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ARBUSCULAR MYCORRHIZAL FUNGI – THEIR LIFE AND FUNCTION IN
ECOSYSTEM
MICHAELA PILIAROVÁ1, KATARÍNA ONDREIČKOVÁ2*, MARTINA HUDCOVICOVÁ2,
DANIEL MIHÁLIK1,2, JÁN KRAIC1,2
1University of Ss. Cyril and Methodius in Trnava, Slovakia
2National Agricultural and Food Centre ‒ Research Institute of Plant Production, Slovakia
PILIAROVÁ, M. – ONDREIČKOVÁ, K. – HUDCOVICOVÁ, M. – MIHÁLIK, D. – KRAIC, J.: Arbuscular
mycorrhizal fungi – their life and function in ecosystem. Agriculture (Polnohospodárstvo), vol. 65, 2019, no. 1,
pp. 3–15.
Mgr. Michaela Piliarová, PhD., Mgr. Daniel Mihálik, PhD., Prof. RNDr. Ján Kraic, PhD., Department of Biotechnology,
Faculty of Natural Sciences, University of Ss. Cyril and Methodius in Trnava, Nám. J. Herdu 2, 917 01 Trnava, Slovakia
Mgr. Katarína Ondreičková, PhD. (*Corresponding author), Mgr. Martina Hudcovicová, PhD., Mgr. Daniel Mihálik, PhD.,
Prof. RNDr. Ján Kraic, PhD., National Agricultural and Food Centre, Research Institute of Plant Production, Bratislavská
cesta 122, 921 68 Piešťany, Slovakia. E-mail: katarina.ondreickova@nppc.sk
Key words: arbuscular mycorrhizal fungi, mycorrhizosphere, plant, symbiosis
3
Arbuscular mycorrhizal fungi living in the soil closely collaborate with plants in their root zone and play very important
role in their evolution. Their symbiosis stimulates plant growth and resistance to different environmental stresses. Plant
root system, extended by mycelium of arbuscular mycorrhizal fungi, has better capability to reach the water and dissolved
nutrients from a much larger volume of soil. This could solve the problem of imminent depletion of phosphate stock, affect
plant fertilisation, and contribute to sustainable production of foods, feeds, biofuel, and raw materials. Expanded plant root
systems reduce erosion of soil, improve soil quality, and extend the diversity of soil microora. On the other hand, symbiosis
with plants affects species diversity of arbuscular mycorrhizal fungi and increased plant diversity supports diversity of fungi.
This review summarizes the importance of arbuscular mycorrhizal fungi in relation to benecial potential of their symbiosis
with plants, and their function in the ecosystem.
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
DOI: 10.2478/agri-2019-0001
Review
Arbuscular mycorrhizal fungi (AMF) are present
on the Earth about 600 million years (Redecker et al.
2000) and probably due to ancient symbiosis with
plants they lost the ability to exist independently and
its life cycle must be completed only in the presence
of the host plant (Requena et al. 2007). About 80%
of terrestrial plant species form the mycorrhizal
symbiosis with AMF (Wang & Qiu 2006) and the
arbuscular mycorrhizal symbiosis is the most wide-
spread type of mycorrhizal symbiosis without host
plant specicity (Klironomos 2000). On the other
hand, Husband et al. (2002) have indicated that at
least some fungi taxa are host specialists. The term
“arbuscular” was derived from characteristic struc-
tures called arbuscules (lat. arbuscula = small tree,
shrub) occurring in the cortical cells of many plant
roots. These structures, together with storage vesi-
cles, are considered diagnostic for arbuscular my-
corrhizal (AM) symbiosis and these fungi belong to
the phylum Glomeromycota (Table 1) (Schüßler et
al. 2001). AMF are obligate symbionts dependent
on the host plant and colonization of plant roots oc-
curred through spores, hyphae, or infected root frag-
ments (Klironomos & Hart 2002). Fungal mycelium
of AMF affects the plant by extending of root sys-
tems, allowing to improve the utilization of water
and minerals from the soil (Smith & Read 1997).
Plants colonized by AMF have better resistance to
© 2019 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License
(http://creativecommons.org/licenses/by-nc-nd/3.0/).
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Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
environmental stresses, such as drought, cold, pollu-
tion (Juniper & Abbott 2006), and better overcome
attacks of bacterial and fungal pathogens (Selvaraj
& Chellappan 2006). Mycorrhizal symbiosis main-
tains and promotes plant growth, signicantly re-
duces the need for synthetic fertilisers, improves
quality of soil, increases soil microoral diversity,
and reduces soil erosion (Azaizeh et al. 1995).
Arbuscular mycorrhizal symbiosis
The arbuscular mycorrhizal symbiosis is a com-
plex of morphological, physiological, and biochem-
ical changes which are formed gradually in several
developmental stages in both symbiotic partners.
The life cycle of AMF starts with germination of
fungal spores in the soil under favourable environ-
mental conditions, spontaneously without the pres-
ence of the host plant (Gianinazzi-Pearson 1996;
Requena et al. 2007). Fungal colonies expand sev-
eral centimetres and characteristic growth structures
are formed (Giovannetti et al. 1994). This asymbi-
otic phase turns into presymbiotic one characterised
by extensive hyphal branching caused by presence
of the host plant (Giovannetti et al. 1993). This is
crucial stage in the AMF life cycle based on the
chemotaxic abilities of AMF that allow the growth
of the hyphae to the roots of host plant and repre-
T a b l e 1
Classication of arbuscular mycorrhizal fungi according to Schüßler & Walker (2010) and Redecker et al. (2013)
Phylum Class
Glomeromycota Glomeromycetes
Orders Families Genera
Glomerales Glomeraceae
Glomus
Funneliformis (former Glomus Group Aa, Glomus mosseae)
Rhizophagus (former Glomus Group Ab, Glomus intraradices)
Sclerocystis (based in former Glomus Group Aa)
Septoglomus
Claroideoglomeraceae Clairoideoglomus (former Glomus Group B, Glomus claroideum)
Diversisporales
Gigasporaceae
Cetraspora
Dentiscutata
Gigaspora
Intraomatospora (insufcient evidence, but no formal action was taken)
Paradentiscutata (insufcient evidence, but no formal action was taken)
Racocetra
Scutellospora
Acaulosporaceae Acaulospora (including the former Kuklospora)
Pacisporaceae Pacispora
Diversisporaceae
Corymbiglomus (insufcient evidence, but no formal action was taken)
Diversispora (former Glomus Group C)
Otospora (insufcient evidence, but no formal action was taken)
Redeckera
Tricispora (insufcient evidence, but no formal action was taken)
Sacculosporaceae Sacculospora (insufcient evidence, but no formal action was taken)
Paraglomerales Paraglomeraceae Paraglomus
Archaeosporales
Geosiphonaceae Geosiphon
Ambisporaceae Ambispora
Archaeosporaceae Archaeospora (including the former Intraspora)
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Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
sent a signicant mechanism functional to host root
location, appressorium formation and symbiosis
establishment (Sbrana & Giovannetti 2005). The
symbiosis phase begins by fungal hyphae connec-
tion with the plant roots through appressorium and
fungi penetrate into the cortex (Giovannetti et al.
1993) to form morphologically distinct specialized
structures – inter- and intracellular hyphae, vesicles,
and arbuscules (Figure 1). The arbuscules represent
the place of active bi-directional transfer of nutri-
ents between plant and fungus (Requena et al. 2007)
and play a major role in arbuscular mycorhizal sym-
biosis. The hyphae penetrate outside of the roots,
into the soil, create extra-radical mycelium, and
complete life cycle by the formation of new asex-
ual spores in extra-radical mycelium (Requena &
Breuninger 2004). Under this symbiosis, the AMF
stimulate growth and reproduction of plants through
better access to nutrients (P and N) and increased
absorption of water from the soil by the extra-rad-
ical and intra-radical mycelium (Bago et al. 2001).
Conversely, the plant provides carbon in the form of
saccharides produced by photosynthesis (Pfeffer et
al. 1999) transferred to the fungi via active or pas-
sive mechanisms (Doidy et al. 2012) by intra-radi-
cal fungal structures. Once AM fungi colonize the
plants, they persist with the root systems and can be
moved into other soil (Mishra et al. 2018).
Rhizosphere affected by mycorrhizas described
by the term ,,mycorrhizosphere” has unique char-
acteristics (Li et al. 1991). Mycorrhizal fungi take
over the role of root hairs and expand root system
of plants leading to increasing of the plant absorp-
tion area, improved absorption capacity of roots,
and better utilization of hardly available nutrients.
The mycorrhizosphere consists of roots, hyphae of
the AMF, associated microorganisms, and the soil
around them (Figure 2) (Mohammadi et al. 2011).
