Studies on Endophytic Actinobacteria as Plant Growth Promoters and Biocontrol Agents

Abstract

The exploration of microbial resources is necessary for plant growth promotion, biological control, and reducing the agrochemicals and fertilizers for sustainable agriculture. Bacteria and fungi are distributed in the biosphere including the rhizosphere and help the host plants by alleviating biotic and abiotic stress through different mechanisms and can be used as bioinoculants for biocontrol and plant growth promotion. Actinobacteria are among the most abundant groups of soil microorganisms. They have been studied for their function in the biological control of plant pathogens, interactions with plants, and plant growth promotion. Streptomyces is the largest genus of actinobacteria. Streptomyces acts as both plant growth promoter and also as plant disease suppressor by various mechanisms like an increase in the supply of nutrients such as phosphorus, iron, production of IAA, and siderophore production. Endophytic actinobacteria help in plant growth-promoting through multiple ways by producing plant hormones; controlling fungal disease through antibiosis and competition. This review briefly summarizes the effects of actinobacteria on biocontrol, plant growth promotion, and association with plants as endophytes.

1. Introduction

Agricultural activity is hampered by various plant diseases and non-living factors i.e., temperature, drought, salinity, etc. [1]. To prevent plant diseases several pesticides are used in the present day. The reason behind environmental pollution and the loss of soil fertility in crop fields is due to excessive use of chemical products in agriculture [2]. In recent years, due to environmental pollution, the use of chemical pesticides and fertilizers has been canceled in several countries. But nowadays many workers have given attention on the utilization of microbial antagonists to reduce the unrestricted use of chemical products which are applied to prevent plant disease. According to Vurukonda et al. [3] in place of chemical pesticides plant growth-promoting microbes are approved as a safe substitute in the agricultural field. Several microorganisms are known to act as a plant growth promoter and they have the capability to suppress plant disease [4, 5, 6, 7]. Among microbes, actinobacteria are known to produce secondary metabolites, antimicrobial compounds, and plant growth-promoting regulators to improve agricultural developments [8, 9, 10]. Actinobacteria are gram-positive bacteria. Various plant pathogens are controlled by different types of antibiotics which are generally obtained from actinomycetes. Extensive use of chemical products in agriculture imparts deleterious effect on the environment and on the health of human too. Microbial pesticides act as a better and safer alternative way of chemical pesticides. For the growth of plants, the production of biological pesticides from actinobacteria is considered to be a more economical and safe method. The formation of biological pesticides is more useful in function compared to chemical pesticides. These harmful chemicals can be replaced by biological products of actinomycetes. The workers have found another way to obtain large vigor in vegetables with safety by applying the group of actinobacteria to avoid chemical fertilizers [11]. These biopesticides maintain the quality of crops as well as productivity of crops without any harmful effect on plants. In nature, actinobacteria are mostly distributed group of microorganisms. Almost 80% of drugs in the world are known to come from species of actinobacteria like Streptomycetes and Micromonospora [12]. According to Qin et al. [13] the rate of discovery of naturally antibiotics derived from the actinobacteria is increasing continuously. Actinobacteria have been reported to be an important producer of secondary metabolites [14] and these metabolites are utilized for different biological activities, such as antibacterial, antifungal, and insecticidal activities. According to Jog et al. [15], Actinobacteria also produce phytohormones. Various secondary metabolites, cell wall degrading enzymes, and antibiotics are produced from different species of actinobacteria like Streptomyces.

The antagonistic activity of Streptomyces is due to the production of the antifungal compound, antibacterial compound, and extra cellular enzymes facilitate [16]. These genera have been found to show a great potential to improve the future of agriculture [17]. The actinobacteria taxa are diverse as composed of streptomycetes and non-streptomycetes, the latter being uncommon, and classified as rare taxa.

