O A RIGINAL

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Advances in Environmental Biology, 5(9): 2742-2749, 2011
ISSN 1995-0756
This is a refereed journal and all articles are professionally screened and reviewed
ORIGINAL ARTICLE
Effects Of Biofertilization On Nodulation, Nitrogen And Phosphorus Content And Yield
Of Pigeon Pea (Cajanus Cajan)
1
Awad Galal Osman, 2Ahmed Mohammed Elhassan Rugheim and 3Elkheir Mohammed Elsoni
1
The National Centre for Research, Khartoum.
Ommdurman Islamic University, Ommdurman, Sudan.
3
Ministry of Agriculture,Algazeira State,Sudan.
2
Awad Galal Osman, Ahmed Mohammed Elhassan Rugheim and Elkheir Mohammed Elsoni: Effects
Of Biofertilization On Nodulation, Nitrogen And Phosphorus Content And Yield Of Pigeon Pea
(Cajanus Cajan).
ABSTRACT
A field experiment was conducted at Elbagair area, central Sudan, for two successive seasons 2009/2010 –
2010/2011 to study the effects inoculation with five introduced or locally isolated Rhizobium or
Bradyrhizobium strains each alone or with Bacillus megatherium var. phosphaticum strain (BMP) alone, and
combination of each rhizobial strain with Bacillus megatherium var. phosphaticum strain (BMP) on the
symbiotic properties, and yield of pigeon pea (Cajanus cajan). Rhizobium and BMP inoculation separately
significantly (P≤0.05) increased nodulation, nodules dry weight, root dry weight, shoot dry weight, nitrogen and
phosphorus content in shoot and seed yield of pigeon pea plants in comparison to the un-inoculated control.
Rhizobium and BMP co-inoculation significantly (P≤0.05) increased nodulation, nodules, root and shoot dry
weights nitrogen and phosphorus content in shoot and seed yield. The results of this study revealed the need for
biological fertilizers with compatible effective strains for application to inoculate pigeon pea, especially this
crop is cultivated in Sudan without fertilization.
Key words: Pigeon Pea, Rhizobium, Bacillus, Inoculation.
Introduction
The legumes and grains families are by far the
world’s most important sources of food, grains
supply starch while legumes which include bean,
peas supply protein and fats [14]. Legumes are very
important not only as food crops but possess high
propensity to grow in depleted soils thereby serving
as a medium of fertilizing succeeding crops through
their unique symbiotic capability with nitrogenfixing Rhizobium bacteria which are inhabited in root
nodules of the legumes, and the nitrogen balance in
the soil is thereby preserved [20].
Pigeon peas are an important food in
developing tropical countries. An excellent source of
protein, the seeds (and sometimes the pods) are eaten
as a vegetable, as a flour additive to other foods, in
soups, and with rice [3]. The performance of pigeon
pea globally is in an upward trend in terms of area
and production from 2.86 million hectares and 1.96
million tons in 1980 to 4.63 million hectares and 3.46
million tons in 2006, respectively. [8]. Pigeon pea
forms root nodules in association with Rhizobium sp.
bacteria and is capable of fixing 41 to 280 kg/ha of
nitrogen [24]. Preparations of the leaves are used to
treat jaundice, inflammation, and sores of the mouth
[23]. In spite of the importance and benefits of this
crop it does not enjoy global popularity, hence there
is limited information available on this plant. Most of
the rhizobia inoculation studies done in Sudan have
concentrated on faba bean, groundnut, alfalfa, guar,
chickpea and common bean [5] with little focus on
such crops as cowpea, fenugreek and pigeon pea.
One of the major problems that limit
economically successful agricultural production
worldwide is poor soil fertility[35,36,37,38].
Therefore, addition of fertilizers is necessary to
correct poor soil fertility by supplying nutrients
needed for optimum crop growth [7]. Chemical
fertilizers became the target for criticisms mainly
because of the heavy use in the world, where they
were suspected of having adverse impact on the
environment through nitrate leaching, eutrophication,
greenhouse gas emissions and heavy metal uptakes
by plants. Consequently, fertilizer use was identified
as a harmful to the environment. Biofertilizer is a
substance which contains living microorganisms
which, when applied to seed, plant surfaces, or soil,
colonizes the rhizosphere or the interior of the plant
and promotes growth by increasing the supply or
Corresponding Author
Awad Galal Osman, The National Centre for Research, Khartoum, Sudan.
