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Citation: Onyeaka, H.N.; Akinsemolu,
A.A.; Siyanbola, K.F.; Adetunji, V.A.
Green Microbe Profile: Rhizophagus
intraradices—A Review of Benevolent
Fungi Promoting Plant Health and
Sustainability. Microbiol. Res. 2024,15,
1028–1049. https://doi.org/10.3390/
microbiolres15020068
Academic Editor: Ligang Zhou
Received: 14 May 2024
Revised: 5 June 2024
Accepted: 13 June 2024
Published: 18 June 2024
Copyright: © 2024 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Review
Green Microbe Profile: Rhizophagus intraradices—A Review of
Benevolent Fungi Promoting Plant Health and Sustainability
Helen N. Onyeaka
1,
* , Adenike A. Akinsemolu
1
, Kehinde Favour Siyanbola
2
and Victoria Ademide Adetunji
2
1School of Chemical Engineering, University of Birmingham, Birmingham B152 TT, UK;
adenike234@gmail.com
2Department of Microbiology, Faculty of Basic and Applied Sciences, Osun State University,
Osogbo 210001, Osun State, Nigeria; siyanbolafavour2204@gmail.com (K.F.S.);
dtnjvictoria@gmail.com (V.A.A.)
*Correspondence: h.onyeaka@bham.ac.uk
Abstract: Arbuscular mycorrhizal fungi (AMF) such as Rhizophagus intraradices (formerly known
as Glomus intraradices) are of great importance to maintaining the soil ecosystem while supporting
sustainable agriculture and practices. This review explores the taxonomy of Rhizophagus intraradices,
their attributes, mycorrhizal symbiosis, plant growth improvement, nutrient recycling in the soil,
soil health and environmental rehabilitation, and challenges that impede the effective use of AMF in
agriculture. AMF impacts soil structure by releasing organic compounds like glomalin, improving
total organic carbon and water-holding capacity, and reducing water scarcity. AMF, in sustainable
agriculture, not only improves crop productivity through nutrient uptake but also enhances soil
fertility and plants’ resistance to so-called stress from abiotic factors as well. The integration of AMF
with other beneficial microorganisms in organic farming will be powerful both to ensure long-term
soil output and to protect food from bacteria. Nevertheless, chemical inputs and spatial biases of the
researchers remain matters to be solved in connection with the broad feasibility of AMF use.
Keywords: Rhizophagus intraradices;Glomus intraradices; arbuscular mycorrhizal fungi; plant health;
sustainability; agriculture
1. Introduction
Glomus intraradices, initially detected within a citrus plantation in Florida by Schenck
and Smith [
1
], is categorized as an arbuscular mycorrhizal fungus (AMF) that predom-
inantly forms its spores intraradically [
2
]. Following the differentiation of Glomus at a
generic level within this specific species, G. Intraradices underwent a reclassification to
Rhizophagus intraradices by Schüssler and Walker [
3
], aligning with the historical utilization
of the genus name for AMF generating spores in roots [
4
,
5
]. Despite the recommendation
put forth by Sieverding et al. [
6
] to replace Rhizophagus with Rhizoglomus, Walker et al. [
7
]
opposed this suggestion, advocating for the preservation of the generic term Rhizophagus,
albeit with an alteration of the type species to R. intraradices. Adhering to the principle
of ‘existing usage’ as prescribed in recommendation 14A.1 of the International Code of
Nomenclature for algae, fungi, and plants (ICNafp) by Turland et al. [
8
] signifies that the
current assignment, Rhizophagus intraradices, will be employed in this investigation, except
in scenarios where previous designations offer added clarity. The utilization of molecular
analysis of ribosomal DNA facilitated the reclassification of all arbuscular mycorrhizal
fungi from the Zygomycota phylum to the Glomeromycota phylum [9].
Rhizophagus intraradices interact with the roots of plants to foster a symbiotic relation-
ship. The balance between organisms being beneficial, mutually beneficial, or potentially
detrimental for plants serves as a foundation for healthy and thriving plant communities.
Formerly, the genus Glomus was transferred to the genus Rhizophagus and classified within
the family Glomeraceae [
2
]. The spores of this fungus come in different colors, including
Microbiol. Res. 2024,15, 1028–1049. https://doi.org/10.3390/microbiolres15020068 https://www.mdpi.com/journal/microbiolres
Microbiol. Res. 2024,15 1029
white, cream, or yellow brown, with a median length of 40 to 140
µ
m. The structure of the
hyphae is cylindrical or flared, and it has a width of 11 to 18
µ
m. It can colonize new plants
by taking over their spores, hyphae, or root fragments. Despite being an ancient and very
simple organism, it seems to be able to develop (undergo meiosis) and recombine genes [
2
].
It acts as a soil inoculant and has agricultural and horticultural significance for plants’
growth and the quality of the soil. It is common in different types of soils and performs
the role of maintaining the biodiversity of the ecosystem and the normal functions of
these ecosystems through the formation of a great number of networks of hyphae. This
microorganism has a vital role in promoting plant health and sustainability and can help in
increasing the scope of research on the topic as it is an agent involving ecological benefits
and agricultural applications [
10
]. This article therefore aims to provide a comprehensive
understanding of the multifaceted benefits of R. intraradices, emphasizing its importance in
sustainable agriculture and its potential to contribute to food security and environmental
health. This review systematically recapitulates all currently available information about
Rhizophagus intraradices and offers an extensive introduction to its life cycle, environmental
conditions, and host plant relations. This is useful to current readers who do not always
have the luxury of time to go through several studies separately and decipher which
findings are the most relevant to the field at the moment. Through a discussion of the
search results in relation to agriculture, the current study centers its findings on the need
for further research into the fungal species to improve plant health and production. From
such discussions arise the probability of an increase in crop yields, better soil quality, and
a decrease in the use of chemical fertilizers and pesticides. This review also highlights
some of the areas where knowledge about the biology of Rhizophagus intraradices may be
lacking, masking the need for further investigation. They can serve as a research agenda
to direct future findings and assist with determining how funds are invested. This article
consists of knowledge from different fields, including microbiology, plant sciences, ecology,
and agronomy, and thus offers a broader perception of the fungi and their usefulness. But
more than simply reviewing current literature, the review also presents new directions
on how to implement Rhizophagus intraradices in modern agriculture. This may involve
techniques for the introduction of beneficial microbes into plants, enhancing symbiosis,
and expanding the application of fungi in various systems of production. Furthermore, the
addition of cases or examples of existing successful uses of Rhizophagus intraradices makes it
more appealing to farmers and the agricultural industry because it encourages its use and
shows a desirable result. Consequently, in addition to informing readers of previous work
in the field, the review also presents several valuable suggestions and points of view for
those who would like to engage in further research and practice in sustainable agriculture
and plant health.
2. Taxonomy and Characteristics
In Table 1,R. intraradices is categorized under the Eukaryota domain, showing that it
possesses nucleus-containing cells. It falls under the fungi kingdom, particularly within
the Glomeromycota division, known for fungi capable of establishing mutually benefi-
cial relationships with the roots of plants. Further classification is identified in the class
Glomeromycetes, order Glomerales, and family Glomeraceae, providing detailed fungal
taxonomical classification. It is then grouped under the genus Rhizophagus, with the
species name R. intraradices, recognized for its important ability to form arbuscular my-
corrhizal associations with plants, thereby leading to enhanced nutrient absorption and
promoting plant growth.
Microbiol. Res. 2024,15 1030
Table 1. Taxonomic classification and identification of Rhizophagus intraradices (formerly known as
Glomus intraradices).
Taxonomy Classification
Domain Eukaryota
Kingdom Fungi
Division Glomeromycota
Class Glomeromycetes
Order Glomerales
Family Glomeraceae
Genus Rhizophagus
Species R. intraradices
Figure 1depicts the spores of Rhizophagus intraradices, captured under a micro-
scope, with three distinct spores, each exhibiting a spherical form with hues ranging from
brown to yellow. The spores are surrounded by transparent, thread-like formations, likely
representing fungal hyphae or other minuscule elements within the microscopic field.
Microbiol.Res.2024,15,FORPEERREVIEW 3
Table1.TaxonomicclassificationandidentificationofRhizophagusintraradices(formerlyknownas
Glomusintraradices).
Taxonomy Classification
DomainEukaryota
KingdomFungi
DivisionGlomeromycota
ClassGlomeromycetes
OrderGlomerales
FamilyGlomeraceae
GenusRhizophagus
SpeciesR.intraradices
Figure1depictsthesporesofRhizophagusintraradices,capturedunderamicro-
scope,withthreedistinctspores,eachexhibitingasphericalformwithhuesrangingfrom
browntoyellow.Thesporesaresurroundedbytransparent,thread-likeformations,likely
representingfungalhyphaeorotherminusculeelementswithinthemicroscopicfield.
