1. INTRODUCTION

In the field of microbiology and plant biology, recent studies have a strong emphasis on plant-microbial interactions. Plant growth development depends highly on the extracellular enzymes produced by plant growth-promoting bacteria (PGPB). Microorganisms constantly interact and turn on the other organisms within their community [1]. Plants and their closely related species are influenced by the presence of unicellular or multicellular organisms. Interactions between microorganisms and plants occur both internally (via the formation of plant microbial endospheres) and externally (surface of roots) [2]. Plants and microbes always maintain mutually beneficial symbiotic relationships with endophytes by providing some benefit to their living community [3,4]. Through the symbiotic relationship between plants and microorganisms, endophytes may act as a convenient substitute to replace the use of pesticides [5,6]. The excessive application of agrochemicals and insect control in modern agriculture based on organic principles is difficult to maintain and results in crop loss. Additionally, the current scenario has led to increased pathogens with pesticide or drug resistance and soil infertility [7].

Microorganisms that are endophytic, such as bacteria, fungi, and actinomycetes, inhabit the surface layer of plant tissues through symbiotic relationships. Actinomycetes are one of the prominent bacterial species, including the largest genera, Streptomyces. The production of secondary metabolites, including bioactive substances and antibiotics, is a standout characteristic of Streptomyces and guanine and cytosine content was high in the genome [8]. Hundreds of distinctive plant growth regulators, antibiotics, and bioactive components have been discovered in terrestrial microorganisms, particularly from the genus Streptomyces. The relationship between endophytes and plants is dominantly reported as commensalism. Various applications have been reported in the plant growth components extracted from the Streptomyces sp. [9,5]. The earlier studies revealed that endophytic Streptomyces notably increase the growth and tolerance in varieties of monocot and dicot plant species [10,11]. The upsides of the Streptomyces endophytes for biocontrol and promoting plant growth are illustrated in this review. Recent studies of Streptomyces endophytes on various crops for their biological pesticide, natural fertilizing ability, and plant growth stimulating factor were also discussed.

2. BIODIVERSITY OF ENDOPHYTIC Streptomyces

The composition of the cell envelope in Streptomyces was used to differ from other Gram-negative bacteria, and cell composition was used as the identification characteristic [12]. Plants extensively interact with the different ranges of microorganisms and acquire benefits through minerals and nutrition exchange [13,7]. The endophytes colonized the plant’s roots and mainly contributed to nitrogen fixation and solubilization of mineral nutrients. The studies on the root-associated microbes, especially rhizobacteria, influence the morphology and physiology of the plants to prevent the pathogenic insect attack. Plant defense mechanisms will initiate and express salicylic acid, ethylene, and jasmonic acid. A plant’s root releases metabolic signals such as alkaloids, flavonoids, terpenoids, and strigolactones that attract the microbial communities around the rhizosphere (Fig. 1). Endophytic Streptomyces influence the richness of soil with nutrients and significant growth with many components. In addition to the endophytes’ phosphate solubilization ability, which produces the various enzymes that break the complex nutrients into simple minerals such as cellulase, chitinase, β-fructofuranosidase (invertase), lipase, keratinase, pectinase, protease, peroxidase, phytase, and xylanase. Antimicrobial peptides and biocontrol components are identified through the metabolic studies on endophytes Streptomyces. Microbial interactions revealed the unique features of endophytes beneficial for biocontrol and biofertilization in potatoes [14,15].

Figure 1. Interaction and tolerance of PGPMs to plant. [Click here to view]

3. METHODS FOR ISOLATING ENDOPHYTIC Streptomyces

Isolation of endophytic Streptomyces is carried out in different plant parts, such as a different scale of primordium of meristem, leaf, and roots. The sequencing approach was made to screen the diversity of endophytes in the seed and needles of Pinus monticola. Isolation of endophytes is still challenging, and broad reviews were established to isolate Streptomyces. Endophytes are isolated from the plant tissue extract or ground tissues by inoculating in the Streptomyces-specific media. Different culture mediums were employed to isolate endophytic fungi from the roots and fruits of Azadirachta indica [48]. The study confirmed that the mycological agar medium yielded many isolates with species richness. Streptomyces peucetius were isolated using surface-sterilization methods and identified by morphological characteristics.

