© The Authors, 2022, Published by the Universidad del Zulia
*Corresponding author: bmurillo04@cibnor.mx
Yuneisy Milagro Agüero-Fernández
Bernardo Murillo-Amador*
José Manuel Mazón-Suástegui
Alejandra Nieto-Garibay
Carlos Michel Ojeda-Silvera
Daulemys Batista-Sánchez
Rev. Fac. Agron. (LUZ). 2022, 39(2): e223953
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n4.08
Crop Production
Associate editor: Professor Andreina García
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
Keywords:
Arbuscular mycorrhizal fungi
Basil
Abiotic stress
Biochemistry
Biochemical response of Ocimum basilicum L. inoculated with Rhizophagus fasciculatus as a
NaCl-stress mitigator
Respuesta bioquímica de Ocimum basilicum L. inoculado con Rhizophagus fasciculatus como
mitigador del estrés por NaCl
Resposta bioquímica de Ocimum basilicum L. inoculado com Rhizophagus fasciculatus como
mitigador de estresse por NaCl
Centro de Investigaciones Biológicas del Noroeste S.C.,
Avenida Instituto Politécnico Nacional No. 195. Colonia Playa
Palo de Santa Rita Sur. La Paz, Baja California Sur, México.
C.P. 23096.
Received: 05
-07-2022
Accepted: 24-10-2022
Published: 24-11-2022
Abstract
Basil (Ocimum basilicum L.) is a medicinal and aromatic plant of
commercial interest; it can be grown in salinized soils by applying a stress
mitigator. The objective was to evaluate the biochemical response of two
basil varieties inoculated with AMF Rhizophagus fasciculatus and appraise
its usefulness as a NaCl-stress mitigator. A completely randomized design
with a factorial arrangement, four replicates per treatment and four plants
per replicate was used. Three factors were considered, (1) two basil varieties
(Napoletano and Nufar); (2) three NaCl concentrations (0, 50 and 100 mM);
and (3) R. fasciculatus inoculum absence or presence (0 and 10 g). The
variables evaluated were a substrate chemical analysis; shoot (STP) and root
(RTP) total protein content; shoot (SP) and root (RP) proline content; shoot
(SGA) and root (RGA) glutathione peroxidase activity; spore count and
colonization. The spore content was 50 to 70 spores per gram of inoculum.
The STP and RTP were highest in both varieties in 0 mM with AMF and
decreased in Napoletano in 100 mM. The SP and RP were highest in Nufar in
50 and 100 mM with AMF and lowest in Napoletano in 0 and 50 with AMF.
The SGA and RGA were highest in Napoletano in 50 and 100 mM with
AMF. The colonization was high; however, decreased as NaCl increased.
These results suggest that inoculation with AMF has a positive effect to
mitigate NaCl-stress and a biochemical benet for basil plants.
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Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239533 October-December. ISSN 2477-9407.
2-6 |
Resumen
La albahaca (Ocimum basilicum L.) es una planta medicinal y
aromática; se puede cultivar en suelos salinizados aplicando un
mitigador del estrés. El objetivo fue evaluar la respuesta bioquímica
de dos variedades de albahaca inoculadas con HMA Rhizophagus
fasciculatus y valorar su utilidad como mitigador del estrés por NaCl.
Se utilizó un diseño completamente al azar con arreglo factorial con
cuatro repeticiones por tratamiento y cuatro plantas por repetición.
Se consideraron tres factores, (1) dos variedades de albahaca
(Napoletano y Nufar); (2) tres concentraciones de NaCl (0, 50 y 100
mM) y (3) ausencia o presencia del inóculo R. fasciculatus (0 y 10
g). Las variables evaluadas fueron el análisis químico del sustrato;
contenido total de proteínas en brotes (PTB) y raíces (PTR); prolina
en brotes (PB) y raíces (PR); actividad del glutatión peroxidasa en
brotes (GPB) y raíces (GPR) y colonización. El contenido de esporas
fue de 50 a 70 esporas por gramo de inóculo. La PTB y PTR fueron
mayores en ambas variedades en 0 mM con HMA y disminuyó en
Napoletano en 100 mM. La PB y PR fueron mayores en Nufar en 50
y 100 mM con HMA y menores en Napoletano en 0 y 50 con HMA.
La GPB y GPR fueron mayores en Napoletano en 50 y 100 mM con
HMA. La colonización fue alta, pero disminuyó conforme aumentó
NaCl. Estos resultados muestran que la inoculación con HMA
tiene efecto positivo para mitigar el estrés por NaCl y un benecio
bioquímico para albahaca.
