Agriculture, Ecosystems and Environment 140 (2011) 339353
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environmentjournal homepage:
www.elsevier.com/locate/agee
Review
Efcient soil microorganisms: A new dimension for sustainable
agriculture and environmental developmentJay Shankar Singh , Vimal
Chandra Pandey, D.P. SinghDepartment of Environmental Science,
Babasaheb Bhimrao Ambedkar (Central) University, Raibarelly Road,
Lucknow 226025, Uttar Pradesh, India
a r t i c l e
i n f o
a b s t r a c tSustainable agriculture is vital in todays world
as it offers the potential to meet our agricultural needs,
something that conventional agriculture fails to do. This type of
agriculture uses a special farming technique wherein the
environmental resources can be fully utilized and at the same time
ensuring that no harm was done to it. Thus the technique is
environment friendly and ensures safe and healthy agricultural
products. Microbial populations are instrumental to fundamental
processes that drive stability and productivity of agro-ecosystems.
Several investigations addressed at improving understanding of the
diversity, dynamics and importance of soil microbial communities
and their benecial and cooperative roles in agricultural
productivity. However, in this review we describe only the
contributions of plant growth promoting rhizobacteria (PGPR) and
cyanobacteria in safe and sustainable agriculture development. 2011
Elsevier B.V. All rights reserved.
Article history: Received 30 August 2010 Received in revised
form 20 January 2011 Accepted 21 January 2011 Available online 12
February 2011 Keywords: Agriculture Biofertilizers Biocontrol
Cyanobacteria Rhizobacteria
Contents 1. 2. 3. 4. 5. 6. 7. 8. Introduction . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . The efcient
and potential soil microbes . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . Why sustainable agriculture
is so important? . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . The contributions of soil micro-ora in
sustainable agricultural production . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . Microbial management of
soil fertility for sustainable agriculture . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. Benets of better management of the soil microbiota? . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . Efcient soil microbes for
sustainable agriculture and environment . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Plant
growth promoting rhizobacteria and agricultural productivity . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . 8.1. PGPR as biological fertilizers . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . 8.2. PGPR in saline agricultural soils . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3.
1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing
PGPR protect plants from the environmental stresses . . . . . . . .
. . . 8.4. PGPR as biocontrol agents . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
8.5. PGPR as biological fungicides . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.
Contribution of cyanobacteria to agriculture and environmental
sustainability . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . 9.1. Cyanobacteria in stability and productivity of
desert soils . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . 9.2. Reclamation of
saline wastelands by cyanobateria . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . 9.3. Cyanobacteria as potential biocontrol agents . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . 9.4. Soil heavy
metal bioremediation by cyanobacteria . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . 10. Role of rhizospheric microbial interactions in
environment and agriculture sustainability . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . 11. Conclusions . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . References . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 340 340
340 340 341 341 341 341 342 342 343 343 344 344 345 346 346 347 347
349 350 350
Corresponding author. Tel.: +91 522 2998718; fax: +91 522
2441888. E-mail address: jayshankar [email protected] (J.S. Singh).
0167-8809/$ see front matter 2011 Elsevier B.V. All rights
reserved. doi:10.1016/j.agee.2011.01.017
340
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
1. Introduction According to United Nations estimates, the
global human population is projected to reach 8.9 billion by 2050,
with the developing countries of Asia and Africa to absorb the vast
majority of the increase (Wood, 2001). Decreasing irrigational
water supplies and other environmental concerns exacerbate the
challenges we face to meet the nutritional requirements of the
growing population. The various ways in which microorganisms have
been used over the past 50 years to advance medical technology,
human and animal health, food processing, food safety and quality,
genetic engineering, environmental protection, agricultural
biotechnology, and in more effective treatment of agricultural and
municipal wastes collectively the most impressive record. Many of
these technological advances would not have been possible using
straight forward chemical and physical engineering methods, or if
they were, they would not have been practically or economically
viable. Nevertheless, while microbial technologies have been
applied to various agricultural and environmental problems with
considerable success in recent years, they have not been widely
accepted by the scientic community as it is often hard to
consistently reproduce their benecial effects. Microorganisms are
effective only when they are provided with suitable and optimum
conditions for metabolism including the available water, oxygen, pH
and temperature of the ambient environment. The types of microbial
cultures and inoculants available in the market today have
increased rapidly owing to new technologies. Significant
achievements are being made in systems where technical guidance is
coordinated with the marketing of microbial products. Since
microorganisms are useful in overcoming problems associated with
the use of chemical fertilizers and pesticides, are now widely
applied in agriculture. Environmental pollution, by excessive soil
erosion and the associated transport of sediment, chemical
fertilizers and pesticides to surface waters and groundwater, and
ineffective treatment of human and animal wastes poses serious
environmental and social problems throughout the world. Although
engineers attempted to solve such problems using established
chemical and physical methods found that it cannot be done without
deploying microbial methods and technologies. For many years, soil
microbiologists and microbial ecologists differentiated soil
microorganisms as benecial or harmful depending how they affect
soil quality, crop growth and yield. Benecial microorganisms are
those that x atmospheric N, decompose organic wastes and residues,
detoxify pesticides, suppress plant diseases and soil-borne
pathogens, enhance nutrient cycling and produce bioactive compounds
such as vitamins, hormones and enzymes that stimulate plant growth.
The recent interest in eco-friendly and sustainable agricultural
practices (Kavino et al., 2007; Saravanakumar and Samiyappan, 2007;
Harish et al., 2009a,b). Biofertilizer and biopesticide containing
efcient microorganisms, improve plant growth in many ways compared
to synthetic fertilizers, insecticides and pesticides by way of
enhancing crop growth and thus help in sustainability of
environment and crop productivity. The rhizospheric soils contain
diverse type of efcient microbes with benecial effects on crop
productivity. The plant growth promoting rhizobacteria (PGPR) and
cyanobacteria are rhizospheric microbes and produce bioactive
substances to promote plant growth and/or protect them against
pathogens (Glick, 1995; Harish et al., 2009a). This communication
highlighted contributions of PGPR, cyanobacteria and some benecial
microbial interactions in the agriculture improvement and
environment sustainability.
2. The efcient and potential soil microbes Such microorganisms
may comprise of mixed populations of naturally occurring microbes
that can be applied as inoculants to increase soil microbial
diversity. Investigations have shown that the inoculation of
efcient microbial community to the soil ecosystem improves soil
quality, soil health, growth, yield and quality of crops. These
microbial populations may consists of selected species of
microorganisms including plant growth promoting rhizobacteria, N2
-xing cyanobacteria, plant disease suppressive bacteria and fungi,
soil toxicant degrading microbes, actinomycetes and other useful
microbes. Efcient and potential soil microbial biota is only
suitable for sustainable agriculture practices and may not the so
for other alternatives. It is an added dimension to optimizing our
soil and crop management practices such as crop rotation, organic
amendments, conservation tillage, crop residue recycling, soil
fertility restoration, maintenance of soil quality and the
biocontrol of plant diseases. If used adequately, microbial
communities can signicantly benet the agriculture practices. 3. Why
sustainable agriculture is so important? Sustainable agriculture is
a broadbased concept rather than a specic methodology. It
encompasses advances in agricultural management practices and
technology, and the growing recognition indicates that the
conventional agriculture that developed post World War-II, will not
be able to meet the needs of the growing population in the 21st
Century. Conventional agriculture is facing either reduced
production or increased costs, or both. Farming monocultures, such
as wheat elds, repeated on the same land results in the depletion
of topsoil, soil vitality, groundwater purity and benecial microbe,
insect life, making the crop plants vulnerable to parasites and
pathogens. An everincreasing amount of fertilizers and pesticides
as well as the energy requirements for tilling to aerate soils and
increasing irrigation costs are of prime concern. While
conventional methods enabled large increases in crop yields, thus
high prots only initially, have failed to be considered as the
ideal approach for future. The steady increase in corporate farming
based conventional methods in the last few decades, primarily prot
driven, has increased the destabilization of rural communities as
well as speeded up the detrimental effects on both the farmland
ecology and neighboring natural environments. Cost cutting efforts
have frequently targeted farm workers; nancial recompense for the
work performed, has degraded signicantly compared to other areas of
human endeavor. This not only decreases their own standard of
living but has a ow on effect impacting the economic viability of
small, rural towns. The expansion of urban population and business
and industrial complexes has reduced the available farmland. The
location of much of the worlds primary and best quality farmland is
in areas that are steadily becoming prime real estate for top end
residential assets. In economic terms, farming simply cannot
compete. The prots from transforming the farmland into residential
subdivisions are astronomically higher than those achievable from
farming it by any method. 4. The contributions of soil micro-ora in
sustainable agricultural production A fundamental shift is taking
place worldwide in agricultural practices and food production. In
the past, the principal driving force was to increase the yield
potential of food crops and their productivity. Today, the drive
for productivity is increasingly combined
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
341
with the desire and even the demand for sustainability.
Sustainable agriculture involves successful management of
agricultural resources to satisfy human needs while maintaining
environmental quality and conserving natural resources for future.
Improvement in agricultural sustainability requires the optimal use
and management of soil fertility and its physico-chemical
properties. Both rely on soil biological process and soil
biodiversity. This implies management practices that enhance soil
biological activity and thereby buildup long term soil productivity
and crop health. Such practices are of major concern in marginal
lands to avoid degradation and in restoration of degraded lands and
in regions where high external input agriculture is not feasible.
5. Microbial management of soil fertility for sustainable
agriculture The central paradigm for the biological management of
soil fertility is to utilize farmers management practices to
inuence soil microbial populations and processes in such a way as
to achieve benecial effects on soil productivity. Microbial
populations and processes inuence soil fertility and structure in a
variety of ways, each of which has an ameliorating effect on the
main soil-based constraints to productivity: Symbionts such as PGPR
and cyanobacteria, etc. increase the efciency of nutrient
acquisition by plants. A wide range of microbial community
participates in decomposition, mineralization, and nutrient
availability (microbe-mediated unusable P-availability), and
therefore inuence the efciency of nutrient cycles. Soil microbial
communities mediate both the synthesis and decomposition of soil
organic matter and therefore, inuence cation exchange capacity, the
soil N, S, P reserve, soil acidity and toxicity and soil water
holding capacity. The burrowing and particle transport activities
of soil microora, and the aggregation of soil particles by fungi
and bacteria, inuence soil structure and soil water regime. 6.
