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Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation

May 2021
Symbiosis 84(12)

May 2021
84(12)

DOI:10.1007/s13199-021-00756-6

Authors:

Parashuram Bhantana

Huazhong Agricultural University

Muhammad Shoaib Rana

Huazhong Agricultural University

Mohamed G. Moussa

International Centre for Biosaline Agriculture

Show all 15 authorsHide

Arbuscular mycorrhizae fungi (AMF) are a big player of the ecosystem which shows a major concern over plant nutrition by providing access to the soil-derived nutrients. Naturally, an intimate association between plant roots and AMF is observed. AMF are involved in improvement on the soil water regime and nutrient uptake both in the biotic and abiotic stress situations such as drought, temperature extreme, heavy metals, salinity, pathogen and metal pollution. This kind of symbiotic relationship between plant roots and fungal hyphae is observed to be 80% of the terrestrial plant species worldwide. In plant AMF association fungal hyphae are benefitted by obtaining sugar from the host plants root and host plants root are ameliorated by improved uptake of water and nutrients from soil surface. AMF have a dual role to manage the Zn nutrition in soil. For example below a critical Zn concentration, Zn uptake is enhanced by AMF application and above the critical level, Zn translocation to plant shoots is restricted. Synergistic association between Zn and AMF is important for sustainable yield and quality. It is observed that grain Zn content in the field is increased with applying AMF. AMF help in the plant growth, development and reproduction, as the Zn is essential for pollen tube formation. By AMF application there is an increment in the content of lycopene, vitamin C, vitamin A and antioxidant activities than non AMF plants in tomato. In traditional driven agriculture, inherent soil fertility is the major source of P with an occasional supply of manure for the crops. But after modernization in agriculture results in overexploitation of the P and results in low crop yield and farm income. Rock phosphate is the major source of the phosphatic fertilizer and is non-renewable which could be exhausted in the next 50–100 years. Moreover, the stimulation of secondary metabolites synthesis results in the improvement of crop quality by sustainable use of phosphatic fertilizers. So P application techniques which can also ameliorate AMF are widely promising. This is how AMF play a pivotal role in developing present era farming practices towards sustainable agriculture. Phytoremediation of heavy metals from different soil types has potential benefit of using AMF in soil. Mycorrhizae disrupt the uptake of the different heavy metals from the rhizosphere and movement from the root to the aerial parts. The major role of AMF in plant growth and development during stressful environments is to translocate important immovable nutrients like Cu, Zn and P and reducing metal toxicity in the host plant.

ew of microscopic examination of soybean root under a light microscope (40X) in a work from the Nepal Agricultural Research Council, Agricultural Research Station, Pakhribas Dhankuta Nepal. (a) Root section not colonized in the control treatment (b) root section colonized with Piriformospora indica (Black arrow showed the position of the chlamydospore inside cortical root cells)

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Arbuscular mycorrhizal fungi and its major role in plant growth, zinc

nutrition, phosphorous regulation and phytoremediation

Parashuram Bhantana

1,2,3

&Muhammad Shoaib Rana

1,2

&Xue-cheng Sun

1,2

&Mohamed G. Moussa

1,2

Muhammad Hamzah Saleem

&Muhamad Syaifudin

1,2

&Ashrafuzzaman Shah

1,2

&Amrit Poudel

Amar Bahadur Pun

&Mufid Alam Bhat

&Dhanik Lal Mandal

&Sujit Shah

3,6

&Dong Zhihao

1,2

&Qiling Tan

1,2

Cheng-Xiao Hu

1,2

Received: 5 November 2020 / Accepted: 9 February 2021

#The Author(s), under exclusive licence to Springer Nature B.V. 2021

Abstract

Arbuscular mycorrhizae fungi (AMF) are a big player of the ecosystem which shows a major concern over plant nutrition by

providing access to the soil-derived nutrients. Naturally, an intimateassociation between plant roots and AMF is observed. AMF

are involved in improvement on the soil water regime and nutrient uptake both in the biotic and abiotic stress situations such as

drought, temperature extreme, heavy metals, salinity, pathogen and metal pollution. This kind of symbiotic relationship between

plant roots and fungal hyphae is observed to be 80% of the terrestrial plant species worldwide. In plant AMF association fungal

hyphae are benefitted by obtaining sugar from the host plants root and host plants root are ameliorated by improved uptake of

water and nutrients from soil surface. AMF have a dual role to manage the Zn nutrition in soil. For example below a critical Zn

concentration, Zn uptake is enhanced by AMF application and above the critical level, Zn translocation to plant shoots is

restricted. Synergistic association between Zn and AMF is important for sustainable yield and quality. It is observed that grain

Zn content in the field is increased with applying AMF. AMF help in the plant growth, development and reproduction, as the Zn

is essential for pollen tube formation. By AMF application there is an increment in the content of lycopene, vitamin C, vitamin A

and antioxidant activities than non AMF plants in tomato. In traditional driven agriculture, inherent soil fertility is the major

source of P with an occasional supply of manure for the crops. But after modernization in agriculture results in overexploitation of

the P and results in low crop yield and farm income. Rock phosphate is the major source of the phosphatic fertilizer and is non-

renewable which could be exhausted in the next 50–100 years. Moreover, the stimulation of secondary metabolites synthesis

results in the improvement of crop quality by sustainable use of phosphatic fertilizers. So P application techniques which can also

ameliorate AMF are widely promising. This is how AMF play a pivotal rolein developing present era farming practices towards

sustainable agriculture. Phytoremediation of heavy metals from different soil types has potential benefit of using AMF in soil.

Mycorrhizae disrupt the uptake of the different heavy metals from the rhizosphere and movement from the root to the aerial parts.

The major role of AMF in plant growth and development during stressful environments is to translocate important immovable

nutrients like Cu, Zn and P and reducing metal toxicity in the host plant.

Keywords AMF .Zinc .Phosphorous .Phytoremediation .Nutrient uptake .Fruit quality

*Parashuram Bhantana

pabh@webmail.hzau.edu.cn

*Cheng-Xiao Hu

hucx@mail.hzau.edu.cn

Key Laboratory of Arable Land Conservation (Middle and Lower

Reaches of Yangtze River), Ministry of Agriculture, Micro-elements

Research Center, College of Resource and Environment, Huazhong

Agricultural University, Wuhan, Hubei Province 430070, People’s

Republic of China

Hubei Provincial Engineering Laboratory for New Fertilizers,

Huazhong Agricultural University, Wuhan, Hubei Province 430070,

People’s Republic of China

Agricultural ResearchStation, Nepal, Agricultural Research Council,

Pakhribas, Dhankuta, Nepal

Key Laboratory of Crop Ecophysiology and Farming system (Core

in the Middle reaches of the Yangtze River), Ministry of Agriculture,

College of Plant Science and Technology, Huazhong Agricultural

University, Wuhan 430070, China

National keylaboratory of crop genetic improvement, College of life

science and technology, Huazhong Agricultural University,

Wuhan 430070, China

Daffodil Agro Biological Research Center, Lalitpur, Nepal

Symbiosis

https://doi.org/10.1007/s13199-021-00756-6

1 Arbuscular mycorrhizal fungi (AMF)

The incorporation of arbuscular mycorrhizal fungi (AMF) are

one of the promising technology in studying the soil plant

atmosphere continuum. The use of AMF in the field crop

production is increasingly used in biodynamic farming

(Malik et al. 2011). Instances in which AMF responded to

crop plants are the improvement of plant and water uptake

as a result of root expansion with fungal hyphae, protecting

against biotic and abiotic stresses and enhancement of plant

antioxidant status (Basu et al. 2018; Begum et al. 2019). Even

more, AMF establish symbiotic associations with more than

80% of the terrestrial plants, and the colonization rate partic-

ularly depends upon the fungi, plant species and environmen-

tal factors for example soil characteristics (Kim et al. 2017). It

is highly important to use AMF for the production of fruit,

vegetable and medicinal crops as AMF increased the accumu-

lation of macroelements (N, P) and microelements (Zn, S, Cu,

Fe and Mn) (Chen et al. 2017). AMF species are different in

the effect of soil biota from different soil management prac-

tices that affect yield and quality. An increase in the seed

protein is observed in AMF treated soil than the untreated

one. Similarly, there is an increment in the oleic acid and a

decrease in the linoleic acid in comparison to untreated con-

trol. Major research findings suggested that the yield and qual-

ity of soybean are affected by crop management practices and

soil biota composition (Marro et al. 2020). Different soil mi-

croorganisms affect the yield and quality of the crop. Among

these, AMF are one of the major plant root symbionts. The

more diverse the AMF community the higher the plant growth

(Marro et al. 2020). Change in the AMF composition affects

the cropping system of plant and their diversity (Rillig et al.

2019).

AMF improve soil water nutrients and water regimes and

increase tolerance of a plant to drought, temperature extremes,

heavy metals, salinity, pathogen and metal pollution (Begum

et al. 2019). Moreover, the stimulation of secondary metabo-

lites synthesis results in the improvement of crop quality. So

AMF play a pivotal role in developing present era farming

practices towards sustainable agriculture. At the beginning

of the twenty-first-century agricultural sector has paid atten-

tion to ecologically sound, economically viable and nutrition-

ally rich AMF approach (Golubkina et al. 2020b). There are

both a comparative and competitive advantage of using AMF

in agriculture. Therefore three major factors that support the

application of AMF to Allium plants are increasing economic

importance of the plant, decreasing the use of mineral fertil-

izers and herbicides and production of a high amount of anti-

carcinogenic substances (Golubkina et al. 2020b).

Declining use of chemical fertilizers and agrochemicals

and improvement of the quality of food crops, fruits, vegeta-

bles, and the ornamental plant is the prerequisite in the current

scenario of organic farming (Golubkina et al. 2020b). AMF

inoculation in plants are host-specific and the activity of AMF

on the host is governed by a set of biotic, abiotic and environ-

mental factors like temperature and precipitation (Golubkina

et al. 2020b). In comparison to natural ecosystems, most ag-

ricultural soil has a lower content of AMF. Disruption of the

hyphal network in agroecosystem due to tilling, crop rotation,

use of agrochemicals and fallow periods has caused the dif-

ference between an agricultural ecosystem and natural habitat.

AMF diversity are not the only factor affecting onion yield

under conventional and organic farming, however is an im-

portant contributor.

Mycorrhization is the degree to which plant roots get col-

onized with AMF. Mychorrhization is calculated as the ratio

of root segments which is colonized to the number of seg-

ments examined (Singh et al. 2020). AMF impart a major role

in major agronomical and horticultural crops. Colonization

value of 28.2–36.4% of the total root length was observed

by Kim et al. 2017 and Bianciotto et al. 2018. AMF also help

in the regulation of water stress in a plant by penetrating hy-

phae towards wet areas. AMF are well known that plants

colonized with AMF are suited to grow in less fertile soil

due to the increased absorption of mineral elements by hy-

phae. AMF may have an important role in maintaining soil

health. Besides, AMF boost plant enlargement and accelerate

biochemical and enzymatic activities (Sivakumar et al. 2020).

The frequency of colonization varied from 27 to 50% and

mycorrhization of about 10% is observed (Copetta et al.

2020). In most of the horticultural crops, the colonization is

estimated up to 80% (Tarkka et al. 2018). Uptake of P from

the soil via AMF caused increased colonization of plant roots

to absorb soil nutrients (Sadhana 2014). Also, there isa hyphal

web for significantly enhancing the uptake of nutrients. The

rhizosphere zone that is called as mycorrhizosphere is influ-

enced by AMF. Enhanced plant nutrient uptake, antioxidant,

root architecture modification and enzyme production are af-

fected by AMF. Similarly, other roles of AMF in crop pro-

duction are stress tolerance, activation of defense mechanism

and accumulation of several phytochemicals (Olowe et al.

2018). Beyond increasing yield, incorporation of mycorrhiza

has shown to increase the nutritive value of horticultural crops

(Rouphael et al. 2017). Modification of primary and second-

ary metabolites and production of phytochemicals caused en-

hanced taste and better health protection (Sbrana et al. 2014).

An understanding of AMF in association with the complexity

of the soil-plant environment complex is essential before the

beginning of the targeted experiment. The function of native

AMF in the root of cashew replace the artificially inoculated

AMF. Thus the AMF inoculated did not have a significant

impact on the uptake of mineral nutrients, growth, yield and

biomass of cashew seedlings. Even more, the role of AMF on

the cashew plant was suppressed in the studied soil (Ibiremo

et al. 2012). So AMF have promising results in fruit trees and

additional knowledge on the cultivation of fruit trees in

Bhantana P. et al.

relation to AMF need to be done. Differences between root

colonized and non-colonized hyphae are observed in soybean

roots under a light microscope with AMF mimicking mycor-

rhiza, Piriformospora indica. The pear-shaped structure chla-

mydospore is shown in Fig. 1.

AMF applied crops require chemical fertilizer and plant

protection chemicals in lower amounts than non-AMF applied

crops. Since there is less application ofchemical fertilizers and

agrochemicals, AMF application increased crop quality

(Rouphael et al. 2015) The use of organophosphorus pesti-

cides both in soil and vegetables has been decreased signifi-

cantly by the application of AMF(Bennett and Meek 2020).

AMF influence plant reproduction by affecting pollen deliv-

ery, pollen tube growth, pollen germination, fertilization and

seed germination (Bennett and Meek 2020). The mycorrhizal

pathway is one of the ways to enhance uptake of phosphorus

(P) and Zn. The benefit of AMF is higher in soil deficient in

available Zn and also in the soil where Zn is applied

(Lehmann et al. 2014). There is also an increment in the yield

afterAMFapplicationasAMFarealsoreferredtoas

biofertilizers. Moreover, the AMF are acting as a major ele-

ment for phytoremediation able to alleviate the toxic effect of

Ag, Fe and Zn NPs (nanoparticles) (Cao et al. 2016). The

increment in the global consumption of fertilizer is increasing

rapidly in recent years. The consumption of N and P fertilizers

has increased by 9.1 and 4.3 times respectively (IFA 2019)

with only a 3.4 times increase in the food grain production

(FAO 2019). The recovery efficiency of the applied N and P

fertilizeris 50% and 30% respectively. The excess application

of N fertilizer caused environmental pollution through green-

house gas emissions. The conventional technique of fertilizer

recommendation based on soil tests ignore spatial and tempo-

ral variability in soil N supply and are not a suitable plan for

judicious N use (Singh et al. 2020). Dramatic changes in the

agricultural practices of the twentieth century have been taken

place with the widespread use ofchemical fertilizers, advance-

ment in breeding techniques for the production of high yield-

ing crops and their varieties (Smil 1999; Pingali 2012). In the

scenario of changing world climate driven by the appearance

of novel plant protection measures, increasing exposure of the

plant to stress environments, declining availability of organic

nitrogen a new approach of climate-smart agriculture is nec-

essary (Cassman 1999).

More recently the impact of AMF symbiosis in N uptake

have practiced. AMF have a direct or indirect role in N-cycling

processes in the soil. Changes in the soil aggregation and aer-

ation in the soil show an impact on the denitrification processes

and reduce leachate of inorganic N. There is a strong correla-

tion between leaf chlorophyll content and photosynthesis. And

N has an important role in chlorophyll formation. So a direct

relation between N content, CO

assimilation rate, chlorophyll

content and rubisco activity is reported (Coskun et al. 2017;

Valkov et al. 2020). Moreover the presence of AMF in soil

affect pH and N availability in soil. Shifting the microbial

community in the rhizosphere and the surrounding bulk soil

using both fungal and AM mediated root exudates. AMF pre-

ferred to uptake N in the form of NH

and transferred to

cytoplasm which is translocated into the intraradical hyphae

via vacuole and the NH

is released in the apoplastic com-

partment (Jin et al. 2005; Govindarajulu et al. 2005). In the

case of a non-colonized plant the reduction of NO

mainly

occur in the leaves but in AMF colonized plant the reduction

of NO

occurs in plant roots (Kaldorf et al. 1998). Besides, the

glutamine synthetase-glutamate synthase (GS and GOGAT)

activities are significantly higher in plants colonized with

AMF than non-colonized (Field and Mooney 1983; Pilbeam

2018). It is still unclear how the plants uptake the ammonium

released by the AM fungi (Balestrini et al. 2020). In the roots of

the mycorrhizal plant high amount of several amino acids have

been transferred to the amino acid of the colonized host. AMF

symbiosis can affect the modification of the physiology and

environment of the host caused enhanced nutrient uptake,

without the aid of direct phosphorous. Perhaps, increased in

colonized plants for a changein the composition ofsoil micro-

bial community (Elliott et al. 2020). Increasing nutrient use

efficiency and tolerance to abiotic stresses is the key role of

AMF in agriculture (Carillo et al. 2020).AMFhelpincrop

productivity and reduce the negative factors in agriculture.

