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Abstract Effects of arbuscular mycorrhizal fungi (AMF)
and salt stress on nutrient acquisition and growth of two
tomato cultivars exhibiting differences in salt tolerance
were investigated. Plants were grown in a sterilized,
low-P (silty clay) soil-sand mix. Salt was applied at satu-
ration extract (ECe) values of 1.4 (control), 4.9 (medium)
and 7.1 dS m–1 (high salt stress). Mycorrhizal coloniza-
tion occurred irrespective of salt stress in both cultivars,
but AMF colonization was higher under control than un-
der saline soil conditions. The salt-tolerant cultivar Pello
showed higher mycorrhizal colonization than the salt-
sensitive cultivar Marriha. Shoot dry matter (DM) yield
and leaf area were higher in mycorrhizal than nonmycor-
rhizal plants of both cultivars. Shoot DM and leaf area
but not root DM were higher in Pello than Marriha. The
enhancement in shoot DM due to AMF inoculation was
22% and 21% under control, 31% and 58% under medi-
um, and 18% and 59% under high salinity for Pello and
Marriha, respectively. For both cultivars, the contents of
P, K, Zn, Cu, and Fe were higher in mycorrhizal than
nonmycorrhizal plants under control and medium saline
soil conditions. The enhancement in P, K, Zn, Cu, and Fe
acquisition due to AMF inoculation was more pro-
nounced in Marriha than in the Pello cultivar under sa-
line conditions. The results suggest that Marriha benefit-
ed more from AMF colonization than Pello under saline
soil conditions, despite the fact that Pello roots were
highly infected with the AMF. Thus, it appears that
Marriha is more dependent on AMF symbiosis than
Pello.
Keywords Arbuscular mycorrhizal fungi · Cultivar ·
Growth · Lycopersicon esculentum · Salinity
Introduction
One of the most serious agricultural problems in arid and
semiarid regions is the accumulation of salt on the soil
surface, which renders fields unproductive. In general,
salinity inhibits plant growth and productivity. Detrimen-
tal effects of salinity on plant growth result from direct
effects of ion toxicity (Al-Karaki 2000a; Ayers and
Westcot 1985; Hasegawa et al. 1986) and/or indirect ef-
fects of saline ions that cause soil/plant osmotic imbal-
ance (Wyn Jones and Gorham 1983). Incorporating or
applying factors that enable plants to better withstand
salt stress could help improve crop production under sa-
line conditions.
The introduction of arbuscular mycorrhizal fungi
(AMF) to sites with saline soil may improve plant toler-
ance and growth (Al-Karaki 2000b; Jain et al. 1989).
The improved productivity of AMF plants has been at-
tributed especially to enhanced acquisition of low mobil-
ity nutrients such as P, Zn, and Cu (Al-Karaki and
Al-Raddad 1997; Al-Karaki and Clark 1998; George
et al. 1994; Marschner and Dell 1994) and improved wa-
ter relations (Al-Karaki 1998; Bethlenfalvay et al. 1988;
Sylvia et al. 1993). Mycorrhizal association with plant
roots not only enhances growth and mineral element up-
take, but mycorrhizal plants may have a greater tolerance
of salt stress (Al-Karaki 2000b; Ruiz-Lozano et al.
1996). Improved salt tolerance following mycorrhizal
colonization may be caused by more efficient P uptake
by mycorrhizal plants in P-deficient soils (Poss et al.
1985), leading to increased growth and subsequent dilu-
tion of toxic ion effects (Juniper and Abbott 1993). In
some cases, however, salt tolerance of AMF plants
appears to be independent of plant P concentration
(Danneberg et al. 1992; Ruiz-Lozano et al. 1996).
Salinity tolerance in tomato (Lycopersicon esculen-
tum Mill) plants is of major importance in Mediterranean
regions, where plants are often subjected to high levels
of salinity in the soil from soluble salts in irrigation wa-
ter and fertilizers; there is a negative correlation between
excess salinity and yield (Al-Karaki 2000a; Feigin et al.