An endophyte is a bacterial (including actinomycetes) or fungal microorganism, which spends the whole or part of its life cycle inside the healthy tissues of the host plant by colonizing inter- or intracellularly, typically without causing any harm to the host plant [18, 19]. Thus, an endophyte is an organism, which lives inside a plant [20]. Host plant becomes benefited from entophytic actinobacteria, which can inhibit the other harmful microbes and helps the host plants by increasing nutrient uptake like iron, phosphorus, etc. [21]. Endophytes make a colony in the internal tissue of the plants and are able to accelerate physiological plant responses [22, 23]. Endophytic actinobacteria in plants can produce different types of metabolites which are used for different applications, such as plant growth promoters [24, 25], biocontrol agents [26, 27], antimicrobials [28, 29, 30].

Endophytic actinobacteria help the host plants by means of growth promotion, stress tolerance, and reduction in disease symptoms [31]. From the tissues of the medicinal plants, actinobacteria are being consistently discovered [32, 33, 34, 35]. For pharmaceutical industries and agricultural applications, endophytic actinobacteria could be a potential source of novel antimicrobial compounds [36]. In developing sustainable systems of crop production, endophytic bacteria–plant interactions have an important role [37].

2. Distribution of actinobacteria

According to Oskay et al. [38], actinobacteria are globally distributed soil-inhabiting microorganisms. Basilio et al. [39] reported that lots of actinobacteria including Micromonospora, Streptomyces were obtained from soil, and also many workers have identified Nocardia, Actinoplanes, Streptosporangium, Streptomyces as members of actinobacteria [40]. Pandey et al. [12] reported about the isolation of strains of actinobacteria from Lucknow. Actinobacteria were isolated from the soil samples of various regions around Jaipur, Sikar of Rajasthan [41]. According to Ababutain et al. [42], in Saudi Arabia, the existence of actinobacteria was observed from soil samples of different places and from sea sediment of Caspian [43]. Srinivasan et al. [44] reported that actinobacteria are a heterogeneous and widely distributed group of bacteria in nature. They grow as hyphae like fungi accountable for the characteristically “earthy odor of freshly turned healthy soil” [45].

In several habitats the actinobacteria are found to survive in nature [46]. They are originally soil inhabitants [47]. But they have been reported in various range of an ecosystem, like from deep-sea [48], in terrestrial soil as well as in extreme environments. Takami et al. [49] reported actinomycetrs from greatest depth Mariana Trench. According to Williams et al. [50], actinobacteria can be found in a wide range of soils. Microbispora, Nocardia, Microtetraspora, Amycolaptosis, Actinomadura, and Saccharothrix are thermo-tolerant (up to 50°C) actinobacteria, reported by Takahashi et al. [51].

2.1 Endophytic actinobacteria

The word endophyte means “in the plant” (endon Gr. = within, phyton = plant). In 1866, de Bary had given the term endophyte. According to his definition, “Endophytes are the microorganisms, which reside inside the plant tissues and are significantly different from those found on the plant surface”. Microorganisms that live within the host place either intra or intercellularly, known as endophytes [52] without causing any harmful effect on their host, and have proven to be the richest source of bioactive natural products. By secreting phytohormones entophytes help the plants in nutrition improvement and enhancement the growth of plants by protecting them against phytopathogens [53]. According to Petrini et al. [54], all organisms inhabiting plant organs can colonize internal plant tissues without causing harm to the host at some time in their life. According to Singh and Dubey [55], several microorganisms like bacteria, fungi, as well as actinobacteria form symbiotic associations within the host plant cell.

Normally the endophytes without subjecting the plant to any disadvantage complete their life cycle within the host plants. When groups of actinobacteria reside within living plant cells cooperatively that is called endophytic actinobacteria, such as nitrogen-fixing endophytes Frankia. It is reported that endophytic actinobacteria help to promote the growth of host plants and can reduce disease symptoms. Endophytes are ubiquitous in nature and they produce phytohormones and other growth-promoting factors to enhance the growth of the host plants. In return, the host plant helps the endophytes with nutrients and shelter. The endophytic actinobacteria form one of the interesting groups of microorganisms that is associated with a wide range of plant species. Recently the scientific community have shown interest in research on endophytic actinobacteria due to produce novel and host-origin natural compounds, and various other benefits like growth enhancement and herbivore resistance.

