rhizobacterial potential to alter auxin content and growth of vigna radiata (l.)
TRANSCRIPT
ORIGINAL PAPER
Rhizobacterial potential to alter auxin content and growthof Vigna radiata (L.)
Basharat Ali • Anjum Nasim Sabri •
Shahida Hasnain
Received: 1 August 2009 / Accepted: 4 January 2010 / Published online: 14 January 2010
� Springer Science+Business Media B.V. 2010
Abstract Potential of non-symbiotic plant growth pro-
moting rhizobacteria (PGPR) to influence the endogenous
indole-3-acetic acid (IAA) content and growth of Vigna
radiata (L.) was evaluated. The bacterial strains used
belonged to Pseudomonas, Escherichia, Micrococcus and
Staphylococcus genera. All strains were able to produce
IAA (1.16–8.22 lg ml-1) in the presence of
1,000 lg ml-1 of L-tryptophan as revealed by gas chro-
matography and mass spectrometric (GC–MS) analysis.
However, strains exhibited variable results for other growth
promoting traits such as phosphate solubilization and sid-
erophore or hydrogen cyanide production. Bacterial IAA
production showed significant positive correlation with
endogenous IAA content of roots (r = 0.969; P = 0.01)
and leaves (r = 0.905; P = 0.01) under axenic conditions.
Bacterization of V. radiata seeds significantly enhanced
shoot length (up to 48.10%) and shoot fresh biomass (up to
43.80%) under fully axenic conditions. Bacterial strains
applied under wire-house conditions also improved shoot
length, number of pods, and grain weight up to 58, 65, and
17.15% respectively, over control. Hence, free living (non-
symbiotic) PGPR have the ability to influence endogenous
IAA content and growth of leguminous plants.
Keywords Non-symbiotic PGPR � Endogenous IAA �Growth promoting traits � L-Tryptophan � Axenic
conditions
Introduction
Indole-3-acetic acid (IAA) is quantitatively the most
abundant type of auxins that play a crucial role in many
developmental processes in plants (Woodward and Bartel
2005). Although plants are able to synthesize IAA them-
selves, the microorganisms that are the inhabitants of rhi-
zosphere also contribute to the plant’s auxin pool
(Arkhipova et al. 2005). Due to this ability, IAA producing
bacteria have been used as inoculants to enhance the
growth and yield of crops (Asghar et al. 2004; Khalid et al.
2004). Bacterial strains from different genera have been
shown to produce IAA in the presence of L-tryptophan (Ali
et al. 2009a). The release of L-tryptophan in root exudates
may result in its conversion into IAA by rhizosphere
microbes (Kravchenko et al. 2004). However, IAA pro-
duced by rhizobacteria can influence plant growth only if it
is absorbed by plant roots and not utilized by other
microorganisms present in the vicinity (Martens and
Frankenberger 1994). The application of plant growth
promoting rhizobacteria (PGPR) as crop inoculants for
biofertilization, phytostimulation, and biocontrol would be
an attractive option to reduce the use of chemical fertilizers
which also cause environmental pollution (Bloemberg and
Lugtenberg 2001). Symbiotic associations between legu-
minous plants and rhizobia are well documented for posi-
tive effect on the growth and yield of legumes (Raza et al.
2004; Shaharoona et al. 2006). Auxin regulates the
expression of different genes in Rhizobium-legume inter-
action that involved in plant signal processing and attach-
ment to plant roots. Moreover, changes in auxin balance in
host plant are prerequisite for nodule organogenesis
(Mathesius et al. 1998; Spaepen et al. 2009). In the present
study, we demonstrated the effect of free living (non-
symbiotic) PGPR on the growth of a leguminous plant, i.e.,
B. Ali � A. N. Sabri � S. Hasnain (&)
Department of Microbiology and Molecular Genetics, University
of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan
e-mail: [email protected]
123
World J Microbiol Biotechnol (2010) 26:1379–1384
DOI 10.1007/s11274-010-0310-1
Vigna radiata (mungbean). The ability of PGPR to alter
endogenous IAA content of V. radiata was examined in
order to determine if growth promotion by PGPR is med-
iated by changes in the plant IAA levels. In addition to
auxin production, the bacterial strains were also screened
for other growth promoting attributes, i.e., phosphate sol-
ubilization and siderophore or hydrogen cyanide (HCN)
production.