Figure1.SporesofRhizophagusintraradices(formerlyknownasGlomusintraradices)[6].
Table2providesasummaryofthemorphologicalfeatures,distribution,colonization
behavior,andreproductionmethodofRhizophagusintraradices.
Table2.MorphologicalfeaturesofRhizophagusintraradices(formerlyknownasGlomusintraradices).
FeaturesDescription
SporesColor:Paleyellow,greyishyellow.
Shape:Ellipticalwithirregularities.
Size:Generally,between40–140µm.
Formation:Predominantlyformssporesintraradically.
Figure 1. Spores of Rhizophagus intraradices (formerly known as Glomus intraradices) [6].
Table 2provides a summary of the morphological features, distribution, colonization
behavior, and reproduction method of Rhizophagus intraradices.
Microbiol. Res. 2024,15 1031
Table 2. Morphological features of Rhizophagus intraradices (formerly known as Glomus intraradices).
Features Description
Spores Color: Pale yellow, greyish yellow.
Shape: Elliptical with irregularities.
Size: Generally, between 40–140 µm.
Formation: Predominantly forms spores intraradically.
Hyphae Shape: Cylindrical or slightly flared.
Size: Width: 11–18 µm.
Distribution Found in almost all soils, especially those populated with
common host plants, and in forests and grasslands.
Colonization
Colonization peaks earlier than many other fungi in
Rhizophagus, with extensive hyphal networking and intense
intraradical spores associated with the older roots of host plants.
Reproduction Colonizes new plants using spores, hyphae, or fragments of
roots colonized by the fungus.
Table 3provides an overview of the metabolic, genetic, ecological, and physiological
characteristics of the organism Rhizophagus intraradices.
Table 3. Physiological features of Rhizophagus intraradices (formerly known as Glomus intraradices).
Features Description
Metabolism
Capable of osmotic adjustment, antioxidation, and expression
of aquaporin Plasma Membrane Intrinsic Proteins, PIP genes
under drought stress [11].
Meiosis and recombination
Possesses homologs of 51 meiotic genes, indicating the
capability of undergoing conventional meiosis and genetic
recombination [12].
Mycorrhizal association Forms arbuscular mycorrhizal symbiosis with plant roots [2].
Growth temperature range Mesophilic, optimum growth temperature around 25–30 ◦C
Growth substrate Grows in soil, forming mycorrhizal networks with plant
roots [10].
Nutrient utilization and uptake
Utilizes organic carbon compounds for growth.
Can use both organic and inorganic nitrogen sources.
Efficiently absorbs and transports phosphorus to the host [
10
].
3. Mycorrhizal Symbiosis
Within the domain of terrestrial vegetation, mycorrhizal fungal associations are ac-
knowledged as important breakthroughs. A mycorrhiza signifies a symbiotic association
between plant roots and fungi, with plants providing carbohydrates synthesized from
photosynthesis to the fungi while the fungi offer nutrients, and water, and protect the plant
from diverse environmental pressures in return [13].
Mycorrhizal symbiosis’s importance in the ecosystem stems from its influence on
plant productivity and diversity. While generally boosting plant productivity, mycorrhizal
fungi can display diverse relationships with species, ranging from mutualism to parasitism,
depending on differences in the condition of the environment [
14
]. Instances can occur
where mycorrhizal fungi establish parasitic relationships with plants, particularly when
the total benefits are greater than the cost. The complex nature of mycorrhizal symbiosis
requires comprehension of the different factors affecting the functions, structure, and
physiology of both the plant and fungi interacting, as well as the biotic and abiotic elements
within the rhizosphere across various ecological levels [13].
Microbiol. Res. 2024,15 1032
The research by Zhang and Gong [
2
] underscores the substantial role played by
mycorrhizal symbioses in facilitating revegetation and ecological restoration efforts in
areas contaminated with arsenic (As). The classification of mycorrhizal relationships
into four principal types, namely arbuscular mycorrhiza (AM), ectomycorrhizal (EcM)
(Figure 2), ericoid mycorrhiza (ErM), and orchid mycorrhiza (OM), is based on anatomical
characteristics and the identities of the partners involved [15].
Microbiol.Res.2024,15,FORPEERREVIEW 5
ericoidmycorrhiza(ErM),andorchidmycorrhiza(OM),isbasedonanatomicalcharac-
teristicsandtheidentitiesofthepartnersinvolved[15].
Figure2.Imagedepictingtheroot-colonizationarbuscularmycorrhiza(AM)andectomycorrhizal
(EcM)[16,17].
Arbuscularmycorrhizae(anexemplarofarbuscularmycorrhizaisRhizophagusintra-
radices),forinstance,aretraceableinsubterraneanpartsofancientplantfossilsandplay
acrucialroleinnutrientuptakebyplantsinexchangeforphotosynthate.Theynotonly
contributesignificantlytoplanthealthbutcanalsoinfluencethecompositionofplant
communities.Thehyphalnatureofarbuscularmycorrhizae,alongwiththeirdevelop-
mentofhighlybranchedhaustoria,facilitatesefficientnutrientexchangewiththehost
rootcells[15].
AstudybyRamírez-Floresetal.[10]demonstratedthatmaizegrowthunderlow
potassiumconditionswassignificantlyenhancedthroughinoculationwithRhizophagus
intraradices.Mycorrhizalplantsexhibitdenserandintricatelybranchedrootsystems.The
augmentedcontentofmostquantifiedelementsinmycorrhizalplantscorrelateswithroot
andoverallplantgrowth.Nonetheless,theelevatedconcentrationsofboron,calcium,
magnesium,phosphorus,sulfur,andstrontiumsurpasstheanticipatedvaluesestablished
solelyonthesizeoftherootsystem,suggestinganadditionalfunctionoffungaltransport
innutrientabsorption.Inadditiontosupplyingnutrients,AMFalsopromoterootdevel-
opment,therebybenefitingtheplanthost.Begumetal.[18]suggestedthatahigherratio
ofrootstoshootsindicatesasignificantdegreeofmycorrhizalefficacy.Improvementsin
seedlingquality,manifestedingrowthtraitscomparedtothecontrolgroup,furthervali-
datetheideathatinfectedseedlingsenhancedtheirstrength,resilience,growth,andsub-
sequentperformanceaftertransplantation.TheintroductionofAMF,particularlyR.in-
traradices,wasconsideredadvantageousforseedlings[19].Moreover,studieshaveshown
thatmycorrhizalinoculationcanimprovecropconsistency,reducetransplantfatalities,
andincreasetheyieldofvarioushorticulturalcropscultivatedonsoillesssubstratesde-
voidofAMfungi[20].
StudieshaveshownthatR.intraradiceshelpsreducetransplantshockinplantseed-
lings[18].AstudyexaminedtheimpactofvariousAMFspeciesonmicropropagated
grapevineplantlets.ThestudyrevealedthatcolonizationofAMFeffectivelyreduced
stresscausedbytransplantation.Thestudyobservedhighlevelsofprolineinmycorrhizal
plants,whichisanon-proteinaminoacidgoenfromplanttissueduringunfavorable
weather.Manystudiessupportthisassertionandshowthatprolineiscrucialforthereg-
ulationofosmosisandproteinprotectioninharshconditions[20].
ThestudybyPonsetal.[21]examinedhowamycorrhizalarbuscularfunguscalled
Rhizophagusintraradicesyieldsphytohormones.Theresearchersextractedphytohormones
frommethionine,includingisopentenyladenosine,indole-aceticacid,andgibberellinA4.
Figure 2. Image depicting the root-colonization arbuscular mycorrhiza (AM) and ectomycorrhizal
(EcM) [16,17].
Arbuscular mycorrhizae (an exemplar of arbuscular mycorrhiza is Rhizophagus in-
traradices), for instance, are traceable in subterranean parts of ancient plant fossils and
play a crucial role in nutrient uptake by plants in exchange for photosynthate. They not
only contribute significantly to plant health but can also influence the composition of plant
communities. The hyphal nature of arbuscular mycorrhizae, along with their development
of highly branched haustoria, facilitates efficient nutrient exchange with the host root
cells [15].
