Endophytic actinomycetes in bioactive compounds production and plant defense system

Endophytic actinomycetes in bioactive compounds production and plant defense system

9

Mohd Aamir1, Krishna Kumar Rai2, Andleeb Zehra1, Manish Kumar Dubey1, Swarnmala Samal1, Mukesh Yadav1, Ram Sanmukh Upadhyay1 1 Laboratory of Mycopathology and Microbial Technology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, India, 2Division of Crop Improvement and Biotechnology, Indian Institute of Vegetable Research, Indian Council of Agricultural Research (ICAR), Varanasi, India

9.1

Introduction

For centuries, plants and their parts have served as a provenance of various therapeutic bioactive compounds with analeptic naturopathic properties. However, recently endophytes either bacteria or fungi that belongs to endosymbiotic group of microorganisms which complete their whole or fraction of life cycle by colonizing in several parts of the plants such as root, stem, petioles, etc. are now being exploited as bioactive resource without hampering their growth and development (Singh et al., 2017). Astonishingly, several research in the recent years have contemplated the role of endophytic microorganisms which are symbiotically associated with plants, synthesize molecules/compounds with high pharmaceutical potential (Singh and Dubey, 2015). Endophytic microorganisms in association with plants have been known to produce wide varieties of functional metabolites having antibiotic and anticancer properties with potential use in food, agriculture, and cosmetic industries (Omojate Godstime et al., 2014). Albeit, the endophytic microorganism has been neglected until now and was contemplated as disease-causing agent, however, momentarily their symbiotic interaction with plants is now being cherished owing to their biotechnological potential which can cause a paradigm shift in pharmaceutical and agricultural sector (Gos et al., 2017). Endophytic actinomycetes are unicellular, Gram-positive aerobic bacteria belonging to class of branched microorganism which are actively involved in the generation of vital compounds by degrading organic matter (Nimnoi et al., 2010). In the recent years, endophytic actinomycetes have emerged as an untapped resource of promising drug discovery (Matsumoto and Takahashi, 2017). Several endophytic actinomycetes have been identified, isolated, and exploited as biomedical agent to fabricate new/key drugs, a task which had become extremely difficult owing to the limitation of finding novel compounds as well as has facilitated efficient detection of bioactive compounds (Omojate Godstime et al., 2014). Till date, approximately 40 genera belonging to Microbial Endophytes: Prospects for Sustainable Agriculture. https://doi.org/10.1016/B978-0-12-818734-0.00009-7 © 2020 Elsevier Inc. All rights reserved.

190

Microbial Endophytes: Prospects for Sustainable Agriculture

endophytic actinobacteria have been identified via restriction fragment length polymorphism (RFLP) technique in Triticum aestivum residing on both surface and inside plant roots which was later confirmed by employing fluorescence in situ hybridization (FISH), scanning electron microscope (SEM), and tissue-specific expression of target genes (Passari et al., 2015). They are also considered as a potential source of several secondary metabolites displaying antibacterial, anticancer, and plant growthpromoting (PGP) properties, which are important prerequisite for agricultural and pharmaceutical industries (Passari et al., 2015). Increasing evidences have reported the existence of several fundamental groups of actinomycetes producing bioactive compounds in various tissues with novel chemical structures (Nimnoi et al., 2010). Till date, very little is known about the tissue-specific distribution and their association with traditional medicinal plants residing in discrete environments. Several endophytes have potentially exploited for therapeutic purposes since 4–5 decades generating 9000–10,000 functional bioactive compounds of which only 20%–25% have currently been isolated from actinomycetes clearly indicating under exploitation of actinomycetes over Streptomyces. Recently, the “rare/ unexplored” groups of actinomycetes have gained tremendous attention in pharmaceutical research programs to counteract infections caused by pathogenic microorganisms that have become resistant by repeated use of broad-spectrum antibiotics (Borrero et al., 2014). Currently, many of the pharmaceutical industries have deflated their attempt to search for novel bioactive compounds owing to exasperating reasons and economic problems. Therefore, concerted effort is required to identify endophytic actinomycetes living symbiotically with medicinal plants located in unexplored condition. Still, it remains elusive whether this propitious source of functional bioactive compounds will endure or retreat. Analysis of gene expression profiling of polyketide synthase (PKS) or non-ribosomal peptide synthase (NRPS) indicated that 21%– 80% of soil endophytic actinomycetes contain types I and II PKS possessing wide range of biological activities. So, in this paper, we will outline the biochemical potential of endophytic actinomycetes illustrating the function of novel bioactive compounds and their role in improving plant growth and health.

9.2

Isolation, abundance, and phylogenetic diversity

9.2.1 Isolation environment Actinomycetes are free-living microorganism mainly found in soil and interacting with root system of plants. In the rhizosphere, the roots of plants tissue secrete exudates that remarkably influence interaction between plant and microbes (Schenk et al., 2012). Isolation of endophytic actinomycetes has been reported from terrestrial plants such as Chinese cabbage, medicinal, and other tropical plants (Dinesh et al., 2017; Nalini and Prakash, 2017). Qin et al. (2009) reported that medicinal plants from tropical rain forest were copious source of desirable endophytic actinomycetes.

Endophytic actinomycetes in bioactive compounds production and plant defense system

191

Endophytic actinomycetes are omnipresent in different habitat such as arid, aquatic and mangroves, and halophytes ecosystem. It is apparent that endophytic actinomycetes have been reported amply in roots, somewhat in stem and minimum numbers in leaves (Gangwar et al., 2014). The changes in meteorological characters increase the diversity within their vegetation and the inhabitant microorganism (Singh and Dubey, 2018). Strobel and Daisy (2003) reported that temperate and subtropical regions have more diversified form of endophytic actinomycetes as compared to another habitat.

9.2.1.1 Endophytic actinomycetes from arid ecosystem The plants residing within the arid ecosystem are often exposed to harsh environment that stimulate progression of several physio-biochemical and molecular response. Asaf et al. (2017) reported inhabitant actinomycetes in plants, assisting them to endure under adverse environments by developing acclimatization approach. Mohammadipanah and Wink (2016) discussed that actinobacteria inhabiting in deserts exhibit enormous potential to endure under harsh conditions and possess notable genes that activate synthesis pathways of various bioactive compounds. Limited reports are available on the endophytic actinomycetes isolated from plants inhabiting under arid conditions, hence it will be wise to study and investigate phylogeny of novel actinomycetes from arid region (Thumar et al., 2010). Several genera of actinomycetes were isolated from plants of arid zones such as Streptomyces, Micromonospora, Nonomurea, Nocardia, and Amycolatopsis (Huang et al., 2012). Yandigeri et al. (2012) reported drought-resistant endophytic actinobacteria which included different species like Streptomyces olivaceus DE10, Streptomyces geysiriensis DE27, and Streptomyces coelicolor DE07. In all, 22 Streptomyces spp. and five non-Streptomyces spp. were isolated arbitrary from five different plants that were acclimatized to arid climates of Algerian Sahara (Goudjal et al., 2014). Streptomyces mutabilis strain IA1, and novel actinomycetes such as Frigoribacterium endophyticum and Labedella endophyticum were isolated from T. aestivum and Anabis eliator (Toumatia et al., 2016; Wang et al., 2015a, 2015b). Sequestering of novel endophytic actinomycetes species like Streptomyces zhaozhouensis, Streptomyces ginkgonis, and Glycomyces anabasis from Candelabra aloe, seeds of Ginkgo biloba and roots of Anabasis aphylla L. have been widely reported (He et al., 2014; Zhang et al., 2018). Thamchaipenet et al. (2010) also reported the isolation of endophytic genera such as Streptomyces, Amycolatopsis, Kribbell, Microbispora, and Actinoallomurus from the radicle of wattle tree, Acacia auriculiformis. Streptomyces species inhabit as major endophytic actinomycetes under water and nutrient exhausted conditions in arid ecosystem.

9.2.1.2 Endophytic actinomycetes from saline ecosystems The wetlands such as marshes, mud-lands, backwaters, deltas, creeks, and estuaries are the major region for mangrove forest (Singh and Dubey, 2018). The temperature, pH, salinity, humidity, and nutrients of mangroves forest are extremely assorted and

192

Microbial Endophytes: Prospects for Sustainable Agriculture

dissimilar (Amrita et al., 2012; Xu et al., 2014). Huang et al. (2008) and Azman et al. (2015) reported that soil of mangrove environments is the good source of new actinomycetes as compared to endophytic actinobacteria. In all, 105 endophytic actinomycetes were isolated from 19 different mangrove plants (Gupta et al., 2009). Wei et al. (2010) recorded 118 actinomycetes spp. from plant of Shankou biosphere Reserve, China. Among 118 spp., majority of them were Streptomyces and Micromonospora spp. Bruguiera gymnorrhiza inhabiting several species of endophytic actinomycetes were recorded from mangrove of the Andaman Islands (Baskaran et al., 2012). Zhang et al. (2013) also reported that salt tolerant Saccharopolyspora dendranthemae was isolated from a plant inhabiting under the marshy region with high salinity. Different strains of actinomycetes such as Streptomyces, Pseudonocardia, Isoptericola, Agrococcus, and Nocardiopsis have been described from mangrove vegetation (Yang et al., 2015a, 2015b). Mangrove plants are known to harbor large numbers of heterogeneous species of endophytic actinomycetes ( Jiang et al., 2017; Sun et al., 2017). A novel endophyte, Mangrovihabitans endophyticus was isolated from mangrove resident of Bruguiera sexangula (Liu et al., 2017). Endophytic actinomycetes have also been isolated from different saline habitat instead of mangrove. An endophyte, Okibacterium endophyticum residing in the roots of salt tolerant, Salsola affinis, able to grow at elevated pH and NaCl concentration was reported by Wang et al. (2015a, 2015b, 2015c). The novel actinomycete endophyte possessing antimicrobial and antioxidant attributes have been isolated from halophyte. Furthermore, numerous species of actinobacteria still needs to be explored.

9.2.1.3 Endophytic actinomycetes from aquatic ecosystem The marine habitat is one of the abundant sources of different life forms present on earth, among them actinobacteria could be considered as the first microorganisms associated with poorly developed roots of marine plants ( Jensen et al., 2007). Aquatic ecosystem is well enriched with different nutrients essential for the growth and development of microorganisms. Actinomycetes were isolated from wetlands rice plant related with crop productivity and accelerated production of methane-promoting changes in climatic conditions (Bernstein et al., 2007). Wu et al. (2012) reported diverse form of actinobacteria, isolated from seagrass. In all, 21 endophytic actinomycetes isolated from marine seaweed were utilized in producing nanoparticles and tested for their efficacy against pathogenic bacteria (Singh and Dubey, 2018). A multidrug resistant, actinomycetes was isolated from Cauler pataxifolia, a marine green alga (Rajivgandhi et al., 2018). Thus, the goal of most of current research in this direction was to isolate and identify numerous secondary metabolites produced by endophytic actinomycetes from aquatic habitats. Some endophytic actinomycetes have been reported from marine non-mangrove habitats. The aquatic plants are able to survive under high salt and water-logged conditions due to the intimated association of novel actinomycetes in host plant. These endophytic microorganisms have been demonstrated to play a major role in survival of marine plants under such harsh conditions.

Endophytic actinomycetes in bioactive compounds production and plant defense system

193

9.2.1.4 Source of endophytic actinomycetes Endophytic actinomycetes represent to microorganisms inhabiting in the tissue of root, stem, leaves, and bark of healthy plants (Qin et al., 2011). Actinomycetes have been isolated from variety of plants such as medicinal plants, crop plants, halophytes, and even some woody tree species (Qin et al., 2009). The novel metabolites of actinomycetes mainly isolated from medicinal plants have been extensively used as antimicrobial, antiviral, anticancer, and anti-inflammatory agents (Matsumoto and Takahashi, 2017; Nalini and Prakash, 2017). A total number of 46 actinomycetes were isolated from root, stem, and leaf samples of 15 cultivars of Camellia sinensis (Shan et al., 2018). A novel strain WPS1-2T, Micromonospora globbae, an endophytic actinomycete was isolated from roots of Globba winitii C. H. Wright (Kuncharoen et al., 2018). Entophytic actinomycetes isolated from wide range of plants including medicinal plants, crop plants, woody plants, and other plants have been listed in Table 9.1.

9.2.2 Biochemical potential of endophytic actinomycetes “Endophytes” are the microorganisms that spend part of their life cycle or whole life inside plant tissue without causing any harm to the host and are producers of several bioactive compounds (Hasegawa et al., 2006). They exhibit complex interactions with their hosts which involves mutualism and antagonism (Khare et al., 2018). Endophytes colonize inside approximately 300,000 plant species growing in unexposed area on the earth and the presence of large number of different endophytes plays an important role on ecosystems with greatest biodiversity (Dutta et al., 2014). Endophytic actinomycetes are ubiquitous in most plants and colonize plants without exhibiting pathogenicity (Kumar and Jadeja, 2016). It has been reported that some endophytic actinomycetes can also produce useful pharmaceutical compounds of biotechnological interest (Gos et al., 2017). Production of plenty of valuable bioactive compounds by endophytic actinomycetes may provide protection and favorable survival conditions to their host plant and also have potential for commercial use in industry, agriculture, and medicines (Strobel et al., 2004). Independent evolution of endophytic actinomycetes is somehow related to the production of bioactive compounds which allow them to better adapt into the host plants environment and protect them from pathogens, insects, and grazing animals (Dudeja et al., 2012). Variety of bioactive compounds produced by endophytic actinomycetes possess antibiotic, enzymatic, and PGP or inhibiting activities (Hasegawa et al., 2006; Das and Varma, 2009). Endophytes are chemical synthesizer inside plants; in other words, they play a role as a selection system for microbes to produce bioactive substances with low toxicity toward higher organisms (Owen and Hundley, 2004). Recently, several researchers have been focused to appraise and enlighten the potential of endophytic actinomycetes for the production of bioactive compounds applied on biotechnological processes (Matsumoto and Takahashi, 2017; Segaran et al., 2017). Moussa et al. (2011) reported that the high ability of endophytic actinomycetes to inhibit phytopathogenic fungi is mainly by the production of bioactive compounds, such as antibiotics and cell wall degrading enzymes and thus highlighted their importance as ecofriendly candidates

194

Table 9.1 Isolation of endophytic actinomycetes from different parts of plants Host Plants

Endophytic actinomycetes

Source of host tissue

References

Mirabilis jalapa Rauwolfia densiflora Lonicera maackii Centella asiatica Aplysina fistularis

Actinomycete sp. Streptomyces longisporoflavus Allonocardiopsis opalescens Streptomyces sp. Streptomyces sp. Hedaya48

Leaf, stem, root, and flower Stem, leaf, and inflorescence Fruit Root, stem, and leaf Inner healthy tissue

Aloe vera Catharanthes roseus

Actinopolyspora sp. Streptomyces cavourensis AB184264.1

Root, stem, and leaf Leaf

Achillea millefolium, Aloe arborescens Phyllanthus niruri Tinospora crispa Spermacoce verticillata Centella asiatica Tinospora crispa, Lobelia clavatum Aloe arborescens, Aloe barbadensis Psammosilene tunicoides

Micromonospora sp, Nocardiopsis sp., Streptomyces sp. Actinomadura sp. Streptomyces olivochromogenes Microbispora sp Streptomyces sp. Streptomyces olivochromogenes Pseudonocardia endophytica YIM 56035T Micrococcus aloeverae AE-6T, Streptomyces zhaozhouensis NEAU-LZS-5T Allostreptomyces psammosilenae YIM DR4008T Streptomyces sp., wenchangensis 234402, Actinoplanes brasiliensis IFO13938, Couchioplanes caeruleus SCC 1014, Gordonia otitidis IFM 10032

Leaf

Passari et al. (2015) Akshatha et al. (2014) Du et al. (2013) Dochhil et al. (2013) El-Gendy and EL-Bondkly (2010) Gangwar et al. (2014) Kafur and Basheer Khan (2011) Machavariani et al. (2014)

Medicinal plants

Roots

Mini Priya (2012) Pujiyanto et al. (2012) Conti et al. (2012) Dochhil et al. (2013) Pujiyanto et al. (2012) Chen et al. (2009) He et al. (2014), Prakash et al. (2014) Huang et al. (2017)

Roots, stolons, and leaves

Ernawati et al. (2016)

Microbial Endophytes: Prospects for Sustainable Agriculture

Centella asiatica

Root Root, leaf, and stem Leaf Root, stem, and leaf Root, leaf, and stem Stems, leaves, and roots Leaf

Micromonospora terminaliae CAP94T Nonomuraea syzygii sp. nov.