G.N. Al-Karaki (✉) · R. Hammad · M. Rusan
Faculty of Agriculture,
Jordan University of Science and Technology, P.O. Box 3030,
Irbid, Jordan
e-mail: gkaraki@just.edu.jo
Mycorrhiza (2001) 11:43–47 © Springer-Verlag 2001
ORIGINAL PAPER
Ghazi N. Al-Karaki · R. Hammad · M. Rusan
Response of two tomato cultivars differing in salt tolerance
to inoculation with mycorrhizal fungi under salt stress
Accepted: 22 January 2001
1987; Shalhevet and Hsiao 1986). Wide variation in
plant responses to AMF inoculation has been reported
for different plant species under environmental stresses
(Al-Karaki and Al-Raddad 1997; Hirrel and Gerdemann
1980; Poss et al. 1985). It has been suggested that my-
corrhizal colonization is a host-dependent and heritable
trait (Lackie et al. 1988; Mercy et al. 1990).
Symbiotic interactions (especially in terms of growth
and mineral nutrient acquisition) between AMF and host
plants (e.g. differing in salt tolerance) need to be studied
under salt-stress conditions in order to optimize the ben-
eficial effects of AMF. The objectives of this present
study were to determine the effects of salt stress and
AMF inoculation on growth and mineral nutrient acqui-
sition by two tomato cultivars differing in salt tolerance.
Materials and methods
A greenhouse experiment was conducted at 25±5°C under natural
illumination during the spring of 1999. Tomato plants were grown
in a silty clay soil (fine, mixed, thermic, Typic Xerochrept) mixed
with sand [soil:sand, 2:1 (v/v)]. Soil properties before mixture
with sand were 6.5% sand, 45% silt, 48.5% clay, 1.2% organic
matter, pH 8.1(soil:water, 1:1), electrical conductivity (ECe)
1.4 dS m–1; 0.26 P (NaHCO3-extractable), 23.1 K, 6.2 Na, 0.2 Fe,
0.02 Zn, and 0.03 Cu (5 mM DTPA-extractable) in mmol per kg
soil. The soil mix was fumigated with methyl bromide under air-
tight plastic sheets for 3 days and the fumigant allowed to dissi-
pate for 10 days. The soil mix was dispensed into plastic pots
(4.5 kg soil per pot) for plant growth. No P was added to the soil.
Half of the pots received the AMF Glomus mosseae (Nicol.
And Gerd.) Gerd. And Trappe by placing 50 g (moist weight) of
inoculum in the soil directly adjacent to the roots of tomato seed-
lings. The AMF inoculum consisted of soil and root fragments and
~1,350 chlamydospores per kg air-dried soil. The inoculum was
isolated initially from a wheat (Triticum durum desf.) field in
northern Jordan (Al-Raddad 1993) and multiplied in pot cultures
using chickpea (Cicer aritinum L.) as host (Al-Karaki and
Al-Raddad 1997). Control treatments received no AMF inoculum.
Seeds of tomato cultivars Pello (salt tolerant) and Marriha (salt
sensitive) (Al-Karaki 2000c) were germinated in a moist mix of
peat and sand in polystyrene trays. Three 20-day-old seedlings,
uniform in size, were transplanted into each pot. Nitrogen as
NH4NO3was added at a rate of 30 mg N per kg soil 7 days after
transplantation.
Plants were established for 3 weeks before being subjected
to three salt levels by addition of a solution of NaCl and CaCl2
(1 M NaCl, 1 M CaCl2) to soil with the irrigation water. This gave
saturation extract (ECe) values of 1.4 (control), 4.9 (medium), and
7.1 (high salt stress) dS m–1. Electrical conductivity’s in soil were
measured with a Model LF539 Conductivity Meter (WTW, Weil-
heim, Germany). The soil was salinized step-wise to avoid sub-
jecting plants to an osmotic shock. Plants were watered with tap
water (EC= 0.4 dS m–1 ) until harvest. When leaching occurred,
the leachate was collected and added back to soil to maintain sa-
linity treatments near target levels.