Benets of better management of the soil microbiota? Agriculture
provides a major share of national income and export earnings in
many developing countries, while ensuring food security, income and
employment to a huge proportion of the population. Farmers are
increasingly comlaint that declining soil fertility is the major
problem. As a result, controlling erosion and improving the
management of soil fertility, are now major issues on the
development policy agenda. Soil microorganisms contribute a wide
range of essential services to the sustainability of all
ecosystems, by acting as the primary driving agents of nutrient
cycling, regulating the dynamics of soil organic matter, soil
carbon sequestration and greenhouse gas emission, modifying soil
physical structure and water regimes, enhancing the efciency of
nutrient acquisition by the vegetation and enhancing plant health.
These services are not only essential to the functioning of natural
ecosystems but constitute an important resource for the sustainable
management of agricultural and environmental ecosystems. Direct and
indirect benets of adopting microbiological management of soil for
sustainable agriculture production are: Economic benets (reduced
input costs by enhancing resource use efciency especially
decomposition, nutrient cycling, N2 xation, bioavailability of P,
water storage and movement). Environmental protection (prevention
of pollution and land degradation especially through reducing use
of agro-chemicals and maintains soil structure and cation exchange
capacity).
Food security (improve yield and crop quality especially through
controlling pests and diseases and enhancing plant growth).
Restoration and reclamation of wastelands (microbe mediated
remediation and rehabilititation of non-fertile waste area into
fertile lands). 7. Efcient soil microbes for sustainable
agriculture and environment Agriculture, in a broad sense, is the
activity in which the farmer attempts to integrate certain
agro-ecological factors and production inputs for optimum crop and
livestock production. Thus, it is reasonable to assume that farmers
should be interested in ways and means of controlling useful soil
microorganisms as the important components of the agricultural
environment. Nevertheless, this idea has often been rejected by
naturalists and proponents of nature farming and organic
agriculture. The argument is that useful soil microorganisms will
increase naturally with organic amendments to such soils as carbon,
energy and nutrient sources. This indeed may be true where there is
the abundance of organic materials for recycling only is in small
scale farming. However, in most cases, soil microorganisms,
benecial or harmful, have often been controlled advantageously when
crops in various agroecological zones are grown and cultivated as
crop rotations and without pesticides use. This explains why
scientists have long been interested in the use of potential and
efcient microorganisms as soil and plant inoculants to shift the
microbiological equilibrium in ways that would enhance soil quality
and the eco-friendly agriculture crops. Low agricultural production
efciency is closely related to a poor coordination of energy
conversion which, in turn, is inuenced by crop physiological
factors, the environment, and other biological factors including
soil microbes. The soil and rhizosphere microora can accelerate the
growth of plants and enhance their resistance to pathogens and
harmful insects by producing bioactive metabolites. Such
microorganisms maintain growth of plants, and thus have primary
effects on both soil and crop quality. A wide range of benets are
possible depending on their predominance and activity at any one
time. However, there is a growing consensus that it is feasible to
obtain maximum economic agronomic yield of high quality at higher
net returns, without the use of articial fertilizers, herbicides,
insecticides and pesticides. Until recently, this was not thought
to be the very likely possibility using conventional agricultural
practices. However, it is important to recognize that the best soil
and agricultural management practices to attain a more sustainable
and green agriculture will also enhance the growth, number and
activities of efcient soil microora that, in turn, can enhance the
growth, yield and agriculture quality. In particular, healthy
living soil with improved quality is the very foundation of a
future sustainable agriculture. 8. Plant growth promoting
rhizobacteria and agricultural productivity In the broadest sense,
plant growth promoting rhizobacteria include the N2 -xing
rhizobacteria that colonize the rhizosphere, providing N to plants
in addition to the well characterized legume rhizobia symbioses.
Regardless of the mechanism(s) of plant growth promotion, PGPR must
colonize the rhizosphere around the roots, the rhizoplane (root
surface) or the root itself (within root tissue). PGPR can affect
plant growth either indirectly or directly; indirect promotion of
plant growth in affected when PGPR lessen or antagonize the
deleterious effects of one or more phytopathogens; while direct
route by PGPR involves either providing plants with the compounds
synthesized by the bacterium or facilitating the uptake of certain
nutrients from the environment (Glick, 1995). PGPR reg-
342
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
Table 1 Plant growth promoting rhizobacteria (PGPR) regulating
various growth parameters/yields of crop/fruit plants. PGPR
Rhizobium leguminosarum Pseudomonas putida G 122 Azospirillum
brasilense and A. irakense strains P. uorescens strain P. putida
strain Azotobacter and Azospirillum strains P. alcaligenes PsA15,
Bacillus polymyxa BcP26, and Mycobacterium phlei MbP18,
Pseudomonas, Azotobacter and Azospirillum strains R. leguminismarum
(Thal-8/SK8) and Pseudomonas sp. strain 54RB P. putida strains
R-168 and DSM-291; P. uorescens strains R-98 and DSM-50090; A.
brasilense DSM-1691 and A. lipoferum DSM-1690 P. putida strain
R-168, P. uorescens strain R-93, P. uorescens DSM 50090, P. putida
DSM291, A. lipoferum DSM 1691, A. brasilense DSM 1690 P. uorescens
strains, CHA0 and Pf1 Crop parameters Direct growth promotion of
canola and lettuce Early developments of canola seedlings Growth of
wheat and maize plants Growth of pearl millet Growth stimulation of
tomato plant Growth and productivity of canola Enhance uptake of N,
P and K by maize crop in nutrient decient calcisol soil Stimulates
growth and yield of chick pea (Cicer arietinum) Improve the yield
and phosphorus uptake in wheat Improves seed germination, seedling
growth and yield of maize References Noel et al. (1996) Glick et
al. (1997) Dobbelaere et al. (2002) Niranjan et al. (2003) Gravel
et al. (2007) Yasari and Patwardhan (2007) Egamberdiyeva (2007)
Rokhzadi et al. (2008) Afzal and Asghari (2008) Nezarat and Gholami
(2009)
Seed germination, growth parameters of maize seedling in
greenhouse and also grain yield of eld grown maize
Gholami et al. (2009)
Increase growth, leaf nutrient contents and yield of banana
cv.Virupakshi (Musa spp. AAB) plants
Kavino et al. (2010)
ulation of various growth parameters/yields of crop/fruit plants
has been listed in Table 1. Among the diverse bacteria identied as
PGPR, the Bacilli and Pseudomonads are the predominant ones (Podile
and Kishore, 2007). PGPR exert a direct effect on plant growth by
production of phytohormones, solubilization of inorganic
phosphates, increased iron nutrition through iron-chelating
siderophores and the volatile compounds that affect the plant
signaling pathways. Additionally, by antibiosis, competition for
space and nutrients and induction of systemic resistance in plants
against a broad-spectrum of root and foliar pathogens, PGPR reduce
the populations of root pathogens and other deleterious
microorganisms in the rhizosphere, thus beneting the plant
growth.
8.1. PGPR as biological fertilizers A group of biofertilizers
comparising benecial rhozobacteria identied as PGPR, are strains
from genera of Pseudomonas, Azospirillum, Azotobacter, Bacillus,
Burkholdaria, Enterobacter, Rhizobium, Erwinia and Flavobacterium
(Rodriguez and Fraga, 1999). Free-living PGPR have shown promise as
biofertilizers (Podile and Kishore, 2007). Many studies and surveys
reported plant growth promotion, increased yield, uptake of N and
some other elements through PGPR inoculations (Sheng and He, 2006;
Glick et al., 2007). In addition, treatments with PGPR enhance root
growth, leading to a root system with large surface area and
increased number of root hairs (Mantelin and Touraine, 2004). In
general, huge bulk articial fertilizes is applied to replenish soil
N and P with the resultant in high cost and environmental risk.
Most of P in insoluble compounds are unavailable to plants. N2
-xing and P-solubilizing bacteria (PSB) are important for crop
plants as they increase N and P uptake and play a crucial role as
PGPR in the biofertilization (Zahir et al., 2004; Zaidi and
Mohammad, 2006).Thus, the application of such microbes as
environment friendly biofertilizer may contribute to minimize the
use of expensive phosphatic fertilizers. Phosphorus biofertilizers
increase the availability of accumulated P (by solubilization),
efciency of biological N2 -xation and the availability of Fe, Zn,
etc., due to generation of plant growth promoting substances (Kucey
et al., 1989). Inoculation of N2 xing and PSB in combination was
more effective than the single microbe in providing a more balanced
nutrition to agriculture crops such as sorghum, barley, black gram,
soybean and wheat (Alagawadi and Gaur, 1992; Belimov
et al., 1995; Abdalla and Omer, 2001; Tanwar et al., 2002;
Galal, 2003). Reports on co-inoculation of Rhizobium and PSB on
wheat are rare and especially in India, very little work has been
done on such lines. Therefore, extensive investigations to explore
the effect of single and dual inoculations of N2 -xing and
P-solubilizing bacterial species on yields of various crops are
required urgently. More recent ndings indicated that the treatment
of arable soils with PGPR inoculations signicantly increases
agronomic yields (Harish et al., 2009a,b; Yazdani et al., 2009).
The PGPR strains Pseudomonas alcaligenes PsA15, Bacillus polymyxa
BcP26 and Mycobacterium phlei MbP18 had the pronounced stimulatory
effects on plant growth and uptake of N, P and K by maize in
nutrient-decient calcisol soils (Egamberdiyeva, 2007). The
enhancement in various agronomic yields by PGPR was because of the
production of growth promoting phytohormones, phosphate
mobilization, production of siderophore and antibiotics, inhibition
of plant ethylene synthesis and induction of plant systemic
resistances to pathogens (Han et al., 2004; Zahir et al., 2004;
Ramazan et al., 2005; Wua et al., 2005; Zaidi and Mohammad, 2006,
Turan et al., 2006; Kohler et al., 2006). Very recently, Kavino et
al. (2010) reported that P. uorescens strain, CHA0 in combination
with chitin increased growth, leaf nutrient contents and yield of
banana plants under perennial cropping systems thus suggesting that
in view of the environmental problems, due to excessive use and
high production costs of fertilizers, PGPR may represent the
potential soil microora to be deployed for sustainable and
eco-friendly agriculture.
