METABOLITOS SINTETIZADOS
EN LA SIMBIOSIS MICORRÍCICA:
DE LA RAÍZ A LAS PARTES AÉREAS
METABOLITES SYNTHESIZED IN THE MYCORRHIZAL
SYMBIOSIS: FROM THE ROOT TO THE AERIAL PARTS
Kena Casarrubias Castillo
Universidad de Guadalajara, México
Marco Miguel Plancarte de la Torre
Universidad de Guadalajara, México
Ernesto Ramírez Briones
Universidad de Guadalajara, México
Julia Zañudo Hernández
Universidad de Guadalajara, México
pág. 2981
DOI: https://doi.org/10.37811/cl_rcm.v10i3.24283
Metabolitos Sintetizados en la Simbiosis Micorrícica: De la Raíz a las
Partes Aéreas
Kena Casarrubias Castillo1
kena.casarrubias@academicos.udg.mx
https://orcid.org/0000-0003-1831-8642
Universidad de Guadalajara
Centro Universitario de Ciencias Biológicas y
agropecuarias
Departamento de Ecología Aplicada
México
Marco Miguel Plancarte de la Torre
marco.plancarte@academicos.udg.mx
https://orcid.org/0000-0003-1831-8642
Universidad de Guadalajara.
Centro Universitario de
Ciencias Biológicas y agropecuarias
Departamento de Ecología Aplicada
México
Ernesto Ramírez Briones
ernestor.briones@academicos.udg.mx
https://orcid.org/0000-0002-1428-2542
Universidad de Guadalajara
México
Julia Zañudo Hernández
julia.zanudo@academicos.udg.mx
https://orcid.org/0000-0002-0834-6626
Universidad de Guadalajara
México
RESUMEN
Los hongos micorrícicos arbusculares (HMA) forman la asociación simbiótica más frecuente (80%)
con las raíces de las plantas terrestres. Esta relación se establece mediante un diálogo de señalización
que comienza en el suelo, induciendo cambios fisiológicos en toda la planta. Tras el contacto físico
entre las hifas fúngicas y la raíz, los HMA desarrollan estructuras especializadas dentro de las células
corticales. Posteriormente, la colonización interna del hongo facilita el intercambio de nutrientes entre
ambos organismos. Hace tres décadas, se descubrió que la inoculación con HMA aumenta los niveles
de ciertos aminoácidos y proteínas solubles, lo que demuestra que esta asociación simbiótica altera
significativamente el metabolismo de la planta. Durante la simbiosis, los compuestos sintetizados como
respuesta defensiva a la presencia del hongo pueden inducir cambios en los metabolitos secundarios y
los compuestos bioactivos en diversos tejidos vegetales. Esta revisión describe cómo se activan los
metabolitos en respuesta a los HMA, así como su función ante estímulos adicionales como el estrés
abiótico y biótico.
Palabras clave: hongos micorrícicos arbusculares; estrés; metabolitos
1 Autor principal.
Correspondencia: julia.zanudo@academicos.udg.mx
DOI: https://doi.org/10.37811/cl_rcm.v10i3.24283
Metabolitos Sintetizados en la Simbiosis Micorrícica: De la Raíz a las
Partes Aéreas
Kena Casarrubias Castillo1
kena.casarrubias@academicos.udg.mx
https://orcid.org/0000-0003-1831-8642
Universidad de Guadalajara
Centro Universitario de Ciencias Biológicas y
agropecuarias
Departamento de Ecología Aplicada
México
Marco Miguel Plancarte de la Torre
marco.plancarte@academicos.udg.mx
https://orcid.org/0000-0003-1831-8642
Universidad de Guadalajara.
Centro Universitario de
Ciencias Biológicas y agropecuarias
Departamento de Ecología Aplicada
México
Ernesto Ramírez Briones
ernestor.briones@academicos.udg.mx
https://orcid.org/0000-0002-1428-2542
Universidad de Guadalajara
México
Julia Zañudo Hernández
julia.zanudo@academicos.udg.mx
https://orcid.org/0000-0002-0834-6626
Universidad de Guadalajara
México
RESUMEN
Los hongos micorrícicos arbusculares (HMA) forman la asociación simbiótica más frecuente (80%)
con las raíces de las plantas terrestres. Esta relación se establece mediante un diálogo de señalización
que comienza en el suelo, induciendo cambios fisiológicos en toda la planta. Tras el contacto físico
entre las hifas fúngicas y la raíz, los HMA desarrollan estructuras especializadas dentro de las células
corticales. Posteriormente, la colonización interna del hongo facilita el intercambio de nutrientes entre
ambos organismos. Hace tres décadas, se descubrió que la inoculación con HMA aumenta los niveles
de ciertos aminoácidos y proteínas solubles, lo que demuestra que esta asociación simbiótica altera
significativamente el metabolismo de la planta. Durante la simbiosis, los compuestos sintetizados como
respuesta defensiva a la presencia del hongo pueden inducir cambios en los metabolitos secundarios y
los compuestos bioactivos en diversos tejidos vegetales. Esta revisión describe cómo se activan los
metabolitos en respuesta a los HMA, así como su función ante estímulos adicionales como el estrés
abiótico y biótico.
Palabras clave: hongos micorrícicos arbusculares; estrés; metabolitos
1 Autor principal.
Correspondencia: julia.zanudo@academicos.udg.mx
pág. 2982
Metabolites Synthesized in the Mycorrhizal Symbiosis: From the Root to
the Aerial Parts
ABSTRACT
Arbuscular mycorrhizal fungi (AMF) form the most prevalent symbiotic association (80%) with the
roots of terrestrial plants. This relationship is established through a signaling dialogue that begins in the
soil, inducing physiological changes across the plant. Upon physical contact between fungal hyphae
and the root, AMF develop specialized structures within the cortical cells. Subsequently, internal fungal
colonization facilitates the exchange of nutrients between both organisms. Three decades ago, it was
discovered that AMF inoculation increases levels of certain amino acids and soluble proteins,
demonstrating that this symbiotic association significantly alters plant metabolism. During symbiosis,
compounds synthesized as a defense response to the fungal presence can induce changes in secondary
metabolites and bioactive compounds throughout various plant tissues. This review describes how
metabolites are activated in response to AMF, as well as their role under additional stimuli such as
abiotic and biotic stress.
Keywords: arbuscular mycorrhizal fungi; stress; metabolites
Artículo recibido 25 abril 2026
Aceptado para publicación: 25 mayo 2026
Metabolites Synthesized in the Mycorrhizal Symbiosis: From the Root to
the Aerial Parts
ABSTRACT
Arbuscular mycorrhizal fungi (AMF) form the most prevalent symbiotic association (80%) with the
roots of terrestrial plants. This relationship is established through a signaling dialogue that begins in the
soil, inducing physiological changes across the plant. Upon physical contact between fungal hyphae
and the root, AMF develop specialized structures within the cortical cells. Subsequently, internal fungal
colonization facilitates the exchange of nutrients between both organisms. Three decades ago, it was
discovered that AMF inoculation increases levels of certain amino acids and soluble proteins,
demonstrating that this symbiotic association significantly alters plant metabolism. During symbiosis,
compounds synthesized as a defense response to the fungal presence can induce changes in secondary
metabolites and bioactive compounds throughout various plant tissues. This review describes how
metabolites are activated in response to AMF, as well as their role under additional stimuli such as
abiotic and biotic stress.
Keywords: arbuscular mycorrhizal fungi; stress; metabolites
Artículo recibido 25 abril 2026
Aceptado para publicación: 25 mayo 2026
pág. 2983
INTRODUCTION
Arbuscular mycorrhizal fungi (AMF) symbiosis is the most widespread among land plants;
approximately 80% of species establish this association. Indeed, it is believed that terrestrial plant life
was made possible by this symbiosis (Selosse & Le Tacon, 1998; Redecker et al., 2000; Brundrett,
2009; Wang et al., 2010). Root colonization by AMF alters plant physiology and the production of
phytohormones. Both partners interact through a molecular dialogue initiated by physical interaction in
the soil.
Strigolactones are plant hormones identified as root-exuded signals recognized by AMF. Upon
perceiving these signals, fungal hyphae begin to expand to facilitate root contact. The fungus then
produces chitin oligomers (CO) and lipo-chito-oligosaccharides (LCO), which act as signals to induce
changes in calcium levels and gene expression within the plant. Receptors with lysin-motifs (LysM) are
required for successful mycorrhization; these receptors are also involved in the perception of LCOs
derived from fungal cell walls. This mechanism helps plants discriminate endosymbionts from
pathogenic microorganisms using structurally related LCOs and COs (Gough & Cullimore, 2011;
Oldroyd, 2013; Rush et al., 2020).
Among strigolactones are the so-called "branching factors" (Buee et al., 2000) that trigger CO
production (Genre et al., 2013). However, the specific structure of strigolactones depends on the plant
species and its interaction with the fungal species (Kee et al., 2023). For example, in Eustoma
grandiflorum (Gentianaceae), the monoterpene glycosides gentiopicroside and swertiamarin were
found in response to gibberellin (GA) treatment. These compounds stimulate hyphal branching in
Rhizophagus irregularis and R. clarus (Glomerales) but do not induce branching in Gigaspora
margarita (Diversisporales) (Tominaga et al., 2023).
When the fungal hyphae and plant root make physical contact, AMF develop structures within the inner
cortical cells. The hyphae then form tree-like structures called arbuscules, which serve as the physical
site for nutrient exchange: the plant receives phosphorus (P) and nitrogen (N), while the fungus receives
carbon (C) from the host.
Approximately 30 years ago, it was discovered that certain amino acids and soluble proteins increased
following AMF inoculation in soybean, maize, and tobacco plants (Pacovsky, 1989; Dumas et al., 1990;
INTRODUCTION
Arbuscular mycorrhizal fungi (AMF) symbiosis is the most widespread among land plants;
approximately 80% of species establish this association. Indeed, it is believed that terrestrial plant life
was made possible by this symbiosis (Selosse & Le Tacon, 1998; Redecker et al., 2000; Brundrett,
2009; Wang et al., 2010). Root colonization by AMF alters plant physiology and the production of
phytohormones. Both partners interact through a molecular dialogue initiated by physical interaction in
the soil.
Strigolactones are plant hormones identified as root-exuded signals recognized by AMF. Upon
perceiving these signals, fungal hyphae begin to expand to facilitate root contact. The fungus then
produces chitin oligomers (CO) and lipo-chito-oligosaccharides (LCO), which act as signals to induce
changes in calcium levels and gene expression within the plant. Receptors with lysin-motifs (LysM) are
required for successful mycorrhization; these receptors are also involved in the perception of LCOs
derived from fungal cell walls. This mechanism helps plants discriminate endosymbionts from
pathogenic microorganisms using structurally related LCOs and COs (Gough & Cullimore, 2011;
Oldroyd, 2013; Rush et al., 2020).
Among strigolactones are the so-called "branching factors" (Buee et al., 2000) that trigger CO
production (Genre et al., 2013). However, the specific structure of strigolactones depends on the plant
species and its interaction with the fungal species (Kee et al., 2023). For example, in Eustoma
grandiflorum (Gentianaceae), the monoterpene glycosides gentiopicroside and swertiamarin were
found in response to gibberellin (GA) treatment. These compounds stimulate hyphal branching in
Rhizophagus irregularis and R. clarus (Glomerales) but do not induce branching in Gigaspora
margarita (Diversisporales) (Tominaga et al., 2023).
When the fungal hyphae and plant root make physical contact, AMF develop structures within the inner
cortical cells. The hyphae then form tree-like structures called arbuscules, which serve as the physical
site for nutrient exchange: the plant receives phosphorus (P) and nitrogen (N), while the fungus receives
carbon (C) from the host.
Approximately 30 years ago, it was discovered that certain amino acids and soluble proteins increased
following AMF inoculation in soybean, maize, and tobacco plants (Pacovsky, 1989; Dumas et al., 1990;
pág. 2984
Charest et al., 1993), demonstrating that this symbiotic association alters plant metabolism. A
metabolome analysis represents the physiological status of the plant and provides a comprehensive view
of the adaptive capacities conferred by the plasticity of each species (Sardans et al., 2011).
During mycorrhizal symbiosis, compounds typically associated with defensive responses to fungal
colonization are synthesized. These signaling mechanisms between the host plant and fungi may induce
changes in secondary metabolite content, as well as specific bioactive compounds in fruits, leaves,
shoots, and roots (Table 1). Understanding the dynamics of specialized metabolites within the
mutualistic or parasitic AMF relationship offers deeper molecular insight into this symbiosis. These
molecules play a significant role in all stages of the process, from spore germination and hyphal
branching to the establishment of a functional association (Akiyama et al., 2005; Genre et al., 2013).
Table 1. Metabolites that have been investigated for single AMF effects and/or upon biotic-abiotic.
