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Growth Promotion of Maize (Zea

mays L.) by Plant-Growth-Promoting
Rhizobacteria under Field Conditions
a a a
Ahmad Gholami , Atena Biyari , Manoochehr Gholipoor & Hadi
b
Asadi Rahmani
a
Department of Agronomy, Shahrood University of Technology,
Shahrood, Iran
b
Soil and Water Institute, Tehran, Iran

To cite this article: Ahmad Gholami , Atena Biyari , Manoochehr Gholipoor & Hadi Asadi Rahmani
(2012) Growth Promotion of Maize (Zea mays L.) by Plant-Growth-Promoting Rhizobacteria under
Field Conditions, Communications in Soil Science and Plant Analysis, 43:9, 1263-1272, DOI:
10.1080/00103624.2012.666302

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 Communications in Soil Science and Plant Analysis, 43:12631272, 2012
Copyright Taylor & Francis Group, LLC
ISSN: 0010-3624 print / 1532-2416 online
DOI: 10.1080/00103624.2012.666302

Growth Promotion of Maize (Zea mays L.)

by Plant-Growth-Promoting Rhizobacteria
under Field Conditions

AHMAD GHOLAMI,1 ATENA BIYARI,1 MANOOCHEHR

GHOLIPOOR,1 AND HADI ASADI RAHMANI2
1
Department of Agronomy, Shahrood University of Technology, Shahrood, Iran
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2
Soil and Water Institute, Tehran, Iran

Plant-growth promoting rhizobacteria (PGPR) play an important role in plant health

and soil fertility. The experiment was conducted as factorial experiment with two factors
of Azospirillum and Azotobacter. The bacterial strains were Azospirillum lipoferum
s-21, A. brasilense DSM 1690, A. lipoferum DSM 1691, Azotobacter chroococcum s-5,
and A. chroococcum DSM 2286. The results indicated that growth promotion by PGPR
appears from early stages of growth, 45 days after inoculation (DAI). Beneficial effects
of bacterial inoculation on ear growth were observed after 75 DAI. Inoculation with
PGPR increased dry weights of leaf, stem, and grain and hence total biomass sampled
at 90, 105, and 120 (harvest time) DAI. The greatest grain weight was produced by
Azospirillum s-21 inoculation. Dual inoculation with Azotobacter s-5 + Azospirillum
s-21 significantly increased total dry weight up to 115%. Results of this study showed
that leaf area index and crop growth index were significantly affected by bacterial
treatments.

Keywords Azospirillum, Azotobacter, maize, PGPR

Introduction
The plant rhizosphereT is a dynamic ecological environment of intense microbeplant
interaction for harnessing essential micro- and macronutrients from limited nutrient condi-
tions. Beneficial plantmicroorganism interactions in the rhizosphere are the determinants
of plant health and soil fertility. The interactions in the rhizosphere play an important role
in transformation, mobilization, and solubilization from a limited nutrient pool in the soil
and subsequent uptake by plants to the realize full genetic potential of the crop. Also, soil
microorganisms are very important in the biogeochemical cycles of nutrients in the soil
and in the maintenance of soil health and quality (Jeffries et al. 2003).
Plant-growth-promoting rhizobacteria (PGPR) are beneficial native soil bacteria that
colonize plant roots (Cleyet-Marcel et al. 2001; Glick 1995; Kloepper 1994) and can
improve the plant growth directly and or indirectly. In the past few decades, a large
array of bacteria including species of Pseudomonas, Azospirillum, Azotobacter, Klebsiella,
Enterobacter, Alcaligens, Arthobacter, Burkholderia, Bacillus, and Serratia have been

Received 24 March 2010; accepted 6 September 2011.

