Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: Evidence for reduced sodium and improved magnesium uptake

Abstract

A field experiment was conducted to examine the effect of the arbuscular mycorrhizal fungus Glomus macrocarpum and salinity on growth of Sesbania aegyptiaca and S. grandiflora. In the salt-stressed soil, mycorrhizal root colonisation and sporulation was significantly higher in AM-inoculated than in uninoculated plants. Mycorrhizal seedlings had significantly higher root and shoot dry biomass production than non-mycorrhizal seedlings grown in saline soil. The content of chlorophyll was greater in the leaves of mycorrhiza-inoculated as compared to uninoculated seedlings. The number of nodules was significantly higher in mycorrhizal than non-mycorrhizal plants. Mycorrhizal seedling tissue had significantly increased concentrations of P, N and Mg but lower Na concentration than non-mycorrhizal seedlings. Under salinity stress conditions both Sesbania sp. showed a high degree of dependence on mycorrhizae, increasing with the age of the plants. The reduction in Na uptake together with a concomitant increase in P, N and Mg absorption and high chlorophyll content in mycorrhizal plants may be important salt-alleviating mechanisms for plants growing in saline soil.

Full text

Mycorrhiza (2004) 14:307–312
DOI 10.1007/s00572-003-0274-1
ORIGINAL PAPER
Bhoopander Giri · K. G. Mukerji
Mycorrhizal inoculant alleviates salt stress in
Sesbania aegyptiaca
and
Sesbania grandiflora
under field conditions:
evidence for reduced sodium and improved magnesium uptake
Received: 15 January 2003 / Accepted: 18 September 2003 / Published online: 23 October 2003
 Springer-Verlag 2003
Abstract A field experiment was conducted to examine
the effect of the arbuscular mycorrhizal fungus Glomus
macrocarpum and salinity on growth of Sesbania aegyp-
tiaca and S. grandiflora. In the salt-stressed soil, mycor-
rhizal root colonisation and sporulation was significantly
higher in AM-inoculated than in uninoculated plants.
Mycorrhizal seedlings had significantly higher root and
shoot dry biomass production than non-mycorrhizal
seedlings grown in saline soil. The content of chlorophyll
was greater in the leaves of mycorrhiza-inoculated as
compared to uninoculated seedlings. The number of
nodules was significantly higher in mycorrhizal than non-
mycorrhizal plants. Mycorrhizal seedling tissue had
significantly increased concentrations of P, N and Mg
but lower Na concentration than non-mycorrhizal seed-
lings. Under salinity stress conditions both Sesbania sp.
showed a high degree of dependence on mycorrhizae,
increasing with the age of the plants. The reduction in Na
uptake together with a concomitant increase in P, N and
Mg absorption and high chlorophyll content in mycor-
rhizal plants may be important salt-alleviating mecha-
nisms for plants growing in saline soil.
Keywords Arbuscular mycorrhiza · Soil salinity ·
Mycorrhizal dependency · Glomus macrocarpum · Plant
establishment
Introduction
Soil salinity is a widespread problem, restricting plant
growth and biomass production especially in arid, semi-
arid and tropical areas (Apse et al. 1999). The develop-
ment of salt-tolerant crops or desalination of soil by
leaching excessive salts, though successful, is not eco-
nomical for sustainable agriculture (Hamdy 1990; Can-
trell and Linderman 2001). In this respect, biological
processes such as mycorrhizal application to alleviate salt
stress and use of moderately salt-tolerant tree species are
better options (Hartmond et al. 1987; Dixon et al. 1993).
The reclamation of saline soil with multipurpose, fast-
growing tree species (MPTS) such as Sesbania and
Acacia sp., which are moderately salt-tolerant legume
trees, are commonly used for overcoming salt stress
problems (Sharma et al. 2001; Giri et al. 2002). However,
these trees usually exhibit a considerable dependence on
mycorrhizae, especially arbuscular mycorrhizae (AM) for
an adequate supply of phosphorus enabling them to thrive
under salt stress conditions (Plenchette et al. 1983; Barea
et al. 1992). Many workers have reported the presence of
the AM association in salt stress environments (Pond et
al. 1984; Ruiz-Lozano and Azcon 2000; Aliasgharzadeh
et al. 2001). AM fungi enhance the ability of plants to
cope with environmental stresses generally prevalent in
the degraded ecosystem.
