Endophytic bacteria from the medicinal plants and their potential applications

Endophytic bacteria from the medicinal plants and their potential applications

2

R. Aswani, P. Jishma, E.K. Radhakrishnan School of Biosciences, Mahatma Gandhi University, Kottayam, India

2.1

Introduction

Medicinal plants have been extensively used in the traditional medicine to promote human health and immunity. They have also been identified to possess a wide spectrum of pharmacological properties due to their potential to synthesize broad range medicinal natural products (Akerele et al., 1991). Diverse types of medicinal plants are traditionally used for the treatment of various diseases such as asthma, skin disorders, respiratory, gastrointestinal and urinary problems, etc. (Akerele et al., 1991; Bajguz, 2007). This is due to their bioactive compounds which can have a primary role to protect the plants from different biotic and abiotic stresses (Cushnie et al., 2014; Vardhini and Anjum, 2015; Zhao et al., 2011a). The presence and quantity of these biologically active metabolites in medicinal plants may vary depending on the plant species, soil type, and their association with microbial communities (Morsy, 2014; Faeth, 2002). The genetic recombination between the medicinal plants and the associated microorganisms over the evolutionary period is also considered to play an important role in the bioactive metabolites production (Sun et al., 2013). Plantassociated microorganisms generally include epiphytes and endophytes. Epiphytes are the microorganisms that reside on plant surfaces and endophytes are the microorganisms that reside within the plant. Endophytic microorganisms, the important components of plant micro-ecosystems, have recently been identified to be the most widespread inhabitants of plant tissues which provide beneficial effects to the host plant. The endophytic microorganisms are described to be distributed in all plant parts including roots, leaves, stems, flowers, fruits, and also in seeds and it can be isolated from the surface-disinfected plant tissues using sodium hypochlorite or similar agents (Egamberdieva et al., 2010; Lodewyckx et al., 2002). Surface sterilization is a prerequisite for the isolation of endophytic microorganisms from various plant sources. This can help to eliminate possible contaminants, foreign materials, and epiphytic microorganisms and to favor the specific growth of internal microorganisms. Cutting the plant material into many small pieces has also been demonstrated to enhance the efficiency of sterilization (Mich and Balandreau, 2001). The success of surface sterilization and the complete removal contaminated microorganisms can be confirmed by the absence of any microbial growth by plating of last wash of surface sterilization Microbial Endophytes: Prospects for Sustainable Agriculture. https://doi.org/10.1016/B978-0-12-818734-0.00002-4 © 2020 Elsevier Inc. All rights reserved.

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Microbial Endophytes: Prospects for Sustainable Agriculture

procedure onto the culture media or by imprinting of sterilized material on agar surface (Mich and Balandreau, 2001). Many recent studies have been focused on the isolation and characterization of endophytic microorganisms and these are reported to have important role in plant growth and protection. This in turn has made endophytes to be used as an excellent source of bioinoculant for various agricultural applications. The long-term applications of agrochemicals for the enhancement of crop productivity and to manage plant diseases have negatively influenced the soil quality and caused environmental pollution (Sabu et al., 2017). To minimize the negative effects of the conventional agriculture techniques, innovative methods based on the microbial inoculation have projected to have much interest. The plants and endophytic microorganisms form a symbiotic association by which both the partners are benefitted. Plants provide habitat for the microbes and plants in turn rely on their microbiome for the specific requirements including growth promotion, nutrient mobilization and acquisition, induced systemic resistance, and protection from biotic and abiotic stress factors (Aktar et al., 2009; Egamberdieva et al., 2010, 2017; Sessitsch et al., 2013). Many studies have demonstrated the production of valuable metabolites from medicinal plants, however, the production of some of these are also reported from endophytic microbiome which indicates its significance. The established relationship of endophytes with their host plants indicates its significant influence on the formation of metabolic products in plants (Fig. 2.1). Therefore, exploration of new resources for the endophytic microbe isolation, identification, and screening for the production of bioactive metabolites is of great importance. Studies on endophytic microorganisms showed its important role in the biosynthesis of metabolites from medicinal plants and also in its quality as well as quantity (Berg et al., 2014). However, very little is known about the plant growth-promoting endophytes of medicinal plants. Therefore, the chapter describes about the relationship between endophytes and medicinal plants including plant growth and bioactive metabolite production mechanisms.