Fig. 1 View of microscopic

examination of soybean root

under a light microscope (40X) in

a work from the Nepal

Agricultural Research Council,

Agricultural Research Station,

Pakhribas Dhankuta Nepal. (a)

Root section not colonized in the

control treatment (b) root section

colonized with Piriformospora

indica (Black arrow showed the

position of the chlamydospore

inside cortical root cells)

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

AMF have an important role in increasing the growth and

productivity of tomatoes and other crops. AMF increase the

number of fruits per plant (Carillo et al. 2020).

2 Plant growth

Some common features of AMF affecting plant growth and

development are nutrient acquisition, growth (Kim et al.

2017), resistance against the pathogens (Pérez-de-Luque

et al. 2017), drought (Chitarra et al. 2016) and harsh environ-

ments (Begum et al. 2019). As the world is increasing need for

Zn in the crops and their varieties are differentiated as sensi-

tive or tolerant ones. The field experiment conducted by Al

Mutairi et al. 2020separated five barley varieties into sensitive

and tolerant varieties as Amaji Nijo, Lofty Nijo and Haruna

Nijo are Zn sensitive and Compass and La Trobe are tolerant

varieties (Genc et al. 2004). There is a reduction in the dry

biomass of mycorrhizal associated barley plants that showed a

negative response to AMF inoculation (Al Mutairi et al.

2020). All five varieties of barley have the same level of root

colonization (Al Mutairi et al. 2020). The results cited previ-

ously showed the formation of mycorrhizal colonization in

barley is a factor of both cultivar and AMF species-

dependent (Al Mutairi et al. 2020). Environmental fluctuation

and short term heat or drought stress affect yield, biomass and

growth of the plant. Barley variety Compass and La Trobe

have higher straw Zn concentrations in comparison to other

varieties. In bread wheat plant with higher Zn content is more

competitive than Zn deficient. Barley is non-responsive to

AMF where other crops like rice, wheat, millet and corn

responded to the AMF positively (Zhang et al. 2019).

However, there is a possibility of increased mean grain weight

suggesting potential increase grain weight through AMF in-

oculation (Ercoli et al. 2017; Zhang et al. 2019),as it has been

shown in durum wheat, bread wheat and barley an improve-

ment in the yield is achievable with the application of

R. irregularis (Ercoli et al. 2017; Zhang et al. 2019).

Plant growth and development are directly linked to the

assimilation of CO

by the photosynthetic apparatus

(Balestrini et al. 2020). The rhizosphere plays a vital role in

plant growth and development by providing water and nutri-

ent uptake. Soil microbiota residing inside the rhizosphere

have a prominent role in photosynthesis. Similarly, mycorrhi-

zal biomass helps to sustain the growth and development of

the plants and their wild relatives. Microbial activities in a thin

layer of soil are considered one of the most complex ecosys-

tems and a hot spot (Compant et al. 2019). AMF are one of the

most important groups of plant symbionts and positively af-

fects growth, tolerance to biotic and abiotic stress, and plant

nutrition (Chen et al. 2018). The role of AMF in plant nutrition

is to exchange mineral nutrition to plant with carbohydrates

and lipids. However, a variety of studies are done the factors

which accentuate trade between AMF symbiosis are lacking

(Wipf et al. 2019; Walder and van der Heijden 2015). An

increase in photosynthesis rate due to enhanced rhizospheric

sink strength and increasing accumulation of P has been re-

ported with AMF (Black et al. 2000). The level of increase in

chlorophyll, photosynthetic enzymes, ATP and inorganic

P(Pi) in leaves can stimulate the rate of photosynthesis but

the fact is that photosynthesis is regulated by the relationship

between source and sink. Notably, 20% of the photosynthates

are being released to the rhizosphere in the form of root exu-

dates and signaling compounds (Jansson et al. 2018). The

mature leaves in plants are exporters of the excess of photo-

synthates mainly in the form of sucrose to the sink tissues i.e.

net importers of photosynthate such as roots, seeds, stems, or

young leaves where it is metabolized or stored (Jansson et al.

2018. However, a significant amount of photosynthetically

fixed C did not allot to fungal symbionts supplementing the

soil with a commercial AMF inocula (Elliott et al. 2020).

Drought stress limits the soil water availability and uptake

of mineral nutrients in plants (Kaya et al. 2009). From a recent

review, it has been stated that under AMF colonized root there

is an increase in photosynthesis and stomatal conductance in

well-watered conditions (Quiroga et al. 2020). Some attributes

which are directly linked to the growth and development of

the plant-like stomatal conductance, leaf water potential, rela-

tive water content, photosystem II efficiency and CO

assim-

ilation are all affected by AMF inoculation (He et al. 2017;

Chandrasekaran et al. 2019). Similarly, the application of

AMF increased above-ground biomass. Also, AMF increased

dry matter accumulation, soil moisture uptake, and tolerance

to drought and salinity. The use of AMF to a greater extent

helps maintain various ecosystems and contributes to a higher

scale to organic farming for growth promotion and yield max-

imization. Ortas 2012, suggested that soon there will be the

possibility of replacement of chemical fertilizers by the effec-

tive application of AMF. Up to 50% reduction of the chemical

fertilizer is possible by the application of AMF (Begum et al.

2019). The internode length and inflorescence per branch have

increased significantly under AMF treated plants than untreat-

ed control (Bona et al. 2017).

Rising pollution due to the increasing use of chemical fer-

tilizer caused soil pollution and results in a decline in produc-

tivity. Plant growth-promoting microorganisms have a major

role in the rhizosphere to promote growth and development

(Sivakumar et al. 2020).

The use of plant growth-promoting microorganisms is suit-

able not only for food diversification but also for supporting

different life forms. To date, major progress has been met in

using microorganisms to refine soil fertility. The exploitation

of indigenous soil organisms is a method of maturity and

protection to the intensification of soil fertility (Dar et al.

2018). Organic fertilizer has a major role in soil physicochem-

ical and biological properties. Organic fertilizer not only

Bhantana P. et al.

provides nitrogen but also other nutrients uniformly

(Sivakumar et al. 2020).

More than 80% of the plant species including vascular and

non-vascular plants are linked with AMF. The presence of

AMF are observed in a wide area ofthe landscape from grass-

land to tropical rain forest in different parts of the globe

(Sharma et al. 2015). The study aforementioned focused on

the diversity of AMF in different parts of the world and orig-

inal crop plant species (Piliarová et al. 2019). Several articles

published to date presented the role of AMF in sustainable

agriculture due to its activity toward reducing chemical fertil-

izer and sustaining plant productivity (Bona et al. 2017).

Symbiotic association between the host plant and AMF

help to mineral nutrition of higher plants and physiology to

withstand abiotic factors and pathogen (Emmanuel and

Babalola 2020). The inoculation of AMF along with plant

growth-promoting bacteria has a synergistic effect on crop

growth, yield and quality (Emmanuel and Babalola 2020).

Uptake of different nutrients like phosphorous (P), nitrogen

(N), potassium (K), sulfur (S), copper (Cu), Calcium (Ca) and

Zinc (Zn) is facilitated by the incorporation of AMF in the

soil-plant system (Turrini et al. 2018). The demand for the

sugars is fulfilled by the rhizosphere association with plants

in return helping the plant for the uptake of the mineral nutri-

tion (Emmanuel and Babalola 2020). Due to the lack of root

hairs, the growth of the citrus plant is highly influenced by

AMF emphasized the importance of AMF in root colonization

(Wu et al. 2014). An increase in growth is observed with the

application of AMF in tarragon and lavender plant, but hyssop

exhibited a slow developmental response (Golubkina et al.

2020c). A 20–35% increase in biomass is recorded after the

application of AMF in Artemisia dracunculus and Hyssopus

officinalis (Golubkina et al. 2020c). An application of AMF

based formulation increased plant growth and yield by 1.4 and

1.45 times respectively in Allium cepa and Allium. sativum

(Golubkina et al. 2020d).

A decrease in the accumulation of P increases the plant

sensitivity to AMF (Tawarava et al. 2001). Arbuscules fre-

quency and a higher degree of mycorrhization were observed

under AMF treated plants than untreated control (Bona et al.

2017). Enhancing cotton growth in terms of strength of cotton,

rate of germination, plant height, length of the fruiting branch,

number of fruiting per branch due to AMF application. The

fruiting branch is a major trait affecting cotton growth and

yield with enhanced P uptake or transportation with growth,

development and photosynthesis. AMF directly affect the ear-

ly growth stages of R. laciniata and S. gigantea (Majewska

et al. 2017). Variability in growth is reported with AMF inoc-

ulation but the efficiency of the treatment may depend on the

interaction between plant and AMF genotype (Schüßler et al.

2016). Improvement in the soil physicochemical characteris-

tic, aboveground and belowground biodiversity, the survival

of tree or shrub seedling, lack of moisture and nutrient in the

rhizosphere is significantly improved by the application of

AMF in soil (Asmelash et al. 2016). Improvement in the plant

vegetative and reproductive growth are possible with the ap-

plication of AMF. The maturity of the cotton boll is increased

and the time for the maturity is prolonged. Similarly, the fiber

maturity standard is high (Gao et al. 2020).

3Yield

There is an increment in the yield of maize by 17% without N

treatment than with N fertilization under mycorrhizal applica-

tion (Singh et al. 2020). The agronomic and recovery efficien-

cies of fertilizer applied are up to 38.6 and 34.9% respectively.

There is a beneficial effect of AMF in P-use efficiency in

maize (Singh et al. 2020). There are no significant differences

in mean grain yield either in the mycorrhizal seed coating or

non-mycorrhizal seed coating (Singh et al. 2020). The preci-

sion farming with the use of different optical sensing tech-

niques using 30 Kg/ha less fertilizer than fertilizer dose based

on the soil test. Both soil test-based fertilizer recommendation

and the optical sensing techniques have similar N uptake

(Singh et al. 2020). It has been reported that the yield of carrot

and green onion is increased by AMF inoculation (Wang et al.

2011). H. officinalis showed an increase in biomass, produc-

tivity and essential oil yield (Golubkina et al. 2020c). A syn-

ergistic relationship between AMF and saprophytic fungi

caused an increase in yield of A. cepa by 50% (Golubkina

et al. 2020b). The improved intensity of I and Se accumulation

resulted in a higher yield, dry weight and also beneficial for

increasing the antioxidants, proteins and macro as well as

micronutrients (Golubkina et al. 2020a). Higher values for

seed yield, Se, I, N, P, Ca, protein and antioxidant levels are

observed in earlier planting. Se and I showed a synergistic

effect on stimulating the accumulation of Se and I in chickpea

seeds. For sustainable farming tools for improving the chick-

pea seed yield, quality, chemical composition for energy pro-

duction and metabolite extraction is important (Golubkina

et al. 2020a). Application of the AMF in improving water

and nutrient uptake by establishing a symbiotic relationship

with chickpeaplant is important with widened hyphae system.

AMF also have a role to plant resistance against biotic and

abioticstresses(Begumetal.2019). Yield, harvest index and

1000 grain weight of the chickpea are improved by the appli-

cation of AMF (Golubkina et al. 2020a).

4 Quality

Sweetness and aroma are the important parameters of the fruit

quality. Sweetness is mainly governed by sugar concentration

in the fruit flesh. The glucose and fructose content of young

fruits is increased during developmental stage until fully

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

ripening. Also it is found that sucrose accumulated in the

mesocarp. Fruit aroma is determined by a mixture of different

volatile compounds along with esters like terpens, aldehydes,

lactones and alcohols (Esteras et al. 2018). In AMF inoculated

tomato there is increment in the P, Zn and lycopene content by

60, 28 and 18.5% respectively than non AMF plants

(Giovannetti et al. 2012). Quality seedling is an essential at-

tribute of healthy crop and healthy life. So AMF have another

role in seedling survival and establishment. Onion plants in-

oculated with AMF have increased proteins, soluble sugars

and proline in leaves (Bettoni et al. 2014). Tolerance of onion

seedling with environmental stress is enhanced due to appli-

cation of AMF for the production (Bettoni et al. 2014). AMF

inoculated cucumber seedling has higher survival rate, P and

Zn shoot concentration (Ortas 2010). Uniformity in fruit rip-

ening, better flowering,enhanced fruit yield and quality, early

flowering and maturing ensuring early harvest which fetch

higher market price is all possible after application of AMF

to tomato plants (Ortas et al. 2013).

Early flowering, increase in the number of flowers and high

content of sugars and carotenoids in pulp are observed in

AMF plant than in non-AMF condition. Similarly, germina-

tion and root elongation are also affected in the first stages of

growth in the field. So it is concluded that on a commercial

scale AMF significantly improved fruit quality in the field.

This signifies the development of seeds with increasing ger-

mination rate and plant fitness (Copetta et al. 2020). An ap-

plication of AMF to plants increases the content of essential

oils in plant leaves (Copetta et al. 2020). The content of grain

starch is higher in the mycorrhizal plants than in non-

mycorrhizal plants. Similarly higher the grain starch is record-

ed in the wheat variety Compass than Haruna Nijo (Al Mutairi

et al. 2020). Furthermore, in the variety Compass, the mean

spectra for mycorrhizal are higher than non-mycorrhizal

plants. This is due to amide I band associated protein (Al

Mutairi et al. 2020).

A significant increase in oil content of three species of

A. dracuncullus,Lavandula angustifolia and H. officinalis is

observed (Golubkina et al. 2020c). There is not a clear differ-

ence in antioxidant activity and phenolic content at harvest

between the control and AMF inoculated plants. Generally,

it is reported that worsening in plant quality including antiox-

idant activity and phenolics is observed during storage condi-

tions with high temperature and humidity. During storage

conditions with application of AMF caused a significant in-

crease in antioxidant capacity at high humidity and tempera-

ture compared to untreated control (Golubkina et al. 2020c).

Whereas a decrease in ascorbic acid, chlorophyll content and

phenolics as well as a decline in antioxidant activity was ob-

served in control plants (Golubkina et al. 2020c). In compar-

ison to control leaf volatile oil content of Artemisia annua

increased by 45% and 25% with the application of Glomus

mosseae and G. versiforme respectively (Kapoor et al. 2007).

An improvement in essential oil content was stimulated in

L. angustifolia (Khaosaad et al. 2006; Copetta et al. 2006).

Higher chlorophyll content of AMF treated plant is observed

than non-AMF inoculated plant (Golubkina et al. 2020c). An

increment in the chlorophyll content of A. cepa is recorded

under AMF application irrespective of the Glomus species

tested (Golubkina et al. 2020b). Onion bulb’s antioxidant ac-

tivity (AOA) is increased remarkably by applying a mixture of

Glomus spp. and saprophytic fungi (Golubkina et al. 2020b).

Experimentation in the field showed a 32% and 15% incre-

ment in the phenolics and AOA (Golubkina et al. 2020d). The

AOA in Allium spp. is governed by sulfur-containing com-

pounds showing cardioprotective and anticarcinogenic effects

(Hanen et al. 2012). Most of the agricultural soil is poor in

sulfur so the application of AMF is essential for the

immunoprotection (Kertesz and Mirleau 2004). Inoculation

of AMF to the plant roots leads to chlorophyll formation af-

fecting sugar metabolism and photosynthesis via stimulation

of biosynthesis of phytohormones like abscisic acid (Rolland

et al. 2006). Similarly, mycorrhizal inoculated plant caused an

increase in 68% of monosaccharides content in A. cepa (Lone

et al. 2015). Similarly, an increment in titrable acidity is re-

corded in tomato, shallot and onion (Golubkina et al. 2019;

Golubkina et al. 2020d; Jansa et al. 2002) under field condi-

tion applied with Rhizophagus irregularis. The production of

organic acid is facilitated via oxidation of photosynthetic as-

similates. Production of amino acids, ATP and maintenance of

redox balance, membrane permeability and acidification of

extracellular spaces. Organic acid released by roots results in

soil acidification thus improving plant nutritional efficiency,

including either P and Fe accumulation or their transport

across xylem (Igamberdiev and Eprintsev 2016). Under

AMF condition there is an increase in citrate and malate of

A. cepa. This nitrogen accumulation and is advantageous to

plant development (Golubkina et al. 2020b). AMF inoculation

resulted in a significant increase in the total dissolved solids

(TDS), proteins, polyphenols and antioxidant activity

(Golubkina et al. 2020a).

Colonization with AMF in strawberries presented increased

levels of secondary metabolites resulting in increased AOA

(Castellanos-Morales et al. 2010). An increment of the dietary

quality of crops by AMF affecting carotenoids and volatiles

(Hartetal.2015) is observed. Also, there are beneficial effects

of AMF on the tomato quality (Bona et al. 2017). Also in-

creased tissue contents of sugars, organic acids, vitamin C,

flavonoids and minerals have been reported by Zeng et al.