A study by Ramírez-Flores et al. [
10
] demonstrated that maize growth under low
potassium conditions was significantly enhanced through inoculation with Rhizophagus
intraradices. Mycorrhizal plants exhibit denser and intricately branched root systems. The
augmented content of most quantified elements in mycorrhizal plants correlates with root
and overall plant growth. Nonetheless, the elevated concentrations of boron, calcium,
magnesium, phosphorus, sulfur, and strontium surpass the anticipated values established
solely on the size of the root system, suggesting an additional function of fungal transport
in nutrient absorption. In addition to supplying nutrients, AMF also promote root devel-
opment, thereby benefiting the plant host. Begum et al. [
18
] suggested that a higher ratio
of roots to shoots indicates a significant degree of mycorrhizal efficacy. Improvements in
seedling quality, manifested in growth traits compared to the control group, further validate
the idea that infected seedlings enhanced their strength, resilience, growth, and subsequent
performance after transplantation. The introduction of AMF, particularly
R. intraradices
,
was considered advantageous for seedlings [19]. Moreover, studies have shown that myc-
orrhizal inoculation can improve crop consistency, reduce transplant fatalities, and increase
the yield of various horticultural crops cultivated on soilless substrates devoid of AM
fungi [20].
Studies have shown that R. intraradices helps reduce transplant shock in plant seedlings [
18
].
A study examined the impact of various AMF species on micropropagated grapevine
plantlets. The study revealed that colonization of AMF effectively reduced stress caused by
transplantation. The study observed high levels of proline in mycorrhizal plants, which
is a non-protein amino acid gotten from plant tissue during unfavorable weather. Many
studies support this assertion and show that proline is crucial for the regulation of osmosis
and protein protection in harsh conditions [20].
Microbiol. Res. 2024,15 1033
The study by Pons et al. [
21
] examined how a mycorrhizal arbuscular fungus called
Rhizophagus intraradices yields phytohormones. The researchers extracted phytohormones
from methionine, including isopentenyl adenosine, indole-acetic acid, and gibberellin A4.
The obtained results, to a certain extent, ought to serve as a hint that there might not only be
a mutualistic interaction between the plants and arbuscular mycorrhiza but also a way for
Rhizophagus intraradices to self-control. Different types of phytohormones majorly control
the various stages of the arbuscular mycorrhiza symbiosis, such as the pre-symbiotic and
the senescent stages, as well as those phases of interaction between plants and fungi. It
stands for the realization of producing detailed explanations about AM symbiosis signaling
pathways and the host–fungal hormonal interactions that are together oriented towards
the benefit of both organisms.
4. Role of R. intraradices in Promoting Plant Growth
Zhang and Gong [2] elucidated in their study that the incorporation of R. intraradices
effectively mitigated toxicity in R. pseudoacacia seedlings. This achievement was attained
via enhancements in botanical development, modifications in root structure, alterations
in phytohormonal levels and proportions, and an increase in soil glomalin concentrations.
A study carried out by Ramírez-Flores et al. [
10
] noted that the introduction of Rhizoph-
agus intraradices resulted in improved growth of maize under circumstances of limited
potassium availability.
Roussis et al. [
22
] ascertained that the use of elevated levels of the AM fungus R. in-
traradices in nutrient solutions within a hydroponic system led to a substantial enhancement
in the quality and development of processing tomato seedlings. Likewise, Roussis et al. [
22
]
determined that Rhizophagus intraradices promoted the growth of processing tomato roots
by increasing the overall root length and dry mass. Seedlings treated with the highest AMF
concentration (AMF3) displayed an approximately 50% higher total root length compared
to non-inoculated ones, potentially resulting in improved nutrient uptake and enhanced
growth in agricultural contexts. Previous research supports these conclusions, underscor-
ing the advantageous influence of R. intraradices on the root formation and biomass of
tomato plants [
23
,
24
]. Generally, it is widely recognized that integrating inoculants during
the initial stages of plant growth can promote AM symbiosis, leading to heightened plant
development in the nursery and improved efficacy in the field after transplantation [
18
,
20
].
Zhang et al. [
2
] showed that planting seedlings with R. intraradices could help to
improve several growth parameters under energy stress, thereby enabling more effective
growth. AMF, which includes R. intraradices, produce a dramatic influence on the growth
and root systems of plants that are grown in soils polluted by arsenic by helping in the
nutrient uptake and establishment of plants. This evidences the capability of AMF, es-
pecially
R. intraradices
, for fostering plants thereby preventing the deleterious effects of
arsenic contamination on plant health and productivity, which has also put these beneficial
microbes into consideration as one of the plant ameliorators. Zhang et al. [
25
] revealed
that the growth-promoting impact of R. intraradices was relatively inferior compared to
R. intraradices
and F. mosseae, which was associated with heightened mycorrhizal coloniza-
tion and increased lipid utilization.
Chen et al. [
26
] established an adverse relationship between arbuscular coloniza-
tion and root biomass, indicating an extended function of maize roots facilitated by
R. intraradices
. Furthermore, the positive correlation between the overall AMF colonization
level and shoot biomass corroborated the notion that R. intraradices makes a beneficial
contribution to maize growth. The study’s discoveries suggest that soil bacteriomes interact
cooperatively with R. intraradices, impacting maize growth by regulating AMF colonization
in the roots.
Xie et al. [
27
] observed that Rhizophagus intraradices, an arbuscular mycorrhizal fungus,
enhances plant growth by associating with plant roots to enhance nutrient absorption, boost
resistance against pathogens and pests, and regulate plant growth via phytohormones.
R. intraradices did not exhibit a mutual enhancement of B. amyloliquefaciens population
Microbiol. Res. 2024,15 1034
density. Simultaneous inoculation with B. amyloliquefaciens and R. intraradices led to the
most significant increase in shoot weight and photosynthetic efficiency in T. repens and
F. Vesca. Xie et al. [
27
] noted that colonization by the sole inoculation of AM fungus
R. intraradices
failed to stimulate the growth of the maize cultivar SY Milkytop, both in
non-saline and saline conditions. Maize root biomass inoculated solely with R. intraradices
was lower than that inoculated solely with bacteriomes. It is plausible that root growth is
induced to recruit microbes and acquire a broader range of substances from the soil with
the sole inoculation of bacteriomes.
Pons et al. [
21
] examine the impact of the arbuscular mycorrhizal fungus Rhizophagus
intraradices on plant growth, with a focus on phytohormone production. Available reports
highlight that this fungus combines the production of various phytohormones, including
auxins, cytokinins, and strigolactones, which trigger major biochemical processes, such as
root growth, absorption of nutrients, and stress reactions, thus boosting plant productivity.
Besides, the sophisticated synergy between plants and mycorrhizal fungi, complex signal-
ing routes, and phytohormones are in charge of growth promotion and bring about many
plant growth contributions along the way. Through the convergent relationship between
plants and arbuscular mycorrhizal fungus, nutrient uptake, stress tolerance, and plant
health are improved, which helps increase plant growth and hence its overall productivity.
5. Nutrient Cycling and Soil Health
Soil nutrient cycling in the soil–plant system of crops relies on the effects of agronom-
ical practices on soil conditions, especially the soil microbial population mediating soil
carbon transformation (either mineralization or stabilization), the nitrogen cycle including
soil nitrogen transformation, uptake and return from plants, and nitrogen losses, and the
fate of other elements mediating these trade-offs, including phosphorous [
28
]. AMF play
a pivotal role in the nutrient cycling processes occurring in ecosystems [
29
]. The intricate
network of mycelium that they possess facilitates the transportation and delivery of nu-
trients, particularly phosphorus, to the plant hosts. This mechanism significantly boosts
the availability of nutrients for plants, thereby enhancing their growth and utilization of
nutrients. Consequently, it creates favorable conditions for the growth of various plant
species. The mycelium network of AMF serves as a crucial link between the soil and
the roots of plants [
30
,
31
]. It extends well beyond the range of plant roots, extensively
exploring the neighboring soil in search of nutrients. Through this exploration, AMF are
able to acquire phosphorus that would otherwise remain inaccessible to plants due to its
limited mobility in soil. Subsequently, these fungi transfer these acquired nutrients directly
to their plant hosts via specialized structures known as arbuscules [
32
,
33
]. The heightened
availability of phosphorus exerts significant impacts on the growth and development of
plants, as phosphorus is an indispensable element necessary for numerous physiological
processes in plants, such as energy transfer and DNA synthesis. By facilitating the uptake
of phosphorus, AMF empower plants to divert more energy towards growth and reproduc-
tion [
34
]. Furthermore, AMF also enhance the efficiency of nutrient utilization in plants by
improving the absorption of other essential elements like nitrogen and potassium through
the expansion of root surface area using their mycelium network. As indicated in a study
by [35], this enhancement enables plants to extract a greater amount of nutrients from the
soil while minimizing losses through leaching or volatilization.