Earlier, biochemical and morphological characteristics were used to identify endophytes belonging to Actinomycetes. Molecular identification by ribosomal DNA (rDNA) sequence analysis is currently used to identify microorganisms. It reduced the biased judgments, and rDNA sequence data are robust in resolving endophytes’ taxonomy (Table 1).

Table 1. Potential soil and plant root, tissue surface of the Streptomyces species. [Click here to view]

4. MOLECULAR APPROACHES FOR CHARACTERIZATION

The identification and characterization of endophytes through metagenomic studies, molecular markers, molecular cloning, and gene expression studies, are the current trends and advanced developments in molecular-level studies. The metagenomic approach is one way to find microorganisms from various environments that are difficult to isolate. A metagenomic system was used to characterize the uncultured endophytic microorganisms colonizing Solanum tuberosum L. contained the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon. It was concluded that metagenomic analysis could supplement polymerase chain reaction-based research and provide information on whole functional genes [49]. Denaturing gradient gel electrophoresis profiles of 16s rRNA gene fragments amplified from complete plants’ DNA were used to detect non- culturable endophytic bacteria by comparing the profile with the bands obtained from the culturable endophytes from citrus plants [50]. The bacterial endophytes community of potato plants was investigated using automated ribosomal intergenic spacer analysis and pyrosequencing [12]. After being spooled and transferred to a screw-capped vial, the DNA was washed with 70% cold ethanol, allowed to air dry, and then suspended in TE buffer.

5. PLANT- Streptomyces INTERACTION

In plant and microbe interaction, specific sRNA responded to the up and down-regulation of the biotic and abiotic stresses and pathogens [51,52]. To analyze and tackle the ecosystem challenges in agriculture, it is obligatory to understand the gene regulation of sRNAs in plant response in endo-microbiome and biocontrol beneficial bacteria. Small regulatory RNAs are highly responsive to cellular functioning, such as oxidative stress response, quorum sensing, carbon starvation, and iron deficiency [53]. sRNA showed gene expression in transcriptional and post-transcriptional stages, and synthetic and functional processes were described [54]. The precise and targeted gene regulation makes plant sRNA distinctive and capable gene modulators. A better acknowledgment of sRNA can be exploited for its myriads of applications, from basic gene function study to targeted genes [55].

sRNA synthesis starts from the transcription of MIR genes by RNA polymerase II. It proceeds through the formation of precursor micro RNA duplexes before single-stranded miRNAs are inserted into the RNA-induced silencing complex (RISC). Following the RISC formation, argonaute (AGO) proteins guide the miRNAs strand to its target mRNA, and another strand of the duplex undergoes degradation [56]. Targeted identification of many miRNA-mRNA duplex modules in plant-microbe interactions, but very few studies have been functionally validated for the importance of agriculture and horticulture [57]. A few studies on microRNAs have been increased, including genome-wide profiling of sRNA and miRNA responses to drought, salt, cold, heat, systematic stress, and pathogenic microflora [51,52,58]. The specific impacted of miRNAs can play distinct roles across species or different crops. However, the advances in miRNAs mediated the regulation of genes related to plant-microbes’ interactions, emphasizing the role of plant miRNAs in disease susceptible and resistance, which can be exploited for improved crop varieties.

6. Streptomyces AS PLANT GROWTH PROMOTERS

In general, actinobacteria may be beneficial to plant nutrition in terms of minerals. This is related to the ability to mobilize metals and fix nitrogen, as well as the uptake of mineral nutrients such as Fe, Zn, and Se. However, metagenomic investigations have not demonstrated the involvement of Streptomycetes in such advantageous procedures [59]. The taxonomic and phylogenetic makeup of these microbial communities is restricted to a few bacterial phyla, including actinobacteria, according to metagenomic studies of the bacterial microbiota in plants.