(2014), due to the application of Glomus versiforme.

Symbiosis with mycorrhizae induces accumulation of chloro-

phyll, anthocyanins, tocopherols, phenolics and various min-

eral nutrients (Baslam et al. 2011). AMF have role in the large-

scale production of maize, yam, potato with confirmation that

AMF show a prominent role in increasing yield (Begum et al.

2019). AMF can also enhance the biosynthesis of valuable

Bhantana P. et al.

phytochemicals in edible plant parts and improve health poten-

tial for the production chain (Rouphael et al. 2015).

Improvement in the citric acid is observed in tomato plants

treated with AMF (Bona et al. 2017). Increased in the content

of lycopene, alanine, vitamin C etc. are observed in the AMF

treated tomato landraces ‘Lucariello’than non-treated control.

In Giagiu tomato landrace, AMF increased Ca, Zn, arginine,

lysine content in the tomato landraces than the untreated con-

trol. In both of the landraces, AMF helps to uptake and bio-

synthesis important molecules involved in the control of oxi-

dative stress and cellular pH. Similarly the beneficial effects of

human health, AMF treated molecules are supposed to in-

crease the shelf life of tomato fruits (Carillo et al. 2020).

5 Elemental composition

The uptake of macronutrients N, P, K and many other

micronutrients increased with inoculation of AMF in A. cepa

(Mohamed et al. 2014). For instance inoculation of A. cepa

with Glomus versiforme resulted in accumulation of N, P and

Zn in comparison to plants treated with Rhizophagus

intraradices (Charron et al. 2001a; Charron et al. 2001b).

The joint application of humic substances and AMF synergis-

tically increased growth and N and P levels as well as protein

content (Bettoni et al. 2014). Interaction between AMF and

humic substances caused the highest accumulation of proteins

and sugars in leaves consequently increased the yield and

quality of onion bulbs (Bettoni et al. 2014). Also, it has been

reported that improving P accumulation is reported in AMF

treated plants than untreated (Sato et al. 2015). Longer dura-

tion of planting increase the accumulation of Se and I of

Chickpea (Golubkina et al. 2020a). Chickpea plants are

planted on two different dates 14th January and 28th

February. Plants planted at an earlier date showed a higher

levelofN,PandCaincomparisontoalaterdate

(Golubkina et al. 2020a). Transferring of organic nutrient car-

bon (c) in the formof sugars and lipids is a key role ofAMF in

this symbiotic association (Jiang et al. 2017). In return, AMF

has stimulated the plant growth environment by associating

with the uptake of several macro and micronutrients (Begum

et al. 2019). Phytoavailability of some micronutrients like Zn

and copper (Cu) has been increased with an increased associ-

ation of AMF (Begum et al. 2019). The use of AMF as

biofertilizer increased leaf area, nitrogen (N), potassium (K),

calcium (Ca) and phosphorous (P) content showing enhanced

plant growth (Balliu et al. 2015). Even in the abnormal con-

dition, AMF provide nutritional support to the plant.

Production of fungal structures like arbuscular mychorrhizae

assists in the exchange of inorganic minerals and the C and P.

In this way AMF provides a huge amount of vigor to the host

plant (Prasad et al. 2017). Under P limited conditions AMF

association improved the supply of the P to the host. This is

how the P amount either in the roots or in the shoots of the

plant can be improved (Garces-Ruiz, 2017). Increased uptake

of N, P, C is directly linked to the increased photosynthesis

helping plant growth and development in higher or lower P

levels under different irrigation regimes (Liu et al. 2018). For

instance, there is increased N, P and Fe in Pelargonium

graveolens L. under drought stress with AMF symbiosis

(Amiri et al. 2017). Similarly, under salt-stressed condition

an increment in the levels of P, Ca and K in Euonymus

japonica due to fungus attachment is observed (Gómez-

Bellot et al. 2015). In a separate study, AMF inoculated

Pistachio plants showed higher levels of P, K, Zn and man-

ganese (Mn) under drought stress (Bagheri et al. 2018). Also

an increment in P and N contents in the Chrysanthemum

morifolium (Wang et al. 2018) and intracellular increase in

, P and N contents together with improved seedling

weight is observed in Leymus chinensis (Lin et al. 2017).

AMF improve the uptake of almost all essential nutrients ex-

cept Na and Cl leading to growth stimulation (Evelin et al.

2012). Several scientists reported that the application of AMF

in the soil is advantageous to promote N and P in growth and

development of the plant (Smith et al. 2011). About 20–75%

of the total N uptake by AM plants is transferred by the AMF

(Hashem et al. 2018).

6Zincnutrition

Zinc(Zn) is one of the key micronutrient elements of great

public health importance. In humans, Zn is involved in several

biological functions and is considered a multipurpose element.

Zn plays catalytic, co-catalytic, or structural roles in many

enzymes (Christie et al. 2004). Zn can bind more than 2000

transcriptional factors, more than 300 enzymes and has a ma-

jor role in more than 1000enzymatic reactions (Chasapis et al.

2020). The human body contains a total of 2–3 g of Zn. Zn is

the second most abundant transition metal in humans.

Similarly, Zn is the second most abundant divalent cation after

calcium (Pae et al. 2012).

Almost 17% of the global population are facing Zn deficien-

cy (Chasapis et al. 2020). Zn deficiency causes retarded growth,

failure of smell and taste, and anorexia in humans (Chasapis

et al. 2020). Such symptoms may appear due to low dietary

intake of Zn (Livingstone 2015). Moreover, disorders in the

stomach, anorexia, bulimia are some symptoms observed in

both infants and adults (Glutsch et al. 2019). A low level of

Zn in blood serum is observed in a patient affected with acute

viral hepatitis (Fota-Markowska et al. 2002). Similarly, a patient

with liver cirrhosis has a lower level of Zn. Also, other diseases

like pancreatic exocrine function and damaged intestinal mucosa

are caused by a reduced level of Zn absorption. In cirrhotic

patients likely alcoholic patients are vulnerable to Zn deficiency

(Prasad 2009).

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

As an essential micronutrient element Zn has several func-

tions in plants like metabolism of proteins, lipids, carbohy-

drates, and nucleic acids compromising not only yield but also

the qualityof the harvest. More than 30% of the world’scereal

productive areas are threatened with Zn deficiency (Bhantana

et al. 2020). By negotiating both the quality and quantity of

the productsZn is continuously keeping the agriculture indus-

try under threat. Synergistic association between Zn and AMF

are important for sustainable yield and quality. It is observed

that grain Zn content in the field is increased with applying

AMF (Ercoli et al. 2017). Also, it is observed that an incre-

ment in Zn concentration together with AMF improve Zn

nutrition (Al Mutairi et al. 2020). The concentration of Zn in

mycorrhizal plant is higher than in the non-mycorrhizal coun-

terpart (Al Mutairi et al. 2020).

Application of Zinc (Zn) fertilizes is one of the ways in

correcting Zn nutrition in field crops. Application of Zn-

graphene oxide (GO) in powder from conferred greater Zn

uptake in both species Barley (Hordeum vulgare)and

Medicago (Medicago truncatula) (Watts-Williams et al.

2020). It showed promising results of Zn-GO formulation

with improvements in biomass accumulation and Zn nutrition

in both crops Barley (Hordeum vulgare) and Medicago

(Medicago truncatula) (Watts-Williams et al. 2020).

Deficiency in Zn for cropping areas of the world including

developing countries is a major threat to crop production.

Enrichment in the Zn concentration in the edible portion of

the plant is crucial to reduce the hidden hunger. Recently the

Zn nanoparticles have been used for fertilization. Within the

last five years, GO has been widely used as it is highly effi-

cient and sustainable to deliver the crops. In the future, the

combination of NPs and GO formulation could enhance the

sustainable use of the resources (Watts-Williams et al. 2020).

The activityof many enzymes and plant processes is governed

by the level ofZn in plant tissue. The uptake and use of Zn are

improved by the application of AMF (Al Mutairi et al. 2020).

The impact of Zn fertilization and AMF on the yield and

quality of five varieties of barley is studied earlier (Al

Mutairi et al. 2020). AMF colonization decreased biomass

but increased grain dimensions and mean grain weight.

Grain yield of barley and biochemical qualities are highly

variable between cultivars. AMF generally increased barley

grain Zn concentration and starch content but grain biochem-

ical traits like βglucan and arabinoxylan amount are not

shown in cultivars, which is unaffected by AMF application.

A spectral study showed that grain characteristics are affected

by AMF (Al Mutairi et al. 2020). Similarly, AMF inoculation

affect the mineral composition, increase the accumulation of

Se, I, and Zn in A. drancunculus, and decreasing the level of

Co, Fe, Li, Mn in H. officinalis (Golubkina et al. 2020a;

Golubkina et al. 2020c).

As a consequence of declining levels of Zn in soils various

plants in cultivated or wild experience reduction in growth,

yield, and low tissue concentrations of Zn. The decline in the

concentrations of Zn in the edible parts of the plant has im-

portance for human Zn nutrition. So the plants are equipped

with AMF and a variable number of specialized structures.

Through AMF plants can uptake nutrients, with Zn and trans-

fer them to the plant thereby enhancing plant nutrition

(Cavagnaro 2008). Accumulation of Zn in the plant is varied

by the concentration of AMF in plant tissue. Lack of Zn in

edible portions of many crops caused a declined in the yield

and production. Impairment in human health is caused by a

lower due to the amount of Zn in the diet. The situation is

aggravated due to the deficiency of Zn in soil (Kochian 2000).

Therefore mechanism by which plants acquire and utilize Zn

is of high importance.

Improved plant nutrition due to colonization of AMF is an

attribute to take up the nutrients via mycorrhizal pathways and

has a direct or indirect relation to the plant morphology and

physiology. Nutrients availability via effects on soil physico-

chemical properties, nutrient cycling, and microbial commu-

nities is very important. The mineral nutrient acquisition is

one of the broadly studied areas of AMF application into the

soil. External hyphae of plants can supply 60% nutrients in-

cluding 25%N, 25% Zn, and 10%K. Although the mechanism

underlying the take-up of these nutrients; nutrient provision

by AMF is beyond that of P. There is a tradeoff between the

plant nutrition acquisition and Zn nutrition. Under low soil Zn,

AMF can improve plant Zn nutrition and under higher Zn

level AMF induced lower Zn accumulation in plant tissue.

Reportedly there is the critical level of Zn concentration below

which Zn uptake is enhanced by AMF and above this level Zn

translocation to plant shoots is reduced. The complication oc-

curs due to absorption of other nutrients for example P via a

mycorrhizal pathway which is due to the dilution effects.

Similarly, a complex interaction between Zn and P occurs in

AMF (Cardoso and Kuyper 2006). So far there is little knowl-

edge in the role of Zn in the extraradical colonization phase;

but both vegetative and reproductive stages of growth of AMF

are impacted by Zn additions (Cavagnaro 2008). Supply of Zn

from 0 to 10 mM ZnSO

can result in a significant decrease in

spore germination, spore density and hyphae (Pawlowska and

Charvat 2004). Moreover, the effect of Zn nutrition differed

between AMF species and spores germination. The germina-

tion of the spores varied on the amount of Zn supplies

(Cavagnaro 2008). Extraradical growth of AMF is affected

by the application of Zn. So some Zn contaminated sites need

tolerant AMF species (Cavagnaro et al. 2005).

The response of Zn addition in the soil can be negative,

positive, and neutral based on the impacts of the extraradical

growth of AMF. Hyphal densities in maize inoculated with

G. intraradices decreased with increasingconcentration of Zn

from 0, 0.24, or 0.48 mg/Kg in micronutrient solution (Liu

et al. 2000). In contrast hyphallength density and intra-radical

colonization increase in soils with the application of ZnSO

Bhantana P. et al.

250 mg/Kg. The difference is mainly due to the set of inter-

actions between edhapic factor, environmental condition and

Zn addition. The addition of AMF to Zn uptake due to differ-

ences in plant and fungal identity are important determinants.

The significance of the extraradical hyphae colonization is due

to the exploitation of organic and inorganic nutrients

(Cavagnaro et al. 2005). This type of response is analogous

due to the plastic behavior of the plant roots which allows

them to respond. Whereas not a direct mechanism of Zn ad-

dition on the extraradical growth of AMF is observed

(Cavagnaro 2008). The critical value of Zn in most of the

crops is 50 ppm (Cavagnaro 2008). Below this amount,

AMF improve plant Z nutrition, and above help in the avoid-

ance of Zn toxicity. Most of the studies currently done on the

intraradical colonization having a focus on Zn inputs. The

colonization of root length in A. cepa decreased from 74%,

47% and 0% in soil application of ZnSO

from 0, 10 and

75 mg/Kg as respectively. In another experiment root coloni-

zation decreased from 55, 42, 39, 12 and 0% with the addition

of Zn amount in soil from 0, 10, 20, 30, 40 and 75 ppm. But

this is not the always case of decreasing colonization with

increasing application of ZnSO

. Contrastingly, increment in

colonization is observed from 14, 29, 48 and 82 percentages in

wild tobacco by application of 0, 20, 100 and 250 mg of Zn

per Kg (Cavagnaro 2008). This is because of the selection of

AMF species that can withstand high Zn concentrations

(Christie et al. 2004). AMF responded differently and re-

sponse is further complicated by their effects on uptake of

other nutrients. The addition of P to the soil modifies the

effects of Zn colonization in red clover root by AMF

(G. mosseae). And a reduction in the percentage of root colo-

nization was significantly observed in low P. Further addition

of Zn as Zn (NO

)

in a wide range of concentration viz. 0, 50

and 400 mg Zn per Kg is observed. The presence of heavy

metals may alter the response of intraradical colonization. A

decrease in the colonization of mycorrhiza in maize from

56%, 55% to 46% with increasing Zn as ZnSO

addition (0,

300 and 900 ppm) is observed. For example, the addition of

Cadmium (Cd) in the form of CdSO

has a variable response

to root intraradical colonization. In kidney bean application of

Zn 5 mg/Kg increased colonization from 24 to 92%. Likewise,

extraradical colonization intraradical colonization showed a

similar response. Soil type, plant characteristics and environ-

mental factors pose a widely varied response (Cavagnaro

2008).

The mechanisms underlying the reduction in colonization

with Zn nutrition have been studied in certain species. In AMF

colonized plants the total amount of Zn uptake 25% appeared

in the shoots, 25% in roots, 15% in the growth medium agar

and 35% in the external hyphae (Cavagnaro 2008). AMF

could take up nutrients from a distance of 40 mm. A study

of the symbiotic relationship with maize root showed a signif-

icant amount of nutrients absorbed by both P and Zn. About

9% of the Zn is transported to plants from a distance of 50 mm

within 25 days (Jansa et al. 2003). An increase in root coloni-

zation by applying AMF is found under Zn uptake after an-

thesis in wheat. AMF and plant Zn nutrition were affected by

the availability of P. Increased plant growth and development

due to improvement in P nutrition can cause dilution of plant

Zn or have an inductive effect on plant growth. The three-way

interaction between P, Zn and AMF has a significant impact

on crop growth and plant nutrition (Cavagnaro 2008).

Increasing tolerance to both P and Zn deficiency was achieved

by the application of AMF. Some evidence has shown the

protection of plants against excessive accumulation of Zn in

soil by the application of AMF (Nguyen et al. 2019).

7 Phosphorous regulation

Phosphorous (P) is a key essential, non-replaceable element for

plant growth and development. Phospholipids a major constit-

uent of P is a component of the cell membrane. Notably, P is

used in energy transfer, photosynthesis, metabolism, intracel-

lular signaling and gene replication and expression. The low

availability of P is the main constraint in much of the low input

agriculture worldwide. There is a huge importance of P in

several crops such as barley, maize, sugarbeet, and common

bean. Hence growth and productivity of major crops world-

wide are limited by P availability. The AMF symbiosis is par-

ticularly of importance with immobile nutrients such as P. The

acquisition and utilization of P in plants is a major factor in the

determination of final crop yield (Sánchez and Salinas 1981).

In traditionally driven agriculture, inherent soil fertility is the

major source of P with an occasional supply of manure for the

crops. But after modernization in agriculture results in overex-

ploitation of the P and results in low crop yield and farm in-

come. Rock phosphate is the major source of the phosphatic

fertilizer and is non-renewable which could be exhausted in the

next 50–100 years (Natasha 2009). With a fuller understanding

of crop dependencyon the mineral, phosphate could be cut off

and a system that is renewable to soil phosphate is demanding

(Schroeder et al. 2013).

Application techniquesof P which can also use AMF wide-

ly in foxtail millet is promising (Setaria italica) (Ceasar et al.

