Endophytic bacteria: Role in sustainable agriculture

Endophytic bacteria: Role in sustainable agriculture

3

Mahendra Prasad*, R. Srinivasan*, Manoj Chaudhary*, Sonu Kumar Mahawer*, Lokesh Kumar Jat† *Crop Production Division, ICAR-Indian Grassland and Fodder Research Institute, Jhansi, India, †Department of Soil Science and Agricultural Chemistry, Agricultural Research Station, S.K.N. Agriculture University, Jobner, India

3.1

Introduction

Agricultural practices in the 21st century are under pressure to provide increased yields to feed the ever-increasing world population, which is projected to reach about 9 billion in 2050 (DESA, 2015). According to the FAO (2009), demand for agricultural production is expected to increase by at least 70% by 2050. To meet the food demand of ever-growing global human population, agricultural practices are largely relied on the application of chemical fertilizers. Use of chemical fertilizers in agriculture has many negative consequences because it causes water contamination through denitrification and leaching, which is detrimental for all living organisms. Furthermore, synthesis of chemical N fertilizers using natural gas and coal has aggravated the emission of greenhouse gases (GHGs) carbon dioxide and nitrous oxide contributing to global warming (Bhattacharjee et al., 2008). To feed the burgeoning human population is the greatest tasks for maintaining the global environmental sustainability. For maintenance of global agriculture sustainability, the thorough understanding of soil complex is primarily important (Paustian et al., 2016; Prasad et al., 2017), not only to supply sufficient food but also to maintain global environmental sustainability for upcoming generations (Ahmad et al., 2016; Zahedi, 2016; Kumar et al., 2017a). The present crop production practices have attained its peak now and are hitherto very tough to increase the agriculture productivity. Hence, it’s high time to explore nonconventional resources for the development of sustainable crop production technologies without damaging the environmental sustainability. Soil microbial population has immense potential in attaining the agricultural sustainability in present environmental conditions (Patil et al., 2014; Vaxevanidou et al., 2015). The endophytic microbes (fungi and bacteria) are promising tool for the management of agricultural productivity. Thus, endophytic bacteria can be utilized to augment the plant growth and plant health without degrading the environment (Sturz et al., 2000; Iniguez et al., 2004; Long et al., 2008; Lugtenberg and Kamilova, 2009). Rhizospheric growth-promoting endophytic bacteria (RGPEB) are a gaggle of bacteria that enhance the plant growth via phosphate solubilization (Senthilkumar et al., 2009), biological N fixation (Rediers et al., 2003), indole-3-acetic acid (IAA) Microbial Endophytes: Prospects for Sustainable Agriculture. https://doi.org/10.1016/B978-0-12-818734-0.00003-6 © 2020 Elsevier Inc. All rights reserved.

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Microbial Endophytes: Prospects for Sustainable Agriculture

synthesis (Armando et al., 2009), production of siderophore (Logeshwaran et al., 2009), production of plant-growth substances (Armando et al., 2009), alleviating the effect biotic or abiotic stresses, and inducing tolerance to pathogen (Fig. 3.1) (Bhattacharyya and Jha, 2012). Usually, density of endophytic bacteria population is lower than rhizospheric bacteria (Hallmann et al., 1997; Rosenblueth and Martinez Romero, 2004). Endophytic as well as rhizospheric bacterial population are significantly governed by different abiotic and biotic conditions (FuentesRamı´rez et al., 1999; Hallmann et al., 1997; Seghers et al., 2004), however, endophytic bacterial could better withstand adverse and external environmental conditions than rhizosphere bacterial (Hallmann et al., 1997). Soil microorganisms provide several benefits to agriculture through improving plant nutrient availability, plant health, and soil quality (Barea et al., 2013; Lugtenberg, 2015). Microorganisms can provide active and passive advantageous impacts on crops by nutrient enhancement and by reducing damages caused by plant pathogens or environmental conditions (Prasad et al., 2019). Generally, crop plants are mutually associated with microbes including endophytes. Endophytes are defined as microorganisms, commonly bacteria and fungi (Wilson, 1995; Strobel and Daisy,

Fig. 3.1 Role of endophytic bacteria for sustainable agriculture.

