Actinobacteria

Chapter 5

Actinobacteria: Eco-Friendly Candidates for Control of Plant Diseases in a Sustainable Manner Pooja Shrivastava and Rajesh Kumar Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India

5.1

INTRODUCTION

At present, two-third of the world’s population mainly rely on agriculture for their livelihood. However, the growth and production of major agricultural crops continue to be hampered year after year due to various abiotic and biotic factors (Elumalai and Rengasamy, 2012). A major concern to worldwide agricultural production is fungal plant diseases, which have been estimated to cause yield loss of up to 25% in western countries, and up to 50% in developing countries (Gohel et al., 2006; Evangelista-Martinez, 2014). The ever-increasing demand for enhanced food production, due to a continuously burgeoning population in 21st century, has pressed the need for controlling plant diseases in agriculture (Emmert and Handelsman, 1999). In fact, plant diseases need to be kept at a minimum check so as to maintain the quality and abundance of food, feed, and fiber to humankind. Several different approaches have been in use to prevent, mitigate, or control plant diseases. Beyond good agronomic and horticultural practices, farmers rely heavily on fungicides, pesticides, and chemical fertilizers. Such agricultural inputs have significantly contributed to spectacular improvements in crop productivity and quality over the past many decades. However, the environmental pollution caused by excessive use/misuse of agrochemicals, as well as warnings by some opponents of pesticides, has led to considerable changes in people attitudes towards the use of pesticides in agriculture (Pal and Gardener, 2006; Revathi et al., 2013). Many of the pesticides currently being used have a tendency to accumulate in plants for an extended time period. In addition, they also enter the food chain, including meat and dairy products, and remain as residues in the soil and the ecosystem for a long duration. This is the reason that at present there is a strict regulation on chemical pesticide use, and also the pressure to remove the most hazardous chemicals from the market and the public chain. Thus, it is urgently required to identify alternatives to such chemicals for plant protection without sacrificing the productivity and profitability of agriculture. Because of the side effects of chemical pesticides, sustainable crop production through eco-friendly, clean, and green management is an essential requirement in the present—alarming—situation (Mishra et al., 2015). A plethora of beneficial microorganisms are present in the soil in general, in rhizosphere soil in particular, and also within healthy plant tissues (endophytic). A proportion of such microbes possess beneficial properties like plant growth promotion and providing resistance to diseases. The application of microorganisms to control diseases from an environment-friendly approach is known as biological control (Lugtenberg and Kamilova, 2009). In the recent past, microbial antagonists have been widely used for the biocontrol of plant diseases as well as for plant growth promotion. The major indirect mechanism of plant growth promotion in rhizobacteria is through these biocontrol agents (Glick, 2012). In general, competition for nutrients, niche exclusion, induced systemic resistance (ISR), and antifungal metabolites production are the chief mode of biocontrol activities in beneficial microbes (Lugtenberg and Kamilova, 2009). Many rhizobacteria have been reported to produce antifungal metabolites such as HCN, phenazines, pyrrolnitrin, 2, 4-diacetylphloroglucinol, pyoluteorin, viscosinamide, and tensin (Bhattacharyya and Jha, 2012). Interaction of some rhizobacteria with the root can result in plant resistance against some pathogenic bacteria, fungi, and viruses. This phenomenon is the above-mentioned induced systemic resistance (ISR). Moreover, ISR involves jasmonate and ethylene signaling within the plant and these hormones stimulate the host plant defense responses against a variety of pathogens New and Future Developments in Microbial Biotechnology and Bioengineering. DOI: https://doi.org/10.1016/B978-0-444-63994-3.00005-9 © 2018 Elsevier B.V. All rights reserved.

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(Ahemad and Kibret, 2014). Worldwide efforts to shift from hazardous chemical control measures to an eco-friendly sustainable alternative have progressed tremendously. Among the huge variety of microbes present in the vicinity of plant and soil, actinobacteria are gram positive filamentous bacteria capable of producing secondary metabolites, viz., antibiotics and antifungal compounds. Approximately 80% of the world’s antibiotics are known to come from actinobacteria, especially from members of the genera Streptomyces (Passari et al., 2017; Hassan et al., 2011). The enormous capability of actinobacteria to produce antibiotics reveals their tremendous potential and superiority over other biocontrol measures for ensuring crop protection. Therefore, this chapter embodies the application of actinobacteria in plant disease suppression, their role as bio-inoculants in sustainable agriculture systems, and describes possible mechanisms underlying host-plant interactions.