2.2

Types of endophytic microorganisms

Endophytic microorganisms associated with plants mainly include bacteria (actinomycetes or mycoplasma) and fungi. Endophytic bacteria reside within the interior tissues of plants and play an important role in plant growth promotion and disease protection. Diverse species of endophytic bacteria reported from various plants range from Gram-positive to Gram-negative bacteria. These include Achromobacter, Acinetobacter, Agrobacterium, Bacillus, Brevibacterium, Microbacterium, Pseudomonas, etc. (Golinska et al., 2015). Endophytic microorganisms mainly belong to the phyla Actinobacteria, Proteobacteria, and Firmicutes (Zhao et al., 2011b). Actinomycetes are the transitional forms between the fungi and bacteria and they belong to the phylum Actinobacteria. Streptomyces is reported as one of the dominant genera and has been commonly isolated as endophyte (Hollants et al., 2011) with the ability to produce bioactive metabolites. Some of the active compounds isolated from endophytic microorganisms include munumbicins (A and B), naphthomycin (A and K),

Endophytic microorganisms from the medicinal plants and their potential applications

17

Antibiotics

Alkaloids

Terpenoids

ACC deaminase

Phytohormones

Biosynthetic potential of endophytic microorganisms Siderophores and HCN

Anticancer compounds

Lytic enzymes

Antioxidants Antimicrobial compounds

Fig. 2.1 Biosynthetic potential of endophytic microorganisms associated with medicinal plants.

clethramycin, coronamycin, cedarmycin (A and B), saadamycin, and kakadumycins (Zhao et al., 2011b). Mycoplasma species are also reported as endophytes having symbiotic association with some red algae, such as Bryopsis pennata and Bryopsis hypnoides (Bhardwaj and Agrawal, 2014). Endophytic fungi have been classified into clavicipitaceous endophytes, which infect some grasses and the nonclavicipitaceous endophytes, which are from asymptomatic tissues of nonvascular plants, ferns and allies, conifers, and angiosperms ( Jalgaonwala et al., 2011). Endophytic fungi also produce some of the most broadly used antibiotic and anticancer drugs including taxol by Taxomyces andreanae and the antimicrobial compounds clavatol by Aspergillus clavatonanicus, sordaricin by Fusarium sp., and javanicin from Chloridium sp. which clearly demonstrate the biosynthetic potential of endophytic fungi from diverse plant sources (Hartmann et al., 2008).

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2.3

Microbial Endophytes: Prospects for Sustainable Agriculture

Adaptation of bacteria to endophytic lifestyle

The studies on the role of bacteria in the rhizosphere have mainly provided the gateway information about the possible mechanisms of bacterial communities inside plants and their endophytic lifestyle. Rhizosphere can be defined as the rootsurrounding the soil characterized by high microbial abundance (Berg et al., 2005; Hardoim et al., 2015). Therefore, it is considered as a nutrient-rich microbial hotspot and thus a highly competitive living environment. To gain a competitive advantage, some of the rhizospheric bacteria penetrate into plant organs and sustain both saprophytic and endophytic lifestyles (Sturz et al., 2000). Endophytic bacteria can enter into the plants through tissue wounds, stomata, lenticels, and via the germinating radicles (Zeidler et al., 2004). Endophytic bacteria are also known to colonize the plants by entering through root cracks, root hairs, and also from the seeds by vertical transmission (Fig. 2.2). During the transition from rhizosphere to the plant endosphere, the colonizing bacteria must have the ability to quickly adapt to a highly different environment in terms of pH, osmotic pressure, carbon source, and the availability of oxygen. They should also have the capability to overcome plant defense responses mediated through the production of reactive oxygen species (ROS) which cause stress to invading bacteria (Reinhold-Hurek et al., 2006). Also the bacterial ability to establish as endophytic population is likely to be dependent on various factors such as recognition of signal molecules, mobility, and penetration capability through the production of various enzymes (Hurek et al., 1994). Once the microbial communities get enter into the plants, they either become localized at the entry point or spread

Fig. 2.2 Various routes of entry of endophytic bacteria into plants.

Endophytic microorganisms from the medicinal plants and their potential applications

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throughout the plant and colonize the intercellular spaces and vascular systems (Bell et al., 1995; Beneduzi et al., 2012).

