochemicals/phytohormones in
edible plants and make them fit and healthy (Rouphael et al., 2015). In watermelon, mycorrhizal
colonization was found to increase not only the plant yield and water use efficiency but also the
quality of the fruits (Kaya et al., 2003). In an extensive study Kim et al., 2017, found that as compared
to uninoculated plants, AM fungi colonized plants had positive effects on the growth of carrot and
sorghum .

VAM fungi help in improvement of soil structure and texture

One of the most important services offered by VAM fungi in natural as well as in agriculture
ecosystems is alternation in soil structure (Leifheit et al., 2014). The highly ramified fungal mycelium
creates a three-dimensional matrix that tangles and crosslinks soil particles. An additional important
agent in stabilization of soil aggregates was found to be a soil glycoprotein (Singh et al., 2013) called
glomalin. It is believed that glomalin is produced in the soil by VAM fungi. Glomalin is often found to
be deposited on outer hyphal walls of VAM fungi and on adjacent soil particles. Glomalin protein
seems to be a rather stable hydrophobic glue that can decrease macroaggregate disruption during
wetting and drying events by stopping water movement into the pores within the aggregate structure
(Miller and Jastrow, 2000). In a study done by Rilling et al., 2003 to investigate the distribution pattern
of glomalin protein across soil horizons, it was found that glomalin was present in A, B, and C
horizons in decreasing concentrations. There is evidence to support that glomalin protein is of VAM

17
fungal origin. When VAM fungi was removed from soil through incubation of soil without host plants,
the amount of Glomalin related soil proteins (GRSP) declined. A similar decline has also been seen in
GRSP concentration in incubated soils from forested, afforested and agricultural land and grasslands
treated with fungicide (Rilling et al., 2003). Glomalin and GRSP represent soil quality determinant and
a very stable carbon sink that has estimated half-life time ranging from several years to decades (Rillig
et al., 2001). Glomalin related soil proteins add to total organic carbon (2-5%) in the soil; they protect
soil organic carbon from degradation by enhanced soil particles aggregation and sequestration of
carbon in the soil (Wilson et al., 2009). Colossal amounts of nutrients are lost from soil through
leaching and gaseous emissions. Nutrient leaching is a serious issue since it brings loss of soil fertility
and pollution of groundwater and surface water like rivers, lakes. These losses can be very damaging
for the environment and expensive in terms of lost agricultural production. Plants associated with
VAM fungi have been shown to reduce nutrients loss from soils by enlarging the nutrient interception
zone and preventing nutrient loss even after rain induced leaching events (Cavagnaro et al., 2015).
VAM fungi aid in water retention capacity of soil that ultimately helps the plant to thrive better.
Benefits of AM fungi like water retention are particularly critical in dry sandy soils in arid regions. In
arid regions the soils show low fertility and high vulnerability to erosion, plantation of mycorrhizal
associated plants in these areas is a suitable way to combat soil erosion and improve soil fertility.

Bioremediation of contaminated soil by AM fungi

Metals are usual contaminants around the world. Presence of high concentrations of heavy metals in
the soil have damaging effects on ecosystems and are a risk to human health as they can easily enter
inside the food chain through agricultural products or contaminated drinking water.
For a long time, there has been a need to find the potential of plants that can reduce the contamination
of soil from heavy metals or organic compounds, and in this scenario AM fungi have the potential to
do so. Mycorrhiza-assisted remediation (MAR) comes out to be a suitable method of remediation that
uses natural organisms like AM fungi for soil remediation. MAR is basically an aspect of
bioremediation that uses mycorrhiza for treatment of contaminated soils. It is a technique that not only
ensures the evacuation of soil pollutants but also ameliorates the structure of the soil and assists in
plant nutrient acquisition Thus, it assists in vegetation/revegetation of polluted land after treatment.