5.2

ACTINOBACTERIA AS PLANT DISEASE SUPPRESSOR

The phenomena of disease suppression in plants occurs due to competition between antagonistic microbes and pathogens for space, nutrients, and survival in the rhizosphere and in the host plant tissues (Siddikee et al., 2010; Palaniyandi et al., 2013a). Antagonism is the property exhibited by one organism due to which it creates adverse environment for another. The antagonistic microbes exhibit various direct (production of antibiotics and lytic enzymes, and parasitism) and indirect (induction of host resistance) mechanisms to suppress pathogens. Numerous actinobacteria strains have been found to protect plants against diseases through their potential to serve as: (1) a source of agroactive compounds; (2) plant growth promoters; and (3) biocontrol agents (Doumbou et al., 2001; Abdallah et al., 2013). The antagonists depicting multiple modes for disease suppression in plants have higher success rates and may serve as potentially good biocontrol agents (Palaniyandi et al., 2013a).

5.2.1

Production of Agro-active Compounds (Antibiotics) and Volatiles by Actinobacteria

Actinomycetes have served as vast reservoir of agroactive metabolites for the past several years (Doumbou et al., 2001; Sharma, 2014; Passari et al., 2015b). Antibiotics are an important class of secondary metabolites produced by microbes which are detrimental to the growth of other microbes at lower concentrations. Antibiotics have been reported frequently from microbes, actinobacteria being the major producers, accounting for B45% of the currently-used antibiotics. Interestingly, out of the 33500 bioactive metabolites reported so far, B13,700 compounds come from actinobacteria (Berdy, 2012). In agro-environments the significance of actinobacteria is established due to their capability to synthesize a wide range of agroactive antibiotic molecules that suppress the growth and development of a broad spectrum of soil-dwelling plant pathogens. Many species of actinomycetes, particularly those belonging to the genus Streptomyces, are well known for their antifungal properties (Gopalakrishnan et al., 2011; Al-Askar et al., 2014) and as antibacterial agents (Zhang et al., 2013a; Shrivastava et al., 2017). It is estimated that three-fourths of all the Streptomyces species are antibiotic producers (Passari et al., 2017; Alexander, 1977). The first antibiotics, cycloheximide and streptomycin, used to control fungal and bacterial diseases in plants, are produced by Streptomyces griseus (Leben and Keitt, 1954). Kasugamycin obtained from Streptomyces kasugaensis is another antibacterial and antifungal metabolite which inhibits protein synthesis in microorganisms but not in mammals (Umezawa et al., 1965). Systematically developed active kasugamycin was used for control of rice blast caused by fungus Pyricularia oryzae, and bacterial diseases caused by Pseudomonas in several crops. Similarly, Isono et al. (1965) isolated two antibiotics, Polymixin B and D, from Streptomyces cacaoi var. asoensis, which primarily interfere with fungal cell wall synthesis by specifically inhibiting the enzyme chitin synthase (Endo and Misato, 1969). The agroactive antibiotic Polymixin B is deployed to control rice sheath blast disease caused by Rhizoctonia solani and also as an inhibitor of a wide range of fungal pathogens causing diseases in vegetables, fruits, and ornamental crops. Mildiomycin is another highly active antifungal metabolite obtained from Streptoverticillium rimofaciens (Iwasa et al., 1978) which inhibits several powdery mildews on various crops. Rothrock and Gottlieb (1984) evaluated biocontrol activity of geldanamycin, a new antifungal agent from Streptomyces hygroscopicus var. geldanus and S. griseus, against Rhizoctonia root rot of pea. A new antifungal antibiotic globopeptin and its in vitro antifungal activities against fungal pathogens was evaluated by Tanaka et al. (1987). Matsuyama (1991) reported AC-1, an antifungal compound from Streptomyces sp. AB-88. Kook and Kim (1995) reported a new antifungal compound Tubercidin that proved to be very effective against Phytophthora capsici blight in Capsicum annuum. Three antimicrobial compounds (guanidyl fungin A, nigericin, and geldanamycin) produced by Streptomyces violaceusniger strain YCED-9, an antifungal biocontrol agent, were reported to be effective against Pythium and Phytophthora spp. (Trejo-Estrada et al., 1998). Streptomyces diastaticus produces macrolide antibiotics Oligomycins A and C, exhibiting a strong activity against Aspergillus niger, Aspergillus

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alternata, P. capsici, and Botrytis cinerea (Yang et al., 2010). Some studies also utilized antibiotic-producing actinobacteria for controlling foliar diseases, viz. leaf spot of alfalfa (Samaca et al., 2003) and anthracnose in yam (Palaniyandi et al., 2011). A rare ant-associated actinobacteria, Propionicimonas sp. ENT-18, inhibited sclerotia formation in Sclerotinia sclerotiorum by the production of secondary metabolites (Zucchi et al., 2010). From time to time, several antifungal antibiotics have been reported from actinobacteria which are important BCAs. Some of the metabolites obtained from actinobacteria active against plant pathogens are listed in Table 5.1. TABLE 5.1 Agro-active Antifungal Metabolites (Antibiotics) Obtained From Actinobacteria Agro-active Metabolite/ Antibiotic

Producing Actinobacterium

Active Against

References

Kasugamycin

Streptomyces kasugaensis

Pyricularia oryzae

Umezawa et al. (1965)