Stem Roots

Kaewkla et al. (2017) Rachniyom et al. (2015)

Kineococcus endophytica KLBMP 1274T, Streptomyces sp. KLBMP 5084 Streptomyces phytohabitans KLBMP 4601T Actinoplanes hulinensis NEAU-M9T, Streptomyces harbinensi NEAU-Da3T, Wangella harbinensis NEAU-J3T Quadrisphaera oryzae sp. nov., Streptomyces oryzae sp. nov. Plantactinospora solaniradicis sp. nov.

Leaf

Bian et al. (2012a)

Root Root

Bian et al. (2012b) Shen et al. (2013)

Leaves, stem Root

Muangham et al. (2018), Mingma et al. (2015) Li et al. (2018)

Leaves

Zhu et al. (2012, 2013)

Root, stem, and leaves

Salam et al. (2017)

Leaves, branches, barks, roots, also flowers, and fruits

Jiang et al. (2018)

Branches

Jiang et al. (2017)

Crop plants Limonium sinense Curcuma phaeocaulis Glycine max

Oryza sativa L. Solanum lycopersicum L.

Woody plants Camptotheca acuminata

Dracaena cochinchinensis Avicennia marina, Aegiceras corniculatum, Kandelia obovota, and Bruguiera gymnorrhiza

195

Thespesia populnea

Blastococcus endophyticus YIM 68236T, Plantactinospora endophytica YIM 68255T Streptomyces sp. (HUST 001, HUST 011, HUST 014, 015, 018), Nocardiopsis sp. HUST 017, Pseudonocardia sp. HUST 013 Streptomyces sp., Curtobacterium sp., Mycobacterium sp., Micrococcus sp., Brevibacterium sp., Kocuria sp., Nocardioides sp., Kineococcus sp., Kytococcus sp., Marmoricola sp., Microbacterium sp. Micromonospora, sp., Actinoplanes sp. Marmoricola endophyticus 8BXZ-J1T

Endophytic actinomycetes in bioactive compounds production and plant defense system

Terminalia mucronata (Syzygium cumini L. Skeels)

Continued

196

Table 9.1 Continued Host Plants

Endophytic actinomycetes

Source of host tissue

References

Nocardia endophytica KLBMP 1256T Mangrovihabitans endophyticus S3Cf-2T Modestobacter roseus KLBMP 1279T Amycolatopsis sp. SX2R71 Glycomyces anabasis EGI 6500139T Saccharomonospora sp. Streptomyces ginkgonis sp. nov. Streptomyces dioscori sp. nov.

Stem Bark Roots Stems and roots Roots Roots Seed Bulbil

Qin et al. (2011) Liu et al. (2017) Qin et al. (2013) Liu et al. (2017) Zhang et al., 2018 Verma et al. (2013) Yan et al. (2018) Wang et al. (2018)

Other plants Jatropha curcas Bruguiera sexangula Salicornia europaea Ferula sinkiangensis Anabasis aphylla L. Azadirachta indica Ginkgo biloba Dioscorea bulbifera L.

Microbial Endophytes: Prospects for Sustainable Agriculture

Endophytic actinomycetes in bioactive compounds production and plant defense system

197

for further investigation in the biocontrol of phytopathogens. Endophytic actinomycetes were also reported to hold the ability of triggering plant-induced systemic resistance (Moussa et al., 2011). Bioactive natural compounds produced by endophytic actinomycetes have promising potential usefulness in safety and human health concerns, although there is still a significant demand of drug industry for synthetic products due to economic and time-consuming reasons.

9.2.3 Endophytic actinomycetes as a source of novel bioactive compounds It is clear that world’s most important bioactive compounds have been obtained from natural products and microorganisms are the primary resource (B
erdy, 2012). The source of exploration of new bioactive compounds is natural products originating from microorganisms (Matsumoto and Takahashi, 2017). Endophytic actinomycetes concorded with plant roots are a relatively pioneer source of plausible new bioactive compounds. Actinomycetes are one of the most attractive sources of novel antibiotics responsible for the production of more than 70% of the naturally derived antibiotics which are in clinical use (Atta et al., 2011). Conn and Franco (2004) reported that the more than 40 genera of actinomycetes have been encountered by terminal RFLP from T. aestivum roots. During the years 1988–92, more than 1000 secondary metabolites from actinomycetes were encountered and about 75% of these compounds are produced by strains of the genus Streptomyces followed by Micromonospora and Actinomadura (Sanglier et al., 1993). Study revealed that other actinomycetes such as Actinoallomurus strains also produce antibiotic compounds at high frequency (Pozzi et al., 2011). Tiwari and Gupta (2012) observed that the only some endophytic actinomycetes have the potential to produce useful bioactive compounds. Pimentel et al. (2011) demonstrated that the increasing levels of drug resistance by plant and human pathogens can be overcome by the discovery of novel antimicrobial metabolites from endophytic actinomycetes. Anticancer properties of several secondary metabolites from endophytes have been examined recently (Savi et al., 2015a, 2015b, 2015c). Bioactive compounds produced by endophytic actinomycetes could be alternative approaches for discovery of novel drugs, since many natural products from endophytes were identified as anticancer agents. Some examples of the potential of endophytic actinomycetes associated with the production of anticancer agents are reviewed (Abd-Elnaby et al., 2016; El-Naggar, 2017). Alkaloids, peptides, steroids, terpenoids, phenols, quinines, and flavonoids are structural classes resembling to a large number of bioactive compounds isolated from endophytic actinomycetes (Yu et al., 2010). Such bioactive metabolites find widerange application as agrochemicals, antibiotics, immune suppressants, antiparasitics, antioxidants, and anticancer agents (Fig. 9.1) (Pimentel et al., 2011; Janardhan et al., 2014). Several bioactive compounds produced by endophytic actinomycetes are given in Table 9.2.

198

Microbial Endophytes: Prospects for Sustainable Agriculture

Fig. 9.1 Pathways for the synthesis of bioactive compounds synthesized by endophytic bacteria.

9.3

Function of novel bioactive compounds in plantactinobacteria interactions

9.3.1 Soil health improvement Application of pesticides, fungicides, insecticides, fertilizers, and synthetic chemicals is being used to improve plant growth, development, and productivity (Aktar et al., 2009). But, constant applications of these compounds had severely affected the soil fertility due to degradation of physico-biochemical properties and decreased diversities of beneficial soil microbes. Further, use of chemical pesticides has developed resistance in the pathogenic microbes and had also resulted in the biomagnification of deleterious agrarian compounds along with the increased residual leftovers inducing significant fitness concerns (Prashar and Shah, 2016). Obviously, proper agricultural practices and packages need to be initiated along with the application of legitimate substitutes. Improvement in number and diversity of beneficial microorganism inhabiting soil and plant could be helpful in enhancing agricultural productivity. The potential implementation of endophytic actinomycetes in soil promotes reduced disease occurrences, increased nutrient availability, growth, and resistance to various environmental stresses (Fig. 9.2).

Endophytic actinomycetes in bioactive compounds production and plant defense system

Table 9.2 Endophytic actinomycetes and their bioactive compounds Bioactive compounds

Source

Activity

Reference

Ansamitocin Fistupyrone Paclitaxel Demethylnovobiocin Cedarmycin A Kakadumycin Clethramycin

Anticancer Antifungal Anticancer Antibiotic Antibacterial Antibiotic Antibiotic

Higashide et al. (1977) Igarashi et al. (2000) Caruso et al. (2000) Sasaki et al. (2001a, 2001b) Sasaki et al. (2001a, 2001b) Castillo et al. (2003) Furumai et al. (2003)

5,7-Dimethoxy-4phenylcoumarin Munumbicins A & B Actinomycin D Salaceyins A and B Pterocidin Naphthomycin K Ansacarbamitocins Lansai A–D

Nocardia sp. No. C-15003 Streptomyces sp. TP-A0569 Kitasatospora sp. strain P&U 22869 Streptomyces sp. TP-A0556 Streptomyces sp. TP- A0456 Streptomyces sp. NRRL 30566 Streptomyces. hygroscopius TP-A0623 S. aureofaciens CMUac130 Streptomyces NRRL 30562 Streptomyces sp. Tc022 S. laceyi MS53 S. hygroscopicus TP-A0451 Streptomyces sp. CS Amycolatopsis CP2808 Streptomyces sp. SUC1

Anticancer

Saadamycin 24-Demethyl-bafilomycin C1 Lupinacidin C Abyssomycin C Aureoverticillactam Bonactin

Streptomyces sp. Hedaya48 Streptomyces sp. CS Micromonospora lupini Verrucosispora maris S. aureoverticillatus Streptomyces sp.

Taechowisan et al. (2007) Castillo et al. (2006) Taechowisan et al. (2006) Kim et al. (2006) Igarashi et al. (2006) Lu and Shen (2007) Snipes et al. (2007) Tuntiwachwuttikul et al. (2008) El-Gendy and EL-Bondkly (2010) Jian et al. (2010) Igarashi et al. (2011) Bister et al. (2004) Mitchell et al. (2004) Schumacher et al. (2003)

Chandrananimycins

Actinomadura sp.

Maskey et al. (2003) Continued

199

Antibiotic Antibiotic Anticancer Anticancer Anticancer Anticancer Antifungal Anticancer Antibiotic Anticancer Anticancer Antibacterial Anticancer Antibacterial Antifungal Antialgal Antibacterial

200

Table 9.2 Continued Bioactive compounds

Source

Streptomyces sp. Dermacoccus sp.

Diazepinomicin Enterocin Frigocyclinone Glaciapyrroles Gutingimycin Lynamicins Mechercharmycins

Micromonospora sp. S. maritimus S. griseus Streptomyces sp. Streptomyces sp. Marinispora sp. Thermoactinomyces sp.

Antifungal Anticancer Anticancer Cytotoxic, Radical scavenging Anticancer Bacteriostatic Antibacterial Antibacterial Antibacterial Antibacterial Anticancer

Reference

Li et al. (2005) Abdel-Mageedet al. (2010)

Charan et al. (2004) Piel et al. (2000) Bruntner et al. (2005) Macherla et al. (2005) Maskey et al. (2004) McArthur et al. (2008) Kanoh et al. (2005)

Microbial Endophytes: Prospects for Sustainable Agriculture

Chinikomycins Dermacozines

Activity

Endophytic actinomycetes in bioactive compounds production and plant defense system

201

Nanoparticle Antimateria

Antidiabetic

Phytohormone

Bioactive compounds produced by Endophytic Actinomycetes

Antibiotic

Antioxidant

Anticancerous Enzyme

Fig. 9.2 Types of functional bioactive compounds produced by endophytic actinomycetes production of secondary metabolites by endophytic actinomycetes is considered to accomplish a resistance mechanism to conquer the pathogenic infection.

9.3.2 Biocontrol of plant diseases It has been previously reported that endophytic actinomycetes can successfully restrict the growth of pathogens (Taechowisan et al., 2003; Cao et al., 2004). Actinomycetes have potential to produce various secondary metabolites such as antimicrobial antibiotics, volatile organic compounds, and cell wall breaking enzymes with growthpromoting features and can be used as biocontrol chemicals. In several studies, Streptomyces spp. has been represented as the major actinomycetes showing promising antifungal activities. Actinomycete strain CEN26 were isolated from Centella asiatica were illustrated to inhibit the germination of asexual spores and growth of mycelia of Alternaria brassicicola (Phuakjaiphaeo and Kunasakdakul, 2015). Actinomycetes residing inside the plant tissue have groundbreaking potential to suppress numerous diseases by pathogen’s cell wall degradation, parasitism, as well as toxin and antibiotic production against leaf blight disease of rice (Wan et al., 2008). Approximately 25% of total actinomycetes isolated from Paeoni lactiflora and Trifalium repens leaves have been reported to suppress the mycelial growth of Rhizoctonia solani (Gu et al., 2006). Fistupyrone, a bioactive compound isolated from Streptomyces sp. TP-A0569 also restricts the pathogenicity of A. brassicicola TP-F0423 causing seedling disease of cabbage (Igarashi et al., 2000). Streptomyces sp. PRY2RB2 isolated from Pseudowintera colorata (Horopito) inhibits growth of several plant pathogens such as Neonectria ditissima ICMP 14417, Neofusicoccum luteum ICMP

202

Microbial Endophytes: Prospects for Sustainable Agriculture

16678, Neofusicoccum parvum MM562, and Ilyonectria liriodendri WPA1C (Purushotham et al., 2018). The AR3 strain of actinomycetes isolated from Emblica officinalis, also exhibited antifungal potential against Fusarium oxysporum (Kamboj et al., 2017). Some of the recent studies regarding plant pathogen interaction have been listed in Table 9.3.

9.3.3 Potential use in improving plant growth and health Endophytic actinomycetes are actinobacteria that promote plant growth and nutrient uptake by producing various PGP activities such as deaminase, indole-3-acetic acid (IAA), 1-aminocyclopropane-1-carboxylic acid, fixation of nitrogen, and phosphate solubilization (Kaur et al., 2013). Among all the PGP factor, IAA is majorly revealed as plant growth hormone from endophytic actinomycetes (Palaniyandi et al., 2013). IAA produced by Streptomyces species has been reported to markedly enhance the growth of Solanum lycopersicum (Verma et al., 2011). Actinomycetes isolated from Dioscorea plants stimulated the growth of Arabidopsis thaliana by producing IAA, P solubilization, and ACC deaminase activity (Palaniyandi et al., 2013). Ethylene is a negative plant growth regulator produced in plants under extreme environmental conditions. Actinomycetes inhabiting in plants growing under such adverse conditions might reduce the adverse effect of stress by producing ACC deaminase. ACC deaminase hydrolyzes the ACC and thus diminishes the ethylene production. Viterbo et al. (2010) and Xing et al. (2012) studied in some plants that ACC deaminase hydrolyzing 1-aminocyclopropane-1-carboxylic acid into α-ketobutyrate and ammonia that could be a source of nitrogen to the microbes for their growth. Phosphorus is an essential element for the growth and development of plants required for several physiological processes such as transport of sugar, activation of cell multiplication, and energy production in the form of ATP (Ahemad and Kibret, 2014). The phosphorus is not easily available to plants because its availability in organic form. Endophytic actinomycetes play essential role in phosphate solubilization and increase its accessibility to plants through various processes like mineralization of organic phosphorus, chelation, and redox changes (Van der Hiejden et al., 2008). In addition to P, iron also play an important role in biological processes via iron chelator, and siderophore produced by Streptomyces acidiscabies E13 that improved the reproductive growth of Vigna unguiculata under heavy metal stress (Dimkpa et al., 2009; Sessitsch et al., 2013). Herbicidin H and gamma-glutamylmethionine sulfoximine (Table 9.4), a bioherbicide extracted from Streptomyces sp. SANK 63997 and Microbispora sp. inhabiting in Setaria viridis var. pachystachys and Carex kobomugi was described to enhance the health of host plants by inhibiting growth of weed (Okazaki, 2003).

