Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical composition of chia (Salvia hispanica L.) leaves

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DOI: 10.1007/s40415-015-0166-6
Cite this publication
Abstract
In this study, chemical composition and growth responses of chia plants (Salvia hispanica L.) to inoculation with an arbuscular mycorrhiza (AM, Glomus mosseae, Nicol. & Gerd.) fungal inoculum (namely MC10) under the influence of soil pH were investigated. The experiment project included six treatments, i.e., control-non-arbuscular mycorrhiza fungi (NAMF, pH 7.1), control-arbuscular mycorrhiza fungi (AMF, pH 7.1), acid-NAMF (pH 5.1), acid-AMF (pH 5.1), alkaline-NAMF (pH 8.2), and alkaline-AMF (pH 8.2). Stunted growth and leaf chlorosis were noticed mainly in plants grown in soil with acidic pH. An increase in fresh biomass was attained in plants amended with AM fungi in alkaline soil pH. Alkaline sandy soil with low levels of available P stimulated AMF colonization of chia roots, which subsequently enhanced P uptake and translocation in plant tissues. Total proteins, carbohydrates, and total fat content in leaves increased in AMF-inoculated plants in neutral and alkaline soil pH, while only fat content enhanced under acidic soil pH. MC10 inoculum resulted in reduced levels of total phenolics under alkaline conditions, whereas under acidic soil resulted in increased levels compared to the non-inoculated plants. The predominant fatty acids of chia leaves were palmitic (18.3 %), a-linolenic (17.1 %), pentadecenoic (11.0 %), linoleic (7.5 %), oleic (7.5 %), and stearic (6.3 %). Higher concentration of stearic, oleic, linoleic, and a-linolenic acids was observed in the leaves of chia plants grown on control (neutral pH) and alkaline soil in the presence of the MC10 inoculum. Alkaline soil combined with AM inoculation enhanced the nutritional value of chia leaves.
1 23
Brazilian Journal of Botany
ISSN 0100-8404
Braz. J. Bot
DOI 10.1007/s40415-015-0166-6
Effects of soil pH and arbuscular
mycorrhiza (AM) inoculation on growth
and chemical composition of chia (Salvia
hispanica L.) leaves
Georgia Ouzounidou, Vasiliki Skiada,
Kalliope K.Papadopoulou, Nikolaos
Stamatis, Victor Kavvadias, Eleftherios
Eleftheriadis, et al.
1 23
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Effects of soil pH and arbuscular mycorrhiza (AM) inoculation
on growth and chemical composition of chia (Salvia hispanica L.)
leaves
Georgia Ouzounidou
1
Vasiliki Skiada
2
Kalliope K. Papadopoulou
2
Nikolaos Stamatis
3
Victor Kavvadias
4
Eleftherios Eleftheriadis
1
Fragiskos Gaitis
5
Received: 18 February 2015 / Accepted: 4 May 2015
Botanical Society of Sao Paulo 2015
Abstract In this study, chemical composition and growth
responses of chia plants (Salvia hispanica L.) to inoculation
with an arbuscular mycorrhiza (AM, Glomus mosseae, Ni-
col. & Gerd.) fungal inoculum (namely MC10) under the
influence of soil pH were investigated. The experiment
project included six treatments, i.e., control-non-arbuscular
mycorrhiza fungi (NAMF, pH 7.1), control-arbuscular
mycorrhiza fungi (AMF, pH 7.1), acid-NAMF (pH 5.1),
acid-AMF (pH 5.1), alkaline-NAMF (pH 8.2), and alkaline-
AMF (pH 8.2). Stunted growth and leaf chlorosis were no-
ticed mainly in plants grown in soil with acidic pH. An in-
crease in fresh biomass was attained in plants amended with
AM fungi in alkaline soil pH. Alkaline sandy soil with low
levels of available P stimulated AMF colonization of chia
roots, which subsequently enhanced P uptake and translo-
cation in plant tissues. Total proteins, carbohydrates, and
total fat content in leaves increased in AMF-inoculated
plants in neutral and alkaline soil pH, while only fat content
enhanced under acidic soil pH. MC10 inoculum resulted in
reduced levels of total phenolics under alkaline conditions,
whereas under acidic soil resulted in increased levels com-
pared to the non-inoculated plants. The predominant fatty
acids of chia leaves were palmitic (18.3 %), a-linolenic
(17.1 %), pentadecenoic (11.0 %), linoleic (7.5 %), oleic
(7.5 %), and stearic (6.3 %). Higher concentration of stearic,
oleic, linoleic, and a-linolenic acids was observed in the
leaves of chia plants grown on control (neutral pH) and al-
kaline soil in the presence of the MC10 inoculum. Alkaline
soil combined with AM inoculation enhanced the nutritional
value of chia leaves.