Plant root systems play a crucial role in the acquisition of nutrients and water within
various environments characterized by limited resources. Modifying the architecture of root
systems is a strategic approach adopted by the majority of terrestrial plants to optimize their
performance. Modifying the architecture of root systems is a strategic approach adopted
by the majority of terrestrial plants to optimize their performance. Various terrestrial
vegetation forms mutually beneficial relationships with arbuscular mycorrhizal fungi to
boost the absorption of nutrients effectively [10].
A notable increase in the levels of chlorophyll, an important pigment vital for pho-
tosynthesis to occur, stems directly from the heightened absorption of nitrogen aided by
Microbiol. Res. 2024,15 1035
arbuscular mycorrhizal fungi [
36
]. Moreover, the boosted supply of phosphorous in plants
facilitated by these fungi may indirectly affect photosynthesis by altering the ATP-to-ADP
ratio or regulating the action of the enzyme ribulose 1,5-bisphosphate (RuBP) carboxy-
lase [
37
]. This finding aligns with elevated levels of phosphorous discovered in seedlings,
as indicated by available data. R. intraradices is capable of improving PEPCase activity,
an essential enzyme for malate production. Malate is the final product of the photosyn-
thetic carbon reduction (PCR) cycle in C3 plants like tomatoes, emphasizing the important
contribution of R. intraradices to photosynthesis [38].
However, it is important to note that, apart from enhancing nutrients and raising
the rates of photosynthesis, other elements can affect the total improvement in survival
and quality of seedlings. Arbuscular mycorrhizal fungi are said to trigger the synthesis of
phytohormones, beyond their functions in improving the absorption of nutrients [39].
Hestrin et al. [
40
] illustrated that the interactions between the mycorrhizal fungus
Rhizophagus intraradices and soil microbial communities have a synergistic effect on nitrogen
acquisition by the model grass Brachypodium distachyon. These intricate microbial interac-
tions result in a significant non-additive enhancement in nitrogen uptake by mycorrhizal
plants from organic sources, surpassing the nitrogen acquisition of non-mycorrhizal plants
cultivated without soil microbes. This newly identified multipartite relationship could
contribute substantially to the annual assimilation of plant nitrogen, thus playing a critical
role in global nutrient cycling and ecosystem functioning. The availability of nitrogen often
limits primary productivity in terrestrial ecosystems. While arbuscular mycorrhizal fungi
enhance plant nitrogen uptake, their ability to access organic nitrogen is limited. Other
soil organisms that mineralize organic nitrogen into plant-usable forms may compete for
nitrogen, potentially affecting plant nutrition simultaneously [40].
The maintenance of soil structure is a fundamental aspect of agricultural management.
Arbuscular mycorrhizal fungi aid in the development of water-stable soil micro-aggregates
by secreting a hydrophobic glycoprotein called glomalin, which acts as a robust binding
agent. By accumulating glomalin on the external hyphal walls and surrounding soil
particles, AMF stimulates the generation of micro-aggregates that evolve into macro-
aggregates, thereby promoting soil aggregation. This results in better capability to retain
water, enhanced air circulation, expanded soil capacity, and elevated levels of organic
material content.
Arbuscular mycorrhizal fungi (AMF) play a crucial role in altering soil fertility, struc-
ture, and stability [
41
,
42
]. The enhancement of soil structure by AMF is facilitated by the
intricate interweaving of their hyphae and the secretion of glomalin-related soil protein
(GRSP), ultimately fostering the development and endurance of soil aggregates [
43
]. In
Lane Late navel orange trees, the introduction of mycorrhizal fungi into the field resulted
in varying levels of soil nutrients, contingent upon the specific AMF species involved.
For instance, D. spurca exhibited no significant impact on soil nitrate nitrogen levels but
did impede the availability of soil potassium while concurrently increasing soil Olsen-P
and ammonium nitrogen levels. Conversely, D. versiformis led to a reduction in levels of
ammonium nitrogen, nitrate nitrogen, and available potassium in the soil, while elevating
the concentrations of Olsen-P. Despite these differences, the collective effect of these AMF
inoculations was a notable enhancement in soil aggregate stability in Lane Late navel
orange trees compared to the non-AMF control group. Similarly, in Newhall navel orange
trees, the presence of D. versiformis and D. spurca resulted in heightened soil Olsen-P levels
and improved aggregate stability [
44
]. In a different context, the inoculation of vetch with
F. mosseae,D. spurca, and R. intraradices led to a significant decrease in soil Olsen-P and
available potassium levels [45].
AMF plays a vital role in improving soil structure and quality. The external hyphal
network aids in soil aggregation by establishing a framework in the mycorrhizosphere.
AMF enhances soil structure by releasing various proteinaceous and non-proteinaceous
organic compounds, with the protein glomalin being particularly efficient in binding soil
Microbiol. Res. 2024,15 1036
particles, consequently ensuring the stability of these aggregates even six months after the
network has vanished [46].
Gou et al. [
47
] performed a simulated erosion study and tested the hypothesis that
exogenous AM fungal inoculation, namely Funneliformis mosseae, alters the gene expression
and enzyme activities linked with N-cycling processes and that such change is related to N
acquisition and loss. It was carried out using treatment factors of AM fungal treatments
(control and AM fungal inoculation), crops (maize and soybean), and the slope of the plots.
The experimental plots received natural rainfall to mimic the erosion incidences. From
the findings of the experiment, the impact of AM fungi was more profound in the maize
soils than in the soybean soils. In the maize soils, AM fungi enhanced the copy numbers of
N-fixing and nitrifying genes and N cycling enzyme activity. The results showed that in the
soybean soil, AM fungi, on average, enhanced the abundance of the N-fixing gene while
reducing the nitrifying gene abundance. The interaction between the bacterial population
and the N fixing gene was positively related to N uptake, but it was inversely related
to N loss. Moreover, AM fungi amplified the responses of mycorrhizal colonization and
moisture on the microbial parameters associated with N-cycling processes but reduced the
response of the nutrients in the soil. Hence, AM fungal inoculation, thereby improving N
uptake and minimizing N loss through the stimulation of N-fixing gene abundance, should
preferably be utilized in low N conditions or in systems where N is restrictively competed.
Bukovskáet al. [
48
], in a study involving two pot experiments both involving root-
free compartments receiving 15N-labeled chitin, concluded that AM fungi were able to
transfer proportions amounting to over 20% of N in the form of chitin to their plant hosts
within 5 weeks. Moreover, the study revealed that in mycorrhizal pots, N leaching and/or
volatilization losses integrated over the time period after the addition of chitin to the soil
were significantly lower than in non-mycorrhizal pots, sometimes even being less than 50%
of the added N. In contrast to the present hypothesis, the AM fungi chitin mineralization
and N uptake rates were not slower but were at least as efficient as green manure (clover
biomass) using direct 15N labeling and tracking down the N. This efficient N recycling from
soil to plant observed in mycorrhizal pots was not much influenced by the structure of AM
fungal communities or by the environmental conditions to which plants were subjected
in the glass house, outside conditions, or under additional mineral N application. This
study has shown that, in general, AM fungi could be considered an important and stable
soil component in relation to several intricate processes occurring in soil, namely, organic
nitrogen cycling.
Zhen et al. [
49
] found that arbuscular mycorrhizal fungal colonization enhanced plant
mineral element uptake, especially phosphorous (P), both in lucerne hay (LH, C:N ratio
of 18) and sugarcane mulch (SM, C:N ratio of 78), which was not significantly affected by
water conditions in the iron (Fe) ore tailings. Symbiosis development in AM effectively
prevented the accumulation of toxic levels of the supplemented nutrients (i.e., potassium
and iron) in plant shoots by reducing their transport from root to shoot. Higher organic-care
AM fungal ability in P uptake and the station of splitting out other elements was detected
in the LH-amended tailings rather than in the SM-amended tailings. Drought reduced AM
fungal capture and processes related to elemental nutrient acquisition and distribution.
These outcomes have revealed how AM fungi produced a significant service involving the
control of plant growth plus nutrition state on Fe ore tailings technosol, which provided an
important input for the use of AM fungi in the eco-engineering of tailings into pedogenesis.
6. Environmental Restoration and Ecosystem Resilience
AMF are essential for improving the quality and health of soil through soil structure,
plant physiology, and interactions with ecological systems. These factors jointly help
to enhance plant functionality, growth, and productivity. Soil structure maintenance
is improved by the development of soil aggregates caused by glomalin production by
AMF. Physiologically, AMF changes the process of nutrient absorption, leading to an
improvement in soil fertility and productivity. By adjusting the physiological conditions of
Microbiol. Res. 2024,15 1037
a plant, AMF helps in preventing biotic (pathogens and weed plants) and abiotic (salinity,
drought, extreme temperature, soil pH, and heavy metals) challenges. AMF, as a biocontrol
agent, forms antagonistic associations with plant pathogens. AMF foster a collaborative
effect on the performance of plants by creating advantageous relationships with other
rhizosphere microorganisms and above-ground organisms [50].