9.4

Biotechnological potential for therapeutic use and in pharmaceutical industries

Endophytic fungi that are residing asymptomatically in internal tissues of all higher plants are of growing interest as promising sources of biologically active agents. They may produce a plethora of bioactive metabolites that may be involved in the

Bioactive compound Fluconazole, Ketoconazol, Miconazole

Saadamycin/5,7Dimethoxy-4-pmethoxylph-enyl coumarin Munumbicins E-4 and E-5 Coronamycin 1-Acetyl-b-carboline, indole-3carbaldehyde, tryptophol, 3-(hydroxyacetyl)-indole, brevianamide F, cyclo-(L-Pro-L-Phe), cyclo-(L-ProL-Tyr) and cyclo-(L-Pro-L-Leu) 1-Vinyl-b-carboline-3-Carboxylic acid, Indole-3- carbaldehyde, Indole-3-acetic acid and Indole-3-carboxylic acid

Endophytic actinomycetes

Host

Target pathogen

References

Streptomyces thermocarboxydus, Streptomyces sp. BPSAC101, Streptomyces olivaceus, Streptomyces sp. BPSA 121 Streptomyces sp. Hedaya 48

Rhynchotoechum ellipticum

Fusarium oxysporum, Fusarium proliferatum

Passari et al. (2017)

Aplysina fistularis

Fusarium oxysporum

Streptomyces sp. NRRL 30562 Streptomyces sp. MSU2110 Aeromicrobium ponti LGMB491

Kennedia nigriscans Monstera sp.

Pythium ultimum, Rhizoctonia solani Pythium ultimum, Fusarium solani, Rhizoctonia solani Staphylococcus spp.

El-Gendy and EL-Bondkly (2010) Castillo et al. (2006) Ezra et al. (2004)

Microbispora sp. LGMB259

Vochysia divergens

Vochysia divergens

Micrococcus luteus NRRL B-2618 and Kocuria rosea B-1106

Gos et al. (2017)

Savi et al. (2015b)

Endophytic actinomycetes in bioactive compounds production and plant defense system

Table 9.3 Antimicrobial compounds produced by endophytic actinomycetes

Continued 203

204

Table 9.3 Continued Bioactive compound Diketopiperazine, gancidin W (GW) 3-Acetonylidene-7-Prenylindolin-2-one and 7-Isoprenylindole-3-carboxylic acid Clethramycin

S-Adenosyl-N-acetylhomocysteine 7-Coctadecenamide, 9,12octadecadienamide (Linoleamide)

Host

Target pathogen

References

Streptomyces sp. SUK10, Streptomyces sp. neauD50 Streptomyces hygroscopicus TP-A0623 Streptomyces sp. TPA0556 Streptomyces sp. BT01

Shorea ovalis

Plasmodium berghei PZZ1/100

Zin et al. (2017)

Dactylosporangiumsp. strain SANK 61299 Micromonospora sp. Nocardia caishijiensis, Pseudonocardia carboxydivorans

Cucubalus sp.

Glycine max Clethra barbinervis

Candida albicans

Aucuba japonica

Gram-positive, Gramnegative Staphylococcus aureus ATCC25932, Bacillus cereus ATCC 7064, Bacillus subtilis ATCC 6633 Gram-positive, Gramnegative Gram-positive, Gramnegative Candida spp., Gram-positive and Gram-negative bacteria

Boesenbergia rotunda (L.)

Pueraria candollei Sonchus oleraceus, Ageratum conyzoides

Zhang et al. (2014) Furumai et al. (2003) Sasaki et al. (2001a, 2001b) Taechowisan et al. (2014)

Okazaki (2003) Boonsnongcheep et al. (2017) Tanvir et al. (2016)

Microbial Endophytes: Prospects for Sustainable Agriculture

70 -Demethylnovobiocin, 500 demethylnovobiocin 7-Methoxy-3,30 ,40 ,6-tetrahydroxyflavone and 20 ,7-Dihydroxy-40 ,50 Dimethoxyisoflavone, Fisetin, Naringenin, 30 -Hydroxydaidzein, Xenognosin Streptol

Endophytic actinomycetes

Endophytic actinobacteria

Host

PGP activities

Reference

Streptomyces sp. MBR-52

Rhododendron ferrugineum

Meguro et al. (2006)

Streptomyces sp. CMU-PA101 and Streptomyces sp. CMU-SK126 Actinoplanes campanulatus, Micromonospora chalcea, Streptomyces spiralis Streptomyces sp. S4202, Nonomuraea sp. S3304, Actinomadura sp. S4215, Pseudonocardia sp. S4201

Curcuma manga

Production of rootingpromoting plant hormones IAA and siderophore

Khamna et al. (2009)

Cucumis sativus

Production of IAA and ACC deaminase

El-Tarabily et al. (2010)

Aquilaria crassna

Nimnoi et al. (2010)

Streptomyces sp. R18(6)

Lycopersicon esculentum

Streptomyces sp. GMKU 3100 Streptomyces sp. En-1 Streptomyces sp. PT2 Streptomyces sp. LPC026, LPC029, PC005, PC052, and PC053

Oryza sativa L. cv. KDML105 Taxus chinensis Plants of Algerian Sahara Garuga pinnata, Gmelina arborea, Stephania venosa, Melastoma malabathricum, Merremia vitifolia Citrus reticulate

Indole-3-acetic acid (IAA), hydroxamate and catechol type siderophore, protease IAA, siderophore production, Phosphate solubilisation Siderophores IAA production Production of IAA Homoserine lactone degrading enzymes

Streptomyces sp., Nocardia sp., Nocardiopsis sp., Spirillospora sp., Microbispora sp. and Micromonospora sp. Streptomyces roseosporus

Ocimum sanctum, Mentha arvensis

De Oliveira et al. (2010) Rungin et al. (2012) Lin and Xu (2013) Goudjal et al. (2013) Chankhamhaengdecha et al. (2013)

IAA Citrus reticulata

Shutsrirung et al. (2013)

IAA production, P solubilization

Gangwar et al. (2014) 205

Continued

Endophytic actinomycetes in bioactive compounds production and plant defense system

Table 9.4 Plant growth promoting factor of endophytic actinomycetes

206

Table 9.4 Continued Endophytic actinobacteria

Host

PGP activities

Reference

Streptomyces sp. mhcr0816, mhce0811

Triticum aestivum

Jog et al. (2014)

Nocardiopsis sp. ac9, Streptomyces, Violaceorubidus 6ca11, Streptomyces sp. ac19 Streptomyces albosporus, Streptomyces cinereus, Micromonospora sp. O6, Saccharopolyspora sp. O9 Streptomyces sp. BPSAC34, Leifsonia xyli BPSAC24, Microbacterium sp. BPSAC 21, 27, 28 and 29 Streptomyces olivaceus, Streptomyces sp. BPSAC101, Streptomyces sp. BPSAC121, Streptomyces thermocarboxydus Streptomyces sp. UKCW/B, Nocardia sp. TP1BA1B

Elaeis guineensis Jacq

Solubilization of phosphate, production of phytase, chitinase, IAA, siderophore, and malate Cellulase, Xylanase, Lignolytic activity

Aloe vera, Mentha arvensis, Ocimum sanctum

IAA production, P solubilization

Gangwar et al. (2014)

Medicinal plants

Siderophores, HCN, ammonia, production of chitinase and IAA IAA and ammonia production, P solubilization

Passari et al. (2015)

Pseudowintera colorata

Phosphate solubilisation and siderophore production

Passari et al. (2017)

Purushotham et al. (2018)

Microbial Endophytes: Prospects for Sustainable Agriculture

Rhynchotoechum ellipticum

Ting et al. (2014)

Endophytic actinomycetes in bioactive compounds production and plant defense system

207

host-endophyte relationship (Strobel, 2003). They are potential sources of novel natural agents for exploitation in the pharmaceutical industry, agriculture, and in environmental applications (Bacon and White, 2000; Strobel and Daisy, 2003). Research in natural products for drug discovery methods is competitive with other synthetic drugs, due to lesser toxicity and broad-spectrum activities in less quantity of compound administration. Endophytic actinomycetes are reported to produce a vast number of novel bioactive metabolites such as antimicrobial, antiviral, antioxidant, anticancer, antidiabetic agents, cholesterol inhibitors, and immunosuppressive agents (Xu et al., 2014).

9.4.1 Antibacterial compounds Endophytic actinomycetes have the ability to produce antimicrobial metabolites. Ding et al. (2011a, 2011b) determined bactericidal property of three newly characterized indole alkaloids viz., sespenine, indosespene, and xiamycin from Streptomyces sp. HK10595 that exhibited strong antibacterial activities against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecalis. In another research, same research group also deciphered molecular mechanism of indole terpenoid pathway in a bacterium and identified two fundamental cyclases such as XiaE and XiaF which play an important role in modifying host enzymes. Li et al. (2012) evaluated the efficiency of metabolites extracted from endophytic actinomycetes of Nerium oleander against the growth of Escherichia coli, Bacillus cereus, Salmonella anatum, S. aureus, Listeria monocytogenes, and Candida krusei. Several studies have also reported bioactive studies of secondary metabolites from mangrove actinomycetes and have confirmed their antimicrobial, antineoplastic activities, for example, 2-allyloxyphenol which has been characterized as synthetic drug showing strong inhibitory activity against Aspergillus niger MTCC 282, Candida albicans MTCC 227, and Saccharomyces cerevisiae MTCC 170 when applied at 0.2–1.75 mg/mL (52). Similarly, an endophytic actinomycetes JBIR-94 discovered from Streptomyces sp. RL23 and RL 66 inhabiting mangrove soil in Japan exhibited strong antioxidative property by scavenging 1,1-diphenyl-2picrylhydrazyl radical (Takagi and Shin-ya, 2011). Furthermore, Ding et al. (2011a, 2011b) also isolated a compound named divergolides A–D from an entophytic actionomycetes that showed strong inhibitory activity against Mycobacterium vaccae as well as against Bacillus subtilis and S. aureus (Table 9.5).

9.4.2 Anticancer compounds Cancer is the second leading cause of death worldwide, and the number of cases is increasing alarmingly every year. The WHO’s GLOBOCAN estimated approximately 14.1 million new cancer cases and 8.2 million deaths worldwide, which are expected to rise to 22 million in the next 2 decades (Torre et al., 2015). Endophytic actinomycetes have been known to possess the ability to produce potential anticancer compounds. Taxol is a highly functionalized diterpenoid which is widely used as anticancer drug (Feling et al., 2003). The anticancer drug, taxol has been found in

Bioactive compounds

Source

Activity

Reference

Saadamycin Antimycin A 18 24-Demethyl bafilomycin A1; 21-O-methyl-24-demethyl-bafilomycin A1; 19, 21-di-O-methyl-24-demethyl-bafilomycin A1; 17,18-dehydro-19, 21-di-O-methyl-24-demethyl-bafilomycin A1; 24-demethyl-bafilomycin D IAA

Streptomyces sp. Hedaya 48 Streptomyces albidoflavus Streptomyces sp. CS

Antifungal Antifungal Antitumor

El-Gendy and EL-Bondkly (2010) Yan et al. (2010) Li et al. (2010)

C-hydroxybutenolide Brevianamide F. Phaeochromycin 6-methyl-2-oxiranyl-hept-5-en-2-ol, 2,6,11,15-tetramethylhexadecane, 3-methyl-1-butanol, 4-methyl-1-pentanol, and 1-nonanal 9-HydroxybafilomycinD 29-HydroxybafilomycinD 2-Amino-3,4-dihydroxy-5-methoxybenzamide 4-Hydroxy-3-methoxybenzoic p-Hydroxytruxinic acids

Antimicrobial Antimicrobial

Masand et al. (2018) Djinni et al. (2014)

Antibacterial

Martinez-Klimova et al. (2017)

Streptomyces sp. YIM56209

Antibacterial

Li et al. (2015)

Streptomyces strain YIM67086TA Streptomyces strain YIM67086TA

Antibacterial, antifungal Antifungal

Yang et al. (2015a, 2015b)

Dochhil et al. (2013) Shutsrirung et al. (2013)

Microbial Endophytes: Prospects for Sustainable Agriculture

Indole acetic acid (IAA)

Streptomyces sp. Streptomyces sp., Nocardia sp., Micromonospora sp., Microbispora sp., Nocardiopsis sp. Streptomyces sp. YIM66017 Streptomyces sp. Streptomyces sundarbansensis Streptomyces sp. A0916

208

Table 9.5 Different bioactive compounds and their endophytic source with potential use against pathogenic microorganisms

Vinaceuline 7-Methoxy-3, 30, 40, 6-tetrahydroxyflavone, 20, 7-dihydroxy-40, 50-dimethoxyisoflavone 1-Vinyl-b-carboline-3-carboxylic acid, 1-vinylb-carboline-3-carboxylic acid Phenol, 2, 4-bis-(1, 1-dimethylethyl), transcinnamic acid Perlolyrine, 1-hydroxy-b-carboline, lumichrome,1H-indole-3-carboxaldehyde

Streptomyces sp. YIM66017 Streptomyces sp. BCC72023 Streptomyces sp. YIM 64018 Streptomyces sp.

Antimicrobial Antibacterial

Supong et al. (2016) Supong et al. (2016)

Antimicrobial

Supong et al. (2016)

Antibacterial

Zhou et al. (2013)

Microbispora sp.

Antibacterial

Savi et al. (2015a, 2015b, 2015c)

Nocardiopsis sp.

Antimicrobial

Sabu et al. (2017)

Jishengella endophytica 161111

H1N1 subtype of the influenza virus Anticancers

Wang et al. (2014)

Nalini and Prakash (2017)

Antitumor

Nalini and Prakash (2017)

Antimicrobial Anticancer Cytotoxic, antimicrobial Cytotoxic, antibacterial, antifungal Anticancer and antifungal Antifungal, plant growth promotion

Li et al. (2012) Xu et al. (2014) Li et al. (2015)

Artemisinin Antimycin Anthracycline-misamycin

Streptomyces sp. (MSU2110) Streptomyces aureofaciens CMUAc130 Pseudonocardia sp. Streptomyces albidoflavus Streptomyces sp.

2, 6-Dimethoxy terephthalic acid

Streptomyces sp.