Specie Fungal specie Tissue Metabolite Analytical
method
Reference
Libidibia ferrea C. etunicatum Leaves Gallic acid HPLC-PDA (Queiroz et al.,
2014)
Ocimum
basilicum
G. intraradices
G. etunicatum
G. fasciculatum1
Aerial parts Linalool,
Eugenol, Ocimene, Methyl
chavicol, Farnesol and
Humulene
GC
UFC
(Rasouli-
sadaghiani et
al., 2010b)
Artemisia annua G. macrocarpum
G. fasciculatum1
Leaves Artemisinin HLPC (Evelin and
Kapoor, 2014)
Anadenanthera
colubrine
G. albida
A. longula
Leaves Carbohydrates, Flavonoids,
Phenolics and Tannins
Spectrophoto
meter
(Pedone-
bonfim et al.,
2012)
Ocimum
basilicum
G. caledonium1
G. mosseae
Shoots3
Roots
Rosmarinic acid and Caffeic
acid
HLPC (Toussaint et
al., 2007)
Hypericum
perforatum
R. intraradices
F. mosseae2
AMF mix
(G. constrictum,
G. geosporum,
F. mosseae, and
R. intraradices)
Shoots Hypericin and
Pseudohypericin
HPLC-FLD,
HPLC-DAD
(Zubek et al.,
2012)
Inula ensifolia G. intraradices3
G. clarum1
Roots
Shoots3
Thymol derivatives NMR
MS
(Zubek et al.,
2010)
Cynara
scolymus
G. intraradices1
G. mosseae
Leaves
Flowers
Phenolic content and
Antioxidant activity
spectrophoto
meter.
(Ceccarelli et
al., 2010)
Arnica montana G. geosporum
G. constrictum
G. intraradices1
Mixture thereof and
G. mosseae
Shoots
Roots2
Sesquiterpene lactones UV spectra
HPLC-DAD
MS-API-ESI
(Jurkiewicz et
al., 2010)
Leaves Phenolic content
Vitis vinifera G. mosseae1
G. fasciculatum
G. intraradices
Mixture thereof
Leaves
Roots2
Phenol content UV
spectrophoto
metry
HPLC
(Eftekhari et
al., 2012)
Leaves
Stem
Flavonoid quercetin
Charest et al., 1993), demonstrating that this symbiotic association alters plant metabolism. A
metabolome analysis represents the physiological status of the plant and provides a comprehensive view
of the adaptive capacities conferred by the plasticity of each species (Sardans et al., 2011).
During mycorrhizal symbiosis, compounds typically associated with defensive responses to fungal
colonization are synthesized. These signaling mechanisms between the host plant and fungi may induce
changes in secondary metabolite content, as well as specific bioactive compounds in fruits, leaves,
shoots, and roots (Table 1). Understanding the dynamics of specialized metabolites within the
mutualistic or parasitic AMF relationship offers deeper molecular insight into this symbiosis. These
molecules play a significant role in all stages of the process, from spore germination and hyphal
branching to the establishment of a functional association (Akiyama et al., 2005; Genre et al., 2013).
Table 1. Metabolites that have been investigated for single AMF effects and/or upon biotic-abiotic.
Specie Fungal specie Tissue Metabolite Analytical
method
Reference
Libidibia ferrea C. etunicatum Leaves Gallic acid HPLC-PDA (Queiroz et al.,
2014)
Ocimum
basilicum
G. intraradices
G. etunicatum
G. fasciculatum1
Aerial parts Linalool,
Eugenol, Ocimene, Methyl
chavicol, Farnesol and
Humulene
GC
UFC
(Rasouli-
sadaghiani et
al., 2010b)
Artemisia annua G. macrocarpum
G. fasciculatum1
Leaves Artemisinin HLPC (Evelin and
Kapoor, 2014)
Anadenanthera
colubrine
G. albida
A. longula
Leaves Carbohydrates, Flavonoids,
Phenolics and Tannins
Spectrophoto
meter
(Pedone-
bonfim et al.,
2012)
Ocimum
basilicum
G. caledonium1
G. mosseae
Shoots3
Roots
Rosmarinic acid and Caffeic
acid
HLPC (Toussaint et
al., 2007)
Hypericum
perforatum
R. intraradices
F. mosseae2
AMF mix
(G. constrictum,
G. geosporum,
F. mosseae, and
R. intraradices)
Shoots Hypericin and
Pseudohypericin
HPLC-FLD,
HPLC-DAD
(Zubek et al.,
2012)
Inula ensifolia G. intraradices3
G. clarum1
Roots
Shoots3
Thymol derivatives NMR
MS
(Zubek et al.,
2010)
Cynara
scolymus
G. intraradices1
G. mosseae
Leaves
Flowers
Phenolic content and
Antioxidant activity
spectrophoto
meter.
(Ceccarelli et
al., 2010)
Arnica montana G. geosporum
G. constrictum
G. intraradices1
Mixture thereof and
G. mosseae
Shoots
Roots2
Sesquiterpene lactones UV spectra
HPLC-DAD
MS-API-ESI
(Jurkiewicz et
al., 2010)
Leaves Phenolic content
Vitis vinifera G. mosseae1
G. fasciculatum
G. intraradices
Mixture thereof
Leaves
Roots2
Phenol content UV
spectrophoto
metry
HPLC
(Eftekhari et
al., 2012)
Leaves
Stem
Flavonoid quercetin
pág. 2985
Solanum
lycopersicum
R. irregularis
F. mosseae
Roots Ferulic acid, Cumaryl alcohol,
Coniferyl alcohol,
Benzylisoquinoline Alkaloids,
Spermidine,
Triferuloyl spermidine,
Products derived from the
oxylipin pathway and Amino
acids3
(Tryptophan, Tyrosine,
Phenylalanine, Alanine, and
Leucine)
HPLC
LC–ESI Q-
TOF MS
(Rivero et al.,
2015)
Triticum durum
Desf
AMF Mix
(S. calospora,
A. laevis,
G. aggregatum,
R. irregulare,
F. mosseae,
G. fasciculatum,
G. etunicatum,
G. deserticola, and G.
margarita)
PGPR+AMF1
Roots Amino acids3
(Glutamic acid, Alanine,
Asparagine and
Phenylalanine) and
Fatty acids3
GC-TOF-MS
HILIC-Q-
TOF-MS
(Saia et al.,
2015)
Lotus japonicus G. mosseae Source
leaves
Sink leaves
Amino acid metabolism3
(Glutamic acid, Aspartic acid,
Glycine, Asparagine, 4-
aminobutanoic acid, 2-methyl-
malic acid)
Organic acids3
(Malic acid, Citric acid and
Succinic acid)
Kestose, Xylitol and Myo-
inositol
GC–MS (Fester et al.,
2011)
Salix purpurea R. irregularis Leaves Amino acids3, Carbohydrates3
Coumaroylquinate,
Caffeoyl-shikimate,
OPC6-CoA, trans-2-enoyl-
OPC6-CoA,
JA, Iso-JA,
Pinostrobin, Isoformononetin,
Rutin, Luteolin-7-O-
glucoside,
Porphyrin, Chlorophyll,
Phenolic glycosides and
Terpenoids
MS
H NMR
(Aliferis et al.,
2015a)
Zea mays G. intraradices Leaves Amino acids3
Organic acids, Lipids, Fatty
acids, Carotenoids,
Antioxidants, Carbohydrates,
α- amyrin and β-amyrin
ICP-MS
LC-MS
HPLC
(Gerlach et al.,
2015a)
Solanum
lycopersicum
R. irregularis
F. mosseae
Roots Ferulic acid, Cumaryl alcohol,
Coniferyl alcohol,
Benzylisoquinoline Alkaloids,
Spermidine,
Triferuloyl spermidine,
Products derived from the
oxylipin pathway and Amino
acids3
(Tryptophan, Tyrosine,
Phenylalanine, Alanine, and
Leucine)
HPLC
LC–ESI Q-
TOF MS
(Rivero et al.,
2015)
Triticum durum
Desf
AMF Mix
(S. calospora,
A. laevis,
G. aggregatum,
R. irregulare,
F. mosseae,
G. fasciculatum,
G. etunicatum,
G. deserticola, and G.
margarita)
PGPR+AMF1
Roots Amino acids3
(Glutamic acid, Alanine,
Asparagine and
Phenylalanine) and
Fatty acids3
GC-TOF-MS
HILIC-Q-
TOF-MS
(Saia et al.,
2015)
Lotus japonicus G. mosseae Source
leaves
Sink leaves
Amino acid metabolism3
(Glutamic acid, Aspartic acid,
Glycine, Asparagine, 4-
aminobutanoic acid, 2-methyl-
malic acid)
Organic acids3
(Malic acid, Citric acid and
Succinic acid)
Kestose, Xylitol and Myo-
inositol
GC–MS (Fester et al.,
2011)
Salix purpurea R. irregularis Leaves Amino acids3, Carbohydrates3
Coumaroylquinate,
Caffeoyl-shikimate,
OPC6-CoA, trans-2-enoyl-
OPC6-CoA,
JA, Iso-JA,
Pinostrobin, Isoformononetin,
Rutin, Luteolin-7-O-
glucoside,
Porphyrin, Chlorophyll,
Phenolic glycosides and
Terpenoids
MS
H NMR
(Aliferis et al.,
2015a)
Zea mays G. intraradices Leaves Amino acids3
Organic acids, Lipids, Fatty
acids, Carotenoids,
Antioxidants, Carbohydrates,
α- amyrin and β-amyrin
ICP-MS
LC-MS
HPLC
(Gerlach et al.,
2015a)
pág. 2986
Hordeum
vulgare
AMF mix
(G. mosseae and
G. intraradices)
Leaves Sucrose3,
Amino acids3
(Glutamic acid and Aspartate),
Chlorophyll3, Lutein3, and
Glutathione3
Free hexoses (3PGA,
PEP, RuBP, Glc1P),
Free inorganic phosphate and
Carboxylates isocitrate and
malate
ESI-MS
ion exchange
chromatograp
hy
HPLC
Spectrophoto
meter
(Kogel et al.,
2010)
Medicago
truncatula
R. irregularis Roots Amino acids
(Glutamic acid, Aspartic acid,
and Asparagine)
Trehalose, Palmitic acid, Oleic
acids, Cyclohexanone,
Mycorradicin derivatives,
Daidzein, ononin,
Malonylononin
cyclohexanone, Mycorradicin
derivatives,
Glucosides of blumenol C,
13-hydroxyblumenol C,
Malonyl conjugates and
Tyrosol
GC–MS
HPLC
LC–MS.
(Schliemann
et al., 2008)
Medicago
truncatula
R. irregularis Roots Propionyl carnitines,
Butyryl carnitines,
13-hydroxylblumenol C 9-O-
β-malonylglucoside,
blumenol C 9-O-β-
malonylglucoside,
Daidzein, Ononin and
Malonylononin
UHPLC–HR–
MS
MS-Q-TOF
(Laparre et al.,
2014)
Lotus japonicus R. irregularis Roots glucosylceramide,
dihexosylceramide,
inositolphosphorylceramide,
palmitic acid,
palmitvaccenic acid,
free sterols, sterol esters, sterol
glucosides, acylated sterol
glucosides
palmitvaccenic (di-16:1)2
tetracosanoic (24:1) acyl
groups2
MS/MS Q-
TOF
TLC
GC
HPL
(Wewer et al.,
2014)
Extraradical
mycelium
palmitvaccenic (di-16:1) and
tetracosanoic (24:1) acyl
groups
Solanum
lycopersicum
G. mosseae Fruits Amino acids
(Glutamine and asparagine)
and
GC-MS (Zouari et al.,
2014)
Veronica
chamaedrys
R. irregularis Leaves Sugar alcohol mannitol GC–MS
LC-MS
GC-DSQII
(Schweiger et
al., 2014)
Medicago
truncatula
Leaves Pinitol,
Ononitol,
Hordeum
vulgare
AMF mix
(G. mosseae and
G. intraradices)
Leaves Sucrose3,
Amino acids3
(Glutamic acid and Aspartate),
Chlorophyll3, Lutein3, and
Glutathione3
Free hexoses (3PGA,
PEP, RuBP, Glc1P),
Free inorganic phosphate and
Carboxylates isocitrate and
malate
ESI-MS
ion exchange
chromatograp
hy
HPLC
Spectrophoto
meter
(Kogel et al.,
2010)
Medicago
truncatula
R. irregularis Roots Amino acids
(Glutamic acid, Aspartic acid,
and Asparagine)
Trehalose, Palmitic acid, Oleic
acids, Cyclohexanone,
Mycorradicin derivatives,
Daidzein, ononin,
Malonylononin
cyclohexanone, Mycorradicin
derivatives,
Glucosides of blumenol C,
13-hydroxyblumenol C,
Malonyl conjugates and
Tyrosol
GC–MS
HPLC
LC–MS.