Address correspondence to Ahmad Gholami, Department of Agronomy, Shahrood University
of Technology, Shahrood, Iran. E-mail: ahgholami@yahoo.com

1263
 1264 A. Gholami et al.

reported to enhance plant growth (Kloepper, Lifshitz, and Zablotowicz 1989; Glick
1995: Okon and Labandera-Gonzalez 1994a; Sturz and Nowak 2000; Sudhakar et al.
2000).
The PGPR inoculants significantly increased yield in plants such as wheat, corn, rice,
and sugarbeet (Cakmakci, Kantar, and Sahin 2001; Dobbelaere et al. 2001; Okon 1994:
Shaharoona et al. 2006). The mechanisms of plant-growth stimulation by these bacteria
are most probably related to production of plant-growth regulators (Egamberdiyeva 2007;
Jeon et al. 2003; Shaharoona, Arshad, and Zahir 2006; Zahir, Arshad, and Frankenberger
2004), asymbiotic dinitrogen (N2 ) fixation (Mrkovacki and Milic 2001; Salantur, Ozturk,
and Akten 2006), biocontrol agents against a wide range of bacterial and fungal pathogens
(Esitken et al. 2002; Kotan et al. 1999), siderophores, antibiotics, enzymes, and/or fungi-
cidal compounds (Ahmad, Ahmad, and Khan 2006; Bharathi et al. 2004; Jeun et al. 2004);
plant competitiveness and responses to external stress factors (Burd, Dixon, and Glick
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2000; DellAmico, Cavalca, and Andreoni 2008); support of plant symbiosis with other
beneficial microorganisms (Vessey 2003); and solubilization of mineral phosphates and
improve plant nutrient uptake (Myoungsu et al. 2005).
Azospirillum are involved with the plant as an associative symbiosis, and they have
been used as inoculum for phytostimulation of crops, especially in the case of A. brasilense
and A. lipoferum strains (Dobbelaere et al. 2001: Jacoud et al. 1999: Okon and Labandera-
Gonzalez 1994b). Inoculation of plants with Azospirillum could result in a significant
change in various growth parameters, such as increase in plant biomass, nutrient uptake,
tissue nitrogen (N) content, plant height, leaf size, and root length of cereals (Bashan,
Holguin, and de-Bashan 2004). Okon (1985) proposed that inoculation of plants with
Azospirillum caused significant change in various growth parameters, such as increase in
plant biomass, plant height, leaf size, and root length of cereals.
The Azotobacter is another N2 -fixing bacterium in the soil and can enhance plant
growth by producing growth regulators such as indoleacetic acid, gibberellins, and
cytokinins (Barea and Brown 1974; Hegde, Dwived, and Sudhakara 1999). Kloepper and
Beauchamp (1992) have shown that wheat yield increased up to 30% with Azotobacter
inoculation and up to 43% with Bacillus inoculation.
Great variations in the plant response to PGPR in laboratory and field assays demon-
strate that the full potential of rhizobacteria and other microorganisms to promote plant
growth should be more extensively investigated.
In this study, we aimed to (1) evaluate the effects of PGPR strains on plant-growth
parameters, (2) find out the time interval between inoculation with bacteria and statistically
significant growth promotion happening in maize, and (3) compare the different strains of
rhizobacteria for the efficiency of growth promotion.

Materials and Methods

Microorganisms
The bacterial strains Azospirillum lipoferum s-21, Azospirillum brasilense DSM 1690,
Azospirillum lipoferum DSM 1691, Azotobacter chroococcum s-5, and Azotobacter
chroococcum DSM 2286 were used as maize seed treatments. Seeds of maize (SC.
647) were surface sterilized with 0.02% sodium hypochlorite for 2 min and rinsed thor-
oughly in sterile distilled water. For inoculation, seeds were coated with 20% gum arabic
as an adhesive and rolled into the suspension of bacteria (108 cfu mL1 ) with perlite until
uniformly coated.
 PGPR Effects on Maize 1265