Most studies concerned with AM-saline soil interac-
tions do not simulate field conditions (Al-Karaki et al.
2001). There have been few attempts to study the role of
AM fungi in establishment and growth of MPTS
seedlings in saline soil. The present study evaluates the
effect of the AM fungus Glomus macrocarpum on growth
and establishment of Sesbania aegyptiaca and S. grandi-
flora seedlings in saline soils.
Materials and methods
The experimental site is located in the Botanical garden, Depart-
ment of Botany, University of Delhi, India, where high salt
concentration has rendered it unproductive, saline fallow. The soil
is a sandy loam (clay 35%, silt 33%, sand 32%). Soil extract using
the method of Adams et al (1980) had the followings chemical
properties: pH 8.9, EC (electrical conductivity) 1.58 S m1 at 32C,
organic C 1.12%, total N 0.85%, and available P, K, Na, Zn, and
Mg 8, 12, 122, 20 and 30 mg/kg, respectively. Soil pH and EC were
determined with a digital pH and EC meter (Toshniwal Pvt, Dehli,
India), organic C by the Walkley and Black method (Singh et al.
2001), total N according to Jackson (Singh et al. 2001), P by the
method of Olsen et al. (1954), and K and Na by the ammonium
B. Giri ()) · K. G. Mukerji
Department of Botany, University of Delhi, 110007 Delhi, India
e-mail: bhoopg@yahoo.com
Tel.: +91-11-7654874
Fax: +91-11-7654874

acetate method (Hanway and Heidel 1952). The Zn concentration
was determined by the DTPA-CaCl2-TEA method (Singh et al.
2001).
Raising mycorrhizal and non-mycorrhizal inoculum
G. macrocarpum Tul. & Tul. is dominant in the experimental site
soil, hence it was chosen for the present study. Spores of G.
macrocarpum were isolated from the soil by the wet sieving and
decanting method (Gerdemann and Nicolson 1963). Pot cultures
were maintained on Sorgham halepense (Sudangrass) plants grown
in a poly-house (temperature 32C/20C; RH 70%) for 6 months in
sterilised soil (autoclaved at 121C; 20 min; 15 psi) from the same
site. Soil inoculum contained about 50–55 infectious AM propag-
ules/10 g. Propagule infectivity was tested according to the method
of Sharma et al. (1996). In addition, some of the pots were
uninoculated and served as non-mycorrhizal controls.
Seed treatment
S. aegyptiaca (Pers.) and S. grandiflora (Pers.) seeds were procured
from the Central Arid Zone Research Institute (CAZRI), Jodhpur,
India and scarified with dilute sulphuric acid for 10 min. Seeds
were washed thoroughly with sterile distilled water and then soaked
in sterile water for 12 h. Thereafter the seeds were placed on
sterilised moist filter paper to allow germination in a poly-house
(temperature 32C/20C; RH 70%).
Experimental design
Topsoil to a depth of 30 cm was fumigated twice with 0.1%
formaldehyde at 7-day intervals. The soil was then dried and the
fumigant allowed to dissipate for a week. The experimental land
was divided into four equal plots of 10 m2, two plots for each plant
species. Two treatments were applied to each plant species: (1)
control without mycorrhiza, (2) inoculated with G. macrocarpum
(Gm). Soil inoculum (500 g with 50–55 AM propagules/10 g soil)
along with 200 mg chopped AM-colonised sorghum roots with an
infection level of 80% were placed in furrows in each plot before
sowing of seed (Kapoor et al. 2002).
