In: Auxins: Structure, Biosynthesis and Functions
Editors: Andrew H. Keller and Michelle D. Fallon
ISBN: 978-1-62100-504-9
©2011 Nova Science Publishers, Inc.
Chapter 7
INDOLE-ACETIC ACID PRODUCTION BY ROOT
ASSOCIATED BACTERIA AND ITS ROLE IN PLANT
GROWTH AND DEVELOPMENT
Egamberdieva Dilfuza
National University of Uzbekistan, Faculty of Biology and Soil Sciences,
Tashkent, Uzbekistan
Indole-3-acetic acid (IAA) is the most abundant endogenous auxin which has roles in
stem elongation and root growth. The auxin level is usually higher in the rhizosphere,
where high percentage of rhizosphere bacteria is likely to synthesize auxin as secondary
metabolites because of the rich supplies of root exudates. The production of auxin (IAA),
has been recognized as an important factor in direct plant-growth-promoting abilities of
rhizosphere bacteria. They stimulate proliferation of lateral roots that increase nutrient
absorbing surfaces and results in better assimilation of water and nutrients from the soil.
This in turn would be expected to significantly increased the shoot and root length of
plants. This review focuses on indole-3-acetic acid produced by root associated bacteria
and its involvement in plant growth promotion and yield increase.
Key words: indole-3-acetic acid, rhizosphere bacteria, plant growth
INTRODUCTION
The microbial composition in the rhizosphere is diverse and differs greatly from one
plant species to another (Kloepper et al. 1989; Lugtenberg et al. 2001; Pinton et al. 2001;
Marschner et al. 2001). The root associated microorganisms influence plant development,
growth, and environmental adaptation, both beneficially and detrimentally (Kloepper et al.
1986; Glick et al. 1995; Lugtenberg and Kamilova 2004). Various soil microorganisms that
are capable of exerting beneficial effects on plants or antagonistic effects on soil-borne pests
and diseases have potential uses in agriculture to support economic crop production
(Lugtenberg and Kamilova 2004; Mayak et al. 2004; Haas and Défago 2005). Some of them
may be able to improve plant growth by increasing the rate of seed germination and seedling
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Egamberdieva Dilfuza
emergence, minimizing the adverse effects of external stress factors, and protecting plants
from soil-borne pests and diseases (Thomashow and Weller 1996; Berg et al. 2005).
It is reported that plant growth promoting rhizobacteria are able to colonize the
rhizosphere, the root surface, or even superficial intercellular spaces of the plants (Kamilova
et al. 2005) and will facilitate to develop a beneficial association with the plants. Increased
nutrient uptake by plants inoculated with effective bacteria has been attributed to the
production of plant growth regulators by the bacteria at the root interface, which stimulated
root growth and facilitated greater absorption of water and nutrients from the subsoil (Haas
and Défago 2005). Therefore, if the increase in the amount of nutrients taken up by the
PGPB-inoculated plants were simply due to an increase in root surface area, the effect of
PGPB would be entirely dependent on root development, and not on the uptake function
(Lugtenberg and Kamilova 2009).
Mechanisms by which bacteria are able to prevent damage caused by plant pathogens and
promote plant growth include antagonism (Thomashow and Weller 1996; Bloemberg and
Lugtenberg et al., 2001; 2004; Raaijmakers et al. 2009), induction of systemic resistance (Van
Loon 2007), competition for nutrients and niches (Kravchenko et al. 2004; Kamilova et al.
2005), mobilization of nutrients (Lifshitz et al. 1987; Lugtenberg et al. 2001) and production
of phytohormones (Costacurta and Vanderleyden 1995; Spaepen et al. 2009).
This chapter presents an overview of the indole-3- acetic acid (IAA) production by root
associated bacteria, provides some discussion of how bacterial IAA effect plant growth and
also elucidates whether biotic and abiotic factors alter their plant growth stimulation
activities.
AUXINS AND ITS EFFECTS ON PLANTS
Plants use a wide variety of phytohormones such as auxins, abscisic acid, cytokinins,
ethylene and gibberellins, which are all relatively small molecules (Teale et al. 2006). Plant
hormones play an important role in plant physiology, such as seed germination, root
formation, blossom formation etc. Indole-3-acetic acid (IAA) is the most abundant naturally
occurring auxin with a well-documented ability to regulate many aspects of plant
development some of them include the differentiation of vascular tissues, elongation growth,
apical dominance, lateral root initiation, fruit setting and ripening (Macdonald 1997;
Woodward and Bartel 2005). Plants produce active IAA both by de novo synthesis and by
releasing IAA from conjugates (Davies 1995; Bartel 1997).
