Advances in Environmental Biology Zea Mays

Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
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Advances in Environmental Biology
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Phosphorus Concentration And Root Colonization As Affected By Arbuscular
Mycorrhizal Fungi In Maize (Zea Mays L.) Under Drought Stress Conditions
1
Mohammadreza Naghashzadeh, 2Amir Modaberi, 3Iman Sharafizad and 4Mehran Sharafizad
1
Ph.D of agronomy, Department of Agricultural and Natural Resources Science and Research Branch, Islamic Azad University, Tehran,
Iran.
2
M.Sc Student of Natural Resources, Faculty of Agriculture, Lorestan University, Korramabad, Iran.
3
Seed and Plant Certification and Registration Institute, Iran.
4
Faculty Member of Seed and Plant Certification and Registration Institute, Iran.
ARTICLE INFO
Article history:
Received 22 October 2013
Received in revised form 14
January 2014
Accepted 20 January 2014
Available online 25 February 2014
Key words:
Mycorrhiza,
Drought Stress, Maize
ABSTRACT
In modern agriculture, reducing fertilizers are the main objectives. Maize plant is an
effective host of mycorrhiza in infertile conditions. In order to study effects of
arbuscular mycorrhizal fungi (AMF) on phosphorus concentration (PC) and root
colonization (RC) in maize (Zea mays L.), two field experiments were conducted in
2011 and 2012 (June 7th). The experiments were carried out split-plot factorial design
based on randomized complete block design with three replications. Irrigation as the
main plot was exerted in three levels; based on 70, 50 and 30% field capacity
respectively. Mycorrhizal biofertilizer as the sub plot was applied in two levels; control
and mycorrhizal biofertilizer application (100 kg ha-1). Phosphorus fertilizer as the sub
plot was applied in three levels; 0, 75 and 150 kg ha-1 triple superphosphate
respectively. The results of combined analysis showed that different irrigation
treatments have significantly affected PC. The measured traits as affected by different
irrigation regimes were decreased by increasing drought stress. Different P fertilizer
levels and mycorrhizal biofertilizer have significantly affected PC and RC. Leaf P
concentration and root colonization were increased and decreased by increasing P
application respectively. AM plants have increased about 12% P concentration to their
leaves compared with non-mycorrhizal.
© 2013 AENSI Publisher All rights reserved.
To Cite This Article: Mohammadreza Naghashzadeh, Amir Modaberi, Iman Sharafizad and Mehran Sharafizad., Phosphorus concentration
and root colonization as affected by arbuscular mycorrhizal fungi in maize (Zea mays L.) under drought stress conditions. Adv. Environ.
Biol., 7(14), 4623-4629, 2013
INTRODUCTION
The word mycorrhiza was used the first time by Frank in 1885, and derived from the Greek mycos and rhiza
that mean fungus and root respectively [7]. Mycorriza is a symbiosis between special soil fungi and root plants
[20]. Nowadays, it is accepted that mycorrhizal symbioses are beneficial for plant nutrition and soil quality [3].
In general, maize plant is highly responsive to mycorrhizal inoculation [23].
One of the major problems constraining the development of an economically successful agriculture is
nutrient deficiency [10]. It is estimated that about 30 to 50% of the increase in world food production since the
1950s is attributable to fertilizer application, including P application [11]. The use of mycorrhiza might help to
overcome this problem [24]. In maize and other species, the most widely recognized contribution of AM fungi
to host-plant nutrition involves their ability to extract P from outside the P depletion zone around plant roots
[16]. Mycorrhiza-inoculated maize plants had higher P concentrations than their non-inoculated counterparts
[23]. Liu et al. [15] in an experiment on maize (Zea mays L.) concluded that mycorrhizal plants had
significantly higher concentrations of P in shoots than non-mycorrhizal plants. Tong-jian et al. [34] reported that
AMF inoculation increased significantly P contents in shoots or roots of mungbean and rice compared with
treatments without AMF inoculation. Benabdellah et al. [4] observed that the content of P increase in inoculated
plants. Ortas et al. [24] reported that in three successive experiments uptake of P was significantly and
positively affected by the mycorrhiza treatments. Zhang et al. [37] in an experiment on maize reported that the
arbuscular mycorrhiza significantly increased plant P concentration.