A study by Sugiura et al. [
46
] showed that the arbuscular mycorrhizal (AM) fungus
Rhizophagus intraradices can grow and produce spores independently when provided
with external myristates (C:14) fatty acids. These findings challenge the conventional
belief that AMF solely rely on their hosts for fatty acids during symbiosis. Rillig et al. [
51
]
suggest that understanding the roles and functions of AM fungi on the ecosystem can
be changed if fungi can come in contact with sources of carbon such as decaying plant
material, litter, or other microbes apart from the ones from their host plants. This indicates
that AMF can interact independently with the ecosystem of the direct host plant carbon
supply through their beneficial effects on soil aggregation and carbon sequestration [
52
,
53
].
Arbuscular mycorrhization contributes to augmenting the soil organic matter content and
water-holding capacity, consequently aiding in the conservation of the soil ecosystem. The
elongated hyphae assume a crucial role in alleviating water scarcity in arid soil conditions
and diminishing evaporation [50].
Hovland et al. [
54
] stated that AMF have the potential to exert significant impacts
on the resilience of ecosystems and their ability to resist invasion in rangelands. The
maintenance of plant community structure is facilitated by AMF through various ecological
feedback mechanisms, including enhancing nutrient cycling and uptake by host plants,
contributing to the stability of soil structure both physically and chemically, and mediating
plant competition. These interactions between plants and AMF could play a crucial role
in arid environments by supporting native plant communities in coping with stressors
such as drought, grazing, and fire, while also defending against the invasion of exotic
plant species. Nevertheless, invasive exotic plants might exploit their associations with
native AMF communities, potentially leading to alterations in these communities. AMF
have been implicated as drivers of plant community composition as well as contributors to
ecosystem functionality.
7. Sustainable Agriculture and Organic Farming
Begum et al. [
18
] asserted that the efficient utilization of specific arbuscular myc-
orrhizal fungi (AMF) in relation to various crops and soils has the potential to enhance
agricultural sustainability. Consequently, AMF are progressively emerging as an indis-
pensable biological instrument for enhancing both crop yield and soil quality. Particularly
within the framework of conventional agriculture, which relies heavily on chemical inputs
and poses a threat to the sustainability of food security as well as human and ecosys-
tem well-being, the adoption of alternative agricultural practices has become imperative.
Hence, the integration of AMF has now become crucial within the realm of environmentally
friendly and natural farming techniques. Within these agricultural landscapes, there is a
notable augmentation of natural biological processes that contribute to the preservation of
soil fertility. Furthermore, crops exhibit heightened intrinsic resilience to pests and diseases
within such agroecosystems. Additionally, these ecosystems exhibit robust health, with the
soil harboring a diverse array of organisms in these agricultural settings.
Kuila and Ghosh [
55
] revealed that the escalating global human population growth, in
tandem with diminishing agricultural land, exerts substantial pressure on crop productivity,
food security, and soil health worldwide, particularly in developing countries. Unsatisfac-
tory land management practices, characterized by heavy dependence on chemical fertilizers
and agrochemicals to boost productivity, have adverse repercussions on human health, the
environment, biodiversity, and sustainability. The utilization of arbuscular mycorrhizal
fungi (AMF) as a bio-fertilizer, either in isolation or in conjunction with other beneficial
microorganisms, has emerged as a burgeoning research domain in the realms of agricul-
ture and life sciences. Prior research has illustrated the favorable impacts of AMF on the
Microbiol. Res. 2024,15 1038
nourishment, development, and yield of crops, along with enhancing soil quality, elevating
biological soil fertility, and fortifying resistance to pathogens. AMF symbionts assume a
pivotal role in bolstering plants’ tolerance to abiotic stresses. When utilized alongside other
beneficial rhizobacteria, AM can function as a feasible substitute for chemical fertilizers in
modern, sustainable organic farming systems [55].
As a bioinoculant, arbuscular mycorrhizal fungi (AMF) contribute positively to sus-
tainable agriculture by establishing symbiotic associations with numerous crop plants [
50
].
Organic agriculture represents an alternative bio-agricultural approach that ensures eco-
nomical and eco-friendly food production. The transition from conventional, high-input
agriculture to organic farming should not solely focus on achieving immediate yield parity.
Organic fertilizers are processed and utilized alongside diverse soil microbes. Imple-
menting organic farming practices with suitable microbial blends customized to specific
environmental conditions, soil attributes, and crops is imperative for ensuring yield stabil-
ity across successive seasons [
56
]. Furthermore, this approach ensures the continual fertility
of the soil and the production of safe and high-quality food products [
57
]. Using arbuscular
mycorrhizal fungi (AMF) as a bio-inoculant provides a compelling avenue that can bring
significant benefits such as sustaining the fertility of the soil, enhanced plant nutrients, and
protection, thus holding considerable promise for sustainable agriculture [58].
Table 4highlights the various benefits of Rhizophagus intraradices in promoting plant
health and sustainability.
Table 4. Benefits of Rhizophagus intraradices in promoting plant health and sustainability.
Benefits Description
Mycorrhizal Symbiosis
Arbuscular mycorrhizae, such as Rhizophagus intraradices,
substantially affect the absorption of nutrients by plants and
the growth of the root system. Mycorrhizal application
improves the consistency of crops, reduces transplant losses,
and increases the yield of numerous horticultural
crops [13,14].
Plant Growth Promotion
Inoculation with Rhizophagus intraradices improves seedling
growth, root development, and biomass. Rhizophagus
intraradices stimulates root growth, nutrient uptake, and
growth parameters under different environmental conditions.
Combined inoculation with Rhizophagus intraradices and other
microbes can increase shoot weight and photosynthetic
efficiency [2,10,22].
Nutrient Cycling
Mycorrhizal fungi such as Rhizophagus intraradices affect
photosynthesis by improving nutrient absorption by plants,
leading to changes in chlorophyll levels and the availability of
phosphorus. Arbuscular mycorrhizal fungi help in obtaining
nitrogen from organic material, affecting nitrogen cycling and
ecosystem functioning [38,40].
Environmental Restoration and
Ecosystem Resilience
Mycorrhizal fungi such as Rhizophagus intraradices play a
crucial role in soil health, plant physiology, and ecological
interactions, improving the function of plants and ecosystem
resilience. Arbuscular mycorrhizal fungi enhance soil organic
matter content and water retention, thereby preventing the
scarcity of water and improving the preservation of the soil
ecosystem [46,51].
Sustainable Agriculture and
Organic Farming
Arbuscular mycorrhizal fungi are important in sustainable
agriculture for improving plant nutrition, growth, and stress
tolerance. Mycorrhizal fungi can function as bio-fertilizers,
enhancing soil quality, fertility, and resistance to pathogens,
thereby improving organic farming practices [50,55,56].
Microbiol. Res. 2024,15 1039
8. Agro-Ecological Relevance of Glomeromycota and R. intraradices
(a)
Plant growth promotion based on nutrient solubilization and phytohormones
Arbuscular mycorrhiza fungi, particularly through species such as Rhizophagus in-
traradices, have an important contribution to the dissolution of various nutrients that are in
the soil to make them available to the plant. This is particularly the case with phosphorus,
which is an essential micronutrient that is immobilized in the soil in relatively stable forms
of organic and inorganic phosphorus. These fungi stretch greatly past the root region,
making the surface area for the uptake of these nutrients larger. They break up organic and
inorganic complex phosphorus compounds into simpler forms that plants can favorably
assimilate [
59
]. Rhizophagus intraradices also access the levels of many phytohormones,
which are organic compounds that control plant growth processes. Phytohormones such as
indole-3-acetic acid (IAA), gibberellic acid (GA), and abscisic acid (ABA) are regulated in
the presence of R. intraradices [
21
]. This fungus causes higher IAA levels, which stimulate
root elongation and branching, resulting in an increase in the surface area of the roots.
