Novel plant growth promoting rhizobacteria—Prospects and potential

Applied Soil Ecology 95 (2015) 38–53

Contents lists available at ScienceDirect

Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil

Review

Novel plant growth promoting rhizobacteria—Prospects and potential Hemlata Chauhana , D.J. Bagyaraja,* , G. Selvakumarb , S.P. Sundaramc a

Center for Natural Biological Resources and Community Development (CNBRCD), Bangalore, India Indian Institute of Horticultural Research, Hessaraghatta Lake Post, Bangalore, India c Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, India b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 5 December 2014 Received in revised form 23 May 2015 Accepted 27 May 2015 Available online xxx

Sustainability in agricultural production has emerged as one of the most significant concerns of present times. Commensurate with the present day aversion to the use of chemical fertilizers and pesticides; there is an overt emphasis on use of organic inputs and microbial inoculants which play an important role in sustainable agriculture. Plant growth promoting rhizobacteria (PGPR) are an important group of microbial inoculants that have been studied extensively for their ability to promote plant growth and improve productivity. PGPR operate through either direct or indirect mechanisms or a combination of both, and there by minimize the environmental impact of chemical intensive farming practices. Direct mechanisms of plant growth promotion include the secretion of plant growth promoting metabolites like indole acetic acid (IAA), cytokinins, gibberellins, etc., and facilitating the uptake of essential nutrients (N, P, Fe, Zn, etc.) from the atmospheric air and soil. Indirect promotion of the plant growth occurs when PGPR lessen or prevent the deleterious effect of phytopathogenic organisms by the production of antibiotics, siderophores, hydrogen cyanide (HCN), etc. Well known PGPRs that have reached the stage of commercial success, include Azospirillium, Azotobacter, Bacillus Burkholderia, Pseudomonas, Rhizobium, and Serratia. But there are several novel PGPR on which considerable information is available, but such organisms have not attained commercial scales of production unlike their better known predecessors. PGPRs like Azoarcus, Exiguobacterium, Methylobacterium, Paenibacillus and Pantoea etc., fall in this category. The information available on these novel PGPRs with regard to their biology and utility are discussed in this review. ã2015 Elsevier B.V. All rights reserved.

Keywords: Novel PGPR Azoarcus Exiguobacterium Methylobacterium Paenibacillus Pantoea

Contents 1.

2. 3.

Introduction . . . . . . . . . . . . . . . Azoarcus . . . . . . . . . . . . 1.1. Exiguobacterium . . . . . . 1.2. Methylobacterium . . . . . 1.3. Paenibacillus . . . . . . . . . 1.4. Pantoea . . . . . . . . . . . . . 1.5. Biosafety of novel PGPR strains Conclusion . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . References . . . . . . . . . . . . . . . .

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38 40 41 41 43 45 47 48 48 48

1. Introduction

* Corresponding author. Tel.: +91 9448465368. E-mail address: [email protected] (D.J. Bagyaraj). http://dx.doi.org/10.1016/j.apsoil.2015.05.011 0929-1393/ ã 2015 Elsevier B.V. All rights reserved.

The rhizosphere is a thin zone of soil surrounding the root zone that is immensely influenced by the root system (Hartmann et al., 2008). Compared to the neighbouring bulk soil, this zone is rich in nutrients, due to the accumulation of a variety of organic compounds released by the roots through exudation, secretion

H. Chauhan et al. / Applied Soil Ecology 95 (2015) 38–53

and rhizodeposition. These organic compounds can be used as carbon and energy sources by microorganisms and microbial activity is particularly intense in the rhizosphere. The rhizosphere is therefore home to a variety of root associated bacteria commonly referred to as rhizobacteria. Such beneficial rhizobacteria that positively influence plant growth are referred to as plant growth promoting rhizobacteria (PGPR). The research on PGPR gains significance due to the need for development of eco-friendly and sustainable agriculture practices for feeding a rapidly growing population. Since the excessive use of chemical fertilizers and pesticides pose adverse effects on the environment, it is imperative to devise eco-friendly biological alternatives and use the best management practices in order to reduce the use of chemicals. Kloepper and coworkers coined the term PGPR (plant growth promoting rhizobacteria) in the late 1970’s (Kloepper and Schroth, 1978), and ever since it has been increasingly appearing in publications from around the world. Plant growth promoting rhizobacteria include multiple genera of soil bacteria, which stimulate the growth and development of plants in whose rhizosphere they remain associated for the major part of their life cycle (Saharan and Nehra, 2011; Pandey et al., 2012). The relationship of PGPR with the host may either be restricted to the rhizosphere (some colonize the rhizosphere, rhizoplane, superficial intercellular spaces or dead root cell layers) or endophytic (while some actually reside within apoplastic spaces inside the host plant with or without forming specialized structures such as nodules) (Vessey, 2003). Bashan and Holguin (1998) proposed the division of PGPR into two classes: viz., biocontrol-PGPB (plant growth promoting bacteria) and PGPB but this classification is difficult to follow due to the overlapping features of most PGPR. A more feasible classification of PGPR, is

39

their separation as extracellular (e-PGPR), to denote those existing in the rhizosphere, on the rhizoplane, and intracellular (i-PGPR), to denote bacteria that exist in the spaces between the cells of the root cortex or in specialized nodular structures (Gray and Smith, 2005). PGPR improve plant growth by indirect or direct mechanisms although the difference between the two is not always distinct (Lugtenberg and Kamilova, 2009; Ashraf et al., 2013). Direct mechanisms include the improvement of nutrient availability to the plant by the fixation of atmospheric nitrogen, production of iron chelating siderophores, organic matter mineralization (thereby meeting the nitrogen, sulfur, phosphorus nutrition of plants), and solubilization of insoluble phosphates. Another important direct mechanism involves the production of plant growth hormones and the stress regulating hormone 1-aminocyclopropane -1-carboxylate (ACC) deaminase. Indirect mechanisms include inhibition of microorganisms that have a negative effect on the plant (by niche exclusion) viz. hydrolysis of molecules released by pathogens, synthesis of enzymes that hydrolyze fungal cell walls, synthesis of HCN, improvement of symbiotic relationships with rhizobia and mycorrhizal fungi, and insect pest control (Das et al., 2013). The number of bacterial species identified as PGPR has increased greatly in the recent past due to the increased availability of molecular tools, for the study of various habitats and the revelation of modes of action of various bacterial species. The term PGPR presently encompasses diverse genera from different sources and habitats representing great physiological, functional, ecological and molecular diversity and their absence from one such source/habitat was more likely due to inadequate techniques of isolation and detection.

Fig. 1. The important criteria of novel PGPR that make them good candidates for application and future commercialization.

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H. Chauhan et al. / Applied Soil Ecology 95 (2015) 38–53