Palabras clave: Hongos micorrízicos arbusculares, albahaca, estrés
abiótico, bioquímica.
Resumo
Manjericão (Ocimum basilicum L.) é uma planta medicinal e
aromática de interesse comercial; puede cultivarse em solos salinizados
aplicando um atenuador. O objetivo foi avaliar a resposta bioquímica
de manjericão inoculada com FMA Rhizophagus fasciculatus
e avaliar sua utilidade como mitigador de NaCl. Utilizou-se o
delineamento inteiramente casualizado com arranjo fatorial, quatro
repetições por tratamento e quatro plantas por repetição. Três fatores
foram considerados, (1) duas variedades de manjericão (Napoletano
e Nufar); (2) três concentrações de NaCl (0, 50 e 100 mM); e (3)
ausência ou presença de inóculo (0 e 10 g). As variáveis avaliadas
foram uma análise química do substrato; teor de proteína total da parte
aérea (STP) e da raiz (RTP); conteúdo de prolina da parte aérea (SP) e
da raiz (RP); atividade da glutationa peroxidase da parte aérea (SGA)
e da raiz (RGA); contagem de esporos e colonização. O conteúdo
de esporos foi de 50 a 70 esporos por grama de inóculo. O STP e
RTP foram maiores em ambas as variedades em 0 mM com FMA e
diminuíram em Napoletano em 100 mM. O SP e RP foram maiores
em Nufar em 50 e 100 mM com FMA e menores em Napoletano em
0 e 50 com FMA. O SGA e RGA foram maiores em Napoletano em
50 e 100 mM com FMA. A colonização foi alta; no entanto, diminuiu
à medida que o NaCl aumentou. Esses resultados sugerem que a
inoculação com FMA tem um efeito positivo para mitigar o estresse
por NaCl e um benefício bioquímico para manjericão.
Palabras-chave: Fungos micorrízicos arbusculares, manjericão,
estresse abiótico, bioquímica.
Introduction
Soil salinization in agricultural production areas is increasing
worldwide and implies challenges to researchers due to its foreseeable
negative impact in the short, medium, and long term. High salinity
promotes imbalance in plant metabolism and in its osmotic
relationships with soil (Agüero-Fernández et al., 2018). The plants
activate physiological mechanisms, such as osmotic adjustment to
ensure ionic homeostasis in response to saline-stress. The increment
of Na and Cl contents in soil produce a decrease in osmotic potential,
and subsequently, in water potential, avoiding ionic toxicity and
interference in the assimilation of important cations. At genetic level,
this adjustment induces the osmotically active organic compound
synthesis, such as glycine-betaine and proline and modies protein
metabolism (González et al., 2005). Proline, betaine, glycine betaine,
various carbohydrates and osmotically active proteins are synthesized
in plants and used as indicators to select tolerant genotypes to
salinity-stress (Feitosa de Lacerda et al., 2001). Some studies have
been demonstrated that, the arbuscular mycorrhizal fungus (AMF)
colonize the roots as an environmental alternative to increases
tolerance to salinity and improves crop productivity (Medina-García,
2016; Agüero-Fernández et al., 2018). Arbuscular mycorrhizal
symbiosis is the effect of benecial interaction among roots and AMF,
so the fungus receives photosynthates from the plant and improves its
ability to absorb nutrients and water, increasing its tolerance stress
(Aggarwal et al., 2012). Mycorrhizal colonization produces physical,
biochemical, and physiological changes in roots. These changes
improve the plant conditions and contribute to alleviating stress
(Medina-García, 2016).
Mexico has regions with great potential to produce aromatic
species. One of them is Baja California Sur, with the highest
production of certied organic basil (SIAP, 2021). Basil generates
income and is an economic and technological diversication for many
farmers. Basil added value derives from its medicinal and culinary
properties (Juárez-Rosete et al., 2013) with therapeutic applications
around the world (Masarovičová and Králóvá, 2007). Baja California
Sur is a semiarid region which soil and water for agriculture tend
to salinization (Mazón-Suástegui et al., 2018). The objective of the
study was to evaluate the biochemical response of two basil varieties
inoculated with AMF R. fasciculatus and appraise its usefulness as a
NaCl-stress mitigator.