8.2. PGPR in saline agricultural soils Soil salinity constitutes
a serious problem for vegetable as well as other crops as
salinisation suppresses plant growth, particularly in arid and
semiarid areas (Parida and Das, 2005). An alteration in physiology
of plants facing salt stress adversely affects nutritional uptake
and also crop growth. More specically, the soil-borne pseudomonads
have received paramount attention because of their catabolic
versatility, efcient root-colonising ability and capacity to
produce a wide range of enzymes and metabolites that help the plant
withstand varied biotic and abiotic stresses (Vessey, 2003). PGPR
facilitate plant growth indirectly by reducing plant pathogens, or
directly by facilitating the nutrient uptake through phytohormone
production (e.g. auxin, cytokinin and gibberellins), by enzymatic
lowering of plant ethylene levels and/or by produc-
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
343
tion of siderophores (Kohler et al., 2006). It has been
demonstrated that inoculations with AM fungi improves plant growth
under salt stress (Cho et al., 2006). Kohler et al. (2006)
demonstrated the benecial effect of PGPR Pseudomonas mendocina
strains on stabilization of soil aggregate. The three PGPR isolates
Pseudomonas alcaligenes PsA15, Bacillus polymyxa BcP26 and
Mycobacterium phlei MbP18 were able to tolerate high temperatures
and salt concentrations and thus confer on them potential
competitive advantage to survive in arid and saline soils such as
calcisol (Egamberdiyeva, 2007). Kohler et al. (2009) investigated
the inuence of inoculation with a PGPR, Pseudomonas mendocina,
alone or in combination with an AM fungus, Glomus intraradices or
Glomus mosseae on growth and nutrient uptake and other
physiological activities of Lactuca sativa affected by salt stress.
Salinity decreased lettuce growth regardless of the biological
treatments and of the salt stress level. The plants inoculated with
P. mendocina had signicantly greater shoot biomass than the
controls and it is suggested that inoculation with selected PGPR
could better effective tool for alleviating salinity stress in salt
sensitive plants. The costs associated with amelioration of soil
salinity are potentially enormous but salinity comes heavily on
agriculture, biodiversity and also the environment. The
contributions of PGPR to plant health and their osmotolerance
mechanisms are vital. As the saline areas under agriculture have
been on the rise every year across the globe, it is of serious
concern (Paul and Nair, 2008). It could be ascertained that the
osmotolerance mechanisms of MSP393 viz. de novo synthesis of
osmolytes and overproduction of salt-stress proteins effectively
nullied the detrimental effects of high osmolarity. Pseudomonas
uorescens MSP-393 could serve as the ideal bioinoculant for crops
in saline soils (Paul and Nair, 2008). Investigations on
interaction of PGPR with other microbes and their effect on the
physiological response of crop plants under different soil salinity
regimes are still in incipient stage. Inoculations with selected
PGPR and other microbes particularly, AM fungi could serve as the
potential tool for alleviating salinity stress in salt sensitive
crops. Therefore, extensive investigations is needed in this area,
and the use of PGPR and other symbiotic microorganisms, especially
AM fungi, can be useful in developing strategies to facilitate
sustainable agriculture in saline soils. 8.3.
1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing
PGPR protect plants from the environmental stresses Relatively
recently, it was discovered that many plant growth promoting
bacteria (PGPB) contain the enzyme 1Aminocyclopropane-1-carboxylic
acid (ACC) deaminase that cleave the ethylene precursor ACC to
-ketobutyrate and ammonia and thereby lower the ethylene levels in
developing or stressed plants (Saleem et al., 2007). Bacterial
strains containing ACC deaminase can, in part, at least alleviate
the stress induced ethylene mediated negative impact on plants.
Such an aspect is extensively studied in numerous PGPBs like
Agrobacterium genomovars and Azospirillum lipoferum, Alcaligenes
and Bacillus, Burkholderia, Enterobacter, Methylobacterium
fujisawaense, Pseudomonas Ralstonia solanacearum, Rhizobium,
Rhodococcus, and Sinorhizobium meliloti and Variovorax paradoxus
(Penrose and Glick, 2001; Belimov et al., 2001, 2005; Ma et al.,
2003; Hontzeas et al., 2004a; Uchiumi et al., 2004; Pandey et al.,
2005a,b; Blaha et al., 2006; Stiens et al., 2006). The ACC
deaminase metabolizes the roots ACC into -ketobutyrate and ammonia
and checks the production of ethylene which otherwise inhibits
plant growth through several mechanisms. The plants treated with
bacteria containing ACC-deaminase may have relatively extensive
root growth due to lowered ethylene levels (Shaharoona et al.,
2006) thus leading to resistance aginst various stresses (Safronova
et al., 2006).
ACC deaminase containing PGPBs when bound to the seed coat or
root of a developing seedlings, act as a sink for ACC, ensuring
that plant ethylene levels do not get elevated to a point that
impairs root growth (Jacobson et al., 1994; Glick, 1995; Glick et
al., 1998, 1999). In addition, by lowering ethylene levels, ACC
deaminase containing PGPBs protect plants from the deleterious
effects of numerous environmental stresses, including ooding
(Grichko and Glick, 2001), metals (Burd et al., 2000; Nie et al.,
2002), drought (Mayak et al., 2004a) and salts (Mayak et al.,
2004b). The importance of ACC deaminase in the bacterium
Enterobacter cloacae UW4 regarding plant growth promotion, has been
demonstrated (Li et al., 2000). Hontzeas et al. (2004b) reported
that ACC deaminase containing PGPB Enterobacter cloacae UW4 induces
root elongation and proliferations in canola (Brassica rapa)
largely by lowering ethylene levels. While it is clear that ACC
deaminase containing PGPR promote growth of a variety of plants
under various environmental stresses, the precise nature of the
changes in plant gene expression by the bacterium, remains to be
elucidated. Utilization of PGPR containing ACC deaminase activity
in promoting plant growth and development both under stress and
normal conditions and genetic manipulation of cultivars with genes
expressing this enzyme, has attracted attentions of many (Sergeeva
et al., 2006). Therefore, further developments in this area are
extremely important possibly via various biotechnological
approaches for agriculture sustainability. 8.4. PGPR as biocontrol
agents The PGPR is a group of rhizosphere colonizing bacteria that
produces substances to increase the growth of plants and/or protect
them against diseases (Harish et al., 2009a). PGPR may protect
plants against pathogens by direct antagonistic interactions with
the pathogen, as well as through induction of host resistance. PGPR
that indirectly enhance plant growth via suppression of
phytopathogens do so by a variety of mechanisms. These include, the
ability to produce siderophores to chelate iron, making it
unavailable to pathogens, to synthesize anti-fungal metabolites
such as antibiotics, fungal cell wall lysing enzymes, or hydrogen
cyanide that suppress the growth of fungal pathogens, to
successfully compete with pathogens for nutrients or specic niches
on the root and to induce systemic resistance (Glick et al., 1995;
Bloemberg and Lugtenberg, 2001; Persello Cartieaux et al., 2003).
The PGPR as biocontrol agents against various plant diseases has
been presented Table 2. The ability of PGPRs as biocontrol agents
against various plant diseases has been listed in Table 3. Among
the various PGPRs identied, Pseudomonas uorescens is one of the
most extensively studied rhizobacteria, because of its antagonistic
actions against several plant pathogens (Kavino et al., 2007;
Saravanakumar and Samiyappan, 2007; Harish et al., 2009a). The
biocontrol depends on a wide variety of traits, such as the
production by the biocontrol strain of various antibiotic
compounds, iron chelators and exoenzymes such as proteases,
lipases, chitinases, and glucanases as well as the competitive root
colonization (ChinAWoeng et al., 2000; Lugtenberg et al., 2001).
The biocontrol efcacy and PGPR uorescent pseudomonads is further
increased by mixing two or more strains of Pseudomonas spp. (Singh
et al., 1999; Saravanakumar et al., 2009) or mixing with chitin or
other substances (Radjacommare et al., 2002). Pseudomonas uorescens
MSP-393 has been proved as biocontrol agent for many of the crops
grown in saline agricultural soils (Paul and Nair, 2008). Banana
bunchy top virus (BBTV) is one of the deadly viruses that severely
affect the yield of banana (Musa spp.) crop in Western Ghats, Tamil
Nadu, India (Kavino et al., 2010). Kavino et al. (2008)
demonstrated that application of P. uorescens strain CHA0 + chitin
bio-formulations, signicantly reduced the BBTV incidence in hill
banana varity under greenhouse and eld conditions. Chitinases
344
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
Table 2 Plant growth promoting rhizobacteria (PGPR) as
biocontrol agents against various plant diseases. PGPR Bacillus
pumilus strain SE34, Kluyvera cryocrescens strain IN114, B.
amyloliquefaciens strain IN937a, and B. subtilus strain IN937b. B.
amyloliquefaciens 937a, B. subtilis 937b, and B. pumilus SE34 B.
pumilus strain INR7 Pseudomonas uorescens based bio-formulation
Experimental sites Greenhouse experiment Disease Cucumber Mosaic
Cucumovirus (CMV) of tomato (Lycopersicon esculentum) Tomato mottle
virus Bacterial wilt disease in cucumber (Cucumis sativus) Sheath
blight disease and leaf folder insect in rice (Oryza sativa) Blue
mold disease of tobacco (Nicotiana) Downy mildew in pearl millet
(Pennisetum glaucum) CMV in cucumber Foliar diseases of tomato
Blight of bell pepper (Capsicum annuum) Saline resistance in
groundnut (Arachis hypogea) Maize (Zea mays) rot Soil borne
pathogen of cucumber and pepper (Piper) Signicantly reduce the
Banana Bunchy Top Virus (BBTV) incidence Rice blast Rice Sheath rot
(Sarocladium oryzae) Blight of squash References Zehnder et al.