18
Entry et al. (1999) demonstrated through his work that MAR can also be used to treat soils
contaminated with radionuclides such as 137Cs and 90Sr via phytoextraction.
AM fungi have mineral-scavenging capacities, so they can promote growth of plants even in the
contaminated soils; this is referred to as bioremediation of contaminated soil by AM fungi (Göhre and
Paszkowski, 2006). Remediation of heavy metals by using AM fungi can be done in two ways: 1)
accumulating and sequester toxic metal ions, thereby protecting their host from the contaminants
(GonzalezChavez et al., 2004), 2) deliver them to the host just like mineral nutrients resulting in
accumulation of heavy metal ions in the host plants. In the first case scenario, the plant production is
enabled even in the contaminated substrate with least harm to the crop plants. In the second case
scenario, contaminated plants can be reaped and obliterated to lessen the heavy metal loads in the soil
called phytoextraction. In both the approaches heavy metal tolerant species are required to achieve the
desirable goal. Orɫowska et al. (2012) demonstrated that AM fungi species taken from the metal
polluted soil were able to accomplish better remediation than other species introduced from other
locations; this was due to high adaptability of the indigenous species. To increase the pace of
phytoremediation as a viable strategy, fast growing plants with high metal uptaking capability and
rapid biomass gain are required.
Organic pollutants have an affect on soil properties in diverse ways. Organic pollutants are
hydrophobic in nature that influence soil physical properties such as water holding capacity, and
hydraulic conductivity. Trofimov and Rozanova (2003) reported a reduction in water holding capacity,
and hydraulic conductivity of soils polluted with petroleum hydrocarbon. Remediation of organic
pollutants by utilizing MAR are like that of inorganic pollutants except for most organic pollutants
remediation can also be achieved through biodegradation. For example - polycyclic aromatic
hydrocarbons. Mycorrhizal fungi positively influence the activities of some soil microorganisms
(Harrier and Watson, 2004). Thus, the quantity of pollutants remediated via MAR is increased due to
activities of these microorganisms. Structural organization of the organic pollutant affects the rate of
pollutant removal by MAR. Organic pollutants which have high molecular weight and low water
solubility are degraded slower than those with lower molecular weight. The fact that the efficiency of
MAR relies on the sort of pollutant and the fungi species used. Different species of AM fungi can be
employed for effective clean-up of the polluted soil with organic pollutants. Combining MAR with
other remediation methods such as introduction of other microorganisms that supports biodegradation
would also assist in the removal of organic pollutants from soils (Xiao et al., 2012).

19
VAM in agriculture

Majority of agricultural crops are hosts for VAM fungi and can therefore likely benefit from
inoculation with VAM fungi. VAM fungi absorb and translocate mineral nutrients beyond the
depletion zones of plant rhizosphere and induce changes in secondary metabolism leading to better
nutraceutical values and thus, support plant nutrition. Furthermore, phytohormone balance of host
plants can be intruded by VAM fungi, thereby acting as bioregulators by influencing plant
development and bioprotector by inducing tolerance to soil and environmental stresses.
The VAM symbiosis has also been shown to make significant contributions to soil conservation in
agriculture via its role in the formation of water-stable soil aggregates by the extramatrical hyphae.
These aggregates are crucial for creating and maintaining a macroporous, water permeable soil
structure, which is prerequisite for erosion resistance and also important for efficient nutrient cycling.
The significance of VAM in an agricultural crop production system depends chiefly on our ability to
increase the efficacy of the native mycorrhizal fungal population through soil management.
Conventional farming practices, like tillage, input of heavy fertilizers and fungicides, poor crop
rotations and selection for plants which endure these conditions, impede the potential of plants to form
symbiosis with arbuscular mycorrhizal fungi. It is reported that many agricultural crops are more
productive and perform better after being well colonized by VAM fungi. VAM beneficial symbiosis
increases the phosphorus and micronutrient uptake and growth of their plant host. Management of
VAM fungi is crucial for organic and low agriculture systems where soil phosphorus is typically low,
albeit all agroecosystems can drive benefit by encouraging arbuscular mycorrhizae establishment.
Some crop plants have very low capacity to absorb nutrients present in the soil and thus are largely
dependent on VAM fungi for nutrient uptake. It is generally accepted that the level of colonization of
roots by VAM fungi decreases with increase in phosphorus availability. In agricultural lands farmers
often add phosphorus fertilizers in the soil, as a result availability of phosphorus to the plant roots
increases, the quantity of phosphorus also increases within the plant’s tissues and carbon leaving the
plant by the VAM fungi symbiosis emerges as non-gainful to the plant (Grant et al., 2005). Due to
excessive phosphorus levels there is decline in mycorrhizal colonization which can lead to plant
deficiencies in other micronutrients which have mycorrhizal mediated uptake in plants such as copper
(Timmer and Leyden, 1980). For instance Linum usitatissimum, is a flowering plant of the family
Linaceae having poor chemotaxic ability and thus is fairly dependent on VAM mediated phosphorus