When the soil was fertilized with low doses of P, the colonization of roots increased and there was a change
in the AMF diversity [1]. Arias et al. [2] in their study found that P fertilization with high levels of triple super
Corresponding Author: Mohammadreza Naghashzadeh, Ph.D of agronomy, Department of Agricultural and Natural
Resources Science and Research Branch, Islamic Azad University, Tehran, Iran.
E-mail: [email protected] Tel: +98 916 661 4904
4624
Mohammadreza Naghashzadeh et al, 2013
Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
phosphate inhibited mycorrhizal infection in Stylosanthes capitata plants but not in legume plants. In most
cases, the extent of AM fungal root colonization decreases with increasing soil P supply [33]. Although there is
some evidence that AM fungal spore germination and presymbiotic hyphal growth can be directly impaired by
high soil P levels [21], most research points to host plant mediation of the effects of P upon the extent of AM
fungal root colonization [22]. The extent of root colonization varies with soil and climatic factors [26]. Smith
and Read [31] reported that the root colonization depended on the plant and fungal species involved in the
symbiosis and on the specific growth conditions. However, it is generally assumed that a higher rate of fungal
root colonization will enhance AM effects on plant development. Ortas et al. [24] in three successive
experiments were performance during 1999–2001 observed that plant roots colonization level was significantly
affected by mycorrhizal inoculation for three years experiments. Alguacil et al. [1] reported that the highest
percentage colonization (75.3%) was found in the treatment with low doses of P as rock phosphate and the
lowest degree of root colonization was observed in the treatment where different sources of P were added. Also
Liu et al. [15] in an experiment on maize (Zea mays L.) concluded that phosphorus application decreased the
percentage of AMF colonization. Celebi et al. [8] in an experiment on maize reported that the effect of different
irrigation levels and AMF applications on colonization percentages showed difference for two years according
to irrigation regimes. The lowest colonization percentages were found in the lowest irrigation level where the
most limited water was used in both years.
The aim of this study was to assess the effects of mycorrhizal biofertilizer and drought stress on phosphorus
concentration to decrease P fertilizers application.
MATERIALS AND METHODS
Region of experiment:
Two experiments were conducted at the Agricultural Research Station in Khorramabad-Iran in 2011 and
2012 (June 7th), with Lat. 33˚, 29΄ N; Long. 48˚, 21΄ E; Alt. 1171 m above sea level; mean temperature at the
during growth season in first and second year were 24.90°c and 25.92°c respectively.
Experimental design and agronomic applications:
Two experiments were carried out split-plot factorial design based on randomized complete block design
with three replications. Irrigation as the main plot was exerted in three levels; (a) well-watered conditions (I1),
based on 70% field capacity; (b) moderate drought stress conditions (I2), based on 50% field capacity; (c) severe
drought stress conditions (I3), based on 30% field capacity. Mycorrhizal biofertilizer (species Glomus
intraradices) as the sub plot was applied in two levels; (a) control or without application of mycorrhizal
biofertilizer (M1); (b) application of mycorrhizal biofertilizer (M2) 100 kg ha-1. Phosphorus fertilizer as the sub
plot was applied in three levels; (a) control (P1); without application of phosphorus fertilizer; (b) application of
75 kg ha-1 triple superphosphate (P2); (c) application of 150 kg ha-1 triple superphosphate (P3). Values were
recommended according to the soil testing.
Table 1: Chemical characteristics of substrate soil
Year
Depth
pH
EC × 10 3
2011
0-30
0.55
7.48
30-60
0.67
7.70
2012
0-30
0.50
7.40
30-60
0.62
7.40
T. N. V
32.2
35.0
33.6
35.2
O. C
1.13
0.95
1.20
0.85
P (av.) mg kg-1
3.5
2.2
3.2
2.5
K (av.) mg kg-1
455
340
500
370
According to the mycorrhizal biofertilizer testing by department soil biology research, ten average
mycorrhizal biofertilizer segments had 31 spores per cm 3.
The experimental field was ploughed in fall and disked twice in spring. Each plot was 8 m in length and
consisted of 4 rows separated by 0.75 m, with a distance of 0.20 m between the plants in each row. The studied
hybrid was NS-640. According to the soil testing nitrogen and potassium fertilization were determined,
including 250 kg ha−1 urea and 100 kg ha−1 potassium sulfate. One third of nitrogen (N), all of mycorrhizal
biofertilizer, phosphorous (P) and potassium (K) fertilizers were applied at planting and the remaining N was
applied during the vegetative growth [27]. Farm operations for two years were same.