Polymixin B and D

Streptomyces cacaoi var. asoensis

Wide range of fungal pathogens including Rhizoctonia Solani

Isono et al. (1965)

Mildiomycin

Streptoverticillium rimofaciens

Rhodotorula rubra, powdery mildew on various crops

Iwasa et al. (1978)

Geldanamycin

Streptomyces hygroscopicus var. geldanus, Streptomyces griseus

Rhizoctonia solani

Rothrock and Gottlieb (1984)

Globopeptin

Streptomyces sp. MA-23

Alternaria Kikuchiana, Pyricularia oryzae, Mucor racemosus

Tanaka et al. (1987)

Faeriefungin

Streptomyces griseus

Fusarium spp.

Smith et al. (1990)

AC-1

Streptomyces sp. AB-88 M

Pyricularia oryzae,Botrytis cinerea and Fusariumroseum f. sp.cerealis

Matsuyama (1991)

Gopalamicin

Streptomyces hygroscopicus

Erysiphe cichoracearum,Puccinia recondite, Fusarium culmorum and Pyricularia oryzae

Nair et al. (1994)

Tubercidin

Streptomyces violaceusniger

Phytophthora infestans, Phytophthora capsici

Hwang and Kim (1995)

Nigericin and Guanidylfungin A

Streptomyces violaceusniger YCED9

Rhizoctonia solani

Trejo-Estrada et al. (1998)

Daunomycin

Actinomadura roseola Ao108

Phytophthora capsici and Rhizoctonia solani

Kim et al. (2000)

RhizovitR

Streptomyces rimosus

Alternaria Brassicicola, Pythium spp., Rhizoctonia solani, Phytophthora spp., Botrytis sp.

Marten et al. (2001)

Fungichromin

Streptomyces padanus strainPMS-702

Rhizoctonia solani

Shih et al. (2003)

2,3- dihydroxybenzoic acid, phenylacetic acid, cervinomycin A1 & A2

Micromonospora sp. M39

Pyricularia oryzae

Ismet et al. (2004)

Antimycin A17

Streptomyces sp. GAAS7310

Colletotrichum Nigrum, Curvularia lunata, Rhizopus nigricans

Chen et al. (2005)

Neopeptin A and B

Streptomyces sp. KNF2047

Sphaerotheca fusca

Kim et al. (2007)

Malayamycin

Streptomyces malaysiensis

Stagonospora nodorum

Li et al. (2008)

Natamycin

Streptomyces lydicus strain A01

Monilinia laxa, F. oxysporum, Botrytis cinerea,

Lu et al. (2008)

(Continued )

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TABLE 5.1 (Continued) Agro-active Metabolite/ Antibiotic

Producing Actinobacterium

Active Against

References

Oligomycins A and C

Streptomyces diastaticus

Phytophthora capsici, Aspergillus niger, Botrytis cinerea and Alternaria alternata

Yang et al. (2010)

2-Furancarboxaldehyde

Streptomyces cavourensis subsp.cavourensis SY224

Colletotrichum gloeosporioides

Lee et al. (2012)

Antifungal mycin 702

Streptomyces padanusJAU4234

Magnaporthe grisea

Xiong et al. (2013)

Resistomycin and tetracenomycin D

Streptomyces canus BYB02

Magnaporthe grisea

Zhang et al. (2013b)

Bafilomycins B1 and C1

Streptomyces cavourensis NA4

Fusarium spp., Rhizoctonia solani, and Botrytis cinerea

Pan et al. (2015)

10-(2,2-dimethyl-cyclohexyl)-6,9dihydroxy-4,9-dimethyl-dec-2-enoic acid methyl ester (SH2)

Streptomyces hydrogenans strain DH16

Alternaria brassicicola

Kaur et al. (2016)