The exogenous application of auxins to alfalfa (Gruodien and Zvironaite 1971) and
groundnut (Srinivasan and Gopal 1977) promoted plant growth and nodulation. Hayat et al.,
(2008) also observed where IAA significantly affected the length of mung bean, fresh and dry
mass of roots and shoots, the number of nodules and the nitrogenase activity.
It is thought that the repressive effect of salinity on germination could be related to a
decline in endogenous levels of plant growth hormones or phytohormones (Zholkevich and
Pustovoytova 1993; Jackson 1997; Debez et al. 2001). The salt stress reduces the supply of
cytokinin from root to shoot and also the recovery of diffusible auxin from maize coleoptile
tips (Itai et al. 1968). Sakhabutdinova et al. (2003) also reported that salinity resulted in a
progressive decline in the level of IAA in the root system of plants. In this condition seed
Indole-Acetic Acid Production by Root Associated Bacteria …
3
soaking with plant growth regulators and application of additional natural phytohormones
supplied sufficient hormones for normal plant development and growth in saline conditions
(Kabar 1987, Afzal et al. 2005). In other studies the exogenous application of plant growth
regulators (PGRs) e.g. gibberellins (Prakash and Parthapasenan 1990; Afzal et al. 2005),
auxins (Gul et al. 2000; Khan et al. 2001, 2004), cytokinins (Dhingra and Varghese 1985;
Khan and Weber 1986; Gul et al. 2000) produced some benefit in alleviating the adverse
effects of salt stress and they also improve germination, growth, fruit setting, fresh vegetable
and seed yields and yield quality (Saimbhi 1993). In our observation the plant growth
regulators such as auxin and gibberellins did reverse the growth inhibiting effect of salt-stress
to a certain extent in both shoot and root (Table 1).
Among plant growth regulators the IAA and gibberellins showed high stimulatory effect
on the root (up to 3.1 cm) and shoot growth (up to 1.6 cm) of cucumber seedling at all tested
concentrations in saline condition, compared to root (2.4 cm) and shoot (0.7 cm) length of
control cucumber seedling. Gibberelin and auxin stimulated root and/or shoot growth of
cucumber seedling at concentration 0.1, 0.01 µM in non saline condition as well, where zeatin
had no effect on the stimulation of both shoot and root length. Other authors also reported that
pre-sowing plant seeds with plant growth regulators like IAA, gibberellins alleviated the
growth inhibiting effect of salt stress (Singh and Dara 1971; Datta et al. 1998; Sastry and
Shekhawa 2001; Afzal et al. 2005). The use of IAA producing bacteria in crop cultivation as
inoculums may significantly stimulate seed germination, root growth and yield (Mehnaz and
Lazarovits 2006; Egamberdieva 2009).
In our previous study (Egamberdieva 2009) the inoculation of wheat with IAA producing
bacterial strains P. aureantiaca TSAU22, P. extremorientalis TSAU6, and P.
extremorientalis TSAU20 significantly increased seedling root growth of wheat up to 40%
and shoot growth up to 52% at 100mM NaCl compared to control plants.
Table 1. The effect of different concentrations, 0, 0.1, 0.01, and 0.001 µM of gibberelin
(GB), auxin (IAA) and zeatin (ZT) on the shoot and root growth of cucumber seedling in
0.6% NaCl condition (* significantly different p<0.05).