Measurements and analysis
Five seedlings per treatment were harvested 30 and 60 days after
germination. Root and shoot biomass were determined after oven-
drying at 70C for 72 h. Oven-dried plant matter was ground and
sieved through a 0.5 mm sieve. The ground material (0.2 g) was
digested in a Kjeldahl flask in a triple acid mixture (HNO3:
H2SO4:60% HClO4, 10:1:4) for analysis of P, N, Mg and Na
according to the methods of Allen (1989). The chlorophyll
concentration in the leaves was determined by extracting with
dimethyl sulphoxide according to the chlorophyll extraction
method of Hiscox and Isrealstan (1979) using the equation of
Arnon (1949).
Roots were assessed for AM colonisation 30 and 60 days after
seed germination. Randomly sampled roots were clarified and
stained with Trypan Blue (Koske and Gemma 1989) and cut into
1 cm pieces. Stained root pieces were examined under a compound
microscope (Nikon, Japan) at 40 magnification. All AM fungal
structures (hyphae, arbuscules and vesicles) formed in the roots
were counted, and the extent of AM colonisation was estimated by
the grid line intercept method (Giovennetti and Mosse 1980).
Mycorrhizal dependency was calculated as percent increase in dry
weight of mycorrhizal plants over dry weight of non-mycorrhizal
plants ( Plenchette et al. 1983)
Statistical analysis
Data were statistically analysed using one-way analysis of variance
and the means were separated by Duncan’s multiple range test
(P<0.05) using Costat software (Cohort; Berkeley, Calif.).
Results and discussion
In saline soil, G. macrocarpum successfully colonised the
roots of S. aegyptiaca and S. grandiflora (Fig. 1) although
the level of colonisation varied in each plant species. AM
colonisation did not occur in control plants 30 days after
germination, but very low colonisation was observed in
control plants 60 days after germination, which may be
due to contamination as the experiment was carried out in
open field nursery conditions. In the inoculated plots,
percent AM colonisation and spore numbers increased
significantly even though there was not much increase in
percent colonisation in 30-day-old seedlings. Increased
AM fungal sporulation and colonisation under salt-stress
conditions has also been reported by Aliasgharzadeh et al.
(2001).
In most 30- and 60-day-old seedlings there was a
significant increase in root and shoot dry biomass in
mycorrhizal compared to non-mycorrhizal plants (Fig. 2).
This supports the previous finding that AM-inoculated
plants grow better than non-inoculated plants under salt-
stress conditions (Al-Karaki 2000; Cantrell and Linder-
man 2001). Similar increased biomass production has
been observed previously (Ojala et. al. 1983; Pond et al.
Fig. 1 Effect of salinity and Glomus macrocarpum on arbuscular
mycorrhiza (AM) sporulation and colonisation of Sesbania aegyp-
tiaca (A,B) and S. grandiflora (C,D) 30 and 60 days after
germination. Histograms indicated with the same letter are not
significantly different (P>0.05) by Duncan’s multiple range test;
n=5. C Control, Gm G. macrocarpum
308

1984; Juniper and Abbott 1993; Copeman et al. 1996; Al-
Karaki et al. 2001; Cantrell and Linderman 2001). G.
macrocarpum significantly stimulated growth but the
magnitude of growth response varied among plant
species. Similar results have also been reported by
Cantrell and Linderman (2001). The improved growth
of AM-inoculated plants may be primarily regulated by
supply of nutrients to the root system.
Soil salinity significantly reduces absorption of min-
eral nutrients, especially P because phosphate ions
precipitate with Ca2+ ions in salt-stressed soil and become
unavailable to plants (Poss et al. 1985; Munns 1993;
Grattan and Grieve 1999). Therefore, P improver/fertil-
isation is necessary for plant growth, which may be
helpful in mitigating salt stress by overcoming the P
binding capacity of the soil. AM fungi have been shown
to have a positive influence on the composition of mineral
nutrients (especially poor mobility nutrients such as P) of
plants grown in salt-stress conditions (Al-Karaki and
Clark 1998). In the present study, mycorrhizal S. aegyp-
tiaca and S. grandiflora had higher concentrations of P
compared to non-mycorrhizal plants (Table 1). In saline
soil, higher absorption of P in AM-inoculated plants may
improve their growth rate and salt-tolerance and suppress
the adverse effect of salinity stress. Poss et al. (1985) also
suggested that the salt-tolerance mechanism in onion is
primarily related to P nutrition. Similarly, Pfeiffer and
Bloss (1988) stated that mycorrhizal fungi have the major
effect on salt stress through mediation of P accumulation.
