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. 2018 Aug 14;9:1089. doi: 10.3389/fpls.2018.01089

Table 1.

Secondary metabolites and antioxidant activities in mycorrhizal food plants.

Plant species Variety or cultivar AMF species Measured metabolites/antioxidant activity assay method Effect of AMF inoculation References
(A) GREENHOUSE OR MESOCOSM EXPERIMENTS
Solanum lycopersicum L.
graphic file with name fpls-09-01089-i0001.jpg F1 Hybrid, GS-15 Mix of: Glomus intraradices, Glomus mosseae, Glomus etunicatum (Soil and Water Institute of Iran) Lycopene (FW)
DPPHa
Increased concentration
Increased activity
Ordookhani et al., 2010
Guadalete Mix of: Glomus mosseae, Glomus caledonium, Glomus viscosum, Glomus intraradices, Glomus coronatum Lycopene and β-carotene
Lutein
Ascorbic acid
No effect

No effect
Decreased concentration
Copetta et al., 2011
Moneymaker Glomus intraradices IMA6 Lycopene (FW)
Total phenols (FW)
Ascorbic acid (FW)
Glutathione (FW)
ABTSb (FW)
Increased concentration
No effect
No effect
No effect
No effect
Giovannetti et al., 2012
Nemo-Netta Glomus mosseae (Biocult Ltd., South Africa) Lycopene (FW)

Total flavonoids (FW)
Ascorbic acid (FW)
ABTS
Increased concentration, only at late inoculation time
No effect
No effect
No effect
Nzanza et al., 2012b
Moneymaker Funneliformis mosseae BEG12 and/or Rhizophagus irregularis BB-E (Agrauxine, F) Lycopene (FW) Mixed inoculation: no effect; single isolate inoculation: increased concentration Hart et al., 2015
β-carotene and
total carotenoids (FW)
Mixed inoculation: increased concentration;
single isolate inoculation: no effect
29 Odor-active volatile compounds Distinct phytochemical profiles, but variable quantitative effects
Komeett Rhizophagus irregularis (Premier Tech Inc., Canada) DPPH (DW)
Vitamins B1, B3, B5, B6, ascorbic acid (FW)
Vitamin B6, ascorbic acid (DW)
Total carotenoids (DW)
No effect
No effect

Decreased concentration

Increased concentration
Hart et al., 2015
Capsicum annuum L.
graphic file with name fpls-09-01089-i0002.jpg San Luis Glomus fasciculatum or Mix1 (Glomus constrictum, Glomus geosporum, Glomus fasciculatum, Glomus tortuosum) or Mix2 (Glomus aggregatum, Glomus deserticola, Glomus geosporum, Glomus microaggregatum, Sclerocystis coremioides) Carotenes

Xanthophylls

Capsaicinoids
Increased concentration by Mix2
Increased concentration by Mix2
No effect
Mena-Violante et al., 2006
Cacho de cabra Glomus intraradices (commercial) Glomus claroideum (native) Ascorbic acid (FW) Increased concentration (native), no effect (commercial) Castillo et al., 2009
Fragaria x ananassa Duch.
graphic file with name fpls-09-01089-i0003.jpg Aromas Glomus intraradices (Premier Tech Biotechnologies Company, Canada) Total phenols (DW)
p-coumaric acid (DW)


Gallic, ferulic, ellagic acids (DW)

Cyanidin-3-glucoside (DW)
Pelargonidin-3-glucoside (DW)
Quercetin and kaempferol (DW)
Catechin (DW)
No effect
Increased concentration at intermediate N

No effect or decreased concentration depending on N concentration
Increased concentration at intermediate N
No effect

Increased concentration at intermediate N
No effect
Castellanos Morales et al., 2010
Selva Mix (Mybasol, Italy) Pelargonidin 3-glucoside, Pelargonidin 3-rutinoside and pelargonidin malonyl glucoside (FW)
Pelargonidin acetyl glucoside and cyanidin 3-glucoside (FW)
Total pelargonidins (FW)
Increased concentration





No effect


Increased concentration
Lingua et al., 2013
Selva Mix of: Rhizophagus intraradices, Glomus aggregatum, Glomus viscosum, Claroideoglomus etunicatum, Claroideoglomus claroideum (Mybasol) Ascorbic acid (FW)

Folate (FW)
Increased concentration

No effect
Bona et al., 2015
Fortuna


Sabrina



Splendor
Glomus iranicum var. tenuihypharum (Mycogrowth®, Spain) Total phenols and
Anthocyanins (FW)

Ascorbic acid (FW)
Total phenols, anthocyanins and ascorbic acid (FW)
Total phenols and
Ascorbic acid (FW)
Anthocyanins (FW)
Increased concentration at early inoculation

No effect
No effect


No effect

Decreased concentration
Cecatto et al., 2016
Lactuca sativa L.
graphic file with name fpls-09-01089-i0004.jpg var. capitata, Batavia Rubia Munguía


var. capitata, Maravilla de Verano
Glomus fasciculatum Carotenoids (FW)