Materials and methods
Experimental area
The experiment was carried-out in the Biological Research
Center of the Northwest, S.C. (CIBNOR) located in La Paz, Baja
California Sur, Mexico at 24° 08’ 10.03 LN and 110° 25 ‘35.31 LW,
at 7 m.a.s.l. The experiment was done inside a greenhouse with roof
covered with white anti-aphid model 55. 30 % shade mesh. Under this
mesh, another black mesh model 20 with 35 % shade was placed for
a total shading of 65 %. The site has a type Bw (h’) hw (e) climate
considered as semi-arid with xerophilous vegetation (García, 2004).
The temperatures mean, maximum and minimum in the site were 29°,
30° and 25° C, respectively; the mean relative humidity was 67 %,
dew point of 21°C, with a total precipitation of 14.6 mm and solar
radiation of 293.3 Wm
2
. The weather variables were logged with a
weather station (Vantage Pro2
®
Davis Instruments, USA).
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Agüero-Fernández et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e223953
3-6 |
Basil plant material
The seeds of Napoletano and Nufar varieties with differential
response to NaCl (Batista-Sánchez et al., 2017) were obtained from
the Vis Seed Company
®
(Arcadia, CA, USA).
Seedling production
The seeds were disinfected by soaking for 5 min in calcium
hypochlorite with 5 % active chlorine and successively washed with
sterilized distilled water. Then, were sown in 50-cavity polystyrene
trays with a commercial sterile medium-size expanded horticultural
mineral perlite as substrate (Hortiperl, Termolita
®
S.A de C.V.,
Mexico). Irrigation was applied daily to achieve a uniform seedling
emergence, which was attained at 7 days after sown.
Transplant and experimental design
Transplant was performed when seedlings had an average height
of 15 cm, placing one in each pot of ~10 kg, using the commercial
substrate mentioned. The experimental design was completely
randomized with factorial arrangement being factor 1, two varieties
(Napoletano and Nufar); factor 2, three NaCl (0, 50, and 100 mM)
concentrations; and factor 3, presence or absence of the AMF
R. fasciculatus (0 and 10 g of inoculum) with four replications
per treatment and four plants per replication. The duration of the
experiment was 100 days after transplant with four harvests of
biomass and the evaluation of other variables. The biochemical
variables were determined 50 days after transplant.
Inoculation, irrigation, and nutrition
The AMF R. fasciculatus belong to the CIBNOR no commercial
collection. The seedlings were inoculated with AMF during transplant,
using the dose (control and 10 g of the inoculum), depositing the
inoculum at the bottom of each seedling according to Rivera et al.
(2003). The 10 g of AMF is equivalent to 50-70 spores per gram of
inoculum. Irrigation began with daily application using water with
an electrical conductivity (EC) of 0.04 dS.m
-1
and a nutrient solution
(Samperio, 1997) which was modied in P
+
content, that is, P
+
was
not included in the nutrient solution. One week after transplant, the
gradual application of NaCl began when the plants were established.
The amount applied daily per irrigation was 500 mL, allowing that
the applied solution drained through the holes of the pots to avoid
NaCl accumulation in the substrate. The pH and EC readings were
taken after preparation the saline solution and subsequently to the
drained liquid to compare the values of pH and EC (prepared and
drained). No changes were detected in the drained solution.
Chemical analysis of the substrate (mineral perlite)
The samples of the substrate used were taken and sieved with
mesh No. 10 (2 mm). The EC and pH were determined with a soil
solution ratio of 1:5 using a potentiometer (Hanna
®
, Model 211,
USA) (Jackson, 1958). Electrical conductivity was measured with a
conductivity meter (Hach
®
, Model Sension+, Loveland, CO, USA)
(Jackson, 1976). Phosphorus that is soluble in water (P
+5
, mg.kg
-1
)
was measured from the aqueous extract with a soil solution ratio of
1:5 using Multiskan Acent
®
(Labsystems Model, No. 354, Finland)
(Jackson, 1976). Extractable potassium (K
+
, mg.kg
-1
) was determined
with ame atomic absorption spectrophotometry (GBC
®
, Avanta
model, Australia). The extractable Ca
+2
and Mg
+2
were measured by
complexometric volumetric method by titration (titration with EDTA
0.01 N) (Cheng and Bray, 1951). The organic matter content was
determined by the Walkley and Black method using mesh No. 35 (0.5
mm). Total nitrogen was determined by the Dumas method (Leco
®
,
model FP-528, USA), using mesh No. 100 (0.150 mm).