(Schliemann
et al., 2008)
Medicago
truncatula
R. irregularis Roots Propionyl carnitines,
Butyryl carnitines,
13-hydroxylblumenol C 9-O-
β-malonylglucoside,
blumenol C 9-O-β-
malonylglucoside,
Daidzein, Ononin and
Malonylononin
UHPLC–HR–
MS
MS-Q-TOF
(Laparre et al.,
2014)
Lotus japonicus R. irregularis Roots glucosylceramide,
dihexosylceramide,
inositolphosphorylceramide,
palmitic acid,
palmitvaccenic acid,
free sterols, sterol esters, sterol
glucosides, acylated sterol
glucosides
palmitvaccenic (di-16:1)2
tetracosanoic (24:1) acyl
groups2
MS/MS Q-
TOF
TLC
GC
HPL
(Wewer et al.,
2014)
Extraradical
mycelium
palmitvaccenic (di-16:1) and
tetracosanoic (24:1) acyl
groups
Solanum
lycopersicum
G. mosseae Fruits Amino acids
(Glutamine and asparagine)
and
GC-MS (Zouari et al.,
2014)
Veronica
chamaedrys
R. irregularis Leaves Sugar alcohol mannitol GC–MS
LC-MS
GC-DSQII
(Schweiger et
al., 2014)
Medicago
truncatula
Leaves Pinitol,
Ononitol,
pág. 2987
Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and Isocitrate)
uHPLC-ToF-
MS
Plantago
lanceolata and
Plantago major
Leaves Sorbitol,
Catalpol (only in P. lanceolata)
Plantago
lanceolata,
Plantago major
and
Veronica
chamaedrys
Leaves Aucubin and Verbascoside
Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and isocitrate)
Poa annua Leaves Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and isocitrate)
Plantago
lanceolata and
fungivores
treatmen
(Folsomia
candida)
G. intraradices1
G. custos2
Mixture thereof
Shoots Catalpol3, Verbascoside
and Aucubin2
HPLC (Duhamel et
al., 2013)
Roots Catalpol,2 Verbascoside3 and
Aucubin2
Hyphae Catalpol
Plantago
lanceolata
G. intraradices Roots Aucubin HPLC (Kempel et al.,
2010)
Plantago
lanceolata
G. intraradices Roots Aucubin HPLC (De Deyn et
al., 2009)
Medicago
truncatula
and Medicago
truncatula
mutant mtha1-22
G. intraradices Leaves Phosphate, Sulfate,
Nitrate, Citrate, Fumarate and
Chloride
HPAE (Hubberten et
al., 2015)
Solanum
lycopersicum
G. mosseae1
G. intraradices
Roots OPDA, JA-Ile and SA UPLC-MS (López-Ráez
et al., 2010)
Olea europaea G. intraradices Leaves α-linolenic acid (C18:3ω3 GC (Mechri et al.,
2014)
Trigonella
foenumgraecum
G. intraradices Leaves
Roots
Antioxidant capacity
Ascorbic acid, α-tocopherol,
Glutathione, and Carotenoids
spectrophoto
meter
(Evelin and
Kapoor, 2014)
Solanum
lycopersicum
G. mosseae Roots Antioxidant capacity and
Malonaldehyde2
spectrophoto
meter
( ZhongQun
et al., 2007)
Solanum
lycopersicum
G. intraradices Shoots Proline and
Reactive oxygen species
spectrophoto
meter
(Hajiboland et
al., 2010)
Cajanus cajan G. mosseae Roots
Shoots
Proline and
Glycine betaine
spectrophoto
meter
(Garg and
Manchanda,
2009)
Zea mays Other AMF
G. etunicatum1
G. intraradices1
Leaves Proline,
Malondialdehyde and
Soluble sugar
spectrophoto
meter
(Chen et al.,
2014)
Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and Isocitrate)
uHPLC-ToF-
MS
Plantago
lanceolata and
Plantago major
Leaves Sorbitol,
Catalpol (only in P. lanceolata)
Plantago
lanceolata,
Plantago major
and
Veronica
chamaedrys
Leaves Aucubin and Verbascoside
Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and isocitrate)
Poa annua Leaves Organic acids3 (Citrate,
Malate, Fumarate, Succinate
and isocitrate)
Plantago
lanceolata and
fungivores
treatmen
(Folsomia
candida)
G. intraradices1
G. custos2
Mixture thereof
Shoots Catalpol3, Verbascoside
and Aucubin2
HPLC (Duhamel et
al., 2013)
Roots Catalpol,2 Verbascoside3 and
Aucubin2
Hyphae Catalpol
Plantago
lanceolata
G. intraradices Roots Aucubin HPLC (Kempel et al.,
2010)
Plantago
lanceolata
G. intraradices Roots Aucubin HPLC (De Deyn et
al., 2009)
Medicago
truncatula
and Medicago
truncatula
mutant mtha1-22
G. intraradices Leaves Phosphate, Sulfate,
Nitrate, Citrate, Fumarate and
Chloride
HPAE (Hubberten et
al., 2015)
Solanum
lycopersicum
G. mosseae1
G. intraradices
Roots OPDA, JA-Ile and SA UPLC-MS (López-Ráez
et al., 2010)
Olea europaea G. intraradices Leaves α-linolenic acid (C18:3ω3 GC (Mechri et al.,
2014)
Trigonella
foenumgraecum
G. intraradices Leaves
Roots
Antioxidant capacity
Ascorbic acid, α-tocopherol,
Glutathione, and Carotenoids
spectrophoto
meter
(Evelin and
Kapoor, 2014)
Solanum
lycopersicum
G. mosseae Roots Antioxidant capacity and
Malonaldehyde2
spectrophoto
meter
( ZhongQun
et al., 2007)
Solanum
lycopersicum
G. intraradices Shoots Proline and
Reactive oxygen species
spectrophoto
meter
(Hajiboland et
al., 2010)
Cajanus cajan G. mosseae Roots
Shoots
Proline and
Glycine betaine
spectrophoto
meter
(Garg and
Manchanda,
2009)
Zea mays Other AMF
G. etunicatum1
G. intraradices1
Leaves Proline,
Malondialdehyde and
Soluble sugar
spectrophoto
meter
(Chen et al.,
2014)
pág. 2988
Zea mays G. etunicatum Shoots
Roots
Photosynthetic capacity - (Zhu et al.,
2010)
Zea mays G. mosseae Leaves Amino acids,3
Proline,3
Formic acid3 and
Succinic acid3
HPLC (Sheng et al.,
2011)
Fragaria
ananassa
G. mosseae Leaves Antioxidant capacity
proline
- (Yin et al.,
2010)
Zea mays G. etunicatum Leaves
Roots3
Proline - (Zhu et al.,
2011)
Solanum
lycopersicum
AFM Mix
(G. mosseae,
G. intraradices and
Glomus sp.)
Leaves
Roots3
Essential Isoprenoids
(α-thujene, α-pinene,
D4-carene, β-phellandrene,
Limonene and linalool) and
Nonessential Isoprenoids3
T-system to
two-stage
traps
GC-MS
HPLC
(Asensio et al.,
2012)
Roots Apocarotenoids, and
Strigolactones
Calopogonium
mucunoides
G. etunicatum Leaves Aspartate, Glutamine,
Glycine, Threonine, Alanine,
Isoleucine and Gamma-
aminobutiric acid
Asparagine3,
Histidine3
and Arginine3
RP-HPLC (Souza et al.,
2014)
Cichorium
intybus
R. irregularis
Shoots Caftaric acid and Cichoric acid RF-HPLC (Rozpadek et
al., 2014)
Roots
Sesquiterpene lactones,
8-DeoxyLC, Jacq and LPikr
Sorghum spp. AFM mix
(G. intraradices,
G. mosseae,
G. aggregatum, and G.
etunicatum)
Roots
Shoots
Glycerol-3-galactoside,
Erythrose, adenine,
5-methoxytryptamine,
4-hydroxybenzoate,
Arginine, Proline,
Starch and Sucrose
metabolism and
lipid metabolism (only with
PGPB)
ALEX-CIS
GC-TOF MS
(Dhawi et al.,
2016)
Asclepias spp. R. intraradices, F.
mosseae, G.
aggregatum, and C.
etunicatum
Root Non-Polar
Cardenolides and Polar
cardenolides
UPLC (Vannette et
al., 2013)
Leaves Non-Polar cardenolides
Plantago
lanceolata
G. intraradices Shoots (Z)-3-hexenyl acetate GC-MS
HPLC
LC-MS
(Fontana et al.,
2009)
Zea mays G. mosseae Roots
Leaves
2,4-dihydroxy-7-methoxy-
2H-1,4-benzoxazin-3(4 H)-
one
HPLC (Song et al.,
2013)
1. More efficient symbiont
2. No differences being noted
3. Lowest concentration/or negative impact/down-regulate
Zea mays G. etunicatum Shoots
Roots
Photosynthetic capacity - (Zhu et al.,
2010)
Zea mays G. mosseae Leaves Amino acids,3
Proline,3
Formic acid3 and
Succinic acid3
HPLC (Sheng et al.,
2011)
Fragaria
ananassa
G. mosseae Leaves Antioxidant capacity
proline
- (Yin et al.,
2010)
Zea mays G. etunicatum Leaves
Roots3
Proline - (Zhu et al.,
2011)
Solanum
lycopersicum
AFM Mix
(G. mosseae,
G. intraradices and
Glomus sp.)
Leaves
Roots3
Essential Isoprenoids
(α-thujene, α-pinene,
D4-carene, β-phellandrene,
Limonene and linalool) and
Nonessential Isoprenoids3
T-system to
two-stage
traps
GC-MS
HPLC
(Asensio et al.,
2012)
Roots Apocarotenoids, and
Strigolactones
Calopogonium
mucunoides
G. etunicatum Leaves Aspartate, Glutamine,
Glycine, Threonine, Alanine,
Isoleucine and Gamma-
aminobutiric acid
Asparagine3,
Histidine3
and Arginine3
RP-HPLC (Souza et al.,
2014)
Cichorium
intybus
R. irregularis
Shoots Caftaric acid and Cichoric acid RF-HPLC (Rozpadek et
al., 2014)
Roots
Sesquiterpene lactones,
8-DeoxyLC, Jacq and LPikr
Sorghum spp. AFM mix
(G. intraradices,
G. mosseae,
G. aggregatum, and G.
etunicatum)
Roots
Shoots
Glycerol-3-galactoside,
Erythrose, adenine,
5-methoxytryptamine,
4-hydroxybenzoate,
Arginine, Proline,
Starch and Sucrose
metabolism and
lipid metabolism (only with
PGPB)
ALEX-CIS
GC-TOF MS
(Dhawi et al.,
2016)
Asclepias spp. R. intraradices, F.
mosseae, G.
aggregatum, and C.
etunicatum
Root Non-Polar
Cardenolides and Polar
cardenolides
UPLC (Vannette et
al., 2013)
Leaves Non-Polar cardenolides
Plantago
lanceolata
G. intraradices Shoots (Z)-3-hexenyl acetate GC-MS
HPLC
LC-MS
(Fontana et al.,
2009)
Zea mays G. mosseae Roots
Leaves
2,4-dihydroxy-7-methoxy-
2H-1,4-benzoxazin-3(4 H)-
one
HPLC (Song et al.,
2013)
1. More efficient symbiont
2. No differences being noted
3. Lowest concentration/or negative impact/down-regulate
pág. 2989
Since modulating the plant metabolome can prevent antagonistic defense responses, it may also prepare
plants for enhanced tolerance to environmental stress. These metabolites influence the outcome of the
association through the composition and exchange of both primary and specialized compounds. Thus,
the specificity of the plant-AMF interaction is regulated by changes in the plant’s primary and
specialized metabolome (Kaur & Suseela, 2020).
Although the leaf metabolome in AMF associations has been previously reported (Schweiger & Müller,
2015), the roots of mycorrhizal plants have often been overlooked. This review describes current
findings on metabolites triggered in response to AMF, while also considering additional stimuli such
as abiotic or biotic stress across all plant tissues.
METHODOLOGY
The methodology includes the revision of research documents from the last 37 years. Similarly, for this
literature review, authors were added based on their relevance and pertinence, according to the topics
presented.
Metabolic changes upon AMF colonization in medicinal plants
Currently, while the synthesis of specific compounds is possible, low yields often make it economically
unviable for drug production. However, AMF can enhance the concentrations of certain compounds. A
notable example is gallic acid in Libidibia ferrea; when inoculated with Claroideoglomus etunicatum,
the plant shows an increase in production compared to non-inoculated controls. A proposed mechanism
for this influence is the activation of the shikimic acid metabolic pathway, which is a precursor to
phenolic compounds (Silva et al., 2014).