Many actinomycetes are reported to possess insecticidal properties. Avermectins from soil actinobacteria Streptomyces avermitilis are a series of 16-memeber macrocyclic lactone derivatives possessing antihelminthic and insecticidal properties (Omura and Shiomi, 2007). Worldwide, avermectin B1 (abamectin) has been widely used in agriculture for the development of bioformulations to control phytophagous mites and insect pests on a variety of Agrihorticultural crops. It is currently registered for its use as foliar spray on ornamental plants, cotton, citrus, pear, and vegetable crops. Abamectin does not persist or accumulate in the environment and thus there is the least chance of it contaminating the environment (Lasota and Dybas, 1990). The instar larvae and pupae of cotton leaf worm Spodoptera littoralis were reported to be destructed by secondary metabolites of some actinobacterial isolates including Streptomyces and Streptoverticillium (Bream et al., 2001). Liu et al. (2008) observed that quinomycin A, an active compound extracted from ethyl acetate extract of Streptomyces sp. KN-0647, significantly inhibited the growth of pathogenic insects Culex pipiens, Plutella xylostella, Aphis glycines, Dendrolimus punctatus, and Spodoptera exigua. Avermectin B1 extracted from Streptomyces sp. 173 exhibited a strong insecticidal activity against brine shrimp and Helicoverpa armigera (Xiong et al., 2004). The entomopathogenic properties of Brevibacterium frigoritolerans against Anomala dimidiata and Holotrichia longipennis, and grub mortality occurring between the second and fifth weeks after inoculation under in vitro conditions, was reported by Selvakumar et al. (2011). Recently, Sathya et al. (2016) reported a compound, diketopiperazine cyclo(Trp-Phe) from Streptomyces griseoplanus SAI-25, having insecticidal activity against cotton bollworm, H. armigera. Apart from antibiotic production, some BCAs are also reported to produce volatile compounds as tools for inhibition of pathogens. Some of the important volatile compounds include hydrocyanic acid (HCN), certain acids, alcohols, ketones, aldehydes, and sulfides (Bouizgarne, 2013). Members of the genus Streptomyces have been reported to produce volatile antifungal compounds and their biocontrol (Palaniyandi et al., 2013a). Moore-Landecker and Stotzky (1973) observed several morphological abnormalities in fungi such as Aspergillus giganteus, Fusarium oxysporum, Penicillium viridicatum, Trichoderma viride, and Zygorhynchus vuilleminii, due to the effect of volatile substances from actinomycetes. Streptomyces griseoruber produces methyl vinyl ketone, a volatile substance that inhibits spore germination in Cladosporium cladosporioides (Herrington et al., 1987). Wang et al. (2013) reported that Streptomyces alboflavus TD-1 synthesized compounds which inhibited growth of pathogenic fungi such as Fusarium moniliforme, Aspergillus flavus, Aspergillus ochraceus, Aspergillus niger, and Penicillium citrinum in vitro. The GC-MS analysis revealed 27 different compounds responsible for the inhibitory action, among which dimethyl disulphide was proved to have inhibitory activity towards F. moniliforme in vitro. Boukaew et al. (2013) did more detailed study with Streptomyces philanthi RM-1138, which restricted the growth of R. solani PTRRC-9, Pyricularia grisea PTRRC-18, Bipolaris oryzae PTRRC-36, and Fusarium Fuzikuroi PTRRC-16, and reported that volatiles from 14-day old cultures had stronger inhibitory action compared to 7-day old cultures. This was due to the production of 36 compounds in 14-day old culture in contrast to only 17 compounds produced in 7-day old culture. The volatile substances were able to reduce sheath blast disease

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caused by R. solani PTRRC-9 by destructing its cell wall. The volatiles produced by actinobacteria have tremendous potential as bio-fumigants in agriculture. They may become eco-friendly alternatives to chemical fumigants such as methyl bromide, 1, 3-dichloropropane, or chloropicrin.

5.2.2

Hyperparasitism/Mycoparasitism

Hyperparasitism is a phenomena exhibited by a variety of bacteria and fungi in which they feed upon pathogenic microbes. In hyperparasitism the BCA directly attacks the pathogen, parasitizes and finally kills it. Hyperparasites are reported to penetrate the fungal hyphae forming branches and coagulating its cytoplasm, ultimately leading to destruction of the hyphae (Upadhyay and Rai, 1987). Tu (1998) reported a S. griseus strain which parasitized Colletotrichum lindemuthianum and grew on hyphae surface. The strain exhibited internal parasitism of host hyphae resulting in the formation of several blebs. Cell walls of the parasitized C. lindemuthianum hyphae degenerated, having a sponge-like texture and holes. Similarly, Streptomyces griseoviridis strain K61 (the main component of fungicide Mycostop) has shown mycoparasitism on several fungal pathogens including Pythium, R. solani, and F. oxysporum. S. griseoviridis was the most effective against Alternaria conidia, which were completely colonized by the actinobacteria and finally destructed (Tapio and Pohto-Lahdenpera¨, 1991). In recent years, mycoparasitism has been demonstrated as an antagonistic mechanism towards fungal pathogens in Streptomyces cyaneofuscatus ZY-153, S. kanamyceticus B-49, Streptomyces rochei X-4, and Streptomyces flavotricini Z-13 (Xue et al., 2013). Shrivastava et al. (2017) have reported mycoparasitism in Streptomyces aureofaceins strain K20 against Macrophomina phaseolina. All these strains exhibited a combination of coiling and lysis as mechanisms of hyperparasitism. In addition to Streptomycete actinobacteria, non-Streptomycete actinobacteria have also been reported to exhibit mycoparasitism. Nocardiopsis dassonvillei have been reported to show antibiotic, mycolytic, and parasitic activities against the vegetative hyphae of F. oxysporum f. sp. albedinis (Sabaou et al., 1983). Upadhyay and Rai (1987) observed mycoparasitism (coiling penetration, branching of growing hyphae inside fungal host, and hyphal lysis) in Micromonospora globosa-parasitizing Fusarium udum. Some other non-Streptomycete actinobacteria also show mycoparasitic activity, which has been reviewed in detail by El-Tarabily and Sivasithamparam (2006). It is not necessary that microbes showing mycoparasitic activity in vitro should exhibit the same mechanism to suppress plant diseases under open field conditions. Sutherland and Papavizas (1991) encountered the same issue when actinobacteria which parasitized oospores of P. capsici in vitro were rendered ineffective under greenhouse conditions and failed to control the crown rot of pepper. To now, no study has revealed mycoparasitism as a sole mechanism of disease suppression in plants. Mycoparasitism is always initiated when the antibiotics and hydrolytic enzymes produced by antagonistic microbe weaken the fungal hyphae, making it susceptible for parasitization (El-Tarabily and Sivasithamparam, 2006).

5.2.3

Competition and Rhizosphere Colonization

Soil is a reservoir harboring a plethora of microorganisms that maintain its integrity and structure. There is the existence of a large group of potential competitors in soil, and diverse mechanisms may be responsible for the dominance of certain microbial populations (Hibbing et al., 2010). BCAs compete with the disease-causing pathogens for space and nutrition, thus creating a nutrient limiting environment for the pathogens, making their survival difficult. Monod (1949) demonstrated that nutrient availability plays an important role in microbial competition. The competition between the pathogen and antagonist for space and nutrients mainly occurs in the vicinity of plant roots, i.e., the rhizosphere. The rhizosphere contains both beneficial and harmful microbes with complex interactions (Compant et al., 2010; Glick, 2012). The harmful microbes struggle for nutrients with plants and cause diseases while beneficial microbes support the plants by nutrient mobilization, growth stimulation, protection from abiotic stress, and disease suppression (Compant et al., 2010; Yandigeri et al., 2012; Shrivastava and Kumar, 2015). Roots exude numerous nutrients that include organic acids, amino acids, sugars, vitamins, enzymes, purines/nucleosides, inorganic ions and gases, phytosiderophores, phenolics, flavonoids, and root border cells (Dakora and Phillips, 2002, Palaniyandi et al., 2013a). The exudates secreted by roots play a crucial role in the microbial struggle for nutrients and thus determining the specific community of microbes living in its surroundings. Chemotactic response and active motility towards these chemical attractants present in root exudates govern reception/interaction of BCAs to the root surface (Singh, 2014). Neeno-Eckwall et al. (2001) reported competition and antibiosis as mechanisms of potato scab disease suppression in disease-conducive soil by nonpathogenic Streptomyces scabiei and antibiotic-producing Streptomyces diastatochromogenes.

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New and Future Developments in Microbial Biotechnology and Bioengineering

The most commonly studied type of competition for pathogen suppression in the rhizosphere is for the nutrient, iron. The concentration of iron in the rhizosphere is generally found to be extremely low (Pal and Gardener, 2006) and scarcity of its bioavailability in soil habitats creates a furious competition. Iron is a vital growth element for all living organisms, including plants and microbes. Under iron-limiting conditions, microbes produce high affinity iron chelating compounds called siderophores (Singh, 2014). These chelators bind Fe31 molecules, forming complexes which are taken up by bacteria using specialized receptors (Crosa, 1989) and are made available to plants. Microbes with the potential to produce siderophores with the highest affinity for iron efficiently colonize the rhizosphere while those producing low affinity siderophores are eliminated (Kloepper et al., 1980). Several actinobacteria producing siderophores have been reported to suppress plant pathogen-causing diseases (Sontag et al., 2006; Khamna et al., 2009; Verma et al., 2011; Gopalakrishnan et al., 2013; Passari et al., 2015a). Ruanpanun et al. (2010) reported actinobacterial isolate Streptomyces sp. CMU-MH021 with a high ability to produce IAA and siderophore as potential biocontrol agent against root knot nematode Meloidogyne incognita, and fugal plant pathogen. In a study performed by Barona-Gomez et al. (2006) multiple siderophores production by certain Streptomyces spp. was reported. Moreover, the production of multiple siderophores is advantageous in soil as it minimizes competition from siderophore cross-utilizing bacteria (Challis and Hopwood, 2003; Palaniyandi et al., 2013a). Siderophores produced by Streptomyces albovinaceus, S. griseus, and S. virginiae inhibit the germination of basidiospores of Moniliophthora perniciosa (Macagnan et al., 2008). Siderophores produced by certain actinobacteria were also shown to promote growth of other actinobacteria (D’Onofrio et al., 2010). This cross-utilization of siderophores within the actinobacterial community can result in enrichment of these microbes in the plant rhizosphere, leading to pathogen elimination. Rhizosphere colonization is an essential character for BCAs against the pathogens, and higher colonization of biocontrol agents should reduce disease incidence (Doumbou et al., 2001). The advantages of actinobacterial BCAs (Streptomyces spp.) over other microbes include their ability to colonize plant root surfaces, survive in various types of soil, and spore production which allows them to survive longer in various extreme conditions (Yandigeri et al., 2012). The colonization ability and competitive traits of Streptomyces could result in successful competition against phytopathogenic fungi and suppression of their growth (Law et al., 2017).

5.2.4

Cell Wall Degrading (Hydrolytic) Enzymes

Various extracellular hydrolytic enzymes produced by microbes play an important role in the suppression of plant pathogens. Several biocontrol actinobacteria produce enzymes including chitinases, cellulases, β-1, 3 glucanases, proteases, and lipases that can lyse a portion of the cell wall of many pathogenic fungi (Glick, 2012). Chitinase and β-1, 3-glucanase attack chitin and β-1, 3-glucan, major constituents of the fungal cell wall, resulting in its degradation and further killing of the pathogens (Singh, 2014). Many Streptomyces spp. have been reported as producers of hydrolytic enzymes degrading the fungal cell wall such as hemicellulases, cellulases, proteases, chitinases, and glucanases and the role of these enzymes in biocontrol potential and antifungal activity has been evaluated (Kaur et al., 2013; Passari et al., 2016a,b). Among actinomycetes, species of the genus Streptomyces are well-known producers of chitinase, and hence the potential application of chitinase for biocontrol of fungal phytopathogens is promising (Kim et al., 2003; Mukherjee and Sen, 2006). The chitinase-producing strains could be utilized either directly in biocontrol or indirectly by using purified proteins or through gene manipulation (Doumbou et al., 2001; Sonia et al., 2011). Biocontrol of anthracnose in pepper has in part been attributed to the production of chitinase and glucanase by Streptomyces cavourensis SY224 (Lee et al., 2012). Endophytic Streptomyces strains producing chitinase are considered as potential BCA (Quecine et al. 2008), and a chitinase-producing S. violaceusniger XL-2 was able to suppress wood-rotting fungi (Shekhar et al., 2006). Glucanolytic actinomycetes reduced root rot in raspberry seedlings caused by Phytophthora fragariae var. rubi (Valois et al., 1996). El-Tarabily (2006) reported that isolates of Microbispora rosea, Micromonospora chalcea, and Actinoplanes philippinensis produced β-1,3, β-1,4, and β-1,6 glucanases that caused lysis of Pythium aphanidermatum hyphae in vitro and reduced damping-off disease of cucumber under glasshouse conditions. These isolates were able to suppress damping-off in soil amended with or without cellulose. Yandigeri et al. (2015) reported that a marine actinobacteria Streptomyces vinaceusdrappus S5MW2 endowed with chitinolytic potential provided resistance to tomato plants against the fungal pathogen R. solani. Manivasagan et al. (2010) isolated 10 actinobacteria from sediment samples of the Kodiyakarai coast, Bay of Bengal, India, having multiple enzyme activity including amylase, cellulase, and protease. Involvement of protease in antifungal activity was also demonstrated in a Streptomyces sp. strain A6, that produced a 20-KDa protease with inhibitory action towards F. udum spore germination (Singh and Chhatpar, 2011). Palaniyandi et al. (2013b) reported a novel mechanism of biocontrol by a Streptomyces sp. strain ExPro138, which produces multiple extracellular proteases

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causing inhibition of spore adhesion, germination, and appressorium formation in Colletotrichum coccodes. The protease preparation from this strain reduced anthracnose incidence in tomato. Thus, actinobacteria employing hydrolytic enzymes as one of the mode of actions against phytopathogens could be a good choice to be exploited as BCAs.