2014). The use of AMF significantly increases seed weight in

foxtail millet (S. italica) (Ceasar et al. 2014). In upland cotton

(Gossypium hirsutum L.) AMF influenced the concentrations

of P in plant mass. The increased concentration of P in the

stems, leaves and roots is observed with application

Rhizophagus irregularis in comparison to control. With the

application of mycorrhiza R. irregularis most of the phosphate

transport genes are upregulated in stem leaves and roots.

However, the upregulation is different between tissues (Gao

et al. 2020). A vigorous physio-biochemical reaction occurs in

leaves and roots are made even more complex through a

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

symbiosis between cotton and AMF. Phosphorous is critical

in various metabolic processes. Generally, the expression of

Gh-A02G0203 is a key gene for P transportation in stem, root

and leaves (Gao et al. 2020). Several AMF studies with P

application has been done with root colonization affected var-

ious host plant species. Increased availability of P in soil has

been observed with AMF inoculation in agricultural land (Gao

et al. 2020). Rather than exchange mineral nutrients with a

carbon-containing compound like carbohydrates and lipids,

the plant can directly obtain P from soil. In the AMF inocula-

tion, P concentration in the stems, roots and leaves of cotton is

increased. The concentrations of P in the shoot are affected

significantly (Rydlová et al. 2016). The P content of the inva-

sive species R. laciniata and S.gigantean is enhanced by AMF

application (Majewska et al. 2017). Leaf accumulation of P

with the application of AMF was higher than that of bacterial

symbiosis (Rahimzadeh and Pirzad 2017). With the applica-

tion of P, there is inhibition of AMF colonization with the

expression of certain genes encoding carotenoids, lactone bio-

synthesis as well as symbiotic relations with phosphate trans-

porters is reported (Breuillin et al. 2010). The level of P may

regulate the expression of P transporter family genes and then

increase the trading ratio and the AMF inoculation speed.

Phosphate transporters play a major role in P acquisition and

regulation. Both modes including up-regulation and down-

regulation occurred with phosphate transporter suggesting a

negative and positive functional role in AMF based cotton

(Gao et al. 2020).

Regulation of P in the plant is significantly influenced by

AMF application in crop production. AMF increases the up-

take of the P and tissue concentration. It is reported that under

drought conditions there is an increment in the P and K uptake

with P application (Emmanuel and Babalola 2020). In tomato,

it is crucial to develop an understanding between P and AMF

uptake. Still, it is unknown how the application of P and AMF

fertilizers influence plant growth and development.

Phosphorous is highly immobile in plants. Due to the im-

mobile nature of P in soil, application of AMF has the poten-

tial to increase agricultural production. P fertilizer application

did not have an influence on root colonization and diversity of

the AMF structures in tomato. Root abundance and AMF

colonization are correlated negatively. Therefore an investiga-

tion is required whether AMF communities and P fertilization

develop more effective management of P in tomato (Higo

et al. 2020). In a separate study, the expression of the phos-

phate transporter gene MtZIP5 is observed by application of

AMF and soil Zn availability. Contrastingly, the expression of

MtZIP2 is upregulated in non-AMF roots and increased with

soil Zn availability (Nguyen et al. 2019).

AMF improve the uptake of P via extraradical mycelium,

however, the rate and amount of uptake are varied with spe-

cies. Among the several enzymes, AMF have to produce ex-

tracellular enzymes to solubilize organic P (Sato et al. 2015).

AMF are also helpful in mitigating plants grown under acid

soil (Aguilera et al. 2011). This is how AMF have huge po-

tential to mitigate plant stress under stressful environment.

Generally, high levels of P application have been shown to

decrease colonization by AMF, abundance and richness of

AMF communities in the roots and soil. For instance applica-

tion of a high amount of P decrease the diversity but moderate

P application can enhance the diversity of AMF communities

(Higo et al. 2018; Kahiluoto et al. 2001). The impacts of P

fertilization on AMF communities are contradictory. Different

agricultural settings have been impaired due to poor interac-

tion between AMF and P. Plants had the highest biomass and

productivity in the application of AMF+ 50% phosphate fer-

tilizer. Similarly, AMF colonization was correlated with bio-

mass, soil properties and productivity in Sugarcane (Juntahum

et al. 2020). AMF also have a role in increasing water use

efficiency and has a crucial role in the management of soil

quality and productivity of the agricultural system.

Application of Funneliformis mosseae in Sugarcane increase

plant height, weight compared to non-inoculated plant under

greenhouse conditions. Further, the application of F. mosseae

in sugarcane plantations is desirable.

8 Tolerance to abiotic stress

Different crops and their varieties have a differential response

to plant growth and development with exposure to abiotic

stresses. The enhancement of tolerance to abiotic stress is

highest in A. dracunculus and lowest in H. officinalis with

the application of AMF (Golubkina et al. 2020c). An increase

in antioxidant value and selective absorption of mineral nutri-

ents during crop husbandry are key features in the tolerance of

plants against environmental stresses (Hashem et al. 2018).

Plant performance in abiotic stress tolerance is improved by

AMF symbiosis in the root (Balestrini et al. 2018;

Chandrasekaran et al. 2019; Balestrini et al. 2020). Plant de-

fense with AOA shows a major role in the protection of plants

against biotic and abiotic stresses (Toscano et al. 2019;

Sharma et al. 2019).

Abiotic stresses decrease plant growth and productivity.

The use of fertilizer in excess and pesticides caused an impact

on the crop productivity and a degraded ecosystem. The use of

AMF is an environmentally friendly management technique

and is also known as a biofertilizer. AMF increases tolerance

to host plants against various stressful situations like heat,

salinity, drought, metals and extreme temperatures (Begum

et al. 2019). AMF is helpful in the up-regulation of tolerance

mechanism and prevents the downregulation of major meta-

bolic pathways. Both in the stressed and unstressed environ-

ments AMF provides essential plant inorganic nutrients to

host plants consequently improving growth and yield

(Begum et al. 2019). A vigorous growth under a stressful

Bhantana P. et al.

environment is mediated by a complex interaction between

plant and AMF with enhanced photosynthetic rates, gas ex-

change parameters and enhance water uptake (Birhane et al.

2012).

The improvement of plant nutrition by increasing availabil-

ity and translocation of different nutrients by AMF is one of

the major roles in plants (Rouphael et al. 2015). Similarly,

AMF improves the quality of soil by influencing texture,

structure and plant health (Thirkell et al. 2017; Zou et al.

2016). AMF also protects the plant from fungal attacks

(Jung et al. 2012).

Symbiotic association between plant and mycorrhiza dated

back to 400 million years ago (Selosse et al. 2015). This type

of relationship is a good example of mutualism, which can

regulate the growth and development of plants. The fungus

mycelium grows below the root of the plant promote water

and nutrient uptake in the plant. Moreover, several changes in

plant morpho-physiological cues have occurred in stressful

conditions (Hashem et al. 2015; Begum et al. 2019).

8.1 Drought stress

Drought affects various metabolic processes in many ways

for instance induction of oxidative damage and reduced

rate of transpiration. Drought shows a deleterious effect

on plant growth affecting ion uptake, enzyme activity and

nutrient assimilation (Ahanger et al. 2017). However,

AMF in plant systems enhances the use and uptake of

water in several crops such as maize, wheat, barley, soy-

bean, strawberry and onion (Moradtalab et al. 2019).

Various physical and biochemical processes in plants are

affected by the symbiotic relationship between AMF and

plants. Several phenomena for the alleviation of drought

stress in plants are controlling stomatal regulation by ABA

metabolism, increased osmotic adjustment, accumulation

of proline or increased glutathione level (Begum et al.

2019). Also the AMF symbiosis is caused by enhanced

gas exchange, stomatal conductance, water relations and

transpiration rate. AMF also facilitate ABA responses to

stomatal conductance and other many physiological pro-

cesses (Begum et al. 2019). Higher efficiency in the uptake

of water and nutrient is observed in AMF colonized

A. cepa caused enhanced adaptation to different water

availability in the soil (Bolandnazar et al. 2007;Mosse

et al. 1981). A significant increase in water use of

A. cepa is shown with higher evapotranspiration, increased

leaf area, biomass and higher yield with AMF in compar-

ison to controls.

8.2 Salt stress

Reduced productivity and decreased net assimilation rate are

some of the causes leading to environmental damage and

threat to global food security due to farming in the saline

environment (Ahanger et al. 2017). A decrease in growth,

yield and evapotranspiration is observed in young pomegran-

ate orchards under a salt-stressed environment (Bhantana and

Lazarovitch 2010). Wide-scale attempts are being made to

achieve increasing crop productivity under salt-affected soils

(Santander et al. 2019). Several research reports have been

published earlier regarding the efficiency of AMF on growth

and yield increments in the plant under salt stress (Begum

et al. 2019). AMF increased the growth rate, water use effi-

ciency and leaf water potential of Antirrhinum majus under

salt stress (El-Nashar 2017). Some physiological parameters

viz. photosynthetic rate, leaf water relations and stomatal con-

ductance are affected under salt stress environment. AMF al-

leviated the deleterious effects on photosynthesis. AMF inoc-

ulation has a prominent role in improving water use efficien-

cy, chlorophyll content, photosynthetic rate and gas exchange

traits in Ocimum basilicum L. under salt-stressed environ-

ments (Elhindi et al. 2017). Likewise, under a saline environ-

ment, AMF treated A. sativum plants exhibited higher leaf

area index, fresh and dry biomass. Also, AMF inoculation

improve fresh and dry weights and N concentration of shoot

and root under a mild saline environment (Wang et al. 2018).

AMF is found in salt-affected soils. Recent studies reported

that increment in growth, nutrient uptake and yield in saline

environments is possible with the application of AMF.

Interaction between plant and fungus and also with environ-

ment are prominent factors inthe plant grown under salt stress

environment, therefore the knowledge between plant and fun-

gal interactions is very important. The mechanism of im-

proved salt tolerance is still unclear. Moreover enhanced up-

take of P, Cu and Zn are one of the reasons that help plants to

alleviate salt stress (Kaya et al. 2009). The concentration of P,

N and the N:P ratio is affected by AMF application under salt

stress (Wang et al. 2018). Plant growth in the arid and semi-

arid regions is adversely affected by excessive concentrations

of soluble salts. It is very hard to alleviate salt stress from the

plant-growing environments (Kaya et al. 2009) therefore ap-

plication of AMF may be an economically viable option. In

pepper plants treated with NaCl, there is a huge reduction of

shoot dry matter, root dry matter and fruit yield than without

NaCl application. The concentration of mineral nutrients like

N, P and K in the leaves is reduced significantly under saline

environment however pepper root colonized with mycorrhi-

zae Glomus clarum improved from both saline and non-saline

environments and have reduced cell membrane leakage (Kaya

et al. 2009).

Despite the beneficial role of AMF in plant nutrition, few

studies have been done on the accumulation of secondary

metabolites and mineral nutrition (Khaosaad et al. 2006;

Copetta, et al.,2006; Kapoor et al. 2004). Plant AMF interac-

tion is triggered by converting secondary compounds to signal

molecules (Ponce et al. 2004).

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

9 Phytoremediation of heavy metals

AMF promote the growth of the plant in soil affected by heavy

metals. Accumulation of heavy metals in food crops, fruits,

vegetables and soils cause human health problem (Yousaf

et al. 2016). Increased nutrient uptake in wheat is associated

with AMF under aluminum stress (Aguilera et al. 2014).

Accumulation of heavy metals like Cd, Zn in toxic concentra-

tion caused suppression in shoot and root growth and lead to

leaf chlorosis and even death (Moghadam 2016). A large

number of articles have been published on the AMF-induced

reduction of the metals in plants (Souza et al. 2013). The

toxicity of heavy metals in plants can be minimized with ac-

cumulation in the vacuole or cytoplasm. The major role of

AMF in plant growth and development during stressful envi-

ronments is to translocate important immovable nutrients like

Cu, Zn and P and reducing metal toxicity in the host plant

(Miransari 2017). Reportedly AMF bind the heavy metals like

Cd and Zn in the hyphal wall or cortical cells. In this way

uptake of heavy metals is restricted and leads to increased

growth, development, yield and quality of field crops (Garg

and Chandel 2012). Mycorrhizae disrupt the uptake of the

different heavy metals from the rhizosphere and movement

from the root to the aerial parts (Li et al. 2016a). Cd detoxifi-

cation in rice was due to AMF lowering Cd in both vacuoles

and cell wall (Li et al. 2016b). AMF driven tolerance of Cd in

alfalfa (Medicago sativa L.) is possibly due to the modifica-

tion of chemical forms of Cd in different plant tissues. The

AMF application caused immobilization or restriction of met-

al compounds, precipitation of P in soil, fungal cell wall ab-

sorption in cell and heavy metal chelation inside the fungus

(Begum et al. 2019).

Phytostabilization is the AMF induced immobilization of

heavy metals in soil and enhances the uptake of heavy metals

by roots. This is the process of cleaning of contaminated soil

by associated mycorrhizae depending upon the plant, fungus

and heavy metal interaction (Kumar and Saxena 2019).

Glomalin and organic acid exuded from fungi and plants play

a major role in the immobilization of heavy metals in the soil.

Nutrient and metal ions can be exchanged between the host

plant and fungi through the arbuscule. A reduction of up to

85% of heavy metal incorporation is observed due to the se-

cretion of organic and inorganic compounds (Kumar and

Saxena 2019).

AMF can modify the growth environment according to

their need. Among fungal colony spores of Rhizophagus

irregularis has a higher content of heavy metals than the rest

of the colony. The metals extracted are either bound to the cell

wall or compartmentalized in vacuoles (Kumar and Saxena

2019). AMF detoxify the contamination of heavy metal by

its direct involvement in the adsorption of heavy metal on

the fungal surface together with immobilization in the soil

by glomalin (Ferreira Vilela and Barbosa 2019). The hyphae

create a physical barrier to the entry of heavy metals by having

chelation and sequestration of heavy metals(Riaz et al. 2020).

AMF showed highly acceptable techniques for managing

heavy metal accumulation and some strains can survive even

under a very harsh condition of metal toxicities. This is the

characteristic feature of adaptation and make AMF superior to

other mycorrhizae (Schneider et al. 2013).

The reduction in the bioavailability of heavy metals is pos-

sible due to the secretion of glomalin (Ghasemi Siani et al.

2017). Glomalin-related soil protein (GRSP) is a glycoprotein

that is water-soluble and resistant to extreme temperatures

formed by mycelium and spore walls (Wang et al. 2019).

GRSP is an important compound for the protection of the

environment against harsh situations. Remarkably the GRSP

has a potential role in chelating heavy metals by reducing their

bioavailability through speciation of metal in the rhizosphere

(Wang et al. 2017a;Wangetal.2017b). The previous study

reported that 1 g of GRSP secreted by AMF can effectively

chelate up to 1.12 mg Pb, 0.08 mg Cd and 4.3 mg Cu from

heavy metal contaminated soils. This indicates the variable

ability of glomalin to chelate metals under different conditions

(Wu et al. 2014). In the 140 days of the experimental period,

GRSP absorbed 0.21–1.78% Pb, 0.38–0.98% Ni. In total

GRSP absorbed 4% of the total Pb and Ni. The use of AMF

in Cd contaminated soil increases the concentration of

glomalin as a protective mechanism in the rhizosphere. As a

result, there is a reduction of translocation of Cd in sorghum

roots and limiting Cd contents in the plant tissues (Babadi

et al. 2019). Inoculation of a mycorrhiza Glomus aggregatum

caused a significant decrease in Cd, Pb, Zn and Cu. Chelating

of the heavy metal in the soil is possible by releasing GRSP in

the hyphae of the AMF. Symbiotic association of some AMF

species R. irregularis, G. versiforme and F. mosseae caused

an increase in total GRSP in soil and decreased Pb and Cd

accumulation in maize with increased soil pH (Riaz et al.

2020).

Soil is the indispensable unit for the supply of nutrients and

tolerance of the plant to biotic and abiotic stress factors. An

optimum soil structure is possible after genuine manipulation

of physicochemical and biological processes with the secre-

tion of root exudates and sticky material in hand (Barbosa

et al. 2019; Rabot et al. 2018). The rearrangement strategy

by which the GRSP like material functioned as bridges to glue

together soil particles provide stability to them (Rillig et al.

2017). Long term contamination of heavy metals poses seri-

ous threats in soil and AMF characteristics have potential in

their management by disturbing the GRSP development and

aggregate formation. Although detailed information on soil

quality, particle size, the formation of soil aggregates in the

heavy metals contaminated sites is lacking. A recuperation

techniques of heavy metal contaminated site is possible after

understanding the impact of GRSP on soil physicochemical

properties and their connection with heavy metals.