Endophytic actinobacteria may be of two types “obligate” and “facultative”.The growth of obligate endophytes depend on the host plant. Facultative endophytes can exist outside the host plant [22]. Endophytic actinobacteria have been isolated from different plant parts, such as roots [35, 56], stem [57], leaves [58], and fruits [59] . Endophytic actinobacteria in plants are found to produce different types of metabolites that can be used for different applications, such as antimicrobials [28], plant growth promoters [25], and biocontrol agents [27]. According to Passari et al. [60], the presence of PKS/NRPS gene clusters in endophytic actinobacteria is responsible for secondary metabolite biosynthesis. Endophytic actinobacteria are reported to produce several plant growth promotion compounds such as auxins, cytokinins, and gibberellins or producing siderophore to improve nutrient uptake [61, 62]. Coombs and Franco [63] reported that different strains of actinobacteria including Microbispora, Nocardia, Streptomyces were recognized from the tissues of vigorous wheat plants. Streptomyces aureofaciens is one of the endophytic actinobacteria which were obtained from the root of Zingiber Officinale and that endophyte was found to inhibit the growth of Candida albicans [64]. Endophytic actinobacteria form a symbiotic relationship by the formation of the colony within plant cells to get nutrition, shelter from host plants and in return, they produce several secondary compounds which is used by the plant for its growth and productivity [65]. These metabolites prevent the growth of other harmful pathogens in host plants. According to Loria et al. [66], Streptomyces species can produce active secondary metabolites like antibiotics. According to Nalini and Prakash [67], Masand et al. [41], endophytic actinobacteria are diversely distributed in the ecosystem. In China, Qin et al. [68] studied different strains of endophytic actinobacteria that were recognized from several medicinal and crop plants. Streptomyces spp. and non-Streptomyces spp. are the two types of endophytic actinobacteria. Yandigeri et al. [69] reported in the plants of arid regions drought tolerant endophytic actinobacteria like Streptomyces olivaceus DE10, Streptomyces geysiriensis DE27 and Streptomyces coelicolor DE07. Information on the diversity of endophytic actinobacteria and their organ-specificity is significant for helping in the screening of beneficial strains and also for understanding their ecological roles. It is reported that most of the endophytic actinobacteria are generally available in roots than in other plant parts [70, 71]. The density of endophytic actinobacteria in wheat roots was demonstrated by Conn and Franco [72].

Endophytes are reported in plants that are growing in tropical and temperate forests with the hosts ranging from herbaceous plants in various habitats such as extreme arctic, alpine, and xeric environments. Many studies have reported that endophytic actinobacteria are found in different types of plant tissue such as seeds and ovules, fruits, stems, roots, root nodes, leaves, flowers, tubers, buds, xylem, rachis, and bark [60, 73].

3. Plant growth promoting (PGP) activities byendophytic actinobacteria

Roots are the most favorite part of the plants to be colonized by the microbes. Such interaction between the plants and the microbes may result in an endosymbiotic relationship between them. In many cases, the endophytic microbes play a significant role in the protection of plants against pathogenic agents [74, 75]. Studies have been performed with endophytes by inoculating the host plant with endophytes [76] for evaluation of the colonization pattern of vegetative tissues and the effect of endophytes on the host plant. This technique comprehends plant biology and microbial ecology [74].

Actinobacteria are found as symbionts or parasites within plants. According to Hallmann et al. [77], endophytic actinobacteria usually originated from epiphytic actinobacteria colonizing soil, and through any wound or opening on the plant surface, they might have got the opportunities to enter the plant tissues and become endophytes. Individual bacterial cells are not able to penetrate intact epidermal cells as they do not posses mycelium like fungi while actinobacteria colonize on the external part and grow on plant surface by forming branching hyphae and penetrate through natural or by mechanical openings injury [78]. Petrini et al. [54] suggested that the endophytes produce enzymes that are able to degrade most substrates present on the surfaces or in the cell wall of the host. According to Gohain et al. [79], colonization of endophytic actinobacteria is influenced by different climatic conditions and the rate of colonization is high in summer than in winter. The genera Microbispora, Micromonospora, Saccharopolyspora, Micrococcus, Amycolatopsis, Microbacterium, and Nocardia were isolated only in summer; however, the genus Streptomyces was often isolated in both the seasons. By producing plant hormones, fixing nitrogen and by preventing the growth of phytopathogens, endophytes help to increase plant growth. Antibiotics are produced by endophytes with the help of an induced resistance system [80, 81]. Endophytic actinobacteria can offer the opportunity for further research aimed at understanding the correlation between the metabolism of plants and their endophytes.

