Vol.3, No.5, 738-744 (2012) Agricultural Sciences
http://dx.doi.org/10.4236/as.2012.35089
Influence of fungicides and vesicular arbuscular
mycorrhiza on growth and nutrient balance of
soybean by used DRIS equation
Dalshad A. Darwesh1*, Kadija K. Mustafa2
1Department of Environmental Sciences, College of Science, University of Salahaddin, Hawler, Iraq;
*Corresponding Author:
2Department of Biology, College of Science Education, University of Salahaddin, Hawler, Iraq
Received 13 June 2012; revised 20 July 2012; accepted 1 August 2012
ABSTRACT
A pot experiment was conducted to study the
effect of mycorrhiza, fungicides in difference
concentration and there combination on growth
and nutrients balance index of soya bean. Tow
AM treatments including with and with out my-
corrhiza and tow fungicides (parasmid and ant-
arcol) each of them including four concentration
(0.0, 0.25, 0.5 and 1 kg·donum−1) were tested in
factorial completely randomized design in the
three replication. The results indicates that the
higher value of total dry matter weight was re-
corded from combination treatment (F1M1C1)
which attained 11.09 gm·pot−1, while the lower
value 2.25 gm·pot−1 was produced by combina-
tion treatment (F2M2C3), however the same com-
bination treatments was showed that the nitro-
gen, phosphorus, magnesium and iron in the
shoot tissues in the mycorrhizal plant with lower
concentration of fungicides were significantly
greater (P < 0.01) compared to control and higher
concentration treatments. The higher concen-
tration of the above mentioned nutrients (28.33,
8.36, 6.34 mg·g−1, 251.00 mg·Kg−1) was recorded.
The result of nutrient index and nutrient balance
index revealed that the lower NBI (56.18) was
recorded in combination treatments (F1M1C1),
while the higher NBI (2033.81) was produced
from combination treatments (F2M2C3), moreover
the results shows significant negative correla-
tion ship between NBI and total dry matter
weight (r = −0.63*) .
Keywords: VA-Mycorrhi za ; DRIS; Nutrients
Balance Index
1. INTRODUCTION
Mycorrhizal symbioses are essential components of
approximately 80% of plant systems, and the beneficial
role that mycorrhizal fungi play in agricultural production
is well recognized [1]. Although the use of pesticides,
herbicides and fungicides is fundamental for cultivation,
there is now a growing body of evidence of their effects
and impact on plant growth and on microorganisms such
as mycorrhizal fungi [2,3]. Systemic fungicides applied to
soil around plants can be absorbed by roots and translo-
cated to other parts of the plant. These kinds of fungicides
are persistent in the plant and their action on mycorrhizal
fungi can either be against their vegetative or their re-
production structures [4]. Benomyl is among the most
frequently used systemic fungicides against pathogenic
fungi of cereals and oil seed plants [5]. It has been found
to negatively affect mycorrhizal symbioses by delaying or
preventing the formation of AM symbiosis between fungi
and roots and by decreasing plant P-uptake [6]. Benomyl
suppresses mycelial growth by preventing nuclear divi-
sion. In fact, this fungicide inhibits mitosis by blocking
the formation of microtubules when chromosomes are
separated. Combined use of multiple types of fungicide
can amplify the negative effects on mycorrhiza. When the
soil was treated with the two fungicides in combination,
mycorrhiza did not appear at all on the roots. This dem-
onstrates that fungicides used against different soil borne
pathogens can have significant side effects on mycorrhiza
in soil, the extent of which may be dependent on the type
of fungicide [7]. The results of [8] show that benomyl
inhibited fungal activity of both internal and external
hyphae at the low application level (1 mg·g–1 soil) corre-
sponding to the recommended field dose. Propiconazole
decreased the activity of the external hyphae at the low
application level (0.21 mg·g–1 soil) but did not affect the
internal activity at any application level. Treating seeds
with different chemicals such as fungicides to ensure their
higher germination is a common practice before planting
[9]. However such treatments may influence soil micro-
bial population including arbascular mycorrhizal fungi