Through its influence on plant hormone regulation, the fungus helps the plant gain better
access to the soil and nutrients [
60
]. The effect of the fungal-induced ABA and GA reduction
may further assist the plant in managing stressful conditions and continuing to grow, even
under suboptimal conditions [
61
]. Rhizophagus intraradices enhances the root architecture
and improves solubilization. It also helps maintain an optimal balance of phytohormones,
a vital compound that is used in regulating the growth of plants [
2
]. R. intraradices play
a role in the formation of glomalin-related soil proteins that have a significant role in the
agglomeration forces of the soil particles. These proteins also help in the processes of
carbon and metal ion storage enhancement, which belongs to the non-negligible ecological
advantages of this symbiosis [
62
]. This is true since beneficial members of ecosystems are
known to help increase yields and contribute to overall stability. They develop the structure
of the soil due to the release of glomalin, which is a glycoprotein that helps in holding the
soil particles, thereby preventing soil erosion and enhancing water retention. This also has
consequences for carbon storage, as plants with mycorrhizal associations can store more
carbon, which helps to protect the climate [63].
(b) Mycorrhiza–plant interaction: yielding plant disease biocontrol
Glomeromycota and Rhizophagus intraradices are specific mycorrhizal fungi that can
benefit plant growth and development through enhanced nutrient uptake and defense
against diseases. Relating to disease biocontrol, mycorrhizal fungi are regarded as having
a protective function. They can improve the plant’s ability to repel numerous pathogens,
from fungi and bacteria to nematodes [64].
Mycorrhizal fungi with a network of hyphae can occupy the surface of roots in a
way that pathogens cannot easily compete for the space. They prevent pathogens from
infecting the plant roots by occupying this location and using up the nutrients needed by
the pathogens, leading to their inhibition [65].
The mutualistic mutualism between the mycorrhizal fungi and the plant results in a
systemic rearrangement of the immune system of the plant, improving its defense against
diseases [
66
]. According to Dutta and Ghosh [
67
], in addition to serving as an efficient
biofertilizer, mycorrhizae provide plants with some measure of immune system called
Mycorrhiza-Induced Resistance (MIR). This immunity is useful against most airborne and
soil-transmitted diseases. Plant receptor protein complexes, or pattern-recognition recep-
tors, detect the Effector Proteins (EP) and Microbe-Associated Molecular Patterns (MAMPs)
in mycorrhizae since these are closely linked to possible pathogens. Consequently, the
MAMP-Triggered Immunity response (MTI) is induced in plants and limits the subse-
quent penetration of pathogens. It provides short-term and long-term protection in plants
with systemic acquired resistance and induced systemic resistance. During this process,
defense-related genes become induced for various pathogens, and antipathogenic second
metabolites are synthesized. They also change plant root exudation to recruit beneficial
microbes, which also provide induced systemic resistance and form consortiums [67].
Microbiol. Res. 2024,15 1040
Fungal mycelium forms a complex, dense network around the roots and is thus
considered to be a first line of defense against pathogens. This barrier does not only arrest
the physical invasion by pathogens but also facilitates a less hostile environment for the
pathogens [
68
]. It is known that the root exudates are altered in their chemical composition
in the presence of mycorrhizal fungi. These alterations may allow for the synthesis of
products that are lethal or non-permissive to pathogens; hence, the chances of disease
establishment are eliminated [
64
]. Mycorrhizal fungi can effectively elicit plant defense
mechanisms where the plant starts to produce chemical compounds like phytoalexins,
pathogenesis-related proteins, and enzymes like chitinase and glucanase. These compounds
have the ability to protect against a range of pathogen species, offering broad-spectrum
action [69].
The mutualism underlying the interaction between mycorrhizal fungi and plants not
only enhances plant growth and health but also forms a disease management strategy.
Thus, the use of mycorrhizal fungi for biocontrol in the agro-ecological system reduces
chemical pesticide reliance, in line with sustainable agriculture. This synergy is particularly
relevant in the case of organic farming since it employs it in the case of managing plant
diseases in a natural and sustainable manner, leading to increased crop yield and minimized
ecological impact. The mycorrhizal fungi can therefore be used to highlight an integrated
pest management technique that is both efficient and sustainable.
(c) Mycorrhiza–microorganisms interaction
The hyphae of these arbuscular mycorrhizal (AM) fungi have more area for contact
with other microbes and act as a major route of transport of energy-rich plant assimilations
to the soil [
55
]. Using different AM fungi, soil leachates, and model microbial communities,
Jin et al. [
70
] described organic P conditions where AM fungi may preferentially attract
P-mobilizing bacteria to the exclusion of other types of bacteria. Standardly, they found
out that the isolate Streptomyces sp. D1 had a privileged interaction with either the carbon
source derived from the fungus, which was obtained by the bacterium capable of converting
organic P into inorganic P, or the bacterial community that lives on the surface of hyphae,
which can be at least partially controlled by the bacterium of the genus Streptomyces. This
is done mainly by limiting the activity of bacteria that have low P-mineralizing potential,
thus allowing AM fungi to access P [70,71].
Mycorrhizal helper bacteria (MHB) are a subset of those beneficial bacteria that func-
tion to improve mycorrhizal formation. These can support mycorrhizal fungi growth,
enhance the uptake of nutrients by plants, and also safeguard the plant from diseases [
72
].
Yang et al. [
73
] sampled 45 kinds of bacterial strains from the rhizosphere soil of Vaccinium
uliginosum and selected MHB strains by aiming at dry-plate confrontation and the promo-
tion of extracellular bacterial metabolites. The growth rate of Oidiodendron maius 143, an
ericoid mycorrhizal fungal strain, was enhanced by 33.33 and 77.77% for bacterial strain L6
and LM3 exposure, respectively, as revealed by the dry plate confrontation assay. Moreover,
L6 and LM3 caused a profound enhancement in the extracellular production of biomass,
which facilitated the growth of O. maius 143 mycelial filaments in other wells at a mean
growth rate of 40.9 and 57.1%, respectively. Compared with the control group, the cell
wall-degrading enzyme activities and the genes of O. maius 143 increased distinctly. In
this case, strains L6 and LM3 were considered the most probable MHB strains due to a
relatively low number of differences. Furthermore, the co-inoculated treatments resulted
in improved blueberry growth, nitrate reductase, glutamate dehydrogenase, glutamine
synthetase, and glutamate synthase activity in blueberry leaves, and enhanced nutrient ac-
quisition in blueberries. From the results of the physiological tests and the 16Sr DNA gene
molecular analysis, strain L6 was identified as Paenarthrobacter nicotinovorans and strain
LM3 was identified as Bacillus circulans. The results of the metabolomics analysis showed
that mycelial exudates provide rich substrates, including sugar, organic acid, and amino
acid, which could effectively promote the growth of MHB. Thus, the growth of L6 and LM3
and O. maius 143 is self-promoting, and the co-inoculation of L6 and LM3 and
O. maius
143
can promote the growth of blueberry seedlings and provide theoretical guidance for the
Microbiol. Res. 2024,15 1041
exploration of the mechanism of the ericoid mycorrhizal fungi-MHB-blueberry symbiotic
relationship. It provided the technical premise for the comprehensive development of
biocontrol strain resources and the formulation of biological fertilizer [73].
Berrios et al. [
74
] gathered soil cultures in Bishop pine forests over a climate-latitude
gradient of the California coast, separated the cultures based on their proximity to EcM
colonized roots, analyzed the microbial communities by amplicon sequencing, and estab-
lished linear regression models demonstrating the effect that selected bacterial phylotypes
have on the density of EcM fungi. Moreover, they used transcriptome data to confirm the
direction of these associations and to unveil which genes EcM-synergist bacteria induce
during tripartite symbioses, as well as using greenhouse experiments. According to the
outcome, ectomycorrhizas (that is, roots where the bacteria colonize) promote the presence
of conserved bacterial species across climatically diverse locales. Here, they unveiled rela-
tionships between phylogenetically distinct EcM synergists and plant and fungal growth
and reported that EcM synergists and antagonists differ in gene expression profiles. All in
all, they help define the general processes that enable diverse and expansive multipartite
symbioses, which shed light on how plants evolve within complex environments [74].
(d) Mycorrhiza–soil interaction
Yu et al. [
75
] find that both AMF infection rates and the number of AMF spore species
are increasing before emergent plants, proving that there is higher competitive mutualism
between both AMF and plants. Concentrations of carbon (C), nitrogen (N), and phospho-
rous (P) in the above-ground biomass and in the root stock and the C/N and C/P ratios
differ significantly in those four emergent plants. Furthermore, the infection frequency of
AMF positively affected the shoot N concentration, negatively affected the aboveground
and total biomass N (p< 0.05), and positively affected arbuscular mycorrhiza formation
rate and versicular formation. The rate of AMF after root infection affected root N and
root N/P. Regarding the relationship of the AMF infection characteristics with the soil
properties, total C, total N, total P, and oxidation–reduction potential (ORP) showed a
significant correlation with the parameters studied. Hence, the main conclusions drawn
from this study are that redundancy and path analysis supported the notion that the quan-
tity of soil C, N, and P and the ORP directly influenced the concentration and ratio of
these macronutrients in plants. However, it might also control the direction of change in
plant ecological stoichiometry through shifting the AMF mycorrhiza. Accordingly, our
data emphasize that both the reciprocal exchange between AMF and soil are involved in
the determination of plant ecological stoichiometry, and, therefore, these partners can be
considered to have integral properties when analyzing the interactions between plant and
soil [75].