Stimulation of plant growth by endophytic actinobacteria are of two types, direct and indirect. In the first mechanism, phytohormones such as IAA, cytokinins are produced along with solubilization of minerals like iron, and phosphorus by the production of siderophores for enhancing plant nutrition and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase [82]. Indirectly endophytic actinobacteria help the plants as a biocontrol agent. They can destroy the harmful phytopathogen by stimulating the resistance system of the plant. Besides it, they can also produce extracellular enzymes which can lysis the cell wall of dangerous fungus [83]. Different unique secondary metabolites have been produced from endophytes that are associated with medicinal plants and these secondary metabolites can be applied in pharmaceutical, agricultural and other industries. According to Cattelan et al. [84], endophytic actinobacteria can increase plant growth promotion by several way. They are able to form phytohormones, they can fix nitrogen also and they can prevent the growth of phytopathogen by their antagonism activity and they help in the solubilization of phosphate also.

Numerous actinobacterial species such as endophytes with plants have been reported to have various plant growth-promoting (PGP) properties [85] s. They have also been found to show antagonistic properties against many root-borne and disease-causing plant pathogens [86]. Plant growth-promoting actinobacteria (PGPA) have been reported to be mostly endophytic (Table 1). Plant growth-promoting attributes have been presented in Figure 1.

Plant growth-promoting attributes	Endophytic Actinobacteria	Isolated from	References
IAA, siderophore	Streptomyces sp. CMU PA 101	Carcuma mangga	Khamna et al. [10]
IAA, hydrxymate and catechol type siderophore, protease	Streptomyces sp. S4202, Nonomuraea sp. S3304, Actinomadura sp.S4215	Aquilaria crassna	Nimnoi et al. [62]
Solubilization of phosphate	Streptomyces sp. Nhcr0816	Triticum aestivum	El-Tarabily et al. [87]
Production of IAA and ACC deaminase	Actinoplanes campanulatus, Streptomyces spirilis	Cucumis sativus	El-Tarabily et al. [87]
Production of chitinase, phosphatase activity, and siderophore	Streptpmyces sp. AB131–1,LBRO2	Isolates of microbiology laboratory, Bogal Agricultural University	Hastuti et al. [88]
Siderophore production	Streptomyces sp. GMKU3100	Oriza sativa L.cv.KDML 105	Rungin et al. [89]
Production of IAA	Streptomyces sp. PT2	Plants of Algerian Sahara	Goudjal et al. [90]
IAA production	Streptomyces sp. Nocardia sp.	Citrus reticulata	Shutsrirung et al. [25]
Solubilization of phosphate, production of siderophores	Streptomyces sp. BPSAC34	Medicinal plants	Passari et al. [60]
Phosphate solubilization, siderophore production	Streptomyces sp. UKCW/B, Nocardia sp. TP1BA1B	Pseudowintera colorata	Purushotham et al. [91]

Table 1.

Plant growth promotion by endophytic actinobacteria.

Figure 1.

Plant-endophytic actinomycetes interactions favoring plant growth and biocontrol of phytopathogens [92].

3.1 Production of plant growth hormone - indole acetic acid (IAA) by endophytic actinobacteria

In leguminous plants and in cereals, endophytic actinobacteria function as a plant growth promoter; as a result, they have the capacity to influence plant growth and can increase the ability of nutrition absorption by plants [85].

