Plant growth promoting microbes: a future trend for environmental sustainability

Chapter 10

Plant growth promoting microbes: a future trend for environmental sustainability G. Chennappa1, M.K. Naik2, Nidoni Udaykumar1, M. Vidya3, M.Y. Sreenivasa4, Y.S. Amaresh2 and P.F. Mathad1 1

Department of Processing and Food Engineering, CAE, UAS, Raichur, India, 2Department of Plant Pathology, College of Agriculture, UAS,

Raichur, India, 3Centre for Nanotechnology, CAE, UAS, Raichur, India, 4Department of Studies in Microbiology, University of Mysore, Mysore, India

Chapter Outline 10.1 10.2 10.3 10.4

Introduction Plant growth promoting microbes Plant growth promoting rhizobacteria Azotobacter species 10.4.1 Growth promoters (vitamins, amino acids, indole acetic acid, gibberellic acid) 10.4.2 Hydrogen cyanide 10.4.3 Siderophores 10.4.4 Biodegradation of pesticides 10.4.5 Biocontrol 10.5 Pseudomonas species 10.5.1 DAPG 10.5.2 Pyoluteorine 10.5.3 Siderophores

10.1

163 164 164 165 165 166 166 166 167 167 167 168 168

10.5.4 Phenazine 10.5.5 Pyrrolnitrin 10.5.6 Induction of systemic resistance 10.5.7 Biocontrol 10.6 Trichoderma species 10.6.1 Secondary metabolites 10.6.2 Antibiotic compounds 10.6.3 Mycoparasitism 10.6.4 Cellulolytic enzymes 10.6.5 Biocontrol 10.7 Common applications formulations and shelf life 10.8 Seed biopriming with formulations 10.9 Conclusion References

168 168 168 169 169 169 170 170 170 171 172 172 173 173

Introduction

In agriculture, crop protection against phytopathogens relies heavily on agrochemicals. Different approaches are being used to prevent, mitigate, or control plant diseases. Beyond good agronomic practices, growers often rely heavily on chemical fertilizers and pesticides but also pesticides pose adverse effects on human health, environment, and soil biodiversity (Singh, 2013, 2015; Tiwari and Singh, 2017; Singh et al., 2018). Plant diseases result in severe losses of agricultural and horticultural crops every year and thus need to be controlled to maintain the quality and abundance of food, feed, and fiber. These losses can bring about reduced food supplies, poor quality products, and economic hardship for growers and processors. Due to unscientific methods and their extensive use, pesticides are largely distributed and contaminate soil and ground water and get deposited as sediments (Castillo et al., 2011). On the other hand, the demand for agricultural crops is increasing day by day due to the rapidly growing industrialization along with increasing population. Pesticides and chemical fertilizers reaching the soil in significant quantities have direct effect on soil microbiological aspects, environmental pollution, and health hazards (Martin et al., 2011; Chennappa et al., 2014). This to leading to alterations in ecological balance of the soil microflora, adversely affecting soil fertility and crop productivity, inhibiting nitrogen (N2) fixing bacterial activity, suppressing nitrifying bacteria and soil microbe interaction, altering nitrogen balance of the soil, interfering with ammonification, and hampering mycorrhizal symbiosis or nodulation in plants, as well as plant growth, soil structure, organic matter decomposition, and biogeochemical cycling of elements New and Future Developments in Microbial Biotechnology and Bioengineering. DOI: https://doi.org/10.1016/B978-0-12-818258-1.00010-8 © 2019 Elsevier B.V. All rights reserved.

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(Aleem et al., 2003; Reinhardt et al., 2008; Sachin, 2009; Chennappa et al., 2013, 2014; Chennappa, 2015). Increasing awareness and long-term effects of chemical residues in the soil have resulted in the need for alternative agricultural practices that are less destructive to the environment (Tiwari et al., 2018; Singh and Gupta, 2018; Vimal et al., 2018). Understanding the application of microbes for plant growth and their role in disease management is very essential. An ideal antagonistic microorganism must have the potential to compete and colonize successively in the rhizosphere to exist in a nutritionally limited environment.

10.2

Plant growth promoting microbes

The group of microbes that have a positive influence on plant growth and health are referred to as plant growth promoting microorganisms (PGPMs). The group PGPMs includes Azotobacter, Azospirillum, Pseudomonas, Acetobacter, Burkholderia, Bacillus, Paenibacillus, and members of the fungi, viz., Trichoderma, Gleocladium, and vascular arbuscular mycorrhiza. The beneficial effects of these PGPMs have been broadly attributed to their ability to produce various compounds such as phytohormones, organic acids, siderophores, atmospheric nitrogen fixation, phosphate solubilization, and antibiotics and induced systemic resistance to control plant diseases (Glick, 1995). These microbial inoculants are also used as biofertilizers, biocontrol agents, phytostimulators, and bioremediators as well (Lugtenberg et al., 2001; Chennappa, 2015; Chennappa et al., 2016a,b, 2017a,b). PGPMs produce secondary metabolites and play a crucial roles in microbe host interactions; these metabolites are important for combating the plant pathogens by altering the environment and improving their ability to compete with pathogens by inhibiting the activity of pathogens or by triggering host defenses. Biological control involves the use of beneficial microorganisms, such as specialized fungi and bacteria control plant pathogens (Monte, 2001; Raaijmakers et al., 2002). Utilization of these PGPMs against plant pathogens in agricultural crops has been proposed as an alternative to chemical pesticides (Pal and McSpadden-Gardener, 2006). Isolation and exploitation of indigenous strains with more than one antimicrobial compound having multiple and broad spectrum action will be beneficial to the farming community, which will go a long way in ensuring sustainable crops and the environment. Biological control of soil-borne diseases by PGPMs is a well-established phenomenon and has been shown to play a major role in suppression of several plant pathogens (Handelsman and Stabb, 1996). Among PGPMs, plant growth promoting rhizobacteria (PGPR) are rhizosphere competent bacteria that aggressively colonize plant roots and have ability to multiply and colonize across the ecological niches found on the roots at all stages of plant growth in the presence of competing microflora (Antoun and Kloepper, 2001).

10.3

Plant growth promoting rhizobacteria

The term PGPR was first described by Kloepper and Schroth (1980). The PGPR are a group of bacteria that actively colonize plant roots and promote plant growth and increase yield of agricultural produce. Rhizobacterial strains are found to increase plant growth after inoculation of seeds and therefore are called PGPR. Free living, root-colonizing bacteria have been studied for the past century as possible inoculants for increasing plant productivity (Kloepper, 1992). PGPR are able to increase plant nutrient uptake by introducing nitrogen fixing bacteria associated with roots (Azotobacter, Azospirillum) for nitrogen uptake, iron uptake from siderophores producing bacteria (Pseudomonas), sulfur uptake from sulfur-oxidizing bacteria (Thiobacillus), phosphorus uptake from phosphate mineral solubilizing bacteria (Bacillus, Pseudomonas), and potassium uptake from potassium solubilizing bacteria (Bacillus) respectively (Myresiotis et al., 2012). Azospirillum is also one of the best-studied growth hormone producers and other bacteria belonging to the genera are Aeromonas, Burkholderia, Azotobacter, Bacillus, Enterobacter, Pseudomonas, and Rhizobium (Ahmad et al., 2008; Ghosh et al., 2010; Chennappa et al., 2013, 2014). Enhanced supply of other plant nutrients by PGPR such as phytochrome production leads to increases in shoot and root length as well as seed germination of several agricultural crops (Ahmad et al., 2005). The production of plant growth regulators is one of the major mechanisms through which PGPR influence the plant growth and development (Javed et al., 2009). The ability to synthesize phytohormone is widely distributed among plant associated bacteria and 80% of the bacteria isolated from the plant rhizosphere are able to produce plant growth promoting substances. PGPR are characterized by a number of functions, which include improvement of plant establishment, increased plant nutrients, enhancement of nutrient uptake, improvement of soil structure, and protection against diseases (Glick, 1995). They survive in soil, multiply in the rhizosphere in response to the exudates rich in carbohydrates and amino acids, and attach to root surfaces and become endophytic by colonizing in the root cortex region (Kloepper, 1992). Plant growth promotion is also mediated by these rhizobacteria through different mechanisms, which include production of lytic enzymes

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FIGURE 10.1 Pure cultures of Azotobacter, Pseudomonas, and Trichoderma species.

such as chitinase and β-1, 3 glucanase, phenylalanine ammonia lyase, and polyphenol oxidases (Anand et al., 2010). PGPR bacteria having these properties are important for crop health management. Among the PGPR group, Azotobacter and Pseudomonas are known for their beneficial activities.

10.4

Azotobacter species

Among the entire PGPR group, Azotobacter are ubiquitous, and free living in soil, water, and sediments. Being the major group of soil-borne bacteria, Azotobacter play different beneficial roles and are known to produce varieties of plant growth promoting substances in the rhizosphere soil (Fig. 10.1). These growth promoting substances have direct influence on shoot and root length as well as seed germination of several agriculture crops. Azotobacter species are efficient in fixation, production of indole acetic acid, gibberellic acid, and phosphate solubilization (Chennappa et al., 2013, 2016a,b, 2017a,b). The species of Azotobacter can grow and survive at extreme environmental conditions; they are tolerant to higher salt concentration, pH values, and they can survive even at maximum temperature. Azotobacter species are known to produce antimicrobial compounds that are able to inhibit the growth of common phytopathogens. The species of Azotobacter are known to tolerate and survive pesticide concentration and also have the ability to degrade heavy metals and pesticides (Chennappa et al., 2014, 2018a,b; Chennappa, 2015). Azotobacter strains are potential bioagents for sustainable agriculture and control the ecological imbalance in the environment.

10.4.1

Growth promoters (vitamins, amino acids, indole acetic acid, gibberellic acid)

Vitamins, amino acids, and plant growth hormones [indole acetic acid (IAA), gibberellic acid (GA)] are essential for the growth and development of the plant and are produced by certain species of PGPR bacteria. These growth promoters are produced under congenial conditions and Azotobacter species (A. vinelandii and A. chroococcum) produce different types of vitamins such as niacin, pantothenic acid, riboflavin, and biotin, which belong to the B-group vitamins. These vitamins produced by Azotobacter are used to maintain metabolic processes of living beings and several factors that are responsible for the production of vitamins include growth conditions, pH, temperature, and availability of nutrient sources (Almon, 1958; Revillas et al., 2000). Amino acids are the building blocks of life and amino acids are biologically important organic compounds that combine to form proteins composed of amine (NH2) and carboxylic acid (2COOH). Species of Azotobacter produce different types of amino acids such as aspartic acid, serine, glutamic acid, glycine, histidine, threonine, arginine, alanine, proline, cysteine, tyrosine, valine, methionine, lysine, isoleucine, leucine, tryptophan, glutamic acid, and phenylalanine under diazotrophic conditions (Lopez et al., 1981; Revillas et al., 2000). Different bacteria genera are known to produce IAA, which is common to inhabitants of all soil ecosystems (Barazani and Friedman, 1999). Some of the bacterial species that can produce the highest amount of IAA belong to the PGPR group. IAA producing bacteria grow in more saline soil and in saline soil 75% of the bacterial isolates are more active in IAA production. Several species of Azotobacter including A. salinestris, A. tropicalis, A. vinelandii, A. armenicaus, A. nigricans, and A. chroococcum are found to produce IAA in the range of 2.09 33.28 μg mL21 (Chennappa et al., 2013; Chennappa, 2015). IAA producing PGPR strains are known to increase plant vigor (root and shoot length), seed germination, and root biomass, resulting in greater root surface area, which enables plants to access more nutrients from the soil. IAA is responsible for the division, expansion, and differentiation of plant cells and tissues and stimulates root elongation (Patten and Glick, 2002; Spaepen et al., 2007). Another important growth promoter is GA, which is produced naturally within the plant rhizosphere by bacteria and fungi. GA was first discovered by Japanese scientist Eiichi Kurosawa from a fungus called Gibberellafuji kuroi in rice plants. Gibberellins are important in seed germination and enzyme production, which mobilizes growth of new cells. GA promotes flowering, cellular

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division, and seed growth after germination (Upadhyay et al., 2009). Similarly, different species of Azotobacter isolates (A. salinestris, A. tropicalis, A. vinelandii A. armenicaus, A. nigricans, and A. chroococcum) produced GA in the range of 10.81 17.55 μg 25 mL21 (Chennappa et al., 2013, 2016a,b; Chennappa, 2015).

10.4.2

Hydrogen cyanide

Hydrogen cyanide (HCN) is a volatile, secondary metabolite that suppresses the growth or development of microorganisms and that also influences the growth and development of plants. HCN is one of the significant inhibitors of cytochrome C oxidases and other metalloenzymes, which are involved in the metabolic activities of phytopathogens. HCN is mainly synthesized by an enzyme, HCN synthetase, which is known to be associated with plasma membrane of certain rhizobacteria. Presently many bacterial species have shown to be capable of producing HCN, including species of Azotobacter, Alcaligenes, Aeromonas, Bacillus, Pseudomonas, and Rhizobium (Ahmad et al., 2008; Naik et al., 2013). As per the Lorck assay method Azotobacter species produced light orange to red color HCN metabolites (Chennappa, 2015). Some studies showed that about 50% of the Pseudomonas isolates obtained and characterized from wheat and potato rhizospheric soil are able to produce HCN. Various studies reported that HCN can inhibit the growth of phytopathogenic nematodes such as Meloidogyne javanica and Thielaviopsis basicola, which are known to cause root knot, and blackrot of tomato and tobacco in the rhizospheric soil. The subterranean termite Odontotermes obesus, an important pest in agricultural and forestry crops in India, is also controlled by HCN produced by rhizobacteria (Kannapiran and Ramkumar, 2011).

10.4.3

Siderophores

Siderophores are iron-chelating agents that are produced and utilized by a number of bacteria and fungi. These low molecular weight compounds are produced in soil rhizosphere under neutral to alkaline pH condition. Iron is one of the essential components for the cellular growth and metabolic activities of the bacteria. The bacteria utilize iron through siderophore production, which plays an essential role in determining the ability of bacteria to colonize plant roots and also in competing for iron with other microbes (Johri et al., 2003; Naik et al., 2013). A. vinelandii produces siderophores under limited iron conditions. Recently, it has been found that A. vinelandii produces different types of siderophores that are antibiotic in nature such as 2,3-dihydroxybenzoic acid, aminochelin, azotochelin, protochelin, and azotobactin (Page and Von Tigerstrom, 1988; Kraepiel et al., 2009; Barrera and Soto, 2010). The main biotechnological applications of siderophores are as drug delivery agents, antimicrobial agents, and for soil remediation. The PGPR with the siderophores producing ability can prevent the root infection by phytopathogens in the rhizospheric region. In certain conditions, plants can also use microbial siderophores as iron sources where there is a lack of sufficient iron concentration in soil (Mollmann et al., 2009; Naik et al., 2013).

10.4.4

Biodegradation of pesticides

Several physical, chemical, and biological forces act upon the pesticides when they reach the soil. However, biological forces, particularly microbes, play a more significant role in degrading the pesticides than the physical and chemical forces. Several biodegradation studies have been carried out to minimize the pesticide residues in food and feed. Many soil microorganisms have the ability to act upon pesticides and convert them into simpler nontoxic compounds. Bacterial genera like Pseudomonas, Rhodococcus, Arthrobacter spp., Burkholderia spp., Azotobacter, Clostridium, Bacillus, Thiobacillus, Achromobacter, etc., and fungal genera like Trichoderma, Penicillium, Aspergillus, Rhizopus, and Fusarium play an important role in the degradation of the toxic chemicals or pesticides in soil. Species of Azotobacter viz., A. vinelandii (RCR-4), A. tropicalis (KOP-11), A. armeniacus (GVT-11), A. salinestris (GVT-1), and A. chroococcum (SND-4-2) biodegraded three prominent pesticides such as pendimethalin, chloropyrifos, and carbendazim (up to 97%). Among them, A. tropicalis (KOP-11), A. vinelandii (RCR-4), and A. salinestris (GVT-1) isolates degraded the pendimethalin by 100% over the control (Chennappa, 2015; Chennappa et al., 2016a,b, 2018a,b). Similarly, Phorate, an insecticide, has been degraded by Rhizobium, Pseudomonas species isolated from paddy cultivated fields (Bano and Musarrat, 2003). The biodegradation abilities of bacterial species including Azotobacter and Pseudomonas fluorescens were tested for glyphosate (herbicide) and it was found that all species degraded glyphosate efficiently (Moneke et al., 2010). Azotobacter facilitates the mobility of heavy metals in the soil and thus enhances bioremediation of soil from heavy metals, such as cadmium, mercury, and lead. Reports are also revealed that A. chroococcum has the ability to degrade hydrocarbon and can be used as a biosurfactant in the treatment of marine oil

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contamination (Helmy et al., 2010). Degradation of pesticides is often considered to be by mineralization process and the degradation pathways are catechol, protocatechuic acid, gentisic acid, ferulic acid, resorcinol, and 2,4-dichloro phenoxyacetic acid (Mrkovacki et al., 2002).

10.4.5

Biocontrol

The antibiotics produced by PGPR are shown to be effective against phytopathogens and can provide protection against soil-borne fungi such as Aspergillus, Fusarium, Curvularia, Alternaria, and Helminthosporium (Khan et al., 2008; Mali and Bodhankar, 2009). The species of Azotobacter produce different types of secondary metabolites, which include 2,3dihydroxybenzoic acid, aminochelin, azotochelin, protochelin, and azotobactin (Kraepiel et al., 2009) and act as biocontrol agents by inhibiting the pathogen infections. Azotobacter species act as biocontrol agents for many plant pathogens (Agarwal and Singh, 2002; Mali and Bodhankar, 2009; Nagaraja et al., 2016). The species of Azotobacter have inhibited root colonization of different species of Fusarium viz., F. verticillioides, F. poae, F. sporotrichiodes, F. culmorum, etc., which are causal agents of infection in cereals. The metabolites produced by Azotobacter have suppressed fumonisin B-1 production by A. nigricans (Nagaraja et al., 2016; Chennappa et al., 2016a,b, 2017a,b). Antifungal activity of A. vinelandii showed maximum zone of inhibition (40 mm) against Fusarium oxysporum, which is commonly known to cause several diseases in agriculture crops such as chili and pigeon pea (Cavaglieri et al., 2005; Bhosale et al., 2013).

10.5

Pseudomonas species

Pseudomonas is a Gram-negative bacteria and it includes fluorescent as well as nonfluorescent species such as P. fluorescens, Pseudomonas putida, Pseudomonas chlororaphis, Pseudomonas aureofaciens, and Pseudomonas aeruginosa (Anand et al., 2010). Among the various PGPRs, fluorescent Pseudomonas is considered as the most important as they have both plant growth promotion activity, induced systemic resistance (ISR), and production of secondary metabolites (Fig. 10.1). In recent years, several plant root-colonizing Pseudomonas species have shown to be potent biocontrol agents in various plant pathogen systems (Thomashow and Weller, 1996). The primary mechanism of biocontrol by fluorescent Pseudomonas involves production of antibiotics such as 2,4-diacetylphloroglucinol, pyoluteorin, pyrrolnitrin, phenazine-1-carboxyclic acid, 2-hydroxy phenazines, phenazine-1-carboxamide, rhamnolipids, oomycin A, cepaciamide A, ecomycins, viscosinamide, butyrolactones, N-butylbenzene, sulfonamide, pyocyanin, pseudomonic acid, azomycin, cepafungins, and karalicin. These antibiotics are known to possess antiviral, antimicrobial, insecticidal, antihelminthic, antioxidant, cytotoxic, and antitumor activities (Fernando et al., 2005). Among the various extracellular metabolites produced by Pseudomonas species 2,4-DAPG (2,4-di-acetyl-phloro-glucinol), HCN, phenazine, pyoverdine, and pyoluteorine have prime importance in plant protection because genes involved in the production have ubiquitous distribution among fluorescent pseudomonads diversity, different mode of action, and broad spectrum activity against plant diseases (Naik et al., 2016; Vinay et al., 2016).

10.5.1

DAPG

The 2,4-DAPG exhibits antibacterial, antifungal, antiviral, antihelminthic (Bowden et al., 1965), and herbicidal properties and has played a significant role in the biological control of tobacco, wheat, tomato, rice, and sugar beet diseases (Kataryan and Torgashova, 1976; Velusamy et al., 2006; Carine et al., 2012). DAPG is the major determinant secreted by P. fluorescens in the biological control of plant pathogens (Bangera and Thomashow, 1996). Fluorescent bacterial strains positive for 2,4-DAPG obtained from rice rhizosphere showed antibiosis and suppressed growth of Xanthomonas oryzae pv. oryzae (up to 64%), the causal agent of bacterial blight of rice disease (Vasudevan et al., 2002). These results suggest that the production of 2,4-DAPG in crop rhizosphere is yet another important mechanism that reduces the severity of bacterial blight in rice (Naik et al., 2014; Vinay et al., 2016). Furthermore, detection of 2,4-DAPG gene in the endophytic region was first reported and isolated from sorghum, chickpea, pigeon pea, and green gram. Indian soils are considered to be poor in 2,4-DAPG gene possessing isolates but few isolates were obtained having 2,4-DAPG gene indicating the possibility of exploiting the rhizospheric soils for obtaining wide ranging antibiotic and other useful traits for emerging pests and diseases (Rajalaxmi et al., 2012; Naik et al., 2014). DAPG positive Pseudomonas species evaluated against plant-parasitic nematodes such as Helicotylenchus indicus, Xiphinema americanum, and Meloidogyne incognita and were found effective against plant-parasitic nematodes (Yuan et al., 1998; Khan et al., 2012). Similarly, Pseudomonas brassicacearum, a 2,4-DAPG positive strain, was found to be effective against Ralstonia solanacearum and results showed strong antibacterial activity (Zhou et al., 2012; Vinay et al., 2016).

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10.5.2

Pyoluteorine

Pyoluteorine is a aromatic chlorinated polyketide with resorcinol ring that is produced by fluorescent Pseudomonads and resorcinol ring is linked to a bichlorinated pyrrole moiety (Kitten et al., 1998; Nowak-Thompson et al., 1999). It was first isolated from P. aeruginosa followed by P. fluorescens Pf-5 (Bender et al., 1999). Pyoluteorin has bactericidal, herbicidal, and fungicidal properties. Application of Pyoluteorin to cotton seeds suppressed cotton damping-off disease. Pyoluteorin is found to be more effective especially against Pythium ultimum, which causes damping-off disease (Howell and Stipanovic, 1980; Maurhofer et al., 1992, 1994).

10.5.3

Siderophores

Siderophores are green fluorescent, low molecular weight compounds that are produced under iron limiting conditions, chelate the ferric ion (Fe 1 3) with a high specific activity, and serve as vehicles for the transport of Fe 1 3 into a microbial cell (Neilands, 1981), to play a vital role in controlling several plant diseases. The role of siderophores produced by fluorescent Pseudomonas in plant growth promotion was first reported by Kloepper and Schroth in 1981 (Bakker et al., 1986; Becker and Cook, 1988). Several species of fluorescent Pseudomonads like P. fluorescens, P. putida, P. aeruginosa, and P. chlororaphis produce siderophores. Siderophores produced by P. aeruginosa were evaluated for antifungal activity against three phytopathogenic fungi, Fusarium moniliformae, Alternaria solani, and Helminthosporium halodes. Siderophores inhibited the growth of F. moniliformae (92%), A. solani (89%), and H. Halodes (80%) respectively (Sharma et al., 2007; Naik et al., 2016). In addition P. aeruginosa produces another siderophore called pyochelin with a lower affinity for iron. They function as biocontrol agents by depriving the pathogens from iron nutrition thus resulting in increased yield of crops. Pyoviridines, pyochelin, salicylic acid, and quinolobactins are the major siderophores produced by fluorescent Pseudomonas. Fluorescent yellow green siderophores have been named as pyoverdines or pseudobactins. Hayen and Volmer (2005) studied siderophores including enterobactin, ferrioxamine B, ferrichrome, ferrirhodin, rhodotorulic acid, and coprogen.

10.5.4

Phenazine

Phenazine is a nitrogen containing heterocyclic antimicrobial compound that plays a vital role in the management of soil-borne phytopathogens (Pierson et al., 1995). Phenazines are synthesized by species of Pseudomonas and all phenazines exhibited broad spectrum activity against bacteria and fungi (Leisinger and Margraff, 1979; Vinay et al., 2016). The major phenazine derived by P. aeruginosa was pyocyanin (1-OH-5-methyl phenazine).

10.5.5

Pyrrolnitrin

Pyrrolnitrin is a broad spectrum antifungal metabolite produced by fluorescent and nonfluorescent Pseudomonas strains (Kirner, 1998). A phenyl pyrrol derivative of pyrrolnitrin has been developed as an agricultural fungicide. Schnider et al. (1995) reported that pyrrolnitrin actively persists in soil for at least 30 days. It did not readily diffuse and was released only after lysis of host bacterial cells. This property of slow release facilitated protection against common plant pathogen such as Rhizoctonia solani (Vinay et al., 2016; Reshma et al., 2018). Species of Pseudomonas (P. putida and P. fluorescens) having 2,4-DAPG, phenazine, siderophores, and HCN tested the antagonistic activity against R. solani (sheath blight of rice), and F. oxysporum f. sp. Ciceris (chickpea wilt). These secondary metabolites inhibited the growth of mycelium and significantly reduced the germination capacity of the sclerotia produced by pathogens (Rosales et al., 1995; Nandakumar et al., 2002; Mazurier et al., 2009).

10.5.6

Induction of systemic resistance

Induced resistance is a state of enhanced defensive capacity developed by a plant when appropriately stimulated (Van Loon et al., 1998). Inducing the plant’s self defense mechanisms by prior application of a biological inducer is thought to be a novel plant protection strategy (Ramamoorthy et al., 2001). Resistance inducing rhizobacteria offer an excellent alternative in providing a natural, effective, safe, persistent, and durable protection (Reshma et al., 2018). One classical biotic inducer is the plant growth promoting bacterium P. fluorescens Migula (Iavicoli et al., 2003). Induced resistance

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is generally systemic and can be triggered by pathogens, certain chemicals, and nonpathogenic rhizosphere bacteria. Inducing the plant’s self defense mechanisms by prior application of a biological inducer is thought to be a novel plant protection strategy (Ramamoorthy et al., 2001; Reshma et al., 2018).

10.5.7

Biocontrol

Fluorescent pseudomonads produce different secondary metabolites including a wide range of antibiotic compounds that have been used for biocontrol activity. Antibiotics include a chemically heterogeneous group of small organic molecules of microbial origin, and at low concentrations are deleterious to the growth or metabolic activities of other microorganisms (Thomashow and Weller, 1996). All these secondary metabolites contribute to disease suppression in various pathogen host plant systems. Howell and Stipanovic (1980) first established the importance of antibiotic production in the suppression of seedling pathogens such as P.ultimum causing damping off in cotton using P. fluorescens (Pf-5).

10.6

Trichoderma species

As a group, fungi have a deep impact on human life and ecosystem functionality. Fungi are the principal decomposers in the ecosphere and are essential for recycling nutrients in the environment. Trichoderma species are ubiquitous, colonizes on cellulosic materials and also in the rhizosphere of plants (Kubicek et al., 2008; Jaklitsch, 2009). Trichoderma species are free living fungi that are present in soil and root ecosystems and other natural habitats especially those containing high organic matter (Harman et al., 2004; Chennappa et al., 2017a,b). Trichoderma species have been isolated from decomposed organic matter, root surface of various plants, and decaying barks. The genus Trichoderma consists of nine species including T. aureoviride, T. hamatum, T. harzianum, T. koningii, T. longibrachiatum, T. piluliferum, T. polysporum, T. pseudokoningii, and T. viride aggregates defined largely by conidiophore morphology (Fig. 10.1). Among them, the most important species used in the field of biological control are T. atroviride, T. harzianum, T. virens, T. asperellum, and T. reesei (Benitez et al., 2004; Chennappa et al., 2017a,b). Among the different groups of fungi, Trichoderma has gained immense importance over the last few decades due to its biological control activity and use of secondary metabolites. Trichoderma species are ubiquitous and are often the predominant component of the mycoflora in soil ecosystem and play an important role in ecosystem health (KomonZelazowska et al., 2007). The ecological adaptability of Trichoderma species is evidenced by their widespread distribution, including under different environmental conditions and on various substrates. This physiological flexibility together with the antagonistic action of Trichoderma species and the ability of these fungi to promote plant growth have made them attractive biological control agents (Mariola et al., 2007). Trichoderma is the only eukaryotic fungi known to possess growth promoting and antagonistic biocompounds against a broad range of soil-borne pathogens such as that of bacteria; that is, Azotobacter, Pseudomonas, and Trichoderma are eco-friendly by nature, which makes them significantly suitable for sustainable organic agriculture practices. The beneficial action of Trichoderma species is not limited to fighting with pathogens; they have also been shown to be opportunistic plant symbionts, enhancing systemic resistance of plants (Shoresh et al., 2010).

10.6.1

Secondary metabolites

Species of Trichoderma can produce antibiotics (peptaibols), mycotoxins, and more than 100 metabolites with antibiotic activity including polyketides, pyrones, terpenes, amino acids, and polypeptides (Sivasithamparam and Ghisalberti, 1998). Paracelsin is the first characterized secondary metabolite to be isolated and characterized from Trichoderma species, which has antibiotic properties; later, different types of peptaibols were identified (Degenkolb et al., 2008; Stoppacher et al., 2008). Trichoderma asperellum has the ability to produce 43 different major volatile secondary metabolites such as 1,2-benzene dicarboxylic acid, 2-butoxy-2-oxoethyl butyl ester, 1,2-benzene dicarboxylic acid dibutyl ester, 2H-pyran-2-one, palmitic acid, several phenolic isomers, methyl cyclohexane, 1-methyl-2-nitrobenzene, isoquinoline, dibutyl ester, butyl 8-methylnonyl ester, trimethylsilyl palmitate, trans-9-octa decenoic acid, trimethylsilyl ester, p-aminotoluene, several phenol isomers (p-tert-amylphenol, 4-nonylphenol, 4-dodecylphenol, 4-(1,1,3,3-tetra methylbutyl) Phenol), n-eicosane, 8-propyl quinoline, 5-ethyl-5-propyl undecane, tetrade-cane, heptadecane, cyclooctyl methyl phosphono-fluoridoate, etc. (Nitish and Kumar, 2017).

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10.6.2

Antibiotic compounds

Most of the Trichoderma species produce antibiotics or diffusible compounds during interactions with pathogens, these compounds inhibit the colonization of pathogenic fungi. The metabolites include harzianic acid, almethicins, tricholin, peptaibols, antibiotics, 6 pentyl α-pyrone, massoilactone, viridin, glioviridin, gliosporens, and heptelidic acid (Vey et al., 2001; Reino et al., 2008). T. harzianum produced pyrone antibiotics, which are effective in controlling the Gaeumannomyces graminis var. tritici, and T. virens showed biocontrol efficiency by producing gliovirin (Howell, 1998). Trichoderma species are recognized for numerous mechanisms including competition for space and nutrients, mycoparasitism, antibiosis, inactivation of the pathogen’s enzymes, and induced resistance (Sivan and Chet, 1989; Kapulnik and Chet, 2000; Roco and Perez, 2001). Peptaibols have strong antimicrobial properties against bacteria and fungi. Peptaibols along with cell wall degrading enzymes can inhibit the growth of fungi more effectively. More than 190 peptaibols have been documented that are produced by species of Trichoderma (Neuhof et al., 2007). Gliotoxin belongs to nonribosomal peptides and it was the first metabolite isolated from species of Trichoderma (Brian, 1944). Gliotoxin is a fungistatic metabolite and it has recorded good antagonistic activity against Rhizoctonia. It is effective in cotton disease control (Whilhite and Stanley, 1996). It is also one of the most important antifungal compounds produced by species of Trichoderma and it is a very effective biocontrol metabolite. Pyrones have plant growth promoting activities and are especially effective against Sclerotium rolfsii, a common plant pathogen (Evidente et al., 2003; Reither et al., 2005).

10.6.3

Mycoparasitism

Biological mechanisms involving Trichoderma species operate by way of mycoparasitism, antibiosis, and competition. The mechanism of parasitism includes interaction such as the coiling of hyphae around the pathogen, penetration by haustoria, and release of antibiotics or other chemicals that are harmful to the pathogens and inhibit their growth (Harman et al., 2004). The antagonistic interaction established between two fungal species, which consists of the direct attack of one fungus on another, is known as mycoparasitism and this depends on recognition, attack, penetration, and killing of the host. Trichoderma is also one of the best-studied mycoparasitic fungi and it can invade many plant pathogens in a root system. Mycoparasitism is considered as the effective biocontrol strategy and Trichoderma species are effective biocontrol agents due to their antagonistic capacities against a broad range of phytopathogenic fungi. Another important factor that makes Trichoderma more effective is the production of hydrolytic enzymes and this is the key step in the successful establishment of a mycoparasitic relationship with pathogens. Trichoderma species are highly efficient producers of many extracellular enzymes like cellulases, chitinases, glucanases, proteases, etc. They are capable of secreting hydrolytic enzymes and cause mycoparasitism on fungal pathogens of plants. Trichodermin, Dermadin, Sesquierpene, Harzianum A, Harzianolide and Trichodermol, which will antagonize soil-borne pathogens (Nakkeeran et al., 2002; Kucuk and Kyvanc, 2008). They are known to possess cell wall degrading enzymes such as chitinase, β-1, 3-glucanase, β-1, 6-glucanase, cellulose, and protease (Coley-Smith et al., 1991; Bunker and Mathur, 2001; Muhammad and Amusa, 2003; Jayalakshmi et al., 2009).

10.6.4

Cellulolytic enzymes

The cell wall is the first barrier between pathogens and mycoparasites, for example, Trichoderma. The degradation of the cell wall is mediated by different set of enzymes such as chitinase, glucanase [β-(1 4), β (1 3) and β (1 6)], N-acetylglucosaminidase, and protease. Chitin is the major structural component of the fungal cell wall and is divided into 1, 4-β acetylglucosaminidases, endochitinases, and exochitinases. The second most important polymer in the cell wall is β-1 3 glucan, which is hydrolyzed by β-1 3 glucanases. Glucanases have been detected and identified in the infected region of the host and are produced by the interaction of pathogens and Trichoderma. Overproduction of these enzymes influences biocontrol efficiency, which in turn inhibits the growth and spore germination of many pathogens. Overexpression of the glucanase by T. harzianum inhibited the growth of Botrytis cinerea, R. solani, and Phytophthora citrophthora (Ihrmark et al., 2010). Proteases are also important in the degradation of fungal cell wall and T. atroviride and T. virens have more enzymes than T. reesei. Trichoderma species produce different types of proteases during mycoparasitism, which include asprtyl and subtilin like groups (Geremia et al., 1993; Seidi et al., 2009). T. harzianum inactivated hydrolytic enzymes produced by B. cinerea pathogens by secreting proteases and act as a biocontrol agents (Howell, 2003).

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171

Biocontrol

The defensive actions of Trichoderma species involve application of lytic enzymes (Kubicek et al., 2001; Viterbo et al., 2002), proteolytic enzymes (Kredics et al., 2005; Suarez et al., 2007; Chen et al., 2009), volatile metabolites (Calistru et al., 1997; Eziashi et al., 2006), and other secondary metabolites (Reino et al., 2008) against pathogens (Benitez et al., 2004). T. koningii showed its antifungal activity by producing secondary metabolites such as δ-decanolactone, 6-pentylα-pyranone and 6-(4-oxopentyl)-2H-pyran-2-one in the rhizosphere region and inhibited the common soil-borne pathogenic fungi such as R. solani, S. rolfsii, Macrophomina phaseolina, and F. oxysporum respectively (Vivek et al., 2014). Similar volatile compounds are also documented from the GCMS analyses; as many as 278 compounds such as cyclohexane, cyclopentane, fatty acids, alcohols, esters, sulfur-containing compounds, simple pyrane, and benzene derivatives from liquid cultures of T. harzianum. The compounds isolated from Trichoderma species have strong antifungal activity and the compounds include 3-methyl-heptadecanol, methyl cyclohexane, 6-nonylene alcohol, methylcyclopentane, 2-methyl heptadecanol, N-methyl pyrollidine, dermadin, ketotriol, koningin-A, palmitic acid, 3-(2ʹhydroxy propyl)-4-(hexa-2ʹ-4-dineyl)-2-(5H)-furanone, and 3-(propenone)-4-(hexa-2ʹ-4ʹ-dineyl)-2-(5H)-furanone (Dubey et al., 2011; Siddiquee et al., 2012). The Trichoderma species are able to control ascomycetes, basidiomycetes, oomycetes, and also nematodes (Monte, 2001; Benitez et al., 2004; Kyalo et al., 2007). Species of Trichoderma viz., T. aureoviride, T. virens, T. reesei, T. hamatum, T. atroviride, T. hamatum, T. harzianum, T. koningii, T. longibrachiatum, T. piluliferum, T. polysporum, T. pseudokoningii, and T. viride recorded the highest growth inhibition rate against major plant pathogens and a few of them are crop and host specific. Plant pathogens infect all parts of the plant and major infection occurs in the root system and the pathogens include Phytophthora parasitica (black eye rot of tomato), Colletotrichum capsici (Anthracnose of chili), F. solani (wilt of chili), M. phaseolina (charcoal rot of sorghum), A. solani (early blight), Rhizoctonia solani (rice sheath blight/chickpea damping-off), S. rolfsii (collar rot of orchids), Pythium sp. (damping off), F. oxysporum (wilt.), Aspergillus niger (collar rot), Aspergillus flavus (foot root), Alternaria porri (purple blotch), and S. rolfsii (bean white mold); many reports are available on biocontrol efficacy (Fig. 10.2) of Trichoderma species FIGURE 10.2 Biocontrol efficacy of Trichoderma (A1), Azotobacter (B1), and Pseudomonas (C1) isolates against plant pathogens.

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(Khan and Sinha, 2007; Kolte and Raut, 2007; Mandhare and Suryawanshi, 2008; Bagwan, 2011; Nainwal and Vishunavat, 2016; Chennappa et al., 2017a,b). Among all these compounds, 2H-Pyran-2- has been validated in mycotoxin detoxification. Additionally 2H-Pyran-2-, and volatile compounds like diethyl phthalate, 1, 2-benzene dioxylic acid esters, tetra-decanoic acid were reported to be responsible for antagonism against F. oxysporum and possesses enhanced biocontrol activity. Studies on the efficacy of volatile metabolites produced by different species of Trichoderma tested against Alternaria alternata and volatile metabolite (T. harzianum- ISO-1) showed a maximum reduction in the mycelial growth (44.60%) of A. alternata followed by T. harzianum ISO-2 (35.50%) and T. piluliferum (36.24%) respectively. T. viride has recorded maximum growth inhibition of Colletotrichum gloeosporioides (34.37%) followed by A. alternata (20%), F. oxysporum (15.21%), Rhizoctonia solani (12%), and Curvularia lunata (13.63%) (Divya, 2015). Similarly, T. harzianum has showed highest growth inhibition of C. gloeosporioides (35%) followed by F. oxysporum (14.80%), A. alternata (11.11%), C. lunata (9.52%), and R. solani (4.54 %) respectively (Sangle et al., 2016). The volatile metabolites assay revealed that the metabolites of Trichoderma species had potentially inhibited the mycelia growth of pathogens.

10.7

Common applications formulations and shelf life

Different types of formulations have been developed using P. fluorescens, B. subtillis, A. chroococcum, and T. viride either to increase crop health or to manage plant disease depending on the development formulations with suitable carriers that support the survival of bacteria for longer periods. The carriers may be either organic or inorganic in nature, and include peat, talc, lignite, kaolinite, pyrophyllite, zeolite, montmorillonite, alginate, press mud, sawdust, vermiculite, etc. The carriers maintain the survival rate of biocontrol agents by protecting them from desiccation and cell death (Heijnen et al., 1993; Dandurand et al., 1994). The aflotoxin contamination in chili and ground nut was brought down drastically with P. fluorescens, which is used for soil enrichment and foliar application (Naik and Sudini, 2011). The Trichoderma species induce various mechanisms to affect growth of plant pathogens, control disease, and improve overall plant health (Singh et al., 2004). The last decade has witnessed a tremendous breakthrough in this aspect, especially in terms of standardization of production techniques of T. harzianum or T. viride, P. florescence (against fungal diseases) for use against many insect pests and diseases. Biocontrol agents like Trichoderma are acclaimed as effective, eco-friendly, and cheap. Trichoderma is one of the common fungal biocontrol agents being used worldwide for suitable management of various foliar and soil-borne plant pathogens like Ceratobasidium, Fusarium, Rhizoctonia, Macrophomina, Sclerotium, Pythium, and Phytophthora species (Divya, 2015). Trichoderma also serve plants as biofertilizers due to their phosphorus solubilizing activity and their ability to decompose organic matter resulting in increased availability of micronutrients to the plants (Singh et al., 2004). Formulations are usually prepared as carrier-based inoculants containing effective microorganisms. Incorporation of microorganisms in carrier material enables easy handling, high effectiveness, and long-term storage.

10.8

Seed biopriming with formulations

Biopriming is a process of seed treatment using liquid formulations or biocontrol agents to protect seeds from diseases and physiological damages. Nowadays, biopriming is gaining wide importance in crop disease management. Biopriming of cowpea seeds with T. harzianum reduced root rot incidence at preemergence stage (64%) and postemergence stage (68%) after 40 days of sowing (El-Mohamedy et al., 2006). Similar reports are also recorded on biopriming of faba bean with T. viride, T. harzianum, B. subtillis, and P. fluorescens. All the biocontrol agents are effective in protecting the seeds against the incidence of faba bean root rot (El-Mougy and Abdel-Kader, 2008). Maize seeds were bioprimed with T. harzianum (1 3 108 spore mL21) and evaluated against F. verticillioides incidence, seed germination, seedling vigor field emergence, yield, and seed weight, and fumonisin production. It was recorded that the T. harzianum was more effective in reducing the disease incidence and production of fumonisin by F. verticillioides (Chandranayaka et al., 2010). Chickpea seeds on priming with bioagents (T. viride and T. harzianum) significantly reduced the wilt incidence and increased seed germination and plant growth parameters as compared with chemical fungicides (Kumar et al., 2014). Efficacy of 2,4-DAPG positive fluorescent Pseudomonas isolates were tested against chili diseases. The result showed that a consortium (P. fluorescens and T. viride) recorded the least incidence of damping off (8.50%), wilt (8.60%), followed by the application of Pseudomonas fluorescens alone (7.50% and 14%) for damping off (Naik et al., 2014).

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10.9

173

Conclusion

Hence, biodegradation of pesticides and chemical fertilizers plays an important role in agricultural practice to serve safe food to the world and clean environment for the future generations. PGPMs are natural inhabitants of the rhizosphere and have the ability to utilize the abovementioned herbicides and insecticides as a sole carbon source for their energy. Hence, use of PGPMs will help in organic farming to improve soil fertility and quality of the food produce and also to remove environmentally hazardous chemicals from the food chain, thereby ensuring the supply of healthy food for mankind. Therefore this study reveals the application of PGPMs will certainly serve as a safe alternative to chemical pesticides in the management of diseases with their potent plant growth properties.

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