Treatments
Control (0.6% NaCl)
IAA
1.0
0.1
0.01
0.001
GB
1.0
0.1
0.01
0.001
ZT
1.0
0.1
0.01
0.001
Root length, cm
2.4 ± 0.6
Shoot length, cm
0.7 ± 0.3
1.4 ± 0.1
1.8 ± 0.4
2.6* ± 0.9
3,1* ± 0.5
0.6 ± 0.6
0.5 ± 0.5
0.9* ± 0.5
1.2* ± 0.4
2.0 ± 0.8
2.6 ± 0.6
2.9* ± 1.0
3.0* ± 0.9
0.5 ± 0.7
0.9 ± 0.7
1.4* ± 1.5
1.6* ± 0.9
2.2 ± 1.0
2.0 ± 1.0
2.2 ± 0.7
2.5 ± 0.5
0.4 ± 0.7
0.6 ± 0.5
0.5 ± 0.6
0.6 ± 0.5
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Egamberdieva Dilfuza
In addition IAA plays also an important role in plant–pathogen interactions (Jameson
2000). Several studies reported where auxins involved in the infection process of root
pathogens, such as P. ultimum (Rey et al. 2001; Le Floch et al. 2003). Gravel et al. (2007)
studied the effect of IAA on the development of symptoms caused by Pythium ultimum on
tomato plants and where found that low concentrations of IAA (0–0.1 mg ml-1) within the
rhizosphere of plantlets increased the severity of the symptoms caused by P. ultimum, while
higher concentrations (10 mg ml-1), applied either by drenching to the growing medium or by
spraying on the shoot, reduced the symptoms caused by this pathogen.
Fernández-Falcón et al. (2003) suggested that the exogenous application of indoleacetic
acid to banana plants induce resistance to Panama disease and that the resistance induction is
more effective when performed using low doses and frequent applications. Similar result
obtained by Sharaf and Farrag (2004) where IAA reduced infection rate of tomato wilt caused
by Fusarium oxysporum lycopersici. In their study disease suppression exerted by application
of IAA, was achieved through either increasing plant growth exerting a direct harmful effect
on the target pathogen and/or inducing resistance in host tissue.
IAA PRODUCTION BY RHIZOSPHERE MICROORGANISMS
IAA is produced through L-TRP metabolism by many of soil micro-organisms such as
bacteria, fungus and algae (Sarwar and Kremer 1995). Rhizosphere microorganisms
associated with various plants synthesize and release auxin as secondary metabolites because
of the rich supplies of substrates exuded from the roots compared with non rhizospheric soils
(Kampert et al. 1975; Lugtenberg et al. 2001; Shahab et al. 2009, Egamberdieva and
Kucharova 2009). In earlier works Lindberg et al. (1985) and Frankenberger and Arshad
(1995) suggested that root colonizing bacteria that produce phytohormones, when bound to
the seed coat of a developing seedling may act as a mechanism for plant growth stimulation.
In response to root exudates, the root associated microorganisms including symbiotic
species within the genera Rhizobium synthesize indoleacetic acid (IAA) (Costacurta and
Vanderleyden 1995; Frankenberger and Arshad 1995; Mehnaz and Lazarovits 2006).
Tsavkelova and others (2007) studied interactions of rhizobacteria with orchid
Dendrobium moschatum via indole-3-acetic acid (IAA) and they found that bacterial strains
which belong to genera such as Rhizobium, Microbacterium, and Mycobacterium were among
the most active IAA producers. Plant cells take up some of the IAA that is secreted by the
bacteria and, together with the endogenous plant IAA, can stimulate plant cell proliferation
(Glick et al. 2007).
Earlier reports showed that Rhizobium meliloti associated with alfalfa, produced 20 µg/ml
of IAA (Williams and Singer 1990), whereas Rhizobium leguminosarum produced 2.0 µg/ml
of IAA (Beltra et al. 1980). IAA produced by nodule bacteria is transported to other parts of
the plant and might be involved in several stages of the symbiotic relationship (Wheeler et al.
1979; Hunter 1989; Badenoch-Jones et al. 1983). Lindow et al. (1998) studied IAA producing
bacteria associated with pear trees and found relatively high percentage of epiphytic bacteria
on pear leaf and fruit surfaces. They were belonging to different genera such as Pantoea
agglomerans, Pseudomonas syringae, P. viridiflava, P. fluorescens, P. putida, and Rahnella
aquaticus. Barea et al. (1976), found that 90% rhizosphere bacteria isolated from various
Indole-Acetic Acid Production by Root Associated Bacteria …
5
plants were able to produce IAA. In other studies also reported that most of Pseudomonas
strains produced auxin like compounds (Ataei 2005; Zadeh 2006; Khakipaour et al. 2008).
Ruanpanun et al. (2010) found high IAA producing nematophagous actinomycete and fungal
isolates such as Aspergillus sp., Streptomyces sp. Tsavkelova et al. (2006) observed IAA
production in fungi in genera Aspergilllus sp., Fusarium sp. and Paecilomyces sp.