3-Acetonylidene-7-prenylindolin-2-one, 3-cyanomethyl-6-prenylindole Indole acetic acid (IAA), siderophores

Streptomyces sp.

Coronamycin 4-Arylcoumarin

Wang et al. (2014) Gangwar et al. (2014)

Continued

209

Streptomyces griseofuscus, Streptomyces cinereus, Streptomyces flavus

Zhou et al. (2014)

Endophytic actinomycetes in bioactive compounds production and plant defense system

Alpiniamide Oxohygrolidin

210

Table 9.5 Continued Bioactive compounds

Source

Activity

Reference

Thaxtomin A

Streptomyces scabies

Francis et al. (2015)

Albaflavenol B Strepturidin

Harmaomycin Bacteriocins Saadamycin 3-Nitropropionic acid (3) Munumbicin C

Streptomyces sp. Streptomyces albus DSM 40763 Streptomyces cinnamonensis Streptomyces sp. YIM66403 Streptomyces sp. Lysinibacillus sp. and B. cereus Streptomyces sp. B. subtilis Cryptosporiopsis quercina Phomopsis sp. Streptomyces sp.

Cellulose synthesis inhibitor As sesquiterpene Immunotherapy

Kakadumycin A Koningiopisins A–H

Streptomyces sp. Trichoderma koningiopsi

Phomapyrrolidones A, B Efomycins M and G, oxohygrolidin, abierixin, 29-O-methylabierixin Indosespene (6)

Monensin

Lowicki and Nski (2013) Li et al. (2015) Brayfield (2013) Singh et al. (2017)

Phoma sp. Streptomyces sp.

Antibacterial Antibacterial Antibacterial Antibacterial Antiprotozoal, antibacterail, antifungal Antiprotozoal Antibacterail, antifungal Antibacterial Antiprotozoal

Bae et al. (2015) Sansinenea and Ortiz (2011) Dutta et al. (2014) Ganihigama et al. (2015) Castillo et al. (2002)

Wijeratne et al. (2013) Supong et al. (2016)

Streptomyces sp.

Antibacteria

Ding et al. (2011a, 2011b)

Ganihigama et al. (2015) Liu et al. (2016)

Microbial Endophytes: Prospects for Sustainable Agriculture

Anthracyclin Doxorubicin Camptothecine

Prevent coccidiosis Antitumor Anticancer Anti-cancer

Raju et al. (2015) Pesic et al. (2014)

Aspernolide F

Curvularide B (2) Androprostamines Treponemycin

Colletotrichum dematium Aspergillus terreus

Curvularia geniculata Streptomyces sp. MK932CF8 Streptomyces Strain MS-6-6

Antifungal

Ren et al. (2008)

Antifungal, antibacterial, antiprotozoa Antifungal Anti-prostate cancer Anti-tuberculous

Ibrahim et al. (2015)

Chomcheon et al. (2010) Yamazaki et al. (2015) Mahmoud et al. (2015)

Endophytic actinomycetes in bioactive compounds production and plant defense system

Collutellin A

211

212

Microbial Endophytes: Prospects for Sustainable Agriculture

many genera of endophytic fungi such as Alternaria, Fusarium, Monochaetia, Pestalotia, Pestalotiopsis, Pithomyces, and Taxomyces (Strobel et al., 1996). A cyclizidine compound named JBIR-102 isolated from Saccharopolyspora sp. RL78 shown to have cytotoxic properties against HeLa cell lines and ACC-MESO1 with IC50 values of 29 and 39 μM (Izumikawa et al., 2012). Secalonic acid D, a mycotoxin (ergochrome class) extracted from the mangrove actinomycetes was reported to have high cell toxicity against K562 and HL60 leukemia cells. It was shown to induce toxicity through apoptosis (Potts and Lam, 2010). Researchers have also isolated p-aminoacetophenonic acids from an endophyte actinomycetes Streptomyces griseus HKI0412 and HK10552 of a mangrove plant Kandelia candel have also reported to show strong cytotoxic activity against HeLa cell lines as well as against VSVG/HIV-luc psedotyping virus (Wang et al., 2010). Dilactone antimycins discovered from mangrove actinomycetes such as Antimycin A18 have also been reported to exhibit strong activity against wide range of pathogens (Williams et al., 2005). The compound antimycin A18 have also been recorded to have cytotoxic activity, thus inhibiting the growth HepG2 and KB human cancer cell line with IC50 values ranging from 0.12 to 0.92 μg/mL (Endo and Danishefsky, 2005). Similarly, Han et al. (2012) have also identified two new antimycin A analogs from actinomycetes Streptomyces lusitanus XM52 of the mangrove plant Avicennia mariana showed strong activity against B. subtilis, S. aureus, and Loktanella hongkongensis with MIC values of 8.0–32.0 μg/mL. Several dilactones isolated from an actinomycete strain N2010-37 from Zhanjiang mangrove have been shown cytotoxic activities against human chronic granulocytic leukemia cell line K562 with an IC50 value of 1.36 μM (Zhou et al., 2011). Three novel 2-pyranone compounds such as norcardiatones A, B, and C isolated from cultures of nocardiopsis sp. A00203 inhabiting leaves of Aegiceras corniculatum exhibited strong cytotoxicity against HeLa cells at 10 and 20 μg/mL (Lin et al., 2010).

9.4.3 Antioxidant compounds The importance of compounds with antioxidant activity is their protective effect against the oxidative stress caused by oxygen-derived free radicals (Selim et al., 2014). In this line of the study, researchers have identified a novel antioxidative compound known as 2-allyloxyphenol which has also been characterized as an important synthetic drug. This antioxidative compound was first isolated from Streptomyces sp. MS1/7 with potential cytotoxic activity against three of the main fungus, that is, S. cerevisiae, A. niger, and C. albicans (Arumugam et al., 2011). The compound 2-allyloxyphenol isolated from strain MS1/7 residing in the sediments of Sundarbans mangrove forest, India showed substantial antioxidant activity with IC50 of 25 μg/mL (Takagi and Shin-ya, 2011). Another compound named JBIR-94 characterized from Streptomyces sp. RL23 and RL 66 also showed strong antioxidant scavenging activity against 1,1-diphenyl-2-picrylhydrazyl radical (Kawahara et al., 2012). An isoflavone group 100-O-methyl-8-hydroxymethyldaidzein is free radical-scavenging compounds, isolated from Streptomyces sp. YIM65408 (Yang et al., 2013). Zhou et al.

Endophytic actinomycetes in bioactive compounds production and plant defense system

213

reported two other antioxidant compounds such as 2, 6-dimethoxy terephthalic acid and yangjinhualine A isolated from Streptomyces sp. YIM66017 (Tanvir et al., 2014).

9.4.4 Antiviral compounds There is a global need for new antiviral compounds to solve drug-resistance problems. Endophytic actinomycetes are known to produce many antiviral agents such as cyclopentenone derivatives which have been isolated from leaves of Aegiceras comiculatum which is a mangrove plant from China exhibited strong antimicrobial as well as antiviral activity (Lin et al., 2005). Xiamycin which is an indolosesquiterpene compound isolated from endophytic actinomycetes showed strong antiviral activity by blocking HIV-1 infection, however, its methyl ester derivative was even more efficient and exhibited wide range of antimicrobial, antioxidative, and antiviral properties (Ding et al., 2010). Apart from xiamycin, researchers have also identified indosespene and sespenine both isolated from Streptomyces sp. HKI0595 that also exhibited substantial antiviral activity (Ding et al., 2011a, 2011b). Similarly, a novel staurosporine compound streptocarbazoles isolated from an endophytic actinomycetes of mangrove plants known to contain glycosidic linkage between two indole nitrogen atoms and two carbon atoms of glycosyl moiety. Studies have shown that streptocarbazoles A possess antiviral activity and capable of showing cytotoxic activity against HeLa cell lines with IC50 value of 1.4–35 μM (Fu et al., 2012). Furthermore, the antiviral properties of streptocarbazoles A were also confirmed by performing gene inactivation experiment followed by heterologous expression of that particular gene in S. coelicolor M1152 (Li et al., 2013). Additionally, in another study, Li et al. (2011) identified a novel staurosporine analog that also exhibited strong antiviral activity against human colon tumor cell HCT-116 with IC50 of 0.37 μM.

9.4.5 Antimalarial compounds Endophyte strains isolated from Shorea ovalis like Streptomyces sp. SUK10 that producing bioactive compounds diketopiperazine gancidin W, an antimalarial agent against Plasmodium berghei PZZ1/100 (Tanvir et al., 2018). In a study, SYBR Green assay was used to confirm the anti-malarial activity of marine actinomycete Salinispora tropica. The result of the study showed that the marine actinomycete exhibited strong inhibitory effect against several human malignant cell types. Furthermore, researchers have also identified an antimalarial compound Salinospoamide A as a potent inhibitor of melanoma cells as well as also exhibited strong proteolytic activity against 20S proteasome without inhibiting other proteases (Tanvir et al., 2018). In addition, researchers have also identified four new antimalarial compounds, that is, β-carboline, indolactum alkaloids, 13-N-demethyl-methylpendolmycin, and pendolmycin that exhibited strong inhibitory activity against Plasmodium falciparum (Huang et al., 2011). All these alkaloids have also been reported to show antimalarial activity under in vivo condition in mice. All these alkaloids belong to small group of nine-membered indolactum alkaloids displaying antimalarial activity over wide range of targets (Huang et al., 2011).

214

Microbial Endophytes: Prospects for Sustainable Agriculture

9.4.6 Antidiabetic compounds Some endophytes produced antidiabetic compounds like a-glucosidase that inhibits alpha-amylase. Endophytic actinomycetes such as Lysimachia ciliata, Streptomyces longisporoflavus, isolated from the stem of Leucas ciliata and Rauwolfia densiflora isolated from the endophytic strain such as Microbispora sp. GMKU 363 isolated from Clinacanthus siamensis that produces bioactive compound linfurone. Their bioactivity was reported in antidiabetic and antiatherogenic assays (Nalini and Prakash, 2017). Several studies have confirmed that the endophytic actinomycetes are able to inhibit α-amylase which is a key enzyme actively involved in the hydrolysis of starch. Researchers around the globe have documented that cultures of Streptomyces hygroscopicus ssp. limonetus, Streptomyces diastaticus ssp. Amylostaticus, and Streptomycetes calvus had actively inhibited yeast α-amylase (Akshatha et al., 2014). In another study, 13 endophytic actinomycetes were screened for their ability to produce α-glucosidase inhibitor, out of which 10 isolates were found to synthesize α-glucosidase inhibitor (Pujiyanto et al., 2012). Furthermore, researchers also examined crude extract of BWA65 isolates from Tinospora crispa for synthesizing α-glucosidase inhibitor enzyme and found that it was able to produce highest inhibition of α-glucosidase of about 80% compared to control (Singh and Dubey, 2015). Parallel to this, clinical trials conducted in rats and rabbits have indicated that regular administration of aqueous or alcoholic extract of BWA65 isolates from Tinospora cordifolia is effective in reducing blood sugar level and decreasing hyperglycemia (Akshatha et al., 2014).

9.5

Concluding remark and future prospective

Endophytic actinomycetes are unexplored class of microorganisms with tremendous source of functional bioactive compounds having wide range of functions which are effective against various pathogens. However, apart from their pharmaceutical use member of Gram-positive genus per se, Actinomycetes have been reported to have beneficial associations with plants having agronomic importance. The variety of bioactive compounds produced by these endophytic actinomycetes contain substances/ compounds which the potential to improve plant growth, thus recognizing as plant growth-promoting actinomycetes (PGPA). Therefore, it has become imperative to analyze, scrutinize, and highlight the previous attainments, ongoing research and recent advancements made in the exploration of endophytic actinomycetes to draw the attention of scientific community toward the endless possibility and the available sources for their exploitation in pharmaceutical, agricultural, food, and cosmetic industries.

References Abdel-Mageed, W.M., Milne, B.F., Wagner, M., Schumacher, M., Sandor, P., Pathom-aree, W., Goodfellow, M., Bull, A.T., Horikoshi, K., Ebel, R., Diederich, M., 2010. Dermacozines, a

Endophytic actinomycetes in bioactive compounds production and plant defense system

215

new phenazine family from deep-sea dermacocci isolated from a Mariana Trench sediment. Org. Biomol. Chem. 8 (10), 2352–2362. Abd-Elnaby, H., Abo-Elala, G., Abdel-Raouf, U., Abd-elwahab, A., Hamed, M., 2016. Antibacterial and anticancer activity of marine Streptomyces parvus: optimization and application. Biotechnol. Biotechnol. Equip. 30 (1), 180–191. Ahemad, M., Kibret, M., 2014. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud. Univ. Sci. 26, 1–20. https://doi.org/ 10.1016/j.jksus.2013.05.001. Akshatha, V.J., Nalini, M.S., D’souza, C., Prakash, H.S., 2014. Streptomycete endophytes from anti-diabetic medicinal plants of the Western Ghats inhibit alpha-amylase and promote glucose uptake. Lett. Appl. Microbiol. 58 (5), 433–439. Aktar, M.W., Sengupta, D., Chowdhury, A., 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip. Toxicol. 2, 1–12. https://doi.org/10.2478/v10102-0090001-7. Amrita, K., Nitin, J., Devi, C.S., 2012. Novel bioactive compounds from mangrove derived actinomycetes. Int. Res. J. Pharm. 3, 25–29. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.M., Bertalan, M., 2011. Enterotypes of the human gut microbiome. Nature 473 (7346), 174. Asaf, S., Khan, M.A., Khan, A.L., Waqas, M., Shahzad, R., Kim, A.Y., et al., 2017. Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. J. Plant Interact. 12, 31–38. https://doi.org/10.1080/17429145.2016.1274060. Atta, H.M., Bayoumi, R., Sehrawi, M., Galal, G.F., 2011. EI-Taxonomic studies and phylogenetic characterization of Streptomyces rimosus-KH-isolated from Al-Khurmah Governorate KSA. Researcher 3 (9), 1223–1255. Azman, A.S., Othman, I., Velu, S.S., Chan, K.G., Lee, L.H., 2015. Mangrove rare actinobacteria: taxonomy, natural compound, and discovery of bioactivity. Front. Microbiol. 6856. https://doi.org/10.3389/fmicb.2015.00856. Bacon, C.W., White, J.F., 2000. Microbial Endophytes. Marcel Dekker, New York. Bae, M., Chung, B., Oh, K.B., Shin, J., Oh, D.C., 2015. Hormaomycins B and C: new antibiotic cyclic depsipeptides from a marine mudflat-derived Streptomyces sp. Mar. Drugs 13, 5187–5200. https://doi.org/10.3390/md13085187. Baskaran, R., Mohan, P.M., Sivakumar, K., Raghavan, P., Sachithanandam, V., 2012. Phyllosphere microbial populations of ten true mangrove species of the Andaman Island. Int. J. Microbiol. Res. 3, 124–127. https://doi.org/10.5829/idosi.ijmr.2012.3.2.6221. B
erdy, J., 2012. Thoughts and facts about antibiotics: where we are now and where we are heading. J. Antibiot. 65 (8), 385. Bernstein, L., Bosch, P., Canziani, O., Chen, Z., Crist, R., et al., 2007. Summary for policymakers of the synthesis report. In: Allali, A. (Ed.), Climate Change, 2007: Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p. 22. Bian, G.K., Feng, Z.Z., Qin, S., Xing, K., Wang, Z., Cao, C.L., Jiang, J.H., 2012a. Kineococcus endophytica sp. nov., a novel endophytic actinomycete isolated from a coastal halophyte in Jiangsu, China. Antonie Van Leeuwenhoek 102 (4), 621–628. Bian, G.K., Qin, S., Yuan, B., Zhang, Y.J., Xing, K., Ju, X.Y., Jiang, J.H., 2012b. Streptomyces phytohabitans sp. nov., a novel endophytic actinomycete isolated from medicinal plant Curcuma phaeocaulis. Antonie Van Leeuwenhoek 102 (2), 289–296.