Mycorrhiza also inuences the colonization of roots
by other microorganisms; increases resistance of
roots to soil pathogens (Pozo et al. 2002); affects the
relationship between soil, plant, and water; promotes
adaptation of plants to adverse conditions such as
drought and soil salinity (Giri et al. 2003); and has
an important role in maintaining the overall soil sta-
bility (Azaizeh et al. 1995). AMF also detoxify the
plant environment containing higher concentration
of heavy metals (Hildebrandt et al. 1999) and induce
the production of several phytohormones. Danne-
berg et al. (1993) observed in the roots and shoots
of plants colonized by AMF increased amounts of
several substances, such as abscisic acid, auxins,
gibberellins, and substances similar to cytokinins.
Simultaneously, in the plant tissues an increased ac-
Figure 1. Typical intracellular structures (A – arbuscules and V – vesicle) of arbuscular mycorrhiza produced by Glomus
species (left). A mature arbuscule (right up) and vesicles (right down) of Glomus (Brundrett 2008, photos © Mark Brundrett
with permission)
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Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
tivity of some enzymes (peroxidases, phosphatases,
alkaline phosphatases), enhanced photosynthesis
activity, concentration of chlorophyll, and increased
levels of reducing saccharides, lipids, fatty acids,
amino acids, and proteins were observed (Selvaraj
& Chellappan 2006).
Mineral nutrition
The extensive AMF mycelium obtains from
soil nutrients such as phosphorus, nitrogen, zinc,
copper, iron, potassium, calcium, magnesium, and
others (Clark & Zeto 2000). In some cases, the nu-
trients can control the development or start the sym-
biosis (Ryan & Angus 2003). AMF can also cause
a change in absorption of more nutrients at the same
time but the effect on individual nutrients may be
different. Sometimes, there may be increased and in
other cases decreased intake of individual nutrients
(Azaizeh et al. 1995; Mohammad et al. 2003).
Phosphorus. Phosphorus is one of the key bio-
genic macroelements necessary for growth and me-
tabolism of plants (Zou et al. 1992). Phosphorus
has an important role in the transfer of energy by
the establishment of energy-rich esters of phospho-
ric acid, and is a basic element of macromolecules,
such as nucleotides, nucleic acids, and phospho-
lipids (Marschner 1995). A large part of inorganic
phosphate applied to the soil as fertilisers is rapidly
converted to the unavailable form of low solubili-
ty. The soluble phosphate is then released from the
insoluble form by various reactions involving the
participation of other rhizosphere microorganisms
(Khan et al. 2007). The phosphate ions are extreme-
ly immobile in the soil due to the formation of in-
soluble complexes with the prevailing soil cations,
such as Fe3+, Al3+, and Ca2+. Consequently, the phos-
phate ions diffuse in soil very slowly but in the sur-
rounding soil occupied by the roots (depletion zone)
phosphate is exhausted very quickly. Then the rate
of uptake is not dened by plant physiology but by
slow diffusion of phosphate ions in the soil (Hel-
gason & Fitter 2005). The presence of phosphate
in the rhizosphere, respectively in the mycorrhizo-
sphere, is the major factor contributing to the cre-
ation of mycorrhiza association. AMF increase in-
take of relatively immobile phosphate ions for their
host plant due to the ability of fungal extra-radical
growth (George et al. 1995). The depletion zone is
around the host plant root, where plant roots are able
to pump the necessary nutrients. AMF extra-radical
mycelium grows beyond the depletion zone and ac-
quires phosphate unavailable directly for the plant
(Smith et al. 2003). Phosphate is then transported in
Figure 2. The area of soil occupied by plant roots only (rhizosphere, left) and by plant roots colonized by mycorrhizal fungi
(mycorrhizosphere, right) (Mohammadi et al. 2011)
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Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
the form of polyphosphates from soil through AMF
into intra-radical mycelium (Bucher 2007), already
present in the roots of the host plant (Figure 3). The
phosphate intake into plants is via plant phosphate
transporters, which are produced during the de-
velopment of AM symbiosis (Pumplin & Harrison
2009). Due to the fact that plant obtains most of the
phosphorus through fungal symbiosis, it is possi-
ble to assume that the plant phosphate transporters,
which partially regulate the phosphate intake, have
a great importance to productivity and plant growth
in most ecosystems (Smith et al. 2003). Increased
absorption of phosphorus is generally considered as
the most important contribution that AMF provided
for the host plant. Simultaneously, the phosphorus
level in the plants is often a major factor in regulat-
ing the relationship between plants and AMF. How-
ever, there are plants that do not respond to coloni-
zation of AMF due to high concentration of phos-
phorus in the soil and the colonization of plants by
AMF is suppressed (Kahiluoto et al. 2001). Cheng
et al. (2013) in their study conrmed that higher
content of phosphorus in the soil is associated with
lower mycorrhizal root colonization rates and lower
AMF diversity.
Nitrogen. AMF can efciently mediate transfer
large amounts of nitrogen from the soil into the roots
of host plants (Jackson et al. 2008). AMF extra-rad-
ical hyphae receive from the soil great amounts of
nitrogen in the form of ammonium cations (NH4+),
nitrates (NO3-) or amino acids and subsequently
transfer to the plants (Johansen et al. 1992; Bago
et al. 1996; Hawkins et al. 2000). Inorganic nitro-
gen is transmitted from the extra-radical mycelium
to the fungal intra-radical structures in the form of
amino acids which are transported to the plant in the
form of the ammonium cations (Govindarajulu et al.
2005). AM symbiosis is involved in the process of
mineralization of nitrogen in the soil, controls the
recycling of plant residues in the production of bio-
mass, and affects the structure of soil microorgan-
isms (Atul-Nayyar et al. 2008; Leigh et al. 2009).
AMF and abiotic factors of environment
The abiotic factors affecting the composition and
effectiveness of AMF community in soil are: pH, or-
Figure 3. The scheme of phosphate direct uptake from a depletion zone through the root hair cells directly into the root and
also using AMF transporters located in the extra-radical hyphae. Phosphate is transferred via the hyphae to the roots, where
cortical cells are involved in the absorption of phosphate (Smith et al. 2010)
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Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
ganic matter, phosphorus availability, heavy metals,
agricultural practice, and others. Changes in these
factors can lead to differences in symbiotic efcien-
cy and demonstrate the functional diversity among
the different AMF. Mycorrhizal symbiosis can im-
prove the physiological effectiveness of plants ex-
posed to stress.
Soil salinity. AMF presented in the environment
with increased soil salinity inuence on the forma-
tion and function of mycorrhizal symbiosis (Kumar
et al. 2010). The increased soil salinity negatively
affects the plant growth through reducing nutri-
ents uptake and increasing osmotic stress of plants
(Abdel-Ghani 2009). Some studies suggest that
AM fungi increase the plant’s ability to cope with
increased salinity (Yano-Melo et al. 2003; Rabie &
Almadini 2005; Al-Karaki 2006; Cho et al. 2006;
Sannazzaro et al. 2006). This can be achieved by
increasing the intake of nutrients such as P, N, Zn,
Cu, and Fe (Cantrell & Linderman 2001; Asghari et
al. 2005; Al-Karaki 2006), inhibiting high uptake of
Na and Cl and their transport to plant shoots (Daei
et al. 2009), improving water uptake (Ruiz-Lozano
& Azcon 2000), accumulating of proline and poly-
amines (Evelin et al. 2009; Ibrahim et al. 2011), or
increasing any of enzymatic antioxidant defence
system (Wu et al. 2010). Other arbuscular mycor-
rhizal mechanisms can include osmotic adaptation
assisted in maintaining the leaf turgor pressure, in-
uence the photosynthesis, transpiration, stomatal
conductance, and water use efciency (Juniper &
Abbott 1993).
Plant-water relationship. AMF have an impact
on the plant-water relationship, thereby increasing
the host plant resistance to drought. Plants colonized
by AMF are able to absorb more water from the soil
in comparison with not colonized plants (Khalva-
ti et al. 2005) and the amount of received water is
dependent on the fungal species (Marulanda et al.
2003). Furthermore, AMF affect the efcient use
of water and root conductivity (Auge 2001). An in-
creased tolerance to water stress relates to the fact
that endophytes have an impact on the increased
conductivity of the leaves, transpiration, and in-
take of phosphorus and potassium. Potassium plays
a key role in plants exposed to water stress when the
free cations are responsible for the activity of leaf
stomata. The specic physiological (CO2 xation,
transpiration, water use efciency) and nutritional
(P and K) mechanisms of the AMF are involved in
the symbiosis to contribute to the alleviation of the
drought stress (Ruiz-Lozano et al. 1995).