Soil water content measurement:
Soil water content was measured by weighing the soil before and after drying at 105◦C for 24 h. Moisture
weight percentage was calculated by using the following equation proposes by Kirkham [13].
θm =
W1 − W2
×100
W2
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Mohammadreza Naghashzadeh et al, 2013
Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
Өm, W1 and W2 are water content (moisture content) percentage, soil wet weight and soil dry weight
respectively. Samples were collected from the 0 – 30 and 30 – 60 cm depths. The soil texture was clay loam.
Bulk density was 1.35 g cm -3. Moisture weight percentage in field capacity was 26.5 and 24.2 in 2011 and 2012
respectively. Hydrogen ion concentration (pH) was 7.5.
Irrigation time was determined by weighting soil samples (by Auger in root extension depth) to obtain
moisture weight percentage. Then by using the following equation proposes by Doorenbos and Pruitt [9]
irrigation water volume was calculated.
V=
( FC − βm) × ρb × Dr × A
100
V is the irrigation water volume (m 3), FC is the gravimetric soil water content at field capacity (%), βm, is
the soil water content before irrigation by weight (%), ρb is the bulk density of the soil (g cm-3), Dr is the root
extension depth (m) and A is the irrigated area (m2).
Irrigation duration was determined by using the following equation:
T=
V
Q
T is the Irrigation duration (s), V is the irrigation water volume (m3) and Q is the discharge (m3 s-1).
Leaf phosphorus measurement:
Inductively Coupled Plasma–Optical Emission Spectrometry (ICP–OES) was used to determine P content
after digestion with nitric and perchloric acids [29].
Root colonization percentage measurement:
Roots were cut into segments about 1 cm long. About 0.5 g root segments were cleared in 10 percent (w/v)
KOH in autoclave at 120◦C for 15 min. After cooling, the root samples were washed and stained with 1 percent
(w/v) HCl and 0.05 (w/v) trypan blue respectively [25]. Thirty root segments were mounted on slides in a
polyvinyl alcohol–lactic acid–glycerol solution [14] and examined at 100 – 400 × magnification under Olympus
BH2 microscope. The percentage of root colonization by AMF was calculated according to the method of
McGonigle et al. [18]. The colonization data for specific AMF structures are expressed as percentage of root
length [18].
Statistical analysis:
The recorded data were statistically analyzed using the software MSTATC and SAS. Means comparisons
were calculated using Duncan’s Multiple Range Test at P ≤ 0.05.
Results:
The results of combined variance analysis showed that year, different irrigation treatments, different P
fertilizer levels, mycorrhizal biofertilizer application and interaction between different irrigation treatments and
different P fertilizer levels have significantly affected P concentration (Table 2). AM plants have increased
about 12% P concentration to their leaves compared with non-mycorrhizal. The results of mean comparisons
showed that PC was decreased by increasing drought stress. There were not significantly different in PC
between well-watered (70% field capacity) and moderate drought stress (50% field capacity) at P ≤ 0.05.
Whereas severe drought stress (30% field capacity) have significantly decreased PC. Leaf P concentration was
increased by increasing P application. Application of triple superphosphate 150 kg ha -1 had the highest PC of all
application of P fertilizer levels (Table 3). Although there was no significant difference in interaction between
application of mycorrhizal fungi, different irrigation treatments and different P fertilizer levels on leaf P
concentration, AM plants had higher leaf P concentration than non AM plants. Application of triple
superphosphate 75 kg ha -1 were higher leaf P concentration than application of triple superphosphate 150 kg ha 1
as affected by three-way effects in moderate drought stress in AM plants (Table 5).
The results of combined variance analysis showed that different P fertilizer levels and mycorrhizal
biofertilizer application have significantly affected root colonization. Year and different irrigation treatments
have not significantly affected root colonization (Table 2). The results of mean comparisons showed that RC
was decreased by increasing P application. Application of triple superphosphate 150 kg ha -1 had the lowest RC
of all application of P fertilizer levels (Table 3). Although there was no significant difference in interaction
between application of mycorrhizal fungi, different irrigation treatments and different P fertilizer levels on root
colonization, AM plants had higher root colonization than non AM plants (Table 5).