Keywords Fatty acids Phosphorus concentration
Proteins Soil pH Total phenolic content
Introduction
Chia (Salvia hispanica L.) is an annual summer herb and a
member of the Lamiaceae family. In pre-Columbian times, it
was one of the basic foods of several Central American
civilizations (Ayerza and Coates 2009). Chia plant is native
to Southern Mexico and Northern Guatemala and is of great
importance, since it can be cultivated in order to produce oil
for both food and industry (Peiretti and Gai 2009). It is a low
water user plant and well adapted to arid and semiarid cli-
mates (Ayerza 2013). Its seed contains up to 39 % of oil
which has the highest known content of a-linolenic acid, up
to 68 % compared with 57 % in flax. Chia is one of the most
efficient omega-3 sources, used for enriching foods. In ad-
dition, chia seeds have a significant content and composition
of protein, antioxidants, and dietary fiber (Ayerza and Coates
2004). Chia seeds and meal have not shown any of the
problems (e.g., fishy flavor, animal weight loss, and digestive
&Georgia Ouzounidou
geouz@nagref.gr; geouz@yahoo.gr
1
Institute of Food Technology, Hellenic Agricultural
Organization-Demeter, 1 S. Venizelou str., 14123 Lycovrissi,
Greece
2
Laboratory of Plant & Environmental Biotechnology,
Department of Biochemistry and Biotechnology, University
of Thessaly, Ploutonos 26 &Aeolou, 41221 Larissa, Greece
3
Fisheries Research Institute, Hellenic Agricultural
Organization-Demeter, N. Peramos, 64007 Kavala, Greece
4
Soil Science Institute of Athens, Hellenic Agricultural
Organization-Demeter, 1 S. Venizelou str., 14123 Lycovrissi,
Greece
5
Laboratory of Attica, Directorate of Laboratory Control,
Hellenic Food Authority (EFET), 31 Anagenisseos & Serron,
14451 Nea Philadelphia, Greece
123
Braz. J. Bot
DOI 10.1007/s40415-015-0166-6
Author's personal copy
problems) associated with other x-3 sources such as flaxseed
or marine products. However, environmental factors like
temperature, light, soil type, and available nutrients affect
fatty acid and protein composition (Ayerza and Coates
2004). Despite the extensive research on chemical compo-
sition in chia seeds, there is no information about the che-
mical composition of its leaves.
AM fungi (AMF) play a significant role in the estab-
lishment of plants in their environment not only because
they enhance nutrient uptake, but also because they in-
crease plant tolerance to drought and salt stress and protect
them against soil pathogens (Koske et al. 2004; Blas-
zkowski and Czerniawska 2011). Little is known about the
participation of mycorrhizal inoculation on crop produc-
tivity where introduced AMF must co-exist and compete
with the AM population of native fungi. In soil, the in-
troduction of an AM inoculum leads to a niche competition
and may have positive or negative effects on plants pro-
duction and development (Omirou et al. 2013). In the first
case, the introduced AMF may affect colonizer AM fungal
diversity and improve plant performance under P limiting
conditions (Lekberg and Koide 2005), whereas in the
second case, an inoculum that is intended to increase plant
production and fitness may actually reduce it (Schwartz
et al. 2006). Furthermore, the introduction of a novel
fungal isolate may also alter the structure of the resident
AM fungal community through either positive (i.e., fa-
cilitation) or negative (i.e., competition) interactions
(Callaway and Walker 1997; Antunes et al. 2009).
The biotic and abiotic factors of the environment can
have a great influence on the functional performance of both
the indigenous and introduced AMF in crop experiments.
Soil pH reflects the nutrients available in soil and directly
regulates the availability of others through ion exchange
processes (Helgason and Fitter 2009). Varying soil pH can
change species richness and community composition. Tol-
jander et al. (2008) observed changes in the AMF com-
munity depending on the fertilization treatment used.
In this study, we investigated the growth and chemical
composition response of chia plants (Salvia hispanica L.)
to inoculation with an introduced AM fungal inoculum,
under the influence of an abiotic factor, the soil pH. We
evaluated the potential ability of this inoculum to mitigate
the adverse effects of an alkaline and/or an acidic envi-
ronment to chia plants, in a soil where an active native AM
fungal population already existed.