D. A. Dar wesh, K. K. Mustafa / Agricultural Sciences 3 (2012) 738-744 739
developing a beneficial symbiosis association with most
of the terrestrial plants including crops plants. Consid-
eration of the actions and interaction between plants and
soil microorganisms including arbascular mycorrhiza,
influenced by different parameters such as chemicals in
the field can be very useful for the development of fa-
vorable strategies, which can enhance the efficiency of
agricultural production although using different chemical
including fungicides may effect AM activities, which are
of great significance for the production and health of
ecosystems [7]. Accordingly, it can very pertinent to
evaluate how different fungicides may effect the activities
of VM in the soil and how AM can interactively adjust the
unfavorable effect of fungicides on soil microbial popu-
lation. This is because AM have some very great abilities,
including alleviating the effects of different soil stresses
on plant growth [10], and also controlling the adverse
effects of soil pathogens [11]. Soy bean is one of the most
important legume crops for human nutrition and has been
traditionally cultivated in saline soils in arid and semi-arid
regions, the agronomical importance of soybean (Glycine
max L.) is linked to its high protein content (25% - 29%)
[12]. Diagnosis and Recommendation Integrated System
(DRIS) is a method to evaluate a plant nutritional status
that uses a comparison of the leaf tissue nutrient concen-
tration ratio of the nutrient pairs with norms from a high
yielding treatment. The first step to implement DRIS or
any other foliar diagnostic system is the establishment of
the standard values or norms ,thus the DRIS norms and
their standard deviation and coefficient of variance for N,
P, Ca, Mg, K, Fe, and total dry matter ratio were calcu-
lated from the high yielding treatments ,that is to say
DRIS norms were established locally depending on the
nutrient concentration and their ratio from the high
yielding plants (treatment) from these different set of
conditions are similar. After the establishment of DRIS
norms, we calculate the index of each nutrient that
ranges from negative to positive values. The negative
index values indicate that the nutrient levels are below
the optimum. Consequently, the more negative index, the
more deficient the nutrient, similarly a positive index
indicates that the nutrient levels are above the optimum,
and the more positive index the more excessive the nu-
trient that is relative to normal, and the DRIS index is
equal to zero indicating that the nutrient is at optimum
levels, but there are authors that do not consider a nutri-
ent deficiency or excessive when the DRIS indices are
negative or positives and near to zero [13]. The DRIS
also computes an overall index, which is the sum of the
absolute values of the nutrient index, called nutrient bal-
ance index, the smaller the absolute sum of al DRIS in-
dices, the lesser the imbalance among nutrient. Little
information exists on the effect of current soybean seed
applied fungicides on colonization of vesicular arbuscular
mycorrhiza in soy beans. Also the information on the
effect of fungicide and mycorrhiza on nutrient balance by
using the DRIS equation are rare. Thus the objects of this
study are to evaluate the effect of some fungicides on
mycorrhiza activities and yield of soybean, also to inves-
tigate the combination effect of fungicide and mycorrhiza
on nutrient balance in soybean.
2. MATERIALS AND METHODS
The research was conducted in the green house of
College of Science Education, University of Salahaddin/
Erbil. The experiment was a factorial on the basis of
completely randomized design including two factors and
three replication the first factors involved AM treatment
and without AM treatment, the second factors was two
fungicides (Brasamid and Antracol) including four con-
centration (0.0, 0.25, 0.5 and 1 kg·donum−1) and their
combination on growth, nutrient status and nutrient bal-
ance in soybean. Hence 16 experimental treatments were
tested in each replicates making the total of 48 pots .The
soil was dispensed in to plastic pots (7 kg soil per pots) the
5 gm of vesicular arbuscular mycorrhizal inoculum were
distributed and the sterilized soy bean seeds (6 seeds)
were planted in each pots after germination thinned to 4
plants. Plant irrigated with tap water to maintain soil
moisture near field capacity by using weight method. Leaf
samples were collected as described by [14] and washed
thoroughly with dilute acid (0.2 N HCl) and pure water
to remove residues. The samples were dried at 65˚C and
then wet digested in H2O2 and H2SO4 acid (1/1, v/v)
mixture [15]. The N content was measured by the micro-
Kjeldahl digestion method of [16], the P content was
determined by the molybdenum blue colorimetric me-
thod of [17], Ca, Mg and Fe were determined by atomic
absorption, the flame photometric method of [18] was
used to determined K. The plants were harvested before
flowering stage and oven dry to obtain total dry weight.
2.1. Soil Properties
Some physical and chemical characteristics of the soil
under study were as follows: texture: sandy loam; CaCO3
150 g·kg−1; pH (saturated paste) 7.7; EC 0.6 dS·m−1; or-
ganic matter 1.7 gm·kg−1, NH4OAc-extractable K 1.49
meq·100 g−1; exchangeable Ca 11.0 meq·100 g−1; Mg 5
meq·100 g−1; total N 0.44 mg·kg−1; NaHCO3-extractable
P 5.6 mg·kg−1 and DTPA-extractable Fe, as 0.009 mg·kg−1,
respectively. Chemical soil analysis was conducted as
described in [19].
2.2. Calculation of DRIS Indices
The DRIS indices were calculated by using the fol-
owing index equations by [20]: l