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Mohammadreza Naghashzadeh et al, 2013
Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
Table 2: Combined analysis of variance for phosphorus concentration and root colonization
Source of Variation
Degree of Freedom
Phosphorus Concentration
Year (Y)
1
3.241*
R(Y)
4
1.146
Irrigation (I)
2
10.222*
2
0.123ns
Y×I
Error (a)
8
0.564
Triple superphosphate (P)
2
2.521**
2
0.070ns
Y×P
4
0.141*
I×P
4
0.122ns
Y×I×P
Mycorrhiza (M)
1
2.344**
1
0.032ns
Y×M
2
0.101ns
I×M
2
0.045ns
Y×I×M
2
0.030ns
P×M
2
0.002ns
Y×P×M
4
0.009ns
I×P×M
4
0.005ns
Y×I×P×M
Error (b)
60
0.041
C. V %
9.09
* and **: Significant at the 5% and 1% probability levels respectively. ns: Non- significant.
Root Colonization
354.579ns
4.405
8.721ns
41.550ns
323.204
152.841**
20.157ns
5.176ns
2.552ns
354.579**
45.773ns
5.283ns
0.136ns
20.960ns
0.007ns
4.855ns
3.693ns
11.807
12.54
Table 3: Means comparison of phosphorus concentration (PC) and root colonization (RC)
Factor
Irrigation
Triple superphosphate
Mycorrhiza
I1
I2
I3
P1
P2
P3
M1
M2
PC
2.702 a
2.336 a
1.652 b
1.971 c
2.218 b
2.500 a
2.083 b
2.377 a
(g kg-1)
RC
27.83 a
27.48 a
26.86 a
29.48 a
27.33 b
25.36 c
25.58 b
29.20 a
(%)
Means, in each row and for each factor, followed by at least one letter in common are not significantly different at the 5% probability levelusing Duncan’s Multiple Range Test.
Discussion:
According to the analysis of variance, the effects of AM fungi on P concentration and root colonization
were significant. Therefore, it can be stated that mycorrhizal fungi have an important role to play in the uptake
of soil P by host plants. Previously Turk et al. [36] have stated that the major role of AM fungal is to supply
infected plant roots with phosphorus, because phosphorus is an extremely immobile element in soils. Even if
phosphorus was added to soil in soluble form soon, it becomes immobilized as organic phosphorus, calcium
phosphates, or other fixed forms. AM fungal are known to be effective in increasing nutrient uptake, particularly
phosphorus and biomass accumulation of many crops in low phosphorus soil. These fungi grow deep into the
soil matrix, accessing soil P that is beyond the roots.
Table 4: Means comparison of phosphorus concentration (PC) and root colonization (RC) as affected by two-way interaction effects
Factor
PC (g kg-1)
RC (%)
Irrigation
Triple superphosphate
I1
P1
2.318 c
30.75 a
P2
2.693 b
27.17 bcd
P3
3.093 a
25.58 cd
I2
P1
2.152 c
29.28 ab
P2
2.300 c
27.75 abcd
P3
2.556 b
25.42 cd
I3
P1
1.443 f
28.42 abc
P2
1.661 e
27.08 bcd
P3
1.852 d
25.08 d
Irrigation
Mycorrhiza
I1
M1
2.503 b
25.61 b
M2
2.900 a
30.05 a
I2
M1
2.243 c
26.02 b
M2
2.429 b
28.94 a
I3
M1
1.501 e
25.11 b
M2
1.803 d
28.61 a
Triple superphosphate
Mycorrhiza
P1
M1
1.799 d
26.79 bc
M2
2.143 c
32.17 a
P2
M1
2.102 c
26.05 cd
M2
2.334 b
28.61 b
P3
M1
2.346 b
23.89 d
M2
2.654 a
26.83 bc
4627
Mohammadreza Naghashzadeh et al, 2013
Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
Means, in each row and for each factor, followed by at least one letter in common are not significantly different at the 5% probability levelusing Duncan’s Multiple Range Test.
They do this through two important mechanisms. First, they are known to produce phosphatase enzymes
that cleave ester bonds that bind P to C in organic matter, thereby releasing phosphate that can be taken up by
the fungi and passed on to the plant. Second, they produce low molecular weight organic acids, such as oxalates,
which enhance the availability of soil P by increasing weathering rates of P contained in clay minerals [7].
Arbuscular mycorrhiza may also promote P uptake by increasing its solubility in soil through pH changes or by
exudation of P mobilizing compounds like organic acids and phosphatases [32]. AM fungi develop an extensive
network of hypha when in symbiosis with the host plant. AM fungi can substantially enhance the uptake of
different nutrients under different conditions, because of their extensive network of hypha and production of
different enzymes such as phosphatase, enhancing the solubility of nutrients including P and the less mobile
micronutrients [27]. Although the mechanism determining the influence of P fertilization on the community
structure of AMF is mostly unknown, the response of AMF to fertilization may be related partly to the changes
in soil quality and therefore to different requirements of the fungi for C, N or P [35]. The results in the present
study are in agreement with the conclusions of Liu et al. [15], Tong-jian et al. [34], Zhang et al. [37] and Ortas
[23] in relation to increasing P uptake in AM plants to non-AM plants.