Bhantana P. et al.

Accumulation of heavy metals in the soil is done by AMF

in their fungal structures and are less toxic to host plants and

promote tolerance to the host. AMF have two different types

of mycelium intraradical and extraradical (Wu et al. 2019).

Mainly accumulation of heavy metals is carried out by

extraradical and intraradical mycelium. Positive charge parti-

cles like cysteine, amino acids, thiol groups and glutathione

cause adsorption and reduction of heavy metals. These types

of mechanisms are an excellent example of heavy metal ho-

meostasis in the ecosystem by translocating heavy metals into

the host’s cytoplasm (Joutey and Sayel 2015).

Secretion of extracellular polymeric substances (EPS) on

the fungal surface by AMF is another mechanism to avoid

heavy metal toxicity on the host plant. The functional group

of EPS is carboxyl amine, phosphoric and hydroxyl groups

which practiced the mechanism of chelation, surface precipi-

tation and ion exchange (More etal. 2014). EPS is much finer

than plants’roots and can absorb minerals and elements. A

study conducted earlier showed that negatively charged phos-

phate groups and their analogs can precipitate Cr(III) on the

fungal surface (Wu et al. 2016). Moreover, compartmentali-

zation of the intraradical fungal structures caused the allevia-

tion of heavy metal toxicity (Krzesłowska 2011). Toxic ele-

ments are mainly distributed through fungal cell walls and

vacuoles.

10 Future prospects

AMF are critical component of the ecosystem which has a

major contribution to plant nutrition by providing access to

the soil-derived nutrients. Naturally, an intimate association

between plant roots and AMF is observed. This type of rela-

tionship benefits the acquisition of the number of soil nutrients

available in the soil with the help of plant roots. Previously P

is considered as one of the key elements for the uptake by

plant root but nowadays a wide array of nutrient elements

have been considered. Mycorrhiza helps in the uptake and

use of many other nutrients. The main cause of enhanced P

uptake is that plants require P in large quantities and its avail-

ability in nature is limited. The use of AMF has now been

observed far beyond its role in P nutrition, with other nutrient

elements too. The current scenarios and future benefits of

using AMF are increased crop yield, protection from certain

root pathogens an increased tolerance to environmental stress

and reduction in the input of agrochemicals. A recent devel-

opment in biotechnology demanded plant species-specific and

high-quality AMF. Some common nutrients that AMF can

alter the uptake of P, Zn, NH

,NO

, Cu, and K. These plant

nutrients are characterized as mobile and immobile. AMF help

in the acquisition of both mobile and immobile nutrients by

the plant root. Furthermore, Zn is helpful in the take up of the

essential plant nutrients and for this purpose, AMF is highly

influential.

Ecological intensification is a new discipline that aims

to achieve foods for billions, one strategy is the sustain-

able use of AMF as biofertilizer. Some other approaches

for ecological intensification are minimum tillage, contin-

uous crop cover, crop diversity and crop rotation. AMF is

a dominant mycorrhiza formed with 80% of plant species.

The role of AMF are highly varied in an ecosystem and

the multifunctional role of AMF in plant nutrition are

highly important. Some agricultural practices like tillage,

fertilization and non-host species tend to negatively affect

the fungal abundance and density. So the development of

an AMF technology for the widespread use and distribu-

tion of fungal inoculum is indispensable. A better under-

standing of the adverse condition that can have minimal

damage to the cropped area, will therefore increase yield

per hectare.

Acknowledgments I am highly grateful to Dr. Ram Chandra Adhikari,

Director of Planning and Coordination, of Nepal Agricultural Research

Council (NARC) for having a fruitful discussion on the topic. Also, Dr.

Adhikari advised me for possible facilities in the NARC to test N and Zn

in the samples preserved from another experiment. Moreover my sincere

gratitude to Mr. Samaya Gairhe for monitoring and evaluating NARC for

his time and contribution in this study. Likely, Basu Regmi chief of the

training and scholarship of NARC managed to read this article

thoroughly.

Funding This review is supported by the College of Resources and

Environment, Huanzhong Agricultural University (HZAU), Wuhan

430070, China.

Declarations

Conflict of interest The authors declare that there is no conflict of

interest.

References

Aguilera P, Borie F, Seguel A, Cornejo P (2011) Fluorescence detection

of aluminum in arbuscular mycorrhizal fungal structures and

glomalin using confocal laser scanning microscopy. Soil Biol

Biochem 43(12):2427–2431

Aguilera P, Cornejo P, Borie F, Barea JM, von Baer E, Oehl F (2014)

Diversity of arbuscular mycorrhizal fungi associated with Triticum

aestivum L. plants growing in an andosol with high aluminum level.

Agri Ecosys Env 186:178–184. https://doi.org/10.1016/j.agee.2014.

01.029

Ahanger MA, Tittal M, Mir RA, Agarwal RM (2017) Alleviation of

water and osmotic stress-induced changes in nitrogen metabolizing

enzymes in Triticum aestivum L. cultivars by potassium.

Protoplasma 254:1953–1963. https://doi.org/10.1007/s00709-017-

1086-z

Al Mutairi AA, Cavagnaro TR, Khor SF, Neumann K, Burton RA,

Watts-Williams SJ (2020) The effect of zinc fertilisation and

arbuscular mycorrhizal fungi on grain quality and yield of

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

contrasting barley cultivars. Funct Plant Biol 47(2):122–133. https://

doi.org/10.1071/FP19220

Amiri R, Nikbakht A, Etemadi N, Sabzalian MR (2017) Nutritional sta-

tus, essential oil changes and water-use efficiency of rose geranium

in response to arbuscular mycorrhizal fungi and water deficiency

stress. Symbiosis 73(1):15–25. https://doi.org/10.1007/s13199-

016-0466-z

Asmelash F, Bekele T, Birhane E (2016) The potential role of arbuscular

mycorrhizal fungi in the restoration of degraded lands. Front

Microbiol 7:1095

Babadi M, Zalaghi R, Taghavi M (2019) A non-toxic polymer enhances

sorghum-mycorrhiza symbiosis for bioremediation of cd.

Mycorrhiza 29:375–387. https://doi.org/10.1007/s00572-019-

00902-5

Bagheri V, Shamshiri MH, Shirani H, Roosta HR (2018)Nutrient uptake

and distribution in mycorrhizal pistachio seedlings under drought

stress. J Agric Sci Technol 14:1591–1604. https://doi.org/10.5367/

oa.2012.0109

Balestrini R, Brunetti C, Chitarra W, Nerva L (2020) Photosynthetic traits

and nitrogen uptake in crops: which is the role of Arbuscular

Mycorrhizal fungi? Plants 9(9):1105. https://doi.org/10.3390/

plants9091105

Balestrini R, Chitarra W, Antoniou C, Ruocco M, Fotopoulos V (2018)

Improvement of plant performance under water deficit with the em-

ployment of biological and chemical priming agents. The J Agric

Sci 156(5):680–688

Balliu A, Sallaku G, Rewald B (2015) AMF inoculation enhances growth

and improves the nutrient uptake rates of transplanted, salt-stressed

tomato seedlings. Sustainability 7(12):15967–15981. https://doi.

org/10.3390/su71215799

Barbosa MV, Pedroso DDF, Curi N, Carneiro MAC (2019) Do different

arbuscular mycorrhizal fungi affect the formation and stability of

soil aggregates? Ciên E Agrotecnol 43. https://doi.org/10.1590/

1413-7054201943003519

Baslam M, Garmendia I, Goicoechea N (2011) Arbuscular mycorrhizal

fungi (AMF) improved growth and nutritional quality of

greenhouse-grown lettuce. J Agric Food Chem 59(10):5504–5515.

https://doi.org/10.1021/jf200501c

Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustain-

able agriculture. Physiol Mol Plant Pathol 102:36–45. https://doi.

org/10.1016/j.pmpp.2017.11.2017

Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ahmed N, AshrafM,

Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant

growth regulation: implications in abiotic stress tolerance. Front

Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068

Bennett AE, Meek HC (2020) The influence of arbuscular mycorrhizal

fungi on plant reproduction. J Chem Ecol 46(8):707–721. https://

doi.org/10.1007/s10886-020-01192-4

Bettoni MM, Mogor ÁF, Pauletti V, Goicoechea N (2014) Growth and

metabolism of onion seedlings as affected by the application of

humic substances, mycorrhizal inoculation and elevated CO2. Sci

Hortic 180:227–235

Bhantana P, Lazarovitch N (2010) Evapotranspiration, crop coefficient

and growth of two young pomegranate (Punica granatum L.) varie-

ties under salt stress. Agric Water Manag 97(5):715–722

Bhantana P, Timlin D, Rana MS, Moussa MG, Zhihao D, Sun X, Tan Q,

Xiao HC (2020) How to cut down the gap between the Zn require-

ment and supply of food chain and crop growth: a critical review. Int

J Plant, Anim Environ Sci 10:001–026

Bianciotto V, Victorino I, Scariot V, Berruti A (2018) Arbuscular mycor-

rhizal fungi as natural biofertilizers: current role and potential for the

horticulture industry. III Int Symposium Woody Ornament

Temperate Zone 1191:207–216. https://doi.org/10.17660/

ActaHortic.2018.1191.29

Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012)

Arbuscular mycorrhizal fungi enhance photosynthesis, water use

efficiency, and growth of frankincense seedlings under pulsed water

availability conditions. Oecologia 169(4):895–904. https://doi.org/

10.1007/s00442-012-2258-3

Black KG, Mitchell DT, Osborne BA (2000) Effect of mycorrhizal-

enhanced leaf phosphate status on carbon partitioning, translocation

and photosynthesis in cucumber. Plant Cell Environ 23(8):797–809

Bolandnazar S, Aliasgarzad N, Neishabury MR, Chaparzadeh N (2007)

Mycorrhizal colonization improvesonion (Allium cepa L.) yield and

water use efficiency under water deficit condition. Sci Hortic 114(1):

11–15

Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A,

Lingua G, D’Agostino G, Gamalero E, Berta G (2017) Arbuscular

mycorrhizal fungi and plant growth-promoting pseudomonads im-

prove yield, quality and nutritional value of tomato: a field study.

Mycorrhiza 27(1):1–11

Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U,

Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C

(2010) Phosphate systemically inhibits development of arbuscular

mycorrhiza in Petunia hybrida and represses genes involved in my-

corrhizal functioning. Plant J 64(6):1002–1017

Cao J, Feng Y, Lin X, Wang J (2016) Arbuscular mycorrhizal fungi

alleviate the negative effects of iron oxide nanoparticles on bacterial

community in rhizospheric soils. Front Environ Sci 4:10

Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility.

Agri Ecosys Environ 116(1-2):72–84

Carillo P, Kyratzis A, Kyriacou MC, Dell’Aversana E, Fusco GM,

Corrado G, Rouphael Y (2020) Biostimulatory action of

Arbuscular Mycorrhizal fungi enhances productivity, functional

and sensory quality in ‘Piennolo del Vesuvio’Cherry tomato land-

races. Agron. 10(6):911. https://doi.org/10.3390/

agronomy10060911

Cassman KG (1999) Ecological intensification of cereal production sys-

tems: yield potential, soil quality, and precision agriculture. Proc

Natio Aca Sci 96(11):5952–5959

Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R,

Cárdenas-Navarro R (2010) Root colonisation by the arbuscular

mycorrhizal fungus Glomus intraradices alters the quality of straw-

berry fruits (Fragaria× ananassa Duch.) at different nitrogen levels. J

Sci Food Agric 90(11):1774–1782. https://doi.org/10.1002/jsfa.

3998

Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving

plant zinc nutrition under low soil zinc concentrations: a review.

Plant and Soil 304(1–2):315–325. https://doi.org/10.1007/s11104-

008-9559-7

Cavagnaro TR, Smith FA, Smith SE, Jakobsen I (2005) Functional di-

versity in arbuscular mycorrhizas: exploitation of soil patches with

different phosphate enrichment differs among fungal species. Plant

Cell Environ 28(5):642–650

Ceasar SA, Hodge A, Baker A, Baldwin SA (2014) Phosphate

concentration and arbuscular mycorrhizal colonisation influ-

ence the growth, yield and expression of twelve PHT1 family

phosphate transporters in foxtail millet (Setaria italica). PLoS

One 9(9):108459. https://doi.org/10.1371/journal.pone.

0108459

Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T (2019)

Impact of arbuscular mycorrhizal fungi on photosynthesis, water

status, and gas exchange of plants under salt stress–a meta-analysis.

Front Plant Sci 10:457. https://doi.org/10.3389/fpls.2019.00457

Charron G, Furlan V, Bernier-Cardou M, Doyon G (2001a) Response of

onion plants to arbuscular mycorrhizae. 1. Effects of inoculation

method and phosphorus fertilization on biomass and bulb firmness.

Mycor 11:187–197

Charron G, Furlan V, Bernier-Cardou M, Doyon G (2001b) Response of

onion plants to arbuscular mycorrhizae: 2. Effects of nitrogen fertil-

ization on biomass and bulb firmness. Mycor 11(3):145

Bhantana P. et al.

Chasapis CT, Nitoupa PSA, Spiliopoulou CA, Stefanidou ME (2020)

Recent aspects of the effect on Zn on human health. https://doi.

org/10.1007/s00204-020-02702-9 Recent aspects of the effects of

zinc on human health

Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial

services of arbuscular mycorrhizal fungi–from ecology to applica-

tion. Front Plant Sci 9:1270

Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Jiang Y, Liu A, Zhao P,

Wang M, Ahammed GJ (2017) Combined inoculation with multiple

arbuscular mycorrhizal fungi improves growth, nutrient uptake and

photosynthesis in cucumber seedlings. Front Microbiol 8:2516

Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P,

Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights

on the impact of arbuscular mycorrhizal symbiosis on tomato toler-

ance to water stress. Plant Phyiol 171(2):1009–1023. https://doi.org/

10.1104/pp.16.00307

Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress

translocation of zinc to shoots of host plants in soils moderately

polluted with zinc. Plant Soil 261(1):209–217

Compant S, Samad A, Faist H, Sessitsch A (2019) A review on theplant

microbiome: ecology, functions, and emerging trends in microbial

application. J Adv Res 19:29–37

Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on

growth, distribution of glandular hairs, and essential oil production

in Ocimum basilicum L. var. Genovese. Mycor 16(7):485–494

Copetta A, Todeschini V, Massa N, Bona E, Berta G, Lingua G (2020)

Inoculation with arbuscular mycorrhizal fungi improves melon

(Cucumis melo) fruit quality under field conditions and plant per-

formance in both field and greenhouse. Plant Biosyst Int J Dealing

Aspects Plant Biol:1–12. https://doi.org/10.1080/11263504.2020.

1813831

Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root

exudates shape the nitrogen cycle. Trends Plant Sci 22(8):661–673

Dar ZM, Masood A, Asif M, Malik MA (2018) Review on arbuscular

mycorrhizal fungi: an approach to overcome drought adversities in

plants. Int J Curr Microbiol App Sci 7(3):1040–1049. https://doi.

org/10.20546/ijcmas.2018.703.124

Elhindi KM, El-Din AS, Elgorban AM (2017) The impact of arbuscular

mycorrhizal fungi in mitigating salt-induced adverse effects in sweet

basil (Ocimum basilicum L.). Saudi J Biol Sci 24(1):170–179.

https://doi.org/10.1016/j.sjbs.2016.02.010

Elliott AJ, Daniell TJ, Cameron DD, Field KJ (2020) A commercial

arbuscular mycorrhizal inoculum increases root colonization across

wheat cultivars but does not increase assimilation of mycorrhiza-

acquired nutrients. In: Plants,people, planet A commercial

arbuscular mycorrhizal inoculum increases root colonization across

wheat cultivars but does not increase assimilation of mycorrhiza‐

acquired nutrients

El-Nashar YI (2017) Response of snapdragon (Antirrhinum majus L.) to

blended water irrigation and arbuscular mycorrhizal fungi inocula-

tion: uptake of minerals and leaf water relations. Photosynthetica

55(2):201–209. https://doi.org/10.1007/s11099-016-0650-7

Emmanuel OC, Babalola OO(2020) Productivity and quality of horticul-

tural crops through co-inoculation of arbuscular mycorrhizal fungi

and plant growth promoting bacteria. Microbiol Res 126569. https://

doi.org/10.1016/j.micres.2020.126569

Ercoli L, Schüßler A, Arduini I, Pellegrino E (2017) Strong increase of

durum wheat iron and zinc content by field-inoculation with

arbuscular mycorrhizal fungi at different soil nitrogen availabilities.

