Rice (Oryza sativa) is an important food crop and it is the staple diet of over three billion people around the world, particularly in Asia¹ (Abdullah et al., 2006; Skamnioti and Gurr, 2009; Hosseyni-Moghaddam and Soltani, 2013). Nearly half of Asia’s population depends on rice as their main food source, making Asia the region with the highest rice consumption—more than 110 kg per capita annually (Hosseyni-Moghaddam and Soltani, 2013; Muthayya et al., 2014). Rice is grown in more than a 100 countries across a wide range of climatic conditions, ranging from rivers deltas to mountainous regions (Kyndt et al., 2014). Asian countries including China, India, Indonesia, Thailand, Philippines, Vietnam, Bangladesh, and Myanmar account for approximately 90% of the world’s total rice production (Khush, 2005; Abdullah et al., 2006; Muthayya et al., 2014). The other rice-producing countries include Egypt, Brazil, sub-Saharan countries, and the USA (Kyndt et al., 2014). Wherever it is grown, however, rice is susceptible to diseases with far reaching economic implications. Infection with phytopathogenic fungi are among the most worrying of these diseases as it may result in significant crop yield losses, and additionally, some of the fungi produce compounds which are potentially toxic upon consumption (Chaiharn et al., 2009; Suprapta, 2012). For instance, several Fusarium, Aspergillus, and Penicillium species are capable of producing mycotoxins (e.g., aflatoxins, citrinin, fumonisins, ochratoxin A, and zearalenone) which can be harmful to human beings if they are ingested via consumption of contaminated rice (Almaguer et al., 2012; Ferre, 2016). Given that the present methods of preventing rice diseases are not entirely satisfactory from several angles, it is imperative to seek new and effective methods of prevention in order to produce rice that is safe for consumption as well as to reduce crop yield losses.

Currently, Magnaporthe oryzae (anamorph Pyricularia oryzae) is regarded as one of the most important phytopathogenic fungi as it is the causal agent of rice blast— the most destructive disease of rice (Dean et al., 2012). M. oryzae B. Couch (anamorph Pyricularia oryzae Cav.), also known as Magnaporthe grisea (Hebert) Barr (anamorph Pyricularia grisea Sacc.), is a haploid filamentous ascomycete fungus (Bussaban et al., 2005). M. oryzae is defined as a new species distinct from M. grisea based on multilocus gene genealogy and laboratory mating experiments by Couch and Kohn (2002). On the basis of phylogenetic analysis, Magnaporthe is now separated into two distinct clades—one clade associated with Digitaria (crabgrass) maintains the name M. grisea, while the other clade associated with rice and other cultivated grasses was characterized as a novel species and given the name M. oryzae. Given the phylogenetic differences, however, there are no morphological differences between the isolates from these two clades. As a result, the names M. oryzae and M. grisea are still used interchangeably by scientists for the fungal isolates that infect rice (Besi et al., 2009; Wilson and Talbot, 2009).

Magnaporthe oryzae infects the aerial parts of the rice plant — including leaves, nodes, stems, and panicles— at all stages of development (Wilson and Talbot, 2009). Infection results in rice blast symptoms such as leaf blast, node blast, collar rot, neck rot, and panicle blast; this generally manifests as purplish/grayish/brownish/whitish spots or lesions as well as withering of leaves (Kato, 2001). This fungus was later discovered to also have the ability to infect the roots of the rice plant; and infection of the root may eventually spread to the aerial tissues, causing rice blast disease (Dufresne and Osbourn, 2001; Sesma and Osbourn, 2004). However, the exact nature and sequence of the process by which rice blast infects the roots of the rice plant has yet to be fully eludicated (Sesma and Osbourn, 2004). Rice blast disease has been reported in approximately 85 countries, mainly in Asia, Africa, and Latin America (Kato, 2001; Besi et al., 2009). Yield loss due to rice blast ranges from approximately 10–30% annually in the various rice producing countries and can reach up to 50% during disease epidemics (Skamnioti and Gurr, 2009; Ashkani et al., 2015).