(2000)
Field condition Field study Rice eld
Murphy et al. (2000) Zehnder et al. (2001) Radjacommare et al.
(2002)
B. pumilus strain SE34 B. subtilis strain GBO3, B. pumilus
strain INR7 and B. pumilus strain T4 B. subtilis strain IN937a B.
cereus strains B101R, B212R, and A068R Bacillus strains BB11 and
FH17 Pseudomonas uorescens Burkholderia strains MBf21 and MBf15 B.
subtilis ME488 P. uorescens strain CHA0 + chitin
bio-formulations
Laboratory condition Greenhouse and eld conditions Greenhouse
bioassays Greenhouse experiment Saline eld condition In vitro and
In vivo Banana under greenhouse and eld conditions Greenhouse study
Rice eld Greenhouse condition
Zhang et al. (2002) Niranjan et al. (2003) Jetiyanon et al.
(2003) Silva et al. (2004) Jiang et al. (2006) Saravanakumar and
Samiyappan (2007) Hernandez Rodriguez et al., 2008 (2008) Chung et
al. (2008) Kavino et al. (2008)
Bacillus sp., and Azospirillum strains SPS2, WBPS1 and Z27
Fluorescent Pseudomonas spp. Bacillus strain
Naureen Zakira et al. (2009) Saravanakumar et al. (2009) Zhang
et al. (2010)
induced by PGPR play an important role in PGPR-mediated insect
management by hydrolyzing chitin as this constitutes a structural
component of the gut linings of insects (Harish et al., 2009b).
Chitinases also degrade fungal cell walls and cause cell lysis
(Radjacommare et al., 2004). 8.5. PGPR as biological fungicides
PGPR and bacterial endophytes play a vital role in the management
of various fungal diseases. But one of the major hurdles
experienced with biocontrol agents is the lack of appropriate
delivery system. Mathiyazhagan et al. (2004) reported that Bacillus
subtilis (BSCBE4), Pseudomonas chlororaphis (PA23), endophytic P.
uorescens (ENPF1) inhibited the growth of stem blight pathogen
Corynespora casiicola. According to them, the combined application
of BSCBE4 and ENPF1 through seedling dip and foliar spray offered
maximum control of stem blight both in vitro and in vivo.
Similarly, seed treatment and soil application of P. uorescens
reduced root rot of black gram by Macrophomina phaseolina
(Jayashree et al., 2000; Shanmugam et al., 2001) and panama wilt of
banana (Raguchander et al., 1997). Seed and foliar application of
P. uoTable 3 Changes in physico-chemical characteristics of saline
soil due to application of cyanobacterial inoculum (Nostoc
calcicola). Physico-chemical soil properties pH Organic-C (%)
Total-N (%) Total-P (%) C/N ratio Na+ (ppm) Uninoculated
cyanobacterial growth condition 10.40 0.12 0.02 0.03 6.00 0.78
Inoculated cyanobacterial growth condition 5.08.80 0.590.66
0.170.18 0.030.3 3.284.00 0.60
rescens reduced sheath blight of rice (Nandakumar et al., 2001).
Manjula and Podile (2001) demonstrated that the formulations of
plant growth promoting B. subtilis AF 1 in peat supplemented with
chitin or chitin-containing materials had better control of
Aspergillus niger and Fusarium udum than AF 1 alone in groundnut
and pigeon pea, respectively. Strains of Burkholderia cepacia have
been shown to have biocontrol characteristics against Fusarium spp.
(Bevivino et al., 1998).
9. Contribution of cyanobacteria to agriculture and
environmental sustainability Due to evolutionary antiquity of
cyanobacteria, they are widely adapted to survive against various
extreme environments such as drought, salinity, low to high
temperatures, etc. During phylogeny, cyanobacteria have been
exposed to a variety of stresses, the main being water and salt
stress. Cyanobacteria are traditionally best adapted to drought and
desiccation probably through the presence of modied vegetative
cells (spores or akinetes) that are resistant to desiccation.
Cyanobacteria represent a continually renewable biomass source that
releases to the environment soluble organic substances as
extracellular products also known as secondary metabolites, which
can be mineralized by the microora and are thus benecial to
agricultural crops. These substances may be the growth promoters
and/or inhibitors for other organisms, including soil microora
(Zulpa et al., 2003). Reports available about cyanobacteria as
biocontrol agents show that these organisms are effective against
plant pathogens (Yuen et al., 1994). However, observations on the
effects of cyanobacteria and their metabolites on other plant
pathogens under eld conditions are scarce. Cyanobacteria occurring
in chronically contaminated environments (with salts, heavy metals,
pesticides and other potential toxicants) have tendency to take up
and accumulate the toxicants
Modied from Pandey et al. (2005a,b).
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
345
intracellularly. The pollutant level in cyanobacterial cells can
even be used as the pollution indicator. Since cyanobacteria are
the principal primary producers of diverse type of ecosystems,
tolerance of such organisms to diverse extreme environments
(salinity, drought, contaminated soils, etc.) is relevant from an
ecological view point. However, little is known about the
mechanisms permitting cyanobacterial adaptations to such extreme
conditions. More investigation is needed to make sound predictions
about the role of such microbes in restoration of wastelands for
sustainable agriculture development. Use of successful indigenous
strains of cyanobacteria as the potential biofertilizer not only
improves the physico-chemical and biological properties of the soil
but also helps in promoting yield of various agricultural crops
such as rice, wheat and pearl millet under saline, drought and
contaminated agroecosystems. Regular application of cyanobacterial
strains adapted to various extreme environments seems promising for
wasteland management and improvement of soil stability, nutrient
status, soil microbial activities, nutrient mineralization and crop
growth in ecologically sustainable manner. Cyanobacterial
biofertilizers mobilize nutritionally important elements such as P
from a non-usable to a usable form through biological processes
(Hegde et al., 1999). Cyanobacteria play an important role in
various chemical transformations of soils and thus, inuence the
bioavailability of major nutrients like P to plants. Cyanobacteria
and PSB have been used as biofertilizer to increase crop production
(Singh et al., 1997; Earanna and Govindan, 2002). In recent years,
biofertilizers have emerged as promising components of the
integrated nutrient supply system in Indian agriculture. The
cyanobacterial ability to mobilize insoluble forms of inorganicP is
evident from the nding of Kleiner and Harper (1977) who reported
more extractable P in soils with cyanobacterial cover than in
nearby soils without cover. Synergistic effects of efcient soil
microbes and cyanobacteria, the excretion of organic acids to
increase P availability and the decrease of sulphide injury by
increased O2 content has also been reported (Ordog, 1999). The
success of biotechnology tools mainly depends upon how much it
costs and how simple it can be during operation and utilization.
One of the biotechnological applications resulting from the
development of a cyanobacterial biofertilizer technology is the
production and distribution of cyanobacterial biofertilizers to
farmers. Plastic bottles, polyethylene and polypropylene sachets
have been used for distribution of liquid cyanobacterial cultures
instead of the expensive glass containers (Suresh et al., 1992).
The basic advantage of this technology is that after obtaining the
soil based starter cyanobacterial culture, farmers can generate the
biofertilizer on their own with least extra additional inputs.
Unfortunately, the outdoor cyanobacterial production technique is
not so popular among the farming community. Cyanobacterial
biofertilizer utilization is also limited due to lack of basic
knowledge regarding the factors involved in the success and failure
of establishment of inoculated cyanobacterial species. Detail eld
investigations regarding development of efcient high quality
cyanobacterial soil inocula and their application in specic regions
such as saline and drought-proven regions are also needed. This
biofertilizer technique is still limited in use and therefore, it
is important to introduce cyanobacterial application under eld
conditions for sustainable agriculture. 9.1. Cyanobacteria in
stability and productivity of desert soils Dryland soils in desert
and semi-arid regions suffer from major constraints like poor
physical properties, low fertility and water deciency (Nisha et
al., 2007). Organic matter content of dryland soils is chemically
and biologically less stable, and tends to decrease very rapidly in
arid regions thus leading to poor organic matter contents. Poor
soil structure usually associated with low organic
carbon, compaction, salinity and sodicity results in reduced
aeration and rates of water inltration, hence more soil
erodability, and the reduced number and biodiversity of micro-ora
ultimately has the adverse impact on plant growth and productivity.
Cyanobacterial application to the organically poor semi-arid soil
played a signicant role in improving the status of carbon, nitrogen
and other nutrients in the soil (Nisha et al., 2007). High
organic-C in treated soils might be attributed to autotrophic
nature of the cyanobacteria, which synthesize and add organic
matter to soil. Diazotrophic cyanobacteria which are
photoautotrophic and N2 -xing improve crop production by acting as
natural biofertilizers through increase in both C and N status of
soils. Biogenic soil crusts comprising mainly cyanobacteria seem to
increase soil fertility by incorporating organic matter in soil
(Belnap et al., 2001). In recent years, there are several studies
to show that cyanobacterial crusts play a signicant role in arid
and semi-arid ecosystems through C and N inputs along with several
micronutrients to improve hydrology and soil stability (Orlovsky et
al., 2004). Cyanobacterial inoculations in disturbed soils have
been reported to restore the population of carbon and nitrogen
cycle microorganisms (Acea et al., 2003). Several studies reported
that cyanobacteria produce extracellular polymeric substances (EPS)
that help them to overcome conditions of water stress and also bind
soil particles (Mazor et al., 1996). Cyanobacterial sheaths and EPS
also play a major role in water retention due to their hygroscopic
nature (Decho, 1990). Thus the soil microora contributes to
increased water holding capacity of soils (Verrecchia et al.,
1995). It has also been reported that cyanobacteria, as carbon and
nitrogen xers, can contribute to the improvement of soil nutrient
status in arid soils (Jeffries et al., 1992; Lange et al., 1994).