Endophytic bacteria: Role in sustainable agriculture

39

2003), which live the whole or some stage of their life cycle in inner plant cells without expressing any adverse effect (Hallmann et al., 1997; Bacon and White, 2000; Long et al., 2008). These microbial associations could be beneficial, neutral, or detrimental (Sturz et al., 2000). Roughly, around 30,000 plant species found on earth has been estimated to serve as the host for one or more endophytes. Owing to the potential role of endophytic bacteria in plant-growth promotion and disease management properties, endophytes can be used as bioinoculants in agriculture to increase crop productivity. Many reports are available with regard to the application of endophytic bacteria to enhance the plant’s resistance to disease and promote plant growth. Thus, employing endophytes in agricultural practices would result in for better soil health and sustainable crop production (Mei and Flinn, 2010). This chapter, therefore, aims to provide detailed information on the potential applications of bacterial endophytes with particular emphasis on improvement in plant nutrition and sustainable agriculture. The knowledge introduced in this chapter could be fruitful to researcher from different disciplines involved in the application of endophytic bacteria in agriculture sustainability.

3.2

Distribution and diversity of endophytic bacteria

The term endophyte is a Greek world which means “inside the plant” (endon, within; phyton, plant) (Schulz and Boyle, 2005). This term is used to describe microorganisms (mainly fungi and bacteria) residing inside plant tissues without expressing any harmful symptoms on host plant (Hallmann et al., 1997; Bacon et al., 2002). Based on the plant-inhabiting life strategies, these bacteria can be classified into three major categories, viz., obligate, facultative, and passive endophytes. Obligate endophytes are found inside of plants tissue; facultative endophytes are free living in soil but may enter into plant tissue through infection (Hardoim et al., 2008) or any other means. Many endophytes responsible for enhancing plant growth have been described to fall in this category (Table 3.1). Passive endophytes are actively colonized in host tissue through various open injuries. This is a rare possibility due to the necessity of cellular machinery for host colonization is lacking (Verma et al., 2004; Rosenblueth and Martı´nez-Romero, 2006), hence passive endophytes are considered as less efficient Table 3.1 Endophytic bacteria isolated from common agricultural crop plants Plant species and organ Alfalfa (Medicago sativa L.) roots

Bacterial endophyte taxa

References

γ-Proteobacteria: Erwinia sp., Pseudomonas sp. Firmicutes: Bacillus megaterium, B. choshinensis Actinobacteria: Microbacterium trichothecenolyticum

Gagne et al. (1987) and Stajkovic et al. (2009)

Continued

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Microbial Endophytes: Prospects for Sustainable Agriculture

Table 3.1 Continued Plant species and organ Carrot (Daucus carota L. var. sativus)

Maize (Zea mays L.) stems, roots

Potato (Solanum tuberosum L., Ipomoea batatas) tubers and stems

Bacterial endophyte taxa

References

α-Proteobacteria: Rhizobium (agrobacterium) radiobacter γ-Proteobacteria: Klebsiella terrigena, Pseudomonas putida, P. fluorescens, P. chlororaphis Firmicutes: Bacillus megaterium α-Proteobacteria: Rhizobium etli β-Proteobacteria: Burkholderia pickettii, B. cepacia, Achromobacter, Herbaspirillum seropedicae γ-Proteobacteria: Erwinia sp., Enterobacter sp., E. cloacae, Stenotrophomonas sp., Klebsiella sp., K. terrigena, K. pneumoniae, K. variicola, Pseudomonas sp., P. aeruginosa, P. fluorescens Firmicutes: Bacillus sp., B. mojavensis, B. thuringiensis, B. megaterium, B. subtilis, B. pumilus, Lysinibacillus, Paenibacillus Actinobacteria: Corynebacterium sp., Arthrobacter globiformis, Microbacterium testaceum α-Proteobacteria: Agrobacterium sp., Sphingomonas sp., Methylobacterium sp. β-Proteobacteria: Acidovorax sp., Alcaligenes sp., Comamonas sp., Enterobacter sp. γ-Proteobacteria: Acinetobacter sp., Erwinia sp., Klebsiella sp., Pantoea sp., P. agglomerans,

Surette et al. (2003)

Fisher et al. (1992), McInroy and Kloepper (1995), Palus et al. (1996), Chelius and Triplett (2001), Zinniel et al. (2002), Rosenblueth and Martinez Romero (2004), and Rai et al. (2007)

Sturz et al. (2000), Reiter et al. (2002), and Sturz et al. (1998)

Endophytic bacteria: Role in sustainable agriculture

41

Table 3.1 Continued Plant species and organ

Radish (Raphanus sativus L.) leaves and roots Red clover (Trifolium Pratense L.), leaves, stems, roots, and fresh nodules

Bacterial endophyte taxa Pasteurella sp., Photobacterium sp., Vibrio sp., Serratia liquefaciens, Xanthomonas sp., Pseudomonas tolaasii, Psychrobacter sp., Shewanella sp., Enterobacter sp., E. asburiae Firmicutes: Bacillus alcalophilus, B. pasteurii, B. sphaericus, B. coryneforms, Leuconostoc sp., Paenibacillus odorifer Bacteroidetes: Capnocytophaga sp. Actinobacteria: Actinomyces sp., Arthrobacter ureafaciens, Corynebacterium sp., Curtobacterium sp., C. citrinum, C. luteum, Micrococcus sp. Proteobacteria: Proteobacteria sp. α-Proteobacteria: Agrobacterium rhizogenes, A. tumefaciens, Methylobacterium sp., Phyllobacterium sp., Rhizobium sp., Sphingomonas sp. β-Proteobacteria: Acidovorax sp., Bordetella sp., Comamonas sp., Variovorax sp. γ-Proteobacteria: Enterobacter sp., Aerobacter cloacae, Escherichia sp., Klebsiella sp., Pantoea agglomerans, Xanthomonas campestris, X. oryzae, Pseudomonas cichorii, P. corrugata, P. fulva,

References

Seo et al. (2010)

Sturz et al. (1998)

Continued

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Microbial Endophytes: Prospects for Sustainable Agriculture

Table 3.1 Continued Plant species and organ

Sugar beet (Beta vulgaris L.) roots

Soybean (Glycine max (L.) Merr.) stems, leaves, roots, and nodules

Tomato (Lycopersicon esculentum Mill.) stems and fruits

Wheat (Triticum aestivum L.) roots

Bacterial endophyte taxa P. syringae, P. tolaasii, Serratia sp., Pasteurella sp., Psychrobacter sp., P. immobilis Firmicutes: Bacillus brevis, B. megaterium Actinobacteria: Arthrobacter ilicis, Cellulomonas sp., Curtobacterium citreum, C. luteum, Micrococcus varians γ-Proteobacteria: Erwinia sp., Pseudomonas sp., Xanthomonas sp. Firmicutes: Bacillus sp., Lactobacillus sp. Actinobacteria: Corynebacterium sp. α-Proteobacteria: Erwinia sp., Agrobacterium sp. γ-Proteobacteria: Pseudomonas citronellolis, P. oryzihabitans, P. staminea, K. pneumoniae, K. oxytoca, Enterobacter sp., Pantoea sp., P. agglomerans Firmicutes: Bacillus fastidiosus γ-Proteobacteria: Pseudomonas sp., P. syringae, P. aeruginosa, Escherichia coli Firmicutes: Brevibacillus brevis β-Proteobacteria: Burkholderia cepacia γ-Proteobacteria: Klebsiella sp. Firmicutes: Bacillus polymyxa Actinobacteria: Mycobacterium sp.

References

Jacobs et al. (1985) and Dent et al. (2004)

Zinniel et al. (2002); Kuklinsky-Sobral et al. (2004)

Pillay and Nowak (1997), Yang et al. (2011), and Patel et al. (2012)

Balandreau et al. (2001), Zinniel et al. (2002), and Iniguez et al. (2004)

From Miliute, I., Buzaite, O., Baniulis, D., Stanys V., 2015. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review, Zemdirbyste-Agr., 102(4), 465–478.

Endophytic bacteria: Role in sustainable agriculture

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as plant-growth promoters. Distribution of endophytes depends on their ability to colonize and suitability of host plant resources. Mundt and Hinkle (1976) probably isolated endophytic bacteria from plants for the first time and till now, in 16 phyla, more than 200 bacterial genera have been reported as endophytes. These include both culturable and unculturable endophyte bacteria. Most of these bacteria fall under different phyla including Actinobacteria, Acidobacteria, Aquificae, Bacteroidetes, Chloroflexi, Cholorobi, Cyanobacteria, Firmicutes, Fusobacteria, Gem-matimonadetes, Nitrospira, Planctomycetes, Proteobacteria, Spirochaetes, and Verrucomicrobia (Mengoni et al., 2009; Manter et al., 2010; Sessitsch et al., 2012). However, the prominent and studied endophytes belong to three major phyla, that is, Proteobacteria, Actinobacteria, and Firmicutes and include members of Pseudomonas (Taghavi et al., 2009), Enterobacter (Taghavi et al., 2010), Bacillus (Deng et al., 2011), Azoarcus (Krause et al., 2006), Burkholderia (Weilharter et al., 2011), and Stenotrophomonas (Ryan et al., 2009).