Total protein content (shoots and roots)
The total protein content was measured by bicinchoninic acid or
BCA method (Provenzano et al., 1985). Briey, digestion of samples
and aliquot of the homogenate was performed. The diluted samples
were taken, placed at the bottom of a microplate and the reagent
prepared from BCA was added. Then, the samples were incubated,
and absorbance was determined (Termo, Multiskan spectrum, Vanta,
Finland). Each sample was analyzed in triplicate.
Proline content (shoots and roots)
The proline content was determined agreeing to Bates et al. (1973).
Briey, samples of plant tissue were homogenized in sulfosalicylic
acid and centrifuged. Then, supernatant sample was pipetted into
borosilicate and ninhydrin reagent. Subsequently, samples were
heated in a boiling water bath and then cooled. The toluene phase was
separated by measuring absorbance (Thermo Helios Omega
®
, Vanta,
Finland). Each sample was analyzed in triplicate.
Glutathione peroxidase (GPx) activity (shoots and roots)
The activity of the glutathione peroxidase enzyme was determined
according to the Folhé and Günzler (1984) method. Briey, the assay
mixture was composed of phosphate buffer, EDTA, sodium azide,
glutathione reductase, NADPH, deionized water, reduced glutathione,
and H
2
O
2
. The absorbance was measured (Beckman Coulter DU 800,
Beckman Coulter, Inc. Brea, CA, USA). One unit of GPx is dened
as the amount of enzyme that oxidizes 1 µmol of NADPH per minute.
Each sample was analyzed in triplicate.
Spore count and colonization
Arbuscular mycorrhizal fungi spores were recovered from
inoculum by wet sieving followed by sucrose gradient centrifugation
method (Daniels and Skipper, 1982). Spores were counted under
×35 magnication in a dissecting microscope and the density was
expressed as the number of spore’s g
-1
in the dry inoculum. The
colonization (%) was calculated agreeing to Abeer et al. (2014) with
the following formula:
Total number of AM positive segments
Colonization (%)= x 100
Total number of segments studied
Statistical analysis
Analysis of variance and multiple comparisons of means were
performed (Tukey’s HSD test p=0.05). The colonization (%) was
transformed by arcsine (Little and Hills, 1989; Steel and Torrie,
1995), to comply with the normality assumption. Statistical analyses
were done with Statistica
®
v. 10.0 for Windows (StatSoft
®
, 2011).
Results and discussion
Chemical analysis of the substrate (mineral perlite)
The mineral perlite showed low fertility with a content of 12.20
mg.kg
-1
of Mg
+2
; low exchangeable K
+
(34.43 mg.kg
-1
); low available
P
+
(12.95 mg.kg
-1
); low N (0.059 %); 0 (zero) organic matter; 40.10
mg.kg
-1
of Ca
+2
; a pH of 7.46 and low EC (0.15 dS.m
-1
). According
to Castellanos et al. (2000) the analysis of the substrate conrmed
its suitability for development seedlings and the R. fasciculatus as
inoculum.
Total protein content (shoots and roots)
The shoot total protein content (STP) showed signicant
differences (Table 1). Nufar showed highest STP in 0 mM with and
without AMF followed by Napoletano without AMF both in 0 mM.
Napoletano showed the lowest STP in 100 mM without AMF. Root
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Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239533 October-December. ISSN 2477-9407.
4-6 |
is evidence that basil under NaCl-stress activate the osmoprotective
compound synthesis to counteract damage caused by NaCl-stress.
Spore count and colonization
The AMF spore content ween to 50 to 70 spores g
-1
of inoculum.
The mycorrhizal colonization (MC) showed signicant differences
(Table 1). Both varieties showed the highest MC in 0 mM with AMF.
The MC tends to decrease as NaCl increased. The uninoculated plants
did not colonize, which indicates that no native strains colonized
the culture medium. The number of spores in the AMF inoculum
was considered adequate for mycorrhizal symbiosis according
to Gloria et al. (2010). This result is related to the infectivity of
the species, its ability to produce external hyphae, hypha speed to
colonize the roots and its ability to maintain colonization levels
in a competitive condition (Rivera et al., 2003). The mycorrhizal
colonization shown by Nufar and Napoletano in 0 mM NaCl
(Table 1), exceeded the reference value (45 %) reported in wheat
(Al-Karaki et al., 2004). However, the mycorrhizal colonization
of this study was lower than those reported (70.3 %) by Rojas-
Martínez (2014) in C. annuum var. inoculated with G. manihotis.
As expected, the colonization tends to decrease as NaCl increased.