Materials and methods
This study was conducted in a non-heated greenhouse at
the Institute of Food Technology, Lycovrissi, Attikis,
during spring and summer of 2012 and 2013. Greenhouse
conditions were as follows: temperature 12 C (min),
32.5 C (max), and 24.3 C (average); average relative
humidity 65 %; and average photosynthetic photon flux
density at leaf level 350 ±40 lmol m
-2
s
-1
. Seven days
old Salvia hispanica L. uniform seedlings, with 8 cm av-
erage shoot height, were transferred in pots containing 5L
(three plants per pot) of soil, differing in pH values and
physicochemical characteristics (Table 1). Soil analysis
was carried out in duplicate subsamples. Particle size dis-
tribution was carried out using the Bouyoucos method
(Bouyoucos 1962); pH and electrical conductivity were
measured in the paste extract using pH/EC meter equipped
with glass electrode; organic matter was determined by
dichromate oxidation (ISO 14235:1998); carbonates using
Bernard calcimeter; total N by the Kjeldahl method (ISO
11261:1995); available phosphorus using sodium hydrogen
carbonate extraction (ISO 11263:1994); exchangeable K
?
,
Ca
2?
, and Mg
2?
using BaCl
2
extraction (ISO 11260:1994).
K, Ca, and Mg were measured in a Varian AA-220 Atomic
Absorption, and P was measured in a HITACHI U3010
Spectrophotometer and Na in a Korning Flame photometer.
Determination of NH
4
?
,NO
3
-
,Cl
-
,PO
4
3-
, and SO
4
2-
was performed in 1:10 water extracts using a Dionex-100
Ionic Chromatography. Methanol extractable phenol
Table 1 Physico-chemical properties of the three different soil types
used as growth medium
Soil characteristics Control Alkaline Acid
Sand (%) 36 68 52
Silt (%) 38.4 14 22.4
Clay (%) 25.6 18 25.6
Soil classification Loam Sandy
loam
Sandy
clay
loam
pH 7.1 8.2 5.1
EC (mS cm
-1)
0.5 0.7 0.3
Organic matter (%) 2.7 1.4 3.2
CaCO
3
(%) 17.6 38
Total N (%) 0.2 0.32 0.2
P-Olsen (m kg
-1
) 8 4 54.8
Exchangable K (meq 100 g
-1
) 0.59 0.8 0.6
Exchangable Mg (meq 100 g
-1
) 1.17 1.4 0.9
Exchangable Ma (meq 100 g
-1
) 0.34 0.3 0.3
Available Cu (mg kg
-1
) 17.2 0.7 3.9
Available Fe (mg kg
-1
) 19.4 3.7 98.9
Available Zn (mg kg
-1
) 0.5 0.39 0.6
Available Mn (mg kg
-1
) 5.4 3.4 9.6
Available B (mg kg
-1
) 0.2 0.2 1.7
G. Ouzounidou et al.
123
Author's personal copy
compounds were quantified by means of the Folin–Cio-
calteu colorimetric method (Box 1983). Available Mn, Fe,
Cu, and Zn were determined using DTPA extraction ac-
cording to ISO 14870. Soil B was extracted with boiling
water using the azomethine-H method (Bingham 1982).
Available Cu, Mn, Fe, and Zn were measured in a Varian
SPECTRAA-220 Atomic Absorption. The experiment
project included six treatments, i.e., control-NAMF
(pH 7.1), control-AMF (pH7.1), acid-NAMF (pH 5.1),
acid-AMF (pH5.1), alkaline-NAMF (pH 8.2), and alkaline-
AMF (pH 8.2). Non-mycorrhizal soils were used as refer-
ences for each soil pH. The inoculum (namely MC10) used
belongs to the collection of University of Thessaly and is
consisted of Glomus mosseae spores, hyphae, and colo-
nized maize roots (kindly provided by I. Ipsilantis).
Inoculation was performed by placing *10 g of the
inoculum in the transplant hole. Plants were irrigated once
a week with tap water (500 mL for each pot), without the
use of fertilizers.
The experiments were set up in completely randomized
block design with 6 different treatments and 4 replications
each year. Twenty four plants were grown in each replica-
tion, and plant tissues were harvested 90 days after trans-
plantation. By the end of the cultivation periods during 2012
and 2013 (almost 3 months), fresh weight of the upper part
of the plants and quality characteristics were recorded.
Roots were cleared in 10 % (w/v) KOH for *30 min at
80 C, rinsed with tap water and acidified in 2 % (v/v) HCl
for 15–20 min, and subsequently stained with Trypan blue
solution (Sylvia 1994). The stained roots were then
mounted on glass slides (20–30 root pieces per slide) for
examinations using the grid intersect method (McGonigle
et al. 1990). Percentage root colonization was determined
by examining 100 intersects on 20–30 root segments per
root sample under a microscope mounted with an eyepiece
crosshair graticule. The presence of any of the endophytic
structures—hyphae, coils, vesicles, and/or arbuscules—
was taken as evidence of mycorrhization and used for es-
timating root colonization intensity.