20
uptake at intermediate and low soil phosphorus concentrations (Thingstrup et al., 1998). To encourage
the formation of arbuscular mycorrhizal association, threshold levels of soil solution phosphorus that
restrict mycorrhizal development must not be exceeded.
Some beneficial agricultural practices such as reduced tillage, low phosphorus fertilizer input, and
perennialized cropping systems promote the formation of functional mycorrhizal symbiosis. Soil
tillage in agricultural lands reduces the inoculation potential of the soil and the efficacy of mycorrhizas
by disrupting the extraradical hyphal network present inside the soil (Miller et al. 1995; Mozafar et al.
2000). By breaking apart the soil macro structure the hyphal network existing inside the soil is
rendered non-infective (Miller et al., 1995; McGonigle and Miller, 1999). The disruption of the hyphal
network decreases the absorptive capabilities of the mycorrhizae because the surface area spanned by
the hyphae is significantly decreased by breaking soil macro structure. This in turn reduces the
phosphorus uptake by plants which is linked to the hyphal network (McGonigle and Miller, 1999).
Unlike heavy tillage systems, heavy phosphorus fertilizer input is not required in reduced tillage or no
tillage systems. This is because of the increase in mycorrhizal network which permits mycorrhizae to
supply the plant with adequate phosphorus (Miller et al., 1995).
In an extensive experimental study conducted by Hijri, 2016 in North America and Europe, reported
that in a large meta analysis of potato production in 231 field trials in which the same AM inoculant
(Rhizophagus irregularis DAOM 197198) was used. Statistical analysis revealed a significant increase
in marketable potato tuber yield for inoculated fields (42.2 tons/ha) as compared with non-inoculated
controls (38.3 tons/ha). The average yield increase came out to be 3.9 tons/ha, representing 9.5 % of
total crop yield. Rhizophagus irregularis inoculation was profitable with a 0.67-tons/ha increase in
yield, approximately 79-80 % of all trials came out to be more profitable. Impressively, in all these
field trials, the farmers themselves carried out the application and evaluation under their respective
conventional farming practices. Results clearly show the benefits of mycorrhizal-based inoculation on
crop yield, using potato as a case study. Application of these fungi also helps in minimizing the usage
of costly fertilizers without decreasing yield, and hence saving revenue. Further knowledge and
improvements on these beneficial inoculants will help us to compensate for crop production deficits
and support organic farming.

21
Role of VAM in Alleviation of Stress in Plants
AMF have the capability of altering plant physiological and morphological properties in a manner by which
the plant can cope with the stress conditions. AM fungi facilitate better survival of plants under stress
conditions through a boost up in uptake of nutrients particularly P, Zn, Cu and water. They make the host
resilient to unfavourable conditions created by stress factors related to soil or climate. The role played by
these fungi in mitigating the stress on the plant due to drought, salinity, extreme temperatures, heavy meals,
biotic stresses are briefly described below:

A. Drought
Drought is one of the major abiotic stresses that affect the plant severely and leads to significant reduction in
productivity. Drought stress imparts deleterious effects on plant growth by affecting enzyme activity, ion
uptake, and nutrient assimilation (Ahanger and Agarwal, 2017; Dalal and Tripathy, 2018)
Water stress provokes stomatal closure with a subsequent reduction of CO 2 influx resulting in low
photosynthetic activity and carbon partitioning by affected plants (Osakabe et al., 2014) and finally leads to
decrease in plant productivity and agricultural yield. During dry conditions, a variety of physio-biochemical
processes in plants to improve plant health such as increased osmotic adjustment that permits plants to
sustain their turgor and physiological activity are regulated by established symbiotic association (Kubikova
et al., 2001), regulation of stomata by controlling Abscisic acid (ABA) metabolism (Duan et al., 1996),
increased accumulation of proline (Yooyongwech et al., 2013), increased glutathione level (Rani, 2016),
expanded surface area for water absorption provided by AM fungi extraradicular fungi hyphae (Augé, R.M.
2001). ABA incites stomatal closure and prevents cell water loss by transpiration. Inoculation of stressed
plants with AM fungi influences the control of stomata functioning by the regulation of abscisic acid
(Ouledali et al., 2019). Under drought stress conditions the concentration of ABA was found lower in roots
and leaves of mycorrhizal plants as compared to non-mycorrhizal plants (Nakmee et al., 2016; Chitarra et
al., 2016). Jasmonic acid (JA) has also been found to relieve water stress in plants (Yosefi et al., 2018). It
regulates plant responses to water stress conditions by interacting with abscisic acid (De Ollas and Dodd,
2016). Other plant hormones like strigolactone and auxin have also been found to help in plant water stress
regulation (Mostofa et al., 2018).
Subramanian et al., 2006 demonstrated that the roots of tomato plants grown in the field were colonized by
the AM fungi R. intraradices permit plants to grow well under water stress conditions through an