Similar effects were described by Wu et al. (2010) in citrus and
Aroca et al. (2013) in lettuce seedlings, while Al-Karaki (2000)
exposed L. esculentum to salinity with AMF and concluded that an
increase of EC from 4.7 to 7.4 dS m
-1
decreased the colonization of
F. mosseae. A decrease in AMF colonization was observed in roots
of tomatoes (Latef and Chaoxing, 2011) and Jatropha curcas L.
(Kumar et al., 2010) subjected to saline-stress. Regardless of NaCl,
the level of colonization by R. fasciculatus in basil is considered too
high compared to other studies (Shekoofeh et al., 2012; Cartmill et
al., 2013). The decrease in colonization despite the increase in NaCl
does not interfere with the benec effect of this endophyte on plant
species development under NaCl-stress.
total protein (RTP) content did not show signicant differences;
however, the highest RTP was observed in both varieties at 0 mM
with and without AMF. This response is related to the salt stress
tolerance of Napoletano and Nufar, which previously showed
to be tolerant to NaCl-stress (Batista-Sánchez et al., 2019). This
tolerance is attributed to the osmoprotective compound synthesis,
such as proteins and proline (Argentel et al., 2012). A prior study
showed that the AMF inoculation increased total soluble proteins in
basil showing the additive effect of the fungus action once it reaches
the time to colonize the root and produce enough external mycelium
(Terry-Alfonso and Leyva-Galán, 2006). The results suggest that
basil synthesized new proteins in response to the NaCl-stress.
Similar results reported Mollasadeghi et al. (2011) in wheat under
water decit.
Proline content (shoots and roots)
Shoot (SP) and root (RP) proline content showed signicant
differences (Table 1). Nufar in 50 and 100 mM with AMF showed
highest SP. Napoletano showed lowest SP in 0 mM without AMF.
The RP content was highest in Nufar in 100 and 50 mM NaCl
with AMF. The RP content was lowest in Napoletano in 0 and 50
mM NaCl with AMF and 0 NaCl without AMF. Both varieties
increased SP or RP as NaCl increased except SP in Nufar. Similar
results reported Larrinaga-Arce (2014), who indicated that basil
has enzymatic capacity to reduce the superoxide radical under 100
mM NaCl. Proline is a biochemical marker to evaluate plants under
saline stress (Shamshiri and Fattahi, 2014). The increase in proline
in basil inoculated with AMF under NaCl-stress is evidence that
AMF act as mitigator of NaCl. The proline protects plants against
salt-stress, acts as an enzymatic protector, pH stabilizer, cytosolic
buffer, and cell balance (Chelli-Chaabouni et al., 2010; Verbruggen
et al., 2013). A variety with higher accumulation of proline under
saline-stress could be assumed to be more tolerant compared to
another one with less proline accumulation, since the increase of
metabolites act as compatible solutes (Munns and Tester, 2008).
Glutathione peroxidase (GPx) activity (shoots and roots)
The shoot (SGA) and root (RGA) glutathione peroxidase activity
showed signicant differences (Table 1). Napoletano showed highest
SGA in 100 and 50 mM NaCl with AMF. Nufar showed lowest
SGA in 50 and 100 mM with and without AMF. Napoletano showed
highest RGA in 100 and 50 mM with AMF while the lowest RGA
was showed by Nufar and Napoletano in 0 mM with and without
AMF. In Nufar with or without AMF, RGA increased as NaCl
increased but SGA with or without AMF showed the contrary. In
Napoletano with or without AMF, SGA and RGA increased as NaCl
increased. Similar results reported Abeer et al. (2015) when plants
inoculated increased proline and glutathione peroxidase, which is
attributed to the AMF effect on these osmoprotective compounds.
The increase in GPx in the inoculated plants is attributed to the
improvement of the proline synthesizing enzyme activity and
reduction of their restricted incorporation during protein synthesis.
Salinity generates reactive oxygen species, causing oxidative stress
at cellular level. Superoxide and hydrogen peroxide cause oxidative
damage through the hydroxyl radical, affecting lipids and proteins
(Porcel et al., 2015). Proline and glutathione peroxidase benet
plants maintaining water input balance, mitigating stress-induced
damage (Ahanger
et al., 2014). This study showed that AMF caused
an increase in proline, glutathione, and protein in the inoculated
plants, which is attributed to the effect of this endophyte in NaCl-
stress. The increase of SGA and RGA activity in 100 mM with AMF
Conclusions
The substrate used is suitable to develop basil seedlings using
R. fasciculatus as inoculum. The colonization was high; however,
decreased as NaCl increased. The results showed a differential
biochemical response to NaCl and the use of AMF between varieties
(Napoletano and Nufar). Both varieties increased STP, RTP with
AMF while SP and RP increased as NaCl increased except SP
in Nufar. In Napoletano with AMF, SGA and RGA increased as
NaCl increased. These results conrm that mycorrhization favors
synthesis of osmoprotector compounds, increasing the biochemical
response of basil plants to increase the capacity to facing NaCl-
stress conditions.