Flaibani et al. (1989) reported that exopolysaccharides from
cyanobacteria also contribute to reclaimation and improvement of
desert soils.Cyanobacteria seem to exert a mechanical effect on
soil particles by the supercial network of the trichomes/laments as
well as enmeshing with soil particles at depth (Nisha et al.,
2007). Some native cyanobacterial strains have been reported to
play an important role in improving soil aggregation, water holding
capacity and soil aeration in paddy and several other agriculture
elds (Rogers and Burns, 1994; DeCaire et al., 1997; Hegde et al.,
1999). A number of studies demonstrated that cyanobacteria play a
very crucial role in bioamelioration of soils and enhancing crop
yield not only aggregation initiation but also through protection
of soil porosity due to reduction of the damaging effect of water
addition (Marathe, 1972; Falchini et al., 1996). The diazotrophic
cyanobacteria contribute substantially to the fertility of the soil
especially under tropical paddy eld conditions. However, most of
these studies have been carried out on paddy, and there is scanty
information regarding the possible role of bioameliorant
cyanobacteria in relation to other crops in semi-arid areas where
paddy cannot be grown due to constraints of water availability. The
native strains of cyanobacteria in semi-arid soils showed
remarkable potential for improving structural stability, nutrient
status and productivity of the soil due to their inherent tolerance
capacity under limited soil moisture condition (Manchanda and
Kaushik, 2000; Nisha et al., 2007). Cyanocover produced organic
matter, which increased soil organic C as well as water-stable soil
aggregates (MalamIssa et al., 2001). Better soil aggregation in
cyanobacterial bio-fertilizer treated soils may be attributed to
polysaccharides produced by the blue green algae (Ahmed et al.,
2000). Increase in total sugar content in soils having a
cyanobacterial mat has been found to correspond to the enhanced
soil aggregation process. The cyanobacterial consortium used as
biofertilizer also produces abundant EPS about 25% of their total
biomass (Nisha et al., 2007). Algal biomass and activity in soil
crust are concentrated in the upper soil layers and EPS have gluing
effect on soil particles leading to accelerates soil
aggregation.
346
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
EPS produced by the cyanobacteria also seem to promote the
activity of soil microora as indicated by high soil enzymatic
activities. Such microbial ora, in turn, may produce more EPS, thus
further amplifying the effect. Cyanobacteria thus play a very
important role in xing C and N in soil, and have been considered
very important for desert ecosystem. Removal of cyanobacteria from
the arid sites reduces productivity and increases erosion by
exposing unprotected subsurface soils to wind and water (Belnap and
Gillette, 1997). Several workers reported that formation of algal
crust by Microcoleus vaginatus and M. chthonoplastes in extremely
dry climates, make signicant contributions in stability of soils
(Campbell, 1979; Belnap and Harper, 1995). The above observations
indicate that the application of drought resistant indigenous
strains of cyanobacterial biofertilizers at a relatively higher
dose as mentioned in most of the experiments not only improves the
physico-chemical and biological properties of the soil but also
helps in promoting crop yield under drought and water-limited
agriculture. Applications of such cyanobacterial members are
predicted to be very crucial for enhancing soil quality, soil
nutrient status, soil microora, nutrient mineralization and crop
growth in desert and semi-arid soils in the ecologically
sustainable manner. The understanding of the biology of drought
resistant cyanobacteria may be useful in sustainable agricultural
and particularity in drought crops. It is evident from the above
points that indigenous strains of cyanobacteria from semi-arid
environment could be effective under a stress soil moisture-stress
regime. The remarkable tolerance of cyanobacterial strains to
osmotic stress can makes them successful in agriculture of arid and
semi-arid soils where scarcity of water is imminent. Further, the
cyanobacterial strains, adapted to high osmotic stress conditions
can be the suitable strategy to enhance crop productivity and
reclamation of such wastelands for sustainable agriculture. 9.2.
Reclamation of saline wastelands by cyanobateria Soil salinization
is predicted to result in 30% loss of fertile agriculture lands
globally within the next 25 years, and up to 50% by the year 2050.
The water-logged situation for long periods leads to soil
salinization. In countries like China and India, the situation can
be worst given to the increasing demand for rice as a staple food
by the indiscriminate increasing population. Diverse cyanobacterial
members are assumed of special signicance in saline soils habitats.
Due to the morphological and genomic diversity cyanobacteria are
adapted to survive in saline environments. The remediation and
rehabilitation of saline soils what are also extensively
distributed in India, is urgently required in order to convert
these huge wastelands to fertile lands. Physico-chemical methods
such as pyrite and sulfur or excessive irrigation usually
applicable in the reclamation of alkaline soils, are not so
effective in the removal of soluble salts and exchangeable Na+ from
the soil system (Pandey et al., 2005a,b). Cyanobacteria can be used
to rehabilitate and reclaim the saline soils as they form a thick
stratum on the soil surface during the favourable months of rainy
and winter seasons (Pandey et al., 2005a,b; Srivastava et al.,
2009). The metabolite synthesized by cyanobacteria when
incorporated in the soil, may help to conserve organic C, organic
N, and organic P as well as moisture, and convert Na+ clay
complexes to Ca2+ clay complexes and enhance soil properties (Singh
and Singh, 1989; Venkataraman, 1993; Vaishampayan et al., 2001).
Organic matter and N added by cyanobacteria may bind the soil
particles, and thus improve soil permeability, aeration and
fertility. Application of mixed cyanobacterial inocula to saline
soils showed a signicant decrease in pH while the increase in total
soil N, P and organic-C (Table 3). The organic metabolites produced
by cyanobacteria and their release in the soil systems can be
mineralized. Some degraded metabolites can accumulate and enhance
the soil organic-N content, and may
consequently maintain the soil fertility and stability year
after year (Kaushik and Misra, 1989; Ladha and Reddy, 1995).Whitton
and Potts (2000) demonstrated that extracellular substances
produced by cyanobacteria improve the physico-chemical structures
of saline soils. The efciency of cyanobacteria in increasing crop
yields may also depends on the soil type. Several eld experiments
conducted on different types of soils showed that cyanobacteria
supplemented with 2535% urea N were more effective for rice crop in
acid, saline and red soils, than in calcareous and neutral soils
(Rogers and Burns, 1994). Cyanobacteria play a major role in
improving soil environment in addition to N2 -xation with their
capacity to reclaim soil salinity thus leading to improves organic
matter content and water holding capacity of soils and also reduced
soil erosion. Nitrogen (N) is the macronutrient required in high
amounts by plants, and its availability in soils may change
substantially at relatively short time intervals (Cameron and
Haynes, 1986). For rapid growth of all plants, nitrogen is probably
the most common limiting factor in saline soils. Hence, an adequate
supply of N in saline agriculture eld is also very important. The
long-term eld experiments showed that the use of only chemical
fertilizers cannot be an efcient option to maintain and enrich the
fertility of such problematic soils. However, some reports
indicated that use of pyrite with cyanobacteria can be the very
effective corrective measures in reclamation and enrichment of
saline soils (Singh et al., 2010). Diazotrophic cyanobacteria are
the dominant microora in rice agriculture, and are presently used
as a supplement to chemical N fertilizers for rice cultivation in
rice-growing countries, including India. This technology suffers
from serious drawback as its use at the farm level, is not gaining
universal acceptance due to some major problems. In order to
signicantly improve the efcient use of cyanobacteria as an N-based
biofertilizer for rice cultivation, studies have been carried out
in different dimensions both in the laboratory and in the eld
(Hashem, 2001a). Cyanobacterial strains were isolated, identied and
quantied from a wide range of distinctively different types of
soils, viz. acid, calcareous, saline, red and neutral soils. The
strains isolated were tested for their N2 -xing capacity and growth
under various stress conditions prevailing in the rice eld, e.g.
pH, combined N, pesticides, salinity and nutrient availability in
order to select suitable strains to be used as biofertilizer. The
eld trials showed that cyanobacterial biofertilizers may reclaim
acidic and saline soils, improve the fertility status and may
supplement 2535% N for use in rice cultivation in these soils.
These biofertilizers may be thus recommended for enriching the soil
productivity of nutrient poor saline soils (Hashem, 2001b).
Further, the role of cyanobacteria as biofertilizers in sustainable
agriculture recorded special signicance, particularly in the
present context of high cost of chemical fertilizers (Kannaiyan,
2002). Based on the above information, it may be deduced that the
application of biofertilizers like cyanobacteria can be a potential
agent to provide essential nutrient and organic matter to saline
soils. Although the fundamental investigations related to the
affect of salinity stress and the effect of different metals on
growth and photosynthesis in cyanobacteria and eld related studies
on nitrogen xation in rice agriculture are well documented (Apte et
al., 1987; Nayak et al., 2004), their application as remediating
agents, is very scare. Thus there exists an urgent need to develop
the efcient and potential alkalophilic and saline tolerant
cyanobacterial strains that can be applied as technology for
reclamation and restoration for huge unused saline waste-lands
usable for sustainable agriculture purposes. 9.3. Cyanobacteria as
potential biocontrol agents Information about the cyanobacteria as
biocontrol agents is mostly based on observations in the
laboratory, and very few
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353 Table 4 Strains of cyanobacterium Nostoc muscorum
exhibiting the antagonistic effects. Cyanobacteria Nostoc muscorum
strain N. muscorum strain N. muscorum strain 79a Plant disease
Damping off Wood blue stain White mold of lettuce (Lactuca sativa)
Pathogenic microorganisms Rhizotocnia solanii Pathogenic fungi
Sclerotinia sclerotiorum References
347
DeCaire et al. (1990) Zulpa et al. (2003) Tassara et al.
(2008)
demonstrations have been conducted under eld condition. In
modern agriculture practices, the conventional control methods of
plant diseases have not been found quite efcient due to survival of
the reproductive structures of pathogens in the soil. At the same
time, fungicides and other articial chemical agents inhibit the
growth and development of crop plants (Nyporko et al., 2002).
However, two contact fungicides, iprodione and vinclozolin, have
been reported with effective and successful results (Westerdijk,
2000). Various antagonistic microorganisms have been identied for
almost every life cycle stage of several plant pathogenic microbes,
and cyanobacteria it is here that are as the efcient antagonistic
agents against several pathogenic microbes (Yuen et al., 1994).