According to Khamna et al. [93], Palaniyandi et al. [94], indole acetic acid (IAA) is a highly reported growth regulator which is produced by endophytic actinobacteria. The naturally-occurring auxin, indole-3- acetic acid (IAA) is produced by plants through different tryptophan-dependent IAA production pathways and also by bacteria and fungi [95]. The type of pathway that bacterium uses to produce IAA within plants can determine the nature of the resulting plant-microbe interactions [22]. The primary form of auxin is indole-3-acetic acid (IAA) which have an important contribution to control the different cellular process of plants. IAA helps in elongation, cell division. To form the root hair and to make short root length IAA performs very important functions. IAA helps to increase the nutrient absorption ability of the plant. Some strains of endophytic actinobacteria were reported to produce IAA to enhance the growth of cucumber plants [4, 5]. Passari et al. [96] reported various strains of actinobacteria including Micromonospora, Streptomyces, Microbacterium, Pseudonocardia which can produce plant growth phytohormone IAA. According to Madhurama et al. [97], actinobacteria Streptomyces sp. has the capability to produce IAA in the high range. In another study by Khamna et al. [93], it is reported that in many medicinal plants IAA was produced by Streptomyces sp.

It is reported that to improve plant growth, genus Streptomyces, such as Streptomyces olivaceoviridis, S. rimosus, S. rochei, and Streptomyces spp. have the ability to produce IAA from tomato rhizosphere [98, 99]. According to Verma et al. [100], Streptomyces strains of endophytic actinobacteria were obtained from Azadirachta indica and in tomato plants, they were found to increase the plants’ growth. Streptomyces strain En-1 had been studied to produce IAA and to stimulate the growth of Arabidopsis plantlets [101]. Many endophytic, as well as rhizospheric actinobacteria, possess the ability to produce IAA, cytokinins, and GA3 [102]. Nimnoi et al. [62] reported that endophytic actinobacteria from eaglewood (Aquilaria crassna) had shown a trait of plant growth promotion by the production of indole-3-acetic acid (IAA) and ammonia. IAA and siderophore-producing actinobacteria that colonize the root in the rhizosphere are studied to promote root elongation and plant growth [103]. Several endophytic actinobacteria including Streptomyces viridis, S. rimosus, S.olivaceoviridis, S. atrovirens, and S. rochei have been exhibited to improve germination as well as root and shoot elongation [104].

3.2 Phosphate solubilization

Phosphorus is an important component’s that is involved in a wide range of cellular processes by developing plant organs and increasing cell enlargement in plants [105].

Phosphorus (P) content is generally very low in soil and it is available in the form of insoluble metallic complexes. For that reason, plants can absorb from soil, a little amount of phosphorus for their growth [106]. Endophytic actinobacteria support the plants to get phosphorus in soluble form through acidification and mineralization of insoluble soil phosphorus to increase the growth of plants [107, 108]. According to Jog et al. [109], endophytic actinobacteria Streptomyces sp. obtained from Triticum aestivum was found to soluble the phosphate to promote the plant growth.

Various genera of actinobacteria such as Streptomyces, Rhodococcus, Arthrobacter, Micromonospora were reported to have P-solubilization potential under in vivo as well as in vitro [109]. Under P-deficient soils, Streptomyces griseus, Micromonospora aurantiaceae has been reported to help in the P-solubilization of wheat crop [109]. According to Hamdali et al. [110], actinobacteria such as S. griseus, Micromonospora aurantiaca were found to soluble rock phosphate to stimulate the plant growth of wheat. In a recent study, it is reported that endophytic actinobacteria Nocardia sp. TP1BA1B and Streptomyces sp. UKCW/B isolated from the native medicinal plant Pseudowintera colorata (Horopito) were found to solubilize phosphate in New Zealand [91].

3.3 Production of siderophore and enhanced iron availability by endophytic actinobacteria

Siderophores are iron-chelating secondary metabolites produced by various microorganisms in order to scavenge iron from their surrounding environment to make this essential element available to the cell. Due to the high affinity for ferric iron, siderophores are secreted out to form soluble ferric complexes that can be taken up by the organisms. According to Bothwell [111], iron plays an important role in the physiological processes of plants. It is available in the soil as insoluble Fe³⁺ form and plants need soluble Fe2⁺ form to uptake from soil [112]. Actinobacteria can converts iron from Fe³⁺ to Fe²⁺ form and it can increase the bioavailability of iron in the plant rhizosphere by the production of siderophores and help the plant uptake of iron.