Table 5: Means comparison of phosphorus concentration (PC) and root colonization (RC) as affected by three-way interaction effects
Factor
PC (g kg-1)
RC (%)
Irrigation
Triple superphosphate
Mycorrhiza
I1
P1
M1
2.115 fg
26.83 bcdef
P2
M1
2.535 cd
26.00 cdef
P3
M1
2.860 b
24.00 ef
P1
M2
2.522 cd
34.67 a
P2
M2
2.852 b
28.33 bcdef
P3
M2
3.327 a
27.17 bcdef
I2
P1
M1
2.043 fg
27.39 bcdef
P2
M1
2.223 efg
26.67 bcdef
P3
M1
2.377 de
24.00 ef
P1
M2
2.262 ef
31.17 ab
P2
M2
2.600 bc
28.83 bcd
P3
M2
2.511 bc
26.83 bcdef
I3
P1
M1
1.240 j
26.17 cdef
P2
M1
1.548 i
25.50 def
P3
M1
1.715 i
23.67 f
P1
M2
1.647 i
30.67 abc
P2
M2
1.773 hi
28.67 bcde
P3
M2
1.988 gh
26.50 bcdef
Means, in each row and for each factor, followed by at least one letter in common are not significantly different at the 5% probability levelusing Duncan’s Multiple Range Test.
The results in this study showed that P supply and root colonization are inversely related. Under severe P
limitation in the soil, increasing P supply by fertilization may favor the AM fungal colonization while the
deficiency is decreased [6]. AM fungal colonization will be decreased if P supply is further increased [5]. Thus,
plants with a higher leaf P concentration down-regulate the carbohydrate supply to the AM mycelia [19]
comparable with the effects of phloem N concentration on nodulation in leguminous plants [5]. Turk et al. [36]
reported that there is a beneficial effect of AM fungal inoculation on nutrient uptake and on plant growth
especially in sterilized soils. Neumann et al. [22] concluded that P uptake was increased by AM inoculation
under low P. Therefore, when the soil nutrient availability is low, AM fungal contribution to plant nutrient
uptake and growth can be significant. Ortas, [23] concluded that inoculation effectiveness was higher under low
P supply than under high P supply. It can be assumed that under high P fertilization levels, P uptake by the AM
fungal pathway was small in relation to P uptake directly by the root surface in all plants. However, plant
transport systems for direct P uptake by the root surface can apparently be down-regulated in response to AM
colonization [30]. Plants could regulate the amount of P taken up by AM hyphae. Besides regulating the AM
hyphae growth, the plants may also regulate the P uptake physiology, for example changing Imax or Km.
However, it cannot be excluded that the plant down regulated the P uptake at the hyphae-root interface. It is well
known that plants regulate P uptake kinetics according to the P supply. For example at high P supply Imax is
down-regulated [28]. There is a weak effect of phosphorus addition on mycorrhizal development. It seems that
AMF application was very effective under high P (100 kg P2 O5 ha-1) levels treatment, relative to low P levels
[12]. P fertilizer application depresses infection by AMF [1] although it may not have any influence [17]. It may
be suggested that the high P levels used in the studies were not high enough to suppress AMF colonization,
which is somehow in accordance with the results of this experiment.
Conclusion:
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Mohammadreza Naghashzadeh et al, 2013
Advances in Environmental Biology, 7(14) December 2013, Pages: 4623-4629
The results showed that leaf P concentration in maize plants have been affected greatly by water stress
conditions. The data showed that the mycorrhizal biofertilizer application improved leaf P concentration and
root colonization in maize plants as a consequence of enhancing extension of the root system, water status of the
plants and nutrients uptake, in particular phosphorus. Generally, AM plants have a greater effect than non-AM
plants. Different P fertilizer levels have significantly affected P concentration and root colonization in maize
plants. P supply and root colonization are inversely related. With respect to environmental problem associated
with fertilizer and water limitation in future, it is essential that we apply water resources appropriately and
decrease fertilizers application in order to improve soil fertility, productivity and water quality.
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