Materials and methods
Rhizobacteria and determination of growth promoting
traits
Six different PGPR strains, Pseudomonas alcaliphila AvR-
2, Pseudomonas sp. AvH-4, P. aeruginosa As-17, Esche-
richia hermannii SnR-1, Micrococcus sp. AvR-5, and
Staphylococcus saprophyticus CdR-1 were previously
isolated from the rhizosphere of different plants (Ali et al.
2009a). Bacterial strains were evaluated for different
growth promoting traits such as phosphate solubilization,
siderophore, hydrogen cyanide (HCN) and IAA produc-
tion. Phosphate solubilization was determined qualitatively
by streaking strains on Pikovskaya agar plates (Pikovskaya
1948). Development of a clear zone around the colonies
was observed after incubation at 28�C for 7 days. Bacterial
strains were also assayed qualitatively for siderophore
production on CAS agar medium (Alexander and Zuberer
1991). CAS agar plates were streaked with test organisms
and incubated at 28�C for 72 h. Development of yellow to
orange color around a colony was considered as a positive
test for siderophore production. HCN production was
determined as described by Ahmad et al. (2008). For
quantification of bacterial IAA, strains were grown in
100 ml L-broth medium in the absence and presence
(1,000 lg ml-1) of L-tryptophan. IAA from bacterial cul-
ture supernatant was purified, derivatized, and quantified
by gas chromatography and mass spectrometry (GC–MS)
as described by Ali et al. (2009b).
Determination of endogenous IAA content and growth
of V. radiata
Effect of bacterial inoculation on endogenous IAA content
of V. radiata was determined under in vitro conditions.
Seeds were inoculated in pre-autoclaved glass test tubes
(25 9 160 mm) containing 25 g of moistened sand. Seeds
procured from Punjab Seed Cooperation, Lahore, Pakistan,
were surface sterilized with 0.1% solution of HgCl2 and
washed several times with sterile distilled water. Test tubes
with planted seeds were covered with plastic sheets to
avoid contamination. After seed germination, 2-day old
seedlings were treated with 500 ll of bacterial suspension
(107 CFU ml-1). About 500 ll of sterile solution of L-
tryptophan (1,000 lg ml-1) was also injected into rhizo-
sphere as IAA precursor. For control, water and L-trypto-
phan treated seedlings were kept for comparison.
Amendment of seedlings with bacterial suspension and L-
tryptophan was carried out in laminar air flow cabinet
under fully sterile conditions. Six seedlings of each variant
were grown in the growth chamber (MRL-350H; Sanyo,
Osaka, Japan) as described previously (Ali and Hasnain
2007). Leaf and root tissue was collected after 14 days of
seedling growth and immediately frozen in liquid nitrogen
for quantification of free IAA. The frozen samples con-
taining 15 mg of fresh tissue were homogenized in tripli-
cate in 0.5 ml of 0.05 M sodium phosphate buffer (pH 7.0),
containing 0.02% diethyldithiocarbamic acid as an anti-
oxidant and 5 ng 13C6IAA internal standard, using the
MixerMilll (Retsch) and a 3-mm tungsten carbide beads at
a frequency of 25 Hz for 3 min. The samples were then
incubated for 15 min at 4�C with continuous shaking. The
pH was adjusted to 2.7 with 1 M HCl, and the samples
were purified, derivatized, and analyzed by GC–MS as
described in Andersen et al. (2008). In addition to IAA
quantification, shoot and root length of seedlings was
recorded to observe the effect of microbial IAA on plant
growth.