22
enhancement of nutrient contents and water use efficiency in the tomato plants. These advantageous impacts
of AM fungi on tomatoes have also been seen in other plants such as in Lactuca sativa, Triticum aestivum,
Lavandula spica, Allium cepa, etc.

B. Extreme Temperatures
Temperature is one of the major environmental factors that determine the growth and productivity of plants.
Low and high temperature stress negatively influence numerous physiological and biochemical processes
and functions. Temperature stress leads to the disturbance of many physiological and biochemical processes
and functions happening inside the plant system. Arbuscular mycorrhizal fungi has been shown to be
involved in increasing tolerance of plants to temperature stress.
Heat stress severely affects plant growth and development in many ways like loss of plant vigor and
inhibition of seed germination, retarded growth rate, decreased biomass production, wilting and burning of
leaves and reproductive organs, abscission and senescence of leaves, damage as well as discoloration of
fruit, reduction in yield and cell death, etc. When the plants are exposed to high temperature, AM fungi
assist them to develop their root framework for absorption of water to ensure high photosynthetic activity
and to fend off the photosynthetic apparatus from being harmed (Mathur and Jajoo, 2020). During the heat
stress conditions, the development and productivity rate of plants inoculated with arbuscular mycorrhizal
fungi is generally better than the non inoculated ones (Gavito et al., 2005). The association of AM fungi
Glomus fasciculatum with plants leads to positive changes in growth under the conditions of high
temperature stress (Maya and Matsubara 2013).
On the other hand, AMF also increase plant tolerance to low temperature stress. Many reports have
confirmed that various plants inoculated with AM fungi at low temperature conditions showed better growth
over non AM fungi inoculated plants (Abdel Latef and Chaoxing, 2011b). During cold stress, the
inoculation of Barley plants (Hordeum vulgare) with AM fungi lead to improvement in growth,
photosynthesis, osmotic homeostasis and potassium uptake (Hajiboland et al. 2019). AM fungi have the
ability to retain moisture in the host plant, increase the amount of plant secondary metabolites leading to
strengthen plant immune system, and increase protein content for supporting the plants to combat cold stress
conditions (Abdel Latef and Chaoxing, 2011b). AM fungi lead to a significant improvement in the
concentrations of various metabolites in plants that are subjected to cold stress conditions by improving the
chlorophyll pigment synthesis (Zhu et al., 2010a; Abdel Latef and Chaoxing, 2011b).

23
Although, extremely high and low temperatures reduce the AM fungi growth and prevent the formation of
extra radical hyphae network formation, and hence the fungal activity, AM fungi play a crucial role in
mitigating the temperature stresses on plants and assist them to grow better than the non inoculated ones.