The synthesis of auxin by rhizosphere bacteria often depends on the presence of
phytohormone precursor tryptophan in the root exudates of plants. The presence of Ltryptophan in the medium is a necessary condition of the biosynthesis of indole-3-acetic acid
(IAA) by rhizosphere bacteria (Kravchenko et al. 2004; Kamilova et al. 2006). The
rhizobacteria possesses plant growth–promoting activity when the concentration of
tryptophan in the rhizosphere is sufficiently high (Kravchenko et al. 2004). Rhizosphere
strains consuming of root exudates including available Trp and it is converted to IAA,
whereas plant and bacteria may regulate the IAA biosynthesis in the rhizosphere (Dakora and
Philips 2002). In earlier studies Skerman (1959) observed when the bacteria were grown in
tryptophan supplemented yeast extract mannitol medium, they produced high amount of IAA.
Ahmad et al. (2005) also reported that with an increase in tryptophan concentration from
1 to 5 mg/ml, the production of IAA in fluorescent Pseudomonas isolates increased.
Other studies also reported that Trp considerably stimulates microbial IAA yield in vitro
(Ivanova et al. 2001; Khalid et al. 2004; Egamberdieva and Kucharova 2009). We have also
observed that plant growth promoting bacteria isolated from the rhizosphere of wheat
produced IAA, where Trp increased its biosynthesis (Table 2).
Table 2 The production of IAA by plant growth promoting, root colonizing bacteria (in
medium with tryptophan and without tryptophan).
Bacterial test strain
IAA production
without tryptophan
Pseudomonas putida TSAU1
5,3
Pseudomonas extremorientalis TSAU6
5,7
Enterobacter hormaechei TSAU2
17,6
Psedomonas extremorientalis TSAU20
5,7
Pantoea agglomerans TSAU16
10,5
Pseudomonas `chlororaphis TSAU13
4,3
Alcaligenes faecalis TSAU3
7
Pseudomonas aureantiaca TSAU22
9,2
* Auxin (IAA) level in µg/ml after 5 days of incubation
with tryptophan
100 µg/ml
23,7
4,8
55,6
7,4
23,1
9,4
8,3
41,3
According Ghosh and Basu (2006) among the three different isomers of tryptophan, the
bacteria produced higher amount of IAA with the supplementation of L-tryptophan (138
µg/ml) than in D-tryptophan (15 µg/ml) or DL-tryptophan (84 µg/ml). In earlier work
Dullaart (1970) explained this process due to the utilisation of this essential amino acid partly
in protein synthesis and partly for the formation of other indole compounds in addition to
IAA.
Malhotra and Srivastava (2008) studied IAA biosynthesis by A. brasilense under various
stress conditions and they found that IAA biosynthesis occurs in a Trp dependent manner,
6
Egamberdieva Dilfuza
where exogenous supply of Trp enables the cells to maintain an elevated Trp pool, which is
utilized for IAA biosynthesis.
It has been found that environmental factors affect IAA biosynthesis by rhizosphere
bacteria (Bashan 1998). Ona et al. (2005) reported that oxygen limitation has negative
influence on IAA biosynthesis by A. brasilense. In our study we found that salinity may
inhibit IAA production of root associated bacteria. However salt tolerant bacterial strain
appeared to produce IAA in media with or without tryptophan in saline condition (3%NaCl).
The presence of tryptophan stimulated auxin production of bacterial strains (Figure 1).
Figure 1. The effect of salinity on IAA production ability of P. aureantiaca TSAU22 (bacteria were
grown 7 days in KB medium at 28oC with the absence and presence of 100 µg/ml of the auxin
precursor tryptophan).
Similar findings reported by Malhotra and Srivastava (2008), where A. brasilense SM
was able to withstand the harsh conditions and it could even trigger its IAA synthesizing
ability. Thus nutrient stress affected cellular viability of bacterial strain and significantly
influenced IAA production.
IAA PRODUCING BACTERIA IMPROVE PLANT GROWTH
IAA producing bacteria stimulate seed germination, increase root formation, plant growth
and development (Lugtenberg et al. 2001; Egamberdieva et al. 2010; Shahab et al. 2009).
Different plant seedlings respond differently to variable auxin concentrations and type of
microorganisms (Sarwar and Frankenberger 1994). The low amount of IAA produced by
plant growth promoting rhizobacteria can stimulate the growth of roots, whereas high IAA
production by bacterial strains inhibits the root growth (Loper and Schroth. 1986; Patten and
Glick 1996).