Furthermore, essential oil content was evaluated in the aerial parts of basil (Ocimum basilicum)
inoculated with Glomus intraradices, Glomus etunicatum, and Glomus fasciculatum. The results
revealed that plants inoculated specifically with G. fasciculatum showed a significant increase in
linalool, followed by eugenol, ocimene, methyl chavicol, farnesol, and humulene, among other
compounds (Rasouli-Sadaghiani et al., 2010).
In some cases, the availability of phosphorus (P), nitrogen (N), or both in the soil enhances the
efficiency of mycorrhizal inoculation and improves metabolite production. Examples include increased
levels of artemisinin (Kapoor et al., 2007), proteins and carbohydrates (Pedone-Bonfim et al., 2012),
Since modulating the plant metabolome can prevent antagonistic defense responses, it may also prepare
plants for enhanced tolerance to environmental stress. These metabolites influence the outcome of the
association through the composition and exchange of both primary and specialized compounds. Thus,
the specificity of the plant-AMF interaction is regulated by changes in the plant’s primary and
specialized metabolome (Kaur & Suseela, 2020).
Although the leaf metabolome in AMF associations has been previously reported (Schweiger & Müller,
2015), the roots of mycorrhizal plants have often been overlooked. This review describes current
findings on metabolites triggered in response to AMF, while also considering additional stimuli such
as abiotic or biotic stress across all plant tissues.
METHODOLOGY
The methodology includes the revision of research documents from the last 37 years. Similarly, for this
literature review, authors were added based on their relevance and pertinence, according to the topics
presented.
Metabolic changes upon AMF colonization in medicinal plants
Currently, while the synthesis of specific compounds is possible, low yields often make it economically
unviable for drug production. However, AMF can enhance the concentrations of certain compounds. A
notable example is gallic acid in Libidibia ferrea; when inoculated with Claroideoglomus etunicatum,
the plant shows an increase in production compared to non-inoculated controls. A proposed mechanism
for this influence is the activation of the shikimic acid metabolic pathway, which is a precursor to
phenolic compounds (Silva et al., 2014).
Furthermore, essential oil content was evaluated in the aerial parts of basil (Ocimum basilicum)
inoculated with Glomus intraradices, Glomus etunicatum, and Glomus fasciculatum. The results
revealed that plants inoculated specifically with G. fasciculatum showed a significant increase in
linalool, followed by eugenol, ocimene, methyl chavicol, farnesol, and humulene, among other
compounds (Rasouli-Sadaghiani et al., 2010).
In some cases, the availability of phosphorus (P), nitrogen (N), or both in the soil enhances the
efficiency of mycorrhizal inoculation and improves metabolite production. Examples include increased
levels of artemisinin (Kapoor et al., 2007), proteins and carbohydrates (Pedone-Bonfim et al., 2012),
pág. 2990
antioxidant phytochemicals (Toussaint et al., 2007; Zubek et al., 2010, 2012), and colchicine (Pandey
et al., 2014).
Specifically, inoculation with Glomus macrocarpum and G. fasciculatum increased the artemisinin
concentration in Artemisia annua, with G. fasciculatum proving to be the more efficient symbiont.
However, phosphate fertilization can alter the extent of these AMF-induced effects on artemisinin
production (Kapoor et al., 2007).
In cebil plants inoculated with a mixed consortium of Gigaspora albida and Acaulospora longula, the
content of proteins, carbohydrates, flavonoids, phenolics, and tannins in the leaves increased.
Nevertheless, this benefit to primary metabolism was mitigated at higher P levels (Pedone-Bonfim et
al., 2012). Similarly, in pepper seedlings (Capsicum chinense) inoculated with Entrophospora
etunicata, significant metabolic increases were recorded compared to the control: 77% higher soluble
carbohydrates, 147% more total proanthocyanidins, 140% more total phenols, and 136% more total
saponins. These increases were also reflected in the concentrations of total proteins and foliar flavonoids
(Ribeiro da Luz et al., 2023).
Higher accumulation of antioxidant compounds, such as rosmarinic and caffeic acids, has been reported
in sweet basil shoots (Ocimum basilicum) inoculated with different Glomus species, specifically G.
caledonium and G. mosseae. However, these effects might be attributed to improved phosphorus (P)
nutrition via AMF. Plants colonized by G. caledonium yield higher concentrations of these acids
compared to non-mycorrhizal plants.
A possible mechanism by which G. caledonium and G. mosseae increase these phytochemical
concentrations is through enhanced nitrogen (N) assimilation. This could contribute to the production
of amino acids like tyrosine and phenylalanine, which are essential precursors for phenylalanine
ammonia-lyase (PAL), the primary enzyme involved in the biosynthesis of rosmarinic and caffeic acids
(Toussaint et al., 2007). In Hypericum perforatum, inoculation with Rhizophagus intraradices and an
AMF consortium (Glomus constrictum, G. geosporum, Funneliformis mosseae, and R. intraradices)
improved the concentration of the anthraquinone derivatives hypericin and pseudohypericin in shoots,
even with relatively high soil P content; notably, no significant differences were observed in the F.
mosseae treatment (Zubek et al., 2012).
antioxidant phytochemicals (Toussaint et al., 2007; Zubek et al., 2010, 2012), and colchicine (Pandey
et al., 2014).
Specifically, inoculation with Glomus macrocarpum and G. fasciculatum increased the artemisinin
concentration in Artemisia annua, with G. fasciculatum proving to be the more efficient symbiont.
However, phosphate fertilization can alter the extent of these AMF-induced effects on artemisinin
production (Kapoor et al., 2007).
In cebil plants inoculated with a mixed consortium of Gigaspora albida and Acaulospora longula, the
content of proteins, carbohydrates, flavonoids, phenolics, and tannins in the leaves increased.
Nevertheless, this benefit to primary metabolism was mitigated at higher P levels (Pedone-Bonfim et
al., 2012). Similarly, in pepper seedlings (Capsicum chinense) inoculated with Entrophospora
etunicata, significant metabolic increases were recorded compared to the control: 77% higher soluble
carbohydrates, 147% more total proanthocyanidins, 140% more total phenols, and 136% more total
saponins. These increases were also reflected in the concentrations of total proteins and foliar flavonoids
(Ribeiro da Luz et al., 2023).
Higher accumulation of antioxidant compounds, such as rosmarinic and caffeic acids, has been reported
in sweet basil shoots (Ocimum basilicum) inoculated with different Glomus species, specifically G.
caledonium and G. mosseae. However, these effects might be attributed to improved phosphorus (P)
nutrition via AMF. Plants colonized by G. caledonium yield higher concentrations of these acids
compared to non-mycorrhizal plants.
A possible mechanism by which G. caledonium and G. mosseae increase these phytochemical
concentrations is through enhanced nitrogen (N) assimilation. This could contribute to the production
of amino acids like tyrosine and phenylalanine, which are essential precursors for phenylalanine
ammonia-lyase (PAL), the primary enzyme involved in the biosynthesis of rosmarinic and caffeic acids
(Toussaint et al., 2007). In Hypericum perforatum, inoculation with Rhizophagus intraradices and an
AMF consortium (Glomus constrictum, G. geosporum, Funneliformis mosseae, and R. intraradices)
improved the concentration of the anthraquinone derivatives hypericin and pseudohypericin in shoots,
even with relatively high soil P content; notably, no significant differences were observed in the F.
mosseae treatment (Zubek et al., 2012).
pág. 2991
Experiments with various fungal strains have induced distinct metabolic changes. For instance, Inula
ensifolia was inoculated with two strains of G. intraradices and Glomus clarum. These AMF species
influenced the production of thymol derivatives differently: the highest concentration of all analyzed
compounds in the roots was found after G. clarum inoculation, while the lowest concentrations were
detected in the G. intraradices treatments. Conversely, mycorrhizal plants were characterized by lower
concentrations in the shoots (Zubek et al., 2010).
A significant increase in total phenolic content and antioxidant activity was recorded in the leaves and
flowers of artichoke plants inoculated with G. intraradices and G. mosseae in both greenhouse and field
experiments, with G. intraradices being more effective in stimulating these secondary metabolites
(Ceccarelli et al., 2010).
Mycorrhization was performed in Arnica montana at low N and P levels using different AMF species,
namely G. geosporum, G. constrictum, G. intraradices, and a consortium composed of the
aforementioned species plus G. mosseae. The analysis showed that the concentration of sesquiterpene
lactones was significantly higher in shoots than in roots. In leaves, the total phenolic acid concentration
was higher in plants inoculated with G. intraradices (Jurkiewicz et al., 2010).
On the other hand, the treatments significantly increased the levels of sesquiterpenic acids in the
rhizomes and roots of Valeriana officinalis (Nell et al., 2010). Similarly, a study on Melissa officinalis
reported an increased content of two phenolic compounds (rosmarinic and lithospermic acids) in the
presence of three AMF mixtures; however, these compounds decreased in Majorana hortensis (Engel
et al., 2016).
Finally, the vegetative parts (leaf and stem) of various grape varieties were inoculated with G. mosseae,
G. fasciculatum, G. intraradices, and a consortium of these three species. The results showed a
significantly higher total phenol content in leaf tissues compared to control plants, whereas no
significant differences were found in root tissues. Furthermore, the vegetative parts of grape plants
inoculated with AMF were found to be rich sources of the flavonoid quercetin (Eftekhari et al., 2012).
Metabolites in Targeted and Untargeted Approaches
Metabolomics approaches allow for the separation and detection of a wide range of metabolites through
gas chromatography-mass spectrometry (GC-MS), liquid chromatography-mass spectrometry (LC-
Experiments with various fungal strains have induced distinct metabolic changes. For instance, Inula
ensifolia was inoculated with two strains of G. intraradices and Glomus clarum. These AMF species
influenced the production of thymol derivatives differently: the highest concentration of all analyzed
compounds in the roots was found after G. clarum inoculation, while the lowest concentrations were
detected in the G. intraradices treatments. Conversely, mycorrhizal plants were characterized by lower
concentrations in the shoots (Zubek et al., 2010).
A significant increase in total phenolic content and antioxidant activity was recorded in the leaves and
flowers of artichoke plants inoculated with G. intraradices and G. mosseae in both greenhouse and field
experiments, with G. intraradices being more effective in stimulating these secondary metabolites
(Ceccarelli et al., 2010).
Mycorrhization was performed in Arnica montana at low N and P levels using different AMF species,
namely G. geosporum, G. constrictum, G. intraradices, and a consortium composed of the
aforementioned species plus G. mosseae. The analysis showed that the concentration of sesquiterpene
lactones was significantly higher in shoots than in roots. In leaves, the total phenolic acid concentration
was higher in plants inoculated with G. intraradices (Jurkiewicz et al., 2010).
On the other hand, the treatments significantly increased the levels of sesquiterpenic acids in the
rhizomes and roots of Valeriana officinalis (Nell et al., 2010). Similarly, a study on Melissa officinalis
reported an increased content of two phenolic compounds (rosmarinic and lithospermic acids) in the
presence of three AMF mixtures; however, these compounds decreased in Majorana hortensis (Engel
et al., 2016).
Finally, the vegetative parts (leaf and stem) of various grape varieties were inoculated with G. mosseae,
G. fasciculatum, G. intraradices, and a consortium of these three species. The results showed a
significantly higher total phenol content in leaf tissues compared to control plants, whereas no
significant differences were found in root tissues. Furthermore, the vegetative parts of grape plants
inoculated with AMF were found to be rich sources of the flavonoid quercetin (Eftekhari et al., 2012).
Metabolites in Targeted and Untargeted Approaches
Metabolomics approaches allow for the separation and detection of a wide range of metabolites through
gas chromatography-mass spectrometry (GC-MS), liquid chromatography-mass spectrometry (LC-
pág. 2992
MS), and nuclear magnetic resonance (NMR). These procedures offer the highest capacity for
determining extensive metabolite sets, estimated between 100,000 and 200,000 (Sardans et al., 2011).
Observations on metabolic alterations by Rivero and coworkers identified significant shifts in tomato
roots inoculated with two common AMF: Rhizophagus irregularis and F. mosseae. Products derived
from amino acids, such as phenolic alcohol derivatives, benzylisoquinolines, and conjugated
polyamines, were significantly affected in AMF colonized plants.
Specifically, high quantities of ferulic acid, coumaryl alcohol, coniferyl alcohol, benzylisoquinoline
alkaloids, polyamines (and their conjugates), a putative spermidine, triferuloyl spermidine, and oxylipin
pathway derivatives were found in colonized roots. Conversely, a negative impact was observed on free
amino acids such as tryptophan, tyrosine, phenylalanine, alanine, and leucine. The lower concentration
of these free amino acids suggests their role as precursors for secondary metabolites, particularly
tyrosine and phenylalanine, which are essential for phenylpropanoid biosynthesis (Rivero et al., 2015).