Several researches suggest that some members of cyanobacteria could
also be used as bio-control agents against plant pathogens to
obtain higher yield and good health of crop plants in agriculture
(Zulpa et al., 2003; Biondi et al., 2004; Tassara et al., 2008).
Some strains of cyanobacteria (Nostoc muscorum) showing the
antagonistic affects against plant pathogens have been presented in
Table 4. Among cyanobacteria N. muscorum has been shown to exert
antifungal activity on soil fungi (Rhizotocnia solanii), and
especially those producing damping off (DeCaire et al., 1990). N.
muscorum also inhibits the growth of other pathogenic fungi causing
the disease wood blue stain (Zulpa et al., 2003). DeMule et al.
(1991) demonstrated that methanol extracts and extracellular
products from another axenic strain of N. muscorum inhibited growth
of Sclerotinia sclerotiorum. Tassara et al. (2008) demonstrated
that the bioactive compounds synthesized by N. muscorum are the
useful biological control agent for lettuce white mold caused by S.
sclerotiorum and this treatment can be used for other crops having
similar infection pattern. Nostoc ATCC 53789, a known cryptophycin
producer, is a source of natural pesticides against the fungi such
as S. sclerotiorum, insects, nematodes with cytotoxic effects
(Biondi et al., 2004). Cyanobacteria have been reported as the
potential source of biologically active secondary metabolites with
cytotoxic, antifungal, antibacterial or antiviral activities
(Teuscher et al., 1992). However, the investigations about the use
of these microbes as potent biocontrol agents and their role in
control of several plant diseases for sustainable agriculture in
eld conditions are still awaited in detail. 9.4. Soil heavy metal
bioremediation by cyanobacteria Several chemicals are released into
the soil ecosystem either as a method of disposal or as a
consequence of the technology of their utilization. In particular,
the application of pesticides, many of which are toxic or contain
toxic contaminants, is central to the high yields in modern
agriculture. With the advances in biotechnology, bioremediation has
become one of the major developing research area of environmental
restoration, utilizing microorganisms to reduce the
concentration/toxicity of various chemical pollutants such as heavy
metals, dyes pesticides, etc. Biological treatment especially using
cyanobacteria, for treatment of water bodies has mainfold
advantages over conventional methods, as cyanobacteria are
cosmopolitan in environment and known to accumulate high levels of
metal/pollutant; therefore, the process involved is relatively
cheap and environment friendly.
Biodegradation is increasingly being considered as a less
expensive alternative to physical and chemical means of pollutant
detoxication. Pathways of biodegradation have been characterized
for a number of heterotrophic microorganisms, mostly soil isolates,
some of which have been used for remediation of soil, water and
other polluted sites. Because cyanobacteria are photoautotrophic
and some also x atmospheric nitrogen, their use for decontamination
of polluted soil systems can be a very effective tool for
sustainable and green agriculture. Cyanobacterial strains that
combine aerobic metabolism in their vegetative cells with anaerobic
metabolism in the differentiated cells (heterocysts), are
widespread in many ecosystems, including polluted soils (Sorkhoh et
al., 1992). The viability and metabolic activity of these
cyanobacteria, unlike those of heterotrophic microorganisms, are
not subject to reduction by the decrease in concentrations of
pollutants that they may break down. Cyanobacteria have been shown
to degrade both naturally occurring aromatic hydrocarbons
(Cerniglia et al., 1980) and xenobiotics (Narro et al., 1992).
Kuritz and Wolk (1995) demonstrated that two lamentous
cyanobacteria (Anabaena sp., strain PCC 7120 and Nostoc
ellipsosporum) had the ability to degrade a highly chlorinated
aliphatic pesticide, lindane (g-hexachlorocyclohexane), the results
evidenced that this ability can be enhanced by genetic engineering,
and provided qualitative evidence that these two strains can be
genetically engineered to degrade even chlorinated pollutant,
4chlorobenzoate. Kuritz and Wolk (1995) for the rst time reported
that cyanobacteria can be genetically engineered to enhance their
degradation ability of organic pollutants. Current systems for
introducing organisms for bioremediation of polluted areas are
restricted to the implementation of biodegradative microorganisms
from soil; in general, agriculture soils contaminated with
synthetic chemicals remain largely untreated by remediation
programs. On the basis of previous investigations, it may be
proposed that the use of cyanobacteria can be considered for low
cost, low maintenance remediation of pollutants in agriculture
soils. It appears likely other biodegradative operons responsible
for pollutant degradation can also be introduced and expressed in
cyanobacteria and the modied cyanobacteria will prove useful for
biodegradative applications in decontamination for green and safe
agriculture. Major metal pollutants which are commonly found in
soil systems are Cu, Zn, Ni, Co, Pb, Cr, Cd, etc. (Kaushik et al.,
1999). Among the photoautotrophs, cyanobacteria are relatively more
tolerant to heavy metals (Fiore and Trevors, 1994). The uptake of
metal ions (Cu, Pb, Zn, Ni, Cd, Cr, etc.) has been reported in some
of the efcient cyanobacteria are: Spirulina platensis, Oscillatoria
anguistissima, Microcystis sp., Synechococcus sp. (Verma and Singh,
1995; Rai et al., 1998; Pradhan and Rai, 2000; Yee et al., 2004).
Some efcient cyanobacteria reported for the remediation of heavy
metals polluted soils has been presented in Table 5. 10. Role of
rhizospheric microbial interactions in environment and agriculture
sustainability Because of current public concerns about the
sideeffects of agrochemicals, there is an increasing interest in
improving the understanding of microbial interaction activities
among rhizospheric microbes and how these can be efciently used for
the
348
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353
Table 5 Cyanobacteria reported for the remediation of heavy
metals from soil systems. Cyanobacteria Spirulina platensis Nostoc
calcicola Microcystis sp. Oscillatoria anguistissima, Microcystis
aeruginosa f. osaquae strain C340 Synechococcus sp. Limnothrix
planctonica, Synechococcus leopoldiensis and Phormidium limnetica
Nostoc calcicola and Chroococus sp. Lyngbya and Gloeocapsa.
Toxicants Cu, Pb, Zn, Ni, Cd and Cr Cu Ni and Cd Cu, Pb, Zn, Ni, Cd
and Cr Cd, Cu, Pb, Mn and Zn Cu, Pb, Ni and Cd Hg References Greene
et al. (1987) Verma and Singh (1990) Rai et al. (1998) Ahuja et al.
(1999) Parker et al. (2000) Yee et al. (2004) Lefebvre et al.
(2007)
Cr Cr
Anjana et al. (2007) Kiran et al. (2008)
benet of agriculture and environment (Barea et al., 2004; Lucy
et al., 2004). In soil ecosystems, benecial microbial interactions
are responsible in the regulation of key environmental phenomena,
such as the mineralization of complex organic matters into simpler
available N, and the regulation of plant growth and productivity
(Barea et al., 2004). A conceptual theme showing the future role of
PGPR, cyanobacteria and rhizospheric microbial interactions in the
development of sustainable agricultural and environmental has been
demonstrated in Fig. 1. Many studies indicate that soil microbial
communities interact with plant roots and soil constituents at the
root soil interface (Glick, 1995; Bowen and Rovira, 1999; Barea et
al., 2002). The great
array of root microbe interactions forms a dynamic environment
known as the rhizosphere where microbial communities also interact.
The differing physical, chemical, and biological properties of the
rhizospheric soil, compared with those of the root free bulk soil,
are responsible for changes in microbial diversity and for
increased numbers and activity of microbes in the rhizosphere micro
environment (Kennedy, 1998). Certain microbial interaction
activities can be exploited as a low-input biotechnology, and form
a basis for a strategy to help sustainable, environmentally
friendly practices fundamental to the stability and productivity of
both agricultural systems and natural ecosystems (Kennedy and
Smith, 1995). Although it is acknowledged that diverse soil
micro-ora and micro-fauna affect plant growth and aboveground food
webs (Bonkowski, 2004; Scheu et al., 2005). As PGPR and rhizobia
occupy the same micro-habitats in the rhizosphere, they must
interact during root colonization. In legumes, PGPR can improve
nodulation and N2 -xation (Andrade et al., 1998; LucasGarcia et
al., 2004). Field studies (Dashti et al., 1998; Bai et al., 2003),
particularly those using 15 N-based techniques (Dashti et al.,
1998) reinforce such benecial interaction effects between microbial
communities. PGPR enhance nodule formation implicates their
production of plant hormones among the co-inoculation advantages.
Few Pseudomonas strains, but not all, enhanced nodule number and
reduction of acetylene by B. japonicum in soybean plants (Chebotar
et al., 2001). Using both cell free supernatants of PGPR cultures
and pure chemicals, these authors rst reported that plant growth
regulating substances produced by PGPR affected N2 -xation and root
nodulation. These observations were further extended by Manero et
al. (2003). The possibility that metabolites other than
phytohormones, such as siderophores, phytoalexins,
Fig. 1. A conceptual theme exhibiting the role of PGPR,
cyanobacteria and microbial interactions in soil ecosystem for the
development of sustainable agriculture and environment.