5.2.5

Induction of Systemic Resistance

Certain biocontrol agents show indirect mode of antagonism against the pathogens and induce a state of plant resistance against the pathogens. This nonspecific defense provides resistance to a broad spectrum of pathogens. Induced resistance is the form of defense mechanism in plants, elicited by the interaction with an external factor, which can be of either chemical or biological origin. Two types of nonspecific defense responses are reported in plants: (1) beneficial microbe-induced systemic resistance (ISR); and (2) pathogen-induced systemic acquired resistance (SAR) (Schuhegger et al., 2006). The ISR does not target specific pathogens; rather, it may be effective at controlling diseases caused by different pathogens (Glick, 2012). Regulation of ISR defense response is under phytohormone control, jasmonic acid (JA), and/or ethylene among the major regulators (Pieterse et al., 2009). Different soil-beneficial microorganisms have been shown to trigger ISR in plants, usually relying on JA signaling (van Loon et al., 2006; Pieterse et al., 2014). Lehr et al. (2008) reported systemic resistance in Norway spruce provided by root inoculation with Streptomyces GB 4-2 against needle pathogenic fungus B. cinerea. Streptomyces GB4-2 also extended from root rot caused by Heterobasidion abietinum in Norway spruce seedlings by altering the cell wall architecture. Endophytic actinobacteria isolated from healthy wheat tissue with antagonistic ability against wheat fungal pathogens were reported to induce defense pathways in Arabidopsis thaliana (Conn et al., 2008). Inoculation of A. thaliana (Col-0) with selected endophytic strains induced a low level of SAR and JA/ET gene expression, measured using quantitative polymerase chain reaction. Upon pathogen challenge, endophyte-treated plants demonstrated a higher abundance of defense gene(s) expression compared to those of non-endophyte-treated controls. Resistance to bacterial pathogen Erwinia carotovora subsp. carotovora required the JA/ET pathway, whereas resistance to the fungal pathogen F. oxysporum involved primarily the SAR pathway. The endophytic actinobacteria appear to be able to “prime” both the SAR and JA/ET pathways, up-regulating genes in either pathway depending on the infecting pathogen (Conn et al., 2008). In a study by Zhao et al. (2012) it was observed that culture filtrate from Streptomyces bikiniensis HD-087 induced systemic resistance in cucumber against Fusarium wilt, caused by F. oxysporum f.sp. cucumerinum. In another report, Micromonospora strains isolated from surface sterilized nodules of alfalfa showed in vitro antifungal activity against several pathogenic fungi. Moreover, in tomato plants the root inoculated with these Micromonospora strains effectively reduced leaf infection by the fungal pathogen B. cinerea, despite spatial separation between both microorganisms. The induced systemic resistance, confirmed in different tomato cultivars, was long lasting. The gene expression analyses further confirmed that Micromonospora stimulated the plant capacity to activate defense mechanisms upon pathogen attack. The response of tomato plants inoculated with Micromonospora spp. exhibited stronger induction of jasmonate-regulated defense when challenged with a pathogen (Martı´nez-Hidalgo et al., 2015). Recently, Singh and Gaur (2017) reported endophytic Streptomyces spp. triggered systemic resistance in chickpea under Sclerotium rolfsii stress. The endophytic Streptomyces spp. displayed priming with the plant for mitigation of oxidative stress generated by the pathogen. Hence, it can be concluded that ISR results in alteration of host plant physiology, metabolic responses and strengthening of the plant cell wall, leading to an enhanced synthesis of plant defense chemicals upon challenge by pathogens and/or abiotic stress factors (Nowak and Shulaev, 2003; Singh, 2014).

5.3

COMMERCIAL BIOCONTROL AGENTS FROM ACTINOBACTERIA

Actinobacteria manifest various mechanisms of plant growth promotion and biocontrol. To utilize this potential in sustainable agriculture for crop protection and production, formulation of the actinobacteria is necessary. Several commercial formulations of actinobacteria, viz., antibiotics or microbes as active ingredients are marketed for biocontrol of plant diseases. Streptomyces grieoviridis strain K61 under the name Mycostops is the first commercial actinobacteriabased biocontrol agent made available for crop protection. It contains actinobacteria as active ingredients and is marketed as wettable powder for use against soil-borne fungal pathogens such as Pythium, Alternaria, Fusarium, Botrytis, Phytophthora, and Rhizoctonia (Sabaratnam and Traquair, 2002). Mycostop has also been reported for control of root rot disease of cucumber and fusarium wilt of carnation and it has also been used in greenhouse production to protect flowers from pathogens (White et al., 1990). Another well-studied BCA is Actinovates, a biocontrol formulation of Streptomyces lydicus WYEC 108 registered from AgBio in the United States of America. It has been suggested for a wide range of environments ranging from greenhouses to field conditions for control of soil-borne pathogens and as

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foliar spray (Elliott et al., 2009; Palaniyandi et al., 2013a). MicroPluss, another formulation of S. lydicus WYEC 108, has been reported to control powdery mildew and several root decay fungi. Other commercial Streptomyces biocontrol agents include S. lydicus WYEC108 (Action Irons), and Streptomyces saraceticus KH400 (YAN TEN S. saraceticus) (Elliott et al., 2009; Palaniyandi et al., 2013a). S. violaceusniger YCED9 has been developed into a BCA for thatch removal from lawn under the commercial name “Thatch Control”. Fungal diseases of turfgrass are reported to be reduced with a zeolite formulation of spores from S. hygroscopicus YCED9 and WYE53, which provided protection against P. ultimum, F. oxysporum, R. solani, Gaeumannomyces graminis, and Microdochium nivale to Kentucky blue grass seedlings (Chamberlain and Crawford, 1999). Besides the commercial actinobacterial BCA having actinobacteria as an active ingredient, some of the antibiotic compounds from actinobacteria are also used commercially for biocontrol. For example, Polyoxin D (by Streptomyces cacoi var. asoensis) under the name AFFIRMWDG and PH-Ds are used as fungicide for turf grass fungi. Similarly, streptomycin (produced by S. griseus) is used in different countries as bactericide under the names Agri-Mycin 17 WP (USA), Keystreptot (New Zealand), Streptomycin (Switzerland), Strepto (Belgium), Ag-Plantomycin WG (Germany), and Plantomycin (The Netherlands). Likewise, Kasugamycin (produced by S. kasugaensis) is available commercially as bactericide under name Kasumint in Canada, while in India it comes under the names Biomycin and Omycin and plays dual role as both fungicide and bactericide (Rezzonico et al., 2009; Hamedi and Mohammadipanah, 2015).