Plant and Soil 419(1–2):153–167. https://doi.org/10.1007/s11104-

017-3319-5

Esteras C, Rambla JL, Sánchez G, López-Gresa MP, González-Mas MC,

Fernández-Trujillo JP, Bellés JM, Granell A, Picó MB (2018) Fruit

flesh volatile and carotenoid profile analysis within the Cucumis

melo L. species reveals unexploited variability for future genetic

breeding. J Sci Food Agric 98(10):3915–3925. https://doi.org/10.

1002/jsfa.8909

Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices

inoculation to nutrient acquisition and mitigation of ionic imbalance

in NaCl-stressed Trigonella foenum-graecum. Mycor 22(3):203–

217. https://doi.org/10.1007/s00572-011-0392-0

FAO (2019) Food and agriculture Organization of the United Nations

FAOSTAT, http://www.fao.org/faostat/en/#data/QC

Field C, Mooney HA (1983) Leaf age and seasonal effects on light, water,

and nitrogen use efficiency in a California shrub. Oecologia 56(2–

3):348–355

Fota-Markowska H, Przybyła A, Borowicz I, Modrzewska R (2002)

Serum zinc (Zn) level dynamics in blood serum of patients with

acute viral hepatitis B and early recovery period. In Annales

Universitatis Mariae curie-Sklodowska. Sectio D: Medicina 57(2):

201–209

Gao X, Guo H, Zhang Q, Guo H, Zhang L, Zhang C, Gou Z, Liu Y, Wei

J, Chen A, Chu Z (2020) Arbuscular mycorrhizal fungi (AMF)

enhanced the growth, yield, fiber quality and phosphorus regulation

in upland cotton (Gossypium hirsutum L.). Sci Rep 10:1–12. https://

doi.org/10.1038/s41598-020-59180-3

Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on

growth, cadmium uptake, osmolyte, and phytochelatin synthesis in

Cajanus cajan (L.) Millsp. Under NaCl and cd stresses. J Plant

Growth Regul 31(3):292–308. https://doi.org/10.1007/s00344-011-

9239-3

Genc Y, McDonald GK, Graham RD (2004) Differential expression of

zinc efficiency during the growing season of barley. Plant and Soil

263:273–282. https://doi.org/10.1023/B:PLSO.0000047741.52700.

Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A,

Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C (2012)

Nutraceutical value and safety of tomato fruits produced by mycor-

rhizal plants. Br J Nutr 107(2):242–251

Glutsch V, Hamm H, Goebeler M (2019) Zinc and skin: an update. J

Deutschen Dermatologischen Gesellschaft 17(6):589–596. https://

doi.org/10.1111/ddg.13811

Golubkina N, Amagova Z, Matsadze V, Zamana S, Tallarita A, Caruso G

(2020d) Effects of Arbuscular Mycorrhizal fungi on yield, biochem-

ical characteristics, and elemental composition of garlic and onion

under selenium supply. Plants 9(1):84

Golubkina N, Gomez LD, Kekina H, Cozzolino E, Simister R, Tallarita

A, Torino V, Koshevarov A, Cuciniello A, Maiello R, Cenvinzo V

(2020a) Joint selenium–iodine supply and Arbuscular Mycorrhizal

fungi inoculation affect yield and quality of chickpea seeds and

residual biomass. Plants 9(7):804. https://doi.org/10.3390/

plants9070804

GolubkinaN, Krivenkov L, Sekara A, Vasileva V, Tallarita A, CarusoG

(2020b) Prospects of Arbuscular Mycorrhizal fungi utilization in

production of allium plants. Plants 9(2):279. https://doi.org/10.

3390/plants9020279

Golubkina N, Logvinenko L, Novitsky M, Zamana S, Sokolov S,

Molchanova A, Shevchuk O, Sekara A, Tallarita A, Caruso G

(2020c) Yield, essential oil and quality performances of Artemisia

dracunculus, Hyssopus officinalis and Lavandula angustifolia as

affected by arbuscular mycorrhizal fungi under organic manage-

ment. Plants 9(3):375. https://doi.org/10.3390/plants9030375

Golubkina N, Zamana S, Seredin T, Poluboyarinov P, Sokolov S,

Baranova H, Krivenkov L, Pietrantonio L, Caruso G (2019) Effect

of selenium biofortification and beneficial microorganism inocula-

tion on yield, quality and antioxidant properties of shallot bulbs.

Plants 8(4):102

Gómez-Bellot MJ, Ortuño MF, Nortes PA, Vicente-Sánchez J, Bañón S,

Sánchez-Blanco MJ (2015) Mycorrhizal euonymus plants and

reclaimed water: biomass, water status and nutritional responses.

Sci Hortic 186:61–69. https://doi.org/10.1016/j.scienta.2015.02.022

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW,

Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in

the arbuscular mycorrhizal symbiosis. Nature 435(7043):819–823

Hanen N, Fattouch S, Ammar E, Neffati M (2012) Allium species, an-

cient health food for the future. Sci Health Soc Aspects Food Indust,

pp 343–355

Hart M, Ehret DL, Krumbein A, Leung C, Murch S, Turi C, Franken P

(2015) Inoculation with arbuscular mycorrhizal fungi improves the

nutritional value of tomatoes. Mycor. 25(5):359–376. https://doi.

org/10.1007/s00572-014-0617-0

Hashem A, Abd Allah EF, Alqarawi AA, Aldubise A, Egamberdieva D

(2015) Arbuscular mycorrhizal fungi enhances salinity tolerance of

Panicum turgidum Forssk by altering photosynthetic and antioxi-

dant pathways. J Plant Interact 10(1):230–242. https://doi.org/10.

1080/17429145.2015.1052025

Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani ABF, Aldehaish

HA, Egamberdieva D, Abd Allah EF (2018) Arbuscular mycorrhi-

zal fungi regulate the oxidative system, hormones and ionic equilib-

rium to trigger salt stress tolerance in Cucumis sativus L. Saudi J

Biol Sci 25(6):1102–1114. https://doi.org/10.1016/j.sjbs.2018.03.

009

He F, Sheng M, Tang M (2017) Effects of Rhizophagus irregularis on

photosynthesis and antioxidative enzymatic system in Robinia

pseudoacacia L. under drought stress. Front Plant Sci 8:183.

https://doi.org/10.3389/fpls.2017.00183

Higo M, Azuma M, Kamiyoshihara Y, Kanda A, Tatewaki Y, Isobe K

(2020) Impact of phosphorus fertilization on tomato growth and

arbuscular mycorrhizal fungal communities. Microorganisms 8(2):

178. https://doi.org/10.3390/microorganisms8020178

Higo M, Sato R, Serizawa A, Takahashi Y, Gunji K, Tatewaki Y, Isobe K

(2018) Can phosphorus application and cover cropping alter

arbuscular mycorrhizal fungal communities and soybean perfor-

mance after a five-year phosphorus-unfertilized crop rotational sys-

tem? Peer J 6:e4606. https://doi.org/10.2478/agri-2019-0001

Ibiremo OS, Olubamiwa O, Agbeniyi SO, Akanbi OSO (2012) Response

of cashew seedlings from different nut sizes to phosphate fertilizer

and Arbuscular mycorrhizal inoculation in two soils in Nigeria. Int J

Plant Anim Environ Sci 2:147–158

IFA (2019) International fertilizer association, Paris (France) IFASTAT,

https://www.ifastat.org/databases/plant-nutrition

Igamberdiev AU, Eprintsev AT (2016) Organic acids: the pools of fixed

carbon involved in redox regulation and energy balance in higher

plants. Front Plant Sci 7:1042

Jansa J, Mozafar A, Anken T, Ruh R, Sanders I, Frossard E (2002)

Diversity and structure of AMF communities as affected by tillage

in a temperate soil. Mycor. 12(5):225–234

Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and

Zn through the hyphae of an arbuscular mycorrhizal fungus in sym-

biosis with maize. Agronomie 23:481–488

Jansson C, Vogel J, Hazen S, Brutnell T, Mockler T (2018) Climate-

smart crops with enhanced photosynthesis. J Exp Bot 69(16):

3801–3809

Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen

X, Tang D, Wang E (2017) Plants transfer lipids to sustain coloni-

zation by mutualistic mycorrhizal and parasitic fungi. Sci. 356:

1172–1175. https://doi.org/10.1126/science.aam9970

Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ,Shachar‐Hill Y

(2005) The uptake, metabolism, transport and transfer of nitrogen in

an arbuscular mycorrhizal symbiosis. New Phytol 168(3):687–696

Joutey NT, Sayel H (2015) Mechanisms of hexavalent chromium resis-

tance and removal by microorganisms. RevEnv Cont Toxicol 233:

45–69. https://doi.org/10.1007/978-3-319-10479-9_2

Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012)

Mycorrhiza-induced resistance and priming of plant defenses. J

Chem Ecol 38(6):651–664. https://doi.org/10.1007/s10886-012-

0134-6

Juntahum S, Jongrungklang N, Kaewpradit W, Lumyong S, Boonlue S

(2020) Impact of Arbuscular Mycorrhizal fungi on growth and pro-

ductivity of sugarcane under Field conditions. Sugar Tech 22(3):

451–459. https://doi.org/10.1007/s12355-019-00784-z

Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM

utilization through reduced P fertilization 2. Field studies. Plant and

Soil 231(1):65–79

Kaldorf M, Schmelzer E, Bothe H (1998) Expression of maize and fungal

nitrate reductase genes in arbuscular mycorrhiza. Mol Plant Microbe

Interact 11(6):439–448

Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular

mycorrhiza and phosphorus application on artemisinin concentra-

tion in Artemisia annua L. Mycor. 17(7):581–587

Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil

yield and quality in Foeniculum vulgare mill on mycorrhizal inocu-

lation supplemented with P-fertilizer. Bioresour Technol 93(3):307–

311

Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009)

The influence of arbuscular mycorrhizal colonisation on key growth

parameters and fruit yield of pepper plants grown at high salinity.

Sci Hortic 121(1):1–6. https://doi.org/10.1016/j.scienta.2009.01.

001

Kertesz MA,Mirleau P (2004) The role of soil microbesin plant Sulphur

nutrition. J Exp Bot 55:1939–1945

Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006)

Arbuscular mycorrhiza alter the concentration of essential oils in

oregano (Origanum sp., Lamiaceae). Mycor 16(6):443–446

Kim SJ, Eo JK, Lee EH, Park H, Eom AH (2017) Effects of arbuscular

mycorrhizal fungi and soil conditions on crop plant growth.

Mycobiol. 45(1):20–24. https://doi.org/10.5941/MYCO.2017.45.1.

Kochian LV (2000) Molecular Physiology of Mineral Nutrient

Acquisition, Transport, and Utilization, Biochemistry and

Molecular Biology of Plants. In Buchanan BB, Gruissem W, and

Jones RL (eds) Rockville, pp 1204–1249

Krzesłowska M (2011) The cell wall in plant cell response to trace metals:

polysaccharide remodeling and its role in defense strategy. Acta

Physiolo. Planta. 33(1):35–51. https://doi.org/10.1007/s11738-010-

0581-z

Kumar S, Saxena S (2019) Arbuscular Mycorrhizal fungi (AMF) from

heavy metal-contaminated soils: molecular approach and applica-

tion in phytoremediation. Biofert Sustain Agri Environ:489–

500Springer, Cham. https://doi.org/10.1007/978-3-030-18933-4_

Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular

mycorrhizal influence on zinc nutrition in crop plants–a meta-anal-

ysis. Soil Biol Biochem 69:123–131

Li H, Chen XW, Wong MH (2016a) Arbuscular mycorrhizal fungi re-

duced the ratios of inorganic/organic arsenic in rice grains. Chemo.

145:224–230. https://doi.org/10.1016/j.chemosphere.2015.10.067

Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH

(2016b) Do arbuscular mycorrhizal fungi affect cadmium uptake

kinetics, subcellular distribution and chemical forms in rice? Sci

Total Environ 571:1183–1190. https://doi.org/10.1016/j.scitotenv.

2016.07.124

Lin J, Wang Y, Sun S, Mu C, Yan X (2017) Effects of arbuscular my-

corrhizal fungi on the growth, photosynthesis and photosynthetic

pigments of Leymus chinensis seedlings under salt-alkali stress and

nitrogen deposition. SciTot Env 576:234–241. https://doi.org/10.

1016/j.scitotenv.2016.10.091

Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of

Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in

soil at different P and micronutrient levels. Mycor 9(6):331–336

Liu C, Ravnskov S, Liu F, RubækGH, Andersen MN (2018) Arbuscular

mycorrhizal fungi alleviate abiotic stresses in potato plants caused

Bhantana P. et al.

by low phosphorus and deficit irrigation/partial root-zone drying. J

Agric Sci 156:46–58. https://doi.org/10.1017/S0021859618000023

Livingstone C (2015) Zinc: physiology, deficiency, and parenteral nutri-

tion. Nutri Clini Prac 30(3):371–382. https://doi.org/10.1177/

0884533615570376

Lone R, Shuab R, Wani KA, Ganaie MA, Tiwari AK, Koul KK (2015)

Mycorrhizal influence on metabolites, indigestible oligosaccharides,

mineral nutrition and phytochemical constituents in onion (Allium

cepa L.) plant. Sci Hortic 193:55–61

Majewska ML, Rola K, Zubek S (2017) The growth and phosphorus

acquisition of invasive plants Rudbeckia laciniata and Solidago

gigantea are enhanced by arbuscular mycorrhizal fungi. Mycor.

27(2):83–94

Malik AA, Suryapani S, Ahmad J (2011) Chemical vs organic cultivation

of medicinal and aromatic plants: the choice is clear. Int J Med Arom

Plants 1(1):5–13

Marro N, Cofré N, Grilli G, Alvarez C, Labuckas D, Maestri D, Urcelay

C (2020) Soybean yield, protein content and oil quality in response

to interaction of arbuscular mycorrhizal fungi and native microbial

populations from mono-and rotation-cropped soils. App Soil Ecol

152:103575

Miransari M (2017) Arbuscular mycorrhizal fungi and heavy metal tol-

erance in plants. In: Arbuscular mycorrhizas and stress tolerance of

plants. Springer, Singapore, pp 147–161. https://doi.org/10.1007/

978-3-319-68867-1_4

Moghadam HRT (2016) Application of super absorbent polymer and

ascorbic acid to mitigate deleterious effects of cadmium in wheat.

Pesquisa Agropecuária Trop 46(1):9–18. https://doi.org/10.1590/

1983-40632016v4638946

Mohamed AA, Eweda WE, Heggo AM, Hassan EA (2014) Effect of dual

inoculation with arbuscular mycorrhizal fungi and Sulphur-

oxidising bacteria on onion (Allium cepa L.) and maize (Zea mays

L.) grown in sandy soil under green house conditions. Ann Agri Sci

59(1):109–118

Moradtalab N, Hajiboland R, Aliasgharzad N, Hartmann TE, Neumann G

(2019) Silicon and the association with an arbuscular-mycorrhizal

fungus (Rhizophagus clarus) mitigate the adverse effects of drought

stress on strawberry. Agronomy 9(1):41. https://doi.org/10.3390/

agronomy9010041

More TT, Yadav JSS, Yan S, Tyagi RD, Surampalli RY (2014)

Extracellular polymeric substances of bacteria and their potential

environmental applications. J Environ Manage 144:1–25. https://

doi.org/10.1016/j.jenvman.2014.05.010

Mosse B, Stribley DP, LeTacon F (1981) Ecology of mycorrhizae and

mycorrhizal fungi. Adv Microb Ecol 5:137–210 Springer, Boston,

Natasha G (2009) The disappearing nutrient. Nature 461:716–718

Nguyen TD, Cavagnaro TR, Watts-Williams SJ (2019) The effects of soil

phosphorus and zinc availability on plant responses to mycorrhizal

fungi: a physiological and molecular assessment. Sci Rep 9(1):1–13.

https://doi.org/10.1038/s41598-019-51369-5

Olowe OM, Olawuyi OJ, Sobowale AA, Odebode AC (2018) Role of

arbuscular mycorrhizal fungi as biocontrol agents against Fusarium

verticillioides causing ear rot of Zea mays L.(maize). Curr Plant Biol

15:30–37

Ortas I (2010) Effect of mycorrhiza application on plant growth and

nutrient uptake in cucumber production under field conditions.

Spanish J Agri Res 1:116–122

Ortas I (2012) The effect of mycorrhizal fungal inoculation onplant yield,

nutrient uptake and inoculation effectiveness under long-term field

conditions. Field Crop Res 125:35–48. https://doi.org/10.1016/j.fcr.