Climatic changes. The most commonly consid-
ered global and regional climatic changes affecting
mycorrhiza are elevated atmospheric CO2, increased
tropospheric ozone, ultraviolet radiation, tempera-
ture, and drought (Mohan et al. 2014). However, it
is not just one factor that has implications on the
AM association but the inuence of several factors
must be taken into account. For example, AM colo-
nization of grass roots decreased with warming and
in combination with elevated CO2 decreased even
more (Olsrud et al. 2010). Treseder (2004) con-
rmed that increased atmospheric CO2 contributes
to improved activity of mycorrhizal associations
and has a benecial effect on the mycorrhizal abun-
dance. Other studies have shown that increased at-
mospheric CO2 can affects differently on AMF and it
is important to consider what plant species create an
association with AMF. Garcia et al. (2008) founded
that the increased atmospheric CO2 not affected the
length of hyphae and root colonization in a desert
environment. Similarly, in a warm temperate forest
the increased CO2 have no effect on AMF (Garcia et
al. 2008). On the other hand, in the chaparral eco-
system the amount of AM hyphae and the gloma-
lin protein increased with increasing of CO2 (Allen
et al. 2005) and also in a sandstone grassland the
length of the AM hyphae and root colonization were
increased (Rillig et al. 1999). Most studies exam-
ined the combined effect of temperature on the AMF
and host plant. Generally, internal colonization in-
creases with temperature between 10°C and 30°C
(Wang et al. 2002) but temperature below 15°C may
decrease the colonization (Zhang et al. 1995). At
temperatures above 15°C the AMF provide to the
plants increased amount of phosphorus in compar-
ison with the non-mycorrhizal plants (Wang et al.
2002; Karasawa et al. 2012).
Heavy metals. Nowadays, soil contamination
with heavy metal is a global problem caused main-
ly by anthropogenic activities such as mining, ag-
riculture, smelting, electroplating, and other human
activities (Gomez-Sagasti et al. 2012). Heavy met-
als are heavily degraded in the soil, accumulate in
the soil, and affect the microbial biomass, activity,
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
and diversity (Alguacil et al. 2011; Margesin et al.
2011). Community of AMF is sensitive to the pres-
ence of metals in the soil. The long term application
of sludge with increased amount of heavy metals in
the soil can signicantly reduce the total number of
spores and diversity of AMF (Del Val et al. 1999).
However, symbiosis of AMF with plants could be
a potential biological solution to increase plant re-
sistance to heavy metals and to improve fertility of
contaminated soil (Vivas et al. 2005). The immo-
bilization of metals through the fungal biomass is
one of the possible mechanisms. The benecial use
of AM fungi is through improved nutrient acquisi-
tion and increased growth by arresting metal uptake
in different mycorrhizal structures (Kaur & Garg
2017). Also, plant roots colonized by AMF can form
and strengthen a root barrier against the transfer of
heavy metal and reduce their transmission (Andrade
& Silveira 2008). This effect is ascribed to the ab-
sorption of metal by chitin in the cell walls of the
hyphae, which has a signicant ability to bind met-
als (Joner et al. 2000). Glomalin, a glycoprotein pro-
duced abundantly on hyphae and spores of AMF in
soil and in roots, has also a chelating effect, thereby
decreases the availability of metals to plants (Gon-
zalez-Chávez et al. 2004). Another possible mecha-
nisms are the dilution of concentrations of metals in
plant tissues as a result of plant growth promoting
by AMF (Andrade & Silveira 2008) and increased
exclusion of metals by precipitation or chelation in
the rhizosphere (Kaldorf et al. 1999).
Soil pH. The soil pH is an important factor af-
fecting the AMF community in the soil. The differ-
ent AMF have various claims and sensitivity to the
pH (Hayman & Tavares 1985). Soil acidity affects
the number of AMF spores in the soil (Mohammad
et al. 2003) and species composition (Porter et al.
1987; Sharma et al. 2009). Changes of soil pH may
affect the availability of nutrients for the plant, e.g.
inorganic P is more easily available in the soil with
pH ≈ 6.5. Lower pH decreases the solubility of Fe
and in high pH solubility of Ca phosphates decreas-
es (Marschner 1995).
AMF and biotic factors of environment
Plants. There were found 5–30 AMF species
at a given locality (Douds & Millner 1999) and 8
various AMF species were found colonizing a sin-
gle 5 centimetres root segment in eld experiments
(Tommerup 1988). Increasing of plant diversity
could increase the AMF species diversity and also
affects the production of spores. Some plant species
may support individual AMF species, which may
lead to increasing in species richness. Moreover,
root exudates of different plant species can affect
the germination and growth of AMF species (Douds
et al. 1996). It appears that AMF have benet from
increased plant diversity due to number of possible
host-fungal pairings and elevated density of plant
roots available for colonization, AMF growth and
sporulation (Burrows & Peger 2002). De León
et al. (2018) observed that roots of soybean plants
were colonized by diverse communities of AM fun-
gi and composition of AMF community in roots was
primarily driven by host plant identity.
Plant pathogens. Plants in their natural environ-
ment interact with a large number of harmful her-
bivorous insects and pathogenic microorganisms.
AMF directly do not ensure the protection of plants
against phytopathogens, but they induce the ability
of plants to respond more quickly to the pathogen
attack (Whipps 2004). In some cases, the apparent
plant resistance to pathogens and diseases may be
the result of improved nutrition (Karagiannidis et al.
2002). Probably one of the most important cases is
the elimination of pathogens from the area where the
colonization of root cells by AMF occurs. The ad-
vantage is when the AMF colonize the plant before
pathogen (Slezack et al. 1999). Another factor may
be related with changes in the root exudates compo-
sition (Filion et al. 1999), which can cause changes
in the rhizosphere microbial community structures
(Hassan Dar et al. 1997). Also changes in the root
structure of host plant or biochemical changes as-
sociated with protective mechanisms of plant may
cause the putative plant resistance to pathogens
(Gianinazzi-Pearson 1996; Vigo et al. 2000).
Other soil microorganisms. Bacterial communi-
ties and individual species support the germination
of AMF spores and may increase the rate and extent
of fungal colonization of plant roots (Johansson et al.
2004). Once the arbuscular symbiosis is developed,
AMF hyphae affect the surrounding soil leading to
the development of different microbial communities
(Linderman 1988). AMF communicate with bene-
cial rhizosphere microorganisms in the mycorrhizo-
9
sphere, including bacteria involved in the nitrogen
xation and rhizobacteria (Biró et al. 2000). In the
concept called mycorrhiza helper bacteria (MHB)
the bacteria directly assist in the formation of my-
corrhiza and positively affect symbiosis. MHB
mechanisms stimulate spore germination, growth
of AMF mycelium, improve the soil conditions and
chemistry via alteration of phytohormones level
(Frey-Klett et al. 2007). AMF and Pseudomonas u-
orescens (rhizosphere bacteria) have gained consid-
erable attention among soil microorganisms due to
their positive effect on plant growth (Smith & Smith
2011). Gamalero et al. (2004) studied the effect of
the interaction between the AMF and P. uorescens
on root morphology and the resulted effect was syn-
ergistic or neutral, respectively. Similar study was
carried by Cosme & Wurst (2013). Their results in-
dicated that the positive interactions between AMF
and P. uorescens on the root morphology were de-
pended on the nutrient status in the rhizosphere and
the root hormonal balance. Their result also indicate
that the P. uorescens belongs to MHB, even if it
is not isolated from the rhizosphere of mycorrhizal
plant (Glenn et al. 1985). This means, that the MHB
mechanisms are independent of the rhizobacteria or-
igin (Frey-Klett et al. 2007).
AMF and agriculture
Fertilising, plowing, biocides, and other agricul-
tural practices may have a negative impact on the
AMF community (Jansa et al. 2002) and soils can be
depleted about the AMF diversity (Helgason et al.
1998). Changes in the composition of the AMF can
be caused by various factors, such as the disruption
of AMF hyphal networks, changes in the soil nutri-
ent content, and in the microbial activity (Jansa et al.
2003). Application of fertilisers containing phospho-
rus may leads to less dependence of plants in AMF
colonization, reduced colonization of roots by AMF,
or less spore density of AMF in soils (Kahiluoto
et al. 2001). Also, fertilisers with a high content of
nitrogen may have negative effects on the coloniza-
tion and diversity of AMF (Egerton-Warburton et al.
2007). The soil tillage may signicantly disrupt the
mycorrhizal network, delay or reduce root coloniza-
tion and the soil volume usable for AMF. Simulta-
neously, it may reduce intake of necessary nutrients
by plants, plant growth and production (Evans &
Miller 1990). In some cases, the effects on growth
and nutrient intake are temporary and the effect of
tillage on the AMF community also may depends on
the soil type (Kabir 2005). Säle et al. (2015) demon-
strated that AMF communities were affected by
land use, farming and tillage system, and fertilisa-
tion. Other studies showed that community structure
and diversity of AMF in soils differs between tilled,
reduced, and no-tilled soils (Jansa et al. 2002; Köhl
et al. 2014; Maurer et al. 2014; Wetzel et al. 2014).