Similarly, wheat roots inoculated with a consortium of AMF species (Scutellospora calospora,
Acaulospora laevis, Glomus aggregatum, G. etunicatum, G. deserticola, Gigaspora margarita, R.
irregularis, F. mosseae, and G. fasciculatum) showed decreased concentrations of glutamic acid,
alanine, asparagine, phenylalanine, and saturated fatty acids. In contrast, dual inoculation with PGPR
and AMF increased their accumulation, suggesting that PGPR enhances nitrogen (N) availability,
particularly ammonium and nitrate, for the host plant (Saia et al., 2015).
A decrease in amino acid metabolism has been previously reported in the association between Lotus
japonicus and G. mosseae. This symbiosis results in a reduction of amino acid metabolism —
specifically affecting glutamic acid, aspartic acid, glycine, asparagine, 4-aminobutanoic acid (GABA),
and 2-methylmalic acid— in both source and sink leaves. Furthermore, organic acids involved in central
catabolic pathways, such as malic, citric, and succinic acids, are also reduced. Conversely, an increase
in kestose, xylitol, and myo-inositol has been observed; these compounds serve as indicators of stress
response in L. japonicus (Fester et al., 2011).
In another association involving willow and R. irregularis, leaf metabolic content was significantly
altered. Results revealed that mycorrhization has a negative impact on primary metabolism, primarily
affecting amino acids and carbohydrates. In contrast, an up-regulation was observed in several
MS), and nuclear magnetic resonance (NMR). These procedures offer the highest capacity for
determining extensive metabolite sets, estimated between 100,000 and 200,000 (Sardans et al., 2011).
Observations on metabolic alterations by Rivero and coworkers identified significant shifts in tomato
roots inoculated with two common AMF: Rhizophagus irregularis and F. mosseae. Products derived
from amino acids, such as phenolic alcohol derivatives, benzylisoquinolines, and conjugated
polyamines, were significantly affected in AMF colonized plants.
Specifically, high quantities of ferulic acid, coumaryl alcohol, coniferyl alcohol, benzylisoquinoline
alkaloids, polyamines (and their conjugates), a putative spermidine, triferuloyl spermidine, and oxylipin
pathway derivatives were found in colonized roots. Conversely, a negative impact was observed on free
amino acids such as tryptophan, tyrosine, phenylalanine, alanine, and leucine. The lower concentration
of these free amino acids suggests their role as precursors for secondary metabolites, particularly
tyrosine and phenylalanine, which are essential for phenylpropanoid biosynthesis (Rivero et al., 2015).
Similarly, wheat roots inoculated with a consortium of AMF species (Scutellospora calospora,
Acaulospora laevis, Glomus aggregatum, G. etunicatum, G. deserticola, Gigaspora margarita, R.
irregularis, F. mosseae, and G. fasciculatum) showed decreased concentrations of glutamic acid,
alanine, asparagine, phenylalanine, and saturated fatty acids. In contrast, dual inoculation with PGPR
and AMF increased their accumulation, suggesting that PGPR enhances nitrogen (N) availability,
particularly ammonium and nitrate, for the host plant (Saia et al., 2015).
A decrease in amino acid metabolism has been previously reported in the association between Lotus
japonicus and G. mosseae. This symbiosis results in a reduction of amino acid metabolism —
specifically affecting glutamic acid, aspartic acid, glycine, asparagine, 4-aminobutanoic acid (GABA),
and 2-methylmalic acid— in both source and sink leaves. Furthermore, organic acids involved in central
catabolic pathways, such as malic, citric, and succinic acids, are also reduced. Conversely, an increase
in kestose, xylitol, and myo-inositol has been observed; these compounds serve as indicators of stress
response in L. japonicus (Fester et al., 2011).
In another association involving willow and R. irregularis, leaf metabolic content was significantly
altered. Results revealed that mycorrhization has a negative impact on primary metabolism, primarily
affecting amino acids and carbohydrates. In contrast, an up-regulation was observed in several
pág. 2993
biosynthetic pathways, including those for phenylpropanoids, flavonoids, isoflavonoids,
coumaroylquinate, and caffeoyl-shikimate. Additionally, increases were noted in jasmonic acid (JA),
iso-JA, pinostrobin, isoformononetin, rutin, luteolin-7-O-glucoside, porphyrins, chlorophyll, phenolic
glycosides, and terpenoids. Many of these compounds are directly linked to resistance against
environmental stress (Aliferis et al., 2015).
Similarly, in maize plants, symbiosis with G. intraradices led to a down-regulation of amino acid
content in the leaves, while secondary metabolism was up-regulated, specifically for organic acids,
lipids, fatty acids, carotenoids, antioxidants, and carbohydrates. Interestingly, the terpenoids alpha-
amyrin and beta-amyrin showed strong accumulation (Gerlach et al., 2015).
In other experiments, four genotypes of barley were analyzed using a mixture of the mycorrhizal fungi
G. mosseae and G. intraradices. Leaf contents of sucrose, the two major amino acids (glutamic acid
and aspartate), chlorophyll, lutein, and glutathione decreased in response to AMF. Conversely, levels
of free hexoses, central phosphorylated intermediates (3PGA, PEP, RuBP, Glc1P), free inorganic
phosphate, and the carboxylates isocitrate and malate increased. In general, phosphorylated
intermediates of central metabolism were more abundant in the leaves of AMF-colonized plants (Kogel
et al., 2010).
Regarding amino acid content in symbiotic associations, rhizobia exhibit the opposite phenomenon: an
increase in metabolites connected to amino acid metabolism and a decrease in those related to plant
stress (Fester et al., 2011).
Amino acid dynamics have been discussed by Rivero et al. (2015), particularly their role as precursor
compounds for amino acid-derived secondary metabolites. Certain amino acids, such as glutamate and
aspartate, are crucial for nitrogen (N) uptake by the AMF extra-radical mycelium. Other studies have
shown that AMF have a high N demand and retain most of the N acquired as organic compounds for
their own growth (Hodge & Fitter, 2010). Conversely, increases in amino acid levels have been
interpreted as an indicator of enhanced plastid activity in colonized root cells rather than having direct
nutritional significance (Lohse et al., 2005; Schliemann et al., 2008; Fester et al., 2011).
Changes in mycorrhizal roots have been well studied, particularly in the model plant Medicago
truncatula and the AMF strain R. irregularis. Compared to other experiments, mycorrhization raised
biosynthetic pathways, including those for phenylpropanoids, flavonoids, isoflavonoids,
coumaroylquinate, and caffeoyl-shikimate. Additionally, increases were noted in jasmonic acid (JA),
iso-JA, pinostrobin, isoformononetin, rutin, luteolin-7-O-glucoside, porphyrins, chlorophyll, phenolic
glycosides, and terpenoids. Many of these compounds are directly linked to resistance against
environmental stress (Aliferis et al., 2015).
Similarly, in maize plants, symbiosis with G. intraradices led to a down-regulation of amino acid
content in the leaves, while secondary metabolism was up-regulated, specifically for organic acids,
lipids, fatty acids, carotenoids, antioxidants, and carbohydrates. Interestingly, the terpenoids alpha-
amyrin and beta-amyrin showed strong accumulation (Gerlach et al., 2015).
In other experiments, four genotypes of barley were analyzed using a mixture of the mycorrhizal fungi
G. mosseae and G. intraradices. Leaf contents of sucrose, the two major amino acids (glutamic acid
and aspartate), chlorophyll, lutein, and glutathione decreased in response to AMF. Conversely, levels
of free hexoses, central phosphorylated intermediates (3PGA, PEP, RuBP, Glc1P), free inorganic
phosphate, and the carboxylates isocitrate and malate increased. In general, phosphorylated
intermediates of central metabolism were more abundant in the leaves of AMF-colonized plants (Kogel
et al., 2010).
Regarding amino acid content in symbiotic associations, rhizobia exhibit the opposite phenomenon: an
increase in metabolites connected to amino acid metabolism and a decrease in those related to plant
stress (Fester et al., 2011).
Amino acid dynamics have been discussed by Rivero et al. (2015), particularly their role as precursor
compounds for amino acid-derived secondary metabolites. Certain amino acids, such as glutamate and
aspartate, are crucial for nitrogen (N) uptake by the AMF extra-radical mycelium. Other studies have
shown that AMF have a high N demand and retain most of the N acquired as organic compounds for
their own growth (Hodge & Fitter, 2010). Conversely, increases in amino acid levels have been
interpreted as an indicator of enhanced plastid activity in colonized root cells rather than having direct
nutritional significance (Lohse et al., 2005; Schliemann et al., 2008; Fester et al., 2011).
Changes in mycorrhizal roots have been well studied, particularly in the model plant Medicago
truncatula and the AMF strain R. irregularis. Compared to other experiments, mycorrhization raised
pág. 2994
the levels of certain amino acids, such as glutamic acid, aspartic acid, and asparagine. It also increased
the concentrations of specific metabolites like trehalose, palmitic and oleic acids, cyclohexanone,
mycorradicin derivatives, daidzein, ononin, and malonylononin (Schliemann et al., 2008). Interestingly,
oleic acid has been found to increase spore germination at concentrations of 10-8 M (Rush et al., 2020).
Years later, Laparre et al. (2014), using the same symbiotic association, performed metabolomics and
biological screens based on gene expression responses, identifying two significant compounds:
propionyl and butyryl carnitines. These new symbiotic signals may serve as markers of fungal root
colonization, although further studies are required with other AMF species to confirm their universality
(Laparre et al., 2014).
Root colonization of L. japonicus by R. irregularis revealed specific lipid responses upon
mycorrhization. Glycosylated sphingolipids (glucosylceramide, dihexosylceramide),
inositolphosphorylceramide, free sterols, sterol esters, sterol glucosides, and acylated sterol glucosides
were detected in R. irregularis, primarily containing two predominant fatty acids: palmitic acid and
palmitvaccenic acid.
Notable differences between extraradical mycelium (ERM) and mycorrhizal roots were detected;
specifically, some of the major phosphatidylcholine (PC) molecular species present in the ERM —such
as those containing palmitvaccenic and tetracosenoic acyl groups—are absent from mycorrhizal roots
(Wewer et al., 2014).
The amino acid composition of tomato fruits is modified upon colonization with G. mosseae, which
also accelerates flowering and fruit development while increasing yield. Symbiosis enhances amino
acid abundance, with glutamine and asparagine being the most responsive. In general, mycorrhizal
plants exhibit a higher total free amino acid content compared to control fruits. Although this metabolic
shift was supported by transcriptomic data, no significant differences were noted in gene expression
within the fruits themselves.
The authors propose two possibilities to explain this:
1. Transport Mechanism: The two amides were not synthesized de novo in the fruit but were
translocated from the host roots. These amino acids are recognized as primary nitrogen transport
compounds from source to sink organs, serving as nitrogen reserves.
the levels of certain amino acids, such as glutamic acid, aspartic acid, and asparagine. It also increased
the concentrations of specific metabolites like trehalose, palmitic and oleic acids, cyclohexanone,
mycorradicin derivatives, daidzein, ononin, and malonylononin (Schliemann et al., 2008). Interestingly,
oleic acid has been found to increase spore germination at concentrations of 10-8 M (Rush et al., 2020).
Years later, Laparre et al. (2014), using the same symbiotic association, performed metabolomics and
biological screens based on gene expression responses, identifying two significant compounds:
propionyl and butyryl carnitines. These new symbiotic signals may serve as markers of fungal root
colonization, although further studies are required with other AMF species to confirm their universality
(Laparre et al., 2014).
Root colonization of L. japonicus by R. irregularis revealed specific lipid responses upon
mycorrhization. Glycosylated sphingolipids (glucosylceramide, dihexosylceramide),
inositolphosphorylceramide, free sterols, sterol esters, sterol glucosides, and acylated sterol glucosides
were detected in R. irregularis, primarily containing two predominant fatty acids: palmitic acid and
palmitvaccenic acid.
Notable differences between extraradical mycelium (ERM) and mycorrhizal roots were detected;
specifically, some of the major phosphatidylcholine (PC) molecular species present in the ERM —such
as those containing palmitvaccenic and tetracosenoic acyl groups—are absent from mycorrhizal roots
(Wewer et al., 2014).
The amino acid composition of tomato fruits is modified upon colonization with G. mosseae, which
also accelerates flowering and fruit development while increasing yield. Symbiosis enhances amino
acid abundance, with glutamine and asparagine being the most responsive. In general, mycorrhizal
plants exhibit a higher total free amino acid content compared to control fruits. Although this metabolic
shift was supported by transcriptomic data, no significant differences were noted in gene expression
within the fruits themselves.