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353 Table 6 Plant growth promoting rhizobacteria (PGPR)
and associated plant interactions involved in the remediation of
different pollutants. PGPR Pseudomonas uorescens 279 Kluyvera
ascorbata SUD165, SUD165/26 Brevundimonas sp., KR013, P. uorescens
CR3, Pseudomonas sp., KR017, Rhizobium leguminosarum NZP561
Mesorhizobium huakuii B3 P. putida Flav11, P. putida PML2
Azospirillum brasilense Cd, Enterobacter cloacae CAL 2, P. putidab
UW3 P. putida UW3, A. brasilense Cd and E. cloacae CAL2 E. cloacae
CAL2, E. cloacae UW4 P. uorescens F113 A. lipoferum strains, A.
brasilense strains P. chlororaphis L1391 (pOV17) and P. putida 53a
(pOV17) Pseudomonas sp., A4, Bacillus sp. 32 Bacillus subtilis
SJ101 Azotobacter chroococcum HKN5, B. megaterium HKP1, B.
mucilaginosus HKK1 P. putida UW4,HS2 Bradyrhizobium sp., (vigna)
RM8 Pseudomonas sp., M6, P. jessenii M15 Pseudomonas sp., 29C,
Bacillus sp. 4C Psychrobacter sp., SRA2, SRA1 and B. cereus SRA10
A. chroococcum HKN5 and B. megaterium HKP1 B. pumilus ES4, B.
pumilus RIZO1, and A. brasilense Cd Bradyrhizobium sp., Pseudomonas
sp. and Ochrobactrum cytisi Achromobacter xylosoxidans Ax10 Plants
Wheat Indian mustard (Brassica juncea), Canola (Brassica napus) and
Tomato (Lycopersicon esculentum) None Sites Pot experiments Pot
experiments Pollutants Trichloroethylene (TCE) Ni, Pb and Zn
References Yee et al. (1998) Burd et al. (2000)
349
Culture media
Cd
Robinson et al. (2001)
Astragalus sinicus Arabidopsis Tall fescue (Festuca
arundinacea)
Hydroponics Pot experiments Pot experiments
Cd Polychlorinated biphenyls (PCBs) Polycyclic aromatic
hydrocarbons (PAHs) PAHs
Sriprang et al. (2003) Narasimhan et al. (2003) Huang et al.
(2004b)
Tall fescue (Festuca arundinacea), Kentucky bluegrass (Poa
pratensis) and Wild rye (Elymus canadensis) Tall fescue (Festuca
arundinacea) Alfalfa Wheat Mustard Indian mustard Brassica juncea
Brassica juncea
Pot experiment
Huang et al. (2004a)
Pot experiments Pot experiments Pot experiments Microcosms Pot
experiments Pot experiments Pot experiments
Total petroleum hydrocarbons (TPHs) PCBs Crude oil Naphthalene
Cr Ni Pb and Zn
Huang et al. (2005) Villacieros et al. (2005) Muratova et al.
(2005) Anokhina et al. (2006) Rajkumar et al. (2006) Zaidi et al.
(2006) Wu et al. (2006)
Transgenic canola (Brassica napus) Green gram (Vigna radiate)
Castor bean (Ricinus communis) Indian mustard Brassica juncea and
B. oxyrrhina None Atriplex lentiformis Lupinus luteus
Field study in vitro conditions Pot experiments Greenhouse
condition Pot experiments Solution Greenhouse experiments in
situ
Ni Ni and Zn Ni, Cu and Zn Ni Ni Pb and Cd Phytostabilizing mine
tailings Phytostabilisation of heavy metal polluted soils Cu
Farwell et al. (2007) Wani et al. (2007) Rajkumar and Freitas
(2008b) Rajkumar and Freitas (2008a) Ma et al. (2009a) Wu et al.
(2009) DeBashan et al. (2010) Dary et al. (2010)
Brassica juncea
Pot experiments
Ma et al. (2009b)
and avonoids, might enhance nodule formation (LucasGarcia et
al., 2004), but this hypothesis has not been veried. Some PGPRs and
associated plant interactions, effective in the remediation of
various toxicants from different sites are given in Table 6. 11.
Conclusions An ideal agricultural system is sustainable if
maintains and improves human health, benets producers and consumers
both economically and spiritually, protects the environment, and
produces enough food for an increasing world population.
Indiscriminate population growth, land degradation and increasing
food demand, sustaining agricultural production through improved
soil quality management is critical to the issue of food security
and poverty alleviation in most, if not all, developing countries.
The high cost of chemical nitrogenous fertilizers and the low
purchasing power of most of the farmers restrict its optimal use
thus hampering crop production. Besides, a substantial amount of
the urea N is lost through different mechanisms including ammonia
voatilization, denitrication and leaching losses, causing
environmental pollution problems. The utitilization of biological
N2 -xation technology can decrease the use of urea N, prevent the
depletion of soil organic matter and reduce environmental pol-
lution to a considerable extent. Different bio-fertilizers
systems that include PGPR and cyanobacteria are in use on a limited
scale particularly in rice agroecosystems. Before largescale
extension of microbial biofertilizers systems at the farm level,
further research is needed to determine their N supplement
potentials. Worldwide, considerable research progress has been
achieved in the area of bacterial and cyanobacterial biofertilizer
technology. It has also been demonstrated and proven that this
technology can be the very effective and potential means for
enriching soil fertility and enhancing rice agriculture yield.
However, the technology needs further improvement for its better
exploitation under sustainable agriculture development programs.
Cyanobacteria and PGPR are excellent model systems that can provide
the biotechnologist with novel genetic constituents and bioactive
chemicals with multifact use in agriculture and environmental
sustainability. Current and future progress in our understanding of
PGPR and cyanobacteial diversity, colonization ability, mechanisms
of interactions, formulation and application could facilitate their
development as the reliable components in management of sustainable
agricultural systems. PGPR and cyanobacteria offer an
environmentally sustainable approach to increase crop production
and health. The use of molecular techniques has enhanced our
capacity to understand and
350
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353 Belnap, J., Budel, B., Lange, O.L., 2001. Biological
soil crusts: characteristics and distribution. In: Belnap, J.,
Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function,
and Management. Ecological Studies Series, vol. 150. Springer,
Berlin, pp. 330. Belnap, J., Gillette, D.A., 1997. Disturbance of
biological soil crust: impacts on potential wind erodability of
sandy desert soils in Utah, USA. Land Degrad. Develop. 8, 355362.
Belnap, J., Harper, K.T., 1995. Inuence of cryptobiotic soil crust
on elemental content of tissue of two desert seed plants. Arid Soil
Res. Rehabilit. 9, 107115. Bevivino, A., Sarrocco, S., Dalmastri,
C., Tabacchioni, S., Cantale, C., Chiarini, L., 1998.
Characterization of a free-living maize-rhizosphere population of
Burkholderia cepacia: effect of seed treatment on disease
suppression and growth promotion of maize. FEMS Microbiol. Ecol.
27, 225237. Biondi, N., Piccardi, R., Margheri, M.C., Rodol, L.,
Smith, G.D., Tredici, M.R., 2004. Evaluation of Nostoc strain ATCC
53789 as a potential source of natural pesticides. Appl. Environ.
Microbiol. 70, 33133320. Blaha, D., Combaret, C.P., Mirza, M.S.,
Loccoz, Y.M., 2006. Phylogeny of the
1-aminocyclopropane-1-carboxylic acid deaminase encoding gene acdS
in phytobenefcial and pathogenic Proteobacteria and relation with
strain biogeography. FEMS Microbiol. Ecol. 56, 455470. Bloemberg,
G.V., Lugtenberg, B.J.J., 2001. Molecular basis of plant growth
promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol.
4, 343350. Bonkowski, M., 2004. Protozoa and plant growth: the
microbial loop in soil revisited. New Phytol. 162, 617631. Bowen,
G.D., Rovira, A.D., 1999. The rhizosphere and its management to
improve plant growth. Advan. Agron. 66, 1102. Burd, G.I., Dixon,
D.G., Glick, B.R., 2000. Plant growth-promoting bacteria that
decrease heavy metal toxicity in plants. Can. J. Microbiol. 46,
237245. Campbell, S.E., 1979. Soil stabilization by a prokaryotic
desert crust. Implications for precambrian land biota. Orig. life.
9, 335348. Cerniglia, C.E., Gibson, D.T., van Baalen, C., 1980.
Oxidation of naphthalene by cyanobacteria and microalgae. J. Gen.
Microbiol. 116, 495500. Chebotar, V.K., Asis, C.A., Akao, S., 2001.
Production of growthpromoting substances and high colonization
ability of rhizobacteria enhance the nitrogen xation of soybean
when inoculated with Bradyrhizobium japonicum. Biol. Fertil. Soils
34, 427432. ChinAWoeng, T.F.C., Bloemberg, G.V., Mulders, I.H.M.,
Dekkers, L.C., Lugtenberg, B.J.J., 2000. Root colonization by
phenazine-1-carboxamideproducing bacterium Pseudomonas chlororaphis
PCL1391 is essential for biocontrol of tomato foot and root rot.
Mol. Plant Microbe Inter. 13, 13401345. Cho, K., Toler, H., Lee,
J., Owenley, B., Stutz, J.C., Moore, J.L., Auge, R.M., 2006.
Mycorrhizal symbiosis and response of sorghum plants to combined
drought and salinity stresses. J. Plant Physiol. 163, 517528.
Chung, S., Kong, H., Buyer, J.S., Lakshman, D.K., Lydon, J., Kim,
S.-D., Roberts, D., 2008. Isolation and partial characterization of
Bacillus subtilis ME488 for suppression of soilborne pathogen of
cucumber and pepper. Appl. Microb. Cell Physiol. 80, 115123. Dary,
M., Chamber Perez, M.A., Palomares, A.J., Pajuelo, E., 2010. In
situ phytostabilisation of heavy metal polluted soils using Lupinus
luteus inoculated with metal resistant plant-growth promoting
rhizobacteria. J. Hazard. Mater. 177, 323330. Dashti, N., Zhang,
F., Hynes, R., Smith, D.L., 1998. Plant growth promoting
rhizobacteria accelerate nodulation and increase nitrogen xation
activity by eld grown soybean [Glycine max (L.) Merr.] under short
season conditions. Plant Soil 2, 205213. DeCaire, G.Z., De Cano,
M.S., De Mule, M.C.Z., De Halperin, D.R., 1990. Antimycotic
products from the cyanobacterium Nostoc muscorum against
Rhizoctonia solani. Phyton 51, 14. DeMule, M.C.Z., De Caire, G.Z.,
De Cano, M.S., De Halperin, D.R., 1991. Bioactive compounds from
Nostoc muscorum (Cianobacterias). Cytobios 66, 169172. DeBashan,
L.E., Hernandez, J.P., Bashan, Y., Maier, M.R., 2010. Bacillus
pumilus ES4: candidate plant growth-promoting bacterium to enhance
establishment of plants in mine tailings. Environ. Exp. Bot. 69,
343352. DeCaire, G.Z., De Cano, M.S., De Mule, M.C., Palma, R.M.,
Colombo, K., 1997. Exopolysaccharide of Nostoc muscorum
(cyanobacteria) in the aggregation of soil particles. J. Appl.
