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Bioscience Research
Print ISSN: 1811-9506 Online ISSN: 2218-3973
Journal by Innovative Scientific Information & Services Network

RESEARCH ARTICLE BIOSCIENCE RESEARCH, 201815(3):1645-1652. OPEN ACCESS

The effectiveness of azotobacter sp. In increasing

grown of local maize and sorghum in the
intercropping system in ultisols
Andi Nurmas1*,La Karimuna1, Laode Sabaruddin1, Andi Khaeruni2, Muhidin1,
Rahayu M2, Rachmawati Hasid1 and Robiatul Adawiyah1
1Department of Agrotechnology, Faculty of Agriculture, Halu Oleo University, Kendari Southeast Sulawesi, Indonesia
2Department of Plant Protection, Faculty of Agriculture, Halu Oleo University, Kendari Southeast Sulawesi,
Indonesia.

*Correspondence:nurmas_aksa@yahoo.co.id Accepted:18 May2018 Published online: 04Aug. 2018

The use of Azotobacter sp. on local maize and sorghum crops grown in an intercropping system in
Ultisol has become one of the feasible and sustainable solutions for increasing their yield. Intensive
applications of chemical fertilizers bring about pollutions to the environment; therefore, the use of bio-
fertilizers as an alternative fertilizer or as a supplement for the chemical fertilizers is essential to be
studied in the field trials. This study was to search for the formulation of Azotobacter sp. isolate effective
to promote growth and yield of local maize and sorghum grown in a multiple cropping system. It was
done in based on the Randomized Block Design in a two-factor factorial design. The first factor was
planting system and the second one was the formulation of Azotobacter sp., a mixture of LP7a+KU6e
and LT2d1+KU6e isolate. The results showed an interaction effect between the two factors tested on
growth and yield of local maize and sorghum, LER partial of maize crop and total LER of the maize-
sorghum multiple-cropping system. Therefore, it can be concluded that the formulation of Azotobacter
sp., a mixture of LP7a+KU6e and LT2d1+KU6e isolate, was effective in increasing the plant N and P
availability and in reducing the use of N and P chemical fertilizers on local maize and sorghum grown in
an intercropping system in an Ultisol.
Keywords: Azotobactersp. Maize and sorghum; Intercropping; Ultisol, Land Equivalent Ratio.

INTRODUCTION with their ability to fix nitrogen , to produce plant

Microbial communities are fundamental
components of soil with impact on plant nutrient
acquisition, growth and health (Grossman et al.,
2011). Microorganisms are fundamental in
metabolism of organic matter, including biological
nitrogen (N2) fixation, which catalyzes the
reduction of atmospheric N2 gas to biologically
available ammonium (Arp, 2000; Madigan et al.
2000). Soil microorganisms are closely related to
plant roots and play key roles in promoting plant
growth via a direct or indirect mechanism (Aly et
al., 2012). The direct effect is often associated
hormones such as auxin. gibberellin and cytokinin
(Ahmad et al., 2005; Babalola, 2010), while the
indirect effect is related to the reduction of
pathogen growth through antibiotic production
(Mahmoud et al., 2004).
Soil management practices also affect
populations of rhizobia. Long-term monocultures
reduce diversity of rhizobia compared to crop
rotation with legume host plants (Depret et al.,
2004). Microbial communities are fundamental
components of soil with impact on plant nutrient
acquisition, growth and health (Grossman et al.,
Nurmas et al., Effectiveness of Azotobacter on growing of local maize and sorghum
2011). Intercropping is especially popular on the
small farms in developing countries. It is defined
as the simultaneous of two or more species in the
same area during the most of their life cycle
(Vandermeer, 1989; Singh et al., 2010).
Comparing to sole crop, intercrops are able to
provide many benefits. It was found that
intercropping may increase yields (Zhang et al.
2011: Karimuna et al., 2012), income (Yildirim and
Guvenc, 2005; Singh et al., 2013), availability of
plant nutrients (Betencourt et al., 2012; Syaiful et
al., 2013, Nurmas, 202015, Nurmas et al., 2018),
reduce the occurrence of diseases (Gomez-
Rodriguez et al., 2003), suppress weeds (Sharma
and Banik, 2013), and decrease the demands for
fertilizer and use of pesticides (Carruthers et al.,
2000). It can be a helpful tool for soil remediation
(Sun et al., 2011) and reduction of wind erosion
(Chen et al., 2010).
Planting in a mixed system can provide
important contributions, especially on the high
risks of plant environmental variables by
minimizing harvest failures as a result of biotic
and abiotic stresses, and on the safe harvest and
the nutrition balance in the production system
(Tsubo et al., 2001). Increasing yield per unit land
area per unit time through efficient solar radiation
use and efficient spacing of mixed plant species
(Baldy and Stigter, 1997; Sullivan, 2003).
Therefore, this study aims to evaluate the
formulation of Azotobacter sp. isolates that
effectively promoting the growth and yield of
maize and sorghum intercropping systems in
Ultisols.
MATERIALS AND METHODS
Experiment material: The materials used
during the study were Azotobacters indigenous,
Jensen’s Medium, Asbhy’s Medium, local maize
and sorghum seeds, NPK fertilizers and cow
manure. Azotobacters indigenous isolated from
the District of South Konawe, Southeast Sulawesi,
Indonesia. Isolates used for bio-fertilizer for local
maize and sorghum crops in Ultisols consisted of
LP7a isolated from paddy-rice rhizospheres,
LT2d1 isolated from sugarcane rhizosphere and
KU6e isolated from sweet-potato rhizospheres.
Treatment: The study was arranged according
to Randomized Block Design two-factor in
factorial design. The first factor was three levels of
intercropping. i.e. T0 (sorghum and maize were
planted at the same time), T1 (sorghum was
planted 10 days before planting maize) and T2
(sorghum was planted 10 days after planting
Bioscience Research, 2018 volume 15(3):1645-1652
maize). The second factor was three levels of
Azotobacter sp. formulation. i.e. A0 (without
Azotobacter sp.), A1 (mixture of isolate LP7a and
KU6e), A2 (mixture of isolate LT2d1+KU6e). Each
treatment combination was replicated three times;
therefore, there were 27 experimental units. In
addition, nine experimental units were made for
maize and sorghum plants in monoculture.
Biopriming on maize and sorghum seeds were
done separately prior their sowing. Such a
biopriming was carried out by a 24-hour
immersion in the selected Azotobacter sp.
formulation at a concentration of 108-109cfu mL-1.
The Azotobacter sp. formulation was applied three
times; the first application was via seed
treatments, while the second and the third
application was done 2 and 4 weeks after
planting, respectively, around the plant root
system at a rate of 10 mL plant-1.
Assessment of Land Equivalent Ratio (LER)
and efficiencies of production
Land Equivalent Ratio (LER) was calculated
according to (Dariush et al., 2006) as follows,
𝒏
𝒀𝒑𝒊
𝑳𝑬𝑹 = ∑
𝒀𝒎𝒊
𝒊
i = 1. 2. 3. .... n
where Ypi is the production of the ith plant
grown in the intercropping system and Ym i is the
production of the ith plant grown in monoculture.
Effectiveness (Ef) treatment of cropping
pattern with Azotobacter sp. formulation of maize
and sorghum yield was calculated using formula:
Treatment - control
Ef (%) =
100 Treatment
Statistical Analysis
The data were analyzed with ANOVA at
confidence level of 95%. To assess the significant
difference among treatment means, the least
significant difference (LSD) test at α = 0.05 was
carried out (Steel et al., 1997).
RESULTS
Uptake of total N and available P on maize and
sorghum:
Effect Azotobacter A1 (LP7a + KU6e) and A2
(LT2d1 + KU6e) on the N content of maize leaves
increased significantly at the age of 4, 6 and 8
WAP, but A0 (without Azotobacter) began to
decrease at the age of 8 WAP (Fig. 1).
1646
Nurmas et al., Effectiveness of Azotobacter on growing of local maize and sorghum

10.00 8.12 0.80 0.74

0.650.60

Uptake P (%)
Uptake N (%) 8.00
6.60 6.63 7.00 0.60
0.50
6.00
4.93 T0A0 0.40 0.46 T0A0
4.00 4.20 4.60 0.35
0.26
2.84 T0A1 0.20 T0A1
2.00 2.83
T0A2 0.11 T0A2
0.10
0.00 0.00
4 6 8 4 6 8
Week after planting (WAP) Week after planting (WAP)

Figure 1. The Relationship between N uptake and availability of P in the leaves of maize plants
at the ages of 4, 6 and 8 WAP

12.00 10.80 0.80 0.71

10.00 0.63 0.58
Uptake N (%)

8.87 9.00 0.60

Uptake P (%)
0.60
8.00 0.51
6.64 7.40 0.49 0.43
6.00 6.10 T0A0 0.40 T0A0
4.43
4.00 3.60 T0A1 0.26 T0A1
0.20 0.20
2.00 2.43 T0A2 T0A2
0.00 0.00
4 8 12 4 8 12
Week after planting (WAP) Week after planting (WAP)

Figure 2. The Relationship between N uptake and availability of P in the leaves of sorghum
plants at the ages of 4. 8 and 12 WAP
.Available P on the maize leaves tissue showed
that isolates A1 and A2 gave significant effect
compared to A0 (without Azotobacter) both at the
age of 4 and 6 WAP. At the age of 8 WAP, the
levels of P were decreased atthe treatment A0, A1
and A2. This was due to the corn plants entered
the generative phase and the P element was used
for the formation of panicles and seeds (Fig. 1)
Total N sorghum leaves tissue showed that N
uptake increased at the age of 4, 8 and 12
WAP. A1 and A2 isolates provided better
response than A0 (without Azotobacter). This
proved that the treatment of isolates Azotobacter
(A1 and A2) had the ability to inhibit atmospheric
nitrogen, but the ability of isolates was different in
producing N2 so that plant growth was also
differred whereas treatment A0 (without
Azotobacter) only utilized nutrients derived from
organic and inorganic fertilizers given at planting
time (Fig. 2 ).
Available P analysis on sorghum leaves tissue
showed different response with N uptake. P
uptake started to increase at the age 4 and 8
WAP and decreased at age 12 WAP, but between
treatment of isolate A1 and isolate A2 isolate was
differred from isolate A0 (without Azotobacter).
This proved the isolates of Azotobacter
sp. (A1 and A2) capable of dissolving P thus
available for sorghum and at 12 WAP sorghum
panicles were out due to lower levels of P in the
leaves of plants. This was due to the P element
translocated to the generative plant parts, such as
panicles and seeds (Figure 2).
LER total and effectiveness of production
Interaction effect of cropping pattern treatment
with the isolation formulation of Azotobacteron the
total LER of maize intercropping with sorghum
showed the best results obtained at the interaction
of sorghum treatment planted 10 days before corn
with isolate A2 formulation with total LER value of
1.89. Overall for the three cropping applied
integrated with two isolates mixture Azotobacter
gave LER greater than 1, indicating the favourable
formulation of Azotobacter sp. isolates of the third
cropping pattern (Table 1).

Bioscience Research, 2018 volume 15(3):1645-1652 1647

Nurmas et al., Effectiveness of Azotobacter on growing of local maize and sorghum

Table 1: Effect of the interaction cropping patterns with isolate Azotobacter sp. formulation of the
LER total intercropping of maize and sorghum in Ultisols

Means
Interactions treatment LSD0.05
T0 T1 T2
A0 1.127Qb 1.356Ra 1.060Rb
A1 1.760Pa 1.663Qb 1.412Qc
A2 1.788Pa 1.894Pa 1.697Pa
LSD0.05 0.207

Note: Values in the same column followed by different letters indicate significant differences according to the LSD
test at α = 0.05
Table 2: The effectiveness (%) treatment of cropping pattern with Azotobactersp formulation on maize and
sorghum yield of intercropping system in Ultisols

Average Average Effectiveness

Effectiveness of maize
Treatme maize yield sorghum yield of sorghum
(%)
nt (t ha-1) (t ha-1) (%)
T0A0 0.464 - 0.577 -
T0A1 1.159 59.97 0.857 32.67
T0A2 1.341 65.40 0.993 41.89
T1A0 0.522 - 0.740 -
T1A1 1.050 50.29 0.979 24.41
T1A2 1.141 54.25 1.215 39.10
T2A0 0.514 - 0.449 -
T2A1 0.830 38.07 0.779 42.36
T2A2 1.283 59.94 0.851 47.47
Effectiveness (Ef): treatment of cropping pattern with Azotobacter sp. formulation of maize and sorghum yields.

Table 3: Effectiveness (%) treatment cropping pattern with Azotobacter sp. formulation to partial LER of
maize and sorghum

Treatment LER partial of Effectiveness of LER LER partial of Effectiveness of

maize partial maize (%) sorghum LER partial sorghum
(%)
T0A0 0.560 - 0.566 -
T0A1 0.975 42.56 0.785 27.90
T0A2 0.985 43.15 0.804 29.60
T1A0 0.630 - 0.726 -
T1A1 0.767 17.86 0.896 18.97
T1A2 0.924 31.82 0.970 25.16
T2A0 0.621 - 0.440 -
T2A1 0.698 11.03 0.714 38.78
T2A2 0.948 34.49 0.748 41.18

Effectiveness (Ef): treatment of cropping pattern with Azotobacter sp. formulation of LER partial maize and sorghum.
of corn and sorghum planting pattern was
The effectiveness treatment with the obtained at the interaction of cropping pattern with
formulation of cropping patterns Azotobacter on formulation of isolate Azotobacter on the
maize and sorghum intercropping system showed treatment of the planting pattern of sorghum was
the treatment of planting time and formulations planted simultaneously with the isolated
Azotobacter isolates T0A2, T1A2 and T2A2 was formulation of Azotobacter sp. A2 isolates (T0A2
more effective than other treatments both maize treatment) amounedt to 65.40%, sorghum planted
and sorghum (Table 2). Effectiveness treatment 10 days before maize (T1A2 treatment) amounted