5.4

MERITS OF ACTINOBACTERIAL BCAS

Actinobacterial biocontrol agents and agro-active metabolites are naturally occurring compounds which inhibit plant pathogens and pests by nontoxic mechanisms. The beneficial effects of actinobacterial formulations and metabolites have been well analyzed. Thus the agro-active antibiotics of actinobacteria and bioinoculants containing actinobacteria as an active ingredient are taking commercial importance in the market. The advantages of adopting actinobacterial formulations over other products are due to their strong colonization ability (Kortemaa et al., 1994), and production of spores resistant to heat, irradiation, and drought (Yandigeri et al., 2012). Actinobacteria may convert plant exudates into such forms that are utilized by another plant growth-promoting bacteria in the rhizosphere. Some actinobacterial species have emerged to act both as biopesticides and biofertilizers. Contrary to hazardous chemical pesticides and fertilizers, actinobacterial inoculants when applied to the soil improve the texture and structure of soil, due to their filamentous biomass (Hamedi and Mohammadipanah, 2015). One of the major advantages of actinobacterial BCAs over other microbe-based BCAs is that a number of other microbes have emerged as opportunistic human pathogens. Actinobacterial-based BCAs affect only few specific target pathogens or organisms, and also decompose easily in a shorter period of time, thereby eliminating the chances of environmental pollution. Actinobacteria supports the colonization of mycorrhiza, growth of beneficial insects and earthworms, and moreover augments soil immunity and plant defense to restrict unwanted plant diseases and parasites. Keeping in mind the enormous potential of the actinobacteria and their dominance and frequency in the soil regime, it would be judicious to promote these inoculants as BCAs.

5.5

FUTURE PERSPECTIVES AND CONCLUSION

The integrated pest management in modern agriculture is based mainly on two important principles: one is the maximum reduction in environmental pollution, while controlling the plant pathogen and pests, and the other is enhancing agricultural productivity to feed the increasing global population. Chemical fertilizers and pesticides can meet the aims of integrated pest management, but the indiscriminate use and persistent nature of such chemicals have exerted several adverse effects on the environment, leading to global concerns (Babalola, 2010). That is why global efforts for exploration of alternative natural products for the crop protection market have expanded tremendously in last decade. Bioinoculants, due to their eco-friendly nature and cost-effectiveness, have become a leading choice in sustainable disease management practice and are able to compete with traditional practices involving chemical fertilizers and pesticides. Actinobacteria are excellent candidates as BCAs for the biological control of different plant diseases. They are considered as the most prominent source of bioactive compounds (antibiotics, enzymes, and plant growth modulators) facilitating plant disease suppression as well as growth promotion. Besides making agriculture systems sustainable, soil inhabiting actinobacteria play important roles in various ecological processes such as organic matter decomposition and toxic pollutant and heavy metal bioremediation, thereby contributing to the environmental sustainability and restoration of soil fertility. Although a lot of research has been carried out and is undergoing on antagonistic and plant growth promotory actinobacteria, still the commercial actinobacterial bioinoculants (BCAs) available on market are very limited. To overcome this issue it is necessary to conduct extensive field level evaluations of the BCAs and to have better

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understanding of the interaction between the antagonistic agents with the plant system, indigenous microbes, pathogens, and the environment. Moreover, the factors which are detrimental for proper functioning of the BCA in the field should be focused to obtain the optimum benefits (Bouizgarne, 2013). Challenges for future research work concern not only the biology of these microbes, but also the practices required to protect their biodiversity and to extend their application in the wide range of soil types and eco-systems. Agriculture cannot be successful and sustainable until plants and beneficial microbial species are integrated, a goal for which new knowledge and information-based approaches are urgently needed. It is of utmost importance to educate the farming community and the layperson about the advantages of microbial bioinoculants, without which all the research will remain in laboratories only (Glick, 2012). Eliminating the above-mentioned constraints, it is very sure that in the near future the agriculture sector will shift its focus to the effective use of actinobacterial BCAs, paving a bright and successful path for eco-friendly and sustainable crop protection practices.

ACKNOWLEDGEMENTS The authors are thankful to UGC, New Delhi for providing financial assistance in the form of fellowship and BBAU, Lucknow for providing the platform to work.

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FURTHER READING Li, Q., Ning, P., Zheng, L., Huang, J., Li, G., Hsiang, T., 2012. Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biol. Control 61 (2), 113 120.