216

Microbial Endophytes: Prospects for Sustainable Agriculture

Bister, B., Bischoff, D., Str€obele, M., Riedlinger, J., Reicke, A., Wolter, F., Bull, A.T., Z€ahner, H., Fiedler, H.P., S€ussmuth, R.D., 2004. Abyssomicin C—a polycyclic antibiotic from a marine Verrucosispora strain as an inhibitor of the p-aminobenzoic acid/ tetrahydrofolate biosynthesis pathway. Angew. Chem. Int. Ed. 43 (19), 2574–2576. Boonsnongcheep, P., Nakashima, T., Takahashi, Y., Prathanturarug, S., 2017. Diversity of endophytic actinomycetes isolated from roots and root nodules of Pueraria candollei Grah. ex Benth. and the analyses of their secondary metabolites. Chiang Mai. J. Sci. 44, 1–14. Borrero, N.V., Bai, F., Perez, C., Duong, B.Q., Rocca, J.R., Jin, S., et al., 2014. Phenazine antibiotic inspired discovery of potent bromophenazine antibacterial agents against Staphylococcus aureus and Staphylococcus epidermidis. Org. Biomol. Chem. 12, 881–886. Doxorubicin. Brayfield, A. (Ed.), 2013. Martindale: The Complete Drug Reference. Pharmaceut Press Retrieved 15 April 2014. Bruntner, C., Binder, T., Pathom-aree, W., Goodfellow, M., Bull, A.T., Potterat, O., Puder, C., H€orer, S., Schmid, A., Bolek, W., Wagner, K., 2005. Frigocyclinone, a novel angucyclinone antibiotic produced by a Streptomyces griseus strain from Antarctica. J. Antibiot. 58 (5), 346. Cao, L., Qiu, Z., You, J., Tan, H., Zhou, S., 2004. Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett. Appl. Microbiol. 39, 425–430. https://doi.org/10.1111/j.1472-765X.2004.01606.x. Caruso, M., Colombo, A.L., Crespi-Perellino, N., Fedeli, L., Malyszko, J., Pavesi, A., Quaroni, S., Saracchi, M., Ventrella, G., 2000. Studies on a strain of Kitasatospora sp. paclitaxel producer. Ann. Microbiol. 50 (2), 89–102. Castillo, U., Harper, J.K., Strobel, G.A., Sears, J., Alesi, K., Ford, E., Lin, J., Hunter, M., Maranta, M., Ge, H., Yaver, D., 2003. Kakadumycins, novel antibiotics from Streptomyces sp. NRRL 30566, an endophyte of Grevillea pteridifolia. FEMS Microbiol. Lett. 224 (2), 183–190. Castillo, U.F., Strobel, G.A., Ford, E.J., Hess, W., Porter, H., Jensen, J., Albert, H., et al., 2002. Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscansa. Microbiology 148 (9), 2675–2685. Castillo, U.F., Strobel, G.A., Mullenberg, K., Condron, M.M., Teplow, D.B., Folgiano, V., Gallo, M., Ferracane, R., Mannina, L., Viel, S., Codde, M., 2006. Munumbicins E-4 and E-5: novel broad-spectrum antibiotics from Streptomyces NRRL 3052. FEMS Microbiol. Lett. 255 (2), 296–300. Chankhamhaengdecha, S., Hongvijit, S., Srichaisupakit, A., Charnchai, P., Panbangred, W., 2013. Endophytic actinomycetes: a novel source of potential acyl homoserine lactone degrading enzymes. Biomed. Res. Int. 2013782847. https://doi.org/10.1155/2013/782847. Charan, R.D., Schlingmann, G., Janso, J., Bernan, V., Feng, X., Carter, G.T., 2004. Diazepinomicin, a new antimicrobial alkaloid from a marine Micromonospora sp. J. Nat. Prod. 67 (8), 1431–1433. Chen, H.H., Qin, S., Li, J., Zhang, Y.Q., Xu, L.H., Jiang, C.L., Li, W.J., 2009. Pseudonocardia endophytica sp. nov., isolated from the pharmaceutical plant Lobelia clavata. Int. J. Syst. Evol. Microbiol. 59 (3), 559–563. Chomcheon, P., Suthep, W., Thammarat, A., Nongluksna, S., Nattaya, N., Chulabhorn, M., Somsak, R., Prasat, K., 2010. Curvularides A–E: antifungal hybrid peptide–polyketides from the endophytic fungus Curvularia geniculata. Chem Eur J 16 (36), 11178–11185. Conn, V.M., Franco, C.M., 2004. Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl. Environ. Microbiol. 70 (3), 1787–1794.

Endophytic actinomycetes in bioactive compounds production and plant defense system

217

Conti, R., Cunha, I.G., Siqueira, V.M., Souza-Motta, C.M., Amorim, E.L., Araujo, J.M., 2012. Endophytic microorganisms from leaves of Spermacoce verticillata (L.): diversity and antimicrobial activity. J. Appl. Pharm. Sci. 2 (12), 17. Das, A., Varma, A., 2009. Symbiosis: the art of living. In: Symbiotic Fungi. Springer, Berlin, Heidelberg, pp. 1–28. De Oliveira, M.F., da Silva, G.M., Sand, S.T.V.D., 2010. Antiphytopathogen potential of endophytic actinobacteria isolated from tomato plants (Lycopersicon sculentum) in southern Brazil, and characterization of Streptomyces sp. R18, a potential biocontrol agent. Res. Microbiol. 161, 565–572. https://doi.org/10.1016/j.resmic.2010.05.008. Dimkpa, C.O., Merten, D., Svatos, A., B€uchel, G., Kothe, E., 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107, 1687–1696. https://doi.org/ 10.1111/j.1365-2672.2009.04355.x. Dinesh, R., Srinivasan, V., TES, Anandaraj, M., Srambikkal, H., 2017. Endophytic actinobacteria: diversity, secondary metabolism and mechanisms to unsilence biosynthetic gene clusters. Crit. Rev. Microbiol. 43, 546–566. https://doi.org/10.1080/1040841X. 2016.1270895. Ding, L., Armin, M., Heinz-Herbert, F., Wen-Han, L., Christian, H., 2011a. A family of multicyclic indolosesquiterpenes from a bacterial endophyte. Org. Biomol. Chem. 9 (11), 4029–4031. Ding, L., Maier, A., Fiebig, H.H., G€orls, H., Lin, W.H., Peschel, G., Hertweck, C., 2011b. Divergolides A–D from a mangrove endophyte reveal an unparalleled plasticity in ansa-macrolide biosynthesis. Angew. Chem. 123 (7), 1668–1672. Ding, L., M€unch, J., Goerls, H., Maier, A., Fiebig, H.H., Lin, W.H., Hertweck, C., 2010. Xiamycin, a pentacyclic indolosesquiterpene with selective anti-HIV activity from a bacterial mangrove endophyte. Bioorg. Med. Chem. Lett. 20 (22), 6685–6687. Djinni, I., Defant, A., Kecha, M., Mancini, I., 2014. Metabolite profile of marine-derived endophytic Streptomyces sundarbansensis WR 1 L 1 S 8 by liquid chromatography–mass spectrometry and evaluation of culture conditions on antibacterial activity and mycelial growth. J. Appl. Microbiol. 116 (1), 39–50. Dochhil, H., Dkhar, M.S., Barman, D., 2013. Seed germination enhancing activity of endophytic Streptomyces Isolated from indigenous ethno-medicinal plant Centella asiatica. Int J Pharm. Bio. Sci 4 (1), 256–262. Du, H.J., Zhang, Y.Q., Liu, H.Y., Su, J., Wei, Y.Z., Ma, B.P., Guo, B.L., Yu, L.Y., 2013. Allonocardiopsis opalescens gen. nov., sp. nov., a new member of the suborder Streptosporangineae, from the surface-sterilized fruit of a medicinal plant. Int. J. Syst. Evol. Microbiol. 63 (3), 900–904. Dudeja, S.S., Giri, R., Saini, R., Suneja-Madan, P., Kothe, E., 2012. Interaction of endophytic microbes with legumes. J. Basic Microbiol. 52 (3), 248–260. Dutta, D., Puzari, K.C., Gogoi, R., Dutta, P., 2014. Endophytes: exploitation as a tool in plant protection. Braz. Arch. Biol. Technol. 57 (5), 621–629. El-Gendy, M.M., EL-Bondkly, A.M., 2010. Production and genetic improvement of a novel antimycotic agent, saadamycin, against dermatophytes and other clinical fungi from endophytic Streptomyces sp. Hedaya 48. J. Ind. Microbiol. Biotechnol. 37 (8), 831–841. El-Naggar, A.K., 2017. What is new in the World Health Organization 2017 histopathology classification? Curr. Treat. Options in Oncol. 18 (7), 43. El-Tarabily, K., Hardy, G.E.J., Sivasithamparam, K., 2010. Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions

218

Microbial Endophytes: Prospects for Sustainable Agriculture

in the United Arab Emirates. Eur. J. Plant Pathol. 128, 527–539. https://doi.org/10.1007/ s10658-010-9689-7. Endo, A., Danishefsky, S.J., 2005. Total synthesis of salinosporamide A. J. Am. Chem. Soc. 127 (23), 8298–8299. Ernawati, M., Solihin, D.D., Lestari, Y., 2016. Community structures of endophytic actinobacteria from medicinal plant Centella asiatica L. urban-based on metagenomic approach. Int J Pharm Pharm Sci 8, 292–297. Ezra, D., Castillo, U.F., Strobel, G.A., Hess, W.M., Porter, H., Jensen, J.B., Condron, M.A.M., et al., 2004. Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology 150, 785–793. Feling, R.H., Buchanan, G.O., Mincer, T.J., Kauffman, C.A., Jensen, P.R., Fenical, W., 2003. Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora. Angew. Chem. Int. Ed. 42 (3), 355–357. Francis, I.M., Jourdan, S., Fanara, S., Loria, R., Rigali, S., 2015. The cellobiose sensor CebR is the gatekeeper of Streptomyces scabies pathogenicity. MBio. 6, https://doi.org/10.1128/ mBio.02018-14 e02018-14. Fu, P., Yang, C., Wang, Y., Liu, P., Ma, Y., Xu, L., Su, M., Hong, K., Zhu, W., 2012. Streptocarbazoles A and B, two novel indolocarbazoles from the marine-derived actinomycete strain Streptomyces sp. FMA. Org. Lett. 14 (9), 2422–2425. Furumai, T., Yamakawa, T., Yoshida, R., Igarashi, Y., 2003. Clethramycin, a new inhibitor of pollen tube growth with antifungal activity from Streptomyces hygroscopicus TP-A0623. I. Screening, taxonomy, fermentation, isolation and biological properties. J. Antibiot. 56, 700–704. https://doi.org/10.7164/antibiotics.56.700. Gangwar, M., Dogra, S., Gupta, U.P., Kharwar, R.N., 2014. Diversity and biopotential of endophytic actinomycetes from three medicinal plants in India. Afr. J. Microbiol. Res. 8, 184–191. Ganihigama, U., Sanya, S., Sasithorn, S., Poonpilas, H., Thammarat, A., Chulabhorn, M., Somsak, R., Prasat, K., 2015. Antimycobacterial activity of natural products and synthetic agents: pyrrolodiquinolines and vermelhotin as anti-tubercular leads against clinical multidrug resistant isolates of Mycobacterium tuberculosis. Eur. J. Med. Chem. 89, 1–12. Gos, F.M.W.R., Savi, D.C., Shaaban, K.A., Thorson, J.S., Aluizio, R., Possiede, Y.M., et al., 2017. Antibacterial activity of endophytic actinomycetes isolated from the medicinal plant Vochysia divergens (Pantanal, Brazil). Front. Microbiol. 61642. https://doi.org/10.3389/ fmicb.2017.01642. Goudjal, Y., Toumatia, O., Sabaou, N., Barakate, M., Mathieu, F., Zitouni, A., 2013. Endophytic actinomycetes from spontaneous plants of Algerian Sahara: indole-3-acetic acid production and tomato plants growth promoting activity. World J. Microbiol. Biotechnol. 29, 1821–1829. https://doi.org/10.1007/s11274-013-1344-y. Goudjal, Y., Toumatia, O., Yekkour, A., Sabaoua, N., Mathieuc, F., Zitouni, A., 2014. Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol. Res. 169, 59–65. https://doi.org/10.1016/j.micres.2013.06.014. Gu, Q., Liu, N., Qiu, D.H., Liu, Z.H., Huang, Y., 2006. Isolation, classification and antimicrobial activity of endophytic actinomycetes from plant leaves. Acta Microbiol Sin. 46, 778–782. Gupta, N., Mishra, S., Basak, U.C., 2009. Diversity of Streptomyces in mangrove ecosystem of Bhitarkanika. Iran J. Microbiol. 1, 37–42. Available online at http://ijm.tums.ac.ir/index. php/ijm/article/view/28.26Jul.2018.