2.4

Diversity of bacterial endophytes in medicinal plants

The plant microbiome consists of distinct microbial communities living in association with diverse parts of plants (Qi et al., 2012; Berg et al., 2005). Many studies have focused on endophytic bacteria due to their intimate interaction with the host (ElDeeb et al., 2013) and the phytochemical constituents of plants are considered to have direct or indirect influence on endophytic microbes and their interactions with host plants ( Janardhan and Vijayan, 2012). Due to the huge and diverse range of metabolite richness, medicinal plants are known to harbor potential endophytic microbes (Table 2.1) with distinct biosynthetic features. Therefore, recent studies have been focused on diversity of endophytic microorganisms from medicinal plants and utilization of their potential to synthesize numerous novel secondary metabolic products including antibiotics, anticancer, antifungal, and antiviral compounds. These reports highlight the need for understanding the endophytic microbial diversity in medicinal plants to elucidate their functions and potential applications. Culture-dependent approaches have been generally used for bacterial diversity analysis but it can be influenced by cultivation media and growth conditions. Therefore, endophytic bacterial communities are also analyzed based on 16S rRNA-based techniques like denaturing gradient gel electrophoresis, 16S rRNA gene cloning, and sequencing. It has gained great interest and provided more specific, replicable, and detailed description about the microbial diversity. The introduction of next-generation sequencing (NGS) both by pyrosequencing and Illumina Miseq has also enabled to perform in-depth sequencing of hundreds of samples in one run, making it an excellent tool for endophytic microbial diversity studies (Singh et al., 2017a).

2.5

Biosynthetic potential of bacterial endophytes for plant growth and protection

Plant diseases caused by various bacterial and fungal pathogens cause major limitation to the cultivation of plants and its productivity. Some endophytic microorganisms can mediate priming of plants and systemically elicit a faster and stronger plant defense against the pathogen attack. Primed plants can have limited changes in defense-related gene expression in the absence of a pathogen, but mount an accelerated defense response upon pathogen or insect attack and provide a broad spectrum of resistance ( Jasim et al., 2016a,b). The antimicrobial compounds produced by endophytic bacteria provide promising protection to plants against phytopathogens (Han et al., 2015). This was confirmed by the extraction and purification of various compounds like lipopeptides from Bacillus spp. (Chung et al., 2016; D’Alessandro et al., 2014). Exogenous treatment of purified lipopeptide compounds in cotton plants has been reported to trigger the microbe-associated molecular pattern-based immunity, ROS

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Microbial Endophytes: Prospects for Sustainable Agriculture

Table 2.1 List of selected endophytic bacteria isolated from different medicinal plants Medicinal plant Plectranthus tenuiflorus

Lantana camara Linn.

Tridax procumbens Linn.

Endophytic bacteria

References

Bacillus spp., Bacillus megaterium, Bacillus pumilus, Bacillus licheniformis, Micrococcus luteus, Paenibacillus sp., Pseudomonas sp., and Acinetobacter calcoaceticus Bacillus spp., Chryseobacterium daejeonense, Enterobacter cancerogenus, Enterobacter cloacae, Enterobacter cowanii, Pantoea eucalypti, Pantoea stewartii, Pseudomonas spp., Pseudomonas argentinensis, Raoultella planticola Bacillus spp., Cronobacter sakazakii, Enterobacter spp., Lysinibacillus sphaericus, Pantoea spp., Pseudomonas spp. and Terribacillus saccharophilus Bacillus spp.

Bell et al. (1995)

Azadirachta indica Terminalia arjuna Ferula songorica Glycyrrhiza uralensis B. monnieri

Bacillus mojavensis

B. monnieri

Bacillus sp.

Trichilia elegans A. Juss. Echinacea purpurea

Staphylococcus, Bacillus, Microbacterium, Pseudomonas, and Pantoea

Allium schoenoprasum Chenopodium album Gundelia tournefortii Phaseolus vulgaris Teucrium polium

Bacillus spp. Ralstonia, Bacillus, Pseudomonas, Acinetobacter, Brevundimonas Bacillus atrophaeus and Bacillus mojavensis

Achromobacter sp., Agrococcus sp., Agrobacterium sp. Arthrobacter sp., Flavobacterium, Pseudomonas sp., Kineococcus sp., Microbacterium sp. Bacillus aryabhattai Bacillus pumilus Bacillus sp. Bacillus sp. Pseudomonas graminis

Beneduzi et al. (2012)

Qi et al. (2012)

El-Deeb et al. (2013) El-Deeb et al. (2013) Janardhan and Vijayan (2012) Singh et al. (2017a) Jasim et al. (2016a) Jasim et al. (2016b) Han et al. (2015) Chung et al. (2016)

Beiranvand et al. (2017) Beiranvand et al. (2017) Beiranvand et al. (2017) Beiranvand et al. (2017) Beiranvand et al. (2017)

Endophytic microorganisms from the medicinal plants and their potential applications