Fall et al. [
76
] opined that AMF help to enhance fertility on the ground and that they
improve the fertility of the soils surrounding plant roots. AMF are beneficial to the soil by
synthesizing organic acids and glomalin, help prevent soil erosion, reduce binding between
heavy metals and soil particles, aid in carbon formation, and improve macroaggregation
of soil particles. AMF also attracts the bacteria that precipitate the alkaline phosphatase
mineralization, which is a soil enzyme that relates to the availability of organic phosphorus.
Besides, AMF predetermine the composition, richness, and functionality of the microbial
consortium in the soil by competing or cooperating with disparate partners. All these
activities of the AMF play a role in raising the fertility levels of the soil [76].
AMF affect the structure of the soil in a beneficial way. The AMF are located abundantly
in massive quantities in the soils [
77
]. These mycelia or hyphae have reasons for being able
to form stable elements within the structure of the soil. Mycorrhizal fungi are long-term soil
stabilizing agents, and the extra matrix mycelial structures produce a mineral-adsorbing
glycoprotein known as glomalin [
78
]. This glomalin is a hydrophobic protein that is thermo-
tolerant, which implies that the protein is able to withstand the hot temperature of the soil.
The water-repellency of the glomelin causes the stability of the water in soil aggregations,
whose synthesis reaches its maximum in senescent mycelium. The glycoprotein is slightly
more biodegradable by bacteria and fungi present in the soil, and such degradation is found
Microbiol. Res. 2024,15 1042
to occur slowly. The basic goal of glomalin is to cement the compartments of the soil [
79
,
80
],
to act as a cement that holds smaller maltese-cross micro-aggregations (diameter < 250
µ
m)
as macro-aggregations [
81
]. These soil macro-aggregations enhance better water infiltration
into the soil, reduce surface run-off, minimize soil erosion and nutrient and organic matter
losses, and increase gaseous exchange, improving water and mineral retention, especially
potassium, therefore enhancing plant growth [
82
]. These mechanisms help in avoiding
pressure on soils and ensuring soil fertility [
83
]. In the case of AMF, it can be stated
that these particles are capable of controlling soil structure based on their chemical and
biophysical potential as enmeshing and aligning agents [76].
(e) Biogeochemical cycles and mycorrhiza
Boyno et al. [
84
] aimed to provide an overall perspective on the impact of AMF and
various days between irrigation on CO
2
release, soil property, plant growth, and AMF
features. We noted that the varying irrigation intervals influenced AM symbiosis, and
the extent of this change heightened as the irrigation interval increased. It was suggested
that this AM symbiosis formed with the plant in question cut down on CO
2
emissions.
Moreover, it was established that it controls the structural stability of the soil and enhances
the health and development of plants. From the standpoint of the impact on the global
climate, it can be stated that AMF species help mitigate CO
2
emissions by conserving
water [84].
9. Genomic Research in Glomeromycota
Glomeromycota are unique in their biotrophy, which is obligate, multinucleate in
nature, with large genomes and no sexual reproduction reported. All of these aspects have,
in the past, constituted difficulties in genomic identification and alteration. Nevertheless,
due to enhanced methods of DNA sequencing techniques, little information is available on
the nuclear and mitochondrial genomes, which exhibit higher plasticity and diversification,
and their roles in these organisms [
85
]. For instance, techniques such as suppression
subtractive hybridization have been employed to depict the mechanisms of sleep and
the mitochondrial genome. As the symbiotic characteristics of the Glomeromycota can
only form AM associations with plants, the genetic determination of their specificity
remains closely associated with their capability of forming AM relationships with their
plant partners. This mutualism entails the fungi’s ability to bring nutrients like phosphorus
and nitrogen to the plant in exchange for carbon. Consequently, there are several genes
that have been proposed as being involved in this work of nutrient exchange, including
phosphate transporters and some enzymes that are involved in nitrogen trade [86].
Rosling et al. [
87
] accept three monophyletic linages (Glomeromycota, Mucoromycota,
and Mortierellomycota) as phyla. They provide a balanced taxon sampling and broad
taxonomic representation for phylogenomic analysis; they refute a hard polytomy and
place Glomeromycota in the sister group of the Mucoromycota and Mortierellomycota. The
genes involved in plant cell wall degradation that have low copies cannot be attributed
to the shift to a plant symbiotic life cycle but are likely to be an outcome of their ancestral
phylogeny. While both plant symbiotic lineages—Glomeromycota and Endogonales—are
deficient in many genes involved in thiamine metabolism, the absence of genes for fatty acid
synthesis directly affects only AM fungi. Some of these genes are absent in all the analyzed
phyla, while others can actually be found in some of the analyzed AM fungal lineages. For
instance, the high affinity phosphorus transporter Pho89 is missing in Glomeromycota but
is also absent in some phyla [87].
It has been established that Glomeromycota is one of the oldest groups of fungi that
have coevolved with land plants. New insights from the phylogenomic context provide
additional evidence that Glomeromycota is a sister group to Mucoromycota and Mortierel-
lomycota, indicating that there are two evolutionary shifts to arbuscular mycorrhiza. These
transitions were associated with a genomic context that is not representative of modern
ectomycorrhizal fungi in the phylum Dikarya. Features of obligate endosymbiosis in
Glomeromycota include the following: a low number of genes involved in plant cell wall
Microbiol. Res. 2024,15 1043
degradation as compared to other intracellular mycorrhizal fungi; this has been considered
to be ancestral and not due to symbiosis. Furthermore, the absence of specific genes in-
volved in the metabolism of thiamine has been reported in plant symbiotic groups, whereas
the deficiency of the genes required for the synthesis of fatty acids is known only in AM
fungi [87].
Other studies also show that some of the genes that Glomeromycota need to colonize
their hosts appear to have genes deleted from them, which would have enabled them to
survive without such hosts. This genomic reduction is characteristic of many symbiotic
organisms, and it is a testimony to the mutual dependence of both partners. These fungi
have developed unique structures that aid them in this process, resulting in effective and
widespread mutualism that is vital for the dynamics of the terrestrial biomes.
10. Negative Effects of AMF
In research conducted by Wang et al. [
35
], it was observed that the growth of plant
biomass showed a synergistic increase with elevated levels of both soil water and soil
nutrients. Interestingly, the introduction of arbuscular mycorrhizal fungi (AMF) resulted
in a surprising suppression of plant height, particularly evident under conditions of low
water availability. Additionally, the presence of AMF also led to a reduction in plant
biomass, specifically noticeable under circumstances of low water and nutrient levels.
Moreover, the application of AMF was found to have a significant impact on decreasing
leaf phosphorus concentrations, which were notably heightened under conditions of high
nutrient availability, while showing minimal effects on leaf chlorophyll and proline levels.
In conditions of low water and nutrient levels, there was an enhancement in the specific
root length as a result of AMF inoculation, accompanied by a decrease in the average root
diameter. The adverse effects of AMF on plant development under low water and nutrient
levels may suggest that the inoculation of AMF does not substantially contribute to the
uptake of nutrients and water under such conditions. Conversely, it is plausible that AMF
may have hindered the direct route of water and nutrient absorption by the plant roots,
despite the low levels of mycorrhizal colonization. The presence of AMF led to a decrease
in the population of the foliar herbivore Chrysolina aeruginosa on plants cultivated in low-
nutrient soil, with no significant impact on plants grown in high-nutrient soil. Interestingly,
the fertilization of plants resulted in an increase in the abundance of this herbivore, but
only in plants subjected to high water levels. The reduced presence of the herbivore on
plants with AMF could be correlated with the diminished leaf phosphorus content. This
study suggests that AMF exhibit a negative influence on the growth of Artemisia ordosica
while simultaneously reducing their attractiveness to a prevalent herbivore [35].
A research study conducted by Wang et al. [
88
] utilized benomyl to diminish myc-
orrhizal colonization of maize roots to investigate the impact of arbuscular mycorrhizal
fungi (AMF) on nitrogen (N) uptake by maize plants in both field and greenhouse settings.