Endophytic actinomycetes in bioactive compounds production and plant defense system

219

Han, Z., Xu, Y., McConnell, O., Liu, L., Li, Y., Qi, S., Huang, X., Qian, P., 2012. Two antimycin A analogues from marine-derived actinomycete Streptomyces lusitanus. Mar. Drugs 10 (3), 668–676. Hasegawa, S., Meguro, A., Shimizu, M., Nishimura, T., Kunoh, H., 2006. Endophytic actinomycetes and their interactions with host plants. Actinomycetologica 20 (2), 72–81. He, H., Liu, C., Zhao, J., Li, W., Pan, T., Yang, L., Xiang, W., 2014. Streptomyces zhaozhouensis sp. nov., an actinomycete isolated from candelabra aloe (Aloe arborescens Mill). Int. J. Syst. Evol. Microbiol. 64 (4), 1096–1101. Higashide, E., Asai, M., Ootsu, K., Tanida, S., Kozai, Y., Hasegawa, T., Kishi, T., Sugino, Y., Yoneda, M., 1977. Ansamitocin, a group of novel maytansinoid antibiotics with antitumour properties from Nocardia. Nature 270 (5639), 721. Huang, H., Jiasen, L., Yonghua, H., Fang, Z., Zhang, K., Bao, S., 2008. Micromonospora rifamycinica sp. nov., a novel actinomycete from mangrove sediment. Int. J. Syst. Evol. Microbiol. 58, 17–20. https://doi.org/10.1099/ijs.0.64484-0. Huang, M.J., Rao, M.P.N., Salam, N., Xiao, M., Huang, H.Q., Li, W.J., 2017. Allostreptomyces psammosilenae gen. nov., sp. nov., an endophytic actinobacterium isolated from the roots of Psammosilene tunicoides and emended description of the family Streptomycetaceae [Waksman and Henrici (1943) AL] emend. Rainey et al. 1997, emend. Kim et al. 2003, emend. Zhi et al. 2009. Int. J. Syst. Evol. Microbiol. 67 (2), 288–293. Huang, H., Yao, Y., He, Z., Yang, T., Ma, J., Tian, X., Li, Y., Huang, C., Chen, X., Li, W., Zhang, S., 2011. Antimalarial β-carboline and indolactam alkaloids from Marinactinospora thermotolerans, a deep sea isolate. J. Nat. Prod. 74 (10), 2122–2127. Huang, X.L., Zhuang, L., Lin, H.P., Li, J., Goodfellow, M., Hong, K., 2012. Isolation and bioactivity of endophytic filamentous actinobacteria fromtropical medicinal plants. Afr. J. Biotechnol. 11, 9855–9864. https://doi.org/10.5897/AJB11.3839. Ibrahim, S.R.M., Elkhayat, E.S., Mohamed, G.A., Khedr, A.I.M., Fouad, M.A., Kotb, M.H.R., Ross, S.A., 2015. Aspernolides F and G, new butyrolactones from the endophytic fungus Aspergillus terreus. Phytochem. Lett. 14 (2015), 84–90. Igarashi, Y., Miura, S.S., Fujita, T., Furumai, T., 2006. Pterocidin, a cytotoxic compound from the endophytic Streptomyces hygroscopicus. J. Antibiot. 59 (3), 193. Igarashi, Y., Ogawa, M., Sato, Y., Saito, N., Yoshida, R., Kunoh, H., Onaka, H., Furumai, T., 2000. Fistupyrone, a novel inhibitor of the infection of Chinese cabbage by Alternaria brassicicola, from Streptomyces sp. TP-A0569. J. Antibiot. 53 (10), 1117–1122. Igarashi, Y., Yanase, S., Sugimoto, K., Enomoto, M., Miyanaga, S., Trujillo, M.E., Saiki, I., Kuwahara, S., 2011. Lupinacidin C, an inhibitor of tumor cell invasion from Micromonospora lupini. J. Nat. Prod. 74 (4), 862–865. Izumikawa, M., Hosoya, T., Takagi, M., Shin-ya, K., 2012. A new cyclizidine analog— JBIR-102—from Saccharopolyspora sp. RL78 isolated from mangrove soil. J. Antibiot. 65 (1), 41. Janardhan, A., Kumar, A.P., Viswanath, B., Saigopal, D.V.R., Narasimha, G., 2014. Production of bioactive compounds by actinomycetes and their antioxidant properties. Biotechnol. Res. Int. 2014, 1–8. Jensen, P.R., Williams, P.G., Oh, D.C., Zeigler, L., Fenical, W., 2007. Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl. Environ. Microbiol. 73 (4), 1146–1152. Jian, L., Lu, C., Shen, Y., 2010. Macrolides of the bafilomycin family produced by Streptomyces sp. CS. J. Antibiot. 63 (10), 595.

220

Microbial Endophytes: Prospects for Sustainable Agriculture

Jiang, Z.K., Pan, Z., Li, F.N., Li, X.J., Liu, S.W., Tuo, L., Sun, C.H., 2017. Marmoricola endophyticus sp. nov., an endophytic actinobacterium isolated from Thespesia populnea. Int. J. Syst. Evol. Microbiol. 67 (11), 4379–4384. Jiang, Z.K., Tuo, L., Huang, D.L., Osterman, I.A., Tyurin, A.P., Liu, S.W., et al., 2018. Diversity, novelty, and antimicrobial activity of endophytic actinobacteria from mangrove plants in Beilun Estuary National Nature Reserve of Guangxi, China. Front. Microbiol. 9868. https://doi.org/10.3389/fmicb.2018.00868. Jog, R., Pandya, M., Nareshkumar, G., Rajkumar, S., 2014. Mechanism of phosphate solubilization and antifungal activity of Streptomyces sp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160, 778–788. https://doi.org/10.1099/mic.0.074146-0. Kaewkla, O., Thamchaipinet, A., Franco, C.M.M., 2017. Micromonospora terminaliae sp. nov., an endophytic actinobacterium isolated from the surface-sterilized stem of the medicinal plant Terminalia mucronata. Int. J. Syst. Evol. Microbiol. 67 (2), 225–230. Kafur, A., Basheer Khan, A., 2011. Isolation of endophytic actinomycetes from Catharanthes roseus (L.) G. Don leaves and their antimicrobial activity. Iran. J. Biotechnol. 9 (4), 302–306. Kamboj, P., Gangwar, M., Singh, N., 2017. Scanning electron microscopy of endophytic actinomycete isolate against Fusarium oxysporum for various growth parameters on musk melon. Int. J. Curr. Microbiol. Appl. Sci. 6, 458–464. https://doi.org/10.20546/ijcmas. 2017.611.054. Kanoh, K., Matsuo, Y., Adachi, K., Imagawa, H., Nishizawa, M., Shizuri, Y., 2005. Mechercharmycins A and B, cytotoxic substances from marine-derived Thermoactinomyces sp. YM3-251. J. Antibiot. 58 (4), 289. Kaur, T., Sharma, D., Kaur, A., Manhas, R.K., 2013. Antagonistic and plant growth activities of endophytic and soil actinomycetes. Arch. Phytopathol. Plant Protect. 46, 1756–1768. Kawahara, T., Izumikawa, M., Otoguro, M., Yamamura, H., Hayakawa, M., Takagi, M., Shinya, K., 2012. JBIR-94 and JBIR-125, antioxidative phenolic compounds from Streptomyces sp. R56-07. J. Nat. Prod. 75 (1), 107–110. Khamna, S., Yokota, A., Lumyong, S., 2009. Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J. Microbiol. Biotechnol. 25, 649–655. https://doi.org/ 10.1007/s11274-008-9933-x. Khare, E., Mishra, J., Arora, N.K., 2018. Multifaceted interactions between endophytes and plant: developments and prospects. Front. Microbiol. 9. Kim, N., Shin, J.C., Kim, W., Hwang, B.Y., Kim, B.S., Hong, Y.S., Lee, D., 2006. Cytotoxic 6-alkylsalicylic acids from the endophytic Streptomyces laceyi. J. Antibiot. 59 (12), 797. Kumar, R.R., Jadeja, V.J., 2016. Endophytic actinomycetes: a novel antibiotic source. Int. J. Curr. Microbiol. App. Sci. 5 (8), 164–175. Kuncharoen, N., Pittayakhajonwut, P., Tanasupawat, S., 2018. Micromonospora globbae sp. nov., an endophytic actinomycete isolated from roots of Globba winitii CH Wright. Int. J. Syst. Evol. Microbiol. 68 (4), 1073–1077. Li, T., Du, Y., Cui, Q., Zhang, J., Zhu, W., Hong, K., Li, W., 2013. Cloning, characterization and heterologous expression of the indolocarbazole biosynthetic gene cluster from marinederived Streptomyces sanyensis FMA. Mar. Drugs 11 (2), 466–488. Li, W., Guo, X., Shi, L., Zhao, J., Yan, L., Zhong, X., Xiang, W., 2018. Plantactinospora solaniradicis sp. nov., a novel actinomycete isolated from the root of a tomato plant (Solanum lycopersicum L.). Antonie Van Leeuwenhoek 111 (2), 227–235.

Endophytic actinomycetes in bioactive compounds production and plant defense system

221

Li, J., Lu, C.H., Shen, Y.M., 2010. Macrolides of the bafilomycin family produced by Streptomyces sp. CS. J. Antibiot. https://doi.org/10.1038/ja.2010.95. Li, F., Maskey, R.P., Qin, S., Sattler, I., Fiebig, H.H., Maier, A., Zeeck, A., Laatsch, H., 2005. Chinikomycins A and B: isolation, structure elucidation, and biological activity of novel antibiotics from a marine Streptomyces sp. isolate M045, 1. J. Nat. Prod. 68 (3), 349–353. Li, X.B., Tang, J.S., Gao, H., Ding, R., Li, J., Hong, K., Yao, X.S., 2011. A new staurosporine analog from Actinomycetes Streptomyces sp. (172614). J. Asian Nat. Prod. Res. 13 (8), 765–769. Li, W., Xueqiong, Y., Yabin, Y., Lixing, Z., Lihua, X., Zhongtao, D., 2015. A new anthracycline from endophytic Streptomyces sp. YIM66403. J. Antibiot. 68 (3), 216. Li, W., Yang, X., Yang, Y., Zhao, L., Xu, L., Ding, Z., 2015. A new anthracycline from endophytic Streptomyces sp. YIM66403. J. Antibiot. 68 (3), 216. Li, H., Zhang, Q., Li, S., Zhu, Y., Zhang, G., Zhang, H., Tian, X., Zhang, S., Ju, J., Zhang, C., 2012. Identification and characterization of xiamycin A and oxiamycin gene cluster reveals an oxidative cyclization strategy tailoring indolosesquiterpene biosynthesis. J. Am. Chem. Soc. 134 (21), 8996–9005. Lin, W., Li, L., Fu, H., Sattler, I., Huang, X., Grabley, S., 2005. New cyclopentenone derivatives from an endophytic Streptomyces sp. isolated from the mangrove plant Aegiceras comiculatum. J. Antibiot. 58 (9), 594. Lin, C., Lu, C., Shen, Y., 2010. Three new 2-pyranone derivatives from mangrove endophytic actinomycete strain Nocardiopsis sp. A00203. Rec. Nat. Prod. 4 (4), 176–179. Lin, L., Xu, X., 2013. Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated from medicinal plants. Curr. Microbiol. 67, 209–217. Liu, S.W., Tuo, L., Li, X.J., Li, F.N., Li, J., Jiang, M.G., et al., 2017. Mangrovihabitans endophyticus gen. nov., sp. nov., a new member of the family Micromonosporaceae isolated from Bruguiera sexangula. Int. J. Syst. Evol. Microbiol. 67, 1629–1636. https://doi.org/ 10.1099/ijsem.0.001764. Liu, K., Yabin, Y., Cui-Ping, M., You-Kun, Z., Jin-Lian, C., You-Wei, C., Li-Hua, X., HuiLin, G., Zhong-Tao, D., Li-Xing, Z., 2016. Koningiopisins A–H, polyketides with synergistic antifungal activities from the endophytic fungus Trichoderma koningiopsis. Planta Med. 82 (04), 371–376. Lowicki, D., Nski, A.H., 2013. Structure and antimicrobial properties of Monensin A and its derivatives: summary of the achievements. Biomed. Res. Int. https://doi.org/10.1155/ 2013/742149. Lu, C., Shen, Y., 2007. A novel ansamycin, naphthomycin K from Streptomyces sp. J. Antibiot. 60 (10), 649. Machavariani, N.G., Ivankova, T.D., Sineva, O.N., Terekhova, L.P., 2014. Isolation of endophytic actinomycetes from medicinal plants of the Moscow region. Russia. World Appl. Sci. J. 30 (11), 1599–1604. Macherla, V.R., Liu, J., Bellows, C., Teisan, S., Nicholson, B., Lam, K.S., Potts, B.C., 2005. Glaciapyrroles A, B, and C, pyrrolosesquiterpenes from a Streptomyces sp. isolated from an Alaskan marine sediment. J. Nat. Prod. 68 (5), 780–783. Mahmoud, A.Y., Abdallah, H.M., El-Halawani, M.A., Jiman-Fatani, A.A.M., 2015. Antituberculous activity of Treponemycin produced by a Streptomyces strain MS-6-6 isolated from Saudi Arabia. Molecules 20, 2576–2590. https://doi.org/10.3390/ molecules20022576. Martinez-Klimova, E., Rodriguez-Pena, K., Sanchez, S., 2017. Endophytes as sources of antibiotics. Biochem. Pharmacol. 134, 1–17.

222

Microbial Endophytes: Prospects for Sustainable Agriculture

Masand, M., Sivakala, K.K., Menghani, E., Rangasamy, A., Thangadurai, T., Sharma, G., Sivakumar, N., Jebakumar, S.R., Arul Jose, P., 2018. Biosynthetic potential of bioactive streptomycetes isolated from arid region of the Thar Desert, Rajasthan (India). Front. Microbiol. 9, 687. Maskey, R.P., Li, F.C., Qin, S., Fiebig, H.H., Laatsch, H., 2003. Chandrananimycins AC: production of novel anticancer antibiotics from a marine Actinomadura sp. isolate M048 by variation of medium composition and growth conditions. J. Antibiot. 56 (7), 622–629. Maskey, R.P., Sevvana, M., Uso´n, I., Helmke, E., Laatsch, H., 2004. Gutingimycin: a highly complex metabolite from a marine streptomycete. Angew. Chem. Int. Ed. 43 (10), 1281–1283. Matsumoto, A., Takahashi, Y., 2017. Endophytic actinomycetes: promising source of novel bioactive compounds. J. Antibiot. 70 (5), 514. McArthur, K.A., Mitchell, S.S., Tsueng, G., Rheingold, A., White, D.J., Grodberg, J., Lam, K.S., Potts, B.C., 2008. Lynamicins A E, chlorinated bisindole pyrrole antibiotics from a novel marine Actinomycete. J. Nat. Prod. 71 (10), 1732–1737. Meguro, A., Hasegawa, S., Nishimura, T., Kunoh, H., 2006. Salt tolerance in tissue-cultured seedlings of mountain laurel enhanced by endophytic colonization of Streptomyces padanus AOK-30. In: Abst. 2006 Annu. Meeting of Soc. Actinomycetes Japan2006, p. 97 (in Japanese). Mingma, R., Duangmal, K., Thamchaipenet, A., Trakulnaleamsai, S., Matsumoto, A., Takahashi, Y., 2015. Streptomyces oryzae sp. nov., an endophytic actinomycete isolated from stems of rice plant. J. Antibiot. 68 (6), 368. Mini Priya, R., 2012. Endophytic actinomycetes from Indian medicinal plants as antagonists to some phytopathogenic fungi. Open Access Sci. Rep. 1, 259. Mitchell, S.S., Nicholson, B., Teisan, S., Lam, K.S., Potts, B.C., 2004. Aureoverticillactam, a novel 22-atom macrocyclic lactam from the marine actinomycete Streptomyces aureoverticillatus. J. Nat. Prod. 67 (8), 1400–1402. Mohammadipanah, F., Wink, J., 2016. Actinobacteria from arid and desert habitats: diversity and biological activity. Front. Microbiol. 61541. https://doi.org/10.3389/fmicb. 2015.01541. Moussa, H.E., El-Shatoury, S.A., Abdul, O.A., Dewedar, W., Dewedar, A., 2011. Characterization of endophytic actinomycetes from wild Egyptian plants as antagonists to some phytopathogenic fungi. Egyptian J. Nat. Toxins. 8. Muangham, S., Lipun, K., Matsumoto, A., Inahashi, Y., Duangmal, K., 2018. Quadrisphaera oryzae sp. nov., an endophytic actinomycete isolated from leaves of rice plant (Oryza sativa L.). J. Antibiot. 1. Nalini, M.S., Prakash, H.S., 2017. Diversity and bioprospecting of actinomycete endophytes from the medicinal plants. Lett. Appl. Microbiol. 64 (4), 261–270. Nimnoi, P., Pongsilp, N., Lumyong, S., 2010. Endophytic actinomycetes isolated from Aquilaria crassna Pierre ex. Lec and screening of plant growth-promoters production. World J. Microbiol. Biotechnol. 26, 193–203. https://doi.org/10.1007/s11274-009-0159-3. Okazaki, T., 2003. Studies on actinomycetes isolated from plant leaves. In: Kurtb€ oke, I. (Ed.), Selective Isolation of Rare Actinomycetes. National Library of Australia, Canberra, pp. 102–122. Omojate Godstime, C., Enwa Felix, O., Jewo Augustina, O., Eze Christopher, O., 2014. Mechanisms of antimicrobial actions of phytochemicals against enteric pathogens—a review. J. Pharm. Chem. Biol. Sci. 2 (2), 77–85. Owen, N.L., Hundley, N., 2004. Endophytes—the chemical synthesizers inside plants. Sci. Prog. 87 (2), 79–99.