C. Salinity
Salinity is a soil condition marked by a high concentration of soluble salts present in soil. Soil salinization is
an important factor due to which the crop plant productivity in agricultural ecosystems is impeded. Among
all salts, sodium chloride is the most dissolvable and abundant salt released that contributes to soil
salinization (Munns and Tester 2008). The basic structure of the soil is altered by the excessive
accumulation of salts in soil, especially Na + ions (Mahajan and Tuteja 2005). Due to presence of Na + ions
in the cation exchange complex, it decreases soil porosity and hampers soil aeration (Manchanda and Garg
2008 ). Low circulation of air in soil because of high soil salt concentration has negative effects on all major
living processes of plants for instance - reduction in plant growth, photosynthetic capacity, protein and lipid
metabolism, nutritional disorder, and ion toxicity in plants (Evelin et al. 2012). Inside the plants the
diversion of energy takes place to neutralize the aggregation of salts in the cells may also contribute to the
stunted growth of the plants grown in saline soils (Evelin et al. 2009).
To alleviate the problem of salinity in soil, plant symbiosis with AM fungi comes out to be the possible
solution for mitigating the salinity-induced adverse effects on plants. AM fungi significantly mitigated the
detrimental effects on photosynthesis under salt stress conditions in maize plants (Sheng et al., 2011).
Some ways by which AM fungi inoculated plants can cope from salinity stress by enhancement of water
absorption capacity and nutrient uptake, the accumulation of osmoregulators like proline and sugars
(Yamato et al., 2008), the ionic homeostasis (Munns and Tester, 2008), and the reduction in Na + and Cl−
uptake (Li et al., 2020), improved stomatal conductance. For example, AM fungi inoculated tomato plants
watered with saline water remarkably increased plant biomass, fruit fresh yield, and shoot contents of P, K,
Cu, Fe, and Zn (Al-Karaki, 2006). The filtering effect of AM fungi structures improves the ionic
equilibrium, both in the soil and in the root that forestalls the entry of toxic Na + ions into the plant system
(Evelin et al., 2009; Santander et al., 2019). AM fungi-colonized plants can diminish oxidative stress by
suppressing lipid membrane peroxidation under salinity stress (Talaat and Shawky, 2014)
Enhancement in fresh and dry weights, and N concentration of Chrysanthemum morifolium plants due to
mycorrhizal inoculation under average saline conditions has been reported by Wang et al. (2018). Increased
production of jasmonic acid, salicylic acid, and several other important inorganic nutrients were seen in the

24
plants inoculated with AM fungi. For instance, concentrations of total P, Ca 2+, N, Mg2+, and K+ were greater
in the AM fungi inoculated Cucumis sativus plants as compared to uninoculated plants under salt stress
conditions (Hashem et al., 2018).
The degree of AM fungi response on plant development as well as root colonization fluctuates with fungal
species, and with the level of salinity present in soil.

D. Heavy Metals
Heavy metals occur naturally in the environment and account for a potential hazard for water, soils, plants,
and sediments. Heavy metals get incorporated in agroecosystem from a variety of sources like the increased
use of agro chemicals in the agricultural lands, the application of metal containing wastes such as sewage
sludge, coal, and wood ashes to soils and from atmospheric deposition (Mhatre and Pankhurst 1997). AM
fungi are generally accepted to support plant establishment in soils contaminated with heavy metals, due to
their capability to strengthen the defense system of the AMF colonized plants to promote growth and
development. Various examinations have demonstrated that over 80% of surveyed plants growing on
mining sites are colonized by AM fungi, and a great number of AM fungi species and a huge AM fungi
diversity exist in different mining-impacted sites (Wang, 2017). AM fungi have the ability to cause the
remediation of heavy metals present in soil through hyphal “metal binding”, which decreases the
bioavailability of elements, such as Cu, Pb, Co, Cd, and Zn (Audet and Charest, 2007). In an experimental
study maize plant was grown in soil contaminated with Cd, AM fungi inoculation significantly increased
growth and decreased uptake of Cd in plant, indicating that AM fungi can be used in association with the
roots of plants for the alleviation of heavy metal loads in the soil such as Cd (Liu et al., 2018).
AM fungi transcribe some metal transporters that play a very important role in mitigating heavy metal stress
in plants. Many Zn transporters have been identified in AM fungi that may be involved in heavy metal
tolerance in plants colonized with AM fungi, such as GintZnT1 from R. irregularis (González-Guerrero et
al., 2016). Several genes coding for Cu, Fe, and Zn transporters have also been recognized. AM fungi
presumably tie Cd and Zn in the cell wall of mantle hyphae and cortical cells, thereby limiting their uptake
and resulting in better growth, yield, and nutrient status of metal stressed plants (Garg and Chandel, 2012).
Regardless of expanding information in AM fungi plant interaction under heavy metal stress, only little is
known about whether there is a synergism between plant and fungal heavy metal tolerance. It tends to be
estimated that tolerant AMF may confer additional heavy metal tolerance on its host thus leading to their
higher endurance rate and reproductive success on the contaminated sites.