Bioscience Research, 2018 volume 15(3):1645-1652 1648

Nurmas et al., Effectiveness of Azotobacter on growing of local maize and sorghum
to 54.25 % and sorghum were planted 10 days
after maize (T2A2 treatment) amounted to 59.94
% (Table 2).
This showed that the treatment of cropping
pattern with formulation of isolate Azotobacter sp.
A2 (LT2d1 + KU6e) isolate mixture gave greater
contribution than the mixture of isolate A1 (LP7a +
KU6e) in the intercropping system. In contrast to
the sorghum showed the best treatment obtained
in the cropping pattern with the formulation
mixture Azotobacter sp. isolates A2 (T0A2
treatment) amounted to 47.24 %, i.e. sorghum
planted 10 days after maize (Table 3). The best
partial LER effectiveness was at the T0A2
(43.15%) compared to T2A2 (34.49 %) for maize
plant and T2A2 treatment (41.18 %) was better
than T0A2 (29.60 %) for sorghum plants (Table
3).
DISCUSSION
Results on N total tissue analysis and
available P of corn and sorghum plants showed
that N and P absorption increased significantly,
but the increase between treatment was not the
same (Fig. 1 and 2). The application of
Azotobacter inhibitor with Azospirillum significantly
influenced plant height, number of leaves, number
of branches per plant, chlorophyll content and
rose plant protein compared to single inoculation
and without inoculation (Kaur, 2014). Azotobacter
and Azospirillum as the free-living nitrogen-fixing
bacteria can be considered as biological fertilizers
(Amiri et al., 2013). Free-living nitrogen-free
bacteria such as A. chroococcum and A.
lipoferum. possessing nitrogen-blocking ability
also produce phytohormones such as gibberellin
and IAA, which can promote the growth,
photosynthesis and nutrient uptake of plants (El-
Latief, 2013). Biofertilizers promote plant growth
and production (Hassan et al., 2012). Inoculation
of seed with Azotobacter resulted higher plant
height at time of harvest, and yield of pearl millet
(Patel et al., 2014).
The test results of Azotobacter indigenous
upland rice crop are able to fix up nitrogen from
atmosphere, to produce IAA and to dissolve
phosphate (Nurmas et al., 2014). Phosphate
solvent bacteria are present in the rhizosphere of
food crops, some examples of favorable
associations of PGPR and phosphate solvent
plants are A. chroococcum with wheat (Kumar
and Narula, 1999), E. agglomerans with tomatoes
(Kim et al. 1998), P. Chlororaphis or P. Putida
with soybean (Cattelan et al., 1999). PGPR ability
phosphate solvent in natural habitat depends on
Bioscience Research, 2018 volume 15(3):1645-1652
the nutrients available, the source of carbon,
nitrogen and metal ion (Kim et al. 1998). The
evaluation results of mixed isolates of (LP7a +
KU6e) and (LT2d1 + KU6e) compatible isolates
increased N and P uptake so as to increase
growth and production of maize and sorghum of
the intercropping system on Ultisol. Inoculation of
biological fertilizer mixture formulation is superior
to single isolates. Different microbial inoculation
significantly affect the average total nitrogen (Fig.
1 and 2). In addition, Azotobacter and
Azospirillum treatments have a higher average
nitrogen count than control (without inoculation).
Azotobacter treatment had the highest total
nitrogen at 4 and 6 WAP with the average of
729.77 and 750.47 mg 10-1 kg soil (Mahdi et al.,
2010). Inoculation of Azotobacter sp. a mixture
isolates of (LT2d1+LP7a), (LT2d1+KU6e),
(LP7a+KU6e), and (LT2d1+LP7a+KU6e) was
more effective on stimulating vegetative growth of
local maize compared to single isolates (Nurmas
et al., 2015)
The diversity of PGPR in the rhizosphere
varies according to the type and type of plant, soil,
and nutrients available (Tilak et al., 2005). The
composition of root exudates depends on the
physiological status, species of plants and
microorganisms (Kang et al. 2010). Different
microbial inoculations significantly affect the total
nitrogen. Treatment Azotobacter and Azospirillum
had a total nitrogen is higher than without
inoculation. The azotobacter treatment had the
highest total nitrogen at ages 4 and 6 WAP with
an average of 729.77 and 750.47 mg, azospirillum
produced nitrogen of 610.73 and 631.43 mg and
without inoculation produced nitrogen average
502.04 and 507.21 mg 10 kg-1 soil (Yamprai et al.,
2014).
Increased production of maize and sorghum
crops of intercropping systems can be measured
using Land Equivalent Ratio (LER). The result of
LSD test showed significant difference between
cropping pattern with Azotobacter formulation of
isolate mixture of LP7a + KU6e and LT2d1 +
KU6e isolate compared with no inoculation in both
planting pattern of sorghum and maize (T0),
sorghum was planted 10 days before maize (T1)
and sorghum Planted 10 days after maize (T2)
(Table 1). Land Equivalent Ratio (LER) is a
quantitative index, used to evaluate the efficiency
of cropping patterns (Tables 2 and 3). LER value
is the most appropriate parameter used to
measure the response of different plant species
and grown on the same land (Dariush et al.,
2006). The efficiency of land use in intercropping
1649
Nurmas et al., Effectiveness of Azotobacter on growing of local maize and sorghum
patterns was 38% or even more greater than for
single or monoculture crops (Zhang et al., 2011;
Karimuna, 2013). It has been reported that LER
was significantly influenced by intercropping when
planting sorghum with legumes with LER values
ranging from 1.70 to 1.89 (Dariush et al., 2006).
CONCLUSION
The application of Azotobacter formulation i.e.
isolate LP7a+KU6e and isolate LT2d1+KU6e
were effective in reducing the use of N and P
chemical fertilizers in Ultisol. There was an
interaction effect between intercropping system
and the application of bio-fertilizer Azotobacter sp.
formulation on maize LER partial and maize-
sorghum multiple-cropping total LER. The maize
sowed 10 days after sorghum sowing combined
with Azotobacter sp. formulation of isolate
LT2d1+KU6e showed the best cropping system
treatment in improving local maize and sorghum
growth and yield grown in Ultisol.
CONFLICT OF INTEREST
The authors declared that present study was
performed in absence of any conflict of interest”.
ACKNOWLEGEMENT
The author would like to thank to the Rector of
Halu Oleo University and the Dean of Agriculture
Faculty for providing facilities to carry out this
study.
AUTHOR CONTRIBUTIONS
AN designed and performleed the
experiments and also wrote the manuscript.
Anwar collected the data. LK, LS and AK
performed data analysis and wrote the
manuscript. RM, RH and RA performed field
experiment, MHD reviewed the manuscript. All
authors read and approved the final version.
Copyrights: © 2017 @ author (s).
This is an open access article distributed under the
terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use,
distribution, and reproduction in any medium,
provided the original author(s) and source are
credited and that the original publication in this
journal is cited, in accordance with accepted
academic practice. No use, distribution or
reproduction is permitted which does not comply
with these terms.
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