Experimental Conditions and Plant Material

The field experiment was carried out at the research farm of Shahrood University of
Technology (latitude of 36 25 N and longitude of 54 57 E with an elevation of 1345 m)
in 2007. The experiment was conducted using a randomized complete block design as
factorial experiment with two factors (Azospirillum and Azotobacter strains) and three
replications. Four-row plots were prepared with intra- and interrow distances of 20 cm
and 70 cm, respectively.
Before sowing, the soil samples from 0 to 30 cm deep were collected to determine
the nutrient contents of the soil. On the basis of the soil test results (Table 1), the soil was
amended with 300 kg ha1 urea (50% was applied at sowing time and the rest side-dressed
at the initiation of the reproductive stage), 150 kg ha1 single superphosphate, and 50 kg
ha1 potassium sulfate. For planting, two seeds were placed 5 cm deep, and at the three-
leaf stage, plants were thinned to one plant per hill. The final plants were considered as
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population (75,000 plants ha1 ).

Growth and Yield Attributes

During the growth period, samples were recorded with 15-day intervals starting from
30 days after inoculation (DAI) to final harvest time at 120 DAI. In each sampling date,
five plants in each plot were tagged, and the measurements of leaf stem, tassel, grain and
shoot weight, stem height, and diameter were recorded. Dry weight of the separate organs
was measured after drying in oven at 75 C for 72 h. Leaf area index (LAI) was calculated
as leaf area/ground area. Crop growth index (CGR), the increase in dry weight per unit
ground area of crop in a unit time, was calculated as (W2 W1) / (t2 t1)GA , where GA
is ground area expressed as g m2 d1 , W1 is the dry weight at the start of the period (t1),
and W2 is the dry weight at the end (t2) (Ghosh 2004).

Statistical Analysis
Analysis of variance (ANOVA) was performed on all experimental data, and means were
compared using the Duncans multirange test with SAS software (SAS System ver. 9). All
differences referred to in the text were significant at the 5% level of probability.

Table 1
Soil chemical properties of the top soil
layer (030 cm)

Texture Loamy clay

O.C.(%) 0.75
pH 7.78
EC (dS.m1 ) 3.9
N(%) 0.04
P 6.4
K 230
Fe (mg kg1 ) 2.72
Mn 6.44
Zn 0.54
Cu 0.78
 1266 A. Gholami et al.

Results

Dry-Matter Accumulation
Maize seeds treated with the different bacterial inoculations showed improvement in plant-
growth parameters over untreated seeds during the growing season (Table 2). At the first
sampling date (30 DAI), the dry weight of plants was similar between PGPR strains and
the control, but after 45 DAI, differences were observed between PGPR-treated and non-
inoculated plants. At this sampling date, leaf dry weight in all inoculated treatments was
significantly greater than the control (varied from 78% to 156%). As shown in Table 2,
inoculation of plants with growth-promoting rhizobacteria significantly enhanced the leaf
and total dry weights at 60 DAI. Ear weight was significantly affected by bacterial inoc-
ulants at 75 DAI; this time was adjusted to the tasseling stage in corn, where strain
Azospirillum s-21 (A0 Z1 ) increased ear weight by 181%. Total dry matter of maize plants
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at 75 DAI were significantly greater than in the control plants, and the values ranged from
58.5 to 130.3 g plant1 . At this stage, control plants showed very poor growth, which may
be attributed to nutrient deficiency. Results showed leaf, stem, ear, and total dry weights
were significantly affected by bacterial inoculations at 90 and 105 DAI. All of the inocu-
lated treatments significantly increased yield components as compared with noninoculated
plants. At 90 DAI, all bacterial treatments significantly increased ear dry weight (varied
from 100% to 159%) compared to the control. The greatest stem dry weight was obtained
by application of Azospirillum s-21. At 105 DAI, the greatest ear weight was 207 g plant1 ,
obtained from Azotobacter chroococcum + Azospirillum s-21 treatment (A2 Z1 ).