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burst, disruption of cell-wall integrity, and effect on fungal signaling pathways and thereby protection to the plant from pathogen attack (D’Alessandro et al., 2014). In addition to this, endophytic bacteria are also able to produce volatile organic compounds (VOCs) (Gohain et al., 2015) to confer resistance to plants. D’Alessandro et al. (2014) have demonstrated the inoculation of endophytic Enterobacter aerogenes with the potential to produce VOC 2,3-butanediol (2,3-BD) onto maize plants with the resulting resistance enhancement against Setosphaeria turcica, the causative agent of northern corn leaf blight. As the medicinal plants are enriched with bioactive molecules, an in-depth study on microbiome associated with such plant species can offer promises to identify bioactive compounds from associated microorganisms with applications in various fields of research. Endophytes exist as principal microbial communities coupled with plants and live with symbiotic association by sharing nutrients and protecting the host from pathogens by synthesizing bioactive compounds (Tan and Zou, 2001). The metabolite synthesizing efficacy of endophytes from medicinal plants has a positive relation with host plant because of the genetic recombination with the host over evolutionary time (Clay, 1988). With the production of various secondary metabolites, endophytes effectively compete with the coexisting microorganisms associated with the host plants and colonize successfully in the host. The bioactive metabolites of natural origin are unique in structure and include compounds like alkaloids, benzopyranones, chinones, quinones, saponins, flavonoids, phenols, steroids, tannins, terpenoids, tetralones, and xanthones with broad functions and novel applications in various fields. These are synthesized by various bioresources and the compounds can function as antiviral, antibacterial, antifungal, cytotoxic, and immunosuppressive agents (Shukla et al., 2014; Soujanya et al., 2017). Endophytes form largely unexplored source of such compounds. Endophytic microorganisms have been reported as incredible resource of drugs for various diseases and many bioactive compounds with potential applications in agriculture, food, and cosmetics industries ( Jasim et al., 2015). These bioactive compounds such as camptothecin have been reported to be produced by different species of endophytes isolated from respective plants and indicate their application in both agricultural and pharmaceutical industries (Strobel, 2003; Palanichamy et al., 2018). This biosynthetic property of endophytes has been correlated with the evolution of the host, where endophytic function provides protection to plants from various types of diseases caused by bacteria, fungi, and insects (Clay and Schardl, 2002). In addition to this biosynthetic property, endophytic microorganisms within the root tissues also support plant by modulation of nutrient composition, production of phytohormones, alteration of chemical composition of root exudates, and protection to the plant from biotic and abiotic stresses (Khan et al., 2013; Ryan et al., 2008). One of the major functions of endophytic microbiome is the plant growth promotion and is made possible by the endophytes by indwelling the plant tissues (Franken, 2012). The release of phytohormones from endophytic microorganisms toward plant tissues enhances tissue elongation and differentiation. Endophytes have the ability to solubilize insoluble phosphate by synthesizing various organic acids and they also have the potential to synthesize ACC deaminase, siderophores, HCN, VOCs, and antibiotics which directly or indirectly enhance the plant growth (Pahari et al., 2017).

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Microbial Endophytes: Prospects for Sustainable Agriculture

Many previous studies have reported the biosynthetic potential of various species of both endophytic bacteria and fungi, and their ability to modulate the phytocompound production and these are expected to have more valuable applications. Bacillus sp., an endophytic bacterium isolated from Capsicum annuum was found to induce the production of diosgenin, a pharmacologically significant plantspecific metabolite in Fenugreek (Trigonella foenum-graecum L.) seedlings ( Jasim et al., 2015). Also, camptothecin producing endophytic Bacillus spp. from medicinally important plant Pyrenacantha volubilis Hook. (Family: Icacinanceae) has been reported by Soujanya et al. (2017). These studies pointed out the biosynthetic potential of various endophytic bacteria and its efficient colonization in nonhost plant together with the production of broad spectrum of bioactive compounds or ability to induce such compound production in plants.

2.6

Biosynthetic sharing between bacterial endophytes and the host plant

The endophytic microbial population mediated plant growth promotion and disease protection in plants is mainly acquired through metabolic interactions. A large number of metabolites have been reported from plant microsymbionts which play an important role in plant productivity and defense responses. These secondary metabolites may also serve as excellent source of various compounds with broad applications in agriculture, medicine, food, and cosmetics industries (Berg et al., 2005; Stierle et al., 1993; Heinig et al., 2013). Even though there are so many reports on the production of secondary metabolites from endophytes, synthesis of plant-specific metabolites by endophytes and their capability of synthesizing the same compound in nonhost plant is highly attractive. Coproduction of host-specific bioactive metabolites from both plants as well as their associated fungal endophytes includes the anticancer drugs paclitaxel (Taxol) (Heinig et al., 2013), camptothecin (Puri et al., 2005), podophyllotoxin (Puri et al., 2006), and the natural insecticide azadirachtin (Kusari et al., 2012). Endophytic bacteria have also revealed the sharing of bioactive compounds with their host plant. For example, stem extracts of Alternanthera brasiliana (Family: Amaranthaceae) contained antimicrobial compounds from the oxylipin family and the endophytic bacteria isolated from Alternanthera plants have also been identified to have the ability to produce oxylipins (Trapp et al., 2015). There are several mechanisms proposed for the simultaneous production of these biological compounds. One of the proposed mechanisms is the vertical transmission of endophytes from the seeds to seedlings and by horizontal gene transfer between the host plant and its endophytes (Taghavi et al., 2005; Shahzad et al., 2018). On the other hand, it has been strongly suggested to be the result of extreme adaptation of endophytes to their host and it thereby contributes to the coproduction of these bioactive molecules (B€ omke and Tudzynski, 2009). Study on bacterial endophytes Acinetobacter sp. and Marmoricola sp. from the Papaver somniferum L. also revealed its ability to upregulate the expression of key genes involved in the biosynthesis of benzylisoquinoline alkaloid compounds (Pandey et al., 2016). While in some cases such as in the production of gibberellin, the