Some fungicides signicantly inhibited the abil-
ity of AMF to colonize plants, phosphorus uptake
(Schweiger & Jakobsen 1998), and affect sporula-
tion. Indirect effect of herbicides is due to elimina-
tion of weeds, the potential hosts of AMF (Ryan et
al. 1994). Some biocides may have a negative, neu-
tral (herbicides) or positive (nematicides) effect on
the AMF community (Pattinson et al. 1997).
CONCLUSIONS
Arbuscular mycorrhizal fungi are microorgan-
isms with very important and valuable functions
in growing systems of agricultural crops. Mycelia
of arbuscular mycorrhizal fungi assist in uptake
of nutrients from soil to the plants, such as phos-
phorus, nitrogen, zinc, copper, and other elements.
Mycorrhizal symbiosis can improve the physiolog-
ical response of plants to abiotic and biotic stresses,
increase biomass yield, and retain productivity of
plants. Also, they are useful in decreasing of pol-
lutants in the biosphere, including heavy metals,
organic compounds, and radionuclides. However,
conventional agricultural practices such as fertilis-
ing, tillage, and application of chemical pesticides
acting as biocides, may have a negative impact on
their communities. This can results to depletion of
arbuscular mycorrhizal fungi from agricultural soils,
especially from the genetic diversity point of view,
followed by reduction of intake of necessary nutri-
ents by plants and decreasing of plant growth and
crop productivity. However, the potential of AMF
have to be exploited for the sustainability of agricul-
tural production. Utilization of mycorrhizal symbio-
sis can reduce external inputs into agriculture, while
the crop productivity can remains or may be even
higher. Ecological impacts of particular importance
10
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
are associated with the bellow-ground ecosystem
affected also by AMF and AMF-plant interactions.
To meet the challenge of exploitation of arbuscular
mycorrhizal symbiosis in agricultural practice can
contribute studies of qualitative and quantitative
analysis of AMF diversity in soil.
Acknowledgements. This work was supported
by the Slovak Research and Development Agency
under the contract No. APVV-17-0150 and by the
Operational Programme Research and Development
co-nanced from the European Regional Develop-
ment Fund under the project ITMS 26210120039
“Systems biology for protection, reproduction and
use of plant resources of Slovakia”.
REFERENCES
ABDEL-GHANI, A.H. 2009. Response of wheat varieties from
semi-arid regions of Jordan to salt stress. In Journal of
Agronomy and Crop Science, vol. 195, no. 1, pp. 55–65.
DOI: 10.1111/j.1439-037X.2008.00319.x
ALGUACIL, M.M. – TORRECILLAS, E. – CARAVACA, F. –
FERNÁNDEZ, D.A. – AZCÓN, R. – ROLDÁN, A. 2011.
The application of an organic amendment modies the ar-
buscular mycorrhizal fungal communities colonizing native
seedlings grown in a heavy metal-polluted soil. In Soil Biol-
ogy and Biochemistry, vol. 43, no. 7, pp. 1498–1508. DOI:
10.1016/j.soilbio.2011.03.026
AL-KARAKI, G.N. 2006. Nursery inoculation of tomato with
arbuscular mycorrhizal fungi and subsequent performance
under irrigation with saline water. In Scientia Horticulturae,
vol. 109, no. 1, pp. 1–7. DOI: 10.1016/j.scienta.2006.02.019
ALLEN, M.F. – KLIRONOMOS, J.N. – TRESEDER, K.K.
– OECHEL, W.C. 2005. Responses of soil biota to ele-
vated CO2 in a chaparral ecosystem. In Ecological Appli-
cations, vol. 15, no. 5, pp. 1701–1711. DOI: 10.1890/03-
5425
ATUL-NAYYAR, A. – HAMEL, C. – HANSON, K. – GERMI-
DA, J. 2008. The arbuscular mycorrhizal symbiosis links N
mineralization to plant demand. In Mycorrhiza, vol. 19, no.
4, pp. 239–246. DOI: 10.1007/s00572-008-0215-0
ANDRADE, S.A.L. – SILVEIRA, A.P.D. 2008. Mycorrhiza in-
uence on maize development under Cd stress and P supply.
In Brazilian Journal of Plant Physiology, vol. 20, no. 1, pp.
39–50. DOI: 10.1590/S1677-04202008000100005
ASGHARI, H. – MARSCHNER, P. – SMITH, S. – SMITH, F.
2005. Growth response of Atrilpex nummularia to inocula-
tion with arbuscular mycorrhizal fungi at different salinity
levels. In Plant and Soil, vol. 273, no. 1–2, pp. 245–256.
DOI: 10.1007/s11104-004-7942-6
AUGE, R.M. 2001. Water relations, drought and vesicular–ar-
buscular mycorrhizal symbiosis. In Mycorrhiza, vol. 11, no.
1, pp. 3–42. DOI: 10.1007/s005720100097
AZAIZEH, H.A. – MARSCHNER, H. – RÖMHELD, V. –
WITTENMAYER, L. 1995. Effects of a vesicular-arbuscu-
lar mycorrhizal fungus and other soil microorganisms on
growth, mineral nutrient acquisition and root exudation of
soilgrown maize plants. In Mycorrhiza, vol. 5, no. 5, pp.
321–327. DOI: 10.1007/BF00207404
BAGO, B. – PFEFFER, P.E. – SHACHAR-HILL, Y. 2001.
Could the urea cycle be translocating nitrogen in arbuscular
mycorrhizal fungi? In New Phytologist, vol. 149, no. 1, pp.
4–8. DOI: 10.1046/j.1469-8137.2001.00016.x
BAGO, B. – VIERHEILIG, H. – PICHÉ, Y. – AZCÓN-
AGUILAR, C. 1996. Nitrate depletion and pH changes by
the extraradical mycelium of the arbuscular mycorrhizal
fungus Glomus mosseae grown in monoxenic culture. In
The New Phytologist, vol. 133, no. 2, pp. 273–280. DOI:
10.1111/j.1469-8137.1996.tb01894.x
BIRÓ, B. – KÖVES-PÉCHY, K. – VÖRÖS, I. – TAKÁCS, T.
– EGGENBERGER, P. – STRASSER, R.J. 2000. Interre-
lations between Azospirillum and Rhizobium nitrogenxers
and arbuscular mycorrhizal fungi in the rhizosphere of alfal-
fa at sterile, AMF-free or normal soil conditions. In Applied
Soil Ecology, vol. 15, no. 2, pp. 159–168. DOI: 10.1016/
S0929-1393(00)00092-5
BRUNDRETT, M.C. 2008. Ectomycorrhizas. In Mycorrhizal
Associations: The Web Resource. Version 2.0. 6 Feb 2019.
‹https://mycorrhizas.info›.
BUCHER, M. 2007. Functional biology of plant phosphate
uptake at root and mycorhiza interfaces. In New Phytol-
ogist, vol. 173, no. 1, pp. 11–26. DOI: 10.1111/j.1469-
8137.2006.01935.x
BURROWS, R.L. – PFLEGER, F.L. 2002. Arbuscular mycor-
rhizal fungi respond to increasing plant diversity. In Cana-
dian Journal of Botany, vol. 80, no. 2, pp.120–130. DOI:
10.1139/b01-138
CANTRELL, I.C. – LINDERMANN, R.G. 2001. Preinocula-
tion of lettuce and onion with VA mycorrhizal fungi reduces
deleterious effects of soil salinity. In Plant and Soil, vol.
233, no. 2, pp. 269–281. DOI: 10.1023/A:101056401
CHENG, Y. – ISHIMOTO, K. – KURIYAMA, Y. – OSAKI,
M. – EZAWA, T. 2013. Ninety-year-, but not single, appli-
cation of phosphorus fertilser has a major impact on arbus-
cular mycorrhizal fungal communities. In Plant and Soil,
vol. 365, no. 1–2, pp. 397–407. DOI: 10.1007/s11104-012-
1398-x
CHO, K. – TOLER, H. – LEE, J. – OWNLEY, B. – STUTZ, J.C.
– MOORE, J.L. – AUGÉ, R.M. 2006. Mycorrhizal symbi-
osis and response of sorghum plants to combined drought
and salinity stresses. In Journal of Plant Physiology, vol.
163, no. 5, pp. 517–528. DOI: 10.1016/j.jplph.2005.05.003
CLARK, R.B. – ZETO, S.K. 2000. Mineral acquisition by arbus-
cular mycorrhizal plants. In Journal of Plant Nutrition, vol.