Pot trials under axenic conditions
Pot experiments were conducted to evaluate the ability of
bacterial strains on the growth of V. radiata under axenic
conditions. Seed bacterization was carried out by incubat-
ing sterilized seeds in bacterial cell suspension adjusted
to 107 CFU ml-1. Seeds were inoculated in pots
(6.5 9 6.5 cm) containing autoclaved soil mixture and
vermiculite as mentioned earlier (Ali et al. 2009b). Ini-
tially, eight seeds were inoculated per pot in triplicate and
the experiment was repeated twice. After germination, 5
uniform seedlings were left in each pot. All pots, plastic
trays and covers used during the experiment were sterilized
with 5% solution of sodium hypochlorite for 20 min to
maintain sterility during the experiment. Growth parame-
ters in terms of shoot length, shoot fresh mass, root length
and root biomass were recorded after 2-weeks growth
period. The experiments were conducted at 22 ± 2�C
temperature, 50% humidity and 12 h photoperiod with
light intensity of 150–200 lmol m-2 s-1 in the green
house.
Pot trials under natural conditions
For wire house experiments sterilized seeds treated with
PGPR strains were sown in large pots (30 9 30 cm)
1380 World J Microbiol Biotechnol (2010) 26:1379–1384
123
containing 10 kg of unfertilized garden soil. Seeds were
treated with bacterial suspension as mentioned above.
Initially, 15 sterilized seeds were inoculated in each pot in
six replicates. After germination, seedlings were thinned to
10 per pot. After 6 weeks, further thinning was carried out
by keeping 5 seedlings per pot, which were grown till
maturity. All pots were arranged in a completely random-
ized design in the wire house of Department of Botany,
University of the Punjab, Lahore, Pakistan. Experiment
was conducted between March to June, 2007 under ambi-
ent light and temperature. Plants were irrigated with tap
water when required. At full maturity, growth parameters
including shoot length, number of leaves, number of pods,
and weight of 100 seeds were recorded.
Statistical analysis
For experiments, data were subjected to analysis of vari-
ance (ANOVA) using software SPSS 12 program and
means of different treatments were separated using Dun-
can’s multiple range test (P = 0.05). The correlation
coefficients between bacterial auxin production (in the
presence of L-tryptophan) and different growth parameters
were also calculated at P = 0.01 or P = 0.05.
Results
Growth prompting traits of rhizobacteria
Bacterial strains showed variable growth promoting activ-
ities (Table 1). Phosphate solubilization was detected only
with P. aeruginosa As-17 (Fig. 1). All strains except
E. hermannii SnR-1 were able to produce siderophores.
HCN production was exhibited by P. aeruginosa As-17 and
Micrococcus sp. AvR-5. GC–MS analysis of bacterial
extracts showed positive results for auxin production in the
presence and absence of L-tryptophan with all strains.
However, the strains expressed high IAA levels only when
medium (L-broth) was supplemented with L-tryptophan.
Auxin production ranged from 0.05 to 0.84 and 1.16 to
8.22 lg ml-1 in the absence and presence of L-tryptophan,
respectively (Fig. 2).
Endogenous IAA content and growth of V. radiata
Gas chromatography and mass spectrometric analysis of
plant samples showed elevated levels of IAA when seed-
lings were grown in vitro under bacterial inoculations in
the presence of L-tryptophan (Fig. 3). All bacterial
Table 1 Growth promoting traits of rhizobacteria
Strains Auxin Phosphate
solubilization
Siderophores HCN
P. alcaliphila AvR-2 ? - ? -
Pseudomonas sp. AvH-4 ? - ? -
P. aeruginosa As-17 ? ? ? ?
E. hermannii SnR-1 ? - - -
Micrococcus sp. AvR-5 ? - ? ?
S. saprophyticus CdR-1 ? - ? -
Fig. 1 Phosphate solubilization by P. aeruginosa As-17. Arrowsindicate the clearing zones around colonies
0
2
4
6
8
10
AvR-2 AvH-4 As-17 SnR-1 AvR-5 CdR-1
Bacterial strains
IAA
( g
ml-I
)
Without TRPWith TRP
b
A
a
A
a
A Ab
A
d
b
c
Fig. 2 GC–MS quantification of bacterial indole-3-acetic acid (IAA)
in the presence and absence of L-tryptophan. Each bar represents
mean ± SE of three replicates and bars with same letters are not
statistically different using Duncan’s multiple range test (P = 0.05)
0
100
200
300
400
500
Control TRP AvR-2 AvH-4 As-17 SnR-1 AvR-5 CdR-1
Bacterial strains
En
do
gen
ou
s IA
A (
pg
mg
-I)
Root Leaf
A A
DE
b
ab
Baa a
ab ab
F
C
B
ab
Fig. 3 Effect of bacterial strains on endogenous IAA content of
roots and leaves (pg mg-1 fresh weight) under in vitro conditions.