The authors propose two possibilities to explain this:
1. Transport Mechanism: The two amides were not synthesized de novo in the fruit but were
translocated from the host roots. These amino acids are recognized as primary nitrogen transport
compounds from source to sink organs, serving as nitrogen reserves.
pág. 2995
2. Fungal Synthesis: These amino acids could be synthesized directly by the AMF (Salvioli et al.,
2012).
Analysis of leaves from R. irregularis colonized plants showed a common core of 850 metabolic
features shared between dicotyledonous and monocotyledonous plants. However, metabolic responses
to AMF were highly species-specific. For example:
▪ The sugar alcohol mannitol was only detectable in Veronica chamaedrys.
▪ The cyclic polyols pinitol and ononitol were characteristic of Medicago truncatula.
▪ Sorbitol was common to the genus Plantago.
▪ Aucubin and verbascoside were found exclusively in the Plantaginaceae.
Several organic acids from the citric acid cycle (citrate, malate, fumarate, and partially succinate and
isocitrate) decreased under AMF conditions in P. lanceolata, P. major, V. chamaedrys, and M.
truncatula, but increased in the grass Poa annua. Interestingly, the grass was the least responsive to
AMF symbiosis, although catalpol —a secondary metabolite involved in direct plant defense— was
significantly increased by AMF in P. lanceolata (Schweiger et al., 2014).
Previously, catalpol has been detected in G. intraradices hyphae during symbiosis with P. lanceolata.
AMF inoculation led to a decrease in verbascoside content in roots but increased its concentration in
shoots only when fungivores were present. In contrast, AMF inoculation consistently reduced catalpol
concentrations in shoots and had no effect in roots. While aucubin was detectable in all samples, no
treatment significantly affected its concentration in shoots. Notably, catalpol was consistently found in
AMF hyphae when host plants were exposed to fungivores (Duhamel et al., 2013).
Finally, when different genotypes of P. lanceolata (containing high and low levels of iridoid glycosides,
IG) were inoculated with G. intraradices, results suggested that high root concentrations of aucubin
may have deleterious effects on arbuscular development. Interestingly, AMF increased root aucubin
concentrations specifically in the high-IG genotype (De Deyn et al., 2009).
The mutant mtha1-2 is defective in the symbiotic transfer of nutrients across the periarbuscular space,
which precludes phosphate uptake. In this mutant, no changes were observed in leaf metabolite levels,
such as phosphate, sulfate, nitrate, citrate, fumarate, and chloride, when compared with wild-type plants
inoculated with AMF (Hubberten et al., 2015).
2. Fungal Synthesis: These amino acids could be synthesized directly by the AMF (Salvioli et al.,
2012).
Analysis of leaves from R. irregularis colonized plants showed a common core of 850 metabolic
features shared between dicotyledonous and monocotyledonous plants. However, metabolic responses
to AMF were highly species-specific. For example:
▪ The sugar alcohol mannitol was only detectable in Veronica chamaedrys.
▪ The cyclic polyols pinitol and ononitol were characteristic of Medicago truncatula.
▪ Sorbitol was common to the genus Plantago.
▪ Aucubin and verbascoside were found exclusively in the Plantaginaceae.
Several organic acids from the citric acid cycle (citrate, malate, fumarate, and partially succinate and
isocitrate) decreased under AMF conditions in P. lanceolata, P. major, V. chamaedrys, and M.
truncatula, but increased in the grass Poa annua. Interestingly, the grass was the least responsive to
AMF symbiosis, although catalpol —a secondary metabolite involved in direct plant defense— was
significantly increased by AMF in P. lanceolata (Schweiger et al., 2014).
Previously, catalpol has been detected in G. intraradices hyphae during symbiosis with P. lanceolata.
AMF inoculation led to a decrease in verbascoside content in roots but increased its concentration in
shoots only when fungivores were present. In contrast, AMF inoculation consistently reduced catalpol
concentrations in shoots and had no effect in roots. While aucubin was detectable in all samples, no
treatment significantly affected its concentration in shoots. Notably, catalpol was consistently found in
AMF hyphae when host plants were exposed to fungivores (Duhamel et al., 2013).
Finally, when different genotypes of P. lanceolata (containing high and low levels of iridoid glycosides,
IG) were inoculated with G. intraradices, results suggested that high root concentrations of aucubin
may have deleterious effects on arbuscular development. Interestingly, AMF increased root aucubin
concentrations specifically in the high-IG genotype (De Deyn et al., 2009).
The mutant mtha1-2 is defective in the symbiotic transfer of nutrients across the periarbuscular space,
which precludes phosphate uptake. In this mutant, no changes were observed in leaf metabolite levels,
such as phosphate, sulfate, nitrate, citrate, fumarate, and chloride, when compared with wild-type plants
inoculated with AMF (Hubberten et al., 2015).
pág. 2996
Using the tomato plant as a model, an integrative analysis of the host response to different mycorrhizal
fungi was performed. Levels of 12-oxo-phytodienoic acid (OPDA) were significantly higher in roots
colonized by G. mosseae and G. intraradices. While JA levels remained unaltered, its bioactive
derivative, JA-isoleucine (JA-Ile), and salicylic acid (SA) were higher only in the G. mosseae
association. Abscisic acid (ABA) content did not change in either fungal association. Combined
transcriptional analyses suggest that the oxylipin pathway could regulate AMF symbiosis, specifically
through jasmonate-mediated regulation (López-Ráez et al., 2010).
Additionally, the amount of glycolipids in the leaves of mycorrhizal olive trees (Olea europaea) was
found to be altered. Glycolipid content was higher in plants inoculated with G. intraradices, which also
increased the levels of alpha-linolenic acid within the glycolipid fraction (Mechri et al., 2014).
Metabolites and Biotic/Abiotic Stress
Abiotic and biotic stresses adversely affect plant physiology; however, AMF symbiosis can enhance
plant tolerance to varying degrees. The association with AMF influences interactions between plants
and their natural enemies through several mechanisms, including genetic variability among plants and
fungal species, as well as the susceptibility of these enemies to secondary metabolites triggered by the
AMF-host interaction.
Enhanced antioxidant capacity in both leaves and roots has been observed in Trigonella foenum-
graecum (fenugreek) inoculated with Glomus intraradices under salinity stress. Despite a reduction in
root colonization as salt stress increased, there was a significant rise in the activity of antioxidant
enzymes, such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX),
peroxidase (PX), and glutathione reductase (GR) and in the concentration of antioxidant molecules,
including ascorbic acid, alpha-tocopherol, glutathione, and carotenoids (Evelin & Kapoor, 2014).
Similar findings were previously reported in tomato plants inoculated with G. mosseae (ZhongQun et
al., 2007) and G. intraradices (Hajiboland et al., 2010), as well as in Cajanus cajan inoculated with G.
mosseae, which showed increased osmolyte synthesis and accumulation (Garg & Manchanda, 2009).
Regarding thermal stress, maize plants inoculated with four different AMF species exhibited higher
proline content at low temperatures. Specifically, only G. etunicatum and G. intraradices showed
elevated levels of malondialdehyde and soluble sugars under these stress conditions (Chen et al., 2014).
Using the tomato plant as a model, an integrative analysis of the host response to different mycorrhizal
fungi was performed. Levels of 12-oxo-phytodienoic acid (OPDA) were significantly higher in roots
colonized by G. mosseae and G. intraradices. While JA levels remained unaltered, its bioactive
derivative, JA-isoleucine (JA-Ile), and salicylic acid (SA) were higher only in the G. mosseae
association. Abscisic acid (ABA) content did not change in either fungal association. Combined
transcriptional analyses suggest that the oxylipin pathway could regulate AMF symbiosis, specifically
through jasmonate-mediated regulation (López-Ráez et al., 2010).
Additionally, the amount of glycolipids in the leaves of mycorrhizal olive trees (Olea europaea) was
found to be altered. Glycolipid content was higher in plants inoculated with G. intraradices, which also
increased the levels of alpha-linolenic acid within the glycolipid fraction (Mechri et al., 2014).
Metabolites and Biotic/Abiotic Stress
Abiotic and biotic stresses adversely affect plant physiology; however, AMF symbiosis can enhance
plant tolerance to varying degrees. The association with AMF influences interactions between plants
and their natural enemies through several mechanisms, including genetic variability among plants and
fungal species, as well as the susceptibility of these enemies to secondary metabolites triggered by the
AMF-host interaction.
Enhanced antioxidant capacity in both leaves and roots has been observed in Trigonella foenum-
graecum (fenugreek) inoculated with Glomus intraradices under salinity stress. Despite a reduction in
root colonization as salt stress increased, there was a significant rise in the activity of antioxidant
enzymes, such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX),
peroxidase (PX), and glutathione reductase (GR) and in the concentration of antioxidant molecules,
including ascorbic acid, alpha-tocopherol, glutathione, and carotenoids (Evelin & Kapoor, 2014).
Similar findings were previously reported in tomato plants inoculated with G. mosseae (ZhongQun et
al., 2007) and G. intraradices (Hajiboland et al., 2010), as well as in Cajanus cajan inoculated with G.
mosseae, which showed increased osmolyte synthesis and accumulation (Garg & Manchanda, 2009).
Regarding thermal stress, maize plants inoculated with four different AMF species exhibited higher
proline content at low temperatures. Specifically, only G. etunicatum and G. intraradices showed
elevated levels of malondialdehyde and soluble sugars under these stress conditions (Chen et al., 2014).
pág. 2997
Furthermore, maize plants inoculated with G. etunicatum demonstrated higher stomatal conductance,
alongside improved water status and photosynthetic capacity (Zhu et al., 2010). Conversely, a decrease
in the relative abundance of total free amino acids, proline, formic acid, and succinic acid was detected
in maize plants inoculated with G. mosseae under salt stress (Sheng et al., 2011).
Glomus mosseae has been shown to increase the activity of protective enzymes, osmoregulation, and
antioxidant capacity in strawberry leaves. This symbiosis also promotes the accumulation of free proline
and soluble proteins, while improving the transport speed of soluble sugars under drought stress (Yin
et al., 2010). These findings align with reports on maize inoculated with G. etunicatum, where the
symbiosis increased leaf proline content but decreased it in the roots during drought. In these maize
plants, peroxidase activity was higher in both leaves and roots, whereas superoxide dismutase activity
increased exclusively in the roots (Zhu et al., 2011).
In other studies, tomato plants inoculated with a commercial consortium (G. mosseae, G. intraradices,
and Glomus sp.) prioritized the leaf production of essential isoprenoids over non-essential ones,
particularly under drought conditions. The primary volatile compounds emitted were monoterpenes,
including alpha-thujene, alpha-pinene, delta-4-carene, beta-phellandrene, limonene, and linalool.
Conversely, AMF symbiosis has been found to decrease the root content of volatile isoprenoids while
stimulating the production of other isoprenoid-derived compounds. These include apocarotenoids and
strigolactones, which originate from the oxidative cleavage of carotenoids. Both groups are vital for
various growth processes, with strigolactones being particularly crucial for the functional establishment
of the AMF symbiosis. Authors suggest that this shifts carbon allocation toward specific secondary
compounds, as all isoprenoids share common precursors (Asensio et al., 2012).
In relation to amino acid profiles, mycorrhization in Calopogonium mucunoides inoculated with G.
etunicatum during heavy metal exposure led to an increase in foliar levels of aspartate, glutamine,
glycine, threonine, alanine, isoleucine, and gamma-aminobutyric acid (GABA). In contrast, a depletion
of asparagine, histidine, and arginine was observed. Notably, only amino acids derived from 3-
phosphoglycerate and pyruvate were significantly higher in mycorrhizal plants (Souza et al., 2014).
Furthermore, in chicory plants inoculated with Rhizophagus irregularis, an accumulation of caffeic acid
derivatives, such as caftaric and chicoric acid, was observed in the shoots. In the roots, the concentration
Furthermore, maize plants inoculated with G. etunicatum demonstrated higher stomatal conductance,
alongside improved water status and photosynthetic capacity (Zhu et al., 2010). Conversely, a decrease
in the relative abundance of total free amino acids, proline, formic acid, and succinic acid was detected
in maize plants inoculated with G. mosseae under salt stress (Sheng et al., 2011).
Glomus mosseae has been shown to increase the activity of protective enzymes, osmoregulation, and
antioxidant capacity in strawberry leaves. This symbiosis also promotes the accumulation of free proline
and soluble proteins, while improving the transport speed of soluble sugars under drought stress (Yin
et al., 2010). These findings align with reports on maize inoculated with G. etunicatum, where the
symbiosis increased leaf proline content but decreased it in the roots during drought. In these maize
plants, peroxidase activity was higher in both leaves and roots, whereas superoxide dismutase activity
increased exclusively in the roots (Zhu et al., 2011).