23, no. 7, pp. 867–902. DOI: 10.1080/01904160009382068
COSME, M. – WURST, S. 2013. Interactions between arbus-
cular mycorrhizal fungi, rhizobacteria, soil phosphorus and
plant cytokinin deciency change the root morphology, yield
and quality of tobacco. In Soil Biology and Biochemistry,
vol. 57, pp. 436–443. DOI: 10.1016/j.soilbio.2012.09.024
DAEI, G. – ARDEKANI, M.R. – REJALI, F. – TEIMURI, S.
– MIRANSARI, M. 2009. Alleviation of salinity stress on
wheat yield, yield components, and nutrient uptake using
arbuscular mycorrhizal fungi under eld conditions. In
Journal of Plant Physiology, vol. 166, no. 6, pp. 617–625.
DOI: 10.1016/j.jplph.2008.09.013
DANNEBERG, G. – LATUS, C. – ZIMMER, W. – HUNDE-
SHAGEN, B. – SCHNEIDER-POETSCH, H.J. – BOTHE,
H. 1993. Inuence of vesicular arbuscular mycorrhiza on
phytohormone balances in maize (Zea mays L.). In Jour-
nal of Plant Physiology, vol. 141, no. 1, pp. 33–39. DOI:
10.1016/S0176-1617(11)80848-5
DE LEÓN, D.G. – CANTERO, J.J. – MOORA, M. – ÖPIK,
M. – DAVISON, J. – VASAR, M. – JAIRUS, T. – ZOBEL,
M. 2018. Soybean cultivation supports a diverse arbuscu-
11
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
lar mycorrhizal fungal community in central Argentina. In
Applied Soil Ecology, vol. 124, pp. 289–297. DOI:
10.1016/j.apsoil.2017.11.020
HASSAN DAR, G.H. – ZARGAR, M.Y. – BEIGH, G.M.
1997. Biocontrol of Fusarium root rot in the common bean
(Phaseolus vulgaris L.) by using symbiotic Glomus mosse-
ae and Rhizobium leguminosarum. In Microbial Ecology,
vol. 34, no. 1, pp. 74–80. DOI: 10.1007/s002489900036
DEL VAL, C. – BAREA, J.M. – AZCÓN-AGUILAR, C. 1999.
Diversity of arbuscular mycorrhizal fungus populations in
heavy-metal-contaminated soils. In Applied and Environ-
mental Microbiology, vol. 65, no. 2, pp. 718–723.
DOIDY, J. – GRACE, E. – KÜHN, C. – SIMON-PLAS, F.
– CASIERI, L. – WIPF, D. 2012. Sugar transporters in
plants and in their interactions with fungi. In Trends in
Plant Science, vol. 17, no. 7, pp. 413–422. DOI: 10.1016/j.
tplants.2012.03.009
DOUDS, D.D. – MILLNER, P.D. 1999. Biodiversity of arbus-
cular mycorrhizal fungi in agroecosystems. In Agriculture,
Ecosystems and Environment, vol. 74, no. 1–3, pp. 77–93.
DOI: 10.1016/S0167-8809(99)00031-6
DOUDS, D.D. – NAGAHASHI, G. – ABNEY, G.D. 1996. The
differential effects of cell wall-associated phenolics, cell
walls, and cytosolic phenolics of host and non-host roots
on the growth of two species of AM fungi. In The New Phy-
tologist, vol. 133, no. 2, pp. 289–294. DOI: 10.1111/j.1469-
8137.1996.tb01896.x.
EGERTON-WARBURTON, L.M. – JOHNSON, N.C. – AL-
LEN, E.B. 2007. Mycorrhizal community dynamics follow-
ing nitrogen fertilization: a cross-site test in ve grasslands.
In Ecological Monographs, vol. 77, no. 4, pp. 527–544.
DOI: 10.1890/06-1772.1
EVANS, D.G. – MILLER, M.H. 1990. The role of the exter-
nal mycelial network in the effect of soil disturbance upon
vesicular-arbuscular mycorrhizal colonisation of maize.
In The New Phytologist, vol. 11 4, no. 1, pp. 65–71. DOI:
10.1111/j.1469-8137.1990.tb00374.x
EVELIN, H. – KAPOOR, R. – GIRI, B. 2009. Arbuscular
mycorrhizal fungi in alleviation of salt stress: a review. In
Annals of Botany, vol. 104, no. 7, pp. 1263–1280. DOI:
10.1093/aob/mcp251
FILION, M. – ST-ARNAUD, M. – FORTIN, J.A. 1999. Direct
interaction between the arbuscular mycorrhizal fungus Glo-
mus intraradices and different rhizoshpere microorganisms.
In The New Phytologist, vol. 141, no. 3, pp. 525–533. DOI:
10.1046/j.1469-8137.1999.00366.x
GAMALERO, E. – TROTTA, A. – MASSA, N. – COPETTA,
A. – MARTINOTTI, M.G. – BERTA, G. 2004. Impact of
two uorescent pseudomonads and an arbuscular mycor-
rhizal fungus on tomato plant growth, root architecture and
P acquisition. In Mycorrhiza, vol. 14, no. 3, pp. 185–192.
DOI: 10.1007/s00572-003-0256-3
GARCIA, M.O. – OVASAPYAN, T. – GREAS, M. – TRESEDER,
K.K. 2008. Mycorrhizal dynamics under elevated CO2 and
nitrogen fertilization in a warm temperate forest. In Plant
and Soil, vol. 303, no. 1–2, pp. 301–310. DOI: 10.1007/
s11104-007-9509-9
GEORGE, E. – MARSCHNER, H. – JAKOBSEN, I. 1995.
Role of arbuscular mycorrhizal fungi in uptake of phos-
phorus and nitrogen from soil. In Critical Review in
Biotechnology, vol. 15, no. 3–4, pp. 257–270. DOI:
10.3109/07388559509147412
GIANINAZZI-PEARSON, V. 1996. Plant cell responses to
arbuscular mycorrhizal fungi: getting to the roots of the
symbiosis. In The Plant Cell, vol. 8, pp. 1871–1883. DOI:
10.1105/tpc.8.10.1871
GIOVANNETTI, M. – AVIO, L. – SBRANA, C. – CITERNESI,
A.S. 1993. Factors affecting appressorium development in
the vesicular-arbuscular mycorrhizal fungus Glomus mos-
seae. In The New Phytologist, vol. 123, no. 1, pp. 114–122.
GIOVANNETTI, M. – SBRANA, C. – LOGI, C. 1994. Early
processes involved in host recognition by arbuscular my-
corrhizal fungi. In The New Phytologist, vol. 127, no. 4, pp.
703–709. DOI: 10.1111/j.1469-8137.1994.tb02973.x
GIRI, B. – KAPOOR, R. – MUKERJI, K.G. 2003. Inuence
of arbuscular mycorrhizal fungi and salinity on growth,
biomass and mineral nutrition of Acacia auriculiformis. In
Biology and Fertility of Soils, vol. 38, no. 3, pp. 170–175.
DOI: 10.1007/s00374-003-0636-z
GLENN, M.G. – CHEW, F.S. – WILLIAMS, P.H. 1985. Hyphal
penetration of Brassica (Cruciferae) roots by a vesicular-ar-
buscular mycorrhizal fungus. In The New Phytologist, vol.
99, no. 3, pp. 463–472.
GOMEZ-SAGASTI, M.T. – ALKORTA, I. – BECERRIL, J.M.
– EPELDE, L. – ANZA, M. – GARBISU, C. 2012. Micro-
bial monitoring of the recovery of soil quality during heavy
metal phytoremediation. In Water, Air, & Soil Pollution,
vol. 223, no. 6, pp. 3249–3262. DOI: 10.1007/s11270-012-
1106-8
GONZALEZ-CHÁVEZ, M.C. – CARRILLO-GONZALEZ, R.
– WRIGHT, S.F. – NICHOLS, K.A. 2004. The role of glo-
malin, a protein produced by arbuscular mycorrhizal fungi,
in sequestering potentially toxic elements. In Environmen-
tal Pollution, vol. 130, no. 3, pp. 317–323. DOI: 10.1016/j.
envpol.2004.01.004
GOVINDARAJULU, M. – PFEFFER, P.E. – JIN, H. – ABU-
BAKER, J. – DOUDS, D.D. – ALLEN, J.W. – BÜCKING,
H. – LAMMERS, P.J. – SHACHAR-HILL, Y. 2005. Ni-
trogen transfer in the arbuscular mycorrhizal symbiosis. In
Nature, vol. 435, pp. 819–823. DOI: 10.1038/nature03610
HAWKINS, H.J. – JOHANSEN, A. – GEORGE, E. 2000. Up-
take and transport of organic and inorganic nitrogen by ar-
buscular mycorrhizal fungi. In Plant and Soil, vol. 226, no.