Emphasizing the role of Streptomycetes in the growth and health of plants. Through nutritional interactions and the composition of its root exudate (chemotaxis), the plant has a significant influence in influencing the growth of its root microbiome [60–62]. Flavonoids, strigolactones, and terpenoids are among the metabolic signals found in plant root exudates that have the power to influence the microbial communities in the rhizosphere. It is still unknown what cues draw Streptomycetes into the rhizosphere. Streptomycetes are able to penetrate roots and colonize root tissues and arteries. From there, they can be separated and purified in order to characterize their physiology and the interactions among microbes [37]. Actinobacteria, like Streptomyces species, act as nutrient enhancers and affect soil fertility by interacting with various minerals. They are known to produce a variety of enzymes, such as amylase, chitinase, cellulase, invertase, lipase, keratinase, peroxidase, pectinase, protease, phytase, and xylanase, which convert complicated nutrients into simpler mineral forms, in addition to siderophores and solubilizing phosphate. Their ability to cycle nutrients makes them excellent choices for natural fertilizers [63].

7. INDUCED SYSTEMIC RESISTANCE IN PLANTS

Biologic stress can have a detrimental effect on a plant’s growth, cellular development, inherent biological systems, and productivity. To counter these biotic stress conditions, endophytic microbes are essential to the plant environment. Furthermore, endophytic actinomycetes are naturally occurring symbionts of a number of plants that modify their defense mechanisms and systemic resistance in order to impart resistance to host plants in challenging environments [96]. Unlike synthetic drugs, these microorganisms can successfully manage many plant diseases by inducing systemic resistance (ISR) without posing any environmental harm. The ISR in host plants is triggered by endophytic colonization and operates through a variety of mechanisms to reduce further pathogen attack and disease progression [97]. The endophytic bacteria produce secondary metabolites that shield plants from phytopathogens, in addition to exo-enzyme secretion, which could be aiding plant colonization. Endophytes may accelerate the growth of the plant by phytohormone production and support plant growth under unfavorable biotic and abiotic stress [98].

In an investigation, [99] reported that endophytic Streptomyces sp. triggered systemic resistance in chickpeas under Sclerotium rolfsii stress. Another investigation, [100] revealed that Streptomyces strains promote plant growth and induce resistance against Fusarium verticillioides in maize plants. Chen et al. [101] reported that Streptomyces chromofuscus induces systemic resistance and activates plant defense responses against tomato yellow leaf curl virus infection. Streptomyces chromofuscus maintained relative chlorophyll contents by accelerating the expression of genes (CLH1, HEMA1, and PORA) associated with chlorophyll biogenesis.

8. BIOTECHNOLOGICAL APPLICATIONS IN AGRICULTURE

8.2. Biocontrol Agents

Numerous bioactive compounds that are advantageous to soil and plants are produced by actinobacteria and they have the ability to serve as biocontrol agents [116]. Increasing the resistance of plants to biotic and abiotic stressors [117]. According to a study, several actinobacteria (Actinomyces pactum, A.globisporus, and A. globisporus subsp. globisporus) have the ability to break down fungal pathogens. A light-colored actinomycete called Streptomyces griseoviridis was isolated from Sphagnum peat and is an example of a biocontrol agent that lessens damage from different soil and seed infections [118,119]. According to a study, actinobacteria in soil produce antibiotics that are useful against plant diseases (Fig. 2). To combat plant diseases, Streptomyces violaceusniger, generates antibiotics including headache, gentamycin, and guanidylfingine. Actinobacteria have been shown in earlier research to improve plant development and efficiently treat plant ailments [117,119–121]. The main reason Streptomyces strains are known for their ability to function as biocontrol agents they may produce strong volatile chemicals, metabolites, and antibiotics that have antipathogenic qualities [122].