Each bar represents mean ± SE of three replicates and bars with
same letters are not statistically different using Duncan’s multiple
range test (P = 0.05)
World J Microbiol Biotechnol (2010) 26:1379–1384 1381
123
inoculations enhanced IAA content of roots. Significant
increases were observed with P. aeruginosa As-17 (303%),
Pseudomonas sp. AvH-4 (250%), P. alcaliphila AvR-2
(208%) and E. hermannii SnR-1 (172%), over water treated
seedlings. It was also observed that bacterial treatment
inhibited root elongation. Maximum reduction over water
treated control was observed with Pseudomonas sp. AvH-4
(60.85%) (Fig. 4). Bacterial strains (except Micrococcus
sp. AvR-5) also enhanced IAA content of leaves (Fig. 3).
Significant increases were observed with P. aeruginosa As-
17, Pseudomonas sp. AvH-4 and P. alcaliphila AvR-2 that
showed 294, 245.50 and 244.30% increases, over control.
Increases in IAA content were not accompanied with
concurrent improvement in shoot elongation in majority of
the treatments. However, Pseudomonas sp. AvH-4 and
S. saprophyticus CdR-1 recorded 9.90 and 6.30% increases
respectively, over water treated control plants (Fig. 4).
Bacterial IAA production recorded highly significant
positive correlation with endogenous IAA content of roots
(r = 0.969; P = 0.01) and leaves (r = 0.905; P = 0.01).
Similarly, significant positive correlation (r = 0.961;
P = 0.01) was also observed between IAA content of roots
and leaves. However, in vitro growth of seedlings in terms
of shoot and root length did not show a significant corre-
lation with bacterial auxin production.
Pot trials under axenic conditions
Bacterization of V. radiata seeds with IAA-producing
bacterial strains revealed highly significant increases in
shoot length and shoot fresh mass under axenic conditions
(Table 2). The most pronounced increases in shoot length
were observed with Micrococcus sp. AvR-5 (48.10%),
S. saprophyticus CdR-1 (37.30%), Pseudomonas sp. AvH-
4 (34.20%), E. hermannii SnR-1 (33.10%), P. alcaliphila
AvR-2 (30%) and P. aeruginosa As-17 (29.20%), over
control. Similarly, 43.80, 38.60, 26.60, and 25.75%
increases in shoot fresh weight were observed with Pseu-
domonas sp. AvH-4, P. aeruginosa As-17, P. alcaliphila
AvR-2 and E. hermannii SnR-1, respectively. Bacterial
IAA production positively correlated with shoot fresh mass
(r = 0.936; P = 0.01) but correlation with shoot length
was not significant. For root growth, majority of the bac-
terial strains showed inhibitory effect on root length
(Fig. 5). However, significant increase in root length was
recorded with Micrococcus sp. AvR-5 (35%), over control.
On the other hand, maximum stimulatory effect for root
biomass (32.55%) was observed with P. aeruginosa As-17.