Yield and Growth Parameters

The crop was harvested after 120 DAI, and bacterial inoculation significantly enhanced
leaf, stem, and tassel dry weights. Co-inoculation with Azotobacter s-5 + Azospirillum
s-21 (A1 Z1 ) increased leaf and stem dry weights by 72% and 84%, respectively. In this
study, all bacterial treatments significantly increased grain weight. Grain weight produced
by Azospirillum s-21 was 204.72 g plant1 . Dual inoculation with Azotobacter s-5 +
Azospirillum s-21 significantly increased total dry weight up to 115% compared to control.
Inoculation of maize seeds with bacteria strains significantly increased the stem height
and diameter (Table 3). The greatest height and stem diameter of maize plant were obtained
with coinoculation of Azotobacter s-5 + Azospirillum s-21 (182.58 cm) and Azotobacter
s-5 (2.98 cm), respectively (Table 3). The LAI value was significantly affected by bacterial
treatments compared to the control and increased from 17% to 28%. The positive effect of
some of inoculation treatments on CGR was also significant. The greatest value of CGR
was recorded with application of Azospirillum s-21 (Table 3).

Discussion
In the present investigation, PGPR isolates were evaluated for their effects on growth and
yield of field-grown maize. The results indicated that plant-growth promotion by PGPRs
strains appears from early stages of growth (45 DAI) when seedlings are very vulnerable to
environmental stresses. A greenhouse experiment has shown that soybean growth was pro-
moted by two PGPRs at the early growth stage (Dashti 1996). Rice inoculated with a PGPR
strain showed a significant increase in the roots and shoot when compared with the controls
within 15 and 30 days after sprouting (Beneduzi et al. 2008). Also, the growth promotion
 Downloaded by [University of South Carolina ] at 21:12 15 July 2013

Table 2
Effect of PGPR application on growth characteristics of maize at different growth stages
30 DAI 45 DAI 60 DAI 75 DAI 90 DAI 105 DAI
Treatments TW SW LW TW SW LW TW SW LW TW EW SW LW TW EW SW LW TW EW SW LW
A0 Z0 2.8 1.5 1.3 12.5 6.8 5.7b 31.6c 20.4 10.4b 58.5c 17.5b 26.2 13.3 89.1c 43.6b 29.0e 15.2b 141.8c 85.3c 35.8b 19.0b
A0 Z1 3.9 2.0 1.8 32.3 17.6 14.6a 69.9ab 41.8 27.1a 130.3a 49.3a 55.1 23.4 220.3a 112.5a 73.2a 31.5a 248.4ab 164b 57.2a 24.3a
A0 Z2 2.6 1.3 1.2 24.7 12.9 11.8a 53.2b 29.8 22.8a 85.7b 21.8b 40.0 21.7 163.7b 86.9a 49.7d 24.6a 232.5b 154b 52.4a 23.8a
A0 Z3 3.1 1.7 1.4 29.5 16.9 12.5a 62.1ab 36.3 24.9a 112.6ab 32.2ab 55.2 22.1 205.4ab 103.4a 71.7ab 28.0a 252.4ab 164b 58.9a 27.2a
A1 Z0 3.7 1.8 1.8 22.8 11.8 11.2a 76.7a 47.7 26.8a 113.4ab 42.1ab 45.8 21.5 198.2ab 109.4a 59.8abcd 26.2a 272.2ab 180ab 61.0a 27.8a
A2 Z0 3.7 1.8 1.8 21.6 11.3 10.2a 62.3ab 36.4 25.4a 88.5b 24.4b 41.0 20.9 178.3ab 98.1a 50.1cd 27.7a 251.4ab 169ab 54.4a 25.4a