Efforts have been made by researchers to identify and analyze the avirulence (AVR) genes of M. oryzae. This would serve as the basis of understanding fungal mechanisms of pathogenesis and clarifying the mechanisms responsible for the coevolution of fungal effectors and their host targets (Yoshida et al., 2009). Besides this, development of cultivar-specific resistance involving gene-for-gene system can be achieved by conditioning resistance through high-yielding rice cultivars carrying single dominant disease resistance (R) genes to a single corresponding dominant AVR gene in a particular pathogen strain (Skamnioti and Gurr, 2009). To date, four AVR genes have been isolated from M. oryzae: PWL1 and PWL2 genes which encode Gly-rich hydrophobic proteins with secretion signal sequences, AVR-Pita gene which encodes a putative secreted protein with similarity to metalloproteases, and ACE1 gene which encodes a putative hybrid protein of a polyketide synthase and a peptide synthase (Skamnioti and Gurr, 2009; Yoshida et al., 2009). In contrast, more than 25 resistance (R) genes encoding proteins that recognize M. oryzae AVRs have been mapped on the rice genome (Yoshida et al., 2009).

Besides breeding of cultivar-specific resistance, several control methods have been attempted to manage plant diseases. Among these, chemical control is the most commonly used method yielding effective management of plant diseases (Hirooka and Ishii, 2013). With reference to control of rice blast, chemical control involves the use of pesticides, specifically fungicides (Skamnioti and Gurr, 2009). A number of fungicides have been used against this disease, for instance, azoxystrobin, benomyl, carbendazim, carpropamid, dithiocarbamate, edifenphose, fenoxanil, tiadinil, tricyclazole, pyroquilon, probenazole, iprobenfos, isoprothiolane, metominostrobin, and propiconazole (Kato, 2001; Skamnioti and Gurr, 2009; Pooja and Katoch, 2014). Generally, the effectiveness of fungicides depends on several factors: the compound itself, the timing and method of application, the level of disease present, the efficiency of disease forecasting systems, and the rate of emergence of fungicide resistant strains (Kato, 2001; Skamnioti and Gurr, 2009). Although they are effective at controlling the fungal infections in rice, there are growing public concerns over the use of synthetic fungicides. Misuse and excessive use of synthetic pesticides (e.g., fungicides, insecticides, and herbicides) might cause environmental pollution, residual toxicity, development of pesticide resistance, reduce soil quality, and damage to natural ecosystems (Pimentel et al., 1991; Komárek et al., 2010; Suprapta, 2012; Yoon et al., 2013). Furthermore, human exposure to pesticides may cause poisoning and harmful side-effects to organs and/or biological processes (Fattahi et al., 2015). Pesticide poisoning is a significant occupational health issue in developing countries, likely due to insufficient or poor occupational safety practices. Appropriate work practices are essential to ensure the safety of workers, particularly in the case of agricultural workers who are often exposed to pesticides during application and handling operations such as mixing, cleaning, loading spray equipment, and disposing of empty containers (Kesavachandran et al., 2009). Side effects and symptoms caused by exposure to pesticides have been reported in several developing countries. For instance, farmers in Vietnam reported symptoms such as skin irritation, headache, dizziness, eye irritation, shortness of breath, and acetyl cholinesterase inhibition due to the exposure to various pesticides during mixing and spraying (Dasgupta et al., 2007).

New and improved fungicides with minimal side effects are required in order to prevent these concerns. Nowadays, natural products which are safe for the environment and have low toxicity to living organisms are gaining interest as important sources for the development of fungicides, and these may serve as effective substitutes for synthetic fungicides (Martínez, 2012; Yoon et al., 2013). Moreover, another alternative approach to the use of fungicides is the use of microbial antagonists as biocontrol agents (Suprapta, 2012). Biocontrol agents are microorganisms that suppress plant pathogens (Pal and Gardener, 2006); they can achieve biological control through competition, antibiosis, and hyperparasitism (Montesinos, 2003). Biological control of plant diseases is known to be more cost effective, safe and environmentally friendly as compared to the use of fungicides. Streptomyces bacteria are among the microbial antagonists that have been exploited for the biological control of plant diseases. This review aims to encapsulate the current body of knowledge of the biocontrol potential of Streptomyces against the rice blast fungus, M. oryzae.