Pot trials under wire house conditions
Bacterial strains exhibited variable growth response for
different growth parameters under natural wire house
conditions (Table 3). For instance, P. alcaliphila AvR-2,
Micrococcus sp. AvR-5, Pseudomonas sp. AvH-4 and
P. aeruginosa As-17 showed significant increases of 58,
57.70, 46.60 and 42.35% in shoot length, respectively, over
control. Maximum increase in number of leaves (39%) was
recorded with Micrococcus sp. AvR-5 and P. alcaliphila
AvR-2. Significant increases in number of pods were
observed with Pseudomonas sp. AvH-4 (65%) and
0
2
4
6
8
10
12
Control TRP AvR-2 AvH-4 As-17 SnR-1 AvR-5 CdR-1
Bacterial strains
Len
gth
(cm
)Shoot Root
bcde abcdab
ecde
a
de
A
B B
AA
A A
abc
A
Fig. 4 Effect of bacterial strains on shoot and root length of V.radiata under in vitro conditions. Each bar represents mean ± SE of
six replicates and bars with same letters are not statistically different
using Duncan’s multiple range test (P = 0.05)
Table 2 Effect of bacterial inoculations on growth of V. radiata (L.) under axenic conditions
Strains Shoot length (cm) Shoot fresh weight (g)a Root length (cm) Root biomass (g)
Control 9.00 ± 0.38 (a) 2.33 ± 0.11 (a) 10.3 ± 0.43 (bc) 0.172 ± 0.03 (a)
P. alcaliphila AvR-2 11.70 ± 0.62 (b) 2.95 ± 0.21 (bc) 8.38 ± 0.40 (ab) 0.180 ± 0.01 (ab)
Pseudomonas sp. AvH-4 12.08 ± 1.07 (b) 3.35 ± 0.17 (d) 8.96 ± 0.36 (ab) 0.178 ± 0.05 (ab)
P. aeruginosa As-17 11.63 ± 0.51 (b) 3.23 ± 0.26 (cd) 7.90 ± 0.50 (a) 0.228 ± 0.04 (b)
E. hermannii SnR-1 11.98 ± 0.77 (b) 2.93 ± 0.11 (bc) 10.0 ± 0.29 (bc) 0.165 ± 0.01 (a)
Micrococcus sp. AvR-5 13.33 ± 1.20 (c) 2.77 ± 0.18 (b) 13.9 ± 1.20 (d) 0.201 ± 0.05 (ab)
S. saprophyticus CdR-1 12.36 ± 0.44 (bc) 2.69 ± 0.10 (b) 11.8 ± 0.38 (c) 0.187 ± 0.02 (ab)
Mean ± SE of two repeated experiments (30 plants). Different letters within same column indicate significant difference between treatments
using Duncan’s multiple range test (P = 0.05)a Fresh weight of 5 plants
1382 World J Microbiol Biotechnol (2010) 26:1379–1384
123
E. hermannii SnR-1 (65%) and P. aeruginosa sp. As-17
(57.50%). Similarly, Pseudomonas sp. AvH-4, E. her-
mannii SnR-1, P. aeruginosa As-17 and P. alcaliphila
AvR-2 showed 17.15, 15.80, 13.90 and 10.45% increases
in grain mass as compared to control. Significant positive
correlation between bacterial IAA production and number
of pods (r = 0.854; P = 0.05) and seed weight (r = 0.881;
P = 0.01) were observed under natural wire house condi-
tions. Highly significant positive correlation (r = 0.885;
P = 0.01) was also found between shoot length and
number of leaves as well as number of pods and seed
weight (r = 0.984; P = 0.01).
Discussion
In the present study, we demonstrated the ability of free
living non-symbiotic PGPR to alter endogenous IAA
content and growth of V. radiata (L.). Bacterial strains
were able to produce IAA in liquid culture medium but
showed variable results for different growth promoting
attributes such as phosphate solubilization, siderophore and
HCN production (Table 1). Phosphorus is very essential for
plant growth and inoculation with phosphate-solubilizing
bacteria has been shown to improve phosphate uptake by
plants (Hameeda et al. 2008). Bacterial strains may protect
plants from phytopathogenic fungi due to siderophore and
HCN production (Ahmad et al. 2008). However, growth
promotion of plants by PGPR is mainly attributed to their
phytohormone production ability especially IAA (Asghar
et al. 2004; Idris et al. 2007). We also previously demon-
strated that bacterial auxin in comparison with standard
IAA (as positive control) induced plant growth in vitro,
over control (Ali and Hasnain 2007). Treatment of V.
radiata seedlings with PGPR strains with addition of L-
tryptophan enhanced the endogenous IAA content of roots
(r = 0.969; P = 0.01) and leaves (r = 0.905; P = 0.01) as
indicated by significant positive correlation with bacterial
IAA production. Ability of bacterial strains to increase IAA
content of seedlings showed a close link to the bacterial
IAA production and plant growth promotion. It was
observed that IAA produced in root environment can be
transported to leaves as indicated by positive correlation
(r = 0.961; P = 0.01) between endogenous IAA content
of roots and leaves. However, despite increases in IAA
content, most of the treatments did not showed concurrent
increases in shoot length under in vitro conditions in test
tube experiments. In the case of root growth, all bacterial
treatments recorded reduction in root length that might be
due to the production of high levels of IAA as a result of
microbial transformation of L-tryptophan to IAA in rhizo-
sphere. This is evident from the high concentrations of IAA
in root samples that may be responsible for the inhibitory
effect on root length. The impact of exogenous IAA on
plant growth ranges from positive to negative that depends
on the amount and sensitivity of the plant tissue to IAA
concentrations (Spaepen et al. 2007). On the other hand,
bacterial strains stimulated growth of V. radiata under
axenic and natural wire house conditions in the absence of
L-tryptophan. In pot experiments, plants may have relieved
from high concentrations of IAA in the absence of
Fig. 5 Effect of bacterial strains on root growth of V. radiata (L.)
under axenic conditions. (a) Pseudomonas sp. AvH-4; (b) P. aerugin-osa As-17; (c) Micrococcus sp. AvR-5; (d) Control. Bar is 1 cm
Table 3 Effect of bacterial inoculations on growth of V. radiata (L.) at final harvest under wire house conditions
Strains Shoot length (cm) No. of leaves No. of pods Seed weight (g)
Control 16.46 ± 0.90 (a) 8.40 ± 0.41 (a) 13.33 ± 1.12 (a) 3.73 ± 0.10 (a)
P. alcaliphila AvR-2 26.00 ± 1.16 (c) 11.00 ± 0.46 (c) 19.00 ± 1.64 (ab) 4.12 ± 0.15 (bc)
Pseudomonas sp. AvH-4 24.13 ± 1.10 (bc) 10.00 ± 0.37 (bc) 22.00 ± 2.00 (b) 4.37 ± 0.26 (c)
P. aeruginosa As-17 23.43 ± 2.0 (bc) 10.00 ± 0.47 (bc) 21.00 ± 1.73 (b) 4.25 ± 0.40 (c)
E. hermannii SnR-1 20.36 ± 0.83 (ab) 9.00 ± 0.60 (ab) 22.00 ± 1.52 (b) 4.32 ± 0.13 (c)
Micrococcus sp. AvR-5 25.46 ± 1.48 (c) 11.00 ± 0.43 (c) 17.00 ± 1.50 (ab) 3.92 ± 0.11 (ab)
S. saprophyticus CdR-1 19.20 ± 0.98 (a) 10.00 ± 0.65 (bc) 18.00 ± 1.30 (ab) 3.96 ± 0.10 (ab)
Mean ± SE of six replicates (30 plants). Different letters within same column indicate significant difference between treatments using Duncan’s
multiple range test (P = 0.05)
World J Microbiol Biotechnol (2010) 26:1379–1384 1383
123
precursor. This growth response might be associated to root
exudates containing tryptophan (that may be in low con-
centrations) being released in rhizosphere and favoring the
adaptation of auxin synthesizing bacteria.
It is evident from significant increases in shoot length
(up to 48.10%), shoot fresh mass (up to 43.80%), root
length (35%) and root biomass (32.55%) under axenic
conditions. In wire house experiments, bacterization of
V. radiata seeds significantly increased shoot length
(16.65–58%), number of leaves (7.10–39%), number of
pods (27.50–65%) and seed weight (5–7.15%), over con-
trol. Growth promotion under axenic and natural conditions
reflected the stimulatory effect of low levels of bacterial
IAA in the absence of precursor L-tryptophan.
Conclusion
In conclusion, bacterial strains expressed high levels of IAA
when medium was supplemented with L-tryptophan. In
plant–microbe experiments, non-symbiotic PGPR showed
the potential to alter endogenous IAA content and growth of
V. radiata. It is reasonable to assume that PGPR can be
assayed as non-rhizobial inoculants for leguminous crops in
field trials.
Acknowledgments We thank Dr. Karin Ljung, Umea Plant Science
Centre (UPSC), Swedish University of Agricultural Sciences, Umea,
Sweden, for GC–MS facilities.
References
Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living
rhizospheric bacteria for their multiple plant growth promoting
activities. Microbiol Res 163:173–181
Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents
to evaluate siderophore production by rhizosphere bacteria. Biol
Fertil Soils 12:39–45
Ali B, Hasnain S (2007) Efficacy of bacterial auxin on in vitro growth
of Brassica oleracea L. World J Microbiol Biotechnol 23:779–
784
Ali B, Sabri AN, Ljung K, Hasnain S (2009a) Auxin production by
plant associated bacteria: impact on endogenous IAA content
and growth of Triticum aestivum L. Lett Appl Microbiol 48:542–
547
Ali B, Sabri AN, Ljung K, Hasnain S (2009b) Quantification of
indole-3-acetic acid from plant associated Bacillus spp. and their
phytostimulatory effect on Vigna radiata (L.). World J Microbiol
Biotechnol 25:519–526
Andersen SU, Buechel S, Zhao Z, Ljung K, Novak O, Busch W,
Schuster C, Lohmann JU (2008) Requirement of B2-type cyclin-
dependent kinases for meristem integrity in Arabidopsis thali-ana. Plant Cell 20:88–100
Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudo-
yarova GR (2005) Ability of bacterium Bacillus subtilis to
produce cytokinins and to influence the growth and endogenous
hormone content of lettuce plants. Plant Soil 272:201–209
Asghar HN, Zahir ZA, Arshad M (2004) Screening rhizobacteria for
improving the growth, yield and oil content of canola (Brassicanapus L.). Aust J Agric Res 55:187–194
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant
growth promotion and biocontrol by rhizobacteria. Curr Opin
Plant Biol 4:343–350
Hameeda B, Harinib G, Rupela OP, Wani SP, Reddy G (2008)
Growth promotion of maize by phosphate-solubilizing bacteria
isolated from composts and macrofauna. Microbiol Res
163:234–242
Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-
dependent production of indole-3-acetic acid (IAA) affects level
of plant growth promotion by Bacillus amyloliquefaciensFZB42. Mol Plant Microbe Interact 20:619–626
Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-
promoting rhizobacteria for improving growth and yield of
wheat. J Appl Microbiol 96:473–480
Kravchenko LV, Azarova TS, Makarova NM, Tikhonovich IA (2004)
The effect of tryptophan present in plant root exudates on the
phytostimulating activity of rhizobacteria. Microbiology
73:156–158
Martens DA, Frankenberger WT Jr (1994) Assimilation of exogenous
20-14C-indole-3-acetic acid and 30-14C-tryptophan exposed to
the roots of three wheat varieties. Plant Soil 166:281–290
Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG,
Djordjevic MA (1998) Auxin transport inhibition precedes root
nodule formation in white clover roots and is regulated by
flavonoids and derivatives of chitin oligosaccharides. Plant J
14:23–34
Pikovskaya RI (1948) Mobilization of phosphorus in soil in connec-
tion with viral activity of some microbial species. Microbiologia
17:362–370
Raza W, Akhtar MJ, Arshad M, Yousaf S (2004) Growth, nodulation
and yield of mung bean (Vigna radiata L.) as influenced by
coinoculation with Rhizobium and plant growth promoting
rhizobacteria. Pak J Agric Sci 41:25–130
Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth
promoting rhizobacteria containing ACC-deaminase on maize
(Zea mays L.) growth under axenic conditions and on nodulation
in mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in
microbial and microorganism-plant signaling. FEMS Microbiol
Rev 31:425–448
Spaepen S, Das F, Luyten E, Michiels J, Vanderleyden J (2009)
Indole-3-acetic acid- regulated genes in Rhizobium etliCNPAF512. FEMS Microbiol Lett 291:195–200
Woodward AW, Bartel B (2005) Auxin: regulation, action and
interaction. Ann Bot 95:707–735
1384 World J Microbiol Biotechnol (2010) 26:1379–1384
123