The experiment was terminated by severing shoots from roots
after 8 weeks growth under salt-stress conditions. Leaf area was
determined using an LI-3000 leaf-area meter. Shoots were then
oven-dried at 70°C for 48 h, weighed and saved for mineral analy-
sis. Roots were rinsed free from soil and cut into 1-cm fragments.
The fragments were thoroughly mixed and representative fresh
samples (1 g) were removed for determination of root AMF colo-
nization. The remaining roots were dried and weighed. Root sam-
ples for determination of root colonization with AMF were cleared
with 10% KOH and stained with 0.05% trypan blue in lactophenol
as described by Phillips and Hayman (1970). AMF colonization in
terms of percentage root segments containing arbuscules and vesi-
cles was determined using a gridline intercept method (Bierman
and Linderman 1981).
Dried shoots were ground to pass through a 0.5-mm sieve in a
cyclone laboratory mill and saved for determination of mineral nu-
trients. Shoot P was determined colorimetrically (Watanabe and
Olsen 1965) and Zn, Fe and Cu were determined by atomic ab-
sorption spectroscopy. Potassium and Na in plant shoots were de-
termined using flame photometry (Ryan et al. 1996).
The experiment was randomized in complete blocks with three
salt stress levels, two AMF inoculum treatments and two tomato
cultivars to give a 3×2×2 factorial with four replications. Data
were analyzed statistically using analyses of variance with
MSTATC (Michigan State University, East Lansing, Mich.). Prob-
abilities of significance among treatments and interactions and
LSDs (P<0.05) were used to compare means within and among
treatments. Mean percentages of AMF colonization were calculat-
ed from arcsine transformed data.
Results
Nearly all salinity and AMF treatments produced signifi-
cant effects on growth and nutrient acquisition traits
(Table 1). Salt ×AMF interactions were significant for
shoot and root dry matter (DM) yields, leaf area, AMF
colonization, and P and Fe contents. Cultivars showed
significant differences only for shoot DM, leaf area,
AMF colonization, and P, K and Fe contents. AMF ×
44
Table 1 Significance levels for plant dry matter (DM) and leaf ar-
ea, root colonization by arbuscular mycorrhizal fungi (AMF) and
shoot mineral (P, Na, K, Fe, Cu, Zn) contents in two tomato culti-
vars (C) grown at different salinity levels (salt)and inoculated or
not with AMF. NS Not significant
Trait Salt level AMF status Cultivar (C) Salt×AMF Salt×C AMF×C Salt×AMF×C
Shoot DM ** ** ** ** NS NS NS
Root DM ** ** NS ** NS NS NS
Leaf area ** ** ** ** NS NS NS
AMF colonization ** ** ** ** NS ** NS
P content ** ** ** ** NS NS NS
K content ** ** ** NS NS NS NS
Na content ** NS NS NS NS NS NS
Cu content ** ** NS NS NS NS NS
Fe content ** ** * * NS NS NS
Zn content ** ** NS NS NS NS NS
* Significant at P≤0.05 ** Significant at P≤0.01
cultivar interaction was significant only for AMF coloni-
zation (Table 1).
No AMF colonization was noted in roots of control
plants. Tomato plants grown in nonsaline soil had rela-
tively high AMF root colonization, which decreased as
soil salinity increased (Table 2). Under the conditions
nonsaline (1.4 dS m–1) and high salt (7.1 dS m–1) but not
moderate salt (4.9 dS m–1), the roots of the salt-tolerant
cultivar Pello showed a significantly higher AMF co-
lonization than the roots of the salt-sensitive cultivar
Marriha (Table 2).