Total carbohydrate content of polysaccharides was es-
timated by phenol/sulfuric acid assay of Dubois et al.
(1956) with slight modifications. The total phenolics were
extracted according to the method described by Ou-
zounidou et al. (2012) and determined by the Folin–Cio-
calteu method with calibration curves for gallic acid.
Absorption was determined at a wavelength of 725 nm
with a spectrophotometer (UV-1700 Shimadzu, Tokyo,
Japan). Data were expressed as mg of gallic acid equiva-
lents per g DW. Protein concentration (expressed % DW)
was determined by the method of Kjeldahl (Ouzounidou
et al. 2012). Phosphorus was determined by the vanado-
molybdophosphoric yellow color method (Karla and
Maynard 1991).
For fatty acid analysis, lipids were extracted from the
homogenized fresh leaf portion by the Bligh and Dyer
(1959) method and were further prepared for fatty acid
analysis according to the procedure of Kates (1972).
Methyl esters were prepared by saponification with 0.5 N
NaOH and methylation with 14 % borontrifluoride–
methanol (Metcalfe et al. 1966).
Fatty acid methyl esters were analyzed by a Hewlett
Packard (5890-Series II) gas chromatograph, separating at
177 C, 18 min hold time and 2.3 C/min to 210 C, and
equipped with a flame ionization detector. The capillary
column SGE-BPX 70 (50 m 90.22 mm 90.25 lm) was
used with helium as carrier gas and nitrogen as auxiliary
gas flow rate at 36 mL/min, hydrogen of 30 mL/min, and
compressed air at 330 mL/min. For peak identification,
solutions of reference substances were analyzed under the
same conditions, and their retention times and chro-
matograms were compared to those of samples. The con-
tribution of each identified compound was expressed as the
percentage (%) of its peak area to the total area of all peaks
eluted in each chromatogram. The precision of the results
was always better than ±5 %. For statistics on chro-
matograms, the HPGC-Chem Station, Rev. A. 06.03 [509],
1990–1998 software was used.
The experiments were complete randomized design with
four replications per treatment each year. Significant dif-
ferences between means of experiments were determined
by least significant difference. A significance level of 0.05
(95 %) was chosen. Duncan’s multiple range test was
employed to determine the statistical significance
(PB0.05) of the differences among mean value.
Results and discussion
In the present study, plant growth recorded as total plant
weight was affected by the different soil pH conditions as
well as by the application of the AMF inoculum. Growth
was impaired both under alkaline and acid pH regimes, but
the effect was much pronounced in the latter case. Visible
symptoms like leaf chlorosis and stunted growth were also
noticed mainly in plants grown in soil with acidic pH,
while the toxicity symptoms in all other treatments were
scarce. The effects of AMF inoculation on plant biomass
were related to the pH conditions (Table 2). Thus, while no
effect was observed for plants grown under optimal (con-
trol) conditions, a 10 % increase in fresh weight was at-
tained in plants amended with the AM inoculum and grown
in alkaline soil pH, in comparison to the non-inoculated
(NAMF) plants. It seems that AMF colonization expanded
the volume of the soil that the chia’s root system could
explore and exploit and thus contributed to an improved
growth performance of the plant. On the contrary, in acidic
Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical
123
Author's personal copy
soil, inoculation with AMF resulted in an even lower plant
yield compared with uninoculated plants. It is obvious that
acidic and alkaline soil pH values (5.1 and 8.2, respec-
tively) provided stressful environments for chia plants
growth, especially in the NAMF plants. Mycorrhizal
inoculation improved plant biomass in the alkaline soil at a
considerable extent. The influence of mycorrhizal inocula
on plant growth has been demonstrated by other studies as
well. Nazeri et al. (2014) recorded a slight increase in the
shoot and root dry weight of colonized legume plants ex-
amined compared to the non-colonized ones.
AMF colonization, either by species indigenous to the
soil used in each treatment or by the MC10 inoculum tested
in the current study, was recorded. Non-inoculated plants
exhibited a high degree of AMF colonization (appr.
30–35 %), indicating that an AMF population efficient to
colonize chia plants already existed in the control soil. The
degree of colonization was largely unaffected by the ad-
dition of the MC10 inoculum. Colonization seemed to be
insensitive in pH increase (pH values [7) both in AMF
and NAMF plants, but the MC10 inoculum had a better
performance in the alkaline soil, and a small but significant
increase was observed compared to the colonization level
under neutral pH conditions. Thus, plants grown in control
and in alkaline soil exhibited the highest percentage root
colonization values, increased by about 30 % compared to
the acidic soil (Fig. 1;P\0.05) both for the inoculated
and uninoculated plants. Intracellular hyphae were the
dominant structures in all roots examined, whereas arbus-
cules were scarce. Arbuscules are considered to be the sites
of nutrient exchange such as phosphorus Wright (2005).