2011.08.005

Ortas I, Sari N, Akpinar C, Yetisir H (2013) Selection of arbuscular

mycorrhizal fungi species for tomato seedling growth, mycorrhizal

dependency and nutrient uptake. Europ J Hort Sci 78(5):209–218

Pae M, Meydani SN, Wu D (2012) The role of nutrition in enhancing

immunity in aging. Aging Dis 3(1):91–129

Pawlowska TE, Charvat I (2004) Heavy-metal stress and developmental

patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol

70(11):6643–6649

Pérez-de-Luque A, Tille S, Johnson I, Pascual-Pardo D, Ton J, Cameron

DD (2017) The interactive effects of arbuscular mycorrhiza and

plant growth-promoting rhizobacteria synergistically enhance host

plant defences against pathogens. Sci Rep 7(1):1–10. https://doi.org/

10.1038/s41598-017-16697-4

Pilbeam DJ (2018) The utilization of nitrogen by plants: A whole plant

perspective. Annual Plant Rev 42:305–351. https://doi.org/10.1002/

9781444328608.ch13

Piliarová M, Ondreičková K, Hudcovicová M, Mihálik D, Kraic J (2019)

Arbuscular Mycorrhizal fungi–their life and function in ecosystem.

Agri (Pol'nohospodárstvo) 65(1):3–15

Pingali PL (2012) Green revolution: impacts, limits, and the path ahead.

Proc Natl Acad Sci 109(31):12302–12308

Ponce MA, Scervino JM, Erra-Balsells R, Ocampo JA, Godeas AM

(2004) Flavonoids from shoots and roots of Trifolium repens (white

clover) grown in presence or absence of the arbuscular mycorrhizal

fungus Glomus intraradices. Phytochemistry 65(13):1925–1930

Prasad AS (2009) Zinc: role in immunity, oxidative stress and chronic

inflammation. Curr Opin Clin Nutr Metab Care 12(6):646–652.

https://doi.org/10.1097/MCO.0b013e3283312956

Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A

(2017) Introduction to mycorrhiza: historical development. In:

Mycorrhiza-Function, Diversity, state of the art. Springer, Cham,

pp 1–7. https://doi.org/10.1007/978-3-319-53064-2_1

Quiroga G, Erice G, Aroca R, Delgado-Huertas A, Ruiz-Lozano JM

(2020) Elucidating the possible involvement of maize aquaporins

and arbuscular mycorrhizal symbiosis in the plant ammonium and

urea transport under drought stress conditions. Plants 9(2):148

Rabot E, Wiesmeier M, Schlüter S, Vogel HJ (2018) Soil structure as an

indicator of soil functions: a review. Geoderma 314:122–137.

https://doi.org/10.1016/j.geoderma.2017.11.009

Rahimzadeh S, Pirzad A (2017) Arbuscular mycorrhizal fungi and pseu-

domonas in reduce drought stress damage in flax (Linum

usitatissimum L.): a field study. Mycor 27(6):537–552

Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y,

Zhou Y, Anastopoulos I, Wang X (2020) Arbuscular mycorrhizal

fungi-induced mitigation of heavy metal phytotoxicity in metal con-

taminated soils: a critical review. J Hazard Mater 402:123919.

https://doi.org/10.1016/j.jhazmat.2020.123919

Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR,

Degrune F, Hohmann P, Lammel DR, Mansour I, Roy J, van der

Heijden MG, Yang G (2019) Why farmers should manage the

arbuscular mycorrhizal symbiosis. New Phytol 222(3):1171–1175

Rillig MC, Muller LA, Lehmann A (2017) Soil aggregates as massively

concurrent evolutionary incubators. The ISME J 11(9):1943–1948.

https://doi.org/10.1038/ismej.2017.56

Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signal-

ing in plants: conserved and novel mechanisms. Annu Rev Plant

Biol 57:675–709

Rouphael Y, Cardarelli M, Bonini P, Colla G (2017) Synergistic action of

a microbial-based biostimulant and a plant derived-protein hydroly-

sate enhances lettuce tolerance to alkalinity and salinity. Front Plant

Sci 8:131

Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M,

Agnolucci M, De Pascale S, Bonini P, Colla G (2015) Arbuscular

mycorrhizal fungi act as biostimulants in horticultural crops. Sci

Hortic 196:91–108. https://doi.org/10.1016/j.scienta.2015.09.002

Rydlová J, Püschel D, Dostálová M, Janoušková M, Frouz J (2016)

Nutrient limitation drives response of Calamagrostis epigejos to

arbuscular mycorrhiza in primary succession. Mycor. 26(7):757–

767

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and...

Sadhana B (2014) Arbuscular Mycorrhizal fungi (AMF) as a biofertilizer-

a review. Int J Curr Microbiol App Sci 3(4):384–400

Sánchez PA, Salinas JG (1981) Low-input technology for managing

Oxisols and Ultisols in tropical America. Adv Agron 34:279–406

Academic press

Santander C, Sanhueza M, Olave J, Borie F, Valentine A, Cornejo P

(2019) Arbuscular mycorrhizal colonization promotes the tolerance

to salt stress in lettuce plants through an efficient modification of

ionic balance. J Soil Sci Plant Nutr 19(2):321–331. https://doi.org/

10.1007/s42729-019-00032-z

Sato T, Ezawa T, Cheng W, Tawaraya K (2015) Release of acid phos-

phatase from extraradical hyphae of arbuscular mycorrhizal fungus

Rhizophagus clarus. Soil Sci Plant Nutr 61(2):269–274

Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbi-

onts affecting the production of health-promoting phytochemicals.

Electrophoresis 35(11):1535–1546

Schneider J, Stürmer SL, Guilherme LRG, de Souza Moreira FM, de

Sousa Soares CRF (2013) Arbuscular mycorrhizal fungi in

arsenic-contaminated areas in Brazil. J. Hazard Mater 262:1105–

1115. https://doi.org/10.1016/j.jhazmat.2012.09.063

Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ,

Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa

NK, Tsay YF (2013) Using membrane transporters to improve crops

for sustainable food production. Nature 497(7447):60–66

Schüßler A, Krüger C, Urgiles N (2016) Phylogenetically diverse AM

fungi from Ecuador strongly improve seedling growth of native

potential crop trees. Mycor. 26(3):199–207

Selosse MA, Strullu-Derrien C, Martin FM, Kamoun S, Kenrick P (2015)

Plants, fungi and oomycetes: a 400-million year affair that shapes

the biosphere. New Phytol 206:501–506. https://doi.org/10.1111/

nph.13371

Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B

(2019) Response of phenylpropanoid pathway and the role of poly-

phenols in plants under abiotic stress. Molecules 24(13):2452

Sharma N, Yadav K, Cheema J,Badda N, Aggarwal A (2015) Arbuscular

Mycorrhizal Symbiosis and water stress: a critical review. Pert J

Trop Agri Sci 38(4):427–453

Siani NG, Fallah S, Pokhrel LR, Rostamnejadi A (2017) Natural amelio-

ration of zinc oxide nanoparticle toxicity in fenugreek (Trigonella

foenum-gracum) by arbuscular mycorrhizal (Glomus intraradices)

secretion of glomalin. Plant Physiol Biochem 112:227–238.

https://doi.org/10.1016/j.plaphy.2017.01.001

Singh V, Sharma S, Kunal Gosal SK, Choudhary R, Singh R, Adholeya

A, Singh B (2020) Optical sensing and arbuscular mycorrhizal fungi

for improving fertilizer nitrogen and phosphorus use efficiencies in

maize. J Soil Sci Plant Nutr 20(4):2087–2098. https://doi.org/10.

1007/s42729-020-00277-z

Sivakumar PV, Palanisamy K, Lenin M (2020) Potential role of

arbuscular mycorrizhal fungi (AMF) and vermicompost (vc) on

the maturation of Agri-culture crops-a review. S. Asian J life Sci

8(2):24–37. https://doi.org/10.17582/journal.sajls/2020/8.2.24.37

Smil V (1999) Detonator of the population explosion.Nature 400(6743):

415–415

Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular

mycorrhizas in plant phosphorus nutrition: interactions between

pathways of phosphorus uptake in arbuscular mycorrhizal roots

have important implications for understanding and manipulating

plant phosphorus acquisition. Plant Physiol 156:1050–1057.

https://doi.org/10.1104/pp.111.174581

Souza LA, López Andrade SA, Ribeiro Souza SC, Schiavinato MA

(2013) Evaluation of mycorrhizal influence on the development

and phytoremediation potential of Canavalia gladiata in Pb-

contaminated soils. Int J Phytorem 15(5):465–476. https://doi.org/

10.1080/15226514.2012.716099

Tarkka MT, Drigo B, Deveau A (2018) Mycorrhizal microbiomes.

Mycor. 28(5–6):403–409

Tawarava K, Tokairin K, Wagatsuma T (2001) Dependence of Allium

fistulosum cultivars on the arbuscular mycorrhizal fungus, Glomus

fasciculatum. App Soil Ecol 17(2):119–124

Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are

mycorrhizal fungi our sustainable saviours? Considerations for

achieving food security. J Ecol 105(4):921–929. https://doi.org/10.

1111/1365-2745.12788

Toscano S, Trivellini A, Cocetta G, Bulgari R, Francini A,

Romano D, Ferrante A (2019) Effect of pre-harvest abiotic

stresses on the accumulation of bioactive compounds in hor-

ticultural produce. Front Plant Sci 10:1212. https://doi.org/10.

3389/fpls.2019.01212

Turrini A, Avio L, Giovannetti M, Agnolucci M (2018) Functional com-

plementarity of arbuscular mycorrhizal fungi and associated micro-

biota: the challenge of translational research. Front Plant Sci 9:1407

Valkov VT, Sol S, Rogato A, Chiurazzi M (2020) The functional char-

acterization of LjNRT2. 4 indicates a novel, positive role of nitrate

for an efficientnodule N2‐fixation activity. New Phytol 228(2):682–

696

Vilela LAF, Barbosa MV (2019) Contributionof Arbuscular Mycorrhizal

fungi in promoting cadmium tolerance in plants. In: Cad. Tolerance

plants. Academic, pp 553–586. https://doi.org/10.1016/b978-0-12-

815794-7.00021-7

Walder F, van der Heijden MG (2015) Regulation of resource exchange

in the arbuscular mycorrhizal symbiosis. Nature Plants 1(11):1–7

Wang FY, Tong RJ, Shi ZY, Xu XF, He XH (2011) Inoculations with

arbuscular mycorrhizal fungi increase vegetable yields and decrease

phoxim concentrations in carrot and green onion and their soils.

PLoS One 6(2):16949

Wang L, Ji B, Hu Y, Liu R, Sun W (2017a) A review on in situ

phytoremediation of mine tailings. Chemosphere 184:594–

600. https://doi.org/10.1016/j.chemosphere.2017.06.025

Wang Q, Mei D, Chen J, Lin Y, Liu J, Lu H, Yan C (2019)

Sequestration of heavy metal by glomalin-related soil protein:

implication for water quality improvement in mangrove wet-

lands. Water Res 148:142–152. https://doi.org/10.1016/j.

watres.2018.10.043

WangW,ShiJ,XieQ,JiangY,YuN,WangE(2017b)Nutrient

exchange and regulation in arbuscular mycorrhizal symbiosis.

Mol Plant 10(9):1147–1158. https://doi.org/10.1016/j.molp.

2017.07.012

Wang Y, Wang M, Li Y, Wu A, Huang J (2018) Effects of

arbuscular mycorrhizal fungi on growth and nitrogen uptake

of Chrysanthemum morifolium under salt stress. PLoS One

13(4):e0196408. https://doi.org/10.1371/journal.pone.0196408

Watts-Williams SJ, Nguyen TD, Kabiri S, Losic D, McLaughlin

MJ (2020) Potential of zinc-loaded graphene oxide and

arbuscular mycorrhizal fungi to improve the growth and zinc

nutrition of Hordeum vulgare and Medicago truncatula.

ApplSoil Ecol 150:103464. https://doi.org/10.1016/j.apsoil.

2019.103464

Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty PE (2019)

Trading on the arbuscular mycorrhiza market: from arbuscules to

common mycorrhizal networks. New Phytol 223:1127–1142

Wu QS, Zou YN, Wang GY (2011) Arbuscular mycorrhizal fungi and

acclimatization of micropropagated citrus. Commu Soil Sci Plant

Analy 42(15):1825–1832

Wu S, Zhang X, Chen B, Wu Z, Li T, Hu Y, Sun Y, Wang Y (2016)

Chromium immobilization by extraradical mycelium of arbuscular

mycorrhiza contributes to plant chromium tolerance. Environ Exp

Bot 122:10–18. https://doi.org/10.1016/j.envexpbot.2015.08.006

Wu S, Zhang X, Huang L, Chen B (2019) Arbuscular mycorrhiza and

plant chromium tolerance. Soil Ecol Lett:1–11. https://doi.org/10.

1007/s42832-019-0015-9

Wu Z, McGrouther K, Huang J, Wu P, Wu W, Wang H (2014)

Decomposition and the contribution of glomalin-related soil

Bhantana P. et al.

protein (GRSP) in heavy metal sequestration: field experi-

ment. Soil Biol Biochem 68:283–290. https://doi.org/10.

1016/j.soilbio.2013.10.010

Yousaf B, Liu G, Wang R, Imtiaz M, Zia-ur-Rehman M, Munir MAM,

Niu Z (2016) Bioavailability evaluation, uptake of heavy metals and

potential health risks via dietary exposure in urban-industrial areas.

Environ Sci Pollut Res 23(22):2443–22453. https://doi.org/10.1007/

s11356-016-7449-8

Zeng L, Li J, Liu J, Wang M (2014) Effects of arbuscular mycorrhizal

(AM) fungi on citrus fruit quality under nature conditions.

Southwest China. J Agric Sci 27(5):2101–2105. https://doi.org/10.

16213/j.cnki.scjas.2014.05.067

Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular

mycorrhizal fungi increase grain yields: a meta-analysis. New

Phytol 222(1):543–555. https://doi.org/10.1111/nph.15570

Zou YN, Srivastava AK, Wu QS (2016) Glomalin: a potential soil con-

ditioner for perennial fruits. Int J Agric Biol 18:293–297. https://doi.

org/10.17957/IJAB/15.0085

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Unveiling arbuscular mycorrhizal fungi: the hidden heroes of soil to control the plant pathogens

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Jun 2024
Arch Phytopathology Plant Protect

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Aug 2024

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Belowground nitrogen transfer from Pterocarpus officinalis to Taro under field and controlled conditions

Article

Full-text available

May 2024
PLANT SOIL

Background and Aim: In Guadeloupe’s swamp forests, smallholder farmers traditionally cultivate flooded Colocasia esculenta (taro) monocultures under the canopy of Pterocarpus officinalis stands, without the use of pesticides and fertilizers. To bet- ter understand functioning of this traditional agrofor- estry system, we estimated the ability of the tree leg- ume P. officinalis to fix atmospheric nitrogen (N) and to transfer fixed N to C. esculenta under natural and controlled conditions. Methods: We use the 15N natural abundance and the 15N isotope dilution methods to determine the abil- ity of P. officinalis to fix atmospheric N and to trans- fer fixed N to C. esculenta under three natural sites and controlled conditions via arbuscular mycorrhizal (AM) inoculation, respectively.Results: The proportions of fixed N (%Ndfa) in P. officinalis in swamp forest varied from 72 to 95% in mature trees, from 52 to 81% in seedlings associated with C. esculenta, and from 78 to 84% in seedlings not associated with C. esculenta. The proportion of fixed N transferred from P. officinalis seedlings to C. esculenta neighboring plants was estimated to 27%. The AM inoculation had a significantly positive effect on N2 fixation in P. officinalis, leaf dry weight and leaf P concentration in both P. officinalis and C. esculenta plants in cropping systems. The proportion of fixed N transferred from P. officinalis to C. esculenta in the AM inoculated plants reached 18%. Conclusion: The development of AM mycorrhizal networks may have facilitated the transfer of fixed N from P. officinalis to C. esculenta in field and pot experiments.

Belowground nitrogen transfer from Pterocarpus officinalis to Taro under field and controlled conditions

Article

Full-text available

May 2024
PLANT SOIL

Background and Aim In Guadeloupe’s swamp forests, smallholder farmers traditionally cultivate flooded Colocasia esculenta (taro) monocultures under the canopy of Pterocarpus officinalis stands, without the use of pesticides and fertilizers. To better understand functioning of this traditional agroforestry system, we estimated the ability of the tree legume P. officinalis to fix atmospheric nitrogen (N) and to transfer fixed N to C. esculenta under natural and controlled conditions. Methods We use the ¹⁵N natural abundance and the ¹⁵N isotope dilution methods to determine the ability of P. officinalis to fix atmospheric N and to transfer fixed N to C. esculenta under three natural sites and controlled conditions via arbuscular mycorrhizal (AM) inoculation, respectively. Results The proportions of fixed N (%Ndfa) in P. officinalis in swamp forest varied from 72 to 95% in mature trees, from 52 to 81% in seedlings associated with C. esculenta, and from 78 to 84% in seedlings not associated with C. esculenta. The proportion of fixed N transferred from P. officinalis seedlings to C. esculenta neighboring plants was estimated to 27%. The AM inoculation had a significantly positive effect on N2 fixation in P. officinalis, leaf dry weight and leaf P concentration in both P. officinalis and C. esculenta plants in cropping systems. The proportion of fixed N transferred from P. officinalis to C. esculenta in the AM inoculated plants reached 18%. Conclusion The development of AM mycorrhizal networks may have facilitated the transfer of fixed N from P. officinalis to C. esculenta in field and pot experiments.