D. A. Dar wesh, K. K. Mustafa / Agricultural Sciences 3 (2012) 738-744
740





fNP fNK fNCa fNMg fNFe fNDM
N Indexn
 
;





fNP fNKfNCafNMg fNFe fNDM
P Indexn

;





fNK fPK fKCa fKMg fKFefKDM
K Indexn
 
;







fNCafPCafKCafCa MgfCa FefCa DM
Ca Indexn
 
;







f NMgf PMgf KMgf CaMgf MgFef MgDM
Mg Indexn
 
;







fNFe fPFe fKFe fCaFe fMgFefFeDM
Fe Indexn
 
;







f NDMf PDMf KDMfCaDMf MgDMf FeDM
DM Indexn
 
.

x/y
fXYXYxy1*100k CVif XYxy 
creased the plant growth compared to control .However
the higher concentration of F2 Antracol significantly de-
pressed the total dry weight in comparison with F1
Prasamid concentration in both mycorrhizal and non-
mycorrhizal plants as shown in (Table 4). The higher
total dry matter weight (8.43 gm·pot−1) was recorded in
case application of 0.25 kg·donum−1 fungicides, whereas
the lower value 4.01 gm·pot−1 was recorded in treatment
C3 which include the application of 1 kg·donum−1 of fun-
gicides, the total dry matter of plants was not signifi-
cantly affected by both fungicides, but in general the
Prasamid give higher dry matter than those treated by
Antracol. Soybean shoot treated or not with mycorrhiza
and difference concentration of fungicides are given in
Tables 1-4. The nitrogen, phosphorus, magnesium and
iron in the shoot tissues in the mycorrhizal plant with
lower concentration of fungicides were significantly
greater (P < 0.01) compared to control and higher con-
centration treatments. The higher concentration of the
above mentioned nutrients (28.33, 8.36, 6.34 mg·g−1,
251.00 mg·Kg−1) was recorded in the factorial treatment
(F1M1C1). The application both fungicides with or with-
out mycorrhiza had no significant effect on the Ca2+ and
K+ content in shoot. Fungicide addition in different con-
centration significantly decrease the nitrogen, phosphorus,
magnesium and iron contents of shoot, except Ca2+ and
K+ not effect by fungicides and their concentration. The
higher concentration of above nutrient was recorded in
case of application of (0.25 kg·donum−1) fungicides.

x/y
fX Y1xyXY*100k/CVif x yXY
X and Y = nutrients (N: nitrogen, P: phosphorus: po-
tassium, Mg: magnesium, Ca: calcium, Fe: iron);
N = number of ratios;
x/y mean for X/Y, in reference population (high-yield-
ing treatment, Norm).
CV(x/y) = coefficient of variation for x/y, in reference
population (high-yielding group).
K = sensitivity coefficient (1).
2.3. Statistical Analysis
The experiment was designed in completely random-
ized design with 3 replications (factorial CRD). The ex-
perimental data were analyzed by ANOVA and differ-
ences between the treatment means were separated by
Adj.LSD Test [21].
3. RESULTS
The effects of fungicides applications in different
concentration on plant growth of mycorrhizal and non-
mycorrhizal plants are presented in Tables 1-4. Plant
colonized by mycorrhiza grow well and were significantly
larger (P < 0.01) than non inoculated .The higher value of
total dry matter weight was recorded from combination
treatment (F1M1C1) which attained 11.09 gm·pot−1, while
the lower value 2.25 gm·pot−1 was produced by combi-
nation treatment (F2M2C3). This stimulatory effect of VA
mycorrhiza on total dry matter weight was maintained
with application lower concentration of both fungicides.
In contrast the higher concentration of fungicides de-
The results that are presented in Table 5 show the sig-
nificant effect of mycorrhiza, fungicides, concentration of
fungicides and their combination on nutrient index and
nutrient balance index in soyban. The lower NBI (56.18) e