Endophytic microorganisms from the medicinal plants and their potential applications

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biosynthetic mechanisms for the same compound is considered to be evolved independently in plants and their microbiome (Pieterse et al., 2009).

2.7

Impact of bacterial endophytes on secondary metabolites production in plants

The presence of various biologically active metabolites in the medicinal plants contributes to their application in medicinal, agricultural, and industrial fields. The concentration of these bioactive compounds is species specific and they may vary due to several factors such as plant material, cultivation method, plant treatment, and the extraction methods. Recently, genomics and proteomics approaches have been used to understand the role of endophytes during plant endophyte interaction (Kaul and Sharma, 2016). Proteomic analysis on in vitro grown Zea mays and Chinese hybrid poplar clone 741 showed differential accumulation of proteins between plants treated with endophytic bacteria and the untreated plants (Scherling et al., 2009). This result revealed the possibility of inducing secondary metabolite production in plants by endophytic bacteria. Plant and endophyte metabolism can exhibit various level of relationships with each other for their metabolite production which includes (a) endophytic bacteria-induced modulation of secondary metabolite production in host plant, (b) production of host-specific metabolites by endophytes, and (c) the host metabolism of products from the endophyte and vice versa (Ludwig-M€uller, 2015). (a) Endophytic bacteria-induced modulation of secondary metabolite production in host plant

The established relationship of endophytic bacteria with their host plant indicates their significant influence on the production of various bioactive metabolites in plants. Some endophytic bacteria with potential plant growth promoting and biocontrol features can be exploited as microbial inoculants which in turn can enhance the synthesis and production of biologically active compounds in the host plant. Studies on inoculation of turmeric rhizomes with endophytic Azotobacter chroococcum CL13 were reported to enhance the production of curcumin (Kumar et al., 2014). Endophytic bacteriamediated induction of secondary metabolites was also observed in kidney bean extracts after fermentation in the presence of Bacillus subtilis and Lactobacillus plantarum which also suggested the influence of bacterial endophytes in metabolite production (Bonilla et al., 2014). Introduction of endophytic Stenotrophomonas maltophilia (N5-18) into opium poppy (Papaver somniferum) has also been reported to have significant effect to enhance photosynthetic efficiency, alkaloid, and morphine contents in plants (Limona et al., 2015). Tiwari et al. (2013) have also studied the enhanced production of vindoline, ajmalicine, and serpentine in Catharanthus roseus explants on inoculation with endophytic Staphylococcus sciuri and Micrococcus sp. (b) Production of host-specific metabolites from bacterial endophytes

Many studies have demonstrated the role of endophytic microorganisms on the production of plant-specific bioactive molecules (Zhai et al., 2017). However, the production of host-specific metabolites by bacterial endophytes is least studied. Even though

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Microbial Endophytes: Prospects for Sustainable Agriculture

strong physiological activities are present in plants, insufficient level of production of desirable metabolite in plant can be manipulated by the introduction of beneficial bacteria. The added endophytic bacteria can produce primary and secondary metabolites to favor maximum production of high-quality bioactive metabolites (Zhai et al., 2017). Hence, the association of endophytic microorganisms with plants has been proved to have medicinal potential as compared to the plants alone. The enhanced production of the antimalarial compound artemisinin mediated by endophytic actinobacterium Pseudonocardia sp. strain YIM 63111 in its host plant Artemisia annua also indicated importance of endophytic bacteria in medicinal plants (Sato and Kumagai, 2013). (c) Metabolism of host plant-specific compounds by endophytic bacteria or vice versa

Endophytic bacterial inoculation in to the plants can modulates the synthesis of bioactive compounds which promote plant growth and disease resistance. The production hydrolases, and extracellular enzymes from endophytic bacteria can help the plants to establish systemic resistance against various pathogenic attacks. While phytohormones produced by endophytes play essential role in plant development and drought-resistance management. The high diversity of endophytes and their adaptation to various environmental stresses make them an untapped source of new secondary metabolites (Singh et al., 2017b).