Tomato shoot and root DM and leaf area were gener-
ally higher for mycorrhizal than for nonmycorrhizal
plants (Table 2). However, AMF inoculation had no
significant effects on either shoot DM for Pello or leaf
area for both cultivars at the high salinity treatment.
Moreover, similar root DM values were noted at medi-
um and high salinity for both mycorrhizal and nonmy-
corrhizal plants of both cultivars (Table 2). Shoot and
root DM and leaf area declined in both mycorrhizal and
nonmycorrhizal plants as soil salinity increased (Table
2). Pello had significantly higher shoot DM than Mar-
riha only in nonmycorrhizal plants at the medium and
high salinity levels. Leaf area of Pello was higher than
Marriha for nonmycorrhizal plants in the nonsaline
treatment and for both mycorrhizal and nonmycorrhizal
plants in the medium salinity treatment (Table 2). There
were no significant differences between cultivars in
root DM due to AMF inoculation at any salinity level
(Table 2).
Shoot P contents were generally higher in mycorrhi-
zal than nonmycorrhizal tomato plants of both cultivars
regardless of salinity level (Table 3). However, no signif-
icant differences were noted in shoot P content between
mycorrhizal and nonmycorrhizal plants of Pello at the
high salinity level. Shoot P content decreased with in-
creasing soil salinity in both mycorrhizal and nonmycor-
rhizal plants (Table 3). Differences in P content between
cultivars due to AMF inoculation were noted only under
nonsaline conditions, when Pello had higher shoot P
contents than Marriha. However, Pello shoot P contents
were also higher than Marriha in nonmycorrhizal plants
at the moderate salinity level, suggesting a genotypic dif-
ference between the cultivars.
45
Table 2 Root AMF coloniza-
tion (%), shoot and root dry
matter yields (g per plant) and
leaf area (cm2per plant) of
nonmycorrhizal (NonAMF) and
mycorrhizal (AMF) tomato
cultivars grown at different sa-
linity levels. Different letters in
each column indicate signifi-
cant differences at P<0.05 ac-
cording to LSD
Salt level AMF status Cultivar AMF Dry matter Leaf area
dS m–1 colonization Shoot Root
1.4 NonAMF Pello 0.0 f 4.62 b 0.45 b 317 b
Marriha 0.0 f 4.30 b 0.42 b 286 c
AMF Pello 51.6 a 5.61 a 0.86 a 479 a
Marriha 47.3 b 5.20 a 0.87 a 469 a
4.9 NonAMF Pello 0.0 f 3.19 d 0.31 bc 171 f
Marriha 0.0 f 2.43 e 0.31 bc 139 g
AMF Pello 38.9 c 4.19 bc 0.42 b 250 d
Marriha 36.9 cd 3.83 c 0.34 b 218 e
7.1 NonAMF Pello 0.0 f 1.63 f 0.09 c 78 hi
Marriha 0.0 f 1.14 g 0.06 c 58 i
AMF Pello 33.4 d 1.92 f 0.28 bc 101 h
Marriha 27.0 e 1.81 f 0.14 c 81 hi
Table 3 Shoot contents (mg per plant) of P, K, and Na in nonmy-
corrhizal (NonAMF) and mycorrhizal (AMF) tomato cultivars
grown at different salinity levels. Different letters in each column
indicate significant differences at P<0.05 according to LSD
Salt level AMF status Cultivar Shoot content
dS m–1 PKNa
1.4 NonAMF Pello 4.42 d 175 bc 17.3 c
Marriha 3.85 d 158 cd 17.3 c
AMF Pello 8.86 a 233 a 17.4 c
Marriha 7.71 b 197 b 17.5 c
4.9 NonAMF Pello 2.27 e 103 e 76.2 a
Marriha 1.43 f 66 f 72.8 ab
AMF Pello 5.95 c 144 cd 67.1 ab
Marriha 5.24 c 129 de 60.7 b
7.1 NonAMF Pello 0.94 fg 38 fg 68.7 ab
Marriha 0.51 g 23 g 67.1 ab
AMF Pello 1.66 ef 49 fg 62.5 ab
Marriha 1.35 f 43 fg 61.1 b
Table 4 Shoot contents (µg per plant) of Cu, Fe, and Zn in non-
mycorrhizal (NonAMF) and mycorrhizal (AMF) tomato cultivars