Figure 2. Effects of biopesticides/biocontrol agents. [Click here to view]

A different investigation was conducted using chemicals released by strains of Streptomyces coelicolor, S. violaceusniger, and S. violaceusniger, including siderophore, chitinase, the antibiotic geldanamycin, and the antifungal nigericin. There were two strains of Streptomyces that showed biocontrol potential in this investigation by producing secondary active metabolites that inhibited the growth of harmful bacteria. The dangerous bacterial threat known as glumae, which causes panicle blight in rice plants and jeopardizes rice yields, was effectively controlled [123]. In a report, [124] demonstrated the induction of systemic resistance in Solanum lycopersicum and Capsicum annum seedlings against fusarium wilt by Streptomyces bioformulations. In another report, [125] revealed the formulation of bio-fungicides based on Streptomyces caeruleatus spores and efficacy against Rhizoctonia solani damping-off of tomato seedlings. In an investigation, [126] demonstrated the plant-growth promotion and biocontrol properties of three Streptomyces sp. to control bacterial rice pathogens. In a report, [127] revealed the insecticidal potential of endophytic Streptomyces sp. against Zeugodacus cucurbitae. In a similar report, [124] revealed that Streptomyces sp. bioformulations effectively controlled fusarium wilt in Solanum lycopersicum and Capsicum annum seedlings.

8.3. Breakdown of Pesticides

Since native Streptomycetes are well adapted to live in soil and sediment habitats, using them for bioremediation in pesticide-contaminated environments shows to be a potential approach. The potential metabolic variety, mycelial growth habitat, fast growth rates, semi-selective substrate colonization, and genetic manipulation of Streptomyces strains are their main advantages. Streptomyces may develop into spores, which aid in their persistence and dissemination, they can last lengthy periods of time in soil with low nutrient concentrations and water availability [128]. These benefits have led to the investigation of several Streptomyces strains as viable candidates for bioremediation of contaminated settings using several chemical pesticide families, such as ureas, organochlorines, organophosphates, pyrethroids, and chloroacetanilides [128–130]. Microorganisms called Streptomyces have proven to be highly effective in removing or converting several pollutants at once. It was discovered that lindane and Cr(VI) could be effectively removed from soil polluted with both chemicals by both pure and mixed cultures of Streptomyces strains. In order to lower pesticide concentrations in various environmental matrices and stop their infiltration into the environment, thus lowering human exposure, Streptomyces degradation of pesticides has been thoroughly investigated in biotechnological process development [131] (Table 2).

Table 2. Bioformulations from endophytic Streptomyces and their potential effects. [Click here to view]

9. BOOSTING THE COMPOSTING PROCESS

In order to speed up the rate at which trash breaks down and raise the quality of compost at the end, microbial inoculation techniques introduce capable microorganisms to the compost mixture. These microorganisms can be grown in culture mixtures including soil, manure, and straw, or they can be separated from microbial communities under certain selection pressures [145]. A single strain of effective microorganisms or a combination of them can be used as the inoculums [146] and seasoned compost samples [147]. Researchers are currently investigating the use of mixed inoculants, which is a collection of microorganisms that cooperate with one another [148–150]. Microbial inoculants increase mesophilic and thermophilic bacterial populations, which enhances temperature profile and ammonia emissions. Additionally, it speeds up the process of composting by increasing enzymatic activity and reducing the first lag time of biological processes. When generating compost with a higher nutritional value, microbial inoculation procedures can effectively reduce the discharge of odorous emissions, particularly volatile organic compounds [151,152]. Single or multi-stage applications of microbial inoculums can be made at different points in the composting process. The various stages of inoculum addition show a significant impact on the physicochemical parameters of the composting process [153].

10. FUTURE PROSPECTS

In current agriculture practices, biocontrol agents and biofertilizers mostly contain plant growth-promoting microbes (PGPMs) as the sole ