Plant Growth-Promoting Microbes

for Sustainable Agriculture 2

Suhas P. Wani and S. Gopalakrishnan

Contents
2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
2.2 Mechanisms of PGPR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
2.3 Direct Plant Growth Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
2.4 Indirect Plant Growth-Promoting Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
2.5 PGP Research at ICRISAT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
2.6 Commercialization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
2.7 Inoculant Selection and Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
2.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36

Abstract
Microbes are an integral part of living soil not only in transforming nutrients in
the soil but also with multiple functions in influencing soil health. There are
specific microbes which help the plant to grow well in their presence by various
mechanisms. The direct mechanism may include fixation of atmospheric nitro-
gen, synthesis of various phytohormones and enzymes, and solubilization of
minerals in the soil, while the indirect mechanism includes inhibiting
phytopathogens. Hence, such plant growth-promoting rhizobacteria (PGPR)
need to be harnessed and exploited for sustainable agriculture. Some of the
representative PGPR group includes Azotobacter, Azospirillum, Acinetobacter,
Agrobacterium, Arthrobacter, Bacillus, Burkholderia, Pseudomonas, Serratia,
Streptomyces, Rhizobium, Bradyrhizobium, Mesorhizobium, Frankia, and
Thiobacillus. Demonstrations of these PGPR and their beneficial traits under
glasshouse and field conditions are documented for a range of crops including

S. P. Wani (*) · S. Gopalakrishnan

International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru,
Telangana, India
e-mail: [email protected]; [email protected]

# Springer Nature Singapore Pte Ltd. 2019 19

R. Z. Sayyed et al. (eds.), Plant Growth Promoting Rhizobacteria (PGPR):
Prospects for Sustainable Agriculture,
https://doi.org/10.1007/978-981-13-6790-8_2
20 S. P. Wani and S. Gopalakrishnan

cereals, legumes, fruits, vegetables, herbs, and ornamentals. Several industries are
commercializing the potential PGPR strains as biofertilizers and as biocontrol
agents. However, successful commercialization of PGPR in many developing
countries is a distant dream largely due to the lack of well-developed technology,
quality carrier material, quality control legislation, training programs, and
on-farm demonstrations. The development of quality PGPR inoculum and its
application will definitely lead to an ideal sustainable agricultural system. Further,
PGPR is known for not only reducing the emission of greenhouse gases (GHGs)
and carbon footprint but also increasing nutrient-use efficiency.

Keywords
Plant growth-promoting microbes · Secondary metabolites · Biological control ·
Commercialization · Sustainable agriculture

2.1 Introduction

Food security, agricultural sustainability, energy renewability, and rural livelihoods

depend largely on soil fertility. Land degradation and desertification due to anthro-
pogenic activities causes an estimated loss of 24 billion tons of fertile soil around the
world’s croplands (FAO 2011). It is estimated that, by 2030, the ever-increasing
human population and changing food habits would increase the demand for water by
30%, energy by 45%, and food by 50% (IFPRI 2012). These demands cannot be met
unless the soil fertility is restored. In addition, environmental pollution, today’s
biggest public concern, is largely caused by the use of synthetic pesticides,
fertilizers, and herbicides. This has led to seek an alternative strategy for synthetic
pesticides and fertilizers (Glick et al. 2007). Therefore, a greener and cleaner
approach toward crop protection and production is essential. The use of microbes
for crop protection and production and soil health had been practiced for centuries.
These beneficial microbes are called as “plant growth-promoting rhizobacteria
(PGPR)” (Kloepper and Schroth 1978). These heterogeneous bacteria are usually
found in the rhizosphere and root surfaces and provide benefits to the crops. In recent
years this terminology PGPR has gained a simple expressive term as “plant
probiotics” (Maheshwari 2012).
The rhizosphere soil is rich in nutrients due to the accumulation of sugars,
vitamins, amino acids, organic acids, fatty acids, phenols, and plant growth promoters
released from the roots by secretion, exudation, and deposition. This leads to the
enrichment of microbes (10- to100-fold) which include bacteria, actinobacteria,
fungi, and algae (Uren 2007). The role of rhizospheric microorganisms in plant
growth promotion is widely reported (Vessey 2003; Tilak et al. 2005; Podile and
Kishore 2006). Some of the representative rhizospheric microbes/PGPR include the
genera Acinetobacter, Agrobacterium, Allorhizobium, Arthrobacter, Azorhizobium,
Bacillus, Bradyrhizobium, Brevibacterium, Chromobacterium, Burkholderia,
Hyphomicrobium, Caulobacter, Flavobacterium, Erwinia, Gluconobacter,
Mesorhizobium, Micrococcus, Pseudomonas, Rhizobium, Serratia, Sinorhizobium,
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 21

Sphingomonas, and Streptomyces (Vessey 2003; Vijayabharathi et al. 2016). In

recent years, the plant growth-promoting traits of actinobacteria are getting much
attention (Jog et al. 2012; Gopalakrishnan et al. 2016b).

2.2 Mechanisms of PGPR

PGPR employs a direct and indirect mechanism to enhance plant growth promotion
and protection. The direct mechanisms include the production of growth hormones,
solubilization of phosphorous, fixation of atmospheric nitrogen, and acquisition of
iron. The indirect mechanisms include minimizing the deleterious effects of biotic
stresses through production of low molecular weight compounds such as alcohols,
ammonia, aldehydes, cyanogens, ketones, sulfides, cell wall-degrading enzymes,
and secondary metabolites with antagonistic traits and competition for nutrients
(Glick 2012; Dey et al. 2014).

2.3 Direct Plant Growth Mechanisms

2.3.1 Biological Nitrogen Fixation (BNF)

Nitrogen (N), an essential element for crop growth, is available easily in the air, as
78% of atmosphere is composed of N. However, plants cannot utilize gaseous form
of this N. Currently, a variety of synthetic fertilizers are being used for enhancing
agricultural productivity. Hence, biological alternatives are preferred as these are
addressing economic, environmental, and renewable energy concerns. BNF is a
process of converting atmospheric N into plant assailable N (such as ammonia)
through a reaction between rhizobia and leguminous plants (such as chickpea,
pigeon pea, and groundnut) (Wilson and Burris 1947). Legumes, the major
symbionts of BNF, can meet their own N needs. A major portion of N fixed by
legumes is harvested in grains. The succeeding crop(s) also get benefitted by N in the
form of the root and shoot residues (Bhattacharyya and Jha 2012). Crops such as
sugarcane, wheat, and rice have also the capacity to fix atmospheric N using free-
living bacteria/diazotrophs such as Azoarcus, Cyanobacteria, and Azospirillum.
However, the N fixed by legume-rhizobia symbiosis (13–360 kg N ha
1) is far
greater than the N fixed by free-living bacteria or diazotrophic nonsymbiotic systems
(10–160 kg N ha
1) (Bohlool et al. 1992). Rhizobia are treated on seeds of legumes
for enhanced N fixation (Lindström et al. 1990). They can persist in soil for many
years in the absence of their host (Sanginga et al. 1994). Actinobacteria such as
Streptomyces, Micromonospora, Corynebacterium, Agromyces, Arthrobacter,
Propionibacterium, and Mycobacterium also have been shown to exhibit BNF
(Sellstedt and Richau 2013). Actinobacteria have also been demonstrated for their
BNF capability by acetylene reduction assay (ARA),15N isotope dilution analysis,
ability to grow on nitrogen-free medium, and identification of Nif genes via PCR
amplification (Ghodhbane-Gtari et al. 2010).
22 S. P. Wani and S. Gopalakrishnan

2.3.2 Phosphate Solubilization

Phosphorus (P) plays an important role in cell metabolism and signaling in plants
(Vance et al. 2003). P is present in bound form (with inorganic or organic
molecules), but plants can take only H2PO4
and/or HPO42
form of P (Smyth
2011). Hence, P is extensively used as a synthetic fertilizer, but their excessive
and unmanaged application leads to negative impact on the environment (Correll
1998). The P-solubilizing bacteria mineralize the organic P by several enzymes of
microbial origin, such as acid phosphatases, C-P lyase, D-α-glycerophosphate,
phosphor hydrolases, phosphonoacetate hydrolase, and phytase which solubilizes
the bound form, so that they are available to plants (Gügi et al. 1991; Abd-Alla 1994;
Ohtake et al. 1996; McGrath et al. 1998; Skrary and Cameron 1998; Glick 2012).
Plant growth-promoting (PGP) microbes such as Bacillus, Pseudomonas, and Strep-
tomyces are widely known for P solubilization. Actinomycetes having high
P-solubilizing traits have been reported, for instance, Streptomyces sp. mhcr0816
(TCP 1916 mg l
1, RP 990 mg l
1), Streptomyces sp. (RP 250 mg l
1), and
Arthrobacter sp. (RP 519 mg l
1) are comparable to Pseudomonas sp. (TCP
1500 mg l
1) or Bacillus (TCP 957 mg l
1) strains (Hamdali et al. 2012; Jog et al.
2014). The role of P solubilization by Mesorhizobium mediterraneum in enhancing
plant growth has been reported in barley and chickpea (Peix et al. 2001).

2.3.3 Phytohormone Production

Plant-associated bacteria are known to produce phytohormones (such as auxins) that

regulate plant growth. Phytohormones affect morphological and physiological pro-
cesses of plants even at lower concentrations (Arshad and Frankenberger 1998).
They change growth pattern of the plants and result in branched and lengthier roots
with greater surface area enabling the plants to access water and nutrients from
deeper depths of soils. Several actinobacteria capable of producing auxins,
gibberellins, cytokinins, and abscisic acid are shown in Table 2.1.

2.3.4 Iron Acquisition

In nature, iron exists as insoluble form of hydroxides and oxyhydroxides which are
not accessible to plants. Siderophores (high-affinity iron-chelating compounds) can
be of both the plant and the microbial origin and trap iron present in the soil
(Rajkumar et al. 2010). The mechanism of microbial-origin siderophores in plant
growth is not completely understood, but under low iron available conditions, PGP
is assumed to involve one of the following mechanisms:
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 23

Table 2.1 List of PGP microbes producing growth hormones

Phytohormone/
ACC
deaminase PGP bacteria References
Auxin /IAA Actinomyces sp., Bradyrhizobium, Kaunat (1969), Brown (1972),
Bacillus megaterium, Frankia sp., Wheeler et al. (1984), Abd-Alla
Micrococcus, Methylobacterium (1994), Mahadevan and Crawford
oryzae, Nocardia sp., Rhizobium, (1997), Tokala et al. (2002),
Streptomyces spp., S. atrovirens, Tsavkelova et al. (2006), El-Tarabily
S. griseoviridis K61, S. lydicus (2008), Khamna et al. (2010), Verma
WYEC108, S. olivaceoviridis, et al. (2011), Abd-alla (2013), Lin
S. rimosus, S. rochei, S. viridis and Xu (2013) and Subramanian
et al. (2014)
Gibberellin Actinomyces sp., Bacillus, Katznelson and Cole (1965), Kaunat
Arthrobacter, Micrococcus, (1969), Brown (1972), Merckx et al.
Nocardia sp., Streptomyces sp. (1987) and Tsavkelova et al. (2006)
Cytokinins Arthrobacter, Frankia sp., Leifsonia Sang-Mo et al. (2014), Cacciari et al.
soli, Rhodococcus fascians, (1980), Stevens and Berry (1988),
Pseudomonas, Streptomyces Joshi and Loria (2007) and Pertry
turgidiscabies et al. (2009)
ACC Arthrobacter, Microbacterium El-Tarabily (2008), Dastager et al.
deaminase azadirachtae sp. nov., Leifsonia soli (2010), Madhaiyan et al. (2010a, b)
sp. nov., Micrococcus spp., and Nascimento et al. (2014)
Rhodococcus sp. R04, Streptomyces
spp.
Source: Swarnalakshmi et al. (2016)

1. Microbial-origin siderophores with high redox potential transfer their ferrous

form of iron to a plant’s transport system through apoplastic pathway in roots.
2. Iron chelation by microbial-origin siderophores from soil depends on its concen-
tration, pH, and redox potential and does a ligand exchange with plant-origin
siderophores. During this process, the iron-free plant-origin siderophores are
initially bound to the receptor protein. This complex binds to a receptor, where
the ion exchange between the two siderophores occurs (Crowley 2006).

Besides contributing to plant health, microbial-origin siderophores also involved

in biocontrol of plant pathogens. It functions by acquiring iron, thereby competing
with other pathogenic microbes in the vicinity and supplying it to the plant (Glick
2012). The production of high-affinity siderophores by PGP microbes is perceived as
a means of biocontrol, as phytopathogens produce low-affinity siderophores. PGP
microbes which produce siderophores with high-affinity colonize efficiently in the
rhizosphere (Kloepper et al. 1980). The role of microbial-origin (including
actinobacteria) siderophores in phytopathogens suppression are reported widely
(Yamanaka et al. 2005; Barona-Gomez et al. 2006; Sontag et al. 2006; Macagnan
et al. 2008; D’Onofrio et al. 2010; Johnson et al. 2013).
24 S. P. Wani and S. Gopalakrishnan

2.3.5 Role in Nutrient Cycles

Soil microbes, plant growth-promoting microbes in particular, are the key propellers
of biogeochemical cycles on nutrients including N, C, P, and S (Bloem et al. 1997)
and of which C and N cycle are most important.

2.3.5.1 Carbon Cycle

It is well known that microbes transfer the C primarily for their own survival. For
instance, under aerobic conditions, i.e., in rhizosphere soil and oxic layers of wetland
systems, aerobic methane-oxidizing bacteria (MOB) play the role in C cycle
(Chistoserdova et al. 2005), whereas, under waterlogged anaerobic soils,
hydrogenotrophic archaea and methanogenic bacteria play the role (Trumbore
2006). Microbial C is found maximum in forest soils compared to any other soils.
Typically, microbial C is found a minimum of 100–1000 μg g
1 in well aerated
soils and a maximum of 500–10,000 μg g
1 in undisturbed forest soils with the
intermittent values in ecosystems such as semiarid tropics (SAT) and grasslands
(Kandeler et al. 2005). Microbial biomass C is found about 1–6% of total organic C
in rhizosphere soil with an indirect relationship for increasing soil depth. Formation
of soil organic matter (OM), a major fraction containing soil organic carbon (OC), is
aided by the decomposition process through various hydrolytic enzymes such as
cellulase, protease, amylase, chitinase, glucosidase, and phenoloxidase. These
hydrolytic enzymes convert the macromolecules into low molecular weight
micromolecules for the ready assimilation of microbes (Burns and Dick 2002).

2.3.5.2 Nitrogen Cycle

The first step in the N cycle is assimilation, i.e., biological N2 fixation (BNF). It is
aided by a group of diazotrophic bacteria such as rhizobia, Frankia, Azotobacter,
cyanobacteria, and green sulfur bacteria and of which the first two (rhizobia and
Frankia) occur through the symbiotic process while the last three through the
nonsymbiotic process (Thamdrup 2012). The N fixed, in the form of ammonium,
during the BNF process, is further dissimilated by two-step microbial process, nitrifi-
cation (the aerobic oxidation of ammonium to nitrite and nitrate) and denitrification
(the anaerobic reduction of nitrate to N2 through nitrite, nitric oxide, and nitrous oxide)
(Simon 2002). Nitrification is done by two different sets of microbial groups:
(1) ammonia-oxidizing bacteria (AOB) such as Nitrosomonas, Nitrosospira, and
Nitrosococcus, which transform ammonia to nitrite using ammonia monooxygenase,
and (2) nitrite-oxidizing bacteria (NOB) such as Nitrobacter and Nitrococcus, which
transform nitrite to nitrate using nitrite oxidoreductase (Vaccari et al. 2006).

2.4 Indirect Plant Growth-Promoting Mechanisms

It refers to the use of PGP agents for managing the deleterious effects of biotic
stresses (such as insect pests and pathogens) to improve the overall health of the
plant. Such PGP microbes are also referred as biocontrol agents (BCAs) which
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 25

employ several mechanisms to alleviate the insect pest and pathogen effects. Some
of the important mechanisms are as follows.

2.4.1 Competition

Root exudates of plants play an important role in determining the specific group of
microorganisms living in its vicinity. For instance, flavonoids and phenolic
compounds in the rhizosphere were reported to influence plant symbiosis with
beneficial rhizobacteria (Palaniyandi et al. 2013). Amino acids, organic acids,
vitamins, and sugars were reported to serve as important nutrients for microbes
(Dakora and Phillips 2002). Antagonism through competition for available nutrients
is one form of the biocontrol mechanism used by the beneficial microbes to outlive
pathogens and suppression of disease (Palaniyandi et al. 2013). The production of
hydrolytic enzymes, siderophores, antibiotics, and volatile compounds are some of
the other mechanisms exerted by PGP microbes (Agbessi et al. 2003; Macagnan
et al. 2008; Wan et al. 2008).

2.4.2 Cell Wall-Degrading Enzymes

The cell wall of insect pests and fungal pathogens of plants contain polymers such as
lipids, glucan, chitin, cellulose, and proteins. PGP microbes are known for their
ability to produce cell wall-degrading enzymes. These enzymes disrupt the cell wall
components of insect pests and pathogens which results in cell lysis. PGP microbes
use this as one of the mechanism to manage plant pathogens and insect pests. PGP
microbes are widely reported to produce these hydrolytic enzymes such as peroxi-
dase, chitinase, glucanase, and protease (Gupta et al. 1995; Chater et al. 2010).

2.4.3 Antibiosis

It is one the major biocontrol mechanisms of PGP microbes in nature. The diffusible
compounds produced by BCA and/or PGP bacteria are known to inhibit the
rhizospheric plant pathogens. A broad spectrum of antibiotics such as polyenes,
macrolides, aminoglycosides, nucleosides, and benzoquinones were reported to be
produced by PGP microbes. Actinobacteria are the leading producer of antibiotics.
For instance, the total number of microbial bioactive molecules (as of year 2012) was
about 33,500 and of which 13,700 (41%) were produced by actinobacteria (Berdy
2012). Of these, 1800 metabolites showed antibiosis against pathogenic fungi
(Berdy 2005). Antibiotics produced by actinobacteria are listed in Table 2.2.

2.4.3.1 Induction of Systemic Resistance

Host plant resistance is the best strategy to manage plant pathogens and insect pests
of crops. Induced resistance in plants is elicited by interaction with an external factor
26 S. P. Wani and S. Gopalakrishnan

Table 2.2 List of actinobacteria capable of producing antibiotics

Actinobacterial
species Antibiotic References
Streptomyces sp., Alnumycin, coronamycins, Shockman and Waksman (1951),
S. alboniger, fungichromin, goadsporin, Kondo et al. (1987), Bieber et al.
S. padanus kakadumycins, pamamycin- (1998), Onaka et al. (2001),
607, rhodomycin Castillo et al. (2003), Shih et al.
(2003) and Ezra et al. (2004)
Actinoplanes Teichomycins, teicoplanin Parenti et al. (1978) and Somma
teichomyceticus et al. (1984)
Actinoplanes Friulimicins Vertesy et al. (2000)
friuliensis sp. nov. II.
Actinoplanes Purpuromycin Coronelli et al. (1974)
ianthinogenes N. sp.
Actinoplanes Lipiarmycin Coronelli et al. (1975)
A. utahensis Echinocandin Boeck et al. (1989)
Actinomadura sp. Cationomycin, Nakamura et al. (1981), Patel et al.
chandrananimycins, (1984) and Maskey et al. (2003)
oxanthromicin
Actinomadura Pyralomicins Kawamura et al. (1995)
spiralis
Microbispora sp. Cochinmicins, Igarashi et al. (1998) and Lam et al.
glucosylquestiomycin (1992)
Microbispora aerata Microbiaeratin Ivanova et al. (2007)
Micromonospora Lomaiviticins A and B He et al. (2001)
lomaivitiensis
Micromonospora Sisomicin Reimann et al. (1974)
inyoensis
Micromonospora Everninomicin Weinstein et al. (1964)
carbonacea
Micromonospora Clostomicins Omura et al. (1986)
echinospora subsp.
armeniaca subsp.
nov.
Nocardiopsis New thiopeptide antibiotic Engelhardt et al. (2010)
Nocardia sp. I. Nocathiacins Li et al. (2003)
Nocardia Chemomicin A Sun et al. (2007)
mediterranei subsp.
kanglensis
Source: Swarnalakshmi et al. (2016)

such as PGP microbes or even with a metabolite. In plants, two types of nonspecific
defense systems are widely reported. These are PGP microbe-induced systemic
resistance (ISR) and pathogen-induced systemic acquired resistance (SAR)
(Schuhegger et al. 2006). Hoffland et al. (1995) demonstrated ISR for the first
time in radish. In ISR, plants are treated with PGP microbes providing protection
from pest and pathogen attack (Alstrom 1991; Walters et al. 2013). ISR is regulated
by salicylic acid, ethylene, and jasmonic acid (De Meyer et al. 1999; Verhagen et al.
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 27

Table 2.3 List of antagonistic actinomycetes suppressing plant pathogens

Diseases Pathogen Antagonistic strain References
Root rot of lupine P. cinnamomi M. carbonacea El-Tarabily (2003)
Root rot of P. infestans S. violaceusniger strain Trejo-Estrada et al.
turfgrass YCED-9 (1998)
Root rot of wheat P. infestans S. olivaceoviridis Aldesuquy et al.
(1998)
Lupin root rot P. tabacinum A. missouriensis El-Tarabily (2003)
Lupin root rot F. oxysporum S. halstediiAJ-7 Joo (2005)
Wood rot P. chrysosporium S. violaceusniger XL-2 Shekhar et al. (2006)
Wood rot P. placenta S. violaceusniger XL-2 Shekhar et al. (2006)
Wood rot C. versicolor S. violaceusniger XL-2 Shekhar et al. (2006)
Wood rot G. trabeum S. violaceusniger XL-2 Shekhar et al. (2006)
Damping-off P. aphanidermatum A. campanulatus El-Tarabily et al.
(2009)
Crown rot P. aphanidermatum M. chalcea El-Tarabily et al.
(2009)
Damping off P. aphanidermatum S. rubrolavendulae S4 Loliam et al. (2013)
chickpea
Damping off F. oxysporum Streptomyces sp. Ashokvardhan et al.
chickpea (2014)
Lupin root rot R. solani S. vinaceusdrappus Yandigeri et al.
(2015)
Source: Arasu et al. (2016)

2004). Representative reports on microbes inhibiting plant pathogens and insect

pests are listed in Tables 2.3 and 2.4.

2.5 PGP Research at ICRISAT

PGP microbial research was at a peak in ICRISAT in the 1980s and 1990s but mostly
on BNF. BNF plays an important role in sustaining productivity of soils in the
semiarid tropics (Wani et al. 1995). It was reported to benefit succeeding cereal
crops, such as wheat, rice, sorghum, and maize with a relative yield increase of up to
350% in different cropping systems. Besides calculating the amount of fixed N by
legumes during the determination on legume fixed N in different cropping systems,
it was important to consider the overall N balance of the cropping system. ICRISAT
had gathered such information using chickpea (CP), pigeon pea (PP), cowpea (C),
sorghum (S), safflower (SF), fallow (F), and mung bean (M) on several cropping
system involving S/PP-S þ SF, S þ CP-S þ SF, C/PP-S þ SF, S þ SF-S þ SF,
F þ S-F þ S, F þ CP-F þ S, and M þ S-M þ S (/ intercrop; þ sequential crop; -
rotation) (Wani et al. 1994). It was also suggested that significant contributions
observed in those cropping systems were not only due to legume fixed N but also due
to its N sparing effect, the break-crop effect, and soil microbial activity. It is
28 S. P. Wani and S. Gopalakrishnan

Table 2.4 Lists of microbial compounds with insecticidal and larvicidal properties
Source Compound Activity References
Streptomyces nanchangensisNS3226 Nanchangmycin Insecticidal Sun et al.
(2002)
Streptomyces sp. CP1130 Tartrolone C Insecticidal Lewer et al.
(2003)
Streptomyces galbus Ethyl acetate extract Pesticidal Jo et al.
(2003)
Streptomyces sp.173 Fermented broth Insecticidal Xiong et al.
(2004)
Metarrhizium sp. FKI-1079 Hydroxyfungerins A Insecticidal Uchida et al.
&B (2005)
Streptomyces qinlingensis sp. nov. Fermented broth Insecticidal Zhi-Qin et al.
(2007)
Streptomyces sp.4138 Staurosporine Insecticidal Xiao-Ming
et al. (2008)
Streptomyces sp. KN-0647 Quinomycin A Insecticidal Liu et al.
(2008)
Streptomyces sp. ERI-04 Curde extract Antifeedant Valanarasu
et al. (2010)
Streptomyces microflavus Crude extract Larvicidal El-Bendary
et al. (2010)
Saccharomonospora sp. (LK-1), Crude extract Larvicidal Karthik et al.
Streptomyces roseiscleroticus (2011)
(LK-2), &Streptomyces gedanensis
(LK-3)
Streptomyces sp. CMU-MH021 Fervenulin Nematocidal Ruanpanun
et al. (2011)
Streptomyces microflavus neau3 Macrocyclic lactone Insecticidal Wang et al.
(2011a)
Serratia marcescens NMCC46 Prodiogisin Larvicidal Patil et al.
(2011)
Streptomyces avermitilis NEAU1069 Doramectin Acaricidal Wang et al.
congeners, 1–4 & (2011b)
insecticidal
Streptomyces sp. 2-Hydroxy-3,5,6- Larvicidal Deepika
trimethyloctan-4-one et al. (2011)
Chromobacterium violaceum ESBV Violacein Larvicidal & Baskar and
4400 pupicidal Ignacimuthu
(2012)
Streptomyces sp.,VITSVK5 5- Larvicidal Saurav et al.
(2,4-Dimethylbenzyl) (2011)
pyrrolidin-2-one
(DMBPO)
Saccharopolyspora pogona Butenylspinosyn Insecticides Lewer et al.
(2009)
Source: Vijayabharathi et al. (2014b)
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 29

important to identify high nodulating genotypes for developing an efficient variety.

ICRISAT had done series of research in identifying high nodulating genotypes in all
of its mandate legumes including chickpea, pigeon pea, and groundnut (Nigam et al.
1985; Rupela et al. 1995; Rupela and Johansen 1995). On the other hand, identifying
non-nodulating legumes as a reference for quantifying BNF is a key feature in BNF
research, and ICRISAT had also identified non-nodulating variants in all of its
mandate crops including chickpea (Rupela 1992), pigeon pea (Rupela and Johansen
1995), and groundnut (Nambiar et al. 1986). Such selection, when developed, should
be used not only in crossing programs as sources of high BNF genes but should also
be developed as cultivars after evaluation.
ICRISAT had also contributed significantly to identifying effective rhizobial
strains from chickpea, pigeon pea, and groundnut (Rupela et al. 1991). It also
observed the effect of soil depth, cropping pattern, and season in influencing the
soil rhizobial counts and identified that chickpea rhizobial counts have maintained
even after cropping with pigeon pea, groundnut, and maize but not on rice where the
100-fold decrease was noticed (Rupela et al. 1987). ICRISAT always shared its
rhizobial germplasm to researchers around the world. One set of the rhizobial
collection at ICRISAT was transferred to Indian Agricultural Research Institute
(IARI), New Delhi, India, and another set to University of Queensland, Australia,
and CSIRO, Australia. The collection comprises 800 rhizobia strains nodulating
chickpea, groundnut, and pigeon pea (Rupela 1997).
In addition to the legume-rhizobia symbiosis, nonsymbiotic N fixation has also
been studied mainly on pearl millet and sorghum. Wani (1986) reported genotypic
variation in germplasm lines of sorghum and pearl millet for rhizospheric nitroge-
nase activity. In these studies, of the 184 pearl millet germplasm tested, 18 lines
enhanced nitrogenase activity (> 460 nmol C2H4 h
1 15 cm diam core
1) in the
0–15 cm rhizosphere soils, while 2 lines, J1407 and Gam 73, were reported be to
consistently active over several seasons. Similarly, of the 334 sorghum germplasm,
28 lines enhanced nitrogenase activity (>460 nmol C2H4 h
1 15 cm diam core
1)
(Wani 1986). Dart and Wani (1982) observed the effects of inoculation of Azoto-
bacter and Azospirillum on the grain weight (increased up to 22%) and dry matter
(increased up to 29%) of sorghum. Besides all these significant contributions on
BNF research, ICRISAT had to freeze BNF research in the mid-1990s due to lack of
policy support and funding opportunities. In later years, ICRISAT research focus has
been diverted toward the use of low-cost biological inputs in influencing crop
sustainability. Long-term experiments were conducted for a period of 9 years in
ICRISAT with a new approach in calculating sustainability index with the consider-
ation of nutrient, biological, microbial, and crop indices and demonstrated that the
low-cost biological inputs obtained the highest sustainability index than the conven-
tional systems (Hameeda et al. 2006).
ICRISAT and a few private sector biopesticide manufacturing companies
initiated the ICRISAT-Private Sector Biopesticide Research Consortium (BRC) in
January 2005, which was later renamed as Bio-products Research Consortium to
include PGPR and biofertilizers (Rupela et al. 2005). Eleven biopesticide/
biofertilizer companies joined the consortium as its founding members. The overall
30 S. P. Wani and S. Gopalakrishnan

goal of BRC was to make quality biopesticides and other bio-products to the farming
community at an affordable price. ICRISAT had a collection of >1500 microbial
germplasm (many with PGPR and biopesticidal properties), a few on-the-shelf
technologies [such as Helicoverpa nuclear polyhedrosis virus (HNPV) and a few
proven biopesticidal microbial strains], fermentation technologies, small-scale
fermenters, and expertise in policy issues related to biopesticide testing and registra-
tion. On the other hand, the biopesticide/biofertilizer companies had medium- to
large-scale capacity factories to manufacture bio-products and also the needed
market linkages with a network of agro-dealers. The BRC Phase I was implemented
with good success (2005–2007), and Phase II was started in 2008. Unfortunately,
only 3 out of 11 companies continued their membership.
In recent times, ICRISAT research is focused more toward the usage of PGP
microbes and their secondary metabolites for crop production and protection of our
mandate crops. ICRISAT has isolated and identified more than 1500 PGP
microorganisms including bacteria and actinobacteria, isolated from vermicompost
and rhizospheric soils of rice and chickpea. Of the 1500, 59 PGP bacteria (mostly
Bacillus spp. and Pseudomonas spp.) and actinobacteria (mostly Streptomyces spp.)
were documented for their PGP traits, evaluated under field conditions
(Gopalakrishnan et al. 2014a). Some of the promising PGP bacteria including
Pseudomonas monteilii, P. plecoglossicida, Brevibacterium altitudinis,
B. antiquum, Enterobacter ludwigii, and Acinetobacter tandoii, isolated from system
of rice intensification fields, were documented for their PGP traits under field
conditions on rice. These bacteria enhanced root weight, root length and volume,
tiller numbers, panicle numbers, stover yield, and grain yield (Gopalakrishnan et al.
2012). Actinobacteria such as Streptomyces sp., S. caviscabies, S. globisporus subsp.
caucasicus, and S. griseorubens were also demonstrated for their PGP performance
on rice (Gopalakrishnan et al. 2014b). A PGP diazotrophic bacterium P. geniculata
IC-76, isolated from chickpea nodules, enhanced plant growth and agronomic traits
including nodule weight, pod weight, and seed weight (Gopalakrishnan et al. 2015)
under field conditions on chickpea.
Besides increasing plant growth and yield traits, they also significantly enhanced
rhizospheric available phosphorus (13–44%), total nitrogen (8–82%), and organic
carbon (OC; 17–39%). Production of hydrolytic enzymes, including chitinase,
cellulase, protease, and lipase, by these bacteria and actinobacteria (Table 2.5), is
an additional evidence for the increased soil OC and total nitrogen contents
(Gopalakrishnan et al. 2014a, b). Soil health indicators such as microbial biomass
nitrogen (MBN; 7–321%), microbial biomass carbon (MBC; 23–48%), and dehy-
drogenase activity (14–278%) were also found to enhance on inoculated plots over
the uninoculated control plots on chickpea (Gopalakrishnan et al. 2015), rice
(Gopalakrishnan et al. 2012, 2013, 2014b), and sorghum (unpublished). Figures 2.1,
2.2, and 2.3 illustrate the results of field trials of PGP bacteria/actinobacteria on
enhancing soil health traits.
Apart from their plant growth and yield promotion and soil health traits, PGP
bacteria were also found to have antagonistic traits and act as biocontrol agents. PGP
bacteria including B. antiquum, P. plecoglossicida, E. ludwigii, B. altitudinis,
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 31

Table 2.5 Extracellular enzyme profile identified for PGP bacteria and actinomycetes
Isolates Cellulase Chitinase Lipase Protease
PGP bacteria
SRI-156 + + + +
SRI-158 + + + +
SRI-178 + + + +
SRI-211 + + + +
SRI-229 + + + +
SRI-305 + + + +
SRI-360 + + + +
SBI-23 +

+
SBI-27 +

+
PGP actinomycetes
KAI-26 + + + +
KAI-27 + + + +
KAI-32 + + + +
KAI-90 + + + +
KAI-180 + + + +
SAI-13 + +
+
SAI-25 + + + +
SAI-29 + +
+
Source: Gopalakrishnan et al. (2014a)

A. tandoii, and P. monteilii and actinobacteria including S. setonii, Streptomyces sp.,

S. tsusimaensis, S. africanus, and S. caviscabies were found to have antagonistic
activity against soilborne plant pathogens including Macrophomina phaseolina
(causes charcoal rot in sorghum) and Fusarium oxysporum f. sp. ciceri (causes
wilt in chickpea) under both greenhouse and field conditions (Gopalakrishnan
et al. 2011a, b). These PGP bacteria/actinobacteria were also found to produce
hydrolytic enzymes (in the context of biocontrol) including chitinase and
β-1,3-glucanase (Gopalakrishnan et al. 2014a). In another study, 15 Streptomyces
spp. were found to have broad-spectrum insecticidal activities against lepidopteran
insect pests including Spodoptera litura, Helicoverpa armigera, and Chilo partellus
(Vijayabharathi et al. 2014a). Two insecticidal metabolites, N-(1-(2,2-dimethyl-5-
undecyl-1,3-dioxolan-4-yr)-2-hydroxyethyl)stearamide and cyclo(Trp-Phe), have
been isolated and purified from Streptomyces sp. (Sathya et al. 2016a;
Gopalakrishnan et al. 2016a).
In the context of formulations, ICRISAT is using peat-based formulation for
groundnut, pigeon pea, and chickpea rhizobial inoculants. Quality of microbial
inoculants can be improved only if good carrier is used for maintaining and
multiplying. In order to find whether peat can be used as suitable carrier material
for rhizobial inoculant, a total of 16 rhizobia (six rhizobia specific for chickpea and
five each rhizobia specific for pigeon pea and groundnut) were inoculated on
sterilized peat and allowed to multiply at 28  2  C for 15 days. At the end
32 S. P. Wani and S. Gopalakrishnan

Gopalakrishnan et al. 2015 Control

IC-76

Gopalakrishnan et al. 2014b Control

KAI-180

PGP isolates
Gopalakrishnan et al. 2013 Control
KAI-27
KAI-26

Gopalakrishnan et al. 2012 Control

SRI-360
SRI-305
SRI-229
SRI-211
SRI-178
SRI-158
SRI-156
0 500 1000 1500 2000 2500
Total N (ppm)

Fig. 2.1 Effect of PGP bacteria and actinomycetes on soil total N under field conditions of
chickpea and rice cultivation. Control indicates the treatment groups without any PGP bacterial
inoculation. (Source: Sathya et al. 2016b)

incubation and at 1-month interval for 10 months, peat-based inoculants were tested
for survival and longevity of rhizobia. The rhizobia were enumerated as colony-
forming units (CFU). The results indicated that all 16 rhizobia survived and
maintained purity (at least 108 CFU/ml) up to 9 months in peat-based carrier
materials (Table 2.6).

2.6 Commercialization

Voluminous data and information on better understanding of commercialization are

available for various formulation technologies and longevity and efficacy of the PGP
bacteria and/or rhizobia. However, still the quality of PGP bacteria/rhizobia avail-
able in the market worldwide is of suboptimal or poor quality. Development of
rhizobia as inoculants for leguminous crops is the most valuable contributions ever
made by science to agriculture, as BNF has been demonstrated to reduce N fertilizer
use (Fred et al. 1932). Good quality PGP bacteria/rhizobia are available in the
European Union market for a range of crop species (Guthrie 1896; Perret et al.
2000). However, in Asian countries, still the PGP bacteria/rhizobia inoculant tech-
nology is underdeveloped/slowly developing, and the major reasons are
discussed here.
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 33

1.8 140

1.6
120

Available Phosphorous (ppm)

1.4
Organic carbon (%)

100
1.2
1 80

0.8 60
0.6
40
0.4
20
0.2

0 KA 26 0

C 80

C -76
SR 156

I 8
I- 8
SR 211

I- 9
SR 305
C 60

C -27

l
tro

tro

tro

tro
SR -15
SR -17

SR -22

I-

I-1
I-3

IC
on

on

on

on
I
KA
I-
I

KA
SR

PGP Isolates
Gopalakrishnan Gopalakrishnan Gopalakrishnan Gopalakrishnan
et al. 2012 et al. 2013 et al. 2014b et al. 2015

Fig. 2.2 Effect of PGP bacteria and actinomycetes on soil organic carbon and available phospho-
rous under field conditions of chickpea and rice cultivation. Solid bars ( ) are the % organic
carbon on the left axis, and solid triangles ( ) are the available phosphorous (ppm) on the right
axis. Control indicates the treatment groups without any PGP bacterial inoculation. (Source: Sathya
et al. 2016b)

2.7 Inoculant Selection and Development

The effective PGP microbial strain selection is the core for developing an inoculant.
A set of must-have desirable and essential traits required for selection of inoculant
strains including competence with native microbial flora, host specificity, and
genetic stability are available (Brockwell et al. 1995). Asian countries including
China, India, Myanmar, and Nepal have been reported with a vast diversity of
nodulating rhizobia for many leguminous crops including chickpea, pigeon pea,
and groundnut (Adhikari et al. 2012; Ansari et al. 2014; Htwe et al. 2015; Jiao et al.
2015). Diversity analysis of rhizobia under hostile environments such as soils with
alkalinity, acidity, and micronutrient deficiency was also reported (Biate et al. 2014;
Mishra et al. 2014; Unno et al. 2015; Singh et al. 2016). Biogeographic and
phylogenetic diversity of rhizobia across the world are available through two
genome sequencing reports (Reeve et al. 2015). According to this report, among
the 107 rhizobial strains, only 7 were from Asian origin. This suggests that further
exploration and characterization of rhizobial biodiversity in Asian countries needs to
be done in order to get good quality inoculant.
34 S. P. Wani and S. Gopalakrishnan

200 4000

180
3500
160
MBN and Dehydrogenase activity

3000
140
2500
120

MBC
100 2000

80
1500
60
1000
40
500
20

0 0
KA 26
SR 56

on 0
C 27

l
SR 58

SR 78

SR 11

SR 29

SR 05

C 0

l
tro
tro

tro
8
6

I-
I-1

I-1
I-
I-1

I-1

I-2

I-2

I-3

I-3

on
on

KA
SR

KA

C
PGP Isolates
Gopalakrishnan Gopalakrishnan Gopalakrishnan
et al. 2012 et al. 2013 et al. 2014b

Fig. 2.3 Effect of PGP bacteria and actinomycetes on soil health indicators during field trials of
rice cultivation. Solid bars ( ; ) are the microbial biomass nitrogen (μg g
1 soil) and
dehydrogenase activity (μg TPF g
1 soil 24 h
) on the left axis, and solid diamond ( ) is the
microbial biomass carbon (μg g
1 soil) on the right axis. Control indicates the treatment groups
without any PGP bacterial inoculation. (Source: Sathya et al. 2016b)

2.8 Conclusions

PGP microbe possesses a broad spectrum of benefits including plant growth and
yield, defense against diseases, and survival under stress conditions. This chapter
illustrates the potential of PGP bacteria and highlights its importance in plant growth
induction, defense pathways, and resistance spectrum available against various
stresses on many crops. However, the extent of success in realizing the benefits of
PGP tends to diminish as it moves from laboratory to greenhouse and to fields, which
reflects the scarcity of research on the beneficial effects of PGP microbes under field
conditions. Therefore, the generation of comprehensive knowledge on screening
strategies and intense selection of best strain for rhizosphere competence and
survival is the need of the hour to enhance the field-level successes.
Table 2.6 Viability and longevity of 16 rhizobia in peat formulations over 10 months

Rhizobial Colony-forming units (CFU/ml) at different months (values are mean of 3 replications)
isolates 0 1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10th
Chickpea rhizobia
IC-53 8.5  109 8  109 6.5  109 2.7  109 1.2  109 2.9  108 2.8  108 2.8  108 2.5  108 2  108 1.1  108
9 9
IC-59 3.3  10 2.3  10 2.2  109 1.7  109 2.3  108 1.5  108 1.3  108 1.2  108 1  108 3  107 2.0  107
9 9
IC-76 4.6  10 3.5  10 2.3  109 2  109 1.7  109 4.2  108 4  108 3.9  108 3.7  108 2.65  108 1.2  108
9 9 9 9
IC-2002 16  10 12  10 6.6  10 4.3  10 1.5  109 2.5  108 2.2  108 2  108 1.7  108 0.9  108 2.3  107
9 9 9 9
IC-2018 7.5  10 7.2  10 5.6  10 4.2  10 16  108 4.7  108 4.2  108 3.6  108 3.2  108 1.8  108 1.3  108
9 9 9 9 8
IC-2099 4.4  10 3.8  10 2.4  10 2.1  10 7  10 2.1  108 2  108 1.7  108 1.5  108 9  107 7.0  107
Pigeon pea rhizobia
IC-3195 16  109 8.7  109 3.4  109 2.5  109 1.9  108 1.1  108 9  107 8  107 4  107 1  107 4  106
IC-4059 8.6  109 7.5  109 5.8  109 3.6  109 1  109 5.2  108 4.9  108 3.4  108 2.3  108 1.1  108 4.1  107
IC-4060 18  109 17  109 7.6  109 4.1  109 1  109 4.5  108 4.3  108 4.1  108 3.1  108 1.3  108 7  107
9 9 9 9 9
IC-4061 15  10 11  10 9.7  10 4.2  10 1.7  10 4.4  108 4.2  108 4.1  108 3.6  108 2.2  108 1.1  108
9 9 9 9 8
IC-4062 7.7  10 6.3  10 2.2  10 1.9  10 2.3  10 3.4  108 2.6  108 2.1  108 1.4  108 1  108 6  107
Groundnut rhizobia
IC-7001 5.2  109 4.8  109 4  109 2  109 1.9  108 1.2  108 2.3  108 2.2108 2  108 1  108 2.4  107
9 9 9 9
IC-7017 7.6  10 6.6  10 3  10 2.1  10 2.2  108 1.7  108 1.6  108 1.3  108 1.1  108 7  108 3.3  107
9 9 9 9
IC-7029 8.2  10 6.8  10 5.2  10 3.6  10 2.0  109 5.8  108 5.5  108 5.2  108 4.8  108 1.3  108 1.5  107
9 9 9 9
IC-7100 6.1  10 8.2  10 6.3  10 3.6  10 1.7  109 3.7  108 3.2  108 3  108 2.7  108 1.3  108 7  107
9 9 9 9
IC-7113 8.1  10 7.5  10 5.4  10 4.5  10 2.1  109 5.5  108 5.1  108 4.5  108 3.7  108 1.9  108 1.2  108
Source: Gopalakrishnan et al. (2016b)
36 S. P. Wani and S. Gopalakrishnan

References
Abd-Alla MH (1994) Solubilization of rock phosphates by Rhizobium and Bradyrhizobium. Folia
Microbiol 39:53–56
Abd-Alla MH, El-Sayed ESA, Rasmey AHM (2013) Indole-3-acetic acid (IAA) production by
Streptomyces atrovirens isolated from rhizospheric soil in Egypt. J Biol Earth Sci 3:B182–B193
Adhikari D, Kaneto M, Itoh K, Suyama K, Pokharel BB, Gaihre YK (2012) Genetic diversity of
soybean-nodulating rhizobia in Nepal in relation to climate and soil properties. Plant Soil
357:131–145
Agbessi S, Beausejour J, Dery C, Beaulieu C (2003) Antagonistic properties of two recombinant
strains of Streptomyces melanosporofaciens obtained by intra-specific protoplast fusion. Appl
Microbiol Biotechnol 62:233–238
Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces
on growth and productivity of wheat plants. Folia Microbiol 43:465–470
Alstrom S (1991) Induction of disease resistance in common bean susceptible to halo blight
bacterial pathogen after seed bacterization with rhizosphere pseudomonads. J Gen Appl
Microbiol 37:495–501
Ansari PG, Rao DLN, Pal KK (2014) Diversity and phylogeny of soybean rhizobia in Central India.
Ann Microbiol 64(4):1553–1565
Arasu MV, Esmail GA, Al-Dhabi NA, Ponmurugan K (2016) Managing pests and diseases of grain
legumes with secondary metabolites from actinomycetes. In: Gopalakrishnan S, Sathya A,
Vijayabharathi R (eds) Plant growth promoting actinobacteria. Springer, Singapore, pp 83–98
Arshad M, Frankenberger WT (1998) Plant growth-regulating substances in the rhizosphere:
microbial production and function. Adv Agron 62:45–151
Ashokvardhan T, Rajithasri AB, Prathyusha P, Satyaprasad K (2014) Actinomycetes from Capsi-
cum annuum L. rhizosphere soil have the biocontrol potential against pathogenic fungi. Int J
Curr Microbiol App Sci 3(4):894–903
Barona-Gomez F, Lautru S, Francou FX, Leblond P, Pernodet JL, Challis GL (2006) Multiple
biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomy-
ces coelicolor A3 and (2) Streptomyces ambofaciens ATCC 23877. Microbiology
152:3355–3366
Baskar K, Ignacimuthu S (2012) Bioefficacy of violacein against Asian armyworm
Spodopteralitura Fab. (Lepidoptera: Noctuidae). J Saudi Soc Agric Sci 11:73–77
Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26
Berdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J
Antibiot 65:385–395
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in
agriculture. World J Microbiol Biotechnol 28:1327–1350
Biate DL, Kumar LV, Ramadoss D, Kumari A, Naik S, Reddy KK, Annapurna K (2014) Genetic
diversity of soybean root nodulating bacteria. In: Maheshwari DK (ed) Bacterial diversity in
sustainable agriculture. Springer, Cham, pp 131–145
Bieber B, Nuske J, Ritzau M, Grafe U (1998) Alnumycin a new naphthoquinone antibiotic
produced by an endophytic Streptomyces sp. J Antibiot 51:381–382
Bloem J, de Ruiter P, Bouwman LA (1997) Soil food webs and nutrient cycling in agro-ecosystems.
In: van Elsas JD, Trevors JT, Wellington HME (eds) Modern soil microbiology. Marcel Dekker,
New York, pp 245–278
Boeck VD, Fukuda DS, Abbott BJ, Debono M (1989) Deacylation of echinocandin B by
Actinoplanes utahensis. J Antibiot 42:382–388
Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable
agriculture: a perspective. Plant Soil 141:1–11
Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving
legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 37

Brown ME (1972) Plant growth substances produced by microorganisms of soil and rhizosphere. J
Appl Bacteriol 35:443–451
Burns RG, Dick RP (2002) Enzymes in the environment. Marcel Dekker, New York
Cacciari I, Grappelli A, Lippi D, Pietrosanti W (1980) Effect of growth rate on the production of
phytohormone-like substances by an Arthrobacter sp. in chemostat culture. J Gen Microbiol
118:549–552
Castillo U, Harper JK, Strobel GA, Sears J, Alesi K, Ford E, Lin J, Hunter M, Maranta M, Ge H,
Yaver D, Jensen JB, Porter H, Robison R, Millar D, Hess WM, Condron M, Teplow D (2003)
Kakadumycins, novel antibiotics from Streptomyces sp. NRRL 30566, an endophyte of
Grevillea pteridifolia. FEMS Microbiol Lett 224:183–190
Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of
Streptomyces. FEMS Microbiol Rev 34:171–198
Chistoserdova L, Vorholt JA, Lidstrom ME (2005) A genomic view of methane oxidation by
aerobic bacteria and anaerobic archaea. Genome Biol 6:208
Coronelli C, Pagani H, Bardone MR, Lancini GC (1974) Purpuromycin, a new antibiotic isolated
from Actinoplanes ianthinogenes N. sp. J Antibiot 27:161–168
Coronelli C, White RJ, Lancini GC, Parenti F (1975) Lipiarmycin, a new antibiotic from
Actinoplanes. II. Isolation, chemical, biological and biochemical characterization. J Antibiot
28:253–259
Correll DL (1998) The role of phosphorous in the eutrophication of receiving waters: a review. J
Environ Qual 27:261–266
Crowley DA (2006) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadia J (eds)
Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 169–189
D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010)
Siderophores from neighbouring organisms promote the growth of uncultured bacteria. Chem
Biol 17:254–264
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient
environments. Plant Soil 245:35–47
Dart PJ, Wani SP (1982) Non-symbiotic nitrogen fixation and soil fertility. In: Transactions of the
12th international congress of soil science, 8–16 Feb 1982, New Delhi, India
Dastager SG, Deepa CK, Pandey A (2010) Isolation and characterization of novel plant growth
promoting Micrococcus sp. NII-0909 and its interaction with cowpea. Plant Physiol Biochem
48:987–992
De Meyer G, Capieau K, Audenaert K, Buchala A, Metraux JP, Hofte M (1999) Nanogram amounts
of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the
systemic acquired resistance pathway in bean. Mol Plant Microbe Interact 12:450–458
Deepika TL, Kannabiran K, Gopiesh Khanna V, Rajakumar G, Jayaseelan C, Santhoshkumar T,
Abdul Rahuman A (2011) Isolation and characterization of acaricidal and larvicidal novel
compound (2S,5R,6R)-2-hydroxy-3,5,6-trimethyloctan-4-one from Streptomyces sp. against
blood-sucking parasites. Parasitol Res 111(3):1151–1163
Dey R, Pal KK, Tilak KVBR (2014) Plant growth-promoting rhizobacteria in crop protection and
challenges. In: Goyal A, Manoharachary C (eds) Future challenges in crop protection against
fungal pathogens. Springer, New York, pp 31–58
El-Bendary MA, Rifaat HM, Keera AA (2010) Larvicidal activity of extracellular secondary
metabolites of Streptomyces microflavus against Culex pipiens. Can J Pure App Sci
4:1021–1026
El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis,
with potential for biological control of root rot of lupine caused by Plectosporium tabacinum.
Aust J Bot 51:257–266
El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by
rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing strepto-
mycete actinomycetes. Plant Soil 308:161–174
38 S. P. Wani and S. Gopalakrishnan

El-Tarabily KA, Nassar AH, Hardy GESJ, Sivasithamparam K (2009) Plant growth-promotion and
biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic
actinomycetes. J Appl Microbiol 106:13–26
Engelhardt K, Degnes KF, Kemmler M, Bredholt H, Fjaervik E, Klinkenberg G, Sletta H, Ellingsen
TE, Zotchev SB (2010) Production of a new thiopeptide antibiotic, TP-1161, by a marine
Nocardiopsis species. Appl Environ Microbiol 76:4969–4976
Ezra D, Castillo UF, Strobel GA, Hess WM, Porter H, Jensen JB, Condron MA, Teplow DB,
Sears J, Maranta M, Hunter M, Weber B, Yaver D (2004) Coronamycins, peptide antibiotics
produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera
sp. Microbiology 150:785–793
FAO (2011) The state of the world’s land and water resources for food and agriculture (SOLAW)–
managing systems at risk. Food and Agriculture Organization of the United Nations/Earthscan,
Rome//London
Fred EB, Baldwin IL, McCoy E (1932) Root nodule bacteria and leguminous plants. University of
Wisconsin Press, Madison
Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Chouaia B, Jaouani A, Daffonchio D, Boudabous A,
Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules
of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifca: 15pp.
963401. https://doi.org/10.6064/2012/963401
Glick BR, Todorovic B, Czarny J, Cheng ZY, Duan J, McConkey B (2007) Promotion of plant
growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242
Gopalakrishnan S, Humayun P, Kiran BK, Kannan IGK, Vidhya MS, Deepthi K, Rupela O (2011a)
Evaluation of bacteria isolated from rice rhizosphere for biological control of sorghum caused
by M. phaseolina. World J Microbiol Biotechnol 27(6):1313–1321
Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K,
Rupela O (2011b) Evaluation of actinomycete isolates obtained from herbal vermicompost for
biological control of Fusarium wilt of chickpea. Crop Prot 30:1070–1078
Gopalakrishnan S, Upadhyaya HD, Vadlamudi S, Humayun P, Vidya MS, Alekhya G, Singh A,
Vijayabharathi R, Bhimineni RK, Seema M, Rathore A, Rupela O (2012) Plant growth-
promoting traits of biocontrol potential bacteria isolated from rice rhizosphere. SpringerPlus
1:71
Gopalakrishnan S, Vadlamudi S, Apparla S, Bandikinda P, Vijayabharathi R, Bhimineni RK,
Rupela O (2013) Evaluation of Streptomyces spp. for their plant growth- promotion traits in
rice. Can J Microbiol 59:534–539
Gopalakrishnan S, Srinivas V, Sathya A, Vijayabharathi R, Alekhya G, Vidya MS, Rajyalakshmi K
(2014a) Agriculturally important microbial germplasm database, Information bulletin no:95.
International Crops Research Institute for the Semi-Arid Tropics, Patancheru, pp 1–72
Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Om R, Kudapa H,
Katta K, Varshney RK (2014b) Evaluation of Streptomyces strains isolated from herbal
vermicompost for their plant growth promotion traits in rice. Microbiol Res 169:40–48
Gopalakrishnan S, Srinivas V, Prakash B, Sathya A, Vijayabharathi R (2015) Plant growth-
promoting traits of Pseudomonas geniculata isolated from chickpea nodules. 3 Biotech
5:653–661
Gopalakrishnan S, Vijayabharathi R, Sathya A, Sharma HC, Srinivas V, Bhimineni RK, Gonzalez
SV, Melø TM, Simic N (2016a) Insecticidal activity of a novel fatty acid amide derivative from
Streptomyces species against Helicoverpa armigera. Natl Prod Res 30:2760–2769
Gopalakrishnan S, Sathya A, Vijayabharathi R, Srinivas V (2016b) Formulations of plant growth-
promoting microbes for field applications. In: Singh DP, Singh HB, Prabha R (eds) Microbial
inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 239–251
Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin-Michel JF (1991) Effect of
growth temperature on several exported enzyme activities in the psychrotropic bacterium
Pseudomonas fluorescens. J Bacteriol 173:3814–3820
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 39

Gupta R, Saxena RK, Chaturvedi P, Virdi VS (1995) Chitinase production by Streptomyces

viridificans: its potential in fungal cell wall lysis. J Appl Bacteriol 78:378–383
Guthrie FB (1896) Inoculation of soil for leguminous crops. Agric Gaz NSW7:690–694
Hamdali H, Moursalou K, Tchangbedji G, Ouhdouch Y, Hafidi M (2012) Isolation and characteri-
zation of rock phosphate solubilizing actinobacteria from a Togolese phosphate mine. Afr J
Biotechnol 11:312–320
Hameeda B, Rupela OP, Wani SP, Reddy G (2006) Indices to assess quality, productivity and
sustainable health of soils receiving low cost biological and/or conventional inputs. Int J Soil Sci
1(3):196–206
He H, Ding WD, Bernan VS, Richardson AD, Ireland CM, Greenstein M, Ellestad GA, Carter GT
(2001) Lomaiviticins A and B, potent antitumor antibiotics from Micromonospora
lomaivitiensis. J Am Chem Soc 123:5362–5363
Hoffland E, Pieterse CMJ, Bik L, Van Pelt JA (1995) Induced systemic resistance in radish is not
associated with accumulation of pathogenesis-related proteins. Physiol Mol Plant Pathol
46:309–320
Htwe AZ, Yamakawa T, Sarr PS, Sakata T (2015) Diversity and distribution of soybean-nodulating
bradyrhizobia isolated from major soybean-growing regions in Myanmar. Afr J Microbiol Res
9:2183–2196
IFPRI (2012) Global food policy report. International Food Policy Research Institute, Washington,
DC
Igarashi Y, Takagi K, Kajiura T, Furumai T, Oki T (1998) Glucosylquestiomycin, a novel antibiotic
from Microbispora sp. TP-A0184 fermentation, isolation, structure determination, synthesis and
biological activities. J Antibiot 51:915–920
Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA
barcoding. Mol Ecol Notes 7:544–548
Jiao YS, Liu YH, Yan H, Wang ET, Tian CF, Chen WX, Guo BL, Chen WF (2015) Rhizobial
diversity and nodulation characteristics of the extremely promiscuous legume Sophora
flavescens. Mol Plant-Microbe Interact 28(12):1338–1352
Jo LL, Ensio OJ, Carol MD, Carol MD, Rito JD, Ann BN, Gail MP (2003) Streptomyces galbus
strain with insecticidal activity and method of using as an insecticide. European patent
EP1272611
Jog R, Nareshkumar G, Rajkumar S (2012) Plant growth-promoting potential and soil enzyme
production of the most abundant Streptomyces spp. from wheat rhizosphere. J Appl Microbiol
113:1154–1164
Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilisation and
antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their
application in improving plant growth. Microbiology 160:778–788
Johnson LJ, Koulman A, Christensen M, Lane GA, Fraser K, Forester N, Johnson RD, Bryan GT,
Rasmussen S (2013) An extracellular siderophore is required to maintain the mutualistic
interaction of Epichloë festucae with Lolium perenne. PLoS Pathog 9(5):e1003332
Joo GJ (2005) Purification and characterization of an extracellular chitinase from the antifungal
biocontrol agent Streptomyces halstedii. Biotechnol Lett 27:1483–1486
Joshi MV, Loria R (2007) Streptomyces turgidiscabies possesses a functional cytokinin biosyn-
thetic pathway and produces leafy galls. Mol Plant Microbe Interact 20:751–758
Kandeler E, Stemmer M, Gerzabek MH (2005) Role of microorganisms in carbon cycling in soils.
In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer,
Berlin/Heidelberg, pp 139–157
Karthik L, Gaurav K, BhaskaraRao KV, Rajakumar G, Abdul Rahuman A (2011) Larvicidal,
repellent, and ovicidal activity of marine actinobacteria extracts against Culex tritaeniorhynchus
and Culex gelidus. Parasitol Res 108:1447–1455
Katznelson H, Cole SE (1965) Production of gibberellin like substances by bacteria and
actinomycetes. Can J Microbiol 11:733–741
40 S. P. Wani and S. Gopalakrishnan

Kaunat H (1969) Bidung von indolderivatendurchrhizosphareenspezifisch Bakterien und

Aktinomyzeten. Zentralblatt fuer Bakeriologie Abteilung II 123:501–515
Kawamura N, Sawa R, Takahashi Y, Issiki K, Sawa T, Kinoshita N, Naganawa H, Hamada M,
Takeuchi T (1995) Pyralomicins, new antibiotics from Actinomadura spiralis. J Antibiot
48:435–437
Khamna S, Yokota A, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Strepto-
myces sp. isolated from some Thai medicinal plant rhizosphere soils. Eur Asia J Bio Sci 4:23–32
Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In:
Proceedings of the 4th international conference on plant pathogenic bacteria, vol 2. Station de
Pathologie Vegetale et de Phytobacteriologie, INRA, Angers, France, pp 879–882
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores
produced by plant growth-promoting rhizobacteria. Nature 286:885–886
Kondo S, Yasui K, Katayama M, Marumo S, Kondo T, Hattori H (1987) Structure of pamamycin-
607, an aerial mycelium-inducing substance of Streptomyces alboniger. Tetrahedron Lett
28:5861–5864
Lam YKT, Williams DL, Sigmund JM, Sanchez M, Genilloud O, Kong YL, Stevens-Miles S,
Huang L, Garrity GM (1992) Cochinmicins, novel and potent cyclodepsipeptide endothelin
antagonists from a Microbispora sp. I. Production, isolation, and characterization. J Antibiot
45:1709–1716
Lewer P, Chapin EL, Graupner PR, Gilbert JR, Peacock C (2003) Tartrolone C: a novel insecticidal
macrodiolide produced by Streptomyces sp. CP1130. J Nat Prod 66:143–145
Lewer P, Hahn DR, Karr LL, Duebelbeis DO, Gilbert JR, Crouse GD, Worden T, Sparks TC,
Edwards PMR, Graupne PR (2009) Discovery of the butenyl-spinosyn insecticides: novel
macrolides from the new bacterial strain Saccharopolyspora pogona. Bioorg Med Chem
17:4185–4196
Li W, Leet JE, Ax HA, Gustavson DR, Brown DM, Turner L, Brown K, Clark J, Yang H, Fung-
Tomc J, Lam KS (2003) Nocathiacins, new thiazolyl peptide antibiotics from Nocardia
sp. I. Taxonomy, fermentation and biological activities. J Antibiot 56:226–231
Lin L, Xu X (2013) Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated
from medicinal plants. Curr Microbiol 67:209–217
Lindström K, Lipsanen P, Kaijalainen S (1990) Stability of markers used for identification of two
Rhizobium galegae inoculant strains after five years in the field. Appl Environ Microbiol
56:444–450
Liu H, Qin S, Wang Y, Li W, Zhang J (2008) Insecticidal action of Quinomycin A from
Streptomyces sp. KN-0647, isolated from a forest soil. World J Microbiol Biotechnol
24:2243–2248
Loliam B, Morinaga T, Chaiyanan S (2013) Biocontrol of Pythium aphanidermatum by the
cellulolytic actinomycetes Streptomyces rubrolavendulae S4. Sci Asia 39:584–590
Macagnan D, Romeiro RS, Pomella AWV, deSouza JT (2008) Production of lytic enzymes and
siderophores, and inhibition of germination of basidiospores of Moniliophthora (ex Crinipellis)
perniciosa by phylloplane actinomycetes. Biol Control 47:309–314
Madhaiyan M, Poonguzhali S, Lee JS, Lee KC, Saravanan VS, Santhanakrishnan P (2010a)
Microbacterium azadirachtae sp. nov., a plant growth-promoting actinobacterium isolated
from the rhizoplane of neem seedlings. Int J Syst Evol Microbiol 60:1687–1692
Madhaiyan M, Poonguzhali S, Lee JS, Senthilkumar M, Lee KC, Sundaram S (2010b) Leifsonia
soli sp. nov., a yellow-pigmented actinobacterium isolated from teak rhizosphere soil. Int J Syst
Evol Microbiol 60:1322–1327
Mahadevan B, Crawford DL (1997) Properties of the chitinase of the antifungal biocontrol agent
Streptomyces lydicus WYEC108. Enzym Microb Technol 20:489–493
Maheshwari DK (2012) Bacteria in agrobiology: plant probiotics. Springer
Maskey RP, Li FC, Qin S, Fiebig HH, Laatsch H (2003) Chandrananimycins AC: production of
novel anticancer antibiotics from a marine Actinomadura sp. isolate M048 by variation of
medium composition and growth conditions. J Antibiot 56:622–629
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 41

McGrath JW, Hammerschmidt F, Quinn JP (1998) Biodegradation of phosphonomycin by Rhizo-

bium huakuii PMY1. Appl Environ Microbiol 64:356–358
Merckx R, Dijkra A, Hartog AD, Veen JAV (1987) Production of root-derived material and
associated microbial growth in soil at different nutrient levels. Biol Fertil Soils 5:126–132
Mishra AC, Pandey VK, Rai VP (2014) Effectiveness of fertilizer doses, liming and Rhizobium
inoculation in vegetable pea under acidic soil of Jharkhand. Asian J Hortic 9:140–142
Nakamura G, Kobayashi K, Sakurai T, Sono K (1981) Cationomycin, a new polyether ionophore
antibiotic produced by Actinomadura nov. sp. J Antibiot 34:1513–1514
Nambiar PT, Rego TJ, Rao BS (1986) Comparison of the requirements and utilization of nitrogen
by genotypes of sorghum (Sorghum bicolor (L.) Moench), and nodulating and non-nodulating
groundnut (Arachis hypogaea L.). Field Crops Res 15(2):165–179
Nascimento FX, Rossi MJ, Soares CR, McConkey BJ, Glick BR (2014) New insights into
1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological
significance. PLoS One 6:e99168
Nigam SN, Dwivedi SL, Nambiar PTC, Gibbons RW, Dart PJ (1985) Combining ability analysis of
N2-fixation and related traits in peanut. Peanut Sci 12:55–57
Ohtake H, Wu H, Imazu K, Ambe Y, Kato J, Kuroda A (1996) Bacterial phosphonate degradation,
phosphite oxidation and polyphosphate accumulation. Resour Conserv Recycl 18:125–134
Omura S, Imamura N, Oiwa R, Kuga H, Iwata R, Masuma R, Iwai Y (1986) Clostomicins, new
antibiotics produced by Micromonospora echinospora subsp. armeniaca subsp. nov. I Produc-
tion, isolation, and physico-chemical and biological properties. J Antibiot 39:1407–1412
Onaka H, Tabata H, Igarashi Y, Sato Y, Furumai T (2001) Goadsporin, a chemical substance which
promotes secondary metabolism and morphogenesis in Streptomycetes. I. Purification and
characterization. J Antibiot 54:1036–1044
Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease
suppression and growth-promotion. Appl Microbiol Biotechnol 97:9621–9636
Parenti F, Beretta G, Berti M, Arioli V (1978) Teichomycins, new antibiotics from Actinoplanes
eichomyceticus Nov. Sp. I. Description of the producer strain, fermentation studies and
biological properties. J Antibiot 1:276–283
Patel M, Horan AC, Gullo VP, Loebenberg D, Marquez JA, Miller GH, Waitz JA (1984)
Oxanthromicin, a novel antibiotic from Actinomadura. J Antibiot 37:413–415
Patil CD, Patil SV, Salunke BK, Salunkhe RB (2011) Prodigiosin produced by Serratia marcescens
NMCC46 as a mosquito larvicidal agent against Aedesaegypti and Anopheles stephensi.
Parasitol Res 109:1179–1187
Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martınez-Molina E, Velazquez E
(2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of
Mesorhizobium mediterraneum under growth. Soil Biol Biochem 33:103–110
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic romiscuity. Microbiol
Mol Biol Rev 64:180–201
Pertry I, Vaclavikova K, Depuydt S, Galuszka P, Spichal L, Temmerman W, Vereecke D (2009)
Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the
plant. PNAS 106:929–934
Podile AP, Kishore GK (2006) Plant growth-promoting rhizobacteria. In: Gnanamanickam SS
(ed) Plant-associated bacteria. Springer, Dordrecht, pp 195–230
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for
improving heavy metal phytoextraction. Trends Biotechnol 28:142–149
Reeve W, Ardley J, Tian R, Eshragi L, Yoon JW, Ngamwisetkun P, Seshadri R, Ivanova NN,
Kyrpides NC (2015) A genomic encyclopedia of the root nodule bacteria: assessing genetic
diversity through a systematic biogeographic survey. Stand Genomic Sci 10:14
Reimann H, Cooper DJ, Mallams AK, Jaret RS, Yehaskel A, Kugelman M, Vernay HF,
Schumacher D (1974) Structure of sisomicin, a novel unsaturated aminocyclitol antibiotic
from Micromonospora inyoensis. J Org Chem 39:1451–1457
42 S. P. Wani and S. Gopalakrishnan

Ruanpanun P, Laatsch H, Tangchitsomkid N, Lumyong S (2011) Nematicidal activity of fervenulin

isolated from a nematicidal actinomycete, Streptomyces sp. CMU-MH021, on Meloidogyne
incognita. World J Microbiol Biotechnol 27:1373–1380
Rupela OP (1992) Natural occurrence and salient characters of non-nodulating chickpea plants.
Crop Sci 32:349–352
Rupela OP (1997) Nitrogen fixation research through cooperation and future research needs. In:
Extending nitrogen fixation research to farmers’ fields: proceedings of an International Work-
shop on Managing Legume Nitrogen Fixation in the Cropping Systems of Asia, 20–24 Aug
1996, pp 9–14
Rupela OP, Johansen C (1995) Identification of non-nodulating and low and high nodulating plants
in pigeonpea. Soil Biol Biochem 27:539–544
Rupela OP, Toomsan B, Mittal S, Dart PJ, Thompson JA (1987) Chickpea Rhizobium populations:
survey of influence of season, soil depth and cropping pattern. Soil Biol Biochem 19:247–252
Rupela OP, Rao JVDK, Sudarshana MR, Kiran MU, Anjaiah V (1991) Rhizobium germplasm
resources at ICRISAT Center. Research bulletin no.15
Rupela OP, Wani SP, Danso SKA, Johansen C (1995) Effect of high nodulating selection of
chickpea cultivar ICC 4948 on yield and soil properties of a chickpea-sorghum cropping system.
J Soil Biol Ecol 15:127–134
Rupela OP, Rangarao GV, Rahman SJ, Wani SP, Gowda CLL (2005) Promoting biopesticides for
crop protection though partnerships–an on-going drive. Presented at the Workshop on “Promo-
tion of biopesticides and biofertilizers in agriculture”, 20–22 Sep 2005, Hyderabad, India
Sanginga N, Danso SKA, Mulongoy K, Ojeifo AA (1994) Persistence and recovery of introduced
Rhizobium 10 years after inoculation on Leucaena leucocephala grown on an Alfisol in
Southwestern Nigeria. Plant Soil 159:199–204
Sang-Mo K, Abdul Latif K, Young-Hyun Y, Muhammad K (2014) Gibberellin production by
newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J Microbiol
Biotechnol 24:106–112
Sathya A, Vijayabharathi R, Kumari BR, Srinivas V, Sharma HC, Sathyadevi P, Gopalakrishnan S
(2016a) Assessment of a diketopiperazine, cyclo(Trp-Phe) from Streptomyces griseoplanus
SAI-25 against cotton bollworm, Helicoverpa armigera. App Entomol Zool 51:11–20
Sathya A, Vijayabharathi R, Gopalakrishnan S (2016b) Soil microbes: the invisible managers of
soil fertility. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable
agricultural productivity. Springer, New Delhi, pp 1–16
Saurav K, Rajakumar G, Kannabiran K, Abdul Rahuman A, Velayutham K, Elango G, Kamaraj C,
AbduzZahir A (2011) Larvicidal activity of isolated compound 5-(2,4-dimethylbenzyl)
pyrrolidin-2-one from marine Streptomyces VITSVK5 sp. against Rhipicephalus (Boophilus)
microplus, Anopheles stephensi, and Culex tritaeniorhynchus. Parasitol Res 112(1):215–226
Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M,
Breusegem FV, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in
tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ
29:909–918
Sellstedt A, Richau KH (2013) Aspects of nitrogen-fixing actinobacteria, in particular free-living
and symbiotic Frankia. FEMS Microbiol Lett 342:179–186
Shekhar N, Bhattacharya D, Kumar D, Gupta RK (2006) Biocontrol of wood-rotting fungi with
Streptomyces violaceusniger XL2. Can J Microbiol 52:805–808
Shih HD, Liu YC, Hsu FL, Mulabagal V, Dodda R, Huang JW (2003) Fungichromin: a substance
from Streptomyces padanus with inhibitory effects on Rhizoctonia solani. J Agric Food Chem
51:95–99
Shockman G, Waksman SA (1951) Rhodomycin-an antibiotic produced by a red-pigmented mutant
of Streptomyces griseus. Antibiot Chemother 1:68–75
Simon J (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS
Microbiol Rev 26:285–309
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 43

Singh RP, Manchanda G, Singh RN, Srivastava AK, Dubey RC (2016) Selection of alkalotolerant
and symbiotically efficient chickpea nodulating rhizobia from North-West Indo Gangetic Plains.
J Basic Microbiol 56(1):14–25
Skrary FA, Cameron DC (1998) Purification and characterization of a Bacillus licheniformis
phosphatase specific for D-alphaglycerphosphate. Arch Biochem Biophys 349:27–35
Smyth E (2011) Selection and analysis of bacteria on the basis of their ability to promote plant
development and growth. PhD thesis, University College Dublin, Ireland
Somma S, Gastaldo L, Corti A (1984) Teicoplanin, a new antibiotic from Actinoplanes
teichomyceticus nov. sp. Antimicrob Agents Chemother 26:917–923
Sontag B, Gerlitz M, Paululat T, Rasser HF, Grun-Wollny I, Hansske FG (2006) Oxachelin, a novel
iron chelator and antifungal agent from Streptomyces sp. GW9/1258. J Antibiot 59:659–663
Stevens G, Berry AM (1988) Cytokinin secretion by Frankia sp. HFP ArI3 in defined medium.
Plant Physiol 87:15–16
Subramanian P, Kim K, Krishnamoorthy R, Sundaram S, Sa T (2014) Endophytic bacteria improve
nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium
japonicum MN110. Plant Growth Regul 76:327–332
Sun Y, Zhou X, Liu J, Bao K, Zhang G, Tu G, Kieser T, Deng Z (2002) Streptomyces
nanchangensis, a producer of the insecticidal polyether antibiotic nanchangmycin and the
antiparasitic macrolide meilingmycin, contains multiple polyketide gene clusters. Microbiology
148:361–371
Sun CH, Wang Y, Wang Z, Zhou JQ, Jin WZ, You HG, Zhao LX, Si SY, Li X (2007) Chemomicin
A: a new angucyclinone antibiotic produced by Nocardia mediterranei subsp. kanglensis
1747–64. J Antibiot 60:211–215
Swarnalakshmi K, Senthilkumar M, Ramakrishnan B (2016) Endophytic actinobacteria: nitrogen
fixation, phytohormone production, and antibiosis. In: Gopalakrishnan S, Sathya A,
Vijayabharathi R (eds) Plant growth promoting actinobacteria. Springer, Singapore, pp 123–145
Thamdrup B (2012) New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol
Syst 43:407–428
Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK, Nautiyal CS, Mittal S, Tripathi AK
(2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136–150
Tokala RK, Janice LS, Carina MJ, Don LC, Michelle HS, Lee AD, Bailey JF, Morra MJ (2002)
Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the
pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Trejo-Estrada SR, Sepulveda I, Crawford DL (1998) In vitro and in vivo antagonism of Streptomy-
ces violaceusnigerYCED9 against fungal pathogens of turfgrass. World J Microbiol Biotechnol
14:865–872
Trumbore S (2006) Carbon respired by terrestrial ecosystems – recent progress and challenges.
Glob Chang Biol 12:141–153
Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant
growth-stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126
Uchida R, Imasato R, Yamaguchi Y, Masuma R, Shiomi K, Tomoda H, Omura S (2005) New
insecticidal antibiotics, hydroxyfungerins A and B, produced by Metarhizium sp. FKI-1079. J
Antibiot 58:4–9
Unno Y, Shinano T, Minamisawa K, Ikeda S (2015) Bacterial community shifts associated with
high abundance of Rhizobium spp. in potato roots under macronutrient-deficient conditions. Soil
Biol Biochem 80:232–236
Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizo-
sphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere:
biochemistry and organic substances at the soil–plant interface. CRC Press, Boca Raton, pp
1–22
Vaccari DA, Strom PF, Alleman JE (2006) Environmental biology for engineers and scientists.
Wiley, New York, pp 1–931
44 S. P. Wani and S. Gopalakrishnan

Valanarasu M, Kannan P, Ezhilvendan S, Ganesan G, Ignacimuthu S, Agastian P (2010) Antifungal

and antifeedant activities of extracellular product of Streptomyces sp. ERI-04 isolated from
Western Ghats of Tamil Nadu. J Mycol Med 20:290–297
Vance CP, Ehde-Stone C, Allan DL (2003) Phosphorous acquisition and use: critical adaptations by
plants for screening a renewable resource. New Phytol 157:423–447
Verhagen BWM, Glazebrook J, Zhu T, Chang H-S, Van Loon LC, Pieterse CMJ (2004) The
transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe
Interact 17:895–908
Verma VC, Singh SK, Prakash S (2011) Bio-control and plant growth-promotion potential of
siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. J Basic
Microbiol 51:550–556
Vertesy L, Ehlers E, Kogler H, Kurz M, Meiwes J, Seibert G, Vogel M, Hammann P (2000)
Friulimicins: novel lipopeptide antibiotics with peptidoglycan synthesis inhibiting activity from
Actinoplanes friuliensis sp. nov. II. Isolation and structural characterization. J Antibiot
53:816–827
Vessey JK (2003) Plant growth-promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Vijayabharathi R, RatnaKumari B, Sathya A, Srinivas V, Rathore A, Sharma HC, Gopalakrishnan S
(2014a) Biological activity of entomopathogenic actinomycetes against lepidopteran insects
(Noctuidae: Lepidoptera). Can J Plant Sci 94(4):759–769
Vijayabharathi R, Kumari BR, Gopalakrishnan S (2014b) Microbial agents against Helicoverpa
armigera: where are we and where do we need to go? Afri J Biotech 13:1835–1844
Vijayabharathi R, Sathya A, Gopalakrishnan S (2016) A renaissance in plant growth-promoting and
biocontrol agents by Endophytes. In: Microbial Inoculants in sustainable agricultural productiv-
ity: research perspectives. Springer India, India, pp 37–60
Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance:
challenges for the future. J Exp Bot 64:1263–1280
Wan M, Li G, Zhang J, Jiang D, Huang HC (2008) Effect of volatile substances of Streptomyces
platensis F-1 on control of plant fungal diseases. Biol Control 46:552–559
Wang XY, Zhang J, Liu CX, Gong DL, Zhang H, Wang JD, Yan YJ, Xiang WS (2011a) A novel
macrocyclic lactone with insecticidal bioactivity from Streptomyces microflavus neau 3. Bioorg
Med Chem Lett 21:5145–5148
Wang XY, Zhang J, Wang JD, Huang SX, Chen YH, Liu CX, Xiang WS (2011b) Four new
doramectin congeners with acaricidal and insecticidal activity from Streptomyces avermitilis
NEAU1069. Chem Biodivers 8:2117–2125
Wani SP (1986) Research on cereal nitrogen fixation at ICRISAT. In: Cereal nitrogen fixation. In:
Proceedings of the working group meeting, 9–12 Oct 1984, ICRISAT Center, Patancheru, India
Wani SP, Rego TJ, Kumar Rao JVDK (1994) Contribution of legumes in cropping systems: along-
term perspective. In: Linking biological nitrogen fixation research in Asia: report of a meeting of
the Asia working group on biological nitrogen fixation in legumes, 6–8 Dec 1993, pp 84–90
Wani SP, Rupela OP, Lee KK (1995) Sustainable agriculture in the semi-arid tropics through
biological nitrogen fixation in grain legumes. Plant Soil 174:29–49
Weinstein MJ, Luedemann GM, Oden EM, Wagman GH (1964) Everninomicin, a new antibiotic
complex from Micromonospora carbonacea. Antimicrob Agents Chemother 10:24–32
Wheeler CT, Crozier A, Sandberg G (1984) The biosynthesis of indole-3-acetic acid by Frankia.
Plant Soil 78:99–104
Wilson PW, Burris RH (1947) The mechanism of biological nitrogen fixation. Bacteriol Rev 11
(1):41–73
Xiao-ming PX, Bi-run L, Mei-ying HU, Hui-fang S (2008) Insecticidal constituent of Streptomyces
sp. 4138 and the bioactivity against Spodoptera exigua. Chinese J Biological Control. doi:
CNKI:SUN:ZSWF.0.2008-02-014
Xiong L, Li J, Kong F (2004) Streptomyces sp. 173, an insecticidal micro-organism from marine.
Lett Appl Microbiol 38:32–37
2 Plant Growth-Promoting Microbes for Sustainable Agriculture 45

Yamanaka K, Oikawa H, Ogawa HO, Hosono K, Shinmachi F, Takano H, Sakuda S, Beppu T,

Ueda K (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and
development of Streptomyces tanashiensis. Microbiology 151:2899–2905
Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Strepto-
myces vinaceusdrappus S5MW2 isolated from Chilika lake, India enhances plant growth and
biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J
Microbiol Biotechnol 31(8):1217–1225
Zhi-qin JI, Ji-wen Z, Shao-peng W, Wen-jun W (2007) Isolation and identification of the insecti-
cidal ingredients from the fermentation broth of Streptomyces qinlingensis. Nongyaoxue
Xuebao 9(1):25–28