3.3

Role of endophytic bacteria in sustainable agriculture

Endophytic bacteria play a major role in increasing plant growth through beneficial effects on host plant. These bacteria enhance plant growth through increase in germination percentage, leaf area, chlorophyll content, biomass production, root and shoot ratio, nitrogen concentration, protein content, hydraulic activity and stresses tolerance against drought, flood, salinity, etc. These bacteria also enhance plant-growth actively by increasing plant nutrient availability, reduction in ethylene production, and passively by developing tolerance against myriads of plant pathogens (Bhattacharyya and Jha, 2012). Various beneficial characteristics of different endophytic bacteria are being discussed here.

3.3.1 Biological nitrogen fixation Among all essential plant nutrients, nitrogen is the most important growth-limiting nutrient (Munees and Mulugeta, 2014). It is the seventh most abundant element in the earth crust. It comprises about 78% of the gases in the environment. In the gaseous form (N2), it is unavailable to most of the plants and animals (Pujic and Normand, 2009). Plants absorb nitrogen in the form of nitrate and ammonium ions. Conversion of gaseous nitrogen into ammonium ion through bacterial activity is called as biological nitrogen fixation (BNF). The capacity to convert gaseous nitrogen into ammonium and nitrate form is widespread among prokaryotes including bacteria and archaea (Dekas et al., 2009; Das et al., 2015). The endophytic bacterial population density is highly fluctuating and is mainly determined by the bacterial species, host genotypes, inoculum density, and prevailing environmental conditions (Pillay and Nowak 1997; Tan et al., 2003). Endophytic bacteria equipped with the enzymatic ability to fix atmospheric nitrogen are very less as compared to total endophytic bacterial population (Barraquio et al., 1997; Ladha et al.,

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Microbial Endophytes: Prospects for Sustainable Agriculture

Table 3.2 Contribution of biological nitrogen fixation by associative/endophytic bacteria Endophytic bacteria

Associated plant

% Ndfaa

Rhizobium leguminosarum bv. trifolii

Rice

19–28

Burkholderia

Rice

31

Herbaspirillum

Rice

19–47

Azospirillum

Rice

19–47

G. diazotrophicus, H. seropedicae, H. rubrisubalbicans, A. amazonense and Burkholderia sp. K. pneumoniae 324

Sugarcane

29

Rice

42

Burkholderia vietnamiensis

Rice

40-42

References Yanni et al. (1997) and Biswas et al. (2000) Baldani and Baldani (2005) Ladha and Reddy (2000) Ladha and Reddy (2000) Oliveira et al. (2002) Iniguez et al. (2004) Govindarajan et al. (2008)

a

Nitrogen derived from air.

1983; Martinez et al., 2003) and increasing nitrogen-fixing bacteria populations in host plants could be a remarkable strategy to enhance nitrogen fixation. It is obvious from the reports that the Gluconacetobacter diazotrophicus (Acetobacter diazotrophicus) has the major contribution in endophytic BNF in sugarcane and it has the capacity to fix the atmospheric nitrogen approximately obereiner et al., 1993). Another, potential nitrogen fixing 150 kg N ha 1 year 1 (D€ obligate endophyte is Azoarcus. The bacterium penetrates the roots of kallar grass and increases the hay yield 20–40 t ha 1 year 1 without introduction of nitrogenous fertilizer (Hurek and Reinhold-Hurek, 2003). Growth promotion of radish, mustard, wheat, corn, and certain varieties of rice following seed inoculation with a strain of Rhizobium leguminosarum in pot experiments have also been reported (Hoflich et al., 1995; Webster et al., 1997). These reports confirm that endophytic bacteria have a considerable ability to increase the productivity of leguminous and nonlegumes crop plants in a sustainable manner through BNF. Contribution in atmospheric nitrogen fixation by associative/endophyte bacterial species has been shown in Table 3.2.

3.3.2 Phosphorus solubilization Phosphorus is the most important nutrient for plant growth and development. It has major role in metabolic processes, viz., photosynthesis, respiration, energy transfer, macromolecular biosynthesis, etc. (Anand et al., 2016). Phosphorous is amply present in the universe but it is very less accessible to plants and animals because more than 95% available phosphate is insoluble, immobilized, and precipitated in the forms of

Endophytic bacteria: Role in sustainable agriculture

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mineral salts, that is, dicalcium and tricalcium phosphate, hydroxyapatite, rock phosphate, etc. Therefore, less availability of phosphate in soil certainly hampers the agriculture productivity (Miller et al., 2010; Hani, 2012; Wang et al., 2017). Phosphorus solubilization and mineralization are the important processes to increase its availability. These processes can be performed by rhizosphere colonizing and endophytic bacteria. These bacteria help to lower down the rhizospheric pH through release of different types of organic acids such as carboxylic acid that breaks the bound forms of phosphorous particularly Ca-bonded phosphorus in calcareous soils (Sharma et al., 2013). Therefore, recently, researchers have paid considerable attention on inoculation of phosphate-solubilizing endophytic bacteria as it improves plant growth and yield in an eco-friendly manner. Phosphorus solubilizing bacteria include the genera Arthrobacter, Bacillus, Beijerinckia, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Mesorhizobium, Microbacterium, Pseudomonas, Rhizobium, Rhodococcus, and Serratia (Oteino et al., 2015; Srinivasan et al., 2018). Among these genera, Pseudomonas, Bacillus, and Rhizobium are the most efficient phosphatesolubilizing strains (Rodriguez and Fraga, 1999; Yu et al., 2012; Li et al., 2016). Long et al. (2008) isolated 77 endophytic bacterial strains from the parts of Solanum nigrum from two native habitats and found that six isolates were able to solubilize inorganic phosphate efficiently. In other study, Thamizhvendan et al. (2010) isolated 18 endophytic isolates from ginseng plants in which 9 isolates were reported to have phosphate-solubilizing ability. These studies showed that endophytic bacteria increase the availability of phosphorous to the crop and hence, improves the productivity.

3.3.3 Potassium solubilization Next to phosphorus, potassium (K) is the most essential element required by plant and animals for the growth and development. It plays vital roles in osmotic regulation, energy relation, protein and starch synthesis, and improving resistance to pest and diseases. Most of the amount of existing potassium (>90%) is present as insoluble silicate minerals in rocks. Thus, the availability of potassium is very less in the soil (Parmar and Sindhu, 2013) and insufficiency of potassium has raised a big challenge in sustainable plant nutrition (Nath et al., 2017; Meena et al., 2017). K solubilization is biologically performed by a large range of soil microbes like bacteria, fungi, and actinomycetes (Ahmad et al., 2016; Bakhshandeh et al., 2017). There are several evidences that soil bacteria are capable of transforming insoluble soil K to the soluble forms and make them available to plant effectively (Meena et al., 2014, 2015, 2016). Transformation of K by KSB (K-solubilizing bacteria) from unavailable forms is a major area in respect of increase K availability to crops. The ability to solubilize the insoluble K minerals by Bacillus mucilaginosus, Bacillus circulans, Bacillus edaphicus, Burkholderia, Acidithiobacillus ferrooxidans, Arthrobacter sp., Enterobacter hormaechei, Paenibacillus mucilaginosus, Penicillium frequentans, Cladosporium, Aminobacter, Sphingomonas, and Burkholderia has been reported (Meena et al., 2016). Among the soil bacterial populations, B. mucilaginosus, B. edaphicus, and B. circulans are considered as effective

46

Microbial Endophytes: Prospects for Sustainable Agriculture

K solubilizers (Meena et al., 2014, 2015, 2016). Potassium solubilizing bacteria are usually thriving in all soils and have been isolated from rhizosphere, nonrhizosphere, paddy fields, and saline soils (Bhattacharya et al., 2016; Bakhshandeh et al., 2017). Therefore, use of potassium solubilizing microorganisms as a bio-fertilizer can minimize the external application of synthetic fertilizers and could help to improve the crop productivity in sustainable manner (Setiawati and Mutmainnah, 2016; Basak et al., 2017; Bakhshandeh et al., 2017; Wei et al., 2017).

3.3.4 Zinc solubilization Zinc is the imperative micronutrient which is required for the plant-growth, development, and reproduction (Alloway, 2004). For healthy crop growth and reproduction, it is required relatively in small amount in plant cells. Zinc deficiency in plants affects the synthesis of auxins, carbohydrates, cytochromes, chlorophyll, membrane integrity, and plants get susceptible to heat stress (Singh et al., 2005). The global occurrence of Zn deficiency in crops is because of lesser solubility of Zn minerals in soil leading to less Zn availability (Iqbal et al., 2010; Gontia-Mishra et al., 2016). In Indian context, more than 50% soils are deficient in required Zinc content (Ramesh et al., 2014). According to soil conditions, Zn deficiency is regulated by various factors like soil pH, soil organic matter and bicarbonate content, magnesium to calcium ratio, and availability of P and Fe in the soil (Wissuwa et al., 2006). These facts show that applied soluble forms of Zn fertilizers are turned readily into insoluble forms making them unavailable to plants and leads to Zn deficiency in plants. The deficiency can be mitigated by the use of Zn-based fertilizers in the agricultural crops, however, most of the synthetic fertilizers are costly and adversely affect the natural environment. To surmount this situation, an economically viable and eco-friendly solutions are needed (Kumar et al., 2017b; Mishra et al., 2017). Zinc solubilizing bacteria are the promising alternatives for zinc nutrition and crop enrichment with Zn (Barbagelata and Mallarino, 2013). Several reports are available regarding availability of Zn by plant-growth-promoting (PGP) rhizobacteria (Rokhbakhsh-Zamin et al., 2011; Sharma et al., 2012; Gontia-Mishra et al., 2016; Krithika and Balachandar, 2016). Many bacterial genera including Pseudomonas spp. and Bacillus spp. have been reported for solubilizing zinc from insoluble Zn compounds. These microbes solubilize insoluble Zn compounds through protons and oxido-reductive systems present on the cell surface, membranes, and chelated ligands (Hughes and Poole, 1991a,b; Wakatsuki, 1995). Since Zn is considered as limiting factor in sustainable crop nutrition, Zn solubilizing bacteria could play a very crucial role in Zn nutrition to field crops (Barbagelata and Mallarino, 2013; Gontia-Mishra et al., 2016).

3.3.5 Siderophores production Iron (Fe) is considered as one of the most essential micronutrient for crop production. It plays a major role in several enzymatic activities. Its major role is in photosynthesis, reduction of NO2 and SO4, and nitrogen accumulation and thus, it plays crucial role in

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biosynthesis of chlorophyll (Rashid, 1996). Unfortunately, very little quantity of Fe, out of the total available form (Fe3+) can absorbed by microorganisms (Ammari and Mengel, 2006). Low availability of iron is a global issue for sustainable crop production particularly in calcareous soils of many crops like peanut, soybean, apple trees, and peach (Marschner, 2012; Li et al., 2016). Under iron-limiting conditions, some microorganisms (also biocontrol agents) produce low molecular weight compounds, called as siderophore, which has high iron affinity. They may solubilize and acquire ferric ion followed by transfer to plants and cohabiting microorganism, and thus, depriving pathogen (Compant et al., 2005a,b) for required iron. Because of low availability of iron in many soil conditions, plants first mobilize Fe in the rhizosphere before transporting it into the plant. According to Stintzi et al. (2000), translocation of the ferric complex involves two distinct mechanisms, that is, common iron-siderophore method and shuttle system. Siderophores are categorized into three classes based on the chemical mechanism involved in the Fe chelation, viz. catechol/phenol, hydroxycarboxylic acid, and hydroxamate. Currently, chemical structures of about 270 out of 500 known siderophores have been determined (Hider and Kong, 2010). A cold-resistant mutant of Pseudomonas fluorescens has been reported to increase colonization and plant growth of mungbean crop (Katiyar and Goel, 2004). In another study, maize seed inoculated with siderophore producing Pseudomonas chlororaphis was described to increase the root shoot biomass and germination percentage (Sharma and Johri, 2003). Many bacterial proteins are responsible for Fe uptake and transport. Iron uptake by bacterial species depends on the inherent available concentration of Fe in soil. Very limited research is available with respect to the ability of siderophores in improvement of Fe nutrition in crop plants. Information about the capacity of siderophores to enhance Fe uptake by plants is scanty, hence in-depth research is further required in this context.

3.3.6 Plant-growth promotion Endophytic bacteria-mediated plant-growth enhancement through production of phytostimulator is probably the well-documented mechanism which causes structural and morphological manipulations in the host. From above facts, endophytes can be utilized in crop production system (Sturz et al., 2000). The method of phytostimulator production by endophytic bacteria in host plants is similar to that of plant-growthpromoting bacteria (PGPB) (Table 3.3). In nonlegumes, they may increase their growth through the production of phytohormones like gibberellic acid (Khan, 2014), ethylene (Kang et al., 2012), IAA (Khan, 2014; Patel and Patel, 2014), and auxins (Dutta et al., 2014). IAA is considered as the most important natural auxin which is commonly produced by endophytic bacteria (Ashrafuzzaman et al., 2009). Many bacterial groups were investigated to produce IAA, which controls PGP processes (Ratul et al., 2013). Other important phytohormones are cytokinins which is available in very small quantities in biological samples (Vessey, 2003). This is involved in root development and cell division (Frankenberger and Arshad, 1995) as well as in photosynthesis and

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Microbial Endophytes: Prospects for Sustainable Agriculture

Table 3.3 Efficient endophytic bacteria strains as phytohormone producer in numbers of plants Phytohormone produced IAA

Cytokinin

Gibberellin

Endophytic bacteria

Host

References

Aeromonas veronii Agrobacterium sp.

Rice Lettuce

Azospirillum brasilense Bradyrhizobium sp. Enterobacter cloacae Rhizobium leguminosarum Pseudomonas Pseudomonas, Bacillus Paenibacillus polymyxa Pseudomonas fluorescens, Rhizobium leguminosarum

Wheat Radish Rice Radish Cassia tora Turmeric Wheat Soybean Rape and lettuce Alder

Mehnaz et al. (2001) Barazani and Friedman (1999) Kaushik et al. (2000) Antoun et al. (1998) Mehnaz et al. (2001) Antoun et al. (1998) Kumar et al. (2015) Kumar et al. (2016) Timmusk et al. (1999) Garcia de Salamone et al. (2001) Noel et al. (1996) Gutierrez-Manero et al. (2001)

Bacillus sp.

chloroplast differentiation. Ethylene is a plant-growth hormone which is produced by almost all species of rhizobacteria (Primrose, 1979) and plays an important role as ripening hormone, stimulates germination, promotes root hair formation, induces growth and development, and breaks dormancy of grains and senescence. Plantgrowth promotion by consortia of bacterial genera was reported for oilseed rape, tomato, rice, and soybean (Mercado-Blanco and Lugtenberg, 2014). Root growth promotion in papaya seedlings by endophytic strains of Pantoea and Enterobacter spp. is documented by Thomas et al. (2007). The application of endophytic bacteria Pseudomonas oleovorans for organic seedling production in tomato (Thomas and Upreti, 2016) is also described. Some of the phytohormones producing endophytic bacteria include Arthrobacter, Bacillus, Bradyrhizobium, Brevundimonas, Burkholderia, Enterobacter, Herbaspirillum, Mesorhizobium, Pantoea, Pseudomonas, Rahnella, and Rhizobium genera (Yadegari and Mosadeghzad, 2012; Montan˜ez et al., 2012; Kumar et al., 2014).

3.3.7 Plant disease management Application of endophytic bacteria for suppression of diseases (biological control) can be an eco-friendly approach (Backman and Sikora, 2008; Dutta et al., 2014; Larran et al., 2015; Hong and Park, 2016) in sustainable agricultural practices. Many

Endophytic bacteria: Role in sustainable agriculture

49

endophytes like Fusarium oxysporum f. sp. pisi in pea, F. oxysporum f. sp. vasinfectum in cotton, and Verticillium albo-atrum in cotton have been reported to control several plant diseases (Hallmann, 2001). Use of endophytes to control pathogens has been more focused on soilborne plant diseases. For example, Fusarium wilt pathogen control by endophytic streptomycetes antagonists isolated from sterilized banana roots (Cao et al., 2005), management of lettuce drop caused by Sclerotinia sclerotiorum through application of Streptomyces exfoliates (Chen et al., 2016), and plant protection activity in Indian popcorn seedlings inoculated with endophyte Bacillus amyloliquefaciens subsp. subtilis against Fusarium moniliforme (Gond et al., 2015) are some promising examples of endophytes application in biocontrol of plant pathogens (Table 3.4). Application of endophytic bacteria and their metabolites were found to have promising potential in control of grapevine pathogens and diseases (Compant et al., 2013). Such bacteria may also be good inducers of plant defense mechanism besides exerting direct antagonistic effects on fungal and bacterial pathogens. Induced systemic resistance (ISR) can induce different genes to immunize the crop metabolically or mechanically by alteration of host physiology or metabolic responses, increasing cell wall strength, and enhanced synthesis of plant defense

Table 3.4 Biocontrol activity of associative/endophytic bacteria Endophytic isolates

Plants

Pathogenic fungi/bacteria

P. fluorescens EP1 Burkholderia phytofirmans PsJN Burkholderia phytofirmans PsJN P. denitrificans 1-15 P. putida 5-48 P. fluorescens 63-28

Sugarcane Grapevine

Colletotrichum falcatum Botrytis cinerea

Tomato

Verticillium dahlia

Oak Oak Tomato

P. fluorescens 63-28

Pea

Bacillus pumilus SE34 Bacillus pumilus SE34 Bradyrhizobium Sp. Strain ORS278 Paenibacillus alvei K165 Actinobacteria

Pea Cotton Arabidopsis thaliana A. thaliana A. thaliana

Bacillus cereus AR156

A. thaliana

Ceratocystis fagacearum Ceratocystis fagacearum F. oxysporum f. sp. radicislycopersici Pythium ultimum and F. oxysporum f. sp. pisi F. oxysporum f. sp. Pisi F. oxysporum f. sp. Vasinfectum Transcriptome analysis based study Verticillium dahlia Quantitative PCR analysis based study Pseudomonas syringae

From Jha, P.N., Gupta, G., Jha, P., Mehrotra, R., 2013. Association of rhizospheric/endophytic bacteria with plants: a potential gateway to sustainable agriculture. Greener J. Agr. Sci. 3(2), 073–084.

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Microbial Endophytes: Prospects for Sustainable Agriculture

chemicals. These secondary metabolites save the host from future pathogens attack (Compant et al., 2005a,b). By combining PGP organisms with pathogen antagonistic endophytic microorganisms, a holistic biocontrol strategy can be developed.

3.3.8 Stress management Plant faces a number of biotic and abiotic pressures and reacts by manipulation of own metabolic activities to acquire resistance. The bacterial endophyte may moderate plant modifications under adverse environmental conditions (Quadt-Hallmann et al., 1997). Globally, drought is the most common abiotic stresses limiting the crop productivity. Temperature variations reduce plant growth by inhibiting the photosynthetic activities. Endophytic bacteria have been demonstrated to protect hosts from the adverse temperature conditions. Besides temperature and drought, salinity stress also adversely hampers crop growth, development, and productivity. Based on the United Nations Environment Programme (UNEP) estimates, about 20% of agricultural land and 50% of cropland globally are under salinity stress (Flowers and Yeo, 1995). Endophytes have potential capacity to minimize the impact of these stresses. Several workers have reported that endophytes can enhance cold tolerance by manipulating metabolic activities pertaining to carbohydrate biosynthesis and photosynthesis, eventually resulting into assimilation of cold stress-related metabolites, that is, starch, proline, and phenolics (Barka et al., 2006; Fernandez et al., 2012). Endophytes follow same mechanisms under drought stress (Naveed et al., 2014). Similarly, glycine betaine compound is deposited in host plants under salinity stress by the action of endophytic bacteria ( Jha et al., 2011). Azospirillum lipoferum is documented to produce ABA to escape water stress in maize plants (Cohen et al., 2009). In grapevine, alteration of carbohydrate metabolism and photosynthetic process through deployment of Burkholderia phytofirmans PsJN is known to enhance the cold tolerance (Barka et al., 2006; Fernandez et al., 2012). Further, the endophyte Pseudomonas pseudoalcaligenes was reported to induce deposition of higher concentrations of glycine betaine in rice crop leading to improved tolerance against salinity stress ( Jha et al., 2011). Reports have shown that some PGP endobacteria could lower the ethylene level by secreting ACC deaminase (Nadeem, 2010).

3.4

Concluding remarks

The application of endophytic bacteria for sustainable agriculture is an economically sound, attractive, and eco-friendly approach. These bacteria have shown many beneficial impacts on their host plant and contribute significantly to sustainable agriculture. They have been documented for promoting plant growth through several functional attributes viz., increase in nutrient availability to the plants through fixation and solubilization of nutrients in soil and by producing plant-growth regulators. Besides growth promotion, endophytic bacteria provide a unique opportunity for increased plant resistance to different biotic and abiotic

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stresses. The major impact regarding application of endophytic bacteria in the agriculture is the significant reduction in the indiscriminate application of agrochemicals like pesticides, inorganic fertilizers, other artificial chemicals, etc. Successful utilization of endophytes would make crop production more eco-friendly and sustainable. Lastly and most importantly, to utilize these endophytic bacteria more efficiently, in-depth research would be required for better understanding of associative and endophytic ecology.

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Further reading Jha, P.N., Gupta, G., Jha, P., Mehrotra, R., 2013. Association of rhizospheric/endophytic bacteria with plants: a potential gateway to sustainable agriculture. Greener J. Agr. Sci. 3 (2), 073–084. Miliute, I., Buzaite, O., Baniulis, D., Stanys, V., 2015. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agr. 102 (4), 465–478. Reis, V., 2004. Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int. J. Syst. Evol. Microbiol. 54 (6), 2155–2162.