The mechanism of siderophore was reported by endophytic actinobacteria to stimulate plant growth [100]. Streptomyces acidiscabies E13 is an excellent example of siderophore producer that promotes the growth of Vigna unguiculata under abiotic stress conditions [113]. Several recent studies demonstrated the production of plant growth-promoting compounds such as siderophores in vitro by endophytic actinobacteria [114, 115]. Khamna et al. [93] studied to produce a high amount of siderophore by Streptomyces CMU-SK 126 that was isolated from Curcuma mangga in rhizospheric soil.

3.4 ACC deaminase producing strains of endophytic actinobacteria

The enzyme ACC deaminase can cleave the plant ethylene precursor ACC, and thereby lower the level of ethylene in a developing or stressed plant [116]. Under unfavorable conditions, plant growth becomes reduced and, in that condition, bacterial ACC deaminase performs an important function to increase the plant growth [117]. Nascimento et al. [118] reported that actinobacteria including Mycobacterium, Streptomyces, Rhodococcus were found to contain ACC deaminase producing genes [118].

By the study, it was proved that when ACC deaminase producing endophytic Streptomyces sp. GMKU 336 was inoculated into Thai jasmine rice Khao Dok Mali 105 cultivar (Oryza sativa L. cv. KDML105), Streptomyces sp. GMKU 336 significantly increased plant growth and decreased ethylene under salt stress (150 mM NaCl) conditions. This work demonstrates that ACC deaminase produces Streptomyces sp. GMKU 336 enhances the growth of rice and increases salt tolerance by reduction of ethylene by the action of ACC deaminase [119].

4. Endophytic actinobacteria as biocontrol agents

According to Lee et al. [120], endophytic actinobacteria such as Microbispora rosea, Streptomyces olivochromogenes prevented the growth of phytopathogen of clubroot of Chinese cabbage effectively. Coombs et al. [121] examined the endophytic actinobacteria as a biocontrol agent against Gaeumannomyces graminis var. tritici of wheat. The endophytic actinobacteria can control Pythium aphanidermatum in cucumber which was described by El-Tarabily et al. [4, 5]. Cao et al. [122] reported that endophytic actinobacteria such as Streptomyces spiralis, Micromonospora chalcea were isolated from cucumber root. They were found to promote plant growth by decreasing plant disease like damping off and crown rot. They were identified as biocontrol agents due to the formation of enzymes that can destroy the cell wall of fungal phytopathogen. These endophytic actinobacteria significantly reduced the incidence of damping-off, crown, and root-rot of cucumber roots. Phytopathogenic fungus Sclerotinia sclerotiorum causes stem rot which is a very harmful disease for economically important crops like soybean and sunflower worldwide [123]. Streptomyces sp. NEAU-S7GS2 was obtained from the root cells of Glycine max. In a study, it was observed that the mycelial growth and germination of S. sclerotiorum (99.1%) were inhibited by Streptomyces sp. NEAU-S7GS2 [124]. Shimizu et al. [81] first reported the powerful activity of endophytic actinobacteria biocontrol agent to decrease the foliar disease. The strain MBR-5 identified as Streptomyces galbus, among ten actinobacterial strains, isolated from field-grown Rhododendron plants showed significant antagonistic activities against Phytophthora cinnamomi and Pestalotiopsis sydowiana. According to Cao et al. [122], the growth of plant pathogens was prevented by endophytic actinobacteria to save the host plant from the attack of harmful microbes. Strain CEN26, an endophyte was isolated from Centella asiaticato and the strain was found to inhibit the germination of conidia and morphological development of the fungal pathogen Alternaria brassicicola [73]. It was studied that most of the endophytic actinobacteria were seen to protect the hosts from diseases by inhibiting plant pathogens [94]. In pot experiments, it was observed that the extract of Streptomyces sp. MR14 cells significantly suppressed Fusarium moniliforme [125].

Maggini et al. [126] also discussed the relationship between actinobacteria and their host plants to protect the host from the disease that is caused by the phytopathogen.