2.8

Exploitation of bacterial endophytes for sustainable agriculture development

Intensive dependence on chemical inputs for the enhanced agricultural productivity has severely affected the ecological stability. Hence, it is necessary to identify alternative method, which enriches the agricultural productivity in a sustainable manner. The biosynthetic potential of endophytic microorganisms can be explored for the promotion of agricultural yield in a sustainable manner which is ecologically secure. Endophytic bacteria facilitate habitat adaptation of plants in agricultural field which accordingly enhance plant functioning, metabolism, and protect them from biotic and abiotic stresses. The application of bacterial endophytes in agricultural land can promote vegetative growth of crop plants, early flowering, seed setting, and seed germination which has been frequently observed with species from various plant families (Pahari et al., 2017). An elevated level of phytohormones synthesis by bacterial endophytes and its signaling network is expected to promote early root growth and development and finally increase crop yield. However, the endophyte-mediated plant growth promotion may possibly fluctuate with environmental and experimental conditions in which the plants are grown. Plant-microbe communication can stimulate the crop yield through a variety of mechanisms, which is mainly carried out by the plant-associated microorganisms (Fig. 2.3). The direct mechanisms include atmospheric nitrogen fixation, production of ACC deaminase leading to reduced stress, and solubilization of nutrients in soil thus making it available to host plants. Also, these bacterial endophytes can develop

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Fig. 2.3 Plant beneficial traits of endophytic bacteria and its applications.

Endophytic microorganisms from the medicinal plants and their potential applications

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Microbial Endophytes: Prospects for Sustainable Agriculture

biofilm on plant surfaces and can produce antimicrobial compounds which can protect plant tissues from the pathogen attachment and its harmful establishment within the plant tissues. The bacterial endophytes can also have the potential to degrade other plant or microbially derived compounds in the soil. As per the previous reports, bacterial endophytes can be applied in the agricultural fields as biocontrol agents, which can synthesize and release broad spectrum of bioactive molecules with antimicrobial activity. Such candidate bacterial endophytes can inhibit the infection by phytopathogens in the host tissues from soil or other external sources and induce defense mechanisms in host plants. Hence, the plant-associated microorganisms especially endophytes can be explored as both biofertilizers and biocontrol agents into the agriculture for the sustainable agricultural practices.

2.9

Visualization of endophytic bacterial colonization within the host plant

Once the endophytic bacterium has been applied to the plants, it can colonize in all parts of the plant and provide enhanced growth and productivity of the host plant. To study the interaction and ability of endophytic bacteria to colonize the internal tissues of the plant, cultivation-based and microscopy-based methods have been generally used (Kandel et al., 2017). Cultivation-based methods involve the colony counting of endophytic bacteria isolated from the surface-sterilized tissues of host plant. In the case of microscopy-based methods, different types of microscopy such as bright-field microscopy, florescence microscopy, confocal laser scanning microscopy (CLSM), and transmission electron microscopy (TEM) have been commonly used to capture the colonization patterns of bacterial endophytes. The combination of fluorescence in situ hybridization (FISH), autofluorescent protein (AFP), and β-glucuronidase (GUS) staining are the common microscopic methods used for the colonization studies. For this, fluorochromes or fluorescent dyes are used to label specific bacterial strains. In FISH analysis, universal oligonucleotide probes have been used to target a conserved region of bacterial 16S rRNA gene to facilitate the observation of individual bacterial cells or microcolonies in the plant endosphere. AFP techniques have been utilized to detect and enumerate microorganisms in situ on plant surfaces and in planta (Ryan et al., 2008). Green fluorescent protein (GFP) is a useful biomarker and it does not require any substrates to fluoresce the bacteria. Bacterial endophytes tagged with GFP constitutively express the fluorescent proteins in situ, which allows entire bacterial cells to fluoresce in the presence of ultraviolet light or blue light, and in the presence of oxygen (Ryan et al., 2008). Therefore, many studies have been focused to develop GFP cassettes for chromosomal integration and expression of gfp in a variety of bacteria. Bacterial cells with chromosomal integration of gfp can be identified by epifluorescence microscopy or CLSM (Kumar et al., 2014; Bonilla et al., 2014; Villacieros et al., 2003; Germaine et al., 2004). CLSM of hydroponically grown seedlings of Jaisurya rice, inoculated with gfp-tagged endophytes Pantoea sp. and Ochrobactrum sp. revealed their colonization ability in the intercellular spaces of root cortex (Verma et al., 2004).