In earlier studies Pilet and Saugy (1985) reported that root elongation is inversely
proportional to exogenous IAA concentrations above a threshold of about 10–6 to 10–9 M.
Thus higher amount of IAA produced by bacterial strains often inhibitory to the roots (Xie et
al., 1996). Also Yasmin et al., (2004) reported that increasing the concentration of tryptophan
Indole-Acetic Acid Production by Root Associated Bacteria …
7
from 1 mg/ml to 5 mg/ml resulted in decreased growth in plants. Other studies reported that
Pseudomonas and Alcaligenes strains affects auxin levels in the root by decreasing IAA
concentration, thus eliminating its negative effects on plants (Leveau and Lindow 2005).
Azotobacter paspali significantly increased the dry weight of shoot and roots of several
plant species through IAA producing ability (Barea and Brown 1974), Pseudomonas putida
produced low level of IAA, but also stimulated the seedling growth of canola (Caron et al.
1995). The plant growth promoting bacteria supply additional IAA into rhizosphere and
stimulate growth of lateral roots and root hairs. This increase nutrient absorbing surfaces and
may lead to greater rates of nutrient absorption through which plant growth will increase
significantly (Hoflich et al. 1995).
The inoculation of wheat seedlings with IAA producing Azospirillum brasilense
increased the number and length of lateral roots (Barbieri et al. 1986). IAA production by a
number of Acetobacter diazotrophicus isolates from sugarcane was confirmed, in addition to
a role in nitrogen fixation, this bacterium could promote rooting and improve sugarcane
growth by direct effects on metabolitic processes (Somers et al. 2004). We have also observed
where IAA producing Pseudomonas strains stimulated root and shoot length and dry weight
of wheat grown in gnotobiotic sand system (Table 3).
Similar results were reported in some of the previous studies showing that inoculation
was found to affect early plant and root development, plant and root dry weight, grain yield
and the N-uptake efficiency of plants (Dobbelaere et al. 2002).
Table 3. The effect of IAA producing bacterial strains on shoot, root growth and dry
matter of wheat grown in gnotobiotic sand system.
Treatments
Shoot length, cm
Control
8.7
Pseudomonas putida TSAU1
12.8*
P. extremorientalis TSAU20
11.7*
P. `chlororaphis TSAU13
12.5*
P. aureantiaca TSAU22
12.2*
P. extremorientalis TSAU6
11.8*
7 days old plants, Significantly different at α =0.05
Root length, cm
11.5
13.8*
13.5*
13.6*
14.4*
11.7
Dry weight, g/plant
0.018
0.029*
0.040*
0.037*
0.034*
0.035*
Cakmakci et al (2005) observed that in the greenhouse, inoculations with PGPR
increased sugar beet root weight by 2.8 – 46.7% depending on the species. Leaf, root and
sugar yield were increased by the bacterial inoculation by 15.5 and 20.8 %, respectively.
In other studies IAA producing Pseudomonas inoculants significantly increased root dry
weight in wheat (Walley and Germida 1997; Egamberdieva and Kucharova 2009), maize
(Egamberdieva 2007), yield in sugar beet (Cakmakci et al. 2001), soybean (Cattelan et al.
1999). Inoculations with P. polymyxa which has ability to produce IAA enhanced grain yield
of wheat (de Freitas 2000), stimulated the growth of rice (Sudha et al. 1999) and conifer
species (Bent et al. 2002).
Hasnain and Sabri (1996) showed that inoculation of wheat with Pseudomonas spp.
stimulated plant growth by reducing plant uptake of toxic ions and increasing the auxin
content. Under drought stress, co-inoculation of bean (Phaseolus vulgaris L.) with Rhizobium
tropici and two strains of P. polymyxa resulted in augmented plant height, shoot dry weight
and nodule number (Figueiredo et al. 2008).
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Egamberdieva Dilfuza
We have also observed that the exogenous application of indoleacetic acid producing
bacteria as inoculants to cotton plants induce resistance to cotton root rot caused by Fusarium
oxysporum and Rhizoctonia solani (unpublished data).
In conclusion, the beneficial effect of plant growth promoting rhizobacteria on growth of
many plants can be partly explained by their ability to produce IAA. The bacterial IAA may
be involved in stimulation of root growth, alleviation of salt stress in both shoot and root of
plants and also can trigger induced systemic resistance in plants against various disease.
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