E-mail: [email protected]
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Adv. Environ. Biol., 5(9): 2742-2749, 2011
availability of primary nutrients to the host plant.
[33]. Biofertilizers from microorganisms can replace
chemical fertilizers to increase crop production. In
principle, biofertilizers are less expensive and are
more environmentally-friendly than chemical
fertilizers [9].
The most limiting nutrients for plant growth are
N and P [30,39,40,41,42]. Although soil may contain
vast amounts of either nutrient, mostly are not readily
available for plant.
Atmosphere consists of about 80% nitrogen as a
dinitrogen gas [13]. To be available for plant use,
nitrogen gas must be combined with other elements
(fixed). The process of nitrogen fixation can be
accomplished either biologically by microorganisms
or chemically [18]. Nitrogen fixed symbiotically
mainly by the association between Rhizobium species
and legumes which represents a renewable source of
N for agriculture [2]. Phosphorus is an essential
element for plant nutrition. It has to be added to the
soil as a fertilizer because of its deficiency and low
solubility. Phosphorus is found in an insoluble form
in soil and hence it is unavailable for plants.
However, many microorganisms play a great role in
solubilizing the inorganic insoluble phosphates into a
soluble form through excretion of various organic
acids and also by mineralizing the locked up organic
phosphorus through excretion of various enzymes in
agricultural soils making readily available forms for
plants [6]. This present study was carried out to fill in
one of the gaps in nitrogen and phosphorus
biofertilizer research in Sudan.
Materials And Methods
A field experiment was conducted at Elbagair
area, central Sudan (Latitude 15° 38´ N and longitude
32° 76´ E), for two successive seasons 2009/2010
and 2010/2011 in a factorial design with four
replicates.
In these experiments plants were either
inoculated with five introduced or locally isolated
Rhizobium or Bradyrhizobium strains each alone or
with Bacillus megatherium var. phosphaticum strain
(BMP) alone in addition to combination of each
rhizobial strain with Bacillus megatherium var
phosphaticum strain (BMP). Control plants were kept
for comparison. The land was prepared by deep
ploughing, harrowing then levelling and ridging. The
land was then divided into plots 5 x 4m each.
Three to four seeds were placed in a hole on the
top of the ridge with 20cm spacing (between holes)
and 60cm (between ridges). Plots were immediately
irrigated after sowing and then subsequently irrigated
at 12-15 days intervals. The first sampling was
carried out after four weeks from sowing, and then
sampling was done every two weeks, for eight
weeks. During each sampling, three plants from each
plot were carefully dug out of the soil with their
roots. Plants representing each treatment in each plot
were placed in a paper bag and immediately taken to
the laboratory for the following measurements per
plant: number of nodules, dry weight of nodules,
shoots and roots (after oven drying at 80°C for 48
hours). Plant samples from each treatment were
ground and kept in polyethylene bags for nitrogen
determination by the microkjeldahl method [1].
Shoot phosphorus content was determined
calorimetrically after digestion [11].
Harvest was done at 20 weeks after sowing.
Each plot was harvested separately by cutting the
plants just above soil level. Plants were then threshed
on a large mat, then collected and weighed to
determine yield of each plot. Multifactor analysis of
variance (ANOVA) was used to determine the effect
of different treatments on the measured parameters.
Least significance difference was used to compare
between means [10].
Results and Discussion
Effects of Ttreatments on Nodulation:
Table (1) shows that there was poor nodulation
on the control plants. Schroder and Cruz Perez [31],
reported that nodulation of pigeon pea is frequently
poor. Pigeon pea is nodulated by rhizobia classified
as cowpea miscellany, which are usually abundant in
tropical soils [17]. Rhizobium inoculation
significantly
(P≤0.05)
increased
nodulation
compared to un-inoculated control. The highest
nodule number was obtained by Rhizobium strains
TAL 1132 in the first season and ENRRI 63 in the
second season. In previous studies inoculation of
pigeon pea with different rhizobial strains showed
significant differences on nodulation [17, 28, and
16].