Endophytic actinomycetes in bioactive compounds production and plant defense system

223

Palaniyandi, S., Yang, S.H., Damodharan, K., Suh, J.W., 2013. Genetic and functional characterization of culturable plant-beneficial actinobacteria associated with yam rhizosphere. J. Basic Microbiol. 53, 985–995. https://doi.org/10.1002/jobm.201200531. Passari, A.K., Mishra, V.K., Saikia, R., Gupta, V.K., Singh, B.P., 2015. Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Front. Microbiol. 6e00273 https://doi.org/10.3389/fmicb.2015.00273. Passari, A.K., Mishra, V.K., Singh, G., Singh, P., Kumar, B., Gupta, V.K., Sharma, R.K., Saikia, R., Donovan, A.O., Singh, B.P., 2017. Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci. Rep. 711809. Pesic, A., Steinhaus, B., Kemper, S., Nachtigall, J., Kutzner, H.J., Hofle, G., Sussmuth, R.D., 2014. Isolation and structure elucidation of the nucleoside antibiotic strepturidin from Streptomyces albus DSM 40763. J. Antibiot. 67, 471–477. https://doi.org/10.1038/ ja.2014.16. Phuakjaiphaeo, C., Kunasakdakul, K., 2015. Isolation and screening for inhibitory activity on Alternaria brassicicola of endophytic actinomycetes from Centella asiatica (L.) Urban. J. Agri. Technol. 11, 903–912. Piel, J., Hoang, K., Moore, B.S., 2000. Natural metabolic diversity encoded by the enterocin biosynthesis gene cluster. J. Am. Chem. Soc. 122 (22), 5415–5416. Pimentel, M.R., Molina, G., Dionı´sio, A.P., Maro´stica Junior, M.R., Pastore, G.M., 2011. The use of endophytes to obtain bioactive compounds and their application in biotransformation process. Biotechnol. Res. Int. 2011. Potts, B.C., Lam, K.S., 2010. Generating a generation of proteasome inhibitors: from microbial fermentation to total synthesis of salinosporamide a (marizomib) and other salinosporamides. Mar. Drugs 8 (4), 835–880. Pozzi, R., Simone, M., Mazzetti, C., Maffioli, S., Monciardini, P., Cavaletti, L., Bamonte, R., Sosio, M., Donadio, S., 2011. The genus Actinoallomurus and some of its metabolites. J. Antibiot. 64 (1), 133. Prakash, O., Nimonkar, Y., Munot, H., Sharma, A., Vemuluri, V.R., Chavadar, M.S., Shouche, Y.S., 2014. Description of Micrococcusaloeverae sp. nov., an endophytic actinobacterium isolated from Aloe vera. Int. J. Syst. Evol. Microbiol. 64 (10), 3427–3433. Prashar, P., Shah, S., 2016. Impact of fertilizers and pesticides on soil microflora in agriculture. In: Sustainable Agriculture Reviews. vol. 19. pp. 331–362. https://doi.org/10.1007/978-3319-26777-7_8. Pujiyanto, S., Lestari, Y.U.L.I.N., Suwanto, A., Budiarti, S., Darusman, L.K., 2012. Alphaglucosidase inhibitor activity and characterization of endophytic actinomycetes isolated from some Indonesian diabetic medicinal plants. Int J Pharm Pharm Sci 4 (1), 327–333. Purushotham, N., Jones, E., Monk, J., Ridgway, H., 2018. Community structure of endophytic actinobacteria in a New Zealand native medicinal plant Pseudowintera colorata (Horopito) and their influence on plant growth. Microb. Ecol. 1153–1159. https://doi. org/10.1007/s00248-018-1153-9. Qin, S., Li, J., Chen, H.H., Zhao, G.Z., Zhu, W.Y., Jiang, C.L., et al., 2009. Isolation diversity and antimicrobial activity of rare actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna, China. Appl. Environ. Microbiol. 75, 6176–6186. https://doi.org/ 10.1128/AEM.01034-09. Qin, S., Xing, K., Jiang, J.H., Xu, L.H., Li, W.J., 2011. Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl. Microbiol. Biotechnol. 89, 457–473. https://doi.org/10.1007/s00253-010-2923-6.

224

Microbial Endophytes: Prospects for Sustainable Agriculture

Qin, S., Bian, G.K., Zhang, Y.J., Xing, K., Cao, C.L., Liu, C.H., Dai, C.C., Li, W.J., Jiang, J.H., 2013. Modestobacter roseus sp. nov., an endophytic actinomycete isolated from the coastal halophyte Salicornia europaea Linn., and emended description of the genus Modestobacter. Int. J. Syst. Evol. Microbiol. 63 (6), 2197–2202. Rachniyom, H., Matsumoto, A., Indananda, C., Duangmal, K., Takahashi, Y., Thamchaipenet, A., 2015. Nonomuraea syzygii sp. nov., an endophytic actinomycete isolated from the roots of a jambolan plum tree (Syzygium cumini L. Skeels). Int. J. Syst. Evol. Microbiol. 65 (4), 1234–1240. Rajivgandhi, G., Ramachandran, G., Maruthupandy, M., Saravanakumar, S., Manoharan, N., 2018. Antibacterial effect of endophytic actinomycetes from marine algae against multi drug resistant gram negative bacteria. Exam. Mar. Biol. Oceanogr. 1 (4), 1–8. Raju, R., Gromyko, O., Fedorenko, V., Luzketsky, A., Muller, R., Albaflavenol, B., 2015. Albaflavenol B, a new sesquiterpene isolated from the terrestrial actinomycete, Streptomyces sp. J. Antibiot. 68, 286–288. https://doi.org/10.1038/ja.2014.138. Ren, Y., Gary, A., Strobel, C., Graff, J., Sung, P., Sankar, G., David, T., et al., 2008. Colutellin A, an immunosuppressive peptide from Colletotrichum dematium. Microbiology 154 (7), 1973–1979. Rungin, S., Indananda, C., Suttiviriya, P., Kruasuwan, W., Jaemsaeng, R., Thamchaipenet, A., 2012. Plant growth enhancing effects by a siderophore producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek 102, 463–472. https://doi.org/10.1007/s10482-012-9778-z. Sabu, R., Soumya, K.R., Radhakrishnan, E.K., 2017. Endophytic Nocardiopsis sp. from Zingiber officinale with both antiphytopathogenic mechanisms and antibiofilm activity against clinical isolates. 3 Biotech 7 (2), 115. Salam, N., Khieu, T.N., Liu, M.J., Vu, T.T., Chu-Ky, S., Quach, N.T., Phi, Q.T., Rao, N., Prabhu, M., Fontana, A., Sarter, S., 2017. Endophytic actinobacteria associated with Dracaena cochinchinensis Lour.: isolation, diversity, and their cytotoxic activities. BioMed Res. Int. 2017, Article ID 1308563. Sanglier, J.J., Haag, H., Huck, T.A., Fehr, T., 1993. Novel bioactive compounds from actinomycetes: a short review (1988–1992). Res. Microbiol. 144 (8), 633–642. Sansinenea, E., Ortiz, A., 2011. Secondary metabolites of soil Bacillus spp. Biotechnol. Lett. 33, 1523–1538. https://doi.org/10.1007/s10529-011-0617-5. Sasaki, T., Igarashi, Y., Saito, N., Furumai, T., 2001a. TPU-0031-A and B, new antibiotics of the novobiocin group produced by Streptomyces sp. TP-A0556. J. Antibiot. 54 (5), 441–447. Sasaki, T., Igarashi, Y., Saito, N., Furumai, T., 2001b. Cedarmycins, A., and B, new antimicrobial antibiotics from Streptomyces sp. TP-A0456. J. Antibiot. 54, 567–572. https://doi.org/ 10.7164/antibiotics.54.567. Savi, D.C., Haminiuk, C.W.I., Sora, G.T.S., Adamoski, D.M., Kenski, J., Winnischofer, S.M.B., Glienke, C., 2015a. Antitumor, antioxidant and antibacterial activities of secondary metabolites extracted by endophytic actinomycetes isolated from vochysia divergens. Int. J. Pharm. Chem. Biol. Sci. 5(1). Savi, D.C., Shaaban, K.A., Ponomareva, L.V., Possiede, Y.M., Thorson, J.S., Glienke, C., et al., 2015b. Microbispora sp. LGMB259 endophytic actinomycete isolated from Vochysia divergens (Pantanal, Brazil) producing b- carbolines and indoles with biological activity. Curr. Microbiol. 70, 345–354. https://doi.org/10.1007/s00284-014-0724-3. Savi, D.C., Shaaban, K.A., Vargas, N., Ponomareva, L.V., Possiede, Y.M., Thorson, J.S., Glienke, C., J€urgen, R., 2015c. Microbispora sp. LGMB259 endophytic actinomycete

Endophytic actinomycetes in bioactive compounds production and plant defense system

225

isolated from Vochysia divergens (Pantanal, Brazil) producing β-carbolines and indoles with biological activity. Curr. Microbiol. 70 (3), 345–354. Schenk, P.M., Carvalhais, L.C., Kazan, K., 2012. Unraveling plant microbe interactions: can multi-species transcriptomics help? Trends Biotechnol. 30, 177–184. https://doi.org/ 10.1016/j.tibtech.2011.11.002. Schumacher, R.W., Talmage, S.C., Miller, S.A., Sarris, K.E., Davidson, B.S., Goldberg, A., 2003. Isolation and structure determination of an antimicrobial ester from a marine sediment-derived bacterium. J. Nat. Prod. 66 (9), 1291–1293. Segaran, G., Sundar, R.D.V., Settu, s., Shankar, S., Sathiavelu, M., 2017. A review on endophytic actinomycetes and their applications. J. Chem. Pharm. Res. 9 (10), 152–158. Selim, K.A., El-Beih, A.A., Abdel-Rahman, T.M., El-Diwany, A.I., 2014. Biological evaluation of endophytic fungus, Chaetomium globosum JN711454, as potential candidate for improving drug discovery. Cell Biochem. Biophys. 68, 67–82. Sessitsch, A., Kuffner, M., Kidd, P., Vangronsveld, J., Wenzel, W.W., Fallmann, K., et al., 2013. The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol. Biochem. 60, 182–194. https://doi.org/10.1016/j. soilbio.2013.01.012. Shan, W., Zhou, Y., Liu, H., Yu, X., 2018. Endophytic actinomycetes from tea plants (Camellia sinensis): isolation, abundance, antimicrobial, and plant-growth-promoting activities. Biomed. Res. Int. 20181470305. Shen, Y., Liu, C., Wang, X., Zhao, J., Jia, F., Zhang, Y., Xiang, W., 2013. Actinoplanes hulinensis sp. nov., a novel actinomycete isolated from soybean root (Glycine max (L.) Merr). Antonie Van Leeuwenhoek 103 (2), 293–298. Shutsrirung, A., Chromkaew, Y., Pathom-Aree, W., Choonluchanon, S., Boonkerd, N., 2013. Diversity of endophytic actinomycetes in mandarin grown in northern Thailand, their phytohormone production potential and plant growth promoting activity. Soil Sci. Plant Nutr. 59, 322–330. https://doi.org/10.1080/00380768.2013.776935. Singh, R., Dubey, A.K., 2015. Endophytic actinomycetes as emerging source for therapeutic compounds. Indo Global J. Pharm. Sci. 5, 106–116. Singh, R., Dubey, A.K., 2018. Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches. Front. Microbiol. 9. Singh, M., Kumar, A., Singh, R., Pandey, K.D., 2017. Endophytic bacteria: a new source of bioactive compounds. 3 Biotech 7 (5), 315. Snipes, C.E., Duebelbeis, D.O., Olson, M., Hahn, D.R., Dent Iii, W.H., Gilbert, J.R., Werk, T.L., Davis, G.E., Lee-Lu, R., Graupner, P.R., 2007. The ansacarbamitocins: polar ansamitocin derivatives. J. Nat. Prod. 70 (10), 1578–1581. Strobel, G.A., 2003. Endophytes as source of bioactive products. Microbes Infect. 5, 535–544. Strobel, G.A., Daisy, B., 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev. 67, 491–502. https://doi.org/10.1128/MMBR.67.4.491502.2003. Strobel, G., Daisy, B., Castillo, U., Harper, J., 2004. Natural products from endophytic microorganisms. J. Nat. Prod. 67 (2), 257–268. Strobel, G., Yang, X., Sears, J., Kramer, R., Sidhu, R.S., Hess, W.M., 1996. Taxol from Pestalotio psismicrospora, an endophytic fungus of Taxuswallachiana. Microbiology 142, 435–440. Sun, C.H., Li, F.N., Cai, Z., Wu, L., 2017. Brief introduction of mangrove researches including drug discovery granted by National Natural Science Foundation of China from 1986 to 2016. Chin. J. Antibiot. 42, 241–248. https://doi.org/10.13461/j.cnki.cja.005904.