Streptomyces is the largest genus of the phylum Actinobacteria and was first proposed by Waksman and Henrici (1943). The genus Streptomyces consists of a group of Gram-positive, aerobic, non-motile, catalase positive, and non-acid-fast bacteria with a filamentous form that resembles fungi (Flärdh and Buttner, 2009; Hasani et al., 2014). Currently, over 700 species of Streptomyces have been identified² and these bacteria have relatively large genomes of approximately 8–9 Mbp in size with a high GC content of more than 70% (Wu et al., 2005; Hasani et al., 2014; Ser et al., 2015c).

The members of Streptomyces are well-known for their ability to produce a variety of bioactive compounds with different bioactivities such as antibacterial (Schumacher et al., 2003; Ramesh and Mathivanan, 2009; de Lima Procópio et al., 2012; Kumar et al., 2014; Lee et al., 2014a,b; Ser et al., 2016a), antifungal (Lam, 2006), antiviral (Ara et al., 2014), immunosuppressive (Kino et al., 1987), anticancer, and antioxidant properties (Ser et al., 2015a; Tan et al., 2015, 2016). These bioactive compounds have important applications in various fields. For example, approximately 75% of commercially useful antibiotics were derived from the genus Streptomyces and they are thus the primary antibiotic-producing organisms exploited by the pharmaceutical industry (Pelaez, 2006; Lee et al., 2014b; Kashif et al., 2016). Streptomyces strains also have important applications in the agricultural field through their biological control potential against phytopathogens, particularly phytopathogenic fungi (Gonzalez-Franco and Robles-Hernandez, 2009). In line with this, research on the biological control of rice blast disease using different Streptomyces species has been conducted under laboratory conditions, as well as in greenhouse or growth chamber conditions.

It is known that antagonistic activities of bacteria against fungal pathogens can be achieved through three main mechanisms: competition for nutrients and space, antibiosis, and parasitism (Gonzalez-Franco and Robles-Hernandez, 2009; Boukaew and Prasertsan, 2014). The advantages of Streptomyces spp. include their ability to colonize plant root surfaces, survive in various types of soil and also produce spores which allow them to survive longer and in various extreme conditions (Gonzalez-Franco and Robles-Hernandez, 2009; Ningthoujam et al., 2009). Antibiosis happens when the antagonist present in the plant produces metabolites such as antibiotics or antifungals which can inhibit or kill the pathogen. Streptomyces spp. used as biocontrol agents produced antibiotics such as geldanamycin and nigericin for the control of plant diseases, which were proven by the presence of antibiotics in soil (Rothrock and Gottlieb, 1984; Trejo-Estrada et al., 1998). Likewise, hyperparasitism may occur due to the release of extracellular lytic enzymes such as chitinases and glucanases from the biocontrol agent (Gonzalez-Franco and Robles-Hernandez, 2009; Palaniyandi et al., 2013). It has also been shown that Streptomyces spp. are capable of producing chitinases and glucanases which play important roles in destruction of fungal cell walls (Mahadevan and Crawford, 1997; El-Tarabily et al., 2000; Gonzalez-Franco and Robles-Hernandez, 2009). The colonization ability and competitive traits of Streptomyces could result in successful competition against phytopathogenic fungi and suppression of their growth. It can be presumed that the suppression of rice blast by Streptomyces spp. might be due to these mechanisms, but further studies are required to provide evidence regarding the actual biocontrol mechanisms of Streptomyces against M. oryzae.