BMP
inoculation
as
phosphobacterin
significantly (P≤0.05) increased nodulation at 6 and
8 weeks after sowing compared to un-inoculated
control in both seasons. Similar results were reported
by Kannaiyan et al. [15] for pigeon pea.
Rhizobium
and
BMP
co-inoculation
significantly (P≤0.05) increased nodule number per
pigeon pea plant at 4 and 6 weeks after sowing in the
first season. At the second season interactions
significantly (P≤0.05) increased nodulation at all
sampling times except ENRRI 63 and USDA
3472, where the increments were insignificant at 4
weeks after sowing. The best interactions were
obtained by Rhizobium strain TAL 209 and
phosphobacterin (BMP) in both seasons. Significant
increment in nodule number of pigeon pea by coinoculation was reported previously [15].
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Adv. Environ. Biol., 5(9): 2742-2749, 2011
Table 1: Effects of treatments on nodules number per pigeon pea plant
First season
Treatments
Uninoculated
Rhizobium
Control
ENRRI 63
ENRRI 4
TAL 209
TAL 1132
USDA 3472
Phosphobacterin B
ENRRI 63 + B
ENRRI 4
+B
TAL 209
+B
TAL 1132 + B
USDA 3472 + B
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
4
1.00
3.75
2.00
2.42
2.08
2.08
0.58
4.17
3.00
5.67
2.67
1.00
0.676
0.390
0.956
Effects of Ttreatments on Nodules Dry Weight:
Inoculation with Rhizobium significantly
(P≤0.05) increased pigeon pea nodules dry weight in
both seasons compared to un-inoculated control
(Table 2). It was reported that rhizobia inoculation
improved pigeon pea nodule biomass [4]. BMP
inoculation significantly (P≤0.05) increased pigeon
pea nodule dry weight at 6 and 8 weeks after sowing
in the second season compared to un-inoculated
6
2.75
6.92
5.42
3.08
8.25
8.17
3.67
2.17
3.17
6.67
8.17
6.67
0.738
0.426
1.044
Second season
Weeks after sowing
8
4
1.92
0.50
3.75
1.33
1.17
0.50
5.25
1.25
12.08
1.25
0.75
0.75
5.50
0.50
2.25
0.67
2.25
1.08
2.75
1.08
2.33
1.83
4.75
0.75
0.787
0.353
0.455
0.204
1.113
0.499
6
0.58
5.25
1.50
1.08
2.00
2.00
2.00
1.92
3.59
1.67
1.58
1.58
0.561
0.324
0.794
8
0.50
1.75
3.25
1.42
1.42
2.08
2.25
3.58
2.50
3.58
3.08
2.33
0.540
0.312
0.763
control. This result is in accord with the results
reported by [15] for pigeon pea.
Co-inoculation with Rhizobium strains and
BMP strain significantly (P≤0.05) increased pigeon
pea nodules dry weight in both seasons. The highest
increasing in nodule dry weight was obtained by the
interaction between strain ENRRI 4 and
phosphobacterin at 4 and 8 weeks after sowing in the
second season. This finding supports the findings of
[15] for pigeon pea.