2, pp. 275–285. DOI: 10.1023/A:1026500810385
HAYMAN, D.S. – TAVARES, M. 1985. Plant-growth respons-
es to vesicular-arbuscular mycorrhiza. XV. Inuence of
soil-pH on the symbiotic efciency of different endophytes.
In The New Phytologist, vol. 100, pp. 367–377.
HELGASON, T. – DANIELL, T.J. – HUSBAND, R. – FITTER,
A.H. – YOUNG, J.P.W. 1998. Ploughing up the wood-wide
web? In Nature, vol. 394, p. 431. DOI: 10.1038/28764
HELGASON, T. – FITTER, A. 2005. The ecology and evolution
of the arbuscular mycorrhizal fungi. In Mycologist, vol. 19,
no. 3, pp. 96–101. DOI: 10.1017/S0269-915X(05)00302-2
HILDEBRANDT, U. – KALDORF, M. – BOTHE, H. 1999.
The zinc violet and its colonization by arbuscular mycor-
rhizal fungi. In Journal of Plant Physiology, vol. 154, no.
5–6, pp. 709–717. DOI: 10.1016/S0176-1617(99)80249-1
HUSBAND, R. – HERRE, E.A. – TURNER, S.L. – GAL-
LERY, R. – YOUNG, J.P.W. 2002. Molecular diversity of
arbuscular mycorrhizal fungi and patterns of associations
over time and space in a tropical forest. In Molecular Ecol-
ogy, vol. 11, no. 12, pp. 2669–2678. DOI: 10.1046/j.1365-
294x.2002.01647.x
IBRAHIM, A.H. – ABDEL-FATTAH, G.M. – EMAM, F.M. –
ABD EL-AZIZ, M.H. – SHOKR, A.E. 2011. Arbuscular
mycorrhizal fungi and spermine alleviate the adverse ef-
fects of salinity stress on electrolyte leakage and productiv-
ity of wheat plants. In Phyton, vol. 51, no. 2, pp. 261–276.
JACKSON, L.E. – BURGER, M. – CAVAGNARO, T.R. 2008.
Roots, nitrogen transformations and ecosystem services. In
Annual Review in Plant Biology, vol. 59, pp. 341–363. DOI:
10.1146/annurev.arplant.59.032607.092932
JANSA, J. – MOZAFAR, A. – ANKEN, T. – RUH, R. – SAND-
12
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
ERS, I.R. – FROSSARD, E. 2002. Diversity and structure
of AMF communities as affected by tillage in a temper-
ate soil. In Mycorrhiza, vol. 12, no. 5, pp. 225–234. DOI:
10.1007/s00572-002-0163-z
JANSA, J. – MOZAFAR, A. – KUHN, G. – ANKEN,
T. – RUH, R. – SANDERS, I.R. – FROSSARD,
E. 2003. Soil tillage affects the community struc-
ture of mycorrhizal fungi in maize roots. In Ecologi-
cal Applications, vol. 13, no. 4, pp. 1164–1176. DOI:
10.1890/1051-0761(2003)13[1164:STATCS]2.0.CO;2
JOHANSEN, A. – JAKOBSEN, I. – JENSEN, E.S. 1992. Hy-
phal transport of 15N labelled nitrogen by a vesicular-ar-
buscular mycorrhizal fungus and its effect on depletion of
inorganic soil N. In New Phytologist, vol. 122, no. 2, pp.
281–288. DOI: 10.1111/j.1469-8137.1992.tb04232.x
JOHANSSON, J. – PAUL, L.R. – FINLAY, R.D. 2004. Micro-
bial interactions in the mycorrhizosphere and their signif-
icance for sustainable agriculture. In FEMS Microbiology
Ecology, vol. 48, no. 1, pp. 1–13. DOI: 10.1016/j.fem-
sec.2003.11.012
JONER, E.J. – BRIONES, R. – LEVYAL, C. 2000. Metal
-binding capacity of arbuscular mycorrhizal mycelium.
In Plant and Soil, vol. 226, no. 2, pp. 227–234. DOI:
10.1023/A:1026565701391
JUNIPER, S. – ABBOTT, L. 1993. Vesicular-arbuscular my-
corrhizas and soil salinity. In Mycorrhiza, vol. 4, no. 2, pp.
45–57. DOI: 10.1007/BF00204058
JUNIPER, S. – ABBOTT, L.K. 2006. Soil salinity delays ger-
mination and limits growth of hyphae from propagules of
arbuscular mycorrhizal fungi. In Mycorrhiza, vol. 16, no. 5,
p. 371–379. DOI: 10.1007/s00572-006-0046-9
KABIR, Z. 2005. Tillage or no-tillage: impact on mycorrhizae.
In Canadian Journal of Plant Science, vol. 85, no. 1, pp.
23–29. DOI: 10.4141/P03-160
KAHILUOTO, H. – KETOJA, E. – VESTBERG, M. – SAARE-
LA, I. 2001. Promotion of AM utilization through reduced P
fertilization 2. Field studies. In Plant and Soil, vol. 231, no.
1, pp. 65–79. DOI: 10.1023/A:1010366400009
KALDORF, M. – KUHN, A.J. – SCHRÖDER, W.H. – HIL-
DERBRANDT, U. – BOTHE, H. 1999. Selective element
deposits in maize colonized by a heavy metal tolerance con-
ferring arbuscular mycorrhizal fungus. In Journal of Plant
Physiology, vol. 154, no. 5–6, pp. 718–728. DOI: 10.1016/
S0176-1617(99)80250-8
KARAGIANNIDIS, N. – BLETSOS, F. – STAVROPOULOS,
N. 2002. Effect of Verticillium wilt (Verticillium dahliae
Kleb.) and mycorrhiza (Glomus mosseae) on root coloni-
zation, growth and nutrient uptake in tomato and eggplant
seedlings. In Scientia Horticulturae, vol. 94, no. 1–2, pp.
145–156. DOI: 10.1016/S0304-4238(01)00336-3
KARASAWA, T. – HODGE, A. – FITTER, A.H. 2012. Growth,
respiration and nutrient acquisition by the arbuscular my-
corrhizal fungus Glomus mosseae and its host plant Plan-
tago lanceolata in cooled soil. In Plant Cell & Environ-
ment, vol. 35, no. 4, pp. 819–828. DOI: 10.1111/j.1365-
3040.2011.02455.x
KAUR, H. – GARG, N. 2017. Recent perspectives on cross talk
between cadmium, zinc, and arbuscular mycorrhizal fungi
in plants. In Journal of Plant Growth Regulation, vol. 37,
no. 2, pp. 680–693. DOI: 10.1007/s00344-017-9750-2
KHALVATI, M.A. – HU, Y. – MOZAFAR, A. – SCHMIDHAL-
TER, U. 2005. Quantication of water uptake by arbuscu-
lar mycorrhizal hyphae and its signicance for leaf growth,
water relations, and gas exchange of barley subjected to
drought stress. In Plant Biology (Stuttgart, Germany), vol.
7, no. 6, pp. 706–712. DOI: 10.1055/s-2005-872893
KHAN, M.S. – ZAIDI, A. – WANI, P.A. 2007. Role of phos-
phate solubilizing microorganisms in sustainable agricul-
ture – a review. In Agronomy for Sustainable Development,
vol. 27, no. 1, pp. 29–43. DOI: 10.1051/agro:2006011
FREY-KLETT, P. – GARBAYE, J. – TARKKA, M. 2007. The
mycorrhiza helper bacteria revisited. In The New Phytolo-
gist, vol. 176, no. 1, pp. 22–36. DOI: 10.1111/j.1469-
8137.2007.02191.x
KLIRONOMOS, J. 2000. Host-specicity and functional diver-
sity among arbuscular mycorrhizal fungi. In Microbial Bio-
systems: New Frontiers. Proceedings of the 8th Internation-
al Symposium on Microbial Ecology. Atlantic Canada Socie-
ty for Microbial Ecology. Halifax, Canada, pp. 845–851.
KLIRONOMOS, J.N. – HART, M.M. 2002. Colonization of
roots by arbuscular mycorrhizal fungi using different sourc-
es of inoculum. In Mycorrhiza, vol. 12, no. 4, pp. 181–184.
DOI: 10.1007/s00572-002-0169-6
KÖHL, L. – OEHL, F. – VAN DER HEIJDEN, M.G.A. 2014.
Agricultural practices indirectly inuence plant productiv-
ity and ecosystem services through effects on soil biota.
In Ecological Applications, vol. 24, no. 7, pp. 1842–1853.