Numerous laboratory, greenhouse and field studies are available on the screening and utilization of PGPR for plant growth and a number of PGPR strains have been commercialized. The commercially utilized PGPR strains include species of Agrobacterium, Azospirillum, Azotobacter, Bacillus, Burkholderia, Delfitia, Paenibacillus macerans, Pantoea agglomerans, Pseudomonas, Rhizobium and Serratia (Glick, 2012). However PGPR inoculated crops represents only a small fraction of worldwide agricultural practice. Another issue that needs to be considered here is that many highly efficient strains reported in literature have remained as artifacts of academic value only and have not metamorphosized as commercial products (Bashan et al., 2014). This is due to inconsistent and varied responses obtained in field trials, which are largely influenced by the growing conditions and crop in which they were inoculated. The successful establishment of an introduced bacterial inoculant therefore depends on its survival in soil and the compatibility with the crop on which it is inoculated, besides its interaction with indigenous microflora while several other environmental factors also play an important role in determining the final outcome of the inoculation (Martínez-Viveros et al., 2010). Glick (2012) listed some important aspects to be considered for extensive commercialization of PGPR which include (i) determination of the traits that are most important for efficacious functioning and the subsequent selection of PGPR strains (ii) consistency among regulatory agencies in different countries regarding release in environment and safety issues (iii) better understanding of advantage and disadvantage of using rhizospheric/endophytic bacteria (iv) selection of the strain that works well in a specific environment i.e. those that work in warm and sandy soil versus those that work well in cold and wet environment (v) development of more effective means of application in different setting e.g. nursery versus field (vi) better understanding of the possible interaction between PGPR and soil fungi and host. An ideal PGPR should possess high rhizosphere competence, enhanced plant growth capabilities, ease of mass multiplication, a broad spectrum of action, excellent and reliable biological control activity (wherever applicable), should be safe for environment, should be compatible with other rhizobacteria, and must tolerate desiccation, heat, oxidizing agents and UV radiations (Nakkeeran et al., 2005). Considering the factors discussed above it is quite obvious that the search for functional PGPR inoculants is a dynamic process with ample scope for refinement both in strain selection and inoculant technology. This review will therefore attempt to throw some more light on some novel and lesser utilized PGPR with special reference to the genera Azoarcus, Exiguobacterium, Methylobacterium, Paenibacillus and Pantoea. The most important features of these PGPR that make them potential candidates for application and future commercialization are listed in Fig. 1. 1.1. Azoarcus Azoarcus spp. were originally isolated as endophytic diazotrophs from Kallar grass, an undomesticated C4 plant highly tolerant to soil salinity, alkalinity and water lodged conditions, and widely distributed in tropical to subtropical regions ranging from Australia to Africa. In the Punjab province of Pakistan, it grows as a pioneer plant on saline-sodic, alkaline soils having low fertility (Sandhu and Malik 1975). It grows luxuriantly without the addition of any nitrogenous fertilizer, giving harvests of 20–40 metric tons of hay per ha per year (Sandhu et al., 1981). Though it is associated with several nitrogen-fixing bacteria (Zafar et al., 1987), the diazotrophs that predominate inside the roots were Gramnegative rods which could not be assigned to any previously described taxa and thus a new genus Azoarcus was proposed consisting of two named species, viz., Azoarcus communis and Azoarcus indigens and three additional unnamed groups which

were also distinct at the species level (Reinhold-Hurek et al., 1986; Reinhold-Hurek et al., 1993a). Three new genera viz., Azovibrio restrictus, Azospira oryza and Azonexus fungiphilus were added later (Reinhold-Hurek and Hurek, 2000). Plant associated species of these genera could not be isolated from root free soil as yet or do not survive well in soil. They appeared to be tightly associated with and ecologically dependent on plants (Reinhold-Hurek and Hurek, 1998). Some additional species of Azoarcus, such as Azoarcus tolulyticus (Zhou et al., 1995) or Azoarcus evansii (Anders et al., 1995) and other strains do not originate from living plants but mostly from soil or sediments and are mostly localized in a separate clade within the genus Azoarcus based on phylogenetic analysis of 16S rDNA sequences (Reinhold-Hurek and Hurek, 2000) and most of them are capable of degrading aromatic compounds such as toluene or phenol (Song et al., 1999; Zhou et al., 1995), benzoate (Anders et al., 1995) or resorcinol (Springer et al., 1998) under anoxic conditions. Immunofluorescence microscopy confirmed the localization of the Azoarcus to the intercellular spaces (aerenchyma) in the roots of the plant (Reinhold et al., 1987). Azoarcus enters the roots through wounds, where lateral roots emerge between epidermal and cortical cells. They also appear to occasionally invade the outer cells of undifferentiated root tissue or epidermal cells by passing through the outer tangential longitudinal wall (Reinhold and Hurek, 1988). Hurek et al. (1994) using immunocytochemical localization by light and electron microscopy in combination with histochemical localization of a reporter gene expression confirmed that Azoarcus sp. BH72 can colonize and invade roots of Kallar grass and rice (Oryza sativa) seedlings in a similar pattern in gnotobiotic culture, without causing symptoms of plant disease despite its endophytic growth. Later evidences that Azoarcus sp. may occur in natural association with rice plants were also reported (Hurek et al., 1997). Reinhold-Hurek et al. (1993b) have detected two types of cellulolytic enzymes in Azoarcus sp. BH72, an exoglucanase, which has cellobiohydrolase and glucosidase activity on 1,4-cellooligosaccharides, and a wide substrate spectrum including xylosides. The other enzyme is an endoglucanase, which attacks oligosaccharides larger than cellobiose and releases larger oligomers from substrates such as carboxymethylcellulose. The enzymes are not efficiently excreted into the culture supernatant, but remain bound to the cell surface (Reinhold-Hurek et al., 1993b). The degradation products of this enzyme system are not metabolized by Azoarcus sp. BH72, which neither grows on cellulose, cellobiose nor glucose or any other carbohydrate. This property differentiates it from plant pathogens and is responsible for the less aggressive attack of plant cells by these endophytes. Low O2 concentrations are essential for N2 fixation by the strictly aerobic Azoarcus spp. (Hurek et al., 1987). Transcriptional fusion study using gfp-nif HDK by Egener et al. (1998) revealed that nif genes can be expressed even when the bacteria are inside plant cells and not repressed by plant cell component of combined nitrogen. Immunogold labeling with Azoarcus specific antibodies showed high nitrogenase gene expression in cortex of rice roots (Egener et al., 1999). However, these studies did not prove whether Azoarcus strain BH 72 is capable of contributing significant amount of fixed nitrogen to its host plant and whether Azoarcus is the predominantly active N2- fixing endophyte in its host plant. The contribution of Azoarcus to its host plant was demonstrated by Hurek et al. (2002) by evaluating inoculated plants grown in green house and uninoculated plants from natural environment. Similar to most diazotrophs, the structural genes viz., nif H,D and K are localized in one operon (Egener et al., 2001); however a ferredoxin gene which is apparently involved in electron transport to the nitrogenase is localized on the same transcript (Egener et al., 2001). Several major proteins of the regulatory cascade have been cloned and characterized and their role partially elucidated: such as

H. Chauhan et al. / Applied Soil Ecology 95 (2015) 38–53

three different PII-like proteins (encoded by glnB, glnK, glnY) (Martin et al., 2000; Martin and Reinhold-Hurek 2002), putative ammonium transporters (encoded by amtB, amtY) (Martin et al., 2000), and the regulatory proteins NifA and NifL (Egener et al., 2002). Azoarcus strain BH 72 colonized the interior of rice (Hurek et al., 1994) and wheat (Triticum aestivum) (Wieland and Fendrik 1998) under laboratory conditions. Stein et al. (1997) showed it was able to colonize and contribute fixed nitrogen to sorghum (Sorghum vulgare cv. Beefbuilder) when inoculated in vitro. This genus has not received the attention of the bio-inoculant industry. Therefore it would be appropriate to further intensify research on more field trials and for bio-inoculant formulations using Azoarcus strains. Azoarcus sp. strain BH 72 can work as a model for nitrogen fixing grass endophytes. The complete genome of this bacterium was sequenced and a representative physical map with a high density of marker genes was developed in which 64 aligned BAC clones were able to cover the entire genome (Battistoni et al., 2005). The complete genome (4376,040-bp long and contains 3992 predicted protein-coding sequences) revealed that the coding sequences involved in the synthesis of surface components were more closely related to those of plant-associated bacteria rather than plant pathogenic bacteria. It has only a few enzymes that degrade plant cell walls, lacks type III and IV secretion systems, related toxins and an N-acyl homoserine lactones–based communication system that is typically used by pathogens. The genome contained remarkably few mobile elements, indicating a low rate of recent gene transfer that is presumably due to adaptation to a stable, low-stress microenvironment (Krause et al., 2006). Transcriptional profiling cells of strain BH 72 grown microaerobically on N2 versus ammonium revealed that the expression of 7.2% of the genes was significantly up-regulated, and 5.8% down-regulated upon N2 fixation, respectively. In addition to modulation of genes related to N2 fixation, the expressions of gene clusters that might be related to plant-microbe interaction and of several transcription factors were significantly enhanced (Sarkar and Reinhold-Hurek, 2014).

1.2. Exiguobacterium The genus Exiguobacterium was first described by Collins et al. (1983) with the type species Exiguobacterium aurantiacum. At present it comprises 13 species (Euzeby, 1997; further updates available at http://www.bacterio.net) viz., E. acetylicum formerly identified as Brevibacterium acetylicum, E. aestuarii, E. antarcticum, E. aquaticum, E. artemiae, E. indicum, E. marinum, E. mexicanum, E. oxidotolerans, E. profundum, E. sibiricum, E. soli and E. undae (http:// www.bacterio.net). Isolates of this genus are of low G + C content, gram-positive, facultative anaerobes with high morphological and geographical diversity. Exiguobacterium strains have been isolated or detected by cultivation independent techniques in a wide range of habitats including cold and hot environments with temperatures ranging from
12 to 55  C, and include psychrotrophic, mesophilic, and moderately thermophilic species and strains (Vishnivetskaya and Kathariou, 2005). The cell morphology ranges from ovoid, rods, double rods, or chain of cells depending on species, strain, and environmental conditions (Vishnivetskaya et al., 2007). Exiguobacterium isolates have been reported from hot springs in Yellowstone National Park (Knudston et al., 2001), potato stems in Austria (Reiter et al., 2002), glacial ice core samples in Greenland (Miteva et al., 2004) and the Siberian permafrost environment (Rodriguez et al., 2006). Vishnivetskaya et al. (2009) analysed 24 isolates from extremely different environment using different molecular approaches and suggested that they form two distinct divisions according to their growth temperatures thereby making them model organisms for the investigations on molecular adaptations to the growth habitat.

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Exiguobacterium strains have been reported to produce enzymes such as alkaline proteases, alkali tolerant esterase, dehydrogenase (Kasana and Yadav 2007; Hwang et al., 2005; Wada et al., 2004) and those involved in the biodegradation of azo dyes (Saratale et al., 2011), diesel (Mohanty and Mukherji, 2008) and bioremoval of chromium and arsenic (Okeke, 2008; Anderson and Cook, 2004). Some strains are known to improve the development of Artemia, a crustacean (Hipolito-Morales et al., 2009). A few strains are reported to have plant growth promoting properties. In one of the earliest research of its agro-utility, Exiguobacterium has been reported to suppress fungal diseases of cereal crops in Australia (Barnett et al., 2006). Selvakumar et al. (2009), isolated a cold tolerant Exiguobacterium acetylicum strain from the North Western Himalayas of India, this strain inhibited the growth and development of the plant pathogens Rhizoctonia solani, Sclerotium rolfsii, Pythium sp. and Fusarium oxysporum under in vitro conditions. It also improved the germination and early growth parameters of pea in the presence of R. solani and S. rolfsii under pot culture conditions. A few strains are reported to have plant growth promoting properties. Further it is also been reported to increase the growth and nutrient uptake of wheat seedlings under glass house conditions (Selvakumar et al., 2010). Phosphate solubilizing Exiguobacterium strains were isolated from acidic soils of Argentina (Collavino et al., 2010) and paddy fields of Eastern Uttar Pradesh in India (Kumar et al., 2010). Phosphate solubilizing and antagonistic Exiguobacterium strains isolated from Western Ghats of India are reported to increase growth and biomass of cowpea under green house conditions (Dastager et al., 2010). The presence of Exiguobacterium was also observed in the root nodules of fenugreek (Trigonella foenum-graecum) by Rajendran et al. (2012). A halotolerant PGPR Exiguobacterium oxidotolerans was isolated by Bharti et al. (2013). This strain has been reported to improve yield and bacoside-content in the medicinal plant Bacopa monnieri under salt stress. It also alleviated the negative effects of salinity in Mentha arvensis in a glass house study at salinity levels of 100 and 300 mM NaCl (Bharti et al., 2014). Exiguobacterium acetylicum inhibiting the growth and development of several plant pathogenic fungi and bacterial pathogens of clinical significnce was reported by Azizollahi Aliabadi et al. (2014). Exiguobacterium profundum occurring as an endophyte in Amaranthus spinosus was observed recently by Sharma and Roy (2015). The complete genome sequencing of Exiguobacterium strain MH3, isolated from the rhizosphere of Lemna minor revealed the presence of many stress tolerance related genes including putative genes encoding a regulon for high affinity phosphate uptake, carbon starvation, oxidative stress, detoxification, and cold and heat shock proteins. Genes related to auxin biosyntheis, siderophores and iron metabolism have also been identified in the genome of this bacterium (Tang et al., 2013). The genome analysis of ten Exiguobacterium strains isoalted from various environments by Vishnivetskaya et al. (2014) have revelaed a whole arsenal of stress responsive genes including the two most abundant transposase families, transposase/inactivated derivatives and IS605 (orfB), in all strains. The strains contained two to seven cold shock protein genes (COG1278), one molecular chaperone GrpE (heat shock protein, COG0576), one ribosome associated heat shock protein (S4 paralog, COG1188), three chaperonin GroEL (HSP60 family, COG0459), three cochaperonin GroES (HSP10, COG0234), and four fatty acid desaturase (COG3239) genes per strain. 1.3. Methylobacterium The genus Methylobacterium was first proposed by Patt et al. (1974) to accommodate the methane utilizing Methylobacterium

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organophilum. It was later emended by Green and Bousfield (1983) to accommodate the non-methane utilizing pink pigmented facultatively methylotrophic (PPFM) strains. The genus Methylobacterium comprises of a number of PPFM species, which can utilize one-carbon compounds such as formate, formaldehyde and methanol as the sole source of carbon and energy as well as on a wide range of multi carbon growth substrates. Members of this genus are Gram-negative, strictly aerobic, rod shaped bacteria and most species within this genus are red to pink due to the presence of carotenoids. So far 49 valid species have been added in this genus (Euzeby, 1997; further updates available at: http://www.bacterio.net). Methylobacterium is widely distributed in a variety of habitats (Green and Bousfield, 1983) including soil, fresh water, lake sediments, leaf surfaces, nodules, rice grains, atmospheric air and hospital environments. Recent additions to this group of methanol utilizing bacteria include Enterobacter arachidis, Methylobacterium oryzae and M. phyllosphaerae isolated from the rhizosphere and phyllosphere of groundnut and rice respectively (Madhaiyan et al., 2007a, 2009; Poonguzhali et al., 2008). PPFMs have been isolated from virtually all land plants examined (Corpe, 1985). The association of Methylobacterium with plants has been reported by various workers with different species colonizing roots, leaf surfaces and buds (Lidstrom and Chistoserdova, 2002). In plants, the phyllosphere is the major site from where most of the isolates were obtained (Knief et al., 2008; Madhaiyan et al., 2007a, 2009) or detected by culture independent techniques (Delmotte et al., 2009). However, the composition of the Methylobacterium communities on phyllosphere varies at different sampling sites, or even amongst different plant species

within the same sampling site (Knief et al., 2008, 2010a). Although, they do not grow as rapidly as other phylloplane bacteria on multicarbon sources, they compete well with other phyllospheric bacteria for leaf surface colonization. Utilizing mutants in the pathway for one-carbon metabolism of Methylobacterium together with wild type, Sy et al. (2005) demonstrated that methylotrophy is advantageous to the bacterium colonizing Medicago truncatula under competitive and non-competitive conditions. The methylotrophic deficient mutants as well as wild type were able to colonize the plants which indicated that methanol was not the only carbon source available to Methylobacterium when it is associated with the plant. PPFMs, however, are not limited only to the phylloplane and are also associated with other parts of the plant, concentrated at the actively growing portions. The Phy R protein was reported to play an essential role in plant colonization. It is part of a key regulator for adaptation to epiphytic life of Methylobacterium (Gourioin et al., 2006). Raja et al. (2008) used culture dependent molecular and metabolic techniques to study the phyllosphere methylotrophs in sunflower (Helianthus annuus), maize (Zea mays), soybean (Glycine max) and fenugreek plants and reported that diversity of Methylobacterium in the phyllosphere depends upon the host plant species. Knief et al. (2010b) reported that colonization efficiency of the strains in the model plant Arabidopsis thaliana was linked to their phylogeny rather than their geographical origin or plant host. Methylobacterium tardum and Methylobacterium extorquens were found to be the most competitive colonizers. So far, the species associated with plants are M. extorquens and M. fujisawaense from phyllosphere (Abanda-Nkpwatt et al., 2006; Madhaiyan et al., 2006a), M. populi associated with internal tissues of

Table 1 Plant growth promotion by Methylobacterium species. Plant growth promotion effect

Methylobacterium species

ACC deaminase production and Methylobacterium fujisawaens plant growth promotion Antagonistic effect against phytopathogens

Methylobacterium mesophilicum,M. extorquens

Better shelf life and stress abatement

Methylobacterium oryzae CBMB20/ Methylobacterium suomiense CBMB120 strains withAzospirillum brasilense(CW903) strain M. mesophylicum Methylobacterium spp.

Enhanced iron translocation Ethylene emission and pathogenesis related proteins synthesis Improved nodulation Methylobacterium oryzae Increased dry biomass and Methylobacterium oryzae strain CBMB20 macro nutrient accumulation Increased growth, nutrient Methylobacterium spp., M. oryzae uptake and yield M. oryzae Methylobacterium oryzae Increased mycorrhizal colonization and spore numbers Induce systematic resistance Methylobacteriumsp.,Methylobacterium against plant pathogens oryzae Nitrogenase activity Methylobacteriumsp. strain NPFM-SB3; Methylobacterium oryzae CMB20 Production of plant growth Methylobacteriumsp. regulators, increased seed vigour index, and seed germination Methylobacterium sp., M. oryzae Reduction in heavy metal toxicity Tissue cultured plantlets Methylobacterium sp.

Crop

References

Canola, rice

(Madhaiyan et al., 2006b,c; Madhaiyan et al., 2007a,b,c; Chinnadurai et al., 2009; Krishnamoorthy et al., 2011) Maize (Xanthomonas camprestris, Pseudomonas (Romanovskaya et al., 2001) syringae, Erwinia carotovora, Clavibacter michiganense, andAgrobacterium tumefaciens) (Joe et al., 2014) Tomato

Broad bean and corn Tomato

(Bishop et al., 2011) (Yim et al., 2013)

Soybean Maize and sorghum-sudangrass hybrid

(Parthiban et al., 2012) (Kim et al., 2014)

Cotton, sugarcane, rice, red pepper

(Madhaiyan et al., 2006c, 2010; Lee et al., 2011; Kim et al., 2014)

Red pepper

(Kim et al., 2010)

Ground nut, rice (Rhizoctonia solani, Pseudomonas syringae) Rice

(Madhaiyan et al., 2004a,b, 2006b; Indiragandhi et al., 2008) (Senthilkumar et al., 2009a; Lee et al., 2006) (Lee et al., 2006 2006)

Red pepper and tomato, rice

Tiny wild mustard Enhanced flavour biosynthesis in strawberry and morphogenesis of Triticum aestivum

(Idris et al., 2004; De Marco et al., 2004; Madhaiyan et al., 2007b) (Shirokikh et al., 2007; Zabetakis et al., 1997 Kalyaeva et al., 2003)

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poplar tree (van Aken et al., 2004), M. nodulans ORS2060 nodulating Crotalaria glaucoides (Jourand et al., 2004), and M. goesingense associated with Thlapspi goesingense (Idris et al., 2006). Methylobacterium benefits plants in several ways. In the phyllosphere it acts synergistically, utilizing methanol from leaves as the sole source of carbon and energy and in exchange may produce phytohormones (Madhaiyan et al., 2005). Increase in plant growth and germination improvement by production of cytokinins (Madhaiyan et al., 2005) and auxins (Omer et al., 2004) have been reported for different Methylobacterium strains. The other mechanisms by which Methylobacterium affect plants is by the regulation of the levels of the stress hormone ethylene, by the production of enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase, a pyridoxal 5-phosphate-dependent enzyme that converts ACC to a-ketobutyrate and ammonium. ACC is the precursor of ethylene and is converted to ethylene by ACC oxidase. Ethylene can either promote and inhibit plant growth depending on the cell type, plant species and stress conditions (Vriezen et al., 1999). Lowering of ethylene levels in the plant root facilitates root elongation under stress conditions (Glick et al., 1998). The presence of acc D gene was also confirmed in the rice originating Methylobacterium strains and they showed 98% similarity to the acc D gene of Rhizobium leguminosarum suggesting the possibility of horizontal gene transfer (Chinnadurai et al., 2009). The property of nitrogen fixation has also been attributed to Methylobacterium spp. (Jourand et al., 2004; Raja et al., 2006). Methylobacterium strains with nif H gene were isolated from nodules of Lotononis bainesii a shrubby legume in Africa (Jaftha et al., 2002; Yates et al., 2007). These isolates were not able to grow on methanol; however this did not inhibit their colonization or symbiosis (Ardley et al., 2009). Nitrogen fixing and nodule forming Methylobacterium spp. were isolated from nodules of the legumes Crotalaria glaucoides, Crotalaria perrottetii and Crotalaria podocarpa and the species M. nodulans sp. nov. was proposed by Jourand et al. (2004) to accommodate these novel methylotrophs under the broad umbrella of rhizobia. Raja et al. (2006) isolated nitrogen fixing but non-nodulating Methylobacterium strain. The relationship of M. nodulans with C. podocarpa is symbiotic as it is specifically nodulated by M. nodulans. The molecular signals in this association was studied by Renier et al. (2008) who reported that the flavonoid apigenin was the strongest inducer of nod gene expression and the Nod factor structure was composed of a pentamer of chitin substituted by C18:1 or C16:0 acyl chain on the non-reducing end and 6-O-sulphated on the other end. The ability of methylotrophs to oxidize sulphur was first reported in Methylobacterium oryzae CBMB 20, followed by Methylobacterium goesingense CBMB 5 and Methylobacterium fujisawaense CBMB 37 (Anandham et al., 2009), thereby opening up another exciting avenue for meeting the nutritional requirements of crop plants. Methylobacterium strains have been suggested to contribute to the flavor of strawberries by enhancing flavor components, such as 2,5-dimethyl-4-hydroxy-2H-furan-3one (DMHF) (Nasopoulou et al., 2014) and 2,5-dimethyl-4methoxy-2H-furanone in vitro (Verginer et al., 2010; Zabetakis, 1997); but it has not received a proportionate interest from the point of commercial utilization. Some of the reported instances of plant growth promotion by Methylobacterium species are presented in Table 1. The genome of Methylobacterium sp. has been sequenced and publicably accessible in the NCBI data base (Vuilleumier et al., 2009). Insights into the Methylobacterium genome have revealed the presence of genes encoding several unusual characteristics. In a study with the complete genome sequences of six methylobacterial strains, Marx et al. (2012), annotated the gene clusters that enable methanol oxidation that is activated during plant-

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methylotrophic bacterium interaction and found that the pqqA gene, which is not essential for C1 growth, is missing, and mxaF, which is essential for C1 growth, is duplicated in this genus. This observation was confirmed by Almeida et al. (2013), with the Methylobacterium mesophilicum strain SR1.6/6 isolated from Citrus sinensis. The draft genome sequence of Methylobacterium strain L24, a leaf associated endophytic bacterium isolated from Jatropa curcas by Madhaiyan et al. (2014), revealed that the strain possesses a conserved cluster of genes associated with photosynthesis, including genes encoding the light-harvesting complex and the reaction center, and genes involved in biosynthesis of bacteriochlorophyll (bch) and carotenoids. Several genes involved in metabolic pathways that may contribute to the promotion of plant growth, including genes for the production of auxin biosynthesis, zeatin (miaA), cobalamin synthesis protein (cob), urea metabolism (ureABCDEFG), biosorption of heavy metals or decrease of metal toxicity, endoglucanase (celC), phytase, C-P lyase system (phn), pyrroloquinoline quinone biosynthesis protein (pqqABCDE), methylotrophy gene clusters (mxa) and the gene coding for the 1-aminocyclopropane-1- carboxylate deaminase (acdS) gene were observed in this strain indicating its possible utility in plant growth promotion even under stress conditions. 1.4. Paenibacillus The genus Paenibacillus was proposed by Ash et al. (1993) to accommodate the members of “group 3” within the genus Bacillus with Paenibacillus polymyxa as type species Group ‘30 bacilli comprises over 30 facultative anaerobes and endospore-forming, neutrophilic, periflagellated, heterotrophic, low G + C content, Gram-positive Bacillus species. “Group 3” bacilli are only remotely related to B. subtilis, the type species of the genus Bacillus and represent a phylogenetically distinct group and exhibit high intragroup sequence relatedness on the basis of comparative 16S rRNA sequence analysis. Phenotypically, species of this group react weakly with Gram stain and even young cultures appear Gramnegative. They differentiate into ellipsoidal spores which distinctly swell the mother cell. The combination of morphology and physiology is sufficient to distinguish rRNA “group 3” bacilli from all other mesophilic Bacillus spp. Collins et al. (1994) proposed the transfer of Clostridium durum to Paenibacillus as Paenibacillus durum. Taxonomically it falls in the family Paenibacillaceae of phylum Firmicutes. So far 148 species are included in the genus Paenibacillus (Euzeby 1997; further updates available at www. bacterio.net). Paenibacillus spp. are metabolically diverse and can inhabit different habitats such as soils, roots, and rhizosphere of various crop plants including wheat (Triticum aestivum), maize (Zea mays), sorghum (Sorghum vulgare), sugarcane (Saccharum officinarum) and barley (Hordeum vulgare), and forest trees such as lodgepole pine (Pinus contorta), douglas fir (Pseudotsuga menziesii), marine sediments etc. (von der Weid et al., 2000; Guemouri-Athmani et al., 2000; Ravi et al., 2007) and even extreme environments or in association with AM hypha (Saha et al., 2005). Few studies on the diversity of Paenibacilus have been carried out. Guemouri-Athmani et al. (2000) reported that the long-term cultivation of wheat in Algerian soils (>70 years) seems to modify rhizospheric populations of P. polymyxa by increasing their size, reducing their diversity, selecting a dominant genotype, and increasing the proportion of nitrogen fixers. Later da Mota et al. (2005) developed a specific PCR-DGGE system based on rpoB as molecular marker and studied the diversity of Paenibacillus species in the rhizosphere of four different cultivars of maize sown in different soils. The Paenibacillus DGGE fingerprints showed a clear distinction between communities of Paenibacillus in forest and Cerrado soils, and rhizosphere samples clustered along Cerrado soil. The

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advantage of rpo based DGGE over 16S rRNA based phylogenetic analysis is that sometimes more than one copy of 16S rRNA is found in genome of some Paenibacillus species making the profile difficult to interpret (da Silva et al., 2003). Paenibacillus spp. possess several properties which help in growth promotion. A plant growth promoting compound similar to IAA in activity was reported to be produced by P. polymyxa and was suggested to stimulate growth in crested wheatgrass (Agropyron cristatum) (Holl et al., 1988). It also released iso-pentenyladenine and an unknown cytokinin-like compound during its stationary phase of growth (Timmusk et al., 1999). Cytokinin is known to promote seed germination, de novo bud formation and release of buds from apical dominance, stimulation of leaf expansion and reproductive development and retardation of senescence (Mok, 1994), some of which were reported in wheat by Lindberg and Granhall (1986) when inoculated with P. polymyxa. P. polymyxa strains isolated from different proximities to wheat roots produced auxins and other indolic and phenolic compounds viz. indole-3- ethanol, indole-3lactic, carboxylic and benzoic acid (Lebuhn et al., 1997). The effect of inoculation with P. polymyxa on growth parameters of wheat and spinach (Spinacia oleracea) plants and the activities of enzymes present in the leaves of these plants such as glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, glutathione reductase and glutathione S-transferase have been observed (Cakmakci et al., 2007). The nitrogen fixing ability of P. polymyxa was demonstrated by Guemouri-Athmani et al. (2000) using acetylene reduction assay. P. azotofixans ATCC 35681 has been reported to be a very efficient nitrogen-fixing bacterium (Seldin and Penido, 1986). Other nitrogen fixing species of the genus are Paenibacillus borealis, P. brasilensis, P. graminis, Paenibacillus macerans, P. odorifer and Paenibacillus peoriae strain NRRLBD-62, (von der Weid et al., 2002), P. donghaensis, P. forsythiae, P. massiliensis, P. riograndensis, P. sabinae, P. sonchi, P. wynnii, and P. zanthoxyli (Beneduzi et al., 2010). Nitrogen fixation has been demonstrated in P. jamilae and P. stellifer isolated from rhizosphere of different plants and a novel nif H gene has been detected in P. stellifer from China by Jin et al. (2011). The Paenibacillus spp. containing nif H gene were detected by the culture independent approach in the rhizosphere of sorghum. N fertilization slightly influenced the nif H gene containing Paenibacillus community suggesting the possible role of nitrogen fixation by Paenibacillus (Coelho et al., 2009). Co-inoculation of P. polymyxa with Rhizobium tropici resulted in higher nodule

leghaemoglobin concentration, nitrogenase and nitrogen fixation efficiency in common bean (Phaseolus vulgaris) (Figueiredo et al., 2008). Bal and Chanway (2012) using 15N assays, reported that over 50% of foliar nitrogen of lodgepole pine (Pinus contorta) is derived from newly fixed N after inoculation with an endophytic Paenibacillus strain. Another interesting fact of Paenibacillus was reported by Timmusk and Wagner (1999) who proposed that natural isolates of P. polymyxa induce drought tolerance and antagonize pathogens in the model plant Arabidopsis thaliana. These effects were observed both in a gnotobiotic system and soil (Timmusk et al., 2003). There are a few instances of Paenibacillus inoculation having negative effect on plant growth and development. A. thaliana plants (under both biotic and abiotic stress conditions), when inoculated with P. polymyxa recorded a 30% reduction in plant growth, and a stunted root system, compared to non-inoculated plants. This indicates a possible mild pathogenic effect (Timmusk and Wagner. 1999; Timmusk et al., 2003). This suggests the need for more investigations to prove this pathogenic effect. Studies on the root colonization process were done to understand the relationship between the beneficial and harmful effects of P. polymyxa on A. thaliana by Timmusk et al. (2005), who studied colonization of plant roots by a natural isolate of P. polymyxa tagged with a plasmid-borne gfp gene. It was observed that the bacterium predominantly colonized the root tip, where it formed a biofilm. Later it was hypothesized that biofilm formation and niche exclusion are possible mechanisms for the antagonistic abilities of Paenibacillus (Timmusk et al., 2009). Paenibacillus spp. also shows nematicidal activies under in vitro and green house conditions. Exposure of the root-knot nematode, Meloidogyne incognita to various concentrations of culture filtrates of Paenibacillus polymyxa GBR-1 under in vitro conditions significantly reduced egg hatching, juvenile mortality, root galling and nematode population, while increasing plant growth and rootmass production in tomato (Solanum lycopersicum) (Khan et al., 2008). Similarly inoculation of P. polymyxa alone or together with Rhizobium increased lentil (Lens culinaris) plant growth both in M. javanica inoculated and uninoculated lentil plants (Siddiqui et al., 2007). Combined inoculation of Paenibacillus polymyxa and Paenibacillus lentimorbus was found to suppress the disease complex caused by root-knot nematode and wilt fungus Fusarium, but improved plant growth under pot culture conditions (Son et al., 2009).

Table 2 Antagonistic activity of Paenibacilus species against plant pathogens. Paenibacillus species

Antagonistic action

Crop

References

Paenibacillus brasilensis PB177

Inhibition of Fusarium moniliforme and Diplodia macrospora Alleviates the effect of Phytophthora capsici infection Biocontrol activity against Fusarium oxysporum f. sp. ciceri, improved seed germination, plant height, number of pods/plant, and seed dry weight Suppression of Pythium aphanidermatum and increased growth inhibition of Ralstonia solanacearum Antagonistic activity against Gaeumannomyces graminis var. tritici, Fusarium oxysporum, control of damping off, Phytophthora blight and wilt disease,

Maize

(von der Weid et al., 2005)

Capsicum

(Jung et

Chick pea

(Das Gupta et al., 2006)

Cucumber, tomato

(Li et al., 2007, 2010a).

Paenibacillus illinoisensis Paenibacillus lentimorbus NRRL B30488 P. macerans and Paenibacillus sp.

Wheat, sesame, cucumber, chilli pepper, watermelon Paenibacillus sp. BRF-1 Control of brown stem rot by Phialophora gregata Soybean Paenibacillus sp. HKA-15 Antifungal activity against Rhizoctonia bataticola, Soybean Macrophomina phaseolina and Fusarium udam Production of antimicrobial compounds, P. elgii, P. lentimorbus,P. polymyxa Several crops E681, P. polymyxa JSa-9, P. polymyxa biopreservatives, enzymes and polysaccharides strain OSY-DF, P. polymyxa strain SQR-21 Paenibacillus polymyxa

al., 2006)

(Heulin et al., 1994; Ryu et al., 2006; Zhang et al., 2008; Kim et al., 2009; Wu et al. 2009)

(Zhou et al., 2008) (Senthilkumar et al., 2009b) (Choi et al., 2007; Kurusu et al., 1987; Kajimura and Kaneda, 1996, 1997; Beatty and Jensen, 2002; Karpunina et al., 2003; He et al., 2007; Raza et al., 2010; Canova et al., 2010; Wu et al. 2010; Deng et al., 2011)

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Paenibacillus spp. is also known to elicit the induced systemic resistance (ISR) in plants. Timmusk and Wagner (1999) reported that natural isolates of P. polymyxa B2 induce changes in Arabidopsis thaliana gene expression and confer significant resistance to the plant pathogen Erwinia carotovora upon challenge inoculation. Several P. polymyxa isolates have been shown to induce resistance to plant pathogens viz., Phytophthora palmivora and Pythium aphanidermatum that cause damping-off in Arabidopsis thaliana (Timmusk et al., 2003). The antagonistic activity of different species of Paenibacillus has been studied by several workers (Table 2). Paenibacillus illinoisensis inoculation changed the composition of pathogenesis related proteins in leaves of pepper (Capsicum annuum) plants infected with Phytophthora capsici (Jung et al., 2005). The Paenibacillus spp. was also reported to produce siderophores under decresased iron levels and solubilize insoluble phosphates. (Raza and Shen, 2010; Jisha and Alagawadi, 1996). Paenibacillus spp. have been found to be associated with ectomycorrhizal and arbuscular mycorrhizal (AM) fungi (Poole et al., 2001; Giese et al., 2002). Paenibacillus validus (DSM ID617 and ID618) stimulated the growth of the AM fungus Glomus intraradices, and led to the formation of fertile spores, which recolonized carrot roots (Hildebrandt et al., 2006). Li et al. (2008) reported that different species of Paenibacillus differentially affect cucumber mycorrhizal fungi Glomus intraradices or Glomus mosseae. Paenibacillus polymyxa and P. macerans were reported to suppress the AM fungus Glomus intraradices in the rhizosphere of cucumber plants in a greenhouse experiment by Larsen et al. (2009). Eastman et al. (2014) reported that only three strains of P. polymyxa genomes, those of P. polymyxa E681 (NC_014483), P. polymyxa SC2 (NC_014622), P. polymyxa M1 (NC_017542) have been completely sequenced. They investigated genome sequence of P. polymyxa CR1, PGPR isolated from the corn rhizosphere exhibiting potential for biocontrol and biomass degradation. This strain contained one circular chromosome of 6,024,666 bp with 5283 coding sequences (CDS), 87 tRNAs, and 12 rRNA operons. Li et al. (2014) reported complete genome sequence of Paenibacillus polymyxa SQR-21, a PGPR with antifungal activity and rhizosphere colonization ability isolated from watermelon rhizosphere. The complete genome of P. polymyxa SQR-21 revealed that it is composed of a 5,828,438-bp circular chromosome, with a mean GC content of 45.64%. Several genes involved in plant growth promotion, including genes responsible for production of indole-3-acetic acid (IAA), 3-hydroxy-2-butanone (acetoin), and 2,3butanediol, as well as phytase, were identified in the SQR21 genome. Also the genome harbors a set of genes encoding extracellular enzymes involved in the degradation of plant-derived polysaccharides, which includes xylanase, glucanase, and chitinase. The authors concluded that the genome sequence provides useful information for both basic and applied research, which also facilitates the understanding of the functions and evolutions of P. polymyxa genome. 1.5. Pantoea Genus Pantoea was proposed by Gavini et al. (1989) to separate Enterobacter agglomerans/Erwinia herbicola from the genera Enterobacter and Erwinia, with Pantoea agglomerans as the type species (Grimont and Grimont, 2005). Brenner et al. (1984) separated 124 strains belonging to Erwinia herbicola–Enterobacter agglomerans complex into 13 groups based on their DNA–DNA hybridization relatedness in order to clarify their position. In the years following Brenner’s hybridization study, many of the 13 DNA hybridization groups (HG) were further investigated and classified as novel species or novel genera. DNA HG XIII and DNA HG III were transferd

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to the novel genus Pantoea as Pantoea agglomerans and Pantoea dispersa, respectively (Gavini et al., 1989). Consequently many more species were added to the genus Pantoea by various workers. Brady et al. (2010) emended the description of the genus with addition of few new species. Strains of the genus are Gram-negative, non-spore-forming, facultatively anaerobic, non-encapsulated, straight rods. Some strains form symplasmata. The G + C content of the DNA ranges from 52.7 to 60.6 mol%. At present 22 species are included in the genus viz., P. agglomerans, P.allii, P. ananatis, P. anthophila, P. brenneri, P. calida, P. citrea, P. conspicua, P. cypripedii, P. deleyi, P. dispersa, P. eucalypti, P. eucrina, P. gaviniae, P. punctata, P.rodasii, P. rwandensis, P. septica, P. stewartii, P. terrea, P. vagans, P.wallisii, P. wallisii, (Euzeby, 1997; further update available at http://www. bacterio.net). Pantoea spp. have been isolated from aerial surfaces of plants, within healthy plant tissues, seeds, fruits, rhizosphere, water, papermill-process water, soil, decaying wood, from humans (urine, blood, wounds, and internal organs) and other animals. They are rarely considered to be pathogens; however, a pathogenic role in humans has been assigned in some instances (Grimont and Grimont, 2005). Pantoea has been widely known as a biological control agent both in pre and post harvest stages. P. agglomerans (CPA-2) was reported to control postharvest disease caused by Penicillium expansum, Botrytis cinerea and Rhizopus stolonifer in a semicommercial trial on Golden Delicious apples (Malus domestica) against Penicillium digitatum and against Penicillium italicum in pear (Pyrus communis) (Nunes et al., 2001, 2002). Competition for nutrients was reported to be the mechanism of the antagonistic activity of P. agglomerans CPA-2 but no evidence was found for a possible role of antibiosis or induced systemic resistance (Poppe et al., 2003). Torres et al. (2007) developed a formulation product of Pantoea called FD 10-3 and tested it either alone or in combination with heated sodium bicarbonate (SBC) solutions, in semi-commercial and commercial trials with oranges (Citrus sinensis) and mandarins (Citrus reticulate) from Portugal and Spain. This formulation treatment significantly reduced the percentage of infected fruits and in some cases this reduction was equal to chemical treatments. Pantoea sp. strain 48b/90 was isolated from soybean leaf and reported to show inhibitory action against Pseudomonas syringae, Xanthomonas campestris pathovars, Agrobacterium tumefaciens and also Erwinia amylovora in vitro. It was reported to produce toxin(s) with a wide antibiotic spectrum, siderophores (the known ferrioxamine E and an unknown chatechol-siderophore), and a quorum sensing substance (Völksch and Sammer, 2008). Two Pantoea agglomerans strains (PTA-AF1 and PTA-AF2) were isolated from grapevine (Vitis vinifera) by Trotel-Aziz et al. (2008) who reported them to be efficient antagonist against Botrytis cinerea, the causal agent of grey mould under in vitro conditions. Johnson et al. (2000) evaluated the effect of environmental factors on the growth of Pantoea agglomerans on inoculated pear and apple blossoms and on spread of the bacterium to non-inoculated trees and reported that temperature is a crucial environmental variable that affected the successful spread of this biological control agent from blossom to blossom. Spread of Pantoea agglomerans strain C91S was favoured by periods of warm, dry weather, and was limited when conditions were cooler and wetter. Pantoea agglomerans with Flavobacterium sp. was reported to control the two main pathogens, Colletotrichum musae and Lasiodiplodia theobromae, known to cause crown rot of banana (Musa paradisiacal). However the reduction of conidial germination (in condial germination assay on microscopic slides) and inhibitory effects on pathogens (based on agar well difffusion assay) varied depending on the stage of the life cycle of pathogens (conidia or mycelia) and the preparation of antagonists tested (viable cells and/or spent media) (Gunasinghe and Karunaratne, 2009).

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P. agglomerans and P. dispersa were frequently found to be associated with Erwinia amylovora, the causal agent of the fire blight of apple and pear (Riggle and Klos, 1972) and were harmless to apple and pear trees and were able to protect them against invasion of the pathogen (Johnson et al., 1993). P. agglomerans strain Eh318 was isolated from a symptomless apple stem in New York State and was reported to protect immature pear fruits in the laboratory and apple blossoms in controlled environment and orchard tests (Wodzinski et al., 1994; Hickey and van der Zwet, 1996). The pathogen inhibition has been attributed to the production of two antibiotics pantocin A and B (Wright et al., 2001). Different antibiotics are produced by different strains of P. agglomerans and P. dispersa (Ishimaru et al., 1988). Preventive exclusion of the pathogens Monilina laxa and Rhizopus stolonifer by wound colonization and cell-to-cell interaction was found to be the main mechanisms of biocontrol of brown and soft rot by P. agglomerans EPS125 (Bonaterraa et al., 2003). Endophytic Pantoea were also isolated from six cotton (Gossypium hirsutum) cultivars at different developmental stages and were reported to show antagonistic potential against Verticillium dahliae Kleb V107 and V396 and Fusarium oxysporum f. sp. vasinfectum (F108) (Li et al., 2010b). P. agglomerans is a diazotroph, and is able to fix molecular N2 both in pure culture and in association with wheat (Merbach et al., 1998). Ruppel et al., (1992) reported Pantoea agglomerans to be the most effective bacterial strain associated with winter wheat. This strain was also shown to increase the yield of legumes on inoculation and led to inhibition of phytopathogenic fungi (Höflich and Ruppel, 1994). Its colonization behavior was studied by Remus et al. (2000), in sterile and non-sterile hydroponic system and in soil by means of an immunological detection method and electron microscopy. It was able to compete with the native microflora in hydroponic system. It was also able to colonize the rhizosphere and the phyllosphere of different cereals; however the colonization behaviour of P. agglomerans was somewhat plant species-specific. It colonized the roots of wheat to a greater extent than those of rye (Secale cereale) and barley (Hordeum vulgare), whereas the colonization of shoots was higher in rye and barley compared to wheat. In field experiments, inoculation with P. agglomerans led to an increase in the grain yield of different wheat cultivars (Verma et al., 2004). An endophytic strain of Pantoea agglomerans YS19 was isolated from the rice cultivar Yuefu from a temperate region of China (Feng et al., 2003). This strain was reported to be associated most frequently and in large numbers from all the surface disinfected plant tissues (root, stem, leaf, and seed) sampled at different growth and development stages (Yang et al., 1999). The strain YS19 showed higher nitrogen-fixing activity than any other endophytic bacteria isolated from this plant on the basis of acetylene reduction activity and 15N2-fixing activity, indicating it being a diazotrophic endophyte (Yang et al., 1999). Strain YS19 was verified to promote host plant growth and affect allocation of host photosynthates (Feng et al., 2006). In vitro adsorption dynamics study revealed high rates and a long duration of the YS19-rice root adsorption process, mainly observed on the root hair, through which it enters the plant suggesting a strong interaction between YS19 and rice at the early endophyte-host recognition stage (Miao et al., 2008). Under in vitro conditions, there are two growth stages for this strain viz., the single cell stage existing before the end of the exponential growth phase and the symplasmata formation stage starting from then on (Feng et al., 2003). A symplasmatum is a multicellular aggregate structure in which several (at least two) hundreds of individual cells tightly bind together. Zhang et al. (2010) reported that even though single cells were used for inoculation, YS19 invaded the plant and colonized in rice almost always as symplasmata, clearly suggesting that these structures

are not necessary structures for bacterial invasion but significant for colonization. The main binding components for symplasmata construction are most likely proteins, like SPM43.1. Symplasmata is a kind of adaptive structure for endophytic life and have many advantages such as homogeneity in growth, metabolism and propagation, which provide a relatively stable balance between the symbiont and the host. The aggregate structure together with the matrix fibers may act as a barrier against oxygen diffusion into the internal of the symplasmata allowing an optimal condition for nitrogenase activity (Zhang et al., 2009, 2010). Taurian et al. (2010) reported Pantoea isolate J49, from peanut root nodules and demonstrated its ability to increase the plant biomass of peanut (Arachis hypogaea). The isolates were able to solubilize phosphorus and produce siderophores in vitro, however no change in total P was observed indicating the possibility of other mechanisms of plant growth promotion. A phosphate solubilizing P. agglomerans was isolated by Kim (1997) from wheat rhizosphere. The bacterium was reported to strongly solubilize hydroxyapatite in culture medium (Kim et al., 1997). The effect of organic energy sources on the survival of P. agglomerans and soil microbial activity was studied by Kim et al. (1998) by introducing it into unsterilized soil containing 1% hydroxyapatite and either 1% glucose, phytic acid dodecasodium salt, glycerol-2-phosphate disodium salt, soluble starch or no addition. Organic energy sources incorporated into soils were reported to contribute to the survival and solubilization of phosphate by P. agglomerans. Pantoea agglomerans was also isolated as an active phosphate solubilizing bacterium from the rhizosphere of various crop plants (Chung et al., 2005) in Korea. Son et al. (2006) also reported a novel salt and pH-tolerant phosphate solubilizing Pantoea agglomerans R-42 from soybean rhizosphere. Pantoea agglomerans strain P5, isolated from slightly alkaline soil types, hydrolyzed both inorganic and organic phosphate compounds effectively, a close association was evident between its phosphate solubilizing ability and growth rate which is an indicator of active metabolism. This strain was able to withstand temperature as high as 42  C, concentration of NaCl up to 5% and a wide range of initial pH from 5 to 11 while hydrolyzing phosphate compounds actively, making it a superior candidate for biofertilizer production (Malboobi et al., 2009a). Malboobi et al. (2009b) studied its interaction with Microbacterium laevaniformans strain P7 and Pseudomonas putida (both isolated from same rhizosphere), competitiveness with soil microorganisms and associations with plant root using luxAB reporter genes. Synergism between either P. agglomerans or M. laevaniformans, as acid-producing bacteria, and P. putida, as a strong phosphatase producer, was consistently observed both in liquid culture medium and in root rhizosphere. All laboratory, greenhouse and field experiments proved that these three isolates compete well with naturally occurring soil microorganisms. Consistently, the combinations of either P. agglomerans or M. laevaniformans strains with Pseudomonas putida led to higher biomass and potato tuber yield in greenhouse and in field trials. Selvakumar et al. (2008) reported a cold tolerant Pantoea dispersa strain with multiple plant growth promoting attributes from North Western Himalayas. This strain was able to positively influence and promote the growth and nutrient parameters of wheat under greenhouse conditions. Another phosphate solubilizing Pantoea strain NII-186 was isolated from soils of the Western Ghats of India by Dastager et al. (2009). This strain was reported to grow at a wide range of temperature, pH and salt concentration and possess multiple plant growth attributes such as IAA production, siderophore production, HCN production and could antagonize plant pathogenic fungi like Penicillium chrysogenum, Aspergillus niger and Geotrichum candidum under in vitro conditions. Hu et al. (2010) reported a new phosphate-solubilizing bacterium Pantoea stewartii subsp. stewartii capable of growing at a

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wide range of temperatures, salinity, and pH and suggested its role in the aquaculture pond ecosystems, where the concentrations of total phosphorus were high in the sediment but low in the overlying water. IAA producing Pantoea agglomerans isolated from the rhizosphere of legumes by Sergeeva et al. (2007) were examined for their ability to promote the growth of canola, lentil and pea under gnotobiotic conditions. Presence of ipd C gene which codes for a key enzyme in the tryptophan dependent IAA synthetic pathway was confirmed by colony hybridization. Isolate 3–117 producing significant concentrations of IAA in the presence and absence of tryptophan, was able to use aromatic amino acids as sole source of nitrogen and was most consistent in enhancing the growth of canola, lentil and pea. P. agglomerans was also reported to produce two auxins and two cytokinins in pure culture (Scholz et al., 1991; Scholz-Seidel and Ruppel, 1992). Inoculation of wheat seedlings with a extra—polysaccharide producing strain of Pantoea agglomerans (NAS206) selected from the rhizosphere of wheat growing in a Moroccan vertisol resulted in intense colonization of the wheat rhizosphere and had a positive effect on aggregation and stabilization of root-adhering soil as shown by increased mean aggregate diameter, macroporosity and mechanical stability of the root-adhering soil (Amellal et al., 1999). Table 3 summarizes the plant growth promotion by Pantoea spp. Recent efforts on genome sequencing of the plant growth promoting rhizobacterial Pantoea sp. strain AS- PWVM4; have revealed the presence of 97 genes responsible for motility and chemotaxis, including 16 genes for flagellar motility. Fifty phosphorus metabolism genes, twenty-nine genes for osmotic stress-response and sixty nine for the oxidative stress response have been identified in this organism (Khatri et al., 2013). Genome sequencing of the epiphytic Pantoea agglomerans strain 299R revealed many adaptations consistent with an epiphytic lifestyle, including genes for high-affinity uptake and utilization of the photosynthates sucrose, fructose, and glucose, for repair of UVdamaged DNA, and for production of the osmoprotectants betaine and trehalose. Presence of the ipdC gene for production of the plant hormone indole 3-acetic acid also was confirmed in this genome (Remus-Emsermann et al., 2013). 2. Biosafety of novel PGPR strains With rapid advances in microbial discovery and inoculant technology, the realm of microbial inoculants has seen a significant shift from the conventional range of microbes to include a wide range of rhizobacterial genera that colonize the rhizosphere and promote plant growth in a myriad fashion. While this is definitely a welcome step, it brings along with it a host of pertinent questions, of which the biosafety of the microbial strains used for inoculant formulation is of paramount importance. This rationalization

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becomes imperative in the present scenario, where the etiology and pathogenesis of several hitherto unknown or lesser known bacterial species are being deciphered, and opportunistic pathogenic properties are being attributed to several commonly occurring environmental microbes. Hence a judicious analysis of the benefits and risks associated with novel microbial inoculants need to be addressed, before its eventual usage (Selvakumar et al., 2014). The term biosafety can be broadly described as the measures that need to be taken up for the prevention of large-scale loss of biological integrity, with a primary focus on both ecology and human health. It can also be described as the containment principles, technologies and practices that are implemented to prevent unintentional exposure to pathogens and toxins, or their accidental release in the environment (Anon., 2003). A crucial step in determining the risk status of a novel microbe is the accurate determination of its taxonomy, by the polyphasic approach. This is very important since most studies conducted on clinical/environmental isolates of the Pantoea agglomerans group have reported that majority of the clinical isolates from culture collections were found to be improperly designated as P. agglomerans due to the frequent taxonomic rearrangements undergone by the Enterobacter agglomerans/Erwinia herbicola complex (Rezzonico et al., 2009). Taxonomic determination can be followed by the preliminary risk assessment process based on the risk level assignment of microorganisms provided in the classification database of the American Biological Safety Association (ABSA), for infectious agents (http://www.absa.org/riskgroups/). This could be followed by the utilization of rapid protocols that distinguish clinical isolates from their environmental counterparts. In a study conducted with clinical Pantoea agglomerans strains derived from various culture collections and biocontrol strains obtained from various sources Rezzonico et al. (2009) identified a putative biocontrol-specific fAFLP marker that was present only in biocontrol strains of Pantoea agglomerans. Similarly in study with plant beneficial and clinical Pantoea strains by Bonaterra et al. (2014), it was observed that the clinical strains generally lacked inhibitory activity against fungal or bacterial plant pathogens. Another rapid and reliable approach would be the determination of pathogenic factors in potential bio-inoculant strains by the amplification of genes encoding them. But such laboratory tests need to be validated with a large number of properly identified isolates, since it has been suggested that independent of their origin, all P. agglomerans strains might possess indistinguishable virulence potential (Volksch et al., 2009). The final biosafety of a novel microbial agent, can be determined by acute toxicity tests (usually carried out on small laboratory animals), and its environmental effects on selected animal species like fishes, earthworms, pollinators, etc. (Young et al., 2012). Thus it can be observed that a combination of acute

Table 3 Plant growth promotion by Pantoea species. Pantoea species

Effect

Reference

Pantoea agglomerans

Enhancement of yield and growth of tomato and cucumber Growth promotion in maize and chickpea Systemic resistance against gray leaf spot disease in pepper Increased yield, growth and nutrition of strawberry under high-calcareous soil conditions Salt tolerance and up-regulation of aquaporin genes in tropical corn Plant growth promotion in rice Foliar colonization and growth promotion in red pepper Contribution to nitrogen fixation of sugarcane Inoculated plants show better growth physiology and nutrient content under saline conditions Enhancement of growth, nutrient, and hormone in cabbage

(Dursun et al., 2010)

Pantoea Pantoea Pantoea Pantoea Pantoea Pantoea Pantoea Pantoea Pantoea

agglomerans agglomerans agglomerans agglomerans spp. spp. spp. spp. spp.

(Mishra et al., 2011) (Son et al., 2014) (Ipek et al., 2014) (Gond et al., 2015) (Fei et al. 2011) (Lee et al., 2011) (Taulé et al., 2012) (Jha and Subramanian, 2013) (Turan et al., 2014)

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H. Chauhan et al. / Applied Soil Ecology 95 (2015) 38–53

Table 4 Comparative advantages and disadvantages of novel PGPR genera. Genus

Advantage

Disadvantage

Endophytic origin and difficult to recover from soil, except few species Exiguobacterium Multiple plant growth promotion traits, ability to grow at extreme temperatures and Sporadic prevalence, predominantly reported from the growth conditions temperate soils. Occurrence in tropical soils not frequent Methylobacterium Phyllospheric occurrence and ability to utilize 1C compounds Lack of suitable inoculant formulation strategies for commercial exploitation Paenibacillus Multiple plant growth promotion traits, ability to form endospores, a wide host range, Rhizospheric competency traits not well established in all stimulation of mycorrhiza as helper bacteria, formation of soil aggregates and strains improvement of soil texture Multiple plant growth promotion traits, biocontrol of post harvest diseases of many Some pathogenic strains have also been reported. Requires Pantoea important fruit crops rigorous screening for pathogenic traits Azoarcus

Endophytic occurrence in rice which is an important cereal crop of the world

toxicity tests and environmental evaluation can give a fair estimate of the biohazard potential of a novel microbe, before its eventual usage as an inoculant for crops. 3. Conclusion In summary each of the PGPR discussed above have unique abilities that can be exploited for further research and commercial use. Azoarcus spp. with its ability to colonize and fix nitrogen in graminaceous crops offers exciting possibility in sustainable agriculture practices, as most of the staple food crops of the world belong to Gramineae family which cannot form nodules. Therefore more investigations are needed to understand the inoculation response of staple food crops like rice, maize, wheat, etc. with Azoarcus alone and in combination with other inoculants to exploit its plant growth promoting potential. Exiguobacterium is able to grow in a wide range of temperatures and environmental conditions and thus have potential as an inoculant in extreme and abiotically stressed conditions, which needs further investigation. Amongst the bacterial genera that are found in close association with plants, Methylobacterium appears to be one of the most versatile and ubiquitous organism, but it has not received a proportionate interest from the point of commercial utilization. Close association of Methylobacterium along with its phyllosphere colonization ability, offers newer possibilities of commercial exploitation as a foliar applied inoculant. Biofilm formation by Paenibacillus gives it a competitive advantage over other rhizospheric populations and its spore forming ability makes it an attractive candidate for commercial formulation. Therefore it would be appropriate to intensify research on bioinoculant formulations using Paenibacillus strains. Pantoea are found in a wide range of habitats. Plant growth promoting Pantoea can play an important role in the biocontrol of post harvest disease management and phosphate solubilization in soil. Concerted efforts are required to screen and develop suitable biological inoculant strains belonging to this genus in order to fully harness its potential. Further compatibility among these novel PGPR, and other PGPR and mycorrhizal fungi may be established for developing combination products. Table 4 summarizes the comparative advantages and disadvantages of these novel PGPR. With advances in microbial discovery and functional genomics it is quite obvious that the realm of microbial inoculant technology has moved beyond the traditional bacterial strains that were used for inoculant production. But unfortunately most novel strains reported from different parts of the world continue to remain as artifacts of academic interest only and are not used on a commercial scale. This may be attributed to the lack of intensive studies to prove their efficacy under field conditions and policy issues that do not promote the utilization of novel strains, as microbial inoculants. While both these are detrimental to the utilization of technology for the well being of humankind, a word

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