Endophytic microorganisms from the medicinal plants and their potential applications

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Endophyte colonization has also been visualized with the use of the GUS reporter system. GUS staining was most intense on coleoptiles, lateral roots, and also at some of the junctions of the main and lateral roots ( James et al., 2002). This was well studied in a GUS-marked strain of Herbaspirillum seropedicae Z67 inoculated onto rice seedlings. The result of the study showed that the endophytic bacteria entered into the roots through cracks at the point of lateral root emergence. H. seropedicae subsequently colonized the root intercellular spaces, parenchyma, and cortical cells, with a few penetrating the stele to enter the vascular tissue. The xylem vessels in leaves and stems were also colonized ( James et al., 2002).

2.10

Delivery methods for introducing endophytic bacteria to agriculture

The widely used approaches to introduce bioinoculants in to the agriculture mainly include seed priming, soil drenching, and foliar spray methods. The application of endophytic bacteria through these delivery methods has also reported to have a great success in sugarcane and tomato plants for its enhanced growth and disease protection (Silva et al., 2012; Algam et al., 2005). However, method of application contributes to the survival and efficiency of the plant beneficial bacteria in the field. Most common methods developed and explored include seed treatment, soil amendment, and root dipping in the bacterial suspensions because of its easiness for application. Other methods such as foliar spray or application of bacteria through drip irrigation have also been studied (Podile and Kishore, 2006). Endophytic bacterial priming of Vigna unguiculata seeds with Serratia sp. ZoB14 was reported to have an enhanced growth in bacteria-treated plants compared to the control plants (Sabu et al., 2017). Similar studies on inoculation of endophytic Serratia marcescens AL2-16 on Achyranthes aspera L. and Ralstonia sp. on Vigna radiata seedlings showed significantly enhanced growth parameters in the treatment groups (Devi et al., 2016; Jimtha et al., 2014). Influence of inoculation technique has also been demonstrated with endophytic colonization of rice by Pantoea sp. isolated from sweet potato and Enterobacter sp. isolated from sugarcane and revealed that the colonization of more endophytic bacteria was observed with root-dip inoculation than with the rhizosphere application (Zakria et al., 2008). All of these reports further confirmed the efficiency of bacterial priming and application for enhanced growth and productivity.

2.11

Product designing and field application of endophytic bacteria-based agro-products

The application of endophytic bacterial cultures directly into the agricultural field may not produce expected outcome because of the varying field conditions and fluctuating soil characteristics that could affect the viability of endophytic bacteria. This can be overcome by the development of carrier-based formulation, which is a promising process to develop a potential laboratory bioinoculant to a commercial field product.

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Microbial Endophytes: Prospects for Sustainable Agriculture

Such carrier-based formulation should contain an active component in a suitable carrier with additives that can maintain the stabilization and could act as a protective shield for the living microbial cells during storage and also in the soil after application. It should have important properties like ease in preparation, enhancement in the performance of candidate organism in the field, cost effective, nontoxic to the environment, and convenient for field applications. A significant objective of these types of bioformulation is to provide more suitable microhabitat for survival and functioning in the soil ecosystem (Vendan and Thangaraju, 2007a). Development of endophytic bacteria-based formulations requires several techniques including isolation of a pure culture, screening of its plant growth promoting, and antiphytopathogenic properties by means of different analysis carried out by in vitro and in vivo experiments under greenhouse and field conditions. It is also necessary to optimize the mass multiplication protocols to enhance the quality and quantity of bioformulation, augmentation of bioactivity, and extend shelf life, which eventually determines the efficacy of the product in the agricultural field (Abd El-Fattah et al., 2013). Also, the selection of carrier and additives also determines the successful functioning of the candidate endophytic bacteria in the agricultural field (Tripathi et al., 2015). There are different types of formulations, depending on the carrier used and the method used to introduce candidate bacterial endophytes into the carrier material. These different forms of formulations with agriculturally important microorganisms offer promises for superior plant probiotic functions of bioinoculant. The liquid formulation can maintain high cell count, avoid contamination, provide extended shelf life and better protection against environmental stresses, and increase field efficacy (Gopalakrishnan et al., 2016). In liquid formulation, the microbial cells exist in a dormant spore form and these spores are germinated to active cells after the application in the field in the case of spore forming organisms. These factors enhance the shelf life of such formulation for more than 1 year (Vendan and Thangaraju, 2007b). The effect of solid and liquid bioformulations prepared from Kosakonia radicincitans on Z. mays L. revealed enhanced yield and productivity of the host plant. These bioformulations with a shelf life stability up to 6 months further confirm the efficiency of bacteriabased bioformulations for the superior field performance (Berger et al., 2018). Another important type of formulation is the powder formulation in which powdered carrier material is used. A good carrier material should be able to release specific number of viable cells for proper functioning in good physiological conditions, easily available, and cost effective to the farmers. Commonly used carrier materials are peat, talc, charcoal, cellulose powder, farm yard manure, vermicompost, lignite, bagasse, and press mud for the development of powdered formulations. Even though each formulation has its own advantages and limitations (Table 2.2), peat-based formulation is widely used in different parts of the world (Gopalakrishnan et al., 2016). Also, the talc-based powder formulations are popular in India and various previous studies have reported the advantages of talc-based formulation of different endophytic microorganisms to augment plant growth and disease resistance. Basheer et al. (2018) reported the plant probiotic efficacy of endophytic bacteria Bacillus sp. CaB5 isolated from C. annuum. This species was viable for more than 45 days in talc-based