One of the major challenges encountered during the selection of biocontrol agents is that biocontrol agents that appear efficacious based on in vitro experiments might not be effective in controlling plant diseases in greenhouse or field conditions. The efficacy of biocontrol agents is affected by organic matter, pH, nutrient level, and moisture level of the soil. Owing to the variations in environmental conditions in different locations, biocontrol agents that perform well in in vitro conditions might fail in greenhouse or field experiments. Therefore, the environmental factors at the location where biocontrol agents will be applied should be taken into consideration during the selection of appropriate biocontrol agents. Ideally, the biocontrol agents should be isolated from and applied to locations with similar environmental factors in order to achieve successful biological control (Suprapta, 2012). Furthermore, the formulation (e.g., powder, liquid, or granule) and the method of application of biocontrol agents such as soil inoculation, seed inoculation, and vegetative part inoculation should be examined (Figure 1) as they are important in determining the outcomes of field experiments (Ou, 1980; Dubey, 1993). Soil inoculation involves mixing of the biocontrol agent with soil or spreading the biocontrol agent in sowing furrows by drip systems (Vasudevan et al., 2002). Seed inoculation involves dipping seeds in a culture of the biocontrol agent or mixing the seeds with the inoculant using appropriate wetting agents (Dubey, 1993; Vasudevan et al., 2002; Yang et al., 2008). Vegetative part inoculation involves aerial/foliar spraying of the biocontrol agent or seedling treatment by dipping the roots of the seedlings into a solution containing the biocontrol agent prior to transplantation (Vasudevan et al., 2002; Gopalakrishnan et al., 2014) (Figure 1). The appropriate application method is likely to contribute significantly to the success of the biocontrol agents in the field trials (Suprapta, 2012).

Some Streptomyces spp. have been successfully developed into commercial biocontrol agents and tested for the control of other plant diseases. For example, Streptomyces griseoviridis strain K61 (Mycostop^®), which has been tested for the control of Ceratocystis radicicola that causes black scorch on date palm and soilborne pathogens of tomato such as Fusarium oxysporum f.sp. lycopersici and Verticillium dahliae (Suleman et al., 2002; Minuto et al., 2006). Other commercial Streptomyces biocontrol agents include S. lydicus WYEC108 (Actinovate^®, Micro108^®, Action Iron^®), and S. saraceticus KH400 (YAN TEN S. saraceticus) (Elliott et al., 2009; Palaniyandi et al., 2013). Biocontrol agents are relatively safe toward humans as no adverse effects in users and other workers have been reported following exposure to these commercial products (Pest Management Regulatory Agency, 2003; U. S. Environmental Protection Agency, 2005). However, hypersensitivity may occur in certain individuals on exposure to biological dust produced during handling of S. griseoviridis strain K61 (Mycostop^®) dry end-product (Pest Management Regulatory Agency, 2003). Hence, wearing appropriate safety equipment is required when handling these agents. With reference to the control of rice blast disease, however, commercial Streptomyces biocontrol agents have yet to be developed.

Rice blast, the result of infection by M. oryzae, is the most destructive disease of rice, leading to crop yield losses and economic damage. While chemical control has been the mainstay of controlling this infection, biological control has now been introduced as an alternative for the management of rice blast disease. Biological control of plant diseases is typically inexpensive, long lasting, and safe toward the environment and living organisms; however, biological control can be a slow process and the search for suitable biocontrol agents requires considerable time and effort. Streptomyces spp. certainly demonstrate the potential to be developed as biocontrol agents due to their various beneficial properties. Based on current research findings, S. vinaceusdrappus, S. philanthi RM-1-138, S. griseofuscus, S. hygroscopicus, Streptomyces isolate 339, and S. flavotricini showed antifungal activity against M. oryzae under in vitro conditions. S. sindeneusis isolate 263 and S. globisporus JK-1 demonstrated in vitro antifungal activity against M. oryzae as well as successful biocontrol of rice blast in greenhouse experiments. Streptomyces strain BG2-53, which appears to be a novel strain, showed antifungal activity against M. oryzae under growth chamber conditions. These Streptomyces spp. possess antagonistic activities against M. oryzae, with S. globisporus JK-1 showing high control efficacy of up to 88.3%. Furthermore, studies have revealed that Streptomyces produces various compounds with antifungal activity against M. oryzae. Therefore, they are excellent candidates as biocontrol agents for the biological control of this devastating rice blast disease. In order to establish Streptomyces as biocontrol agents, more field experiments should be conducted to determine their control efficacy under different environmental conditions. Additionally, more work is needed to optimize isolation, formulation and application methods of Streptomyces in order to fully maximize their potential as effective agents to control rice blast.

The literature review and manuscript writing were performed by JL and H-LS, while TK, L-HC, PP, K-GC, B-HG, and L-HL provided vital guidance and insight for the writing. The research topic was conceptualized by L-HL and B-HG.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.