Table 2: Effects of treatments on nodules dry weight (mg/plant) of pigeon pea
First season
Treatments
4
6
Uninoculated
Control
0.93
28.33
Rhizobium
ENRRI 63
1.03
67.33
ENRRI 4
0.65
52.37
TAL 209
1.16
34.21
TAL 1132
1.29
122.25
USDA 3472
1.77
163.33
Phosphobacterin B
0.43
30.84
ENRRI 63 + B
2.25
52.50
ENRRI 4
+B
0.65
77.50
TAL 209
+B
1.91
47.50
TAL 1132 + B
0.98
110.83
USDA 3472 + B
0.33
84.17
Weeks after sowing
8
4
22.50
1.00
64.17
7.50
15.83
1.00
23.84
27.50
75.01
27.50
5.00
2.50
28.34
1.00
32.50
4.00
25.83
54.00
66.67
14.00
18.34
43.00
31.67
7.50
6
1.50
47.50
9.00
5.00
22.50
45.00
22.50
17.50
42.50
9.00
15.00
17.00
8
1.00
90.00
70.00
12.50
60.00
40.00
10.25
90.00
175.00
12.50
35.00
50.00
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
3.547
2.048
2.017
3.837
2.215
5.426
10.198
5.888
14.422
0.194
0.112
0.274
Effects of Treatments on Root Dry Weight:
From the results in (Table 3) Rhizobium
inoculation significantly (P≤0.05) increased the root
dry weight at all sampling times in the first season, at
the second season the root dry weight significantly
(P≤0.05) increased by all strains except ENRRI 4 and
USDA 3472 at 8 weeks after sowing compared to uninoculated control. These results are in accord with
the results obtained by Mustafa, [19] for pigeon pea.
Inoculation with BMP significantly (P≤0.05)
increased pigeon pea root dry weight at 4 and 6
weeks after sowing in both seasons compared to un-
8.192
4.730
11.586
Second season
1.742
1.005
2.463
inoculated control. This result is in accord with the
results obtained by Osman and Abd-Elaziz, [21] for
faba bean.
Co-inoculation with Rhizobium strains and
phosphobacterin significantly (P≤0.05) increased the
root dry weight compared to un-inoculated control at
4 and 6 weeks after sowing in both seasons. Similar
results were reported by Rugheim and Abdelgani
[26] for faba bean. Interaction between strain ENRRI
63 and phosphobacterin gave the highest significant
increment of pigeon pea root dry weight in the first
season compared to un-inoculated control and other
treatments.
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Adv. Environ. Biol., 5(9): 2742-2749, 2011
Table 3: Effects of treatments on root dry weight (g/plant) of pigeon pea
First season
Treatments
Second season
Weeks after sowing
8
4
4
6
6
8
0.03
0.41
1.85
0.19
0.38
1.26
ENRRI 63
0.06
0.54
2.06
0.23
0.75
1.28
ENRRI 4
0.06
0.54
1.74
0.20
0.48
1.47
TAL 209
0.13
0.56
1.72
0.22
0.69
1.26
0.12
0.46
1.74
0.20
0.97
0.98
0.17
0.55
1.70
0.20
0.76
1.44
0.10
0.50
1.83
0.23
0.76
1.02
0.09
0.65
1.78
0.27
0.71
1.31
0.04
0.78
1.45
0.22
0.67
1.33
0.06
0.53
2.09
0.20
0.71
1.09
0.13
0.64
2.48
0.26
0.51
1.23
LSD for Rhizobium
0.04
0.007
0.48
0.028
1.38
0.217
0.26
0.017
0.49
0.142
1.30
0.064
LSD for phosphobacterin
0.004
0.016
0.126
0.010
0.082
0.037
LSD for Rhizobium x phosphobacterin
0.010
0.040
0.307
0.024
0.200
0.091
Uninoculated
Control
Rhizobium
TAL 1132
USDA 3472
Phosphobacterin
B
ENRRI 63
+B
ENRRI 4
+B
TAL 209
+B
TAL 1132
+B
USDA 3472 + B
Effects of Treatments on Shoot Dry Weight:
Inoculation with Rhizobium strains ENRRI 4,
ENRRI 63 and TAL 209 significantly (P≤0.05)
increased pigeon pea shoot dry weight at 4 and 6
weeks after sowing in the first season (Table 4). In
the second season all strains significantly (P≤0.05)
increased the shoot dry weight at all sampling times
compared to un-inoculated control. Inoculation of
pigeon pea by introduced or locally-isolated bacterial
strains improved dry matter production [16]. BMP
inoculation significantly (P≤0.05) increased shoot
dry weight in both seasons compared to uninoculated control. This result supports the finding of
Kannaiyan et al., [15] for pigeon pea plant dry
weight.
Co-inoculation with Rhizobium strains and
phosphobacterin significantly (P≤0.05) increased the
shoot dry weight in the second season. At 4 weeks
interaction between TAL 1132 and phosphobacterin
gave the highest significant increment in shoot dry
weight, at 6 weeks the highest result was obtained by
ENRRI 63 plus phosphobacterin and at 8 weeks by
TAL 209 plus phosphobacterin in the first season
compared to un-inoculated control and other
treatments. Inoculation of pigeon pea seeds with
multiple co-inoculant produced maximum plant
biomass [32].
Table 4: Effects of treatments on shoot dry weight (g/plant) of pigeon pea
First season
Treatments
Uninoculated
Rhizobium
Control
ENRRI 63
ENRRI 4
TAL 209
TAL 1132
USDA 3472
Phosphobacterin B
ENRRI 63 + B
ENRRI 4
+B
TAL 209
+B
TAL 1132 + B
USDA 3472 + B
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
4
0.42
0.52
0.56
0.52
0.44
0.42
0.44
0.55
0.43
0.43
0.69
0.34
0.037
0.021
0.052
Effects of Treatments on Shoot Nitrogen Content:
Inoculation with Rhizobium strains significantly
(P≤0.05) increased pigeon pea shoot nitrogen content
at 8 weeks after sowing in the first season compared
to un-inoculated control (Table 5). In the second
season Rhizobium strain TAL 209 significantly
6
3.39
4.10
3.95
3.93
3.34
2.96
4.05
5.36
5.27
4.12
3.84
3.39
0.465
0.268
0.657
Second season
Weeks after sowing
8
4
12.30
1.05
12.47
1.55
11.74
1.27
12.33
1.35
12.70
1.58
10.86
1.30
13.18
1.44
12.72
1.60
10.44
1.17
16.68
1.36
14.77
1.45
10.09
1.55
0.692
0.046
0.399
0.027
0.979
0.065
6
2.47
4.14
3.75
4.14
5.45
5.81
4.21
4.00
4.30
5.23
3.66
3.59
0.611
0.352
0.611
8
9.24
11.19
16.10
10.61
9.62
10.14
12.17
11.10
10.31
10.67
10.56
9.91
0.255
0.439
1.075
(P≤0.05) increased nitrogen content at 8 weeks after
sowing compared to un-inoculated control. Osman
and Mohamed [22] reported that inoculation of faba
bean with Rhizobium strain TAL 1400 constantly
resulted in severe increment in N2 fixation.
Inoculation with phosphobacterin significantly
(P≤0.05) increased nitrogen content at 8 weeks after
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Adv. Environ. Biol., 5(9): 2742-2749, 2011
sowing in both seasons compared to un-inoculated
control. This result is in accord with the results
obtained by Rugheim and Abdelgani [25] for faba
bean. Co-inoculation with Rhizobium strains and
phosphobacterin strain significantly (P≤0.05)
increased shoot nitrogen content at 8 weeks after
sowing in the first season compared to un-inoculated
control. Inoculation of pigeon pea seeds with
multiple co-inoculant produced maximum total
nitrogen [32].
Table 5: Effects of treatments on nitrogen content (%) of pigeon pea shoot
First season
6
8
1.93
1.40
2.07
1.96
2.03
2.21
1.47
1.65
2.03
1.51
1.68
1.93
1.96
1.82
1.96
1.89
2.07
1.89
1.86
1.93
1.85
1.58
1.88
1.65
0.201
0.121
0.116
0.069
0.285
0.170
Treatments
Uninoculated
Rhizobium
Control
ENRRI 63
ENRRI 4
TAL 209
TAL 1132
USDA 3472
Phosphobacterin B
ENRRI 63 + B
ENRRI 4
+B
TAL 209
+B
TAL 1132 + B
USDA 3472 + B
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
Effects of Treatments on Shoot Phosphorus Content:
Inoculation with Rhizobium strains TAL 209,
TAL 1132 and USDA 3472 strains significantly
(P≤0.05) increased pigeon pea shoot phosphorus
content at 6 weeks after sowing in both seasons
compared to un-inoculated control (Table 6).
Rhizobium Strains USDA 3472, ENRRI 63 and
ENRRI 4 significantly (P≤0.05) increased shoot
phosphorus content at 8 weeks after sowing in both
seasons. Increments in shoot phosphorus content of
faba bean due to Rhizobium inoculation was
previously reported by Rugheim and Abdelgani [25].
Second season
6
8
3.40
2.91
3.50
3.05
3.15
2.94
3.33
3.40
3.26
2.94
3.15
2.86
3.29
3.33
3.33
3.29
3.22
3.12
3.22
2.98
3.33
3.08
3.22
3.05
0.120
0.407
0.069
0.235
0.170
0.575
Phosphobacterin inoculation significantly (P≤0.05)
increased shoot phosphorus content at 6 weeks after
sowing in both seasons and at 8 weeks after sowing
in the second season compared to un-inoculated
control. Similar result was reported by Hassan and
Abdelgani [12] for lablab bean.
Co-inoculation with Rhizobium strain TAL 209
and phosphobacterin gave the highest significant
shoot phosphorus content at 6 and 8 in the first
season, and with strains USDA 3472 and ENRRI 4 in
the second season. Hassan and Abdelgani [12] [12]
found that Co-inoculation increased shoot
phosphorus content of lablab bean.
Table 6: Effects of treatments on phosphorus content (%) of pigeon pea shoot
Treatments
Uninoculated
Rhizobium
Control
ENRRI 63
ENRRI 4
TAL 209
TAL 1132
USDA 3472
Phosphobacterin B
ENRRI 63 + B
ENRRI 4
+B
TAL 209
+B
TAL 1132 + B
USDA 3472 + B
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
Effects of Treatments on Pigeon pea Yield:
All Rhizobial strains except ENRRI 63 and
ENRRI 4 in the first season significantly (P≤0.05)
increased pigeon pea seed yield in both seasons
(Table 7). The highest yield in both seasons was
obtained by TAL 1132. Pulses seeds treated with
specific strains of Rhizobium increases the yield
First season
6
8
0.60
0.66
0.53
0.66
0.59
0.76
0.67
0.76
0.69
0.66
0.69
0.80
0.64
0.66
0.55
0.62
0.62
0.64
0.71
0.86
0.54
0.82
0.70
0.78
0.058
0.123
0.033
0.022
0.082
0.175
Second season
6
8
0.44
0.10
0.39
0.17
0.43
0.18
0.48
0.13
0.55
0.15
0.53
0.13
0.52
0.19
0.54
0.13
0.49
0.17
0.46
0.17
0.48
0.13
0.48
0.20
0.015
0.048
0.009
0.028
0.022
0.068
through better nodulation [29]. BMP inoculation
significantly (P≤0.05) increased seed yield in both
seasons. Rugheim and Abdelgani [27] found that
phosphate
solubilizing
bacteria
individually
significantly increased faba bean yield.
The effects of interaction between nitrogen
fixing and phosphate solubilizing microorganisms on
legume crops were reported to be relatively scarce
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Adv. Environ. Biol., 5(9): 2742-2749, 2011
[34].
Generally,
Rhizobium
strains
and
phosphobacterin
co-inoculation
significantly
(P≤0.05) increased seed yield in both seasons. The
maximum seed yield in both seasons was obtained by
USDA 4372 and phosphobacterin interaction,
followed by TAL 1132 plus phosphobacterin in the
first season and TAL 209 plus phosphobacterin in the
second season.
Table 7: Effects of treatments on pigeon pea seed yield (Kg/ha)
Treatments
Control
ENRRI 63
ENRRI 4
TAL 209
TAL 1132
USDA 3472
Phosphobacterin B
ENRRI 63 + B
ENRRI 4
+B
TAL 209
+B
TAL 1132 + B
USDA 3472 + B
LSD for Rhizobium
LSD for phosphobacterin
LSD for Rhizobium x phosphobacterin
First season
988.51
995.36
1081.55
1251.68
1483.30
1303.63
1356.01
1279.70
1336.19
847.63
1428.27
1515.44
93.494
53.989
132.221
Uninoculated
Rhizobium
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