According to Wan et al. [127], leaf blight disease of rice was suppressed by Streptomyces platensis. In a study, the inhibition activities against various phytopathogens such as Neonectria ditissima ICMP 14417, Ilyonectria liriodendri WPA1C, Neofusicoccum luteum ICMP 16678 were shown by Streptomyces sp. PRY2RB2 [91]. Endophytic actinobacteria as biocontrol agents have been enlisted in Table 2. Prominent antagonistic potential against Rhizoctonia solani was found by Streptomyces avidinii vh32, S. toxybicini vh22, and S. tricolor vh85 which also induced the accumulation of phenolic compounds in tomato [140]. From neem (A. indica), endophytic actinobacteria were isolated by Verma et al. [70]. The most common genera were Streptomyces, Streptosporangium, Microbispora, Streptoverticillium, Sacchromonospora, and Nocardia, which showed antagonistic activities against root pathogens Pythium and Phytophthora sp.

Endophytic actinobacteria	Host plant	Pathogen	References
Streptomyces sp. S30	Solanum lycopersicum	Rhizoctonia solani	Cao et al. [122]
Streptomyces halstedii	Capsicum	Phytophthora capsica	Liang et al. [128]
Microbispora sp. A004 and A011	Brasica rapa	Plasmophora brassicae	Lee et al. [120]
Streptomyces sp. KH-614	Oryza sativa	Pyricularia oryzae	Ningthoujam et al. [129]
Streptomyces sp. S30; Streptomyces sp. R18(6)	Lycopersicon esculentum	Rhizoctonia solani	De Olivera et al. [114]
Streptomyces spiralis; Microsmonopora chalcea	Cucumis sp.	Pythium aphanidermatum	EI-Tarabily et al. [87]
Streptomyces sp.	Cicer arietinum	Fusarium oxysporum f. sp. ciceri	Gopalakrishnan et al. [130]
Streptomyces sp. AzR-051, AzR – 049	Azadirachta indica A. Juss	Alternaria alternata	Verma et al. [100]
Streptomyces sp.	Capsicum frutescens	Alternaria brassicae, Colletotrichum gloeosporioides	Srividya et al. [16]
Streptomyces sp.	Soybean	Xanthomonas campestris pv. glycines	Mingma et al. [131]
Streptomyces indiaensisKJ872546	Capsium	Fusarium oxysporum	Jalaluldeen et al. [132]
Actinobacteriastrains OUA3, OUA5, OUA18, and OUA40	Capsicum annuum	Colletotrichum capsici and Fusarium oxysporum	Ashokvardhan et al. [133]
Streptomyces felleus YJ1	Brrasica napus	Sclerotinia sclerotiorum	Cheng et al. [134]
Streptomyces cyaneus ZEA17I	Lactuca sativa	Sclerotinia sclerotiorum FW361	Kunova et al. [135]
Streptomyces diastaticus, Streptomyces fradiae,; Streptomyces collinus	Medicinal plants	Sclerotium rolfsii, Rhizoctonia solani,; Fusarium oxysporum	Singh and Gaur [136]
Streptomyces sp. DBT204	S. lycopersicum	Fusarium proliferatum	Passari et al. [137]
Streptomyces humidus	Brassica oleracea	Alternaria brassicicola	Hassan et al. [138]
Saccharothrix algeriensis NRRL B-24137	S. lycopersicum	Fusarium oxysporum	Merrouche et al. [139]
Streptomyces sp.PRY2RB2	Pseudowintera colorata	Neofusicoccum luteum ICMP 16678	Purushotham et al. [91]

Table 2.

Endophytic actinobacteria as biocontrol agents.

The growth of the fungal pathogen Alternaria alternata was inhibited by endophytic actinobacteria isolated from the medicinal plant Ferula sinkiangensis [141]. 72 strains endophytic actinobacteria isolated from the medicinal plant Rhynchotoechum ellipticum, were found to inhibit the growth of Fusarium proliferatum, F. oxysporum. Different strains of streptomyces sp. such as S. olivaceus, Streptomyces sp. BPSAC121, Streptomyces sp. BPSAC101 showed antifungal activities. Antifungal antibiotics, fluconazole, ketoconazol and miconazole are produced from S. olivaceus and Streptomyces sp. BPSA 121 [96]. Endophytic Streptomyces sp. showed antifungal activity against Geotrichum candidum, F. oxysporum, Alternaria sp. [142]. According to Passari et al. [137], the growth of various phytopathogens including Fusarium Oxysporum, Fusarium graminearum, Rhizoctonia solani, Colletotrichum capsici were inhibited by endophytic actinobacteria such as Nocardiopsis sp., Streptomyces sp. DBT204, Streptomyces sp. DBT 207 by the formation of cell wall degrading enzymes and HCN. Some species of Streptomyces exhibit biological control activity by stimulating the plant resistance system or by the formation of secondary metabolites like antibiotics, particularly against phytopathogenic fungi such as Fusarium oxysporum, Pythium ultimum, Phytophthora sp. [82]. Biocontrol potentials of endophytic actinobacteria against different phytopathogens have been presented schematically in Figure 1.