The limited numbers of recorded arbuscules may indicate
that although colonization did occur, the chia–AMF inter-
action may not be optimal under the conditions applied in
the current study. Notably, the levels of available phos-
phorus to the plant were elevated to a great extent in the
acidic soil which most probably resulted in the inhibition of
AMF colonization in plants grown under low pH values.
Phosphorus ions may have diminished the liberation of root
exudates and thus reduced the attraction of germinating
hyphae to the roots (Tawaraya et al. 1998; Carrenho et al.
2007). The negative correlation between AMF colonization
of roots and the soil available P is in accordance with
previous studies (Wang et al. 2012). In addition, soil tex-
ture influenced the AMF colonization. It was observed that
the alkaline sandy soil stimulated the development of AMF
association in chia roots. Sandy soils are usually more
porous, warmer, drier, and less fertile than a finer texture,
and these conditions have direct or indirect effects on AMF
association with the plant roots (Carrenho et al. 2007).
Our results are in accordance with previous findings.
Several studies demonstrated lower spore and extra radical
mycelium development in lower pH values (Helgason and
Fitter 2009). Leifheit et al. (2014) showed that AMF ex-
hibit a preference for a near neutral or alkaline soil pH.
Abd-Alla et al. (2014) also observed that root colonization
of faba bean (Vicia faba L.) by AMF was significantly
increased as alkalinity levels of the substrate increased.
Furthermore, mycorrhizal association alleviated acidic soil
stress in sweet potato cultivation (Yano and Takaki 2005).
Plant colonization by AMF is considered as one of the
primary mechanisms facilitating the capability of plants to
assimilate phosphorus. Phosphorus content in chia shoots
and roots increased under the influence of AMF treatment
irrespectively of the soil pH conditions (Table 2). Pre-
cisely, the application of the MC10 inoculum as compared
to the uninoculated plants enhanced the P uptake and
translocation by about 14, 34, and 24 % in the shoots of
plants grown in control, alkaline, and acidic soil, respec-
tively. A slight but not significant increase of P content was
observed in plant roots of control and acid soil pH, whereas
at alkaline pH, the enhancement was noticeable.
The different pH regimes as well as the MC10 inoculum
treatment affected differentially the total phenolics levels
in the plant shoots. The application of the MC10 inoculum
resulted in reduced levels under alkaline conditions and in
increased levels (by about 30 %) under acidic soil condi-
tions, compared to the non-inoculated plants. On the other
Table 2 Response of growth and chemical composition of chia plants on different soil pH with or without AM inoculation
Plant weight
(g plant
-1
)
Shoot P
(% DW)
Root P
(% DW)
Total phenolics
(mg GAE/g DW)
Proteins
(% DW)
Total
carbohydrates
(% DW)
Total fat
content
(% DW)
Control-NAMF 40.2 ±2.8a 6.83 ±0.05b 2.04 ±0.1a 41.4 ±1.1ab 20.15 ±0.87c 9. 5 ±0.38c 2.92 ±0.1b
Control-AMF 38 ±3.0ab 7.80 ±0.1a 2.33 ±0.03a 41 ±1.2b 22 ±1.10ab 9.5 ±0.41c 3.70 ±0.4a
Alkaline-NAMF 33 ±0.9c 5.35 ±0.03c 1.75 ±0.05b 43.5 ±0.9a 21 ±0.70bc 10.3 ±0.50b 2.35 ±0.09b
Alkaline-AMF 36.4 ±1.6b 7.18 ±0.11ab 2.15 ±0.2a 34.5 ±0.8c 22.7 ±1.90a 11.2 ±0.65a 3.85 ±0.2a
Acid-NAMF 29.7 ±2.2d 4.24 ±0.07d 0.75 ±0.1c 22.8 ±0.6e 17.78 ±0.68d 8.3 ±0.33d 1.85 ±0.04c
Acid-AMF 23 ±1.8e 5.24 ±0.04c 0.94 ±0.06c 29.3 ±0.7d 16.54 ±0.53e 7.4 ±0.0.23e 2.57 ±0.3b
Mean ±SE, n=15 for plant growth, n=3 for chemical composition. Values followed by different letters in the same column are significantly
different at P\0.05
G. Ouzounidou et al.
123
Author's personal copy
hand, the MC10 inoculum application had no effect on the
total phenolics levels of plants grown in neutral soil pH
(Table 2).