In other studies, tomato plants inoculated with a commercial consortium (G. mosseae, G. intraradices,
and Glomus sp.) prioritized the leaf production of essential isoprenoids over non-essential ones,
particularly under drought conditions. The primary volatile compounds emitted were monoterpenes,
including alpha-thujene, alpha-pinene, delta-4-carene, beta-phellandrene, limonene, and linalool.
Conversely, AMF symbiosis has been found to decrease the root content of volatile isoprenoids while
stimulating the production of other isoprenoid-derived compounds. These include apocarotenoids and
strigolactones, which originate from the oxidative cleavage of carotenoids. Both groups are vital for
various growth processes, with strigolactones being particularly crucial for the functional establishment
of the AMF symbiosis. Authors suggest that this shifts carbon allocation toward specific secondary
compounds, as all isoprenoids share common precursors (Asensio et al., 2012).
In relation to amino acid profiles, mycorrhization in Calopogonium mucunoides inoculated with G.
etunicatum during heavy metal exposure led to an increase in foliar levels of aspartate, glutamine,
glycine, threonine, alanine, isoleucine, and gamma-aminobutyric acid (GABA). In contrast, a depletion
of asparagine, histidine, and arginine was observed. Notably, only amino acids derived from 3-
phosphoglycerate and pyruvate were significantly higher in mycorrhizal plants (Souza et al., 2014).
Furthermore, in chicory plants inoculated with Rhizophagus irregularis, an accumulation of caffeic acid
derivatives, such as caftaric and chicoric acid, was observed in the shoots. In the roots, the concentration
pág. 2998
of sesquiterpene lactones increased. However, no significant differences were found when plants were
cultivated on substrates enriched with heavy metals such as Zn, Pb, and Cd (Rozpądek et al., 2014).
Sorghum plants were inoculated with a mixture of Plant Growth-Promoting Bacteria (PGPB) and an
AMF consortium containing G. intraradices, G. mosseae, G. aggregatum, and G. etunicatum. The
mycorrhizal treatment resulted in the up-regulation of several metabolites; notably, five were
exclusively up-regulated in the mycorrhizal group: glycerol-3-galactoside, erythrose, adenine, 5-
methoxytryptamine, and 4-hydroxybenzoate. Furthermore, five metabolic pathways were up-regulated,
including arginine and proline metabolism and starch and sucrose metabolism. These changes were
associated with enhanced uptake of macronutrients, microelements, and heavy metals such as copper
and zinc.
The combined treatment of AMF and Pseudomonas increased lipid metabolism during the mycorrhizal
symbiosis, accompanied by heightened transcriptional regulation. Additionally, three pathways
involved in amino acid metabolism and energy generation were common to both the mycorrhizal and
Pseudomonas treatments. These results suggest that mycorrhizae play a role in inducing essential amino
acid precursors and the biosynthesis of plant carbohydrates from fatty acids via glyoxylate and
dicarboxylate metabolism (Dhawi et al., 2016).
In respect of biotic interactions, G. intraradices has shown a positive effect on herbivores; for instance,
a significant increase in the growth of Spodoptera littoralis was observed, suggesting that AMF may
improve food quality for certain herbivores (Kempel et al., 2010). Furthermore, AMF can influence
traits mediating plant-herbivore interactions by altering the relative distribution of secondary
compounds across leaves, stems, and roots. In asclepias plants inoculated with R. intraradices, F.
mosseae, G. aggregatum, and C. etunicatum, the inoculation shifted the distribution of cardenolides
between root and shoot tissues. While cardenolides in fine roots occurred at equal concentrations
regardless of treatment, AMF inoculation increased cardenolide non-polarity in shoots and leaves,
which are generally considered more toxic than their polar counterparts (Vannette et al., 2013).
Plant responses are also highly dependent on species-specific fungal colonization. In a study where
strawberry plants were colonized by G. mosseae and G. fasciculatum, dual colonization had no effect
on Otiorhynchus sulcatus larvae. However, single-species inoculation reduced larval survival and
of sesquiterpene lactones increased. However, no significant differences were found when plants were
cultivated on substrates enriched with heavy metals such as Zn, Pb, and Cd (Rozpądek et al., 2014).
Sorghum plants were inoculated with a mixture of Plant Growth-Promoting Bacteria (PGPB) and an
AMF consortium containing G. intraradices, G. mosseae, G. aggregatum, and G. etunicatum. The
mycorrhizal treatment resulted in the up-regulation of several metabolites; notably, five were
exclusively up-regulated in the mycorrhizal group: glycerol-3-galactoside, erythrose, adenine, 5-
methoxytryptamine, and 4-hydroxybenzoate. Furthermore, five metabolic pathways were up-regulated,
including arginine and proline metabolism and starch and sucrose metabolism. These changes were
associated with enhanced uptake of macronutrients, microelements, and heavy metals such as copper
and zinc.
The combined treatment of AMF and Pseudomonas increased lipid metabolism during the mycorrhizal
symbiosis, accompanied by heightened transcriptional regulation. Additionally, three pathways
involved in amino acid metabolism and energy generation were common to both the mycorrhizal and
Pseudomonas treatments. These results suggest that mycorrhizae play a role in inducing essential amino
acid precursors and the biosynthesis of plant carbohydrates from fatty acids via glyoxylate and
dicarboxylate metabolism (Dhawi et al., 2016).
In respect of biotic interactions, G. intraradices has shown a positive effect on herbivores; for instance,
a significant increase in the growth of Spodoptera littoralis was observed, suggesting that AMF may
improve food quality for certain herbivores (Kempel et al., 2010). Furthermore, AMF can influence
traits mediating plant-herbivore interactions by altering the relative distribution of secondary
compounds across leaves, stems, and roots. In asclepias plants inoculated with R. intraradices, F.
mosseae, G. aggregatum, and C. etunicatum, the inoculation shifted the distribution of cardenolides
between root and shoot tissues. While cardenolides in fine roots occurred at equal concentrations
regardless of treatment, AMF inoculation increased cardenolide non-polarity in shoots and leaves,
which are generally considered more toxic than their polar counterparts (Vannette et al., 2013).
Plant responses are also highly dependent on species-specific fungal colonization. In a study where
strawberry plants were colonized by G. mosseae and G. fasciculatum, dual colonization had no effect
on Otiorhynchus sulcatus larvae. However, single-species inoculation reduced larval survival and
pág. 2999
weight. Although the exact mechanism remains unknown, the authors proposed three potential
explanations: physical, nutritional, and/or chemical effects (Gange, 2001). Subsequently, Fontana et al.
(2009) found that P. lanceolata plants inoculated with G. intraradices emitted lower amounts of
sesquiterpenes during Spodoptera littoralis herbivory but showed an increased emission of the green
leaf volatile (Z)-3-hexenyl acetate, which is considered an indirect defense signal.
Medicago truncatula plants colonized by G. intraradices exhibited increased resistance to the virulent
bacterial pathogen Xanthomonas campestris. This resistance was associated with transcriptional
changes in both roots and shoots; notably, many of the genes induced in the shoots are predicted to be
involved in stress and defense responses (Liu et al., 2007). Similarly, tomato plants colonized with G.
fasciculatum showed systemic induced resistance (SIR) to the foliar pathogen Alternaria alternata.
Mycorrhizal plants displayed a three-fold increase in lipoxygenase (LOX) activity compared to control
plants, a finding supported by the up-regulation of genes involved in jasmonic acid (JA) biosynthesis
and salicylic acid (SA) signaling (Nair et al., 2015).
Consistent with these findings, tomato plants inoculated with F. mosseae demonstrated enhanced
resistance to early blight caused by Alternaria solani Sorauer. Root colonization induced the expression
of defense-related enzymes (PR1, PR2, and PR3) and genes (LOX, AOC, and PAL) in the leaves upon
pathogen challenge. These results further suggest that the JA pathway is essential for mediating such
systemic responses (Song et al., 2015).
In maize (Zea mays), inoculation with G. mosseae significantly reduced the incidence and severity of
sheath blight caused by Rhizoctonia solani. This effect was observed in two varieties: Gaoyou-115
(susceptible) and Yuenong-9 (resistant). The symbiosis led to a significant increase in 2,4-dihydroxy-
7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), a critical phytoalexin in maize involved in
systemic defense. DIMBOA accumulation occurred in the roots of both varieties and specifically in the
leaves of the resistant plants. These chemical changes were supported by the strong activation of
defense-related genes, including BX9-a key gene in the DIMBOA biosynthetic pathway-in the leaves
of both varieties (Song et al., 2011).
weight. Although the exact mechanism remains unknown, the authors proposed three potential
explanations: physical, nutritional, and/or chemical effects (Gange, 2001). Subsequently, Fontana et al.
(2009) found that P. lanceolata plants inoculated with G. intraradices emitted lower amounts of
sesquiterpenes during Spodoptera littoralis herbivory but showed an increased emission of the green
leaf volatile (Z)-3-hexenyl acetate, which is considered an indirect defense signal.
Medicago truncatula plants colonized by G. intraradices exhibited increased resistance to the virulent
bacterial pathogen Xanthomonas campestris. This resistance was associated with transcriptional
changes in both roots and shoots; notably, many of the genes induced in the shoots are predicted to be
involved in stress and defense responses (Liu et al., 2007). Similarly, tomato plants colonized with G.
fasciculatum showed systemic induced resistance (SIR) to the foliar pathogen Alternaria alternata.
Mycorrhizal plants displayed a three-fold increase in lipoxygenase (LOX) activity compared to control
plants, a finding supported by the up-regulation of genes involved in jasmonic acid (JA) biosynthesis
and salicylic acid (SA) signaling (Nair et al., 2015).
Consistent with these findings, tomato plants inoculated with F. mosseae demonstrated enhanced
resistance to early blight caused by Alternaria solani Sorauer. Root colonization induced the expression
of defense-related enzymes (PR1, PR2, and PR3) and genes (LOX, AOC, and PAL) in the leaves upon
pathogen challenge. These results further suggest that the JA pathway is essential for mediating such
systemic responses (Song et al., 2015).
In maize (Zea mays), inoculation with G. mosseae significantly reduced the incidence and severity of
sheath blight caused by Rhizoctonia solani. This effect was observed in two varieties: Gaoyou-115
(susceptible) and Yuenong-9 (resistant). The symbiosis led to a significant increase in 2,4-dihydroxy-
7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), a critical phytoalexin in maize involved in
systemic defense. DIMBOA accumulation occurred in the roots of both varieties and specifically in the
leaves of the resistant plants. These chemical changes were supported by the strong activation of
defense-related genes, including BX9-a key gene in the DIMBOA biosynthetic pathway-in the leaves
of both varieties (Song et al., 2011).
pág. 3000
CONCLUSIONS
Mycorrhizal colonization induces systemic metabolic shifts that extend from the roots to the aerial
components of the host plant. By integrating advanced analytical techniques, it is possible to
characterize a vast array of secondary metabolites regulated by the AMF symbiosis. Plant roots not only
synthesize specific compounds triggered by AMF but also enhance the biosynthesis of various
metabolites in aerial tissues, such as leaves, stems, and fruits.
These symbiotic interactions typically lead to an increased concentration of antioxidants, phenolics,
phytoalexins, organic acids, amino acids, lipids, fatty acids, carotenoids, terpenoids, flavonoids,
isoflavonoids, and polyamines. Conversely, the symbiosis may also result in the depletion of precursor
molecules as they are channeled into secondary metabolic pathways.
While the precise mechanisms by which AMF modulate metabolite concentrations remain to be fully
elucidated, the current literature indicates a frequent reduction in free amino acid pools. This trend
supports the hypothesis that these amino acids serve as primary substrates for the synthesis of more
complex secondary compounds in both roots and shoots.
BIBLIOGRAPHIC REFERENCES
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Asensio, D., Rapparini, F. and Peñuelas, J. (2012). AM fungi root colonization increases the production
of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions
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CONCLUSIONS
Mycorrhizal colonization induces systemic metabolic shifts that extend from the roots to the aerial
components of the host plant. By integrating advanced analytical techniques, it is possible to
characterize a vast array of secondary metabolites regulated by the AMF symbiosis. Plant roots not only
synthesize specific compounds triggered by AMF but also enhance the biosynthesis of various
metabolites in aerial tissues, such as leaves, stems, and fruits.
These symbiotic interactions typically lead to an increased concentration of antioxidants, phenolics,
phytoalexins, organic acids, amino acids, lipids, fatty acids, carotenoids, terpenoids, flavonoids,
isoflavonoids, and polyamines. Conversely, the symbiosis may also result in the depletion of precursor
molecules as they are channeled into secondary metabolic pathways.
While the precise mechanisms by which AMF modulate metabolite concentrations remain to be fully
elucidated, the current literature indicates a frequent reduction in free amino acid pools. This trend
supports the hypothesis that these amino acids serve as primary substrates for the synthesis of more
complex secondary compounds in both roots and shoots.