4.1 Induction of resistance in the host by endophytic actinobacteria

Conn et al. [143] reported that by inducing system acquired resistance (SAR) and jasmonic acid (JA) or ethylene (ET) pathways, the endophytic actinobacteria were able to induce resistance against Erwinia carotovora and Fusarium oxysporum respectively. Conn et al. [143] reviewed that the growth of the pathogen Botrytis cinerea was inhibited by endophytic actinobacteria Streptomyces sp. GB4–2 by stimulating the SAR pathway. Streptomyces has been found to induce host plant resistance on various crops such as vegetables, forages, and eucalyptus [144]; oak [145]. Actinobacteria can act as an antagonist against pathogens due to the production of lytic enzymes that are capable of destroying fungal cell wall. Many researchers have reported the enzyme activity of actinobacteria which can prevent the growth of fungus by destroying the cell wall with their extracellular enzymes like cellulase, chitinase, amylase, etc. [146]. Taechowisan et al. [147] reported the production of chitinase from endophytic Streptomyces aureofaciens CMUAC130. Srividya et al. [16] discussed the enzyme activity (chitinase, glucanase) of Streptomyces sp. to suppress the growth of fungal phytopathogen.

Endophytic actinobacterium- Streptomyces sp. showed hyperparasitic activity. Compant et al. [61] reported the antimicrobial activity of strain NRRL 30562 to prevent the growth of fungal pathogens such as Fusarium oxysporum, Pythium ultimum by producing an antibiotic munumbicins. The strain was obtained from Kennedia nigriscansin in vitro.

The extracellular enzymes- β-1,3-glucosidase, cellulase, and protease; produced by endophytic actinobacteria cause the lysis of hyphae to inhibit the growth of phytopathogens [148]. Hydrolytic enzymes degrade fungal cell wall, cell membrane, and extracellular virulence factors to control plant diseases [149]. According to Yandigeri et al. [69], actinobacteria produced chitinases to inhibit the growth of fungal pathogens. The extracellular antifungal metabolites especially chitinase and β-1,3 glucanase; produced by actinobacteria inhibited the growth of fungi through hyphal swelling, lysis of cell walls in Fusarium oxysporum, and Sclerotium rolfsii [150].

Endophytes are found to produce secondary metabolites, which are active at low concentrations against other microorganisms [151]. A large number of antimicrobial compounds belonging to the classes like alkaloids, peptides, steroids, terpenoids, phenols, quinines, and flavonoids were found to produce from endophytic actinobacteria [152]. Endophytic actinobacteria were found to show antimicrobial activity against phytopathogenic fungi [153]. Another Streptomyces NRRL 30562, isolated from the snake vine possessed activity against many pathogenic fungi [154].

5. Conclusion and future prospects

Actinobacteria can enhance plant growth by producing growth regulators and other compounds and it is well known as a biocontrol agent for the production of antibiotics. Other properties like the production of cell wall degrading enzymes and induced systemic resistance can inhibit the growth of new plant pathogens. This review has been focused on the importance of endophytic actinobacteria as they are widely regarded as an excellent source for plant growth promotion and biocontrol agents by various mechanisms like increasing the supply of nutrients, and production of IAA, cytokinin, controlling fungal diseases through antibiosis and competition. The excessive use of agrochemical is harmful for the environment. The use of biocontrol agents for the management of plant disease is very important. It is very important to review and highlight the previous achievements in endophytic research in order to draw the attention of the research community towards this emerging field. As endophytic actinobacteria help to increase plant growth, so the utilization of actinobacteria can be developed as another way for suitable organic and environmentally helpful agricultural crop production.