D. A. Dar wesh, K. K. Mustafa / Agricultural Sciences 3 (2012) 738-744 741
Table 1. Combination effect of mycorrhiza, fungicides and their concentration on total dry weight and nutrient content of soya bean.
Nutrients concentration
Treatments Nitrogen
(mg/gm)
Phosphorus
(mg/gm)
Calcium
(mg/gm)
Magnesium
(mg/gm)
Potassium
(mg/gm)
Iron
(mg/kg)
Total dry
weight
(gm/pot)
F1M1C0 8.50 5.79 22.50 3.09 26.55 91.33 4.15
F1M1C1 28.33 8.36 35.33 6.34 16.94 251.00 11.09
F1M1C2 19.67 5.36 58.66 1.92 22.28 119.33 6.26
F1M1C3 18.00 5.17 33.00 2.27 23.35 115.00 5.11
F1M2C0 17.83 5.26 47.00 2.51 21.21 128.00 6.20
F1M2C1 16.66 5.51 23.66 3.67 18.01 119.00 7.28
F1M2C2 13.16 5.59 30.66 1.92 28.68 113.33 5.65
F1M2C3 15.50 5.26 35.33 2.27 22.28 71.00 3.29
F2M1C0 12.00 5.69 30.66 2.74 23.35 90.33 5.62
F2M1C1 22.55 7.28 40.00 4.51 22.28 151.33 7.35
F2M1C2 17.83 5.35 35.33 2.27 20.14 130.33 5.70
F2M1C3 16.66 4.52 40.00 2.51 27.61 121.00 5.39
F2M2C0 10.83 3.92 33.00 2.86 27.61 84.33 4.02
F2M2C1 8.50 4.30 35.33 2.74 19.08 124.33 8.02
F2M2C2 12.00 4.36 37.66 2.62 26.55 113.00 5.27
F2M2C3 7.33 3.46 35.33 2.39 22.28 55.67 2.25
Adj. LSD (1%) 9.31 3.48 5.86 16.15 1.96 52.24 2.25
M1 = with mycorrhiza; F1 = Brasamid; F2 = Antraco; M2 = without mycorrhiza; C0 = 0; C1 = 0.25 Kg·donum−1; C2 = 0.5 kg·donum−1; C3= 1 kg·donum−1.
Table 2. Effect of mycorrhiza inoculum on total dry weight and nutrients content of soya bean.
Nutrients concentration
Treatments Nitrogen
(mg/gm)
Phosphorus
(mg/gm)
Calcium
(mg/gm)
Magnesium
(mg/gm)
Potassium
(mg/gm)
Iron
(mg/kg)
Total dry
weight
(gm/pot)
M1 17.95 8.91 36.94 3.20 22.82 131.71 6.33
M2 12.73 7.06 34.75 2.62 23.22 99.08 5.24
Adj. LSD (1%) 3.19 1.19 5.53 0.67 2.01 17.90 0.77
Table 3. Effect of fungicides on total dry weight and nutrients content of soybean.
Nutrients concentration
Treatments Nitrogen
(mg/gm)
Phosphorus
(mg/gm)
Calcium
(mg/gm)
Magnesium
(mg/gm)
Potassium
(mg/gm)
Iron
(mg/kg)
Total dry
weight
(gm/pot)
F1 17.21 8.68 35.77 3.20 22.42 124.00 6.13
F2 13.47 7.29 35.92 2.62 23.62 106.79 5.45
Adj. LSD (1%) 3.19 1.19 5.53 0.67 2.01 17.90 0.77