The total protein content increased in AMF-inoculated
plants compared to NAMF grown both under control and
alkaline conditions. A similar trend was observed for the
total carbohydrate content in inoculated plants grown in the
alkaline soil. In accordance with the poor growth of chia
plants under acidic conditions, total protein and carbohy-
drate content decreased under these conditions compared to
control plants. The negative effect of soil acidity on these
values was much more profound in AMF plants than in the
non-inoculated ones.
Total fat content is a character of particular importance
for the cultivation of chia plants. A substantial and sig-
nificant increase was observed in the MC10-inoculated
plants as compared with the uninoculated ones grown un-
der all soils tested. Thus, AMF plants grown in control,
alkaline, or acidic soil revealed significantly higher oil
content in their leaves compared to NAMF plants (26, 63,
and 38 %, respectively) (Table 2).
A more detailed analysis regarding the composition of
oil content was conducted. Statistically significant differ-
ences (P\0.05) in stearic, oleic, linoleic, and a-linolenic
fatty acids among treatments were detected (Table 3). In
general, plants grown in control and in alkaline soil ex-
hibited higher values of the above acids, which were fur-
thermore increased under the influence of the LC10
inoculation. Oleic acid (18:1) content was significantly
higher in leaves of AMF chia plants grown in control and
alkaline soil, while the lowest values were recorded in
leaves of plants grown in acidic soil with or without AMF
treatment. AM inoculation also enhanced linoleic acid
(18:2) content of leaves in all three soil pH values exam-
ined. On the other hand, myristoleic acid was predominant
and at higher concentrations in samples that received no
AM treatment. Qualitative analysis of the fatty acids was
conducted using the gas chromatographic FID detection
analytical method, and the representative chromatographs
are shown in Figs. 2,3and 4. The chromatographs of chia
plants fatty acids presented in Fig. 2demonstrated that the
predominant fatty acids were as follows: palmitic (18.3 %),
a-linolenic (17.1 %), pentadecenoic (11.0 %), linoleic
(7.5 %), oleic (7.5 %), and stearic (6.3 %). In the leaves of
the MC10-inoculated control plants, the percentage con-
centrations of palmitic (21.2 %), oleic (11.2 %), linoleic
(11.2 %), and a-linolenic (23.0 %) acids were significantly
higher compared to the leaves of control-NAMF plants. In
alkaline soil, the AMF inoculation enhanced the content of
pentadecenoic, arachidic, and beheric acids (by 1.7, 0.2,
and 0.9 %, respectively), in comparison to control samples,
whereas a-linolenic was significantly suppressed (Fig. 3).
a-linolenic and palmitic acids were the dominant fatty
acids of chia leaves grown under acidic conditions, and
they were increased under the influence of the AMF
treatment (Fig. 4).
Generally, the principal function of AMF is to enhance
P acquisition of the host plants from labile and non-labile
sources in soil (Yano and Takaki 2005). The extra radical
mycelium explores a greater volume of soil and translo-
cates nutrients from soil to plants more efficiently, resulting
in improved plant nutrition (Tanwar et al. 2013). The host
plant offers carbohydrates produced through photosynthe-
sis to the invader-fungus, in exchange for water and soil
nutrients such as phosphorus, copper, and zinc. In the
present study, phosphorus absorption was significantly in-
creased in AMF-inoculated chia plants. Even though P
availability in acid environments is high, P absorption by
chia roots is significantly lower, while the inoculation with
MC10 was not sufficient to ameliorate this effect.
Even though much research has been done concerning
the chemical content of chia seeds (Ayerza and Coates
c
d
b
b
a
d
0
10
20
30
40
50
NAMF AMF NAMF AMF NAMF AMF
CONTROL SOIL ALKALINE SOIL ACID SOIL
% root colonization
Fig. 1 Percentage root
colonization by AMF of Salvia
hispanica L. plants grown in
neutral, alkaline, and acidic soil.
AMF indicates plants grown in
inoculated soil with mycorrhizal
inoculum MC10 (G. mosseae).
NAMF indicates plants grown
in non-inoculated soil. Values
are presented as
mean ±standard deviation,
(n=2). Means that differ at
P\0.05 are shown by different
letters
Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical
123
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2009; Peiretti and Gai 2009; Ayerza 2013), little is known
about quality characteristics of its leaves. In the present
study, the chemical composition of chia leaves was
strongly influenced by the soil pH and the mycorrhizal
inoculation. Acidic soil repressed phenols, proteins, car-
bohydrates, and oil content as a result of low P uptake and
reduced plant development. Differences in chemical com-
position in chia seeds and plants during different growth
stages and several environmental conditions were recorded
by Peiretti and Gai (2009) and Ayerza and Coates (2009).