DOI: 10.1890/13-1821.1
KUMAR, A. – SHARMA, S. – MISHRA, S. 2010. Inuence of
arbuscular mycorrhizal (AM) fungi and salinity on seedling
growth, solute accumulation and mycorrhizal dependency
of Jatropha curcas L. In Journal of Plant Growth Regu-
lation, vol. 29, no. 3, pp. 297–306. DOI: 10.1007/s00344-
009-9136-1
LEIGH, J. – HODGE, A. – FITTER, A.H. 2009. Arbuscular my-
corrhizal fungi can transfer substantial amounts of nitrogen
to their host plant from organic material. In The New Phy-
tologist, vol. 181, no. 1, pp. 199–207. DOI: 10.1111/j.1469-
8137.2008.02630.x
LI, X.L. – GEORGE, E. – MARSCHNER, H. 1991. Extension
of the phosphorus depletion zone in VA-mycorrhizal white
clover in a calcareous soil. In Plant and Soil, vol. 136, no. 1,
pp. 41–48. DOI: 10.1007/BF02465218
LINDERMAN, R.G. 1988. Mycorrhizal interactions with the
rhizosphere microora: the mycorrhizosphere effect. In
Phytopathology, vol. 78, pp. 366–371. DOI: 10.1007/978-
94-011-3336-4_73
MARGESIN, R. – PŁAZA, G.A. – KASENBACHER, S. 2011.
Characterization of bacterial communities at heavy-met-
al-contaminated sites. In Chemosphere, vol. 82, no. 11, pp.
1583–1588. DOI: 10.1016/j.chemosphere.2010.11.056
MARSCHNER, H. 1995. Mineral nutrition of higher plants.
London : Academic Press, 889 p. ISBN 978-0-12-473542-2
MARULANDA, A. – AZCÓN, R. – RUIZ-LOZANO, J.M.
2003. Contribution of six arbuscular mycorrhizal fungal
isolates to water uptake by Lactuca sativa plants under
drought stress. In Physiologia Plantarum, vol. 119 , no. 4,
pp. 526–533. DOI: 10.1046/j.1399-3054.2003.00196.x
MAURER, C. – RÜDY, M. – CHERVET, A. – STURNY, W.G.
– FLISCH, R. – OEHL, F. 2014. Diversity of arbuscular
mycorrhizal fungi in eld crops using no-till and conven-
tional tillage practices. In Agrarforschung Schweiz, vol. 5,
no. 10, pp. 398–405.
MISHRA, V. – ELLOUZE. W. – HOWARD. R.J. 2018. Utility
of Arbuscular Mycorrhizal Fungi for Improved Production
and Disease Mitigation in Organic and Hydroponic Green-
house Crops. In Journal of Horticulture, vol. 5, no. 3, pp.
1–10. DOI: 10.4172/2376-0354.1000237
MOHAMMAD, M.J. – MALKAWI, H.I. – SHIBLI, R. 2003.
Effects of mycorrhizal fungi and phosphorus fertilization on
growth and nutrient uptake of barley grown on soils with
different levels of salts. In Journal of Plant Nutrition, vol.
26, no. 1, pp. 125–137. DOI: 10.1081/PLN-120016500
MOHAMMADI, K. – KHALESRO, S. – SOHRABI, Y. –
13
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
HEIDARI, G. 2011. A review: Benecial effects of the
mycorrhizal fungi for plant growth. In Journal of Applied
Environmental and Biological Science, vol. 1, no. 9, pp.
310–319.
MOHAN, J.E. – COWDEN, C.C. – BAAS, P. – DAWADI,
A. – FRANKSON, P.T. – HELMICK, K. – HUGHES, E.
– KHAN, S. – LANG, A. – MACHMULLER, M. – TAY-
LOR, M. – WITT, C.A. 2014. Mycorrhizal fungi medi-
ation of terrestrial ecosystem responses to global change:
mini-review. In Fungal Ecology, vol. 10, pp. 3–19. DOI:
10.1016/j.funeco.2014.01.005
OLSRUD, M. – CARLSSON, B.A. – SVENSSON, B.M. – MI-
CHELSEN, A. – MELILLO, J.M. 2010. Responses of fun-
gal root colonization, plant cover and leaf nutrients to long-
term exposure to elevated atmospheric CO2 and warming in
a subarctic birch forest understory. In Global Change Biolo-
gy, vol. 16, no. 6, pp. 1820–1829. DOI: 10.1111/j.1365-
2486.2009.02079.x
PATTINSON, G.S. – WARTON, D.I. – MISMAN, R. –
MCGEE, P.A. 1997. The fungicides Terrazole and Terra-
clor and the nematicide Fenamiphos have little effect on
root colonisation by Glomus mosseae and growth of cotton
seedlings. In Mycorrhiza, vol. 7, no. 3, pp. 155–159. DOI:
10.1007/s005720050175
PFEFFER, P.E. – DOUDS, D.D. – BÉCARD, G. – SHACHAR-
HILL, Y. 1999. Carbon uptake and the metabolism and trans-
port of lipids in an arbuscular mycorrhiza. In Plant Physio-
logy, vol. 120, pp. 587–598. DOI: 10.1104/pp.120.2.587
PORTER, W.M. – ROBSON, A.D. – ABBOTT, L.K. 1987.
Field survey of the distribution of vesicular–arbuscular my-
corrhizal fungi in relation to soil pH. In Journal of Applied
Ecology, vol. 24, no. 2, pp. 659–662.
POZO, M.J. – CORDIER, C. – DUMAS-GAUDOT, E. –
GIANINAZZI, S. – BAREA, J.M. – AZCÓN-AGUILAR,
C. 2002. Localized versus systemic effect of arbuscular
mycorrhizal fungi on defence responses to Phytophtho-
ra infection in tomato plants. In Journal of Experimental
Botany, vol. 53, no. 368, pp. 525–534. DOI: 10.1093/jex-
bot/53.368.525
PUMPLIN, N. – HARRISON, M.J. 2009. Live-cell imaging
reveals periarbuscular membrane domains and organelle
location in Medicago truncatula roots during arbuscular
mycorrhizal symbiosis. In Plant Physiology, vol. 151, no.
2, pp. 809–819. DOI: 10.1104/pp.109.141879
RABIE, G.H. – ALMADINI, A.M. 2005. Role of bioinoculants
in development of salt-tolerance of Vicia faba plants under
salinity stress. In African Journal of Biotechnology, vol. 4,
no. 3, pp. 210–222.
REDECKER, D. – KODNER, R. – GRAHAM, L.E. 2000. Glo-
malean fungi from the Ordovician. In Science, vol. 289, no.
5486, pp. 1920–1921.
REDECKER, D. – SHÜSSLER, A. – STOCKINGER, H. –
STÜRMER, S.L. – MORTON, J.B. – WALKER, C. 2013.
An evidence-based consensus for the classication of ar-
buscular mycorrhizal fungi (Glomeromycota). In Mycorrhi-
za, vol. 23, no. 7, pp. 515–531. DOI: 10.1007/s00572-013-
0486-y
REQUENA, N. – BREUNINGER, M. 2004. The old arbuscular
mycorrhizal symbiosis in the light of the molecular era. In
ESSER, K. – LÜTTGE, U. – BEYSCHLAG, W. – MURATA,
J. (Eds.) Progress in Botany. Springer, Berlin, Heidelberg,
ISBN 978-3-642-18819-0, pp. 323–356.
REQUENA, N. – SERRANO, E. – OCÓN, A. – BREUNINGER,
M. 2007. Plant signals and fungal perception during arbus-
cular mycorrhizal stablishment. In Phytochemistry, vol. 68,
no. 1, pp. 33–40. DOI: 10.1016/j.phytochem.2006.09.036
RILLIG, M.C. – FIELD, C.B. – ALLEN, M.F. 1999. Soil biota
responses to long-term atmospheric CO2 enrichment in two
California annual grasslands. In Oecologia, vol. 119 , no. 4,
pp. 572–577. DOI: 10.1007/s004420050821
RUIZ-LOZANO, J.M. – AZCÓN, R. – GOMEZ M. 1995. Ef-
fects of arbuscularmycorrhizal Glomus species on drought
tolerance: physiological and nutritional responses. In
Applied and Environmental Microbiology, vol. 61, no. 2,
pp. 456–460.
RUIZ-LOZANO, M. – AZCON, R. 2000. Symbiotic efciency
and infectivity of an autochthonous arbuscular mycorrhizal
Glomus sp. from saline soils and Glomus deserticola under
salinity. In Mycorrhiza, vol. 10, no. 3, pp. 137–143. DOI:
10.1007/s005720000075
RYAN, M.H. – ANGUS, J.F. 2003. Arbuscular mycorrhizae in
wheat and eld pea crops on a low P soil: increased Zn-uptake
but no increase in P-uptake or yield. In Plant and Soil, vol.