1267
A1 Z1 4.0 2.1 1.8 30.7 16.8 13.8a 77.1ab 46.4 29.4a 122.3a 40.4ab 51.8 26.9 209.2ab 113.1a 65.5abcd 27.9a 269.6ab 180ab 58.1a 28.5a
A1 Z2 2.7 1.2 1.4 20.2 9.7 10.4a 66.2ab 38.5 27.7a 109.4ab 24.5b 59.9 22.3 192.8ab 97.1a 64.2abcd 28.5a 277.6ab 184ab 61.8a 28.5a
A1 Z3 3.5 2.1 1.4 27.1 15.0 12.0a 70.1ab 39.6 28.9a 115.2ab 28.1ab 59.5 25.4 177.6ab 86.4a 61.2abcd 27.4a 245.4b 163b 54.5a 24.5a
A2 Z1 2.7 1.4 1.3 24.0 13.7 10.4a 66.8ab 40.9 24.1a 115.3ab 24.6b 63.1 24.7 189.0ab 91.1a 66.8abc 28.1a 300.7a 207a 63.7a 27.2a
A2 Z2 2.8 1.4 1.3 26.9 14.3 12.6a 61.5ab 34.2 27.3a 115.8ab 33.4ab 55.1 24.2 184.6ab 97.7a 59.9abcd 24.8a 259.1ab 170ab 59.4a 26.6a
A2 Z3 4.2 2.4 1.7 27.7 16.8 10.9a 64.3ab 39.4 24.7a 114.5ab 30.1ab 55.9 25.5 191.6ab 104.4a 56.0bcd 28.7a 269.5ab 180ab 59.2a 26.6a

Notes. DAI, days after inoculation; LW, leaf dry weight (g plant1 ); SW, stem dry weight (g plant1 ); EW, ear dry weight (g plant1 ); TW, total dry weight (g plant1 );
A0 , control; A1 , Azotobacter sp. strain 5; A2 , Azotobacter chroococcum DSM2286; Z0 , control; Z1 , Azospirillum sp. strain 21, Z2 , Azospirillum lipoferum DSM 1691; Z3 ,
Azospirillum brasilense DSM1690. Within the same column and year, means followed by the same letter are not different at the 0.05 probability level.
 Downloaded by [University of South Carolina ] at 21:12 15 July 2013

Table 3
Yield, yield components, and some growth indices of corn in response to inoculation with PGPR

Stem diameter Stem height Shoot weight Grain weight Tassel weight Stem weight Leaf weight
Treatment CGR LAI (cm) (cm) (g plant1 ) (g plant1 ) (g plant1 ) (g plant1 ) (g plant1 )
A0 Z0 13.69b 1.90b 2.37c 157.83d 166.49c 87.97c 1.19b 39.8d 17.7c
A0 Z1 59.86a 2.31a 2.88ab 175.08abc 356.23a 204.72a 2.06a 67.6abc 26.4ab
A0 Z2 21.64b 2.39a 2.57bc 163.83cd 271.46b 153.19b 2.16a 52.9cd 23.7b
A0 Z3 48.16ab 2.27a 2.86ab 172.25abc 339.12ab 199.1ab 2.37a 62.9abc 27.4ab
A1 Z0 45.37ab 2.30a 2.98a 177.75abc 353.93a 193.9 ab 2.38a 74.5a 28.7ab
A2 Z0 35.45ab 2.38a 2.72ab 165.25bcd 315.30ab 189.3ab 2.37a 56.7bc 22.8bc