Total phenols and ascorbic acid (FW)
Anthocyanins (FW)
Carotenoids, total phenols and ascorbic acid (FW)
Anthocyanins (FW)
Increased concentration depending on leaf position
No effect

Increased concentration
No effect


Increased concentration
Baslam et al., 2011
var. longifolia, Cogollos de Tudela Glomus fasciculatum or Mix of: Glomus intraradices, Glomus mosseae (Atens, Spain) Carotenoids (FW)
Total phenols (FW)

Anthocyanins (FW)

Ascorbic acid (FW)
No effect
Increased concentration in outer leaves
Increased concentration in inner leaves
Increased concentration in inner leaves by G. fasciculatum
Batavia Rubia Munguía Mix of: Rhizophagus intraradices, Funneliformis mosseae (Atens) Carotenoids (FW)


Total phenols (FW)
Anthocyanins (FW)


Ascorbic acid (FW)
Decreased concentration in autumn in inner leaves and increased in spring
No effect
Increased concentration in winter and spring in inner leaves
Increased concentration in winter and spring in outer leaves
Baslam et al., 2013
Maravilla de Verano Carotenoids (FW)


Total phenols (FW)
Anthocyanins (FW)


Ascorbic acid (FW)
Increased concentration in winter and spring in inner leaves
No effect
Increased concentration in winter in outer leaves and spring in inner leaves
No effect
Batavia Rubia Munguía and Maravilla de Verano Mix of: Rhizophagus intraradices, Funneliformis mosseae (Atens) Total carotenoids (DW) Increased concentration in Batavia Rubia Munguía Goicoechea et al., 2015
Epidermal flavonols

Anthocyanins (by optical monitoring)
Soluble phenols (DW)
DPPH (DW)
Decreased levels in Batavia Rubia Munguía
No effect

No effect
Increased activity in Batavia Rubia Munguía, decreased in Maravilla de Verano
not available Rhizophagus intraradices Superoxide dismutase and catalase
Ascorbate peroxidase
Glutathione reductase
Total carotenoids (FW)
Increased activity

Reduced activity
No effect
Increased concentration
Durán et al., 2016
var. crispa Eluarde and Panisse Funneliformis mosseae AZ225C or Rhizoglomus irregulare IMA6 (formerly Glomus intraradices) ORACc (FW)
Total phenolics (FW)

Total anthocyanins (FW) (only Eluarde)
Increased activity
Increased concentrations with IMA6
Increased concentrations
Avio et al., 2017
Ocimum basilicum L.
graphic file with name fpls-09-01089-i0005.jpg Genovese Glomus mosseae BEG 12, or Gigaspora margarita BEG 34, or Gigaspora rosea BEG 9 Essential oils (13 terpenoids and 2 phenolic compounds) Variable depending on AMF and compound Copetta et al., 2006, 2007
Genovese Italian and
Purple Petra
Glomus intraradices (Native Plants Incorporated, USA) Total anthocyanins (FW)

Total phenolics and phenolic acids (FW)
Increased concentration in Purple Petra
No effect
Lee and Scagel, 2009
not available Glomus fasciculatum or Glomus etunicatum or Glomus intraradices Total essential oils (DW) Increased concentration and distinct phytochemical profiles Rasouli-Sadaghiani et al., 2010
Cinnamon, Siam Queen, Sweet Dani and Red Rubin Rhizophagus intraradices (Native Plants Incorporated) Total anthocyanins (FW)
Total phenolics (FW)
Phenolic acids (FW)
Total flavonoids (FW)
Increased concentration in Red Rubin
No effect
Increased concentration
No effect
Scagel and Lee, 2012
Tigullio and Dark Opal Rhizoglomus irregulare IMA6 (formerly Glomus intraradices) ABTS (DW)
Total carotenoids (DW)
Total phenolics (DW)
Anthocyanins (DW) (Dark Opal)
Rosmarinic acid (DW)
No effect
Decreased concentration
No effect
Decreased concentration

Decreased concentration
Battini et al., 2016b
Cynara cardunculus L. var. scolymus
graphic file with name fpls-09-01089-i0006.jpg Terom Glomus mosseae AZ 225C and/or Glomus intraradices IMA6 Total phenolics (FW) and
DPPH
Increased concentration and activity with dual inoculation and G.intraradices Ceccarelli et al., 2010
Allium cepa L.
graphic file with name fpls-09-01089-i0007.jpg Centurion Mix of: Glomus mosseae, Glomus intraradices, Glomus claroideum, Glomus microaggregatum (Plantworks, UK) Organosulfur compounds (as total pyruvic acid) and total phenolics (DW)

Quercetin monoglycoside (DW)
Quercetin diglycoside (DW)
ABTS and ESRd (DW)
No effect




