Sei sulla pagina 1di 15

Agriculture, Ecosystems and Environment 140 (2011) 339353

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

journal homepage:


Efcient soil microorganisms: A new dimension for sustainable agriculture and environmental development
Jay Shankar Singh , Vimal Chandra Pandey, D.P. Singh
Department 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 t
Sustainable 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 (J.S. Singh). 0167-8809/$ see front matter 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2011.01.017


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


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-


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


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


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


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.


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


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


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)


Culture media


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


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. References
Abdalla, 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 ACC deaminasecontaining plant growth-promoting bacteria. Plant Physiol. Biochem. 39, 1117. Han, H., Supanjani, S.K., Lee, D., 2004. Effect of co-inoculation with phosphate and potassium solubilizing bacteria on mineral uptake and growth of pepper and cucumber. Agron. J. 24, 169176. Harish, S., Kavino, M., Kumar, N., Balasubramanian, P., Samiyappan, R., 2009a. Induction of defense-related proteins by mixtures of plant growth promoting endophytic bacteria against Banana bunchy top virus. Biol. Control 51, 1625. Harish, S., Kavino, M., Kumar, N., Samiyappan, R., 2009b. Differential expression of pathogenesis-related proteins and defense enzymes in banana: interaction between endophytic bacteria banana bunchy top virus and Pentalonia nigronervosa. Biocontr. Sci. Technol. 19, 843857. Hashem, A., 2001a. Problems and prospects of cyanobacterial biofertilizer for rice cultivation. Aust. J. Plant Physiol. 28, 881888. Hashem, M.A., 2001b. Problems and prospects of cyanobacterial biofertilizer for rice cultivation. Aust. J. Plant Physiol. 28, 881888. Hegde, D.M., Dwivedi, B.S., Babu, S.N.S., 1999. Biofertilizers for cereal production in Indiaa review. Indian J. Agric. Sci. 69, 7383. Hernandez Rodriguez, A., Heydrich Perez, M., Acebo Guerrero, Y., Velazquez del Valle, M.G., Hernandez Lauzardo, A.N., 2008. Antagonistic activity of Cuban native rhizobacteria against Fusarium verticillioides (Sacc.) Nirenb. In maize (Zea mays L.). Appl. Soil Ecol. 39, 180186. Hontzeas, N., Saleh, S.S., Glick, B.R., 2004a. Changes in gene expression in canola roots induced by ACC-deaminase-containing plant-growth-promoting bacteria. Mol. Plant Microbe Interac. 17, 865871. Hontzeas, N., Zoidakis, J., Glick, B.R., Abu Omar, M.M., 2004b. Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium P. putida UW4: a key enzyme in bacterial plant growth promotion. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1703, 1119. Huang, X.D., ElAlawi, Y., Gurska, J., Glick, B.R., Greenberg, B.M., 2005. A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem. J. 81, 139147. Huang, X.D., ElAlawi, Y., Penrose, D.M., Glick, B.R., Greenberg, B.M., 2004a. Responses of plants to creosote during phytoremdiation and their signicance for remediation processes. Environ. Pollut. 130, 453463. Huang, X.D., ElAlawi, Y., Penrose, D.M., Glick, B.R., Greenberg, B.M., 2004b. A multiprocess phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ. Pollut. 130, 465476. Jacobson, C.B., Pasternak, J.J., Glick, B.R., 1994. Partial purication and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can. J. Microbiol. 40, 10191025. Jayashree, K., Shanmugam, V., Raguchander, T., Ramanathan, A., Samiyappan, R., 2000. Evaluation of Pseudomonas uorescens (Pf1) against blackgram and sesame root rot diseases. J. Biol. Contr. 14, 5561. Jeffries, D.L., Klopatek, J.M., Link, S.O., Bolton Jr., H., 1992. Acetylene reduction by cryptogamic crusts from a blackbrush community as related to resaturation and dehydration. Soil Biol. Biochem. 24, 11011105. Jetiyanon, K., Fowler, W.D., Kloepper, J.W., 2003. Broad-spectrum protection against several pathogens by PGPR mixtures under eld conditions in Thailand. Plant Disease 87, 13901394. Jiang, Zhi-Qiang, Guo, Ya-Hui., Li, Shi-Mo., Qi, Hong-Ying., Guo, Jian-Hua., 2006. Evaluation of biocontrol efciency of different Bacillus preparations and eld application methods against Phytophthora blight of bell pepper. Biol. Control 36, 216223. Kannaiyan, S., 2002. Biofertilizers for sustainable crop production. In: Kannaiyan, S. (Ed.), Biotechnology of Biofertilizers. Kluwer Academic Publishers, AA Dordrecht, The Netherlands with Narosa Publishing House New Delhi India, pp. 949.