The FA profile of chia leaves varied according to the soil
type and AMF inoculation. It is obvious that alkaline soil
combined with AMF inoculation enhanced nutritional
value of chia leaves. ALA and palmitic were the most
abundant FA in all treatments, followed by pentadecenoic
and then by linoleic and oleic. Based on our results and on
bibliography data (Ayerza and Coates 2009; Peiretti and
Gai 2009), it can be concluded that FA profile and con-
centrations in leaves differ from those found in chia seeds.
In seeds, ALA acid has four times higher concentration
min
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9
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2) C15:1
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4) C18:0
5) C18:1 -9
6) C18:2 -6
7) C18:3 -3
8) C20:0
9) C22:0
1
2
3
456
7
8 9
i-octane
A
B
i-octane
ω
ω
ω
Fig. 2 HPLC chromatograph of fatty acids of Salvia hispanica L. leaves in control-NAMF (a) and control-AMF (b) plants
Table 3 Fatty acid composition of leaves of chia plants grown on different soil pH with or without AM inoculation
Fatty acids (%) Control
NAMF
Control
AMF
Alkaline
NAMF
Alkaline
AMF
Acid
AMF
Acid
AMF
Myristoleic C14:1 3.2 ±0.10b 2.9 ±0.2b 1.8 ±0.09c 2.9 ±0.3b 4.4 ±0.8a 2.9 ±0.43b
Pentadecenoic C15:1 11.0 ±1.1b 8.3 ±0.9d 6. 7 ±0.46e 10.0 ±0.9bc 13.4 ±1.3a 9.3 ±0.85c
Palmitic C16:0 18.3 ±1.33b 21.2 ±1.3a 20. 0 ±1.23a 19.2 ±0.87ab 14.8 ±0.93c 18.4 ±1.0b
Stearic C18:0 6.3 ±0.20a 6.3 ±0.56a 4.1 ±0.65b 4.0 ±0.16b 4.2 ±0.3b 3.8 ±0.34b
Oleic C18:1 7.5 ±0.55b 11.2 ±1.1a 8.4 ±0.62b 10.7 ±0.9a 6.1 ±0.5c 6.1 ±0.37c
Linoleic C18:2 7.5 ±0.37c 11.2 ±0.9a 8.9 ±0.7bc 9.0 ±0.8b 7.4 ±0.67c 8.2 ±0.58c
a-Linolenic C18:3 17.1 ±1.75cd 23.0 ±2.0a 17.9 ±1.1c 16.6 ±0.87d 13.9 ±0.6e 19.2 ±1.8b
Arachidic C20:0 6.3 ±0.23a 5.2 ±0.78b 4.1 ±0.32c 5.4 ±0.35b 6.9 ±0.68a 5.8 ±0.33b
Beheric C22:0 5.0 ±0.64a 3.2 ±0.34c 4.5 ±0.34a 4.1 ±0.09b 3.5 ±0.23c 3.7 ±0.18bc
Mean ±SE, n=3. Values followed by different letters in the same raw are significantly different at P\0.05
G. Ouzounidou et al.
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min
010 20 30 40 50 60
counts
7500
10000
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15000
17500
20000
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34
56
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min
010 20 30 40 50 60
counts
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1) C14:1
2) C15:1
3) C16:0
4) C18:0
5) C18:1 -9
6) C18:2 -6
7) C18:3 -3
8) C20:0
9) C22:0
i-octane
1
2
34
5
6
7
89
A
B
i-octane
ω
ω
ω
Fig. 3 HPLC chromatograph of fatty acids of Salvia hispanica L. leaves in alkaline-NAMF (a) and alkaline-AMF (b) plants
min
010 20 30 40 50 60
counts
7500
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15000
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1) C14:1
2) C15:1
3) C16:0
4) C18:0
5) C18:1 -9
6) C18:2 -6
7) C18:3 -3
8) C20:0
9) C22:0
A
B
i-octane
ω
ω
ω
Fig. 4 HPLC chromatograph of fatty acids of Salvia hispanica L. leaves in acid-NAMF (a) and acid-AMF (b) plants
Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical
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than in leaves, while palmitic acid amounts correspond
only to the one-third of those found on leaves.
Conclusion
It can be concluded that the G. mosseae MC10 inoculum
had different impact on chia plants according to the soil
acidity or alkalinity. AMF, either as an introduced or en-
dogenous inoculum, colonized chia roots better at pH
values ranging from neutral to alkaline. It can be concluded
also that sandy and porous soil with low available P en-
hanced AMF association with chia roots. Based on our
findings, the high protein, phenols, and fat content of chia
leaves makes them a nutritional source of high value,
suitable for both human and animal consumption. Further
research concerning the cultivation conditions of chia
plants will give some insight on the amelioration of chia
leaves chemical content for nutritional purposes.