Increased concentration when NO3--N predominant
No effect

Increased activity when NO3--N predominant
Perner et al., 2008
Nasik red N-53 Mix of: Glomus intraradices, Glomus mosseae Total phenolics (FW) Increased concentration Lone et al., 2015
Alice Mix of: Glomus etunicatum, Glomus microaggregatum, Glomus intraradices, Glomus claroideum, Glomus mosseae, Glomus geosporum (Symbivit, Czech Rep.) or Glomus intraradices BEG140 FRAPe
Ascorbic acid (FW)
Increased activity with Mix
No effect
Albrechtova et al., 2012
Stuttgarter Riesen Mix of: Funneliformis mosseae and Rhizophagus irregularis (INOQ, Germany) Quercetin-diglucoside and quercetin-monoglucoside

Isorhamnetin-glucoside
Increased concentration at high inoculation amount and when NH4+-N predominant
No effect
Mollavali et al., 2018
Ipomea batatas L.
graphic file with name fpls-09-01089-i0008.jpg not available Glomus intraradices (IFP Glintra, INOQ) and/or Glomus mosseae (IFP Glm, INOQ) β-carotene (DW) Increased concentration Tong et al., 2013
(B) FIELD EXPERIMENTS
Solanum lycopersicum L.
graphic file with name fpls-09-01089-i0001.jpg PKM-1 Glomus intraradices # TNAU 120-02 Ascorbic acid (FW) Increased concentration Subramanian et al., 2006
Vitella F1 Glomus sp. (Amykor, Germany) Lycopene (FW)
β-carotene and
Total phenols (FW)
Increased concentration
Increased concentration, under organic management
Ulrichs et al., 2008
Nemo-Netta Glomus mosseae (Biocult Ltd., South Africa) Ascorbic acid (FW) Increased concentration Nzanza et al., 2012a
TC 2000 Mix of: Rhizophagus intraradices, Glomus aggregatum, Glomus viscosum, Claroideoglomus etunicatum and Claroideoglomus claroideum (Mybasol, Italy) Lycopene
β-carotene (FW)
Ascorbic acid (FW)
No effect
No effect
Decreased concentration
Bona et al., 2017
Perfect Peel, Roma, Rio Grande Mix of: Rhizoglomus irregulare IMA6 (formerly Glomus intraradices), Funneliformis mosseae IMA1 Lycopene (FW) No effect Njeru et al., 2017
Cynara cardunculus L. var. scolymus
graphic file with name fpls-09-01089-i0009.jpg Terom Glomus mosseae AZ 225C and/or Glomus intraradices IMA6 Total phenolics (FW)
DPPH
Increased concentration
Increased activity, only with dual inoculation in the second year
Ceccarelli et al., 2010
Romanesco' type cv. C3 Mix of: Glomus mosseae, Glomus intraradices (Italpollina, Italy) (Aeg) or Glomus intraradices (Tecnologiás Naturales Internacional, Mexico) (End) ABTS (DW)
Total phenolics (DW)
No effect
Increased concentration with End; variation in phenolic acids and flavonoid profiles
Palermo et al., 2013
Violetto di Sicilia Glomus viscosum (syn. Septoglomus viscosum) Caffeoylquinic acids,
apigenin and
luteolin (DW)
Increased concentration in receptacles, compared to traditional vegetative reproduced plants Pandino et al., 2017
Romolo and Istar Mix of: Rhizophagus intraradices BEG72, Funneliformis mosseae (Italpollina, Italy) Total phenolics (DW)


ABTS (DW)
DPPH (DW)
Increased concentration in primary heads, decreased in secondary heads
Increased activities
Increased activities in primary heads, no effect or reduced activity in secondary heads depending on cultivar
Rouphael et al., 2017
Allium cepa L.
graphic file with name fpls-09-01089-i0010.jpg Hyskin Vaminoc (MicroBio, UK) or Glomus intraradices BEG87 Quercetin (FW) No effect Mogren et al., 2007
Ipomea batatas L.
graphic file with name fpls-09-01089-i0011.jpg Hongxin Glomus etunicatum BEG 168, Glomus etunicatum HB-Bd45-Gsp4, Glomus intraradices BEG 141, and a mix of them (M3); Glomus mosseae BEG 167, a mix of M3 and BEG 167 (M4); mix of : Glomus intraradices and Glomus mosseae (Biorize, France) Carotene No effect Farmer et al., 2007

Data are reported on a fresh weight (FW) or dry weight (DW) basis; where unspecified, no information was available. The binomial nomenclature of AMF reported in the quoted papers has been maintained.

a

DPPH, 2,2-Diphenyl-1-picrylhydrazyl assay;

b

ABTS, 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) assay;

c

ORAC, oxygen radical absorbance capacity assay;

d

ESR, electron spin resonance spectroscopy;

e

FRAP, ferric reducing ability of plasma assay.