Acknowledgements
The support of CIBNOR technical staff Manuel Salvador
Trasviña-Castro, Myriam Lizzeth Hernández de Haro, Roberto
Hernández-Herrera, Maria Dolores Rondero-Astorga and Lidia
Hirales-Lucero is appreciated. Diana Fischer edited the manuscript
in English.
Funding
This research was funded by the projects JICA-SATREPS-JST-
CONACYT and CONACYT-Problemas Nacionales 2017 (Grant
No. 4631).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Agüero-Fernández et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e223953
5-6 |
Table 1. Variety × NaCl × AMF interaction in response to the effect of Rhizophagus fasciculatum (AMF) as a NaCl stress mitigator on
biochemical and fungal variables of Ocimum basilicum varieties subjected to NaCl stress.
Variety
NaCl
(mM)
AMF
(g)
STP
(mg.g
-1
)
RTP
(mg.g
-1
)
SP
(mg.g
-1
)
RP
(mg.g
-1
)
SGA (U mg
protein)
RGA (U mg
protein)
Colonization (%)
Napoletano 0 CM 22.59±0.13b 16.37±0.109a 0.24±0.00d 0.21±0.00i 0.96±0.00c 0.83±0.02e 64.50±0.58a
Napoletano 50 CM 9.56±0.03g 6.55±0.36a 0.35±0.00b 0.28±0.00de 1.45±0.03ab 2.23±0.00b 50.00±0.00c
Napoletano 100 CM 9.48±0.00g 6.13±0.01a 0.36±0.00b 0.30±0.00c 1.50±0.02a 3.19±0.01a 37.75±0.50e
Napoletano 0 SM 22.20±0.14c 16.17±0.06a 0.22±0.00e 0.21±0.00i 0.97±0.01c 0.74±0.19e 0.00±0.00f
Napoletano 50 SM 9.29±0.00gh 6.40±0.13a 0.29±0.00c 0.21±0.00i 1.43±0.03b 2.02±0.04c 0.00±0.00f
Napoletano 100 SM 9.14±0.00h 6.10±0.00a 0.30±0.01c 0.26±0.01fg 1.44±0.04b 2.10±0.04bc 0.00±0.00f
Nufar 0 CM 24.96±0.15a 16.48±0.06a 0.25±0.01d 0.26±0.00g 0.98±0.01c 0.83±0.01e 65.25±2.06a
Nufar 50 CM 19.44±0.11d 12.86±0.09a 0.46±0.01a 0.32±0.01b 0.44±0.01d 1.71±0.07d 58.50±0.58b
Nufar 100 CM 18.85±0.11e 12.60±0.27a 0.37±0.01b 0.44±0.00a 0.45±0.01d 1.74±0.02d 44.00±1.15d
Nufar 0 SM 22.59±0.13b 16.42±0.03a 0.25±0.00d 0.25±0.00h 0.96±0.00c 0.82±0.01e 0.00±0.00f
Nufar 50 SM 18.22±0.12f 12.55±0.31a 0.30±0.01c 0.27±0.00ef 0.44±0.02d 1.76±0.05d 0.00±0.00f
Nufar 100 SM 18.51±0.12f 12.15±0.09a 0.30±0.00c 0.29±0.00d 0.45±0.00d 1.75±0.02d 0.00±0.00f
Signicance level
***
ns
*** *** ** *** ***
NaCl= Sodium chloride (mM); AMF= Arbuscular mycorrhizal fungi (CM = with AMF, SM = without AMF) (g); STP= Shoot total protein content; RTP= Root total protein
content; SP= Shoot proline content; RP=Root proline content; SGA= Shoot glutathione activity (U mg
-1
of protein); RGA= Root glutathione activity. Average values ±
standard deviation with different letters in the same column differ statistically (Tukey’s HSD, P = 0.05). Signicance level: ns= not signicant; ** = P ≤ 0.01; *** = P ≤
0.001.
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