226

Microbial Endophytes: Prospects for Sustainable Agriculture

Supong, K., Chitti, T., Wilunda, C., Chokchai, K., Dusanee, T., Chamroon, L., Prommart, K., Nonglak, P., Pattama, P., 2016. Antimicrobial compounds from endophytic Streptomyces sp. BCC72023 isolated from rice (Oryza sativa L.). Res. Microbiol. 167 (4), 290–298. Taechowisan, T., Chanaphat, S., Ruensamran, W., Phutdhawong, W.S., 2014. Antibacterial activity of new flavonoids from Streptomyces sp. BT01; an endophyte in Boesenbergia rotunda (L.) Mansf. J. Appl. Pharm. Sci. 4, 8–13. https://doi.org/10.7324/JAPS. 2014.40402. Taechowisan, T., Lu, C., Shen, Y., Lumyong, S., 2007. Antitumor activity of 4-arylcoumarins from endophytic Streptomyces aureofaciens CMUAc130. J. Cancer Res. Ther. 3 (2), 86. Taechowisan, T., Peberdy, J.F., Lumyong, S., 2003. Isolation of endophytic actinomycetes from selected plants and their antifungal activity. World J. Microbiol. Biotechnol. 19, 381–385. https://doi.org/10.1023/A:1023901107182. Taechowisan, T., Wanbanjob, A., Tuntiwachwuttikul, P., Taylor, W.C., 2006. Identification ofStreptomyces sp. Tc022, an endophyte inAlpinia galanga, and the isolation of actinomycin D. Ann. Microbiol. 56 (2), 113–117. Takagi, M., Shin-ya, K., 2011. New species of actinomycetes do not always produce new compounds with high frequency. J. Antibiot. 64 (10), 699. Tanvir, R., Sajid, I., Hasnain, S., 2014. Larvicidal potential of Asteraceae family endophytic actinomycetes against Culex quinquefasciatus mosquito larvae. Nat. Prod. Res. 28 (22), 2048–2052. Tanvir, R., Sajid, I., Hasnain, S., Kulik, A., Gron, S., 2016. Rare actinomycetes Nocardia caishijiensis and Pseudonocardia carboxydivorans as endophytes; their bioactivity and metabolites evaluation. Microbiol. Res. 185, 22–35. https://doi.org/10.1016/j.micres. 2016.01.003. Tanvir, R., Sheikh, A.A., Javeed, A., 2018. Endophytic actinomycetes in the biosynthesis of bioactive metabolites: chemical diversity and the role of medicinal plants. In: Studies in Natural Products Chemistry.vol. 60. pp. 399–424. Thamchaipenet, A., Indananda, C., Bunyoo, C., Duangmal, K., Matsumoto, A., Takahashi, Y., 2010. Actinoallomurus acaciae sp. nov., an endophytic actinomycete isolated from Acacia auriculiformis, A. Cunn. ex Benth. Int. J. Syst. Evol. Microbiol. 60, 554–559. https://doi. org/10.1099/ijs.0.012237-0. Thumar, J.T., Dhulia, K., Singh, S.P., 2010. Isolation and partial purification of an antimicrobial agent from halotolerant alkaliphilic Streptomyces aburaviensis strain Kut-8. World J. Microbiol. Biotechnol. 26, 2081–2087. https://doi.org/10.1007/s11274-010-0394-7. Ting, A.S.Y., Hermanto, A., Peh, K.L., 2014. Indigenous actinomycetes from empty fruit bunch compost of oil palm: evaluation on enzymatic and antagonistic properties. Biocatal. Agr. Biotechnol. 3, 310–315. https://doi.org/10.1016/j.bcab.2014.03.004. Tiwari, K., Gupta, R.K., 2012. Rare actinomycetes: a potential storehouse for novel antibiotics. Crit. Rev. Biotechnol. 32 (2), 108–132. Torre, L.A., Bray, F., Siegel, R.L., Ferlay, J., Lortettieulent, J., Jemal, A., 2015. Global cancer statistics, 2012. CA Cancer J. Clin. 65, 87–108. Toumatia, O., Compant, S., Yekkour, A., Goudjal, Y., Sabaou, N., Mathieu, F., et al., 2016. Biocontrol and plant growth promoting properties of Streptomyces mutabilis strain IA1 isolated from a Saharan soil on wheat seedlings and visualization of its niches of colonization. S. Afr. J. Bot. 105, 234–239. https://doi.org/10.1016/j.sajb.2016.03.020. Tuntiwachwuttikul, P., Taechowisan, T., Wanbanjob, A., Thadaniti, S., Taylor, W.C., 2008. Lansai A–D, secondary metabolites from Streptomyces sp. SUC1. Tetrahedron 64 (32), 7583–7586.

Endophytic actinomycetes in bioactive compounds production and plant defense system

227

Van der Hiejden, M.G.A., Bardgett, R.D., van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x. Verma, V.C., Anand, S., Ulrichs, C., Singh, S.K., 2013. Biogenic gold nanotriangles from Saccharomonospora sp., an endophytic actinomycetes of Azadirachta indica A. Juss. Int. Nano Lett. 3 (1), 21. Verma, V.C., Singh, S.K., Prakash, S., 2011. Biocontrol and plantgrowth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. J. Basic Microbiol. 51, 550–556. https://doi.org/10.1002/jobm.201000155. Viterbo, A., Landau, U., Kim, S., Chernin, L., Chet, I., 2010. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol. Lett. 305, 42–48. https://doi.org/10.1111/j.1574-6968.2010. 01910.x. Wan, M., Li, G., Zhang, J., Jiang, D., Huang, H.C., 2008. Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol. Control 46, 552–559. https://doi.org/10.1016/j.biocontrol.2008.05.015. Wang, P., Fandong, K., Jingjing, W., Yi, W., Wei, W., Kui, H., Weiming, Z., 2014. Alkaloids from the mangrove-derived actinomycete Jishengella endophytica 161111. Mar. Drugs 12 (1), 477–490. Wang, Z., Tian, J., Li, X., Gan, L., He, L., Chu, Y., Tian, Y., 2018. Streptomyces dioscori sp. nov., a novel endophytic actinobacterium isolated from bulbil of Dioscorea bulbifera L. Curr. Microbiol. 75 (10), 1384–1390. Wang, F., Xu, M., Li, Q., Sattler, I., Lin, W., 2010. p-Aminoacetophenonic acids produced by a mangrove endophyte Streptomyces sp.(strain HK10552). Molecules 15 (4), 2782–2790. Wang, H.F., Zhang, Y.G., Chen, J.Y., Guo, J.W., Li, L., Hozzein, W.N., et al., 2015a. Frigoribacterium endophyticum sp. nov., an endophytic actinobacterium isolated from the root of Anabasis elatior (C. A. Mey.) Schischk. Int. J. Syst. Evol. Microbiol. 65, 1207–1212. https://doi.org/10.1099/ijs.0.000081. Wang, H.F., Zhang, Y.G., Cheng, J., Hozzein, W.N., Liu, W.H., Li, L., et al., 2015b. Labedella endophytica sp. nov., a novel endophytic actinobacterium isolated from stem of Anabasis elatior (C. A. Mey.) Schischk. Int. J. Syst. Evol. Microbiol. 107, 95–102. https://doi.org/ 10.1007/s10482-014-03070. Wang, H.F., Zhang, Y.G., Li, L., Liu, W.H., Hozzein, W.N., Chen, J.Y., et al., 2015c. Okibacterium endophyticum sp. nov., a novel endophytic actinobacterium isolated from roots of Salsola affinis C. A. Mey. Antonie Van Leeuwenhoek 107, 835–843. https:// doi.org/10.1007/s10482-014-0376-0. Wei, Y.Z., Zhang, Y.Q., Zhao, L.L., Li, Q.P., Su, J., Liu, H.Y., et al., 2010. Isolation, screening and preliminary identification of endophytic actinobacteria from mangroves at Shankou of Guangxi Province. Microbiol. China 37, 823–828. Wijeratne, E.M., Kithsiri, H., Scott, G., Franzblau, M., Hoffman, A.A., Leslie, G., 2013. Phomapyrrolidones A–C, antitubercular alkaloids from the endophytic fungus Phoma sp. NRRL 46751. J. Nat. Prod. 76 (10), 1860–1865. Williams, P.G., Buchanan, G.O., Feling, R.H., Kauffman, C.A., Jensen, P.R., Fenical, W., 2005. New cytotoxic Salinosporamides from the marine actinomycete Salinispora t ropica. J. Org. Chem. 70 (16), 6196–6203. Wu, H., Chen, W., Wang, G., Dai, S., Zhou, D., Zhao, H., Guo, Y., Ouyang, Y., Li, X., 2012. Culture-dependent diversity of Actinobacteria associated with seagrass (Thalassia hemprichii). Afr. J. Microbiol. Res. 6 (1), 87–94.

228

Microbial Endophytes: Prospects for Sustainable Agriculture

Xing, K., Bian, G.K., Qin, S., Klenk, H.P., Yuan, B., Zhang, Y.J., et al., 2012. Kibdelosporangium phytohabitans sp. nov., a novel endophytic actinomycete isolated from oil-seed plant Jatropha curcas L. containing 1- aminocyclopropane-1-carboxylic acid deaminase. Antonie Van Leeuwenhoek 101, 433–441. https://doi.org/10.1007/ s10482-011-9652-4. Xu, D.B., Ye, W.W., Han, Y., Deng, Z.X., Hong, K., 2014. Natural products from mangrove actinomycetes. Mar. Drugs. 12, 2590–2613. https://doi.org/10.3390/md12052590. Yamazaki, Y., Someno, T., Igarashi, M., Kinoshita, N., Hatano, M., Kawada, M., et al., 2015. Androprostamines A and B, the new anti-prostatecancer agents produced by Streptomyces sp. MK932-CF8. J. Antibiot. 68, 279–285. https://doi.org/10.1038/ja.2014.135. Yan, L.L., Han, N.N., Zhang, Y.Q., Yu, L.Y., Chen, J., Wei, Y.Z., Li, Q.P., Tao, L., Zheng, G.H., Yang, S.E., Jiang, C.X., Zhang, X.D., Huang, Q., Habdin, X., Hu, Q.B., Li, Z., Liu, S.W., Zhang, Z.Z., He, Q.Y., Si, S.Y., Sun, C.H., 2010. Antimycin A18 produced by an endophytic Streptomyces albido flavus isolated from a mangrove plant. J. Antibiot. 63, 259–261. Yan, X., Li, Y., Wang, N., Chen, Y., Huang, L.L., 2018. Streptomyces ginkgonis sp. nov., an endophyte from Ginkgo biloba. Antonie Van Leeuwenhoek 111 (6), 891–896. Yandigeri, M.S., Meena, K.K., Singh, D., Malviya, N., Singh, D.P., Solanki, M.K., et al., 2012. Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul. 68, 411–420. https://doi.org/10.1007/ s10725-012-9730-2. Yang, X., Tianfeng, P., Yabin, Y., Wei, L., Jie, X., Lixing, Z., Zhongtao, D., 2015a. Antimicrobial and antioxidant activities of a new benzamide from endophytic Streptomyces sp. YIM 67086. Nat. Prod. Res. 29 (4), 331–335. Yang, G.L., Yang, L.F., Jiang, M.G., Wu, J.F., Gan, G.H., Tuo, L., et al., 2015b. Isolation, identification and bioactivity of endophytic actinomycetes from mangrove plants in Beilun River. J. Agric. Biol. 23, 894–904. Yang, X., Yang, Y., Peng, T., Yang, F., Zhou, H., Zhao, L., Xu, L., Ding, Z., 2013. A new cyclopeptide from endophytic Streptomyces sp. YIM 64018. Nat. Prod. Commun. 8 (12), 1753–1754. Yu, H., Zhang, L., Li, L., Zheng, C., Guo, L., Li, W., Sun, P., Qin, L., 2010. Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol. Res. 165 (6), 437–449. Zhang, Y.G., Wang, H.F., Alkhalifah, D.H.M., Xiao, M., Zhou, X.K., Liu, Y.H., et al., 2018. Glycomyces anabasis sp. nov., a novel endophytic actinobacterium isolated from roots of Anabasis aphylla L. Int. J. Syst. Evol. Microbiol. 68, 1285–1290. https://doi.org/10.1099/ ijsem.0.002668. Zhang, J., Wang, J.D., Liu, C.X., Yuan, J.H., Wang, X.J., Xiang, W.S., 2014. A new prenylated indole derivative from endophytic actinobacteria Streptomyces sp. neau-D50. Nat. Prod. Res. 28, 431–437. https://doi.org/10.1080/14786419.2013.871546. Zhang, Y.J., Zhang, W.D., Qin, S., Bian, G.K., Xing, K., Li, Y.F., et al., 2013. Saccharopolyspora dendranthemae sp. nov. a halotolerant endophytic actinomycete isolated froma coastal salt marsh plant in Jiangsu, China. Antonie Van Leeuwenhoek 103, 1369–1376. https://doi.org/10.1007/s10482-013-9917-1. Zhou, Z., Jin, B., Yin, W., Chunyan, F.U., Feng, H., 2011. Components in antineoplastic actinomycete strain (N2010-37) of bottom mud in mangrove. Chin. Herb. Med. 3 (3), 165–167. Zhou, H., Yabin, Y., Jucheng, Z., Tianfeng, P., Lixing, Z., Lihua, X., Zhongtao, D., 2013. Alkaloids from an endophytic Streptomyces sp. YIM66017. Nat. Prod. Commun. 8 (10), 1393–1396.

Endophytic actinomycetes in bioactive compounds production and plant defense system

229

Zhou, H., Yang, Y., Peng, T., Li, W., Zhao, L., Xu, L., Ding, Z., 2014. Metabolites of Streptomyces sp., an endophytic actinomycete from Alpinia oxyphylla. Nat. Prod. Res. 28 (4), 265–267. Zhu, W.Y., Zhang, J.L., Qin, Y.L., Xiong, Z.J., Zhang, D.F., Klenk, H.P., Li, W.J., 2013. Blastococcus endophyticus sp. nov., an actinobacterium isolated from Camptotheca acuminata. Int. J. Syst. Evol. Microbiol. 63 (9), 3269–3273. Zhu, W.Y., Zhao, L.X., Zhao, G.Z., Duan, X.W., Qin, S., Li, J., Li, W.J., 2012. Plantactinospora endophytica sp. nov., an actinomycete isolated from Camptotheca acuminata Decne., reclassification of Actinaurispora siamensis as Plantactinospora siamensis comb. nov. and emended descriptions of the genus Plantactinospora and Plantactinospora mayteni. Int. J. Syst. Evol. Microbiol. 62 (10), 2435–2442. Zin, N.M., Baba, M.S., Zainal-Abidin, A.H., Latip, J., Mazlan, N.W., Edrada-Ebel, R., 2017. Gancidin, W., a potential low-toxicity antimalarial agent isolated from an endophytic Streptomyces SUK10. Drug Des. Devel. Ther. 11, 351–363. https://doi.org/10.2147/ DDDT.S121283.

Further reading Hardoim, P.R., Overbeek, L.S., Elsas, J.D., 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463–471. https://doi.org/10.1016/ j.tim.2008.07.008. Lv, Y.L., Fu-shengm, Z., Juan, C., Jin-long, C., Yong-mei, X., Xiang-dong, L., Shun-xing, G., 2010. Diversity and antimicrobial activity of endophytic fungi associated with the alpine plant Saussurea involucrata. Biol. Pharm. Bull. 33 (8), 1300–1306. Potts, B.C., Albitar, M.X., Anderson, K.C., Baritaki, S., Berkers, C., Bonavida, B., Chandra, J., Chauhan, D., Cusack, J.C., Fenical, W., M Ghobrial, I., 2011. Marizomib, a proteasome inhibitor for all seasons: preclinical profile and a framework for clinical trials. Curr. Cancer Drug Targets 11 (3), 254–284. Qiu, P., Feng, Z.X., Tian, J.W., Lei, Z.C., Wang, L., Zeng, Z.G., Chu, Y.W., Tian, Y.Q., 2015. Diversity, bioactivities, and metabolic potentials of endophytic actinomycetes isolated from traditional medicinal plants in Sichuan, China. Chin. J. Nat. Med. 13 (12), 942–953. Xing, K., Qin, S., Fei, S.M., Lin, Q., Bian, G.K., Miao, Q., Li, W.J., 2011. Nocardia endophytica sp. nov., an endophytic actinomycete isolated from the oil-seed plant Jatropha curcas L. Int. J. Syst. Evol. Microbiol. 61 (8), 1854–1858.