Endophytic microorganisms from the medicinal plants and their potential applications

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Table 2.2 Commonly used application methods for bioinoculant and its advantages and disadvantages Application method Talc based bioformulation

Charcoal based formulation Peat based formulation

Vermiculitebased formulations Direct soil application Seed coating and covering Root dipping

Advantages

Disadvantages

Development of bioinoculant formulations for easy and controlled delivery of microorganisms to the host plants is highly significant Easy to handle, increase the activity of the organism in the field, cost-effective and convenient for field applications Easy to handle, increase the activity of the organism in the field, cost effective and convenient for field applications The moisture retention capacity of vermiculite could be the reason behind its better shelf life Easy to handle and no specific machinery is needed for application Easier to apply and less quantity is required Nursery required, simple and easy

Contamination of the carrier materials by unwanted microbes

Contamination and storage problems

Contamination of the inoculants by unwanted microbes, no uniformity on the career, shortterm storage ability Contamination by unwanted microbes Exposure to the sun cause desiccation problems and needs more volume Flexibility in seeding is less Large amount of liquid media and bacterial cells needed. Contamination from the environment

Modified from Mahmood, A., Kataoka, R., 2018. Potential of biopriming in enhancing crop productivity and stress tolerance. In: Advances in Seed Priming. Springer, Singapore, pp. 127–145.

formulation. The study reported that the formulation treatment enhanced seed germination and also growth in cowpea (V. unguiculata) and lady’s finger (Abelmoschus esculentus) plants. Several endophytic bacteria such as Stenotrophomonas maltophilia H8, Pseudomonas aeruginosa H40, and B. subtilis H18 have also reported to have potential field application through the talc-based bioformulations for the management of damping-off disease of cotton seedlings caused by Rhizoctonia solani (Selim et al., 2017). Encapsulation of microbial cells is another important technique to develop new formulations which has several advantages than free cell formulations ( John et al., 2011). This provides (i) tolerance against biotic stresses and abiotic stresses, (ii) increased viability and better physiological activity, (iii) controlled release of nutrients, (iv) enhanced cell densities, and (v) superior cell growth in various internal aerobic

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Microbial Endophytes: Prospects for Sustainable Agriculture

and anaerobic zones of encapsulating gel. These methods can provide enhanced efficacy of endophytes in bioformulations for the application in agricultural field.

2.12

Industrial sustainability and marketing of agro-products

For the successful application of bioinoculant or delivery of products into the market, it should have the following features (i) it must deliver the microbial inoculants in a physiologically active state, (ii) should provide functioning of microbial inoculum at all environmental conditions, (iii) enhanced shelf life and viability of products lasting for a long period of time, and (iv) finally it should have the consistency in field performance and reduced toxicity in the environment (Castro-Sowinski, 2016). During the process of marketing, registration of microbial products requires risk assessment to human health and to the environment and is highly challenging. Previous studies on some Pseudomonas sp. revealed, the ecological impact of these microbes to be less due to the decrease in population after inoculated into the field. Hence, the readily colonizing property of plant beneficial microorganisms could be supportive to environmental safety.

2.13

Conclusion

Health issues and environmental toxicity caused by agrochemicals demand new alternative to conventional agricultural practices. Endophytic microorganisms associated with medicinal plants with both plant growth and disease-resistance properties are considered to have added benefit to the agriculture as it confer protection to host. Hence, in-depth knowledge on plant microbiome association and its potential application as discussed in the chapter can help to generate innovative methods for sustainable agricultural practices.

Acknowledgments Authors acknowledge our heartfelt thanks to KSCSTE-KBC-YIPB Project and KSCSTE-SRS Scheme for funding and support to encourage the field of research.

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Further reading Mahmood, A., Kataoka, R., 2018. Potential of biopriming in enhancing crop productivity and stress tolerance. In: Advances in Seed Priming. Springer, Singapore, pp. 127–145.