D. A. Dar wesh, K. K. Mustafa / Agricultural Sciences 3 (2012) 738-744
742
Table 4. Effect of different concentration of fungicides on total dry weight and nutrients content of soybean.
Nutrients concentration
Treatments Nitrogen
(mg/gm)
Phosphorus
(mg/gm)
Calcium
(mg/gm)
Magnesium
(mg/gm)
Potassium
(mg/gm)
Iron
(mg/kg)
Total dry
weight
(gm/Pot)
C0 12.29 7.75 33.29 2.80 24.68 96.50 4.99
C1 19.01 9.54 33.58 4.31 19.08 159.42 8.43
C2 15.67 7.75 40.58 2.18 24.42 117.00 5.72
C3 14.38 6.90 35.92 2.36 23.88 88.67 4.01
Adj. LSD (1%) 5.43 2.03 9.41 1.14 3.42 30.45 1.31
Table 5. Combination effect of mycorrhiza, fungicide and their concentration on nutrient index and NBI of soybean.
Nutrients Index
Treatments
N Index P Index Ca Index Mg IndexK Index Fe Index TDW Index NBI TDW (gm/pot)
F1M1C0 −387.74 20.44 −76.91 55.02 553.10 −91.53 −72.38 1257.13 4.15
F1M1C1 −4.78 −8.39 −4.86 28.09 −5.10 −1.72 −3.24 56.18 11.09
F1M1C2 −95.27 −12.04 121.88 −30.52 158.15 −92.37 −49.83 560.05 6.26
F1M1C3 127.04 7.07 −146.91 −16.56 165.07 −40.39 −95.31 598.36 5.11
F1M2C0 −85.03 1.51 118.81 2.28 166.15 −166.87 −36.86 577.51 6.20
F1M2C1 38.08 16.09 −173.15 −4.97 149.42 −49.40 23.92 455.04 7.28
F1M2C2 −196.06 −9.55 −65.35 −35.94 362.09 2.26 −57.45 728.70 5.65
F1M2C3 −43.08 44.05 66.67 6.21 288.24 −198.05 −164.04 810.35 3.29
F2M1C0 −195.35 −55.84 14.11 31.96 338.22 −111.90 −21.20 768.57 5.62
F2M1C1 −420.80 −70.37 205.67 11.03 303.19 −53.22 24.49 1088.77 7.35
F2M1C2 −32.69 −5.35 −14.48 −6.29 149.43 −46.15 −44.46 298.85 5.70
F2M1C3 −154.26 −62.08 11.42 −6.12 270.14 30.04 −89.15 623.22 5.39
F2M2C0 −299.44 −68.70 79.68 41.24 489.21 −139.68 −102.31 1220.27 4.02
F2M2C1 −438.04 −57.93 186.00 29.50 253.05 −29.75 57.16 1051.42 8.02
F2M2C2 −280.39 −58.11 95.55 14.59 365.44 −78.99 −58.09 951.17 5.27
F2M2C3 −511.02 −57.62 377.42 75.34 564.15 −216.96 −231.31 2033.81 2.25
was recorded in combination treatments (F1M1C1). While
the higher NBI (2033.81) was produced from combination
treatments (F2M2C3) also the nutrient index in the same
table indicate that inoculation with mycorrhiza fungus
changed the order of nutrients requirements in other word
the presence of endophyte improved the balance of ele-
ments, as shown by the lowest sum of indices for the
mycorrhiza soya bean. Thus the result revealed that the N
index, P index, Ca index, K index Fe index and TDW
index reduced from (−85.03, 1.51, 118.81, 166.15, 36.86
and −166.87) in non-mycorrhizal plant to (−4.78, −8.39,
−4.86, −5.10, −1.72 and −3.24) in mycorrhizal plant,
moreover the result show the application of higher con-
centration of fungicides led to increasing the nutrients
imbalance in soy bean.
4. DISCUSSION
The data in the present study indicates that the meta-
bolic activities of the mycorrhizal fungus in infected soy
bean plants varied with treatments of soil by different
fungicides. Differences were reflected in the growth of
mycorrhizal plants, nutrients accumulation, nutrient index
and nutrients balance index. These results support previ-
ous reports on the variation in the toxicity of fungicides to
vesicular arbuscular mycorrhiza [22]. The dominance of