25
E. Biotic Stress
The capability of micro-symbionts in the management of biotic stresses is gaining importance. Plants are
subjected to attack by various organisms like fungi, bacteria, viruses and nematodes. AM fungi can
significantly mitigate the adverse abiotic stress on plants and permit plants to thrive better in harsh
environmental conditions, but the roles of AM fungi in mitigating the stress are not only limited to abiotic
stress, AM fungi have been found equally potent in alleviating the biotic stress in plants.
Many researches conducted in the last few years have demonstrated that symbiotic associations established
between the plants and AM fungi confers resistance to the plants enabling survival from pathogen attack but
the hidden molecular mechanism governing mycorrhiza-induced resistance (MIR) is not well identified yet.
Cameron et al., 2013 described mycorrhiza-induced resistance (MIR) to diseases. MIR mediated by
mycorrhiza is a complicated response intervened by hormonal crosstalk. The contribution of jasmonic acid
and salicylic acid in MIR against Alternaria alternata was studied by evaluating the degree of enzymes
involved in their biosynthesis as well as the intrinsic levels of these hormones. It was observed that the
higher levels of these enzymes correlated well with the hormonal levels in the inoculated plants. Moreover,
increased expression of genes involved in jasmonic acid biosynthesis as well as salicylic acid responsive
genes like PR1 and wound-inducible polypeptide prosystemin further proved these observations (Nair et at.,
2015).
Fact that AM fungi significantly contribute to plant protection against pathogenic fungi and nematodes is
well archived. Although, it needs to be mentioned that the effectiveness of the formed interactions varies
depending on the host plant and the cultural system. Roots of tomato plants colonized by F. mosseae
induced systemic resistance against both the sedentary nematode Meloidogyne incognita and the migratory
nematode Pratylenchus penetrans (Vos et al., 2012). AM fungi significantly reduced the nematode infection
by 45% and 87% for M. incognita and P. penetrans, respectively, in AM fungi colonized plants as
compared to controls. Further examinations have shown that the reduction of nematode infection in
mycorrhizal plants is most likely related to an alteration of their root exudates by AM fungi (Vos et al.,
2012). AM fungi can also confer protection to other pathogenic fungi which cause harm to many plants for
example - mycorrhizal inoculation with F. mosseae significantly mitigated tomato diseases caused by
Alternaria solani and Fusarium oxysporum (El-Khallal, 2007). Tobacco and alfalfa plants inoculated with
AM fungi have been reported to be resistant against a plethora of fungal pathogens like Phytophthora
megasperma, Pyrenochaeta terrestris, Fusarium oxysporum, Pythium ultimum etc. (Kaye et al., 1984;
Schenk, 1981).

26
 Apart from the role played by mycorrhizas in providing protection against pathogen attack,it has also been
shown to give protection against herbivory. For instance - Inoculation of tomato plants with Glomus
mosseae negatively affected the larval activity of chewing caterpillar Helicoverpa armigera by inducing the
expression of defense-related genes like LOXD, AOC, PI-I, and PI-II and also switch on the jasmonic acid
pathway (Song et al., 2013).
African witchweed Striga is a parasitic plant. It creates socio economic problems that have compelled
numerous poor farmers to relinquish their farms due to high infestation rates. Soil microorganisms including
AM fungi have the potential to stifle or inhibit Striga germination. The interaction between Striga and
cereals can be influenced by AM fungi. It was found that AM fungi negatively impacted Striga seed
germination, decreased the number of Striga seedlings attaching and emerging, and delayed the emergence
time of Striga (Lendzemo et al., 2006). The defensive response inflicted on the plants by mycorrhizal
inoculation is profoundly dependent on the differential impact of the AM fungi on the physiology of the
plants, type of the pathogen and at last the capacity of the plants to adjust to the changing conditions in
response to the biotic stresses.

Table 01: Study to evaluate the effects of VAM on plants

S.No Host Species Organism Observed Responses Remarks References
Used

1. Zea mays vesicular Increased Seed per fruit, Productivity was checked in Mobasser and
arbuscular biological yield, seed yield, water deficit condition. The Tavassoli
mycorrhiza harvest index and protein most biological and seed yield (2013.
content of seeds. was obtained from V4S0
treatment.