The greenhouse segment of the study also examined the repercussions of benomyl on
plant N assimilation and growth in soils that were either sterilized or non-sterilized, as
benomyl’s influences on plant performance extend beyond its effects on AMF. The findings
indicated that maize treated with benomyl exhibited increased shoot N concentration and
content, resulting in higher grain production under field conditions. Moreover, greenhouse
experiments demonstrated that benomyl promoted maize growth, N concentration, and N
content in non-sterilized soil; however, it had no impact on maize biomass or N content
in sterilized soil with the addition of a microbial wash. This suggests that the enhanced
plant performance is partially attributed to the direct effects of benomyl on AMF. The study
concluded that AMF can impede N acquisition, consequently diminishing maize grain
yield in N-deficient soils [88].
Arbuscular mycorrhizal fungi (AMF) may also influence the nutrient uptake pattern,
where nutrient control from the soil may change a little, but this may not be healthy for
the host plant. This suggestion also implies that the fungi might selectively incorporate
specific nutrients, denying the plant a chance to uptake other nutrients that are essential
Microbiol. Res. 2024,15 1044
to its growth [
85
]. In the mutualistic relationship that exists between the members of this
family and fungi, the plant part is expected to supply carbohydrates to the fungi. Where
the plant is under stress or where the benefits of the relationship are negligible, the parasitic
plant may be all but a drain on the plant’s intercalary energy stores [
65
]. Some plants can
lose more in competition with other plants when forming symbiotic relationships with
AMF than others, hence competing for fewer resources. This could potentially precipitate
disturbances in biodiversity and the ecosystem portfolio. AMF themselves have no direct
known negative effect on plants; however, they can alter host soil microbial populations
and compositions. They are capable of changing the soil conditions, which may have some
impact on the number and types of other effective microorganisms within the soil [89].
Table 5summarizes the negative effects of arbuscular mycorrhizal fungi (AMF) based
on the conducted research.
Table 5. Negative effects of Rhizophagus intraradices on plant health and sustainability.
Negative Effects of AMF Description
Plant Growth Suppression
The introduction of arbuscular mycorrhizal fungi (AMF) suppresses plant height,
particularly under conditions of low water availability, as observed by Wang et al. [
35
].
AMF presence also leads to a reduction in plant biomass, specifically noticeable under
circumstances of low water and nutrient levels [35].
Root Morphology Alteration AMF inoculation enhances specific root length and decreases average root diameter,
especially at low water and nutrient levels, according to research by Wang et al. [35].
Nutrient Alteration
Wang et al. [
35
] found that AMF application decreases leaf phosphorus concentrations,
especially under conditions of high nutrient availability.
Herbivore Population Control
AMF presence decreases the population of the foliar herbivore Chrysolina aeruginosa on
plants cultivated in low-nutrient soil, as observed by Wang et al. [
35
], possibly linked
to diminished leaf phosphorus content. This contrasts with the increased abundance
observed in fertilized plants with high water levels [35].
Impaired Nitrogen Acquisition
Arbuscular mycorrhizal fungi (AMF) impede nitrogen (N) acquisition, resulting in
diminished maize grain yield in N-deficient soils, as demonstrated in field conditions
by Wang et al. [88].
11. Challenges and Future Perspectives
In the realm of conventional agrochemical-based agriculture, arbuscular mycorrhizal
(AM) fungi are underutilized due to their obstruction of symbiosis and effectiveness within
this context. The abundance of high levels of major fertilizers, specifically phosphate and
nitrogen, in addition to fungicides, pesticides, extensive tillage, and crop rotations involv-
ing nonmycorrhizal crops, act as barriers to the association, diversity, and activity of AM.
Consequently, in agricultural environments, the diversity and abundance of AM flora and
root colonization experience significant modifications and reductions in comparison to the
adjacent natural soil conditions [
89
]. A recent exploration by
Rodriguez-Morelos et al. [90]
scrutinized the impacts of four fungicides (azoxystrobin, pencycuron, flutolanil, and fen-
propimorph) at concentrations of 0.02 and 2 mg L
−1
, evaluated
in vitro
on the hyphal
branching pattern of Gigaspora sp. MUCL 52331 and Rhizophagus intraradices MUCL 41833.
Detailed observations of reparative occurrences were meticulously carried out under a
dissecting bright-field light microscope. The findings of the investigation accentuated
the exacerbated negative influence of Azoxystrobin on both AM fungi at 2 mg L
−1
, with
fenpropimorph particularly impacting R. intraradices (demonstrating stimulation at low con-
centrations and inhibition at high concentrations). Conversely, flutolanil and pencycuron
did not exhibit any noteworthy effects on either of the two AM fungi.
Kuyper and Jansa [
91
] posit that there are prevailing generalizations concerning AM
symbiosis that are robustly supported by numerous research initiatives. Nevertheless, they
acknowledge the potential presence of a geographic bias in mycorrhizal studies, which
has predominantly developed within temperate and boreal regions. They propose that
Microbiol. Res. 2024,15 1045
investigations carried out in alternative ecological contexts may reveal a wider range of
feasible mycorrhizal and non-mycorrhizal strategies than presently acknowledged. Addi-
tionally, there is a discernible tendency towards excessive data interpretation, which could
potentially obstruct the progression of certain research fields by disregarding experimental
frameworks aimed at elucidating the fundamental principles of processes in preference for
accumulating descriptive observations and correlational evidence.
Zhang et al. [
2
] revealed several problems in the study of the AMF effects on plant
interactions in the presence of arsenic-contaminated soil conditions. These problems include
identifying the actual mechanisms of action of AMF that result in improved nutrition
and tolerance of plants to arsenic stress, considering the distribution of plant species
responses to inoculation, finding the most practical way to use phytoremediation and
crop productivity, and sustaining agriculture in regions where arsenic toxicity is present.
The frame of future perspectives is as follows: AMF serve as a biotechnological tool that
improves plant performance in contaminated environments; the functions of AMF in
enhancing plants’ resistance to various environmental stresses are investigated; the results
of omics approaches are used for the understanding of molecular pathways involved in
the interaction of AMF with plants; and lastly, stakeholders and policymakers cooperate to
apply AMF strategies for environmental Considering AMF’s potential benefits, ongoing
research and innovation must keep up with that to take advantage of this tool for sustainable
agriculture and environmental protection in arsenic-contaminated territories. The study
by Pons et al. [
21
] also unfolds one of the little-known sides of the world of fungi: the
fungal synthesis of phytohormones, a process that was earlier either neglected or studied
indirectly under “indirect assays”. The distinctiveness of the interaction makes it imperative
to carry out the studies directly and comprehensively to properly quantify the extent
of the fungus’s role in hormone production. Considering the situation, decoding the
molecular language and signal routes of the seasonal, persistent symbiotic link between
fungi and plants is a signal of an open road to search for answers. The complexity of
hormone biosynthesis and perception ways in these fungi involves understanding the
greater extent of the ongoing process that occurs over some time. Thus, the pathways
are seen as they evolve into a shared language. Also, the detailed confirmation of the
function of different stimulator hormones arising from the arbuscular mycorrhizal fungi
in the plant-fungus interaction and promotion of plant growth could be a milestone for
the newly developed mycorrhizal-assisted strategies to boost plant productivity using the
symbiotic association with the friendly fungi. However, challenges in investigating the
production of phytohormones through yeast research remain. Nevertheless, the potential
of the future in terms of maximizing our understanding of plant-fungal interactions, as well
as the possibility of exploiting these relationships for agricultural and crop enhancement, is
something that researchers need to consider.
12. Conclusions
Rhizophagus intraradices and other AMF present possible alternatives for both sustain-
able agriculture production and soil ecological preservation. They have the potential to
enhance the natural soil structure or the cycling of nutrients while also stimulating the
growth of plants, and thus afford organic farming systems with the bi-fertilizers that they
need. While chemical inputs and specific geographical limitations to relevant research take
place, integrating AMF into agriculture practice provides for long-term soil fertility, better
crop productivity, and food security. However, there is a need for additional study and
implementation of AMF-driven conservancies to ensure that we take advantage of the full
potential of these beneficial agents in our ecological agriculture.
Author Contributions: Conceptualization, A.A.A. and H.N.O.; methodology, A.A.A.; writing—
original draft preparation, A.A.A., H.N.O., V.A.A. and K.F.S.; writing—review and editing, A.A.A.
and H.N.O. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Microbiol. Res. 2024,15 1046
Institutional Review Board Statement: Not applicable.
Data Availability Statement: Data are contained within the article.
Conflicts of Interest: The authors declare no conflicts of interest.
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