BIBLIOGRAPHIC REFERENCES
Aliferis, K. A., Chamoun, R. and Jabaji, S. (2015). Metabolic responses of willow (Salix purpurea L.)
leaves to mycorrhization as revealed by mass spectrometry and 1H NMR spectroscopy
metabolite profiling. Frontiers Plant Science, 6(344), doi: 10.3389/fpls.2015.00344
Asensio, D., Rapparini, F. and Peñuelas, J. (2012). AM fungi root colonization increases the production
of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions
or after jasmonic acid application. Phytochemistry 77: 149-161.
http://dx.doi.org/10.1016/j.phytochem.2011.12.012.
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Understanding the global diversity of host plants by resolving conflicting information and
developing reliable means of diagnosis. Plant and Soil, 320(1-2), 37-77.
https://doi.org/10.1007/s11104-008-9877-9.
Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R. and Bécard, G. (2000). The pre-symbiotic growth of
arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root
pág. 3001
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mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes.
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enhance growth, nutrient uptake and alter metabolic profile of sorghum grown in marginal soil.
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Duhamel, M., Pel, R., Ooms, A., Bücking, H., Jansa, J., Ellers, J., van Straalen, N. M., Wouda, T.,
Vandenkoornhuyse, P. and Kiers, E. T. (2013). Do fungivores trigger the transfer of protective
metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology, 94(9), 2019-2029.
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Eftekhari, M., Alizadeh, M. and Ebrahimi, P. (2012). Evaluation of the total phenolics and quercetin
content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest
drying on quercetin yield. Industrial Crops and Products, 38(1), 160-165.
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Ceccarelli, N., Curadi, M., Martelloni, L., Sbrana, C., Picciarelli, P. and Giovannetti, M. (2010).
Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke
leaves and flower heads two years after field transplant. Plant and Soil, 335(1), 311-323.
https://doi.org/10.1007/s11104-010-0417-z.
Charest, C., Dalpé, Y. and Brown, A. (1993). The effect of vesicular-arbuscular mycorrhizae and
chilling on two hybrids of Zea mays L. Mycorrhiz,. 4(1), 89-92.
https://doi.org/10.1007/BF00204064.
Chen, X., Song, F., Liu, F., Tian, C., Liu, S., Xu, H. and Zhu, X. (2014). Effect of different arbuscular
mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes.
The Scientific World Journal, 2014(956141), 1-7. http://dx.doi.org/10.1155/2014/956141.
De Deyn, G. B., Biere, A., van der Putten, W. H., Wagenaar, R. and Klironomos, J. N. (2009). Chemical
defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia,
160(3), 433-442. https://doi.org/10.1007/s00442-009-1312-2.
Dhawi, F., Datta, R. and Ramakrishna, W. (2016). Mycorrhiza and heavy metal resistant bacteria
enhance growth, nutrient uptake and alter metabolic profile of sorghum grown in marginal soil.
Chemosphere, 157, 33-41. https://doi.org/10.1016/j.chemosphere.2016.04.11.2
Duhamel, M., Pel, R., Ooms, A., Bücking, H., Jansa, J., Ellers, J., van Straalen, N. M., Wouda, T.,
Vandenkoornhuyse, P. and Kiers, E. T. (2013). Do fungivores trigger the transfer of protective
metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology, 94(9), 2019-2029.
http://www.jstor.org/stable/23597324
Dumas, E., Gianinazzi-Pearson, V. and Gianinazzi, S. (1990). Production of new soluble proteins during
VA endomycorrhiza formation. Agriculture, Ecosystems & Environment, 29(1-4): 111-114.
https://doi.org/10.1016/0167-8809(90)90264-E.
Eftekhari, M., Alizadeh, M. and Ebrahimi, P. (2012). Evaluation of the total phenolics and quercetin
content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest
drying on quercetin yield. Industrial Crops and Products, 38(1), 160-165.
pág. 3002
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Engel, R., Szabó, K., Abrankó, L., Rendes, K., Füzy, A. and Takács, T. (2016). Effect of arbuscular
mycorrhizal fungi on the growth and polyphenol profile of marjoram, lemon balm, and
marigold. Journal of Agricultural and Food Chemistry, 64(19), 3733-3742.
http://dx.doi.org/10.1021/acs.jafc.6b00408.
Evelin, H. and Kapoor, R. (2014). Arbuscular mycorrhizal symbiosis modulates antioxidant response
in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza, 24(3), 197-208.
https://doi.org/10.1007/s00572-013-0529-4.
Fester, T., Fetzer, I., Buchert, S., Lucas, R., Rillig, M. C. and Härtig, C. (2011). Towards a systemic
metabolic signature of the arbuscular mycorrhizal interaction. Oecologia, 167(4): 913-924. DOI
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Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J. and Unsicker, S. B. (2009). The effects of
arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata
L. Journal of Chemical Ecology, 35(7), 833–843. DOI 10.1007/s10886-009-9654-0.
Gange, A. C. (2001). Species-specific responses of a root and shoot-feeding insect to arbuscular
mycorrhizal colonization of its host plant. New Phytologist, 150(3), 611–618.
https://doi.org/10.1046/j.1469-8137.2001.00137.x.
Garg, N. and Manchanda, G. (2009). Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic
and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea). Journal of
Agronomy and Crop Science, 195(2), 110-123. https://doi.org/10.1111/j.1439-
037X.2008.00349.x
Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange,
S., Bécard, G., Bonfante, P. and Barker, D. G. (2013). Short-chain chitin oligomers from
arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their
production is enhanced by strigolactone. New Phytologist, 198(1), 190-202.
https://doi:10.1111/nph.12146.
Gerlach, N., Schmitz, J., Polatajko, A., Schlüter, U., Fahnenstich, H., Witt, S., Fernie, A. R., Uroic, K.,
Scholz, U., Sonnewald, U. and Bucher, M. (2015). An integrated functional approach to dissect
https://doi.org/10.1016/j.indcrop.2012.01.022.
Engel, R., Szabó, K., Abrankó, L., Rendes, K., Füzy, A. and Takács, T. (2016). Effect of arbuscular
mycorrhizal fungi on the growth and polyphenol profile of marjoram, lemon balm, and
marigold. Journal of Agricultural and Food Chemistry, 64(19), 3733-3742.
http://dx.doi.org/10.1021/acs.jafc.6b00408.
Evelin, H. and Kapoor, R. (2014). Arbuscular mycorrhizal symbiosis modulates antioxidant response
in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza, 24(3), 197-208.
https://doi.org/10.1007/s00572-013-0529-4.
Fester, T., Fetzer, I., Buchert, S., Lucas, R., Rillig, M. C. and Härtig, C. (2011). Towards a systemic
metabolic signature of the arbuscular mycorrhizal interaction. Oecologia, 167(4): 913-924. DOI
10.1007/s00442-011-2037-6.
Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J. and Unsicker, S. B. (2009). The effects of
arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata
L. Journal of Chemical Ecology, 35(7), 833–843. DOI 10.1007/s10886-009-9654-0.
Gange, A. C. (2001). Species-specific responses of a root and shoot-feeding insect to arbuscular
mycorrhizal colonization of its host plant. New Phytologist, 150(3), 611–618.
https://doi.org/10.1046/j.1469-8137.2001.00137.x.
Garg, N. and Manchanda, G. (2009). Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic
and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea). Journal of
Agronomy and Crop Science, 195(2), 110-123. https://doi.org/10.1111/j.1439-
037X.2008.00349.x
Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange,
S., Bécard, G., Bonfante, P. and Barker, D. G. (2013). Short-chain chitin oligomers from
arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their
production is enhanced by strigolactone. New Phytologist, 198(1), 190-202.
https://doi:10.1111/nph.12146.
Gerlach, N., Schmitz, J., Polatajko, A., Schlüter, U., Fahnenstich, H., Witt, S., Fernie, A. R., Uroic, K.,
Scholz, U., Sonnewald, U. and Bucher, M. (2015). An integrated functional approach to dissect
pág. 3003
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https://doi.org/10.1094/mpmi-01-11-0019.
Hajiboland, R., Aliasgharzadeh, N., Laiegh, S. F. and Poschenrieder, C. (2010). Colonization with
arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.)
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Hodge, A. and A.H. Fitter. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi
from organic material has implications for N cycling. Proceedings of the National Academy of
Sciences of the United States of America, 107(31), 13754-13759.
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Hubberten, H. M., Sieh, D., Zöller, D., Hoefgen, R. and Krajinski, F. (2015). Medicago truncatula
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Jurkiewicz, A., Ryszka, P., Anielska, T., Waligórski, P., Białońska, D., Góralska, K., Tsimilli-Michael,
M. and Turnau, K. (2010). Optimization of culture conditions of Arnica montana L.: Effects of
mycorrhizal fungi and competing plants. Mycorrhiza, 20(5), 293-306.
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Kapoor, R., Chaudhary, V. and Bhatnagar, A. K. (2007). Effects of arbuscular mycorrhiza and
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arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.)
plants. Plant and Soil, 331(1), 313–327. https://doi.org/10.1007/s11104-009-0255-z.
Hodge, A. and A.H. Fitter. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi
from organic material has implications for N cycling. Proceedings of the National Academy of
Sciences of the United States of America, 107(31), 13754-13759.
https://doi.org/10.1073/pnas.1005874107.
Hubberten, H. M., Sieh, D., Zöller, D., Hoefgen, R. and Krajinski, F. (2015). Medicago truncatula
Mtha1-2\n mutants loose metabolic responses to mycorrhizal colonization. Plant Signaling &
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Jurkiewicz, A., Ryszka, P., Anielska, T., Waligórski, P., Białońska, D., Góralska, K., Tsimilli-Michael,
M. and Turnau, K. (2010). Optimization of culture conditions of Arnica montana L.: Effects of
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581–587. https://doi.org/10.1007/s00572-007-0135-4.
Kee, Y. J., Ogawa, S., Ichihashi, Y., Shirasu, K. and Yoshida, S. (2023). Strigolactones in rhizosphere
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Kempel, A., Schmidt, A. K., Brandl, R. and Schädler, M. (2010). Support from the underground:
Induced plant resistance depends on arbuscular mycorrhizal fungi. Functional Ecology, 24(2),
293–300. https://doi.org/10.1111/j.1365-2435.2009.01647.x.
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17, 291-297 https://doi.org/10.1007/s00572-006-0104-3.
Vannette, R.L., Hunter, M. D. and Rasmann, S. (2013). Arbuscular mycorrhizal fungi alter above- and
below-ground chemical defense expression differentially among Asclepias species. Frontiers in
Plant Science. 4, 361. https://doi.org/10.3389/fpls.2013.00361.
Wang, B., Yeun, L. H., Xue, J. Y., Liu, Y., Ané, J. M. and Qiu, Y. L. (2010). Presence of three
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Zhu, X., Song, F. and Liu, S. (2011). Arbuscular mycorrhiza impacts on drought stress of maize plants
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Agriculture and Environment, 9(2), 583-587.
Zhu, X. C., Song, F. B. and Xu, H. W. (2010). Arbuscular mycorrhizae improves low temperature stress
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ZhongQun, H., ChaoXing, H., ZhiBin, Z., ZhiRong, Z. and HuaiSong, W. (2007). Changes of
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P. (2014). From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis
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2164-15-221.
Zubek, S., Mielcarek, S. and Turnau, K. (2012). Hypericin and pseudohypericin concentrations of a
valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal
fungi. Mycorrhiza, 22(2), 149-156. https://doi.org/10.1007/s00572-011-0391-1.
Zubek, S., Stojakowska, A., Anielska, T. and Turnau, K. (2010). Arbuscular mycorrhizal fungi alter
thymol derivative contents of Inula ensifolia L. Mycorrhiza, 20(7), 497-504.
https://doi.org/10.1007/s00572-010-0306-6.
https://doi.org/10.1016/j.colsurfb.2007.04.023 .
Zouari, I., Salvioli, A., Chialva, M., Novero, M., Miozzi, L., Tenore, G. C., Bagnaresi, P. and Bonfante,
P. (2014). From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis
may affect tomato fruit metabolism. BMC genomics, 15(1), 221. https://doi.org/10.1186/1471-
2164-15-221.
Zubek, S., Mielcarek, S. and Turnau, K. (2012). Hypericin and pseudohypericin concentrations of a
valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal
fungi. Mycorrhiza, 22(2), 149-156. https://doi.org/10.1007/s00572-011-0391-1.
Zubek, S., Stojakowska, A., Anielska, T. and Turnau, K. (2010). Arbuscular mycorrhizal fungi alter
thymol derivative contents of Inula ensifolia L. Mycorrhiza, 20(7), 497-504.
https://doi.org/10.1007/s00572-010-0306-6.