27
2. Marsdenia vesicular Growth parameters The plant biomass was Sandhya et al.
volubilis arbuscular like plant height, root improved along with increasing (2013)
mycorrhiza, length, fresh and dry the incubation periods. After 90
and weight of shoot and root, days total fresh biomass in
phosphate chlorophyll content, T4(combined inoculation of
solubilising reducing and non-reducing VAM and PSB) was highest
bacteria. sugars, starch, lipid and 6.07g and least in T1(control)
protein contents in root and 3.15g.
shoot samples were
maximum with dual
inoculation than
individually.

3. Allium spp. vesicular VAM-inoculated plants AM fungi increased the size and Koch et al.
(Garlic) arbuscular were larger and had more weight of garlic bulbs. The (1997)
mycorrhiza green leaves than plants in mean bulb weights for
uninoculated plots. uninoculated and VAM-treated
Increased photosynthesis plots were 27 g and 51 g
rate, especially at low light respectively.
intensities was observed.

4. Zea mays Glomus Concentrations of P and Cu The effects of mycorrhizae Sylvia et al.
etunicatum were increased in both under different water conditions (1993)
shoot and grain of maize. that are fully irrigated, moderate
Biomass and grain yields water stress and severe water
were increased linearly stress on the growth and grain
with irrigation levels. yield of Zea mays was studied.

5. Tagetes Glomus Available N, P, K contents The treatment inoculated with Swathi et al.
erecta L fasciculatum, of soil were notably Glomus mosseae showed (2017)
Glomus influenced by Glomus maximum available N and P
mossea, fungi. Except N, the (291.67 and 40.67 kg/ ha,
Glomus available P and K content respectively), whereas, G.
intraradices. of soil increased even after fasciculatum showed maximum
harvest of the crop as available K (165.67 kg/ ha) in
compared to initial status. the soil. The treatment
inoculated with G. mosseae
recorded significantly maximum
exchangeable Ca, Mg and
available S content and least
was observed in G.

28
 intraradices.

6. Cenchrus Gigaspora Water use efficiency and Maximum water use efficiency Khan et al.
ciliaris rosea, yield increased by was seen in combination of (2008)
Glomus inoculation of plants with Glomus etunicatum + Glomus
intraradices, mycorrhizae under both the intraradices. Yields were also
Glomus water regimes (100% field increased by increased water use
etunicatum. capacity and 50% field efficiency.
capacity).

7. Ruta Glomus Increased plant height, root The maximum plant biomass Murthy and
graveolens mosseae, length and number of (45.4g/plant) was found with M. (2015)
Glomus compound leaves. dual inoculation of Glomus
fasciculatum. mosseae + Glomus
fasciculatum treated plants, and
minimum in control
(27.5g/plant).

8. Muskmelon Glomus Increased plant height, In soilless grown melon plants, Abak et al.
(Cucumis mosseae, stem diameter, number of four different AM fungi species (2010)
melo) Glomus leaves, fresh weights of significantly increased plant
etunicatum, root, stem and leaves. growth in comparison to control
Glomus treatment. Among AM fungi
fasciculatum species G. caledonium and G.
and Glomus fasciculatum had better
Caledonium compatibility with melon plants
for stimulating plant vegetative
growth.

9. Lycopersicon Rhizophagus A significant increase in Positive correlation between Tallapragada

esculatum, intraradices, biomass, root length, shoot percentage colonization and et al. (2016)
Capsicum Rhizophagus length, and chlorophyll chlorophyll content, root length,
annuum fasciculatum, content was observed. catalase activity, and guaiacol
Burkholderia Reduced proline peroxidase has been observed
seminalis concentration. that shows importance of AM
fungi in drought tolerance.

10. Solanum Pseudomonas Increased flower and fruit VAM improved the citric acid Bona, et al.
lycopersicum strains, VAM production. Enhanced the concentration in tomatoes, while (2017)
concentration of sugars, bacteria positively modulated
organic acids and vitamins sugar production and sweetness

29
 in tomato fruits. Improved in tomatoes.
citric acid levels in
tomatoes.

11. Boswellia AM fungi Increased biomass, Under drought imitated Birhane, et al.
papyrifera (Glomus) stomatal conductance, conditions, mycorrhiza (2012)
phosphorus mass fraction inoculated plants performed
in shoot and root were better in terms of growth, water
observed in mycorrhizal use efficiency, and
inoculated plants. photosynthesis. Increased
assimilation rate per unit leaf
area coincided with higher P
mass fractions in mycorrhizal
seedlings.