Cameron, K.C., Haynes, R.J., 1986. Retention and movement of nitrogen in soils. In: Haynes, R.J. (Ed.), Mineral Nitrogen in the PlantSoil System. Academic Press, Orlando, pp. 166241. Kaushik, B.D., Misra, S., 1989. Growth promoting substances of cyanobacteria, II. Detections of amino acids, sugars and auxins. Proc. Indian Nat. Sci. Acad. Biol. Sci. 55, 499504. Kaushik, S., Sahu, B.K., Lawania, R.K., Tiwari, R.K., 1999. Occurrence of heavy metals in lentic water of Gwalior region. Pollut. Res. 18, 137140. Kavino, M., Harish, S., Kumar, N., Saravanakumar, D., Damodaran, T., Soorianathasundaram, K., Samiyappan, R., 2007. Rhizosphere and endophytic bacteria for induction of systemic resistance of banana plantlets against bunchy top virus. Soil Biol. Biochem. 39, 10871098. Kavino, M., Harish, S., Kumar, N., Saravanakumar, D., Samiyappan, R., 2008. Induction of systemic resistance in banana (Musa spp.) against banana bunchy top virus (BBTV) by combining chitin with root-colonizing Pseudomonas uorescens strain CHA0. Eur. J. Plant Pathol. 120, 353362. Kavino, M., Harish, S., Kumar, N., Saravanakumar, D., Samiyappan, R., 2010. Effect of chitinolytic PGPR on growth, yield and physiological attributes of banana (Musa spp.) under eld conditions. Appl. Soil Ecol. 45, 7177. Kennedy, A.C., 1998. The rhizosphere and spermosphere. In: Sylvia, D.M., Fuhrmann, J.J., Hartel, P.G., Zuberer, D.A. (Eds.), Principles and Applications of Soil Microbiology. Prentice Hall, Upper Saddle River, New Jersey, pp. 389407. Kennedy, A.C., Smith, K.L., 1995. Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170, 7586. Kiran, B., Kaushik, A., Kaushik, C.P., 2008. Metal-salt co-tolerance and metal removal by indigenous cyanobacterial strains. Process Biochem. 43, 598604. Kleiner, K.T., Harper, K.T., 1977. Soil properties in relation to cryptogamic ground cover in Canyon-lands National Park. J. Range. Managem. 30, 202205. Kohler, J., Caravaca, F., Carrasco, L., Roldan, A., 2006. Contribution of Pseudomonas mendocina and Glomus intraradices to aggregates stabilization and promotion of biological properties in rhizosphere soil of lettuce plants under eld conditions. Soil Use Manage. 22, 298304. Kohler, J., Hernandez, Jose, Antonio, Caravaca, F., Roldan, A., 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65, 245252. Kucey, R.M.N., Janzen, H.H., Leggett, M.E., 1989. Microbially mediated increases in plant-available phosphorus. Ad. Agron. 42, 199228. Kuritz, T., Wolk, P., 1995. Use of lamentous cyanobacteria for biodegradation of organic pollutants. Appl. Environ. Microbiol. 61, 234238. Ladha, J.K., Reddy, P.M., 1995. Extension of nitrogen xation to rice: necessity and possibilities. Geol. J. 35, 363372. Lange, O.L., Meyer, A., Zellner, H., Heber, U., 1994. Photosynthesis and water relations of lichen soil crusts: eld measurements in the coastal fog zone of the Namib Desert. Funct. Ecol. 8, 253264. Lefebvre, Daniel, D., Kelly, D., Budd, K., 2007. Biotransformation of Hg (II) by Cyanobacteria. Appl. Environ. Microbiol. 73, 243249. Li, J., Ovakim, D.H., Charles, T.C., Glick, B.R., 2000. An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr. Microbiol. 41, 101105. LucasGarcia, J.A., Probanza, A., Ramos, B., Colon-Flores, J.J., Gutierrez-Manero, F.J., 2004. Effects of plant growth promotingrhizobateria (PGPRs) on the biological nitrogen xation, nodulation and growth of Lupinus albus I. cv Multolupa. Engineer. Life Sci. 4, 7177. Lucy, M., Reed, E., Glick, B.R., 2004. Application of free living plant growth-promoting rhizobacteria Ant. van Leeuw. Int. J. Gen. Mol. Microbiol. 86, 125. Lugtenberg, B.J.J., Dekkers, L., Bloemberg, G.V., 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Ann. Rev. Phytopathol. 39, 461490. Ma, W., Sebestianova, S.B., Sebestian, J., Burd, G.I., Guinel, F.C., Glick, B.R., 2003. Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Anton. van Leeuw. 83, 285291. Ma, Y., Rajkumar, M., Freitas, H., 2009a. Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J. Environ. Manage. 90, 831837. Ma, Y., Rajkumar, M., Freitas, H., 2009b. Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J. Hazard. Mater. 166, 11541161. MalamIssa, O., LeBissonnais, Y., Defarge, C., Trichet, J., 2001. Role of a cyanobacterial cover on structural stability of sandy soils in the sahelian part of western Niger. Geoderma 101, 1530. Manchanda, H., Kaushik, A., 2000. Algal ora of aridisols of Rohtak and salt tolerance of the indigenous cyanobacteria. Trop. Ecol. 41, 217223. Manero, F.J., Probanza, A., Ramos, B., Flores, J.J., Garca-Lucas, J.A., 2003. Effects of culture ltrates of rhhizobacteria isolated from wild lupin on germination, growth, and biological nitrogen xation of lupin seedlings. J. Plant Nutri. 26, 11011115. Manjula, M., Podile, A.R., 2001. Chitin-supplemented formulations improve biocontrol and plant growth promoting efciency of Bacillus subtilis AF 1. Can. J. Microbiol. 47, 618625. Mantelin, S., Touraine, B., 2004. Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J. Exp. Bot. 55, 2734. Marathe, K.V., 1972. Role of some blue-green algae in soil aggregation. In: Ist International Symposium on Taxonomy and Biology of Blue-Green Algae , Madras, India, pp. 328331. Mathiyazhagan, S., Kavitha, K., Nakkeeran, S., Chandrasekar, G., Manian, K.K., Renukadevi, P., Krishnamoorthy, A.S., Fernando, W.G.D., 2004. PGPR mediated management of stem blight of Phyllanthus amarus (schum and thonn) caused


J.S. Singh et al. / Agriculture, Ecosystems and Environment 140 (2011) 339353 Radjacommare, R., Nandakumar, R., Kandan, A., Suresh, S., Bharathi, M., Raguchander, T., Samiyappan, R., 2002. Pseudomonas uorescens based bio-formulation for the management of sheath blight disease and leaf folder insect in rice. Crop Prot. 21, 671677. Radjacommare, R., Ramanathan, A., Kandan, A., Harish, S., Thambidurai, G., Sible, G.V., Ragupathi, T., Samiyappan, R., 2004. PGPR mediates induction of pathogenesis-related (PR) proteins against the infection of blast pathogen in resistant and susceptible ragi [Eleusine coracana (L.) Gaertner] cultivars. Plant Soil 266, 165176. Raguchander, T., Jeyashree, K., Samiyappan, R., 1997. Management of Fusarium wilt of banana using antagonistic microorganisms. J. Biol. Contr. 11, 101105. Rai, L.C., Singh, S., Pradhan, S., 1998. Biotechnological potential of naturally occurring and laboratory grown Microcystis in biosorption of Ni2+ and Cd2+ . Curr. Sci. 74, 461463. Rajkumar, M., Freitas, H., 2008a. Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 99, 34913498. Rajkumar, M., Freitas, H., 2008b. Inuence of metal resistant-plant growthpromoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71, 834842. Rajkumar, M., Nagendran, R., Lee, K.J., Lee, W.H., Kim, S.Z., 2006. Inuence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62, 741746. Ramazan, C., Akmakc, I., Figen, A., Adil, A., Fikrettin, S., Ahin, B.C., 2005. Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different eld soil conditions. Biochemistry 38, 14821487. Robinson, B., Russell, C., Hedley, M., Clothier, B., 2001. Cadmium adsorption by rhizobacteria: implications for New Zealand pastureland. Agric. Ecosyst. Environ. 87, 315321. Rodriguez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotech. Advan. 17, 319339. Rogers, S.L., Burns, R.G., 1994. Changes in aggregate stability, nutrient status, indigenous microbial populations, and seedling emergence, following inoculation of soil with Nostoc muscorum. Biol. Fertil. Soils 18, 209215. Rokhzadi, A., Ahmad, A., Farrokh, D., Ghorban, N.-M., Eslam, M., 2008. Inuence of plant growth-promoting rhizobacteria on dry matter accumulation and yield of Chickpea (Cicer arietinum L.) under eld conditions. Amer. Eur. J. Agric. Environ. Sci. 3, 253257. Safronova, V.I., Stepanok, V.V., Engqvist, G.L., Alekseyev, Y.V., Belimov, A.A., 2006. Root-associated bacteria containing 1-minocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fertil. Soils 42, 267272. Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34, 635648. Saravanakumar, D., Lavanya, N., Muthumeena, K., Raguchander, T., Samiyappan, R., 2009. Fluorescent pseudomonad mixtures mediate disease resistance inrice plants against sheath rot (Sarocladium oryzae) disease. Biocontrol 54, 273286. Saravanakumar, D., Samiyappan, R., 2007. ACC deaminase from Pseudomonas uorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102, 12831292. Scheu, S., Ruess, L., Bonkowski, M., 2005. Interactions between microorganisms and soil micro- and mesofauna. In: Buscot, F., Varma, S. (Eds.), Micro-organisms in Soils: Roles in Genesis and Functions. Springer-Verlag, Heidelberg, Germany, pp. 195212. Sergeeva, E., Shah, S., Glick, B.R., 2006. Growth of transgenic canola (Brassica napus cv, Westar) expressing a bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene on high concentrations of salt. World J. Microbiol. Biotechnol. 22, 277282. Shaharoona, B., Arshad, M., Zahir, Z.A., 2006. Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol. Biochem. 38, 29712975. Shanmugam, V., Sriram, S., Babu, S., Nandakumar, R., Raguchander, T., Balasubramanian, P., Samiyappan, R., 2001. Purication and characterization of an extracellular a-glucosidase protein from Trichoderma viride which degrades a phytotoxin associated with sheath blight disease in rice. J. Appl. Microbiol. 90, 320329. Sheng, X.F., He, L.Y., 2006. Solubilization of potassium-bearing minerals by a wildtype strain of Bacillus edaphicus and its mutants and increased potassium uptake by wheat. Can. J. Microbiol. 52, 6672. Silva, H.S.A., da Silva, R.R., Macagnan, M., de Almeida, H.V.B., Pereira, M.C.B., Mounteer, A., 2004. Rhizobacterial induction of systemic resistance in tomato plants: non-specic protection and increase in enzyme activity. Biol. Contr. 29, 288295. Singh, A.L., Singh, P.K., 1989. Phosphorus fertilization and the growth and N2-xation of Azolla and blue-green algae in rice eld. Indian J. Plant Physiol. 33, 2126. Singh, G.R., Pandya, K.S., Choudhary, K.K., Sharma, R.B., 1997. Biofertilizers in crop production. Indian Farm. 46, 3436. Singh, J.S., Pandey, V.C., Singh, D.P., Singh, R.P., 2010. Inuence of pyrite and farmyard manure on population dynamics of soil methanotroph and rice yield in saline rain-fed paddy eld. Agric. Ecosyst. Environ. 139, 7479. Singh, P.P., Shin, Y.C., Park, C.S., Chung, Y.R., 1999. Biological controls of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89, 9299. Sorkhoh, N., Al-Hasan, R., Radwan, S., Hopner, 1992. Self-cleaning of the Gulf, vol. 359. Nature, London, p. 109. Sriprang, R., Hayashi, M., Ono, H., Takagi, M., Hirata, K., Murooka, Y., 2003. Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from

by Corynespora cassiicola (berk and curt) Wei. Arch. Phytopathol. Plant Prot. 37, 183199. Mayak, S., Tirosh, T., Glick, B.R., 2004a. Plant growth-promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci. 166, 525530. Mayak, S., Tirosh, T., Glick, B.R., 2004b. Plant growth-promoting bacteria that confer resistance in tomato and pepper to salt stress. Plant Physiol. Biochem. 42, 565572. Mazor, G., Kidron, G.J., Vonshak, A., Abeliovich, A., 1996. The role of cyanobacterial exopolysaccharides in structuring microbial crusts. FEMS Microbiol. Ecol. 21, 121130. Muratova, A.Y., Turkovskaya, O.V., Antonyuk, L.P., Makarov, O.E., Pozdnyakova, L.I., Ignatov, V.V., 2005. Oil-oxidizing potential of associative rhizobacteria of the genus Azospirillum. Microbiology 74, 210215. Murphy, J.F., Zehnder, G.W., Schuster, D.J., Sikora, E.J., Polston, J.E., Kloepper, J.W., 2000. Plant growth-promoting rhizobacterial mediated protection in tomato against tomato mottle virus. Plant Disease 84, 779784. Nandakumar, R., Babu, S., Viswanathan, R., Raguchander, T., Samiyappan, R., 2001. Induction of systemic resistance in rice against sheath blight disease by plant growth promoting rhizobacteria. Soil Biol. Biochem. 33, 603612. Narasimhan, K., Basheer, C., Bajic, V.B., Swarup, S., 2003. Enhancement of plantmicrobe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol. 132, 146153. Narro, M.L., Cerniglia, C.E., van Baalen, C., Gibson, D.T., 1992. Metabolism of phenanthrene by the marine cyanobacterium Agmenellum quadruplicatum PR6. Appl. Environ. Microbiol. 58, 13511359. Naureen Zakira, P., Hafeez, Adam H., Roberts, Fauzia Y., Michael, R., 2009. Identication of rice blast disease-suppressing bacterial strains from the rhizosphere of rice grown in Pakistan. Crop Prot. 28, 10521060. Nayak, S., Prasanna, R., Pabby, A., Dominic, T.K., Singh, P.K., 2004. Effect of urea and BGAAzolla biofertilizers on nitrogen xation and chlorophyll accumulation in soil cores from rice elds. Biol. Fertil. Soils 40, 6772. Nezarat, S., Gholami, A., 2009. Screenig plant growth promoting rhizobacteia for improving seed germination, seedling growth and yield of maize. Pak. J. Biol. Sci. 12, 2632. Nie, L., Shah, S., Rashid, A., Burd, G.I., Dixon, D.G., Glick, B.R., 2002. Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growthpromoting bacterium Enterobacter cloacae CAL2. Plant Physiol. Biochem. 40, 355361. Niranjan, S.R., Deepak, S.A., Basavaraju, P., Shetty, H.S., Reddy, M.S., Kloepper, J.W., 2003. Copmparative performance of formulations of plant plant promoting rhizobacteria in growth promotion and suppression of downy mildew in perl millet. Crop Prot. 22, 579588. Nisha, R., Kaushik, A., Kaushik, C.P., 2007. Effect of indigenous cyanobacterial application on structural stability and productivity of an organically poor semi-arid soil. Geoderma 138, 4956. Noel, T.C., Sheng, C., Yost, C.K., Pharis, R.P., Hynes, M.F., 1996. Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can. J. Microbiol. 42, 279283. Nyporko, A.Y., Yemets, A.I., Klimkina, L.A., Blume, Y.B., 2002. Sensitivity of Eleusine indica callus to Triuralin and Amiprophosmethyl in correlation to the binding of these compounds to tubulin. Russ. J. Plant Physiol. 49, 413418. Ordog, V., 1999. Benecial effects of microalgae and cyanobacteria in plant soil-system with special regard to their auxin- and cytokinin-like activity. In: International Workshop and Training Course on Microalgal Biology and Biotochnology , Mosonmagyarovar, Hungary, pp. 4344. Orlovsky, L., Dourikov, M., Babaev, A., 2004. Temporal dynamics and productivity of biogenic soil crusts in the central Karakum desert, Turkmenistan. J. Arid Environ. 56, 579601. Pandey, Kapil D., Shukla, Prabhu N., Giri, Deen D., Kashyap, Ajai##K., 2005a. Cyanobacteria in alkaline soil and the effect of cyanobacteria inoculation with pyrite amendments on their reclamation. Biol. Fertil. Soils 41, 451457. Pandey, P., Kang, S.C., Maheshwari, D.K., 2005b. Isolation of endophytic plant growth promoting Burkholderia sp. MSSP from root nodules of Mimosa pudica. Curr. Sci. 89, 170180. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants: a review. Ecotox. Environ. Saf. 60, 324349. Parker, Dorothy L., Mihalick, Jennifer E., Plude, John L., Plude, Michelle J., Clark, Thomas P., Lynn Egan, Joshua Flom J., Rai, L.C., Kumar, H.D., 2000. Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f. osaquae strain C3-40. J. Appl. Phycol. 12, 219224. Paul, Diby., Nair, Sudha., 2008. Stress adaptations in a Plant Growth Promoting Rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J. Basic Microbiol. 48, 378384. Penrose, D.M., Glick, B.R., 2001. Levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in exudates and extracts of canola seeds treated with plant growthpromoting bacteria. Can. J. Microbiol. 47, 368372. Persello Cartieaux, F., Nussaume, L., Robaglia, C., 2003. Tales from the underground: molecular plantrhizobacteria interactions. Plant Cell Environ. 26, 189199. Podile, A.R., Kishore, K., 2007. Plant growth-promoting rhizobacteria. In: Gnanamanickam, S.S. (Ed.), Plant Associated Bacteria. Springer, The Netherlands, pp. 195230. Pradhan, S., Rai, L.C., 2000. Optimization of ow rate, initial metal ion concentration and biomass density fo maximum removal of Cu2+ by immobilized Microcystis. World J. Microbiol. Biotechnol. 16, 579584.

J.S. Singh et al. / Agriculture, Ecosystems and Environment 140 (2011) 339353 Arabidopsis thaliana coding for phytochelatin synthase. Appl. Environ. Microbiol. 69, 17911796. Srivastava, A.K., Bhargava, P., Kumar, A., Rai, L.C., Neilan, A.B., 2009. Molecular characterization and the effect of salinity on cyanobacterial diversity in the rice elds of Eastern Uttar Pradesh, India. Saline Syst. 5, 117. Stiens, M., Schneiker, S., Keller, M., Kuhn, S., Puhler, A., Schluter, A., 2006. Sequence analysis of the 144-kilobase accessory plasmid psmesm11a, isolated from a dominant Sinorhizobium meliloti strain identiWed during a long-term Weld release experiment. Appl. Environ. Microbiol. 72, 36623672. Suresh, G., Gopinath, T.N., Kathiresan, D., Marutharavindran, C.R., Shanmug Asundaram, S., 1992. Growth of cyanobacteria in sachet packs. In: 32rd Annual Conference Agriculture Microbiolgy , Madurai Kamraj University, Madurai, India, p. 39. Tanwar, S.P.S., Sharma, G.L., Chahar, M.S., 2002. Effect of phosphorus and biefertilizers on the growth and productivity of black gram. Annl. Agric. Res. 23, 491493. Tassara, C., Zaccaro, M.C., Storni, M.M., Palma, M., Zulpa, G., 2008. Biological control of lettuce white mold with cyanobacteria. Int. J. Agric. Biol. 10, 487492. Teuscher, E., Lindequist, U., Mundt, S., 1992. Cyanobakterien, Quellen biogener Wirkstoffe. Pharm. Ztg. Wiss. 137, 5769. Turan, M., Ataoglu, N., Sahin, F., 2006. Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture. Sustain. Agric. 28, 99108. Uchiumi, T., Oowada, T., Itakura, M., Mitsui, H., Nukui, N., Dawadi, P., Kaneko, T., Tabata, S., Yokoyama, T., Tejima, T., Saeki, K., Oomori, H., Hayashi, M., Maekawa, T., Sriprang, R., Murooka, Y., Tajima, S., Simomura, K., Nomura, M., Suzuki, A., Shimoda, S., Sioya, K., Abe, M., Minamisawa, K., 2004. Expression islands clustered on symbiosis island of Mesorhizobium loti genome. J. Bacteriol. 186, 24392448. Vaishampayan, A., Sinha, R.P., Hader, D.P., Dey, T., Gupta, A.K., Bhan, U., Rao, A.L., 2001. Cyanobacterial biofertilizers in rice agriculture. Bot. Rev. 67, 453516. Venkataraman, G.S., 1993. Blue-green algae (cyanobacteria). In: Tata, S.N., Wadhwani, A.M., Mehdi, M.S. (Eds.), Biological Nitrogen Fixation. Indian Council of Agriculture Research, New Delhi, pp. 4576. Verma, S.K., Singh, S.P., 1990. Factors regulating copper uptake in cyanobacterium. Curr. Microbiol. 21, 3337. Verma, S.K., Singh, S.P., 1995. Multiple metal resistance in the cyanobacterium Nostoc muscorum. Bull. Environ. Contam. 54, 614619. Verrecchia, E., Yair, A., Kidron, G.J., Verrecchia, K., 1995. Physical properties of the psammophile cryptogamic crust and their consequences to the water regime of sandy soils, north-western Negev desert, Israel. J. Arid. Environ. 29, 427437. Vessey, J.K., 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571586. Villacieros, M., Whelan, C., Mackova, M., Molgaard, J., Sanchez-Contreras, M., Lloret, J., 2005. Polychlorinated biphenyl rhizoremediation by Pseudomonas uorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl. Environ. Microbiol. 71, 26872694. Wani, P.A., Khan, M.S., Zaidi, A., 2007. Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70, 3645. Westerdijk, C.E., 2000. Biological Control of Leaf Rot in Lettuce. Volleglonds, Bull, pp. 68. Whitton, B.A., Potts, M., 2000. The Ecology of Cyanobacteria, Their Diversity in Time and Space. Kluwer Academic Publ, The Netherlands.


Wood, N., 2001. Nodulation by numbers: the role of ethylene in symbiotic nitrogen xation. Trend. Plant Sci. 6, 501502. Wu, S.C., Cheung, K.C., Luo, Y.M., Wong, M.H., 2006. Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ. Pollut. 140, 124135. Wu, S.C., Peng, X.L., Cheung, K.C., Liu, S.L., Wong, M.H., 2009. Adsorption kinetics of Pb and Cd by two plant growth promoting rhizobacteria. Bioresour. Technol. 100, 45594563. Wua, B., Caob, S.C., Lib, Z.H., Cheunga, Z.G., Wonga, K.C., 2005. Effects of biofertilizer containing N-xer. P and K solubilizers and AM fungi on maize growth. Geoderma 125, 155162. Yasari, E., Patwardhan, A.M., 2007. Effects of Azotobacter and Azospirilum inoculations and chemical fertilizers on growth and productivity of Canola. Asian J. Plant Sci. 6, 7782. Yazdani, M., Bahmanyar, M.A., Pirdashti, H., Esmaili, M.A., 2009. Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.) World Acad. Sci. Engineer. Technol. 49, 9092. Yee, D.C., Maynard, J.A., Wood, T.K., 1998. Rhizoremediation of trichloroethylene by a recombinant, root-colonizing Pseudomonas uorescens strain expressing toluene ortho-monooxygenase constitutively. Appl. Environ. Microbiol. 64, 112118. Yee, N., Benning, L.G., Phoenix, V.R., Ferris, F.G., 2004. Characterization of metalcyanobacteria sorption reactions: a combined macroscopic and infrared spectroscopic investigation. Environ. Sci. Technol. 38, 775782. Yuen, G.Y., Craig, L.M., Kerr, E.D., Steadman, J.R., 1994. Inuences of antagonist population levels, blossom development stage and canopy temperature on the inhibition of the Sclerotinia sclerotiorum on dry edible bean by Erwinia herbicola. Phytopathology 84, 495501. Zahir, A., Arshad, Z.M., Frankenberger, W.F., 2004. Plant growth promoting rhizobacteria. Adv. Agron. 81, 97168. Zaidi, A., Mohammad, S., 2006. Co-inoculation effects of phosphate solubilizing microorganisms and glomus fasciculatum on green grambradyrhizobium symbiosis. Agric. Sci. 30, 223230. Zaidi, S., Usmani, S., Singh, B.R., Musarrat, J., 2006. Signicance of Bacillus subtilis strain SJ101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64, 991997. Zehnder, G., Murphy, J.F., Sikora, E.J., Kloepper, J.W., 2001. Application of rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107, 3950. Zehnder, G.W., Yao, C., Murphy, J.F., Sikora, E.J., Kloepper, J.W., 2000. Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth promoting rhizobacteria. Biol. Contr. 45, 127137. Zang, S., Moyne, A.L., Redddy, M.S., Kloepper, J.W., 2002. The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol. Contr. 25, 288296. Zhang, S., White, T.L., Martinez, M., McInroy, C., Kloepper, J.A., Klassen, J.W.W, 2010. Evaluation of plant growth-promoting rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol. Contr. 53, 129135. Zulpa, G., Zaccaro, M.C., Boccazzi, F., Parada, J.L., Storni, M., 2003. Bioactivity of intra and extracellular substances from cyanobacteria and lactic acid bacteria on wood blue stain fungi. Biol. Contr. 27, 345348.