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    The photosynthetic capacity of carob tree (Ceratonia siliqua L.) and the quality indices of the fruits growing under natural conditions, at Athens and Rethymno in Greece, were measured on diurnal and seasonal basis. The highest photosynthesis is observed during May compared to June and October, which is correlated well with the high developmental rates, the optimal temperatures and water availability. C. siliqua growing at Athens site attained higher photosynthesis parameters than trees growing in Rethymno. The decline of CO2 assimilation rate during the hot and dry season was rather a non-stomatal effect, since it is not accompanied by low stomatal conductance. Photoinhibition damage during June with concomitant reduction in electron transport rate in Photosystem 2 and Photosystem 1 may occur. Despite the low soil water and the extremely high air temperatures during the June, carob showed an important capacity to control water loss (A/gs). The total sugar content significantly increases with seasonal changes and reaches its highest value in October when pods are fully ripe, while polyphenols and proteins gradually decrease. The climatic conditions prevailing in the Mediterranean basin do not threaten the survival of C. siliqua.
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    155 rhizosphere soil and root mixtures were collected from under Ammophila arenaria colonizing maritime dunes of the island Bornholm (Denmark) to determine arbuscular mycorrhizal fungi (AMF) of the phylum Glomeromycota co-existing with this plant. In the laboratory, each mixture was divided into two parts. One part was used to establish a pot culture with Plantago lanceolata as the host plant to initiate sporulation of fungi that had not produced spores in field conditions. In the second part, the numerical and species composition of the spore populations of AMF sporulating in the field was determined. Spores of AMF were found in 70 fieldcollected samples and 134 trap cultures. They represented 26 species and six undescribed morphotypes in six genera of the Glomeromycota. Of them, 20 species and three morphotypes in five genera occurred in the field, and 16 species and three morphotypes in five genera were found in trap cultures. The fungi most frequently revealed were members of the genus Glomus; a total of 17 species and six morphotypes of this genus were recognized. Considering the occurrence of spores in both field samples and trap cultures, the fungi most frequently co-occurring with roots of A. arenaria growing in the dunes of Bornholm were G irregulare (present in 73.6% of samples), followed by Scutellospora dipurpurescens (19.4%) and Archaeospora trappei (10.3%). However, Glomus irregulare mainly sporulated in trap cultures; spores of this fungus were found in only 0.6% of field samples. Other relatively frequently found species were G. aggregatum (9.0%), G. eburneum (7.1%), Paraglomus laccatum (5.2%), and S. armeniaca (6.5%). The species most abundantly sporulating in the field were G. aggregatum (produced 28.36% of all spores isolated), G. badium (11.00%), and 5. dipurpurescens (21.55%).
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    The objective of this study was to investigate the relationship of seed color with protein, oil, fiber, amino acids, and antioxidants content composition of two chia (Salvia hispanica L.) genotypes. Study was carried out using chia genotypes known as Tzotzol and Iztac; the first has black-spotted seed, the second white seed. Results: the lack of significant (p<0.05) difference on biochemical compounds between Tzotzol and Iztac genotypes found in this study could be explained by the small genetic difference between these two genotypes. Conclusion: In summary, this paper showed no relationship of the seed coat color for all measured traits, protein, oil, fiber, amino acids, and antioxidants content composition. In addition, during this work it was found secoisolaricresorcinol diglucoside, an antioxidant not previously reported for this species which perhaps contributes to the stability of chia seed oil.
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    Background and aims Soil aggregation is a crucial aspect of ecosystem functioning in terrestrial ecosystems. Arbuscular mycorrhizal fungi (AMF) play a key role in soil aggregate formation and stabilization. Here we quantitatively analyzed the importance of experimental settings as well as biotic and abiotic factors for the effectiveness of AMF to stabilize soil macroaggregates. Methods We gathered 35 studies on AMF and soil aggregation and tested 13 predictor variables for their relevance with a boosted regression tree analysis and performed a meta-analysis, fitting individual random effects models for each variable. Results and conclusions The overall mean effect of inoculation with AMF on soil aggregation was positive and predictor variable means were all in the range of beneficial effects. Pot studies and studies with sterilized sandy soil, near neutral soil pH, a pot size smaller than 2.5 kg and a duration between 2.2 and 5 months were more likely to result in stronger effects of AMF on soil aggregation than experiments in the field, with non-sterilized or fine textured soil or an acidic pH. This is the first study to quantitatively show that the effect of AMF inoculation on soil aggregation is positive and context dependent. Our findings can help to improve the use of this important ecosystem process, e.g. for inoculum application in restoration sites.