grown at different salinity levels. Different letters in each column
indicate significant differences at P<0.05 according to LSD
Salt level AMF status Cultivar Shoot content
dS m–1 Cu Fe Zn
1.4 NonAMF Pello 55.0 bc 634 b 205 b
Marriha 49.9 c 57 1bc 188 bc
AMF Pello 87.5 a 1041 a 307 a
Marriha 72.9 ab 932 a 268 a
4.9 NonAMF Pello 21.6 d 420 cd 92 de
Marriha 12.0 d 315 d 67 ef
AMF Pello 51.2 c 637 b 142 cd
Marriha 46.3 c 569 bc 126 d
7.1 NonAMF Pello 7.8 d 181 de 40 ef
Marriha 4.0 d 126 e 26 f
AMF Pello 19.9 d 281 de 61 ef
Marriha 14.4 d 259 de 57 ef
Shoot K contents were higher in mycorrhizal than
nonmycorrhizal plants for both cultivars in the nonsaline
and medium salinity treatments (Table 3). Shoot K con-
tent decreased as soil salinity increased. Pello had higher
shoot K contents than Marriha in mycorrhizal plants in
the nonsaline treatment and in nonmycorrhizal plants at
the medium salinity level (Table 3).
Shoot Na contents of both mycorrhizal and nonmy-
corrhizal plants increased significantly as soil salinity in-
creased from the nonsaline to medium salinity levels
(Table 3). No significant differences between cultivars
due to AMF inoculation were noted for Na content re-
gardless of salinity level. However, Na contents of non-
mycorrhizal Marriha and Pello were similar at all salini-
ty levels (Table 3).
Shoot contents of Cu, Fe and Zn were apparently
higher for mycorrhizal than nonmycorrhizal plants, but
the differences were not significant for Cu and Fe at the
high salinity level or for Zn in Pello at medium salinity
and both cultivars at the high salinity level (Table 4).
Shoot contents of Cu, Fe and Zn decreased as soil salini-
ty increased. No significant differences between culti-
vars were noted for shoot contents of Cu, Fe and Zn in
either mycorrhizal or nonmycorrhizal plants.
The overall effects of AMF colonization on shoot DM
yield and mineral nutrient acquisition of saline and non-
saline plants are summarized in Table 5. The enhance-
ment in shoot DM due to AMF inoculation was 22 and
21% under control, 31 and 58% under medium, and 18
and 59% under high salinity level for Pello and Marriha,
respectively. The enhancement in P, K, Zn, Cu, and Fe
acquisition due to AMF inoculation was more pro-
nounced in Marriha than in Pello at the medium and high
salinity levels (Table 5).
Discussion
Plants inoculated with Glomus mosseae had significantly
higher shoot and root DM yields and leaf area than non-
mycorrhizal plants under medium salinity (4.9 dS m–1).
This was also true for shoot DM and leaf area and for
root DM under nonsaline conditions. Enhanced growth
of mycorrhizal plants grown in saline environments has
been related partly to mycorrhizal-mediated enhance-
ment of host plant P nutrition (Al-Karaki 2000b; Hirrel
and Gerdemann 1980; Pond et al. 1984; Poss et al.
1985). In this present study, mycorrhizal plants had high-
er P contents than nonmycorrhizal plants at all salinity
levels, except for Pello plants at the high salinity level.
This may have occurred because of reduced P transport
and uptake under these conditions. Plants grown under
high salinity may have lower H2PO4– activity (preferred
phosphate ion for plant uptake) than under low salinity
conditions (Al-Karaki 1997; Sentenac and Grignon
1985). Reduced uptake of P by mycorrhizal plants grown
at high salinity levels has been reported by other workers
(Al-Karaki 2000b; Hirrel and Gerdemann 1980; Pond
et al. 1984; Poss et al. 1985).