Duke et al. (1986) concluded that, besides enhanced P
uptake, there are some other mechanisms such as
induction of osmotica that lead to osmotic adjustment
and improved salt-tolerance in mycorrhizal plants. How-
ever, Marschner (1995) demonstrated that balanced
nutrition increased the salt-tolerance capacity of plants.
AM-inoculated plants had significantly greater con-
centration of N than non-mycorrhizal plants (Table 1).
Increased N concentration under saline conditions may
help to decrease Na uptake, which may be indirectly
related to maintaining the chlorophyll content of the plant.
Mycorrhizal inoculation had a strong effect on nodule
formation. The number of nodules was higher in mycor-
rhizal than in non-mycorrhizal plants (Fig. 3). Improved
Table 1 Influence of salinity and Glomus macrocarpum on nutri-
ent concentration in Sesbania grandiflora and Sesbania aegyptiaca
60 days after germination. Within a column, values indicated with
the same letter are not significantly different (P>0.05) by Duncan’s
multiple range test; n=5. C Control, Gm G. macrocarpum
Plant species Treat-ment P (%) root Shoot N (%) root Shoot Mg (%) root Shoot Na (%) root Shoot
Sesbania grandiflora C 0.50 a 0.36 a 0.74 a 0.72 a 0.111 a 0.149 a 1.091a 0.921 a
Gm 0.78 b 0.49 b 1.69 b 1.73 b 0.287 b 0.331 b 0.702 b 0.203 b
Sesbania aegyptiaca C 0.52 a 0.40 a 0.89 a 0.96 a 0.165 a 0.202 a 1.25 a 1.020 a
Gm 0.75 b 0.65 b 1.98 b 2.52 b 0.328 b 0.365 b 0.981b 0.431 b
Fig. 3 Influence of salinity and G. macrocarpum on nodules
formation in S. grandiflora and S. aegyptiaca 30 and 60 days after
germination. Histograms indicated with the same letter are not
significantly different (P>0.05) by Duncan’s multiple range test;
n=5. C Control, Gm G. macrocarpum
Fig. 2 Influence of salinity and G. macrocarpum on biomass
production of S. grandiflora (A,B) and S. aegyptiaca (C,D) 30 and
60 days after germination. Within a column, values indicated with
the same letter are not significantly different (P>0.05) by Duncan’s
multiple range test; n=5. C Control, Gm G. macrocarpum
309

nodulation and N-fixation in mycorrhizal plants may be
due to relief from P stress and possibly to uptake of some
essential micro-nutrients, which results both in improved
growth of plants and has an indirect effect on the N-fixing
system (Bethlenfalway 1992; Barea et al. 1992; Founoune
et al. 2002).
It was noteworthy that AM plants exhibited reduced
Na uptake in root and shoot tissues as compared to
uninoculated controls (Table 1). Mycorrhizal S. grandi-
flora and S. aegyptiaca had 0.702% and 0.981%, whereas
non-mycorrhizal plants showed 1.091% and 1.25% Na
concentration in the root tissues, respectively (Table 1).
Mycorrhizal inoculation of both plant species prevented
Na translocation to shoot tissues. It appears that the role
of G. macrocarpum in alleviating salt stress is partly to
prevent Na absorption to root and translocation to shoot
tissues. The accumulation of Na is strongly influenced by
the form of N available (NO3or NH4+) and it may also
be influenced by the synthesis and storage of polyphos-
phate (Orlovich and Ashford 1993) as well as by other
cations, particularly K (Giri et al. 2003). Hence, mycor-
rhizal plants had less Na intake compared to non-
mycorrhizal plants. Plaut and Grieve (1988) found that
increased P results in decreased Na, which is indirectly
related to Ca and Mg uptake. Moreover, Ojala et al.