1268
A1 Z1 50.09ab 2.34a 2.77ab 182.58a 359.78a 202.7ab 2.68a 73.3a 30.6a
A1 Z2 37.83ab 2.45a 2.75ab 168.08bcd 345.72a 199.8ab 1.82ab 67.2abc 26.0ab
A1 Z3 38.40ab 2.28a 2.72ab 168.91abcd 314.60ab 182.0ab 2.31a 60.3abc 24.6ab
A2 Z1 15.48b 2.35a 2.77ab 173.83abc 328.58ab 176.4ab 2.35a 70.7ab 27.3ab
A2 Z2 34.60ab 2.23a 2.69ab 178.25ab 321.43ab 189.1ab 1.81ab 60.2abc 27.4ab
A2 Z3 16.14b 2.26a 2.72ab 175.25ab 298.58ab 163.5ab 2.16a 61.1abc 24.4ab
Notes. A0 , control; A1 , Azotobacter sp. strain 5; A2 , Azotobacter chroococcum DSM2286; Z0, control; Z1 , Azospirillum sp. strain21; Z2 , Azospirillum
lipoferum DSM 1691; Z3 , Azospirillum brasilense DSM1690. Within the same column and year, means followed by the same letter are not different at the
0.05 probability level.
 PGPR Effects on Maize 1269

found in this study is in agreement with the findings of Dobbelaere et al. (2001, 2002),
who assessed the inoculation effect of Azospirillum brasilense on growth of spring wheat.
They observed that inoculated plants resulted in better germination, early development and
flowering, and increased dry weight of both the root system and the upper plant parts as
well as the N-uptake efficiency of plants. Kloepper et al. (1988) showed that PGPR strains
enhanced emergence and early vigor of canola. In sugar beet plants, PGPR inoculation
strongly influenced the weight of root, leaf, and sugar during the early stages of growth
(Cakmakci, Aydn, and Sahin 2006). In potato plantlets grown in vitro, the PGPR strain
increased cytokinin content (Lazarovits and Nowak 1997). However, Piao et al. (2005)
showed that in early growth stages, rice plants inoculated with two Azotobacter strains did
not show any visible growth-promoting effects as compared to the control. At 60 DAI,
significant increase in the amount of leaf and total weight by bacterial inoculation was
observed.
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In this study, beneficial effects of bacterial inoculation on ear growth were observed
after 75 DAI. Seed inoculation with bacterial isolates (except A. lipoferum, A. chroococ-
cum, A. s-5 + A. lipoferum, and A. chroococcum + A. s-21) significantly increased ear dry
weight at this time.
In the present study, inoculation with PGPR at 90, 105, and 120 (harvest time) DAI
significantly improved leaf, stem, ear, and total weights and also LAI and CGR of maize
plants.
Some studies have reported that plant growth may be affected by the synthesis of phy-
tohormones and vitamins, inhibition of plant ethylene synthesis, improved nutrient uptake,
and solubilization of inorganic phosphate (Cakmakci 2006: Dobbelaere, Vanderleyden,
and Okon 2003; Lucy, Reed, and Glick 2004: Puente, Li, and Bashan 2004). Tejera et al.
(2005) showed that the production of stimulatory factors by Azospirillum could be consid-
ered as beneficial factors for increasing growth of sugarcane plants. Some of PGPR strains
may solubilize inorganic P because of excretion of organic acids (Hoberg, Marschner, and
Lieberei 2005).
In this experiment, all bacterial strains increased grain weight compared to the control.
Woodard and Bly (2000) reported that corn inoculated with A. brasilense had greater shoot
dry matter and grain yield. In another study, Azospirillum brasilense and Azospirillum
irakense strains stimulated root development and grain yield of spring wheat and maize
(Dobbelaere et al. 2002). Also, increase in the grain weight, straw yield, and N concen-
trations in spring wheat due to inoculations with Azotobacter chroococcum have been
reported by Kizilkaya (2008). Nandakumar et al. (2001) proposed that the reason may be
the increase in photosynthetic ability of the plants with high chlorophyll content resulting
from PGPR treatment.
In conclusion, inoculation of seed with bacterial strains and in the most cases with dual
inoculation of strains significantly increased grain yield and growth of field-grown maize.
Further research should focus on the effects of various PGPR strains and different crops
and evaluation of the synergistic effects with other rhizospheric microorganisms such as
phosphate-solublizing bacteria, rhizobacteria, and mycorrhiza at various ecological zones
and soil conditions.

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