Many studies have indicated that AMF contributes to
plant growth via enhancement of mineral nutrient up-
take, especially of immobile soil nutrients (P, Cu, Zn)
(Al-Karaki and Al-Raddad 1997; Al-Karaki and Clark
1998; Bethlenfalvay et al. 1988; Marshner and Dell
1994). In this present study, mycorrhizal tomato plants
had higher shoot P contents than nonmycorrhizal plants
regardless of salinity level. Higher Fe and Cu contents in
mycorrhizal than nonmycorrhizal plants were also noted.
The higher mineral nutrient acquisition by mycorrhizal
than by nonmycorrhizal plants likely occurred because
of increased availability or increased transport (absorp-
tion and/or translocation) by AMF hyphae. Enhanced ac-
quisition of P, Cu, and Fe by mycorrhizal plants has been
reported (Al-Karaki and Al-Raddad 1997; Al-Karaki and
Clark 1998; Marshner and Dell 1994; Trimble and
Knowles 1995). However, AMF root colonization had
little effect on shoot K content in plants grown at the me-
dium and high salinity levels. Poss et al. (1985) reported
that K uptake was little affected by AMF root coloniza-
tion in tomatoes grown under saline conditions.
The lack of change in Na content with AMF treatment
may be explained by the dilution effects of plant growth
enhancement caused by AMF colonization. Similar re-
sults were reported by other researchers (Al-Karaki
2000b; Bernstein et al. 1974; Jarrell and Beverly 1981).
Plant growth response to AMF inoculation was higher
in Marriha than in Pello under saline but not under non-
saline conditions, even though AMF colonization was
higher in Pello than in Marriha. However, enhanced
growth may not be related to degree of AMF root coloni-
zation in some plants (Al-Karaki and Clark 1998).
The host plant species, cultivar and growing condi-
tions can influence the effects of AMF symbiosis on nu-
trient acquisition (Al-Karaki 2000b; Al-Karaki and
Al-Raddad 1997; Al-Karaki and Clark 1998; Mercy
et al. 1990). From the results of this present study, it ap-
46
Table 5 Percent change in
shoot dry matter (DM) yield
and nutrient contents due to of
mycorrhizal colonization of
two tomato cultivars grown at
different salinity levels. Shoot
DM=DMAMF–DMnonAMF×
100/DMnonAMF. Nutrient content
(NC) increase/decrease=NCAMF–
NCnonAMF×100/NCnonAMF
Salt level Cultivar Shoot DM Nutrient content
dS m–1 P K Na Cu Fe Zn
1.4 Pello 22 100 33 1 59 64 50
Marriha 21 100 25 1 46 63 43
4.9 Pello 31 162 40 –12 137 52 54
Marriha 58 266 95 –17 286 81 88
7.1 Pello 18 77 29 –9 155 55 53
Marriha 59 165 87 –9 260 106 119
pears that AMF colonization was more effective in in-
creasing P, Cu, Fe and Zn acquisition under saline condi-
tions for the salt-sensitive cultivar Marriha than the salt-
tolerant cultivar Pello. Higher nutrient acquisition in re-
sponse to AMF colonization was suggested to be a plant
strategy for salt-stress tolerance (Hirrel and Gerdemann
1980; Pond et al. 1984; Poss et al. 1985).
Despite the paucity of significant differences between
mycorrhizal Pello and Marriha plants in the different pa-
rameters measured, it is clear that Marriha plants benefi-
ted more from mycorrhizal symbiosis than Pello plants
under increased salinity. This is further confirmation that
mycorrhizal symbiosis is especially beneficial for plant
growth under adverse conditions such as soil salinity.
Acknowledgements Financial support by the Deanship of Scien-
tific Research, Jordan University of Science and Technology is
greatly appreciated.
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