(1983) found that AM-inoculated onion had higher
concentrations of K in shoots and bulbs under salt stress
conditions, which could be beneficial by maintaining a
high K/Na ratio and by influencing the ionic balance of
the cytoplasm (Founoune et al. 2002) or Na efflux from
the plant (Allen and Cunningham 1983). Cantrell and
Linderman (2001) suggested that AM fungi improve P
nutrition of plants under salinity stress and reduce the
negative effects of Na+and Clby maintaining vacuolar
membrane integrity, which prevented these ions from
interfering in growth metabolic pathways. Maintained
membrane integrity facilitates compartmentalisation with-
in vacuoles and selective ion intake (Rinaldelli and
Mancuso 1996).
Further, the chlorophyll content in leaves of mycor-
rhizal S. aegyptiaca and S. grandiflora was significantly
higher than in non-mycorrhizal plants (Fig. 4). The leaves
of non-mycorrhizal plants were more chlorotic than those
of mycorrhizal plants. This suggests that salt interferes
with chlorophyll synthesis more in non-mycorrhizal than
in mycorrhizal plants. Under salinity stress there may be
several reasons for low chlorophyll content in plant
tissues. One explanation might be that Na has an
antagonistic effect on Mg absorption (Alam 1994). In
the present investigation, a higher concentration of Mg
was observed for both plant species as a result of AM
colonisation, which suggests that mycorrhizal fungi
reduce the antagonistic effect of Na (Table 1). We have
already reported that mycorrhizal fungi are effective in
the absorption of Mg and suppression of Na under salt
stress conditions (Giri et al. 2002).
The mycorrhizal dependency (MD) of both the
Sesbanias was calculated based on the plant dry matter
yield, and revealed that S. aegyptiaca depended on G.
macrocarpum to the extent of 69% and 79.2%, and S.
grandiflora to 55.1% and 68.2% 30 and 60 days after
germination, respectively. MD in saline soil was higher in
S. aegyptiaca than in S. grandiflora. However, both
Sesbania sp. had a considerable degree of dependence on
G. macrocarpum under salt stress conditions. A similar
effectiveness of AM fungi for different plant species was
reported by Dixon et al. (1997). In saline soil, the MD of
S. aegyptiaca and S. grandiflora increased with the age of
the plants. Our results show that, under salt stress
conditions, plants need mycorrhiza not only for acclima-
tisation but also for continued nutrient uptake during
progressive growth stages.
The present investigation demonstrates that, in saline
soil, inoculation with G. macrocarpum can promote plant
growth and establishment. Nevertheless, absorption of P
is the major contribution of the mycorrhizal fungi to plant
growth under salt stress. It appears that there are several
possible metabolic processes that could be mediated by P
nutrition or other elements such as N. The improved Mg
and reduced Na concentrations of mycorrhizal plants may
help to increase chlorophyll concentration. Moreover, the
concentration of Na in S. grandiflora decreased to a
higher extent (55%) than in S. aegyptiaca (38%).
However, S. aegyptiaca showed a higher degree of
dependence on AM fungi than S. grandiflora, which
revealed that there may be some involvement of non-
mediated nutritive effects that could play a more major
Fig. 4 Influence of G. macrocarpum on chlorophyll content of S.
aegyptiaca (A) and S. grandiflora (B) 30 and 60 days after
germination under saline conditions. Histograms indicated with the
same letter are not significantly different (P>0.05) by Duncan’s
multiple range test; n=5. C Control, Gm G. macrocarpum
310

role than nutritional effects. Further research must be
undertaken to evaluate such non-nutritional effects.
Acknowledgements The authors thank Dr. Abhinav K. Goswami
(Department of Statistics, University of Delhi) for statistical
analysis and Dr. Rani Gupta and Inderjit Singh for critical
suggestions. The technical assistance of Ms. Meenakshi Sharma
is acknowledged. The senior author is thankful to CSIR for
financial support.
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