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Inoculation with Funneliformis mosseae promotes selenium accumulation and transformation in pepper (Capsicum annuum L.)

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Jun 2024

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Application of AM Fungi in Phytoremediation of Heavy-Metal Contaminated Soil

Chapter

Jun 2024

Arbuscular mycorrhizal (AM) fungi can establish mutualistic relationships with the majority of terrestrial plants and have been found to survive in soils contaminated with heavy metals (HMs). It has been shown that AM fungi not only enhance the tolerance of host plants to HMs, but also accelerate the phytoextraction of HMs, improve the absorption capacity of HMs and stabilize HMs to prevent their migration in the terrestrial ecosystem, which play an important role in phytoremediation of HMs contaminated soil. This chapter aims to summarize the remediation mechanisms and application scenarios of AM fungi for different HMs in soil, and also covers the performance of AM fungi in combination with other techniques.

Success Story of Arbuscular Mycorrhizal Fungi as a Bio Protectant Against Major Plant Pathogens

Chapter

Jun 2024

Arbuscular mycorrhizal fungi (AMF) are considered as most commonly occurring living organisms in soil which play a significant role in improving plant growth and alleviating various environmental stresses. AMF helps in reducing infectious organisms mediated crop damages and facilitates plant growth, development, and stress tolerance, which ultimately results in sustainable agriculture production. It has been shown by several studies that AMF improves plant’s resistance against various plant diseases which are caused by organisms such as viruses, bacteria, nematodes and fungi. Plant pathologists along with environmental scientists have now been looking for more ecofriendly alternatives for controlling plant diseases and pests. The usage of AMF is one such significant bio-based option due to its better efficiency, ecological safety and varied applicabilities. The present chapter discusses the role of AMF in plant nutrition, growth and their potential use as biocontrol agent against major crop diseases and pathogens.

Plant Growth-Promoting Rhizobacteria (PGPR) and Plant Growth-Promoting Fungi (PGPF) for Alleviating Abiotic Stress in Plants

Chapter

May 2024

In the realm of sustainable agriculture, the presence of plant growth-promoting rhizobacteria (PGPR) plays a vital role in mitigating the adverse impacts of abiotic stresses on plants. This chapter offers an analysis of the mechanisms through which PGPR exerts its beneficial effects, including improvements in root morphology and nutrient uptake. Furthermore, it explores the ability of PGPR to stimulate the production of compounds that promote plant growth and activate defense mechanisms against abiotic stress, with a particular focus on mitigating salt stress. The chapter also investigates the signaling mechanisms facilitated by PGPR and the role of phytohormones in promoting plant growth and reducing abiotic stress. Additionally, it examines the contribution of volatile organic compounds (VOCs) produced by PGPR to promoting plant growth and enhancing tolerance to stress. Consequently, this chapter underscores the significance of understanding the interactions between PGPR and plants in order to develop effective strategies for biostimulation. It also highlights the potential of PGPR in achieving sustainable and environmentally friendly agriculture. The insights provided in this chapter are especially relevant for enhancing agricultural productivity and ensuring food security, particularly in light of climate change and the decreasing availability of arable land. The findings underscore the importance of incorporating PGPR-based biostimulants into agriculture to enhance plant growth, improve stress resilience, and promote sustainable crop production.

Photosynthetic Traits and Nitrogen Uptake in Crops: Which Is the Role of Arbuscular Mycorrhizal Fungi?

Article

Full-text available

Aug 2020

Arbuscular mycorrhizal (AM) fungi are root symbionts that provide mineral nutrients to the host plant in exchange for carbon compounds. AM fungi positively affect several aspects of plant life, improving nutrition and leading to a better growth, stress tolerance, and disease resistance and they interact with most crop plants such as cereals, horticultural species, and fruit trees. For this reason, they receive expanding attention for the potential use in sustainable and climate-smart agriculture context. Although several positive effects have been reported on photosynthetic traits in host plants, showing improved performances under abiotic stresses such as drought, salinity and extreme temperature, the involved mechanisms are still to be fully discovered. In this review, some controversy aspects related to AM symbiosis and photosynthesis performances will be discussed, with a specific focus on nitrogen acquisition-mediated by AM fungi.

Joint Selenium-Iodine Supply and Arbuscular Mycorrhizal Fungi Inoculation Affect Yield and Quality of Chickpea Seeds and Residual Biomass

Article

Full-text available

Jun 2020

The essentiality of selenium (Se) and iodine (I) for the human organism and the relationship between these two trace elements in mammal metabolism highlight the importance of the joint Se-I biofortification to vegetable crops in the frame of sustainable farming management. A research study was carried out in southern Italy to determine the effects of the combined inoculation with arbuscular mycorrhizal fungi (AMF) and biofortification with Se and I on plant growth, seed yield, quality, and antioxidant and elemental status, as well as residual biomass chemical composition of chickpea grown in two different planting times (14 January and 28 February). The AMF application improved the intensity of I and Se accumulation both in single and joint supply of these elements, resulting in higher seed yield and number as well as dry weight, and was also beneficial for increasing the content of antioxidants, protein, and macro-and microelements. Earlier planting time resulted in higher values of seed yield, as well as Se, I, N, P, Ca, protein, and antioxidant levels. Se and I showed a synergistic effect, stimulating the accumulation of each other in chickpea seeds. The AMF inoculation elicited a higher protein and cellulose synthesis, as well as glucose production in the residual biomass, compared to the single iodine application and the untreated control. From the present research, it can be inferred that the plant biostimulation through the soil inoculation with AMF and the biofortification with Se and I, applied singly or jointly, proved to be effective sustainable farming tools for improving the chickpea seed yield and/or quality, as well as the residual biomass chemical composition for energy production or beneficial metabolite extraction.

Biostimulatory Action of Arbuscular Mycorrhizal Fungi Enhances Productivity, Functional and Sensory Quality in ‘Piennolo del Vesuvio’ Cherry Tomato Landraces

Article

Full-text available

Jun 2020

Arbuscular mycorrhizal fungi (AMF) are a promising tool to improve plant nutrient use efficiency (NUE) and tolerance against abiotic stresses. Moreover, AMF can potentially increase plant productivity and reduce the negative externalities of the agricultural sector. Our study aimed to elucidate whether AMF (containing Rhizoglomus irregulare and Funneliformis mosseae) could positively affect not only tomato growth and productivity but also the nutritional and nutraceutical quality of yellow-pigmented type (‘Giagiù’) and red-pigmented type (‘Lucariello’) tomatoes (Solanum lycopersicum L.). These cherry tomatoes are landraces of the Protected Designation of Origin (PDO) ‘Pomodorino del Piennolo del Vesuvio’ (PPV), one of the most typical agricultural products of the Campania region (Southern Italy). AMF rose fruit yield by increasing the number of fruits per plant (+49% and +29% in ‘Giagiù’ and ‘Lucariello’, respectively) but not of the fruit mean mass. AMF increased lycopene (+40%), total ascorbic acid (TAA; +41%), alanine (+162%), gamma-Aminobutyric acid (GABA; +101%) and branched-chain amino acids (BCAAs; +53%) in ‘Lucariello’. In ‘Giagiù’, AMF increased calcium (+63%), zinc (+45%), ASP (+70%), GABA (+53%) and the essential amino acids arginine (+58%) and lysine (+45%), also indicating a genotype-specific response. In both landraces, AMF improved nutrient uptake and biosynthesis of important molecules involved in the control the oxidative stress and cellular pH. In addition to the beneficial effects of human health, the molecules influenced by the AMF treatment are expected to extend the shelf life of tomato fruits, thus further promoting the useful agronomic application of AMF for premium tomatoes marketed fresh or in pendulums (‘piennoli’).

The Influence of Arbuscular Mycorrhizal Fungi on Plant Reproduction

Article

Full-text available

Aug 2020
J CHEM ECOL

Arbuscular mycorrhizal (AM) fungi can influence all components of plant reproduction including pollen delivery, pollen germination, pollen tube growth, fertilization, and seed germination. AM fungi associate with plant roots, uptake nutrients, and prime plants for faster defense responses. Our literature review first identified four testable hypotheses describing how AM fungi could alter pollen delivery: (1) We hypothesize AM fungi promote floral display size. The influence of AM fungi on flower size and number is supported by literature, however there are no studies on floral color. (2) We hypothesize AM fungi promote pollen and nectar quality and quantity, and, as reported before, AM fungi promote male fitness over female fitness. (3) We hypothesize AM fungi promote both earlier and longer flowering times, but we found no consistent trend in the data for earlier or later or longer flowering times. (4) We hypothesize AM fungi alter floral secondary chemistry and VOCs, and find there is clear evidence for the alteration of floral chemistry but little data on VOCs. Second, we focus on how AM fungi could alter pollen germination, pollen tube growth, and fertilization, and present three testable hypotheses. We found evidence that AM fungi influence pollen germination and pollen tube growth, production of seeds, and seed germination. However, while most of these influences are positive they are not conclusive, because studies have been conducted in small numbers of systems and groups. Therefore, we conclude that the majority of research to date may not be measuring the influence of AM fungi on the most important components of plant reproduction: pollen germination, pollen tube growth, fertilization, and seed germination.

The functional characterization of LjNRT2.4 indicates a novel, positive role of nitrate for an efficient nodule N2‐fixation activity

Article

Full-text available

Jul 2020
NEW PHYTOL

Atmospheric nitrogen (N2)‐fixing nodules are formed on the roots of legume plants as result of the symbiotic interaction with rhizobia. Nodule functioning requires high amounts of carbon and energy, and therefore legumes have developed finely tuned mechanisms to cope with changing external environmental conditions, including nutrient availability and flooding. The investigation of the role of nitrate as regulator of the symbiotic N2 fixation has been limited to the inhibitory effects exerted by high external concentrations on nodule formation, development and functioning. We describe a nitrate‐dependent route acting at low external concentrations that become crucial in hydroponic conditions to ensure an efficient nodule functionality. Combined genetic, biochemical and molecular studies are used to unravel the novel function of the LjNRT2.4 gene. Two independent null mutants are affected by the nitrate content of nodules, consistent with LjNRT2.4 temporal and spatial profiles of expression. The reduced nodular nitrate content is associated to a strong reduction of nitrogenase activity and a severe N‐starvation phenotype observed under hydroponic conditions. We also report the effects of the mutations on the nodular nitric oxide (NO) production and content. We discuss the involvement of LjNRT2.4 in a nitrate‐NO respiratory chain taking place in the N2‐fixing nodules.

Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review

Article

Sep 2020
J HAZARD MATER

Arbuscular mycorrhizal fungi (AM fungi) directly or indirectly alleviate heavy metal in host plant  AM fungi improve nutrient uptake, plant biomass and antioxidants under heavy metal stress in the host plant  AM fungi remediate heavy metal by accumulating large part of heavy metals in fungal structures Abstract The heavy metal pollution is a worldwide problem and has received a serious concern for the ecosystem and human health. In the last decade, remediation of the agricultural polluted soil has attracted great attention. Phytoremediation is one of the technologies that effectively alleviate heavy metal toxicity, however, this technique is limited to many factors contributing J o u r n a l P r e-p r o o f 3 to low plant growth rate and nature of metal toxicities. Arbuscular mycorrhizal fungi (AMF) assisted alleviation of heavy metal phytotoxicity is a cost-effective and environment-friendly strategy. AMF have a symbiotic relationship with the host plant. The bidirectional exchange of resources is a hallmark and also a functional necessity in mycorrhizal symbiosis. During the last few years, a significant progress in both physiological and molecular mechanisms regarding roles of AMF in the alleviation of heavy metals (HMs) toxicities in plants, acquisition of nutrients, and improving plant performance under toxic conditions of HMs has been well studied. This review summarized the current knowledge regarding AMF assisted remediation of heavy metals and some of the strategies used by mycorrhizal fungi to cope with stressful environments. Moreover, this review provides the information of both molecular and physiological responses of mycorrhizal plants as well as AMF to heavy metal stress which could be helpful for exploring new insight into the mechanisms of HMs remediation by utilizing AMF.

Inoculation with arbuscular mycorrhizal fungi improves melon ( Cucumis melo) fruit quality under field conditions and plant performance in both field and greenhouse

Article

Aug 2020

Previous works have suggested that arbuscular mycorrhizal (AM) fungi can enhance the quality of plant products and fruits. Therefore, the aim of the present study was to investigate the effects of AM fungi on Cucumis melo plant growth, yield, fitness and fruit quality. Inoculated and uninoculated plants of two melon cultivars (Baggio and Expò) were grown in field under common agronomic practices. In addition, a greenhouse test was run on cv. Expò in order to assess the effects of AM inoculation on shoot, leaf and flower development in semi-controlled conditions. In comparison to controls, AM plants flowered earlier, produced more flowers and their pulp contained more sugars and carotenoids. The symbiosis also improved seed size and weight, as well as their germination and root elongation in the first stages of growth in field. Concluding, AM inoculation significantly improved fruit quality in field, under commercial production conditions, also leading to the development of seeds with higher germination rate and increasing plant fitness.

Potential Role of Arbuscular Mycorrizhal Fungi (AMF) and Vermicompost (VC) on the Maturation of Agriculture Crops - A Review

Article

Aug 2020

Productivity and quality of horticultural crops through co-inoculation of arbuscular mycorrhizal fungi and plant growth promoting bacteria

Article

Jul 2020
MICROBIOL RES

Associations between plants and microorganisms exist in nature, and they can either be beneficial or detrimental to host plants. Promoting beneficial plant-microbe interaction for increased crop yield and quality is one pathway to eco-friendly and sustainable crop production. Arbuscular mycorrhizal fungi (AMF) and plant growth promoting bacteria (PGPB) are microorganisms that are beneficial to horticultural crops. Arbuscular mycorrhizal fungi establish symbioses with plant roots which help to improve nutrient uptake by the host plant and alter its physiology to withstand external abiotic factors and pathogens. Plant growth promoting bacteria promote plant growth either directly by aiding resource acquisition and controlling the levels of plant hormones or indirectly by reducing the inhibitory effects of phytopathogens. Co-inoculation of both organisms combines the benefits of each for increased crop productivity. Even though the co-inoculation of PGPB and AMF have been shown to enhance the yield and quality of crops, its benefits have fully not been exploited for horticultural crops. In this review, the response of horticultural crops to co-inoculation with PGPB and AMF with particular interest to the impact on the yield and crop quality was discussed. We explained some of the mechanisms responsible for the synergy between AMF and PGPB in plant growth promotion. Finally, suggestions on areas that need to be researched further to exploit and improve the effects of these organisms were highlighted.

Optical Sensing and Arbuscular Mycorrhizal Fungi for Improving Fertilizer Nitrogen and Phosphorus Use Efficiencies in Maize

Article

Jun 2020

Application of fertilizer nitrogen (N) and phosphorus (P) in excess of crop requirement causes nutritional imbalances in soil along with economic and ecological losses. The optical sensors (leaf color chart, chlorophyll meter, and GreenSeeker) help guide real-time N topdressing decisions and arbuscular mycorrhizal fungi (AMF) further improve nutrient uptake from soil. A four-year field study was conducted to improve N- and P-use efficiencies in maize using different optical sensing tools and coating seeds with AMF. The AMF seed coating improved mycorrhizal colonization in soil. Higher mycorrhization was observed in no-P treatment; however, P fertilization and mycorrhiza inoculation diminish the effect as growth progressed from 30 to 60 days after sowing. The mycorrhizal inoculation increased grain yield by 17.1% in no-N treatment; however, the response diminishes with N fertilization. The optical sensing–based N management sustained grain yield, total N uptake, and root and plant dry weight equivalent to the soil test–based fertilizer N recommendation with the less use of 30 kg N ha−1. The respective improvement in agronomic and recovery efficiencies of applied fertilizer N up to 38.6 and 34.9% highlights the potential of optical sensing tools and the inability of soil test–based N recommendation for precision N management. Mitigated greenhouse and nitrous oxide emissions respectively by 30.7% and 29.7% further underline the prominence of replacing soil test N recommendations with optical sensing–guided N top-dressings. Sufficient inherent soil P restricts the AMF benefits in improving P-use efficiencies in maize.

Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation

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