Phycol. 4, 249253. Decho, A.W., 1990. Microbial exopolymer
secretions in ocean environments: their role(s) in food webs and
marine processes. Oceanogr. Mar. Biol. 28, 73153. Dobbelaere, S.,
Croonenborgh, A., Thys, A., Ptacek, D., Okon, Y., Vanderleyden, J.,
2002. Effect of inoculation with wild type Azospirillum brasilense
and A. irakense strains on development and nitrogen uptake of
spring wheat and grain maize. Biol. Fertil. Soils 36, 284297.
Earanna, N., Govindan, R., 2002. Role of biofertilizers in mulberry
productiona review. Indian J. Seric. 41, 9299. Egamberdiyeva, D.,
2007. The effect of plant growth promoting bacteria on growth and
nutrient uptake of maize in two different soils. Appl. Soil Ecol.
36, 184189. Falchini, L., Sparvoli, E., Tomaselli, L., 1996. Effect
of Nostoc (cyanobacteria) inoculation on the structure and
stability of clay soils. Biol. Fertil. Soils 23, 246252. Farwell,
A.L., Vesely, S., Nero, V., Rodriguez, H., McCormack, K., Shah, S.,
Dixon, D.G., Glick, B.R., 2007. Tolerance of transgenic canola
plants (Brassica napus) amended with plant growth-promoting
bacteria to ooding stress at a metalcontaminated eld site. Environ.
Pollut. 147, 540545. Fiore, M.F., Trevors, J.T., 1994. Cell
composition and metal tolerance in cyanobacteria. Biometals 7,
83103. Flaibani, A., Olsen, Y., Painter, T.J., 1989.
Polysaccharides in desert reclamation: composition of exocellular
proteoglycan complexes produced by lamentous blue-green and
unicellular green edaphic algae. Carbohydrate Res. 190, 235248.
manage the rhizosphere ecosystems, and may lead to new products
with improved effectiveness. Genetic enhancement of PGPR strains
with enhanced colonization and effectiveness, may involve addition
of one or more traits associated with plant growth promotion.
Genetic manipulation of host crops for root-associated traits to
enhance establishment and proliferation of benecial microorganisms
is being pursued. Health and safety testing are also required to
address such issues as the non-target effects on other organisms
including toxigenicity, allergenicity and pathogenicity,
persistence in the environment and potential for horizontal gene
transfer. Acknowledgements Authors are very thankful to Professor
S.P. Singh, Centre of Advanced Study in Botany, Banaras Hindu
University, Varanasi for his help in revision and editing the
manuscript. The authors thank the Head, Department of Environmental
Science, Babasaheb Bhimrao Ambedkar (Central) University,
Lucknow-226025 for providing infrastructural facilities. This work
was possible through grants given to Dr. Jay Shankar Singh as
Senior Research Associate [Scientists Pool Scheme; CSIR sanction
No. 13 (8243-A)/Pool/2008] by Council of Scientic and Industrial
Research, Human Resource Development Group, Government of India,
New Delhi. Vimal Chandra Pandey is thankful to University Grants
Commission, Government of India, New Delhi for nancial support.
ReferencesAbdalla, M.H., Omer, S.A., 2001. Survival of
Rhizobia/Bradirhizobia and a rock phosphate solubilizing fungus
Aspergillus nigeron various carriers from some agroindustrial
wastes and their effect on nodulation and growth of fababean and
soybean. J. Plant Nutri. 24, 261272. Acea, M.J., Prieto Fernandez,
A., Diz Cid, N., 2003. Cyanobacterial inoculation of heated soils:
effect on microorganisms of C and N cycles and on chemical
composition in soil surface. Soil Biol. Biochem. 35, 513524. Afzal,
A., Asghari, B., 2008. Rhizobium and phosphate solubilizing
bacteria improve the yield and phosphorus uptake in wheat. Inter.
J. Agric. Biol. 10, 8588. Ahmed, D., El Gamal, M.S., Ammar, U.M.,
Abd El Raouf, T.M., 2000. Role of some cyanobacteria in enhancement
of soil characteristics. Egypt. J. Plycol. 1, 99106. Ahuja, P.,
Gupta, R., Saxena, R.K., 1999. Zn+ biosorption by Oscillatoria
anguistissima. Process Biochem. 34, 7785. Alagawadi, A.R., Gaur,
A.C., 1992. Inoculation of Azospirillum brasilense and
phosphate-solubilizing bacteria on yield of sorghum (Sorghum
bicolor L. Moench) in dry land. Trop. Agric. 69, 347350. Andrade,
G., Mihara, K.L., Linderman, R.G., Bethlenfalvay, G.J., 1998. Soil
aggregation status and rhizobacteria in the mycorrhizosphere. Plant
Soil 202, 8996. Anjana, K., Kaushik, A., Kiran, B., Nisha, R.,
2007. Biosorption of Cr(VI) by immobilized biomass of two
indigenous strains of cyanobacteria isolated from metal
contaminated soil. J. Hazard. Mater. 148, 383386. Anokhina, T.O.,
Volkova, O.V., Puntus, I.F., Filonov, A.E., Kochetkov, V.V.,
Boronin, M.A., 2006. Plant growth-promoting Pseudomonas bearing
catabolic plasmids: naphthalene degradation and effect on plants.
Process Biochem. 41, 24172423. Apte, S.K., Reddy, B.R., Thomas, J.,
1987. Relationship between sodium inux and salt tolerance of
nitrogen-xing cyanobacteria. Appl. Environ. Microbiol. 53,
19341939. Bai, Y.M., Zhou, X.M., Smith, D.L., 2003. Enhanced
soybean plant growth resulting from coinoculation of Bacillus
strains with Bradyrhizobium japonicum. Crop Sci. 43, 17741781.
Barea, J.M., Azcon, R., Azcon Aguilar, C., 2004. Mycorrhizal fungi
and plant growth promoting rhizobacteria. In: Varma, A., Abbott,
L., Werner, D., Hampp, R. (Eds.), Plant Surface Microbiology.
Springer-Verlag, Heidelberg, Germany, pp. 351371. Barea, J.M.,
Gryndler, M., Lemanceau, Ph., Schuepp, H., Azcon, R., 2002. The
rhizosphere of mycorrhizal plants. In: Gianinazzi, S., Schuepp, H.,
Barea, J.M., Haselwandter, K. (Eds.), Mycorrhiza Technology in
Agriculture: From Genes to Bioproducts. Birkhauser Verlag, Basel,
Switzerland, pp. 118. Belimov, A.A., Hontzeas, N., Safronova, V.I.,
Demchinskaya, S.V., Piluzza, G., Bullitta, S., Glick, B.R., 2005.
Cadmium-tolerant plant growth-promoting bacteria associated with
the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol.
Biochem. 37, 241250. Belimov, A.A., Kojemiakov, P.A., Chuvarliyeva,
C.V., 1995. Interaction between barley and mixed cultures of
nitrogen xing and phosphate-solubilizing bacteria. Plant Soil 17,
2937. Belimov, A.A., Safronova, V.I., Sergeyeva, T.A., Egorova,
T.N., Matveyeva, V.A., Tsyganov, V.E., Borisov, A.Y., Tikhonovich,
I.A., Kluge, C., Preisfeld, A., Dietz, K.J., Stepanok, V.V., 2001.
Characterization of plant growth promoting rhizobacteria isolated
from polluted soils and containing 1-aminocyclopropane1-carboxylate
deaminase. Can. J. Microbiol. 47, 242252.
J.S. Singh et al. / Agriculture, Ecosystems and Environment 140
(2011) 339353 Galal, Y.G.M., 2003. Assessment of nitrogen
availability to wheat (Triticum aestivum L.) from inorganic and
organic N sources as affected by Azospirillum brasilense and
Rhizobium leguminosarum inoculation. Egyptian J. Microbiol. 38,
5773. Gholami, A., Shahsavani, S., Nezarat, S., 2009. The effect of
plant growth promoting rhizobacteria (PGPR) on germination,
seedling growth and yield of maize. World Acad. Sci. Engin.
Technol. 49, 1924. Glick, B.R., Karaturovc, D.M., Newell, P.C.,
1995. A novel procedure for rapid isolation of plant
growth-promoting pseudomonads. Can. J. Microbiol. 41, 533536.
Glick, B.R., Patten, C.L., Holguin, G., Penrose, D.M., 1999.
Biochemical and Genetic Mechanisms Used by Plant Growth Promoting
Bacteria. Imperial College Press, London. Glick, B.R., 1995. The
enhancement of plant growth by free-living bacteria. Can. J.
Microbiol. 41, 109117. Glick, B.R., Chagping, L., Sibdas, G.,
Dumbroff, E.B., 1997. Early development of canola seedlings in the
presence of plant growth-promoting bacterium Pseudomonas putida
GR12-2. Soil Biol. Biochem. 29, 12331239. Glick, B.R., Penrose,
D.M., Li, J., 1998. A model for the lowering of plant ethylene
concentrations by plant growth-promoting bacteria. J. Theor. Biol.
190, 6368. Glick, B.R., Todorovic, B., Czarny, J., Cheng, Z., Duan,
J., McConkey, B., 2007. Promotion of plant growth by bacterial ACC
deaminase. Crit. Rev. Plant Sci. 26, 227242. Gravel, V., Antoun,
H., Tweddell, R.J., 2007. Growth stimulation and fruit yield
improvement of greenhouse tomato plants by inoculation with
Psedomonas putida or Trichoderma atroviride: possible roe of Indole
Acitic Acid (IAA). Soil Biol. Biochem. 39, 19681977. Greene, B.,
McPherson, R., Darnall, D., 1987. In: Patterson, J.W., Passion, R.
(Eds.), Algal Sorbents for Selective Metal Ion Recovery. Lewis
Publishers, Chelsea, MI, pp. 315338. Grichko, V.P., Glick, B.R.,
2001. Amelioration of ooding stress by A