D. A. Dar wesh, K. K. Mustafa / Agricultural Sciences 3 (2012) 738-744 743
sinoculateted treatments with mycorrhiza for nitrogen,
phosphorus, agnesium, iron and total dry weight, this may
be due to the fact that the mycorrhiza increase the ab-
sorption of phosphorus and other essential elements re-
quired for growth these results and explanation are similar
with those reported by [23]. Application of the fungicides
Prasamid and Antracol relatively enhance the plant to
mycorrhizal inoculation these fungicides essentially eli-
minated or reduced the beneficial effect of mycorrhizal
fungus on the growth of plant, macro and micronutrients
nutrition, mycorrhizal fungi can be relatively susceptible
to certain fungicides particularly when the fungicides is
applied to the seeds or into the soil, while other fungi-
cides can stimulate mycorrhiza growth [24]. When Pra-
samid and Antracol were applied half of the field rate
recommended for root diseases control the plant dry
matter nutrients content and nutrient balance were sig-
nificantly increased compared to field rate multiple field
rate application. These results are in agreement with
those of [25] who reported stimulatory effect of lower
concentration of some fungicides on mycorrhizal root
colonization and plant dry matter. It is of interest to note
that the increases in growth of mycorrhizal plants is not
strangely parallel with the concentration of both fungi-
cides, its mean that the dray matter production and nu-
trients uptake reduce with higher rate application of fun-
gicides, this could be explained on the basis that the
fungi toxicity of these fungicides when applied at higher
concentration may be injure fungal cell at many site and
it is also possible that may inhibited a number of en-
zymes involved in nutrient assimilation. [6] reported that
the application of higher concentration of fungicides af-
fect vesicular arbuscular mycorrhizal primarily by inhi-
bition spore germination and infection processes, also
[26]. Their results have indicated that root exudates may
be the factors governing mycorrhizal symbiosis, pesti-
cides that increase root exudation may increase my-
corrhizal infection. Both experimental factors and their
interaction significantly affected soy bean nutrients con-
centration and nutrients balance index. Inoculation of
soybean plants with vesicular arbuscular mycorrhizal
fungi was associated with alterations in the contents of
nutrients in the shoots. Total nitrogen, phosphorus, mag-
nesium and iron tended to be higher in vesicular arbus-
cular mycorrhizal-colonized soybean than in non-colo-
nized plants. the total amount of mentioned nutrients
accumulation in the shoots of soybean were greater when
low concentration of fungicides applied with higher con-
centration of fungicides there was less mycorrhizal effect
on nutrient accumulation. Soya bean plants colonized by
vesicular arbuscular mycorrhiza had no significant dif-
ference in Ca and K content than control, moreover Ca
and K contents of shoot in mycorrhizal and mycorrhizal
plants increase with increasing the concentration of fun-
gicides, however the combination between mycorrhiza
and fungicides enhance the nutrients balance index in
soybean plants. The enhancement of nutrient acquisition
by mycorrhizal infection can be attributed to direct hyphal
uptake or indirect effects brought about by morphological
a physiological changes in the host roots, in addition to
that the VAM differs when subjected to different fungi-
cides and some combination of AM and fungicides may
be more efficient under certain circumstances. According
to our result vesicular arbuscular mycorrhizal inoculation
can significantly alleviate the unfavorable effects of fun-
gicides on soybean yield and nutrients balance. These all
indicated that how using chemicals, among their other
unfavorable effects, particularly on the environments can
influence the nutritional quality of the plants [10].
5. CONCLUSION
The result of this study concluded that the metabolic
activities of the mycorr hizal fungus in infected soy bean
plants varied with treatments of soil by different fungi-
cides. Differences were reflected in the growth of my-
corrhizal plants, nutrients accumulation, nutrient index
and nutrients balance index. These results support previ-
ous reports on the variation in the toxicity of fungicides to
VA mycorrhiza.
6. ACKNOWLEDGEMENTS
Grateful acknowledgement is extended to biology department. Col-
lege of Scientific Education University of Salahaddin-Hawler for pro-
viding laboratory facility.
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[3] Perrin, R. and Plenchette, C. (1993) Effects of some fun-
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