12. Pterocarpus Glomus Improved plant growth and AMF improved flooding Fougnies et al.
officinalis intraradices, phosphorus acquisition in tolerance in Pterocarpus (2007)
Bradyrhizobi leaves. officinalis. Development of
um sp. adventitious roots, aerenchyma
tissue, and hypertrophied
lenticels played a critical role in
flood tolerance by increasing
oxygen diffusion to the
submerged part of the stem and
root zone, and hence
contributing to growth.

13. Cyclamen Glomus Increased heat stress By increased antioxidative Maya and
persicum fasciculatum tolerance, biomass activity, AM fungal colonisation Matsubara
production, activity of mitigated the temperature stress (2013)
antioxidative enzymes such of cyclamen plants
as superoxide dismutase,
ascorbate peroxidase, and
contents of ascorbic acid
and polyphenol. Reduced
leaf browning under heat
stress conditions.

14. Capsicum Glomus Increased plant growth, Under different salinity Beltrano et al.
annuum intraradices mineral content, cell conditions and phosphorus (2013)
membrane integrity, levels, mycorrhizal inoculation

30
 proline content, chlorophyll was capable of alleviating the
content, and reduced shoot damage caused by salt stress on
content of Na. pepper plants.

15. Lycopersicon Glomus sp. Production of antimicrobial Protection of Lycopersicon Kumari and
esculentum compounds from the AMF esculentum from wilt pathogen Prabina
( Infected) colonized root that arrested Fusarium oxysporum f. sp. (2019)
the growth of the fungal Lycopersici by AMF.
pathogen. Increased plant Experiment demonstrated that
biomass, N, P, K content, the pre AMF and post pathogen
chlorophyll content and inoculation to tomatoes
yield of the plant alleviated the disease incidence
and increased the plant
productivity.

5. Significance
The review provides the comprehensive knowledge on vesicular-arbuscular mycorrhiza, and its
symbiotic relationship with the roots of plants. This study is beneficial to provide knowledge on how
the use of chemical fertilizers have adverse effects on plants as well as the environment. This study
encourages the replacement of chemical fertilizers in agriculture to VAM that can be helpful in
achieving the same goal with no bad impacts on plants and the environment. It also focuses on the
capability of VAM against soil pathogens which cause damage to the plants and have adverse effects
on crop production in agriculture. It also highlights the future research directions in mycorrhizal
association with roots of plants and its application in agriculture.

6. Conclusion and Future Prospects

Vesicular arbuscular mycorrhizal fungi have the potential to affect many aspects of plant life. Many
research studies have already documented the role vesicular-arbuscular mycorrhiza in growth and
development of plants associated with VAM fungi. Therefore, in this work, the existing information
related to the different roles of VAM fungi in improving plant health, productivity, and resistance to

31
biotic and abiotic stresses have been taken into account and combined in a coherent way for
understanding VAM fungi symbiosis with roots of plants.
The benefits of the symbiosis for nutrient uptake by plants in restoration, management and
sustainability in agro-ecosystem is very important. In agriculture, the use of chemical fertilizers is the
need of the hour. An environmentally friendly solution to reduce the use of hazardous pesticides and
industrial fertilizers is VAM fungi. Other benefits provided by VAM are like bioremediation of
contaminated soil, improving the structure and texture of soil, and decrease in nutrient leaching from
the soil, thereby contributing to the retention of nutrients in the soil. The mycorrhizal inoculation of
VAM fungi is very useful for plants to uptake phosphorus from the soil as phosphorus is the one of the
major deficit elements for plants in the soil, and can be the eco friendly replacement of phosphorus
fertilizer.
Commercial mycorrhizal products are available in different forms like tablets, granules, powder and
liquid that can be easily applied on crop plants. Encouragement of VAM usage is of immense
importance for modern global agricultural systems for their consistent sustainability.
Genes and gene products that regulate the VAM mediated growth and development regulation under
different conditions have been studied through transcriptomics and proteomics. The focus of future
research should be on the identification and functional characterization of such genes. Understanding
of VAM mediated processes to induce modulations in the tolerance mechanisms and the crosstalk that
triggered to regulate plant performance can help enhance crop productivity. VAM and VAM along
with other microorganisms make the biofertilization affordable for farmers who need their cropping
system to be as highly sustainable as possible to meet the growing demands.

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