250, no. 2, pp. 225–239. DOI: 10.1023/A:1022839930134
RYAN, M.H. – CHILVERS, G.A. – DUMARESQ, D.C. 1994.
Colonisation of wheat by VA-mycorrhizal fungi was found
to be higher on a farm managed in an organic manner than
on a conventional neighbour. In Plant and Soil, vol. 160, no.
1, pp. 33–40. DOI: 10.1007/BF00150343
SÄLE, V. – AGUILERA, P. – LACZKO, E. – MÄDER, P. –
BERNER, A. – ZIHLMANN, U. – VAN DER HEIJDEN,
M.G.A. – OEHL, F. 2015. Impact of conservation tillage
and organic farming on the diversityof arbuscular mycor-
rhizal fungi. In Soil Biology and Biochemistry, vol. 84, pp.
38–52. DOI: 10.1016/j.soilbio.2015.02.005
SANNAZZARO, A.I. – RUIZ, O.A. – ALBERTO, E.O. –
MENÉNDEZ, A.B. 2006. Alleviation of salt stress in Lotus
glaber by Glomus intraradices. In Plant and Soil, vol. 285,
no. 1–2, pp. 279–287. DOI: 10.1007/s11104-006-9015-5
SBRANA, C. – GIOVANNETTI, M. 2005. Chemotropism in
the arbuscular mycorrhizal fungus Glomus mosseae. In
Mycorrhiza, vol. 15, no. 7, pp. 539–545. DOI: 10.1007/
s00572-005-0362-5
SCHÜßLER, A. – SCHWARZOTT, D. – WALKER, C. 2001.
A new fungal phylum, the Glomeromycota: phylogeny and
evolution. In Mycological Research, vol. 105, no. 12, pp.
1413–1421. DOI: 10.1017/S0953756201005196
SCHÜßLER, A. – WALKER, C. 2010. The Glomeromycota: a
species list with new families and new genera. Edinburgh
and Kew : The Royal Botanic Garden Kew, Botanische Sta-
atssammlung Munich, and Oregon State University, 58 p.
ISBN 1466388048
SCHWEIGER, P.F. – JAKOBSEN, I. 1998. Dose-response re-
lationships between four pesticides and phosphorus uptake
by hyphae of arbuscular mycorrhizas. In Soil Biology and
Biochemistry, vol. 30, no. 10–11, pp. 1415–1422. DOI:
10.1016/S0038-0717(97)00259-9
SELVARAJ, T. – CHELLAPPAN, P. 2006. Arbuscular mycor-
rhizae: a diverse personality. In Journal of Central European
Agriculture, vol. 7, no. 2, pp. 349–358.
SHARMA, D. – KAPOOR, R. – BHATNAGAR, A.K. 2009.
Differential growth response of Curculigo orchioides to
native arbuscular mycorrhizal fungal (AMF) communities
varying in number and fungal components. In European
Journal of Soil Biology, vol. 45, no. 4, pp. 328–333. DOI:
10.1016/j.ejsobi.2009.04.005
SLEZACK, S. – DUMAS-GAUDOT, E. – ROSENDAHL,
S. – KJOLLER, R. – PAYNOT, M. – NEGREL, J. –
GIANINAZZI, S. 1999. Endoproteolytic activities in pea
roots inoculated with the arbuscular mycorrhizal fungus
Glomus mosseae and/or Aphanomyces euteiches in relation
to bioprotection. In The New Phytologist, vol 142, no. 3, pp.
517–529. DOI: 10.1046/j.1469-8137.1999.00421.x
SMITH, S.E. – READ, D. 1997. Mycorrhizal symbiosis.
14
Agriculture (Poľnohospodárstvo), 65, 2019 (1): 3−15
San Diego, CA, USA : Academic Press, 605 p. ISBN:
9780080537191
SMITH, F.A. – SMITH, S.E. 2011. What is the signicance of
the arbuscular mycorrhizal colonisation of many econom-
ically important crop plants? In Plant and Soil, vol. 348,
p. 63. DOI: 10.1007/s11104-011-0865-0
SMITH, S.E. – SMITH, F.A. – JAKOBSEN, I. 2003. Mycor-
rizal fungi can dominate phosphate supply to plants irre-
spective of growth responses. In Plant Physiology, vol. 133,
pp. 16–20. DOI: 10.1104/pp.103.024380
SMITH, S.E. – FACELLI, E. – POPE, S. – SMITH, F.A. 2010.
Plant performance in stressful environments: interpreting
new and established knowledge of the roles of arbuscular
mycorrhizas. In Plant and Soil, vol. 326, no. 1–2, pp. 3–20.
DOI: 10.1007/s11104-009-9981-5
TOMMERUP, I.C. 1988. The vesicular–arbuscular mycorrhi-
zas. In Advances in Plant Pathology, vol. 6, pp. 81–91.
DOI: 10.1016/B978-0-12-033706-4.50008-6
TRESEDER, K.K. 2004. A meta-analysis of mycorrhizal re-
sponses to nitrogen, phosphorus, and atmospheric CO2 in
eld studies. In The New Phytologist, vol. 164, no. 2, pp.
347–355. DOI: 10.1111/j.1469-8137.2004.01159.x
VIGO, C. – NORMAN, J.R. – HOOKER, J.E. 2000. Biocon-
trol of the pathogen Phytophthora parasitica by arbuscular
mycorrhizal fungi is a consequence of effects on infection
loci. In Plant Pathology, vol. 49, no. 4, pp. 509–514. DOI:
10.1046/j.1365-3059.2000.00473.x
VIVAS, A. – BAREA, J.M. – AZCÓN, R. 2005. Interactive
effect of Brevibacillus brevis and Glomus mosseae both
isolated from Cd contaminated soil, on plant growth, phys-
iological mycorrhizal fungal characteristics and soil en-
zymatic activities in Cd polluted soils. In Environmental
Pollution, vol. 134, no. 2, pp. 257–266. DOI: 10.1016/j.
envpol.2004.07.029
WANG, B. – QIU, Y.L. 2006. Phylogenetic distribution and
evolution of mycorrhizas in land plants. In Mycorrhiza, vol.
16, no. 5, pp. 299–363. DOI: 10.1007/s00572-005-0033-6
WANG, B. – FUNAKOSHI, D. – DALPE, Y. – HAMEL, C.
2002. Phosphorus-32 absorption and translocation to host
plants by arbuscular mycorrhizal fungi at low root zone
temperature. In Mycorrhiza, vol. 12, no. 2, pp. 93–96. DOI:
10.1007/s00572-001-0150-9
WETZEL, K. – SILVA, G. – MATCZINSKI, U. – OEHL, F.
– FESTER, T. 2014. Superior differentiation of arbuscular
mycorrhizal fungal communities from till and no-till plots
by morphological spore identication when compared to
T-RFLP. In Soil Biology & Biochemistry, vol. 72, pp. 88–
96. DOI: 10.1016/j.soilbio.2014.01.033
WHIPPS, J.M. 2004 Prospects and limitations for mycorrhi-
zas in biocontrol of root pathogens. In Canadian Journal
of Botany, vol. 82, no. 8, pp. 1198–1227. DOI: 10.1139/
b04-082
WU, Q.S. – ZOU, Y.N. – LIU, W. – YE, X.F. – ZAI, H.F. –
ZHAO, L.J. 2010. Alleviation of salt stress in citrus seed-
lings inoculated with mycorrhiza: changes in leaf antioxi-
dant defense systems. In Plant Soil and Environment, vol.
56, no. 10, pp. 470–475. DOI: 10.17221/54/2010-PSE
YANO-MELO, A.M. – SAGGIN, O.J. – MAIA, L.C. 2003.
Tolerance of mycorrhized banana (Musa sp. cv. Pacovan)
plantlets to saline stress. In Agriculture, Ecosystems and
Environment, vol. 95, no. 1, p. 343–348. DOI: 10.1016/
S0167-8809(02)00044-0
ZHANG, F. – HAMEL, C. – KIANMEHR, H. – SMITH, D.L.
1995. Root-zone temperature and soybean [Glycine max
(L.) merr.] vesicular-arbuscular mycorrhizae: development
and interactions with the nitrogen xing symbiosis. In En-
vironmental and Experimental Botany, vol. 35, no. 3, pp.
287–298. DOI: 10.1016/0098-8472(95)00023-2
ZOU, X. – BINKLEY, D. – DOXTADER, K.G. 1992. New
methods for estimating gross P mineralization and mobili-
zation rates in soils. In Plant and Soil, vol. 147, no. 2, pp.
243–250. DOI: 10.1007/BF00029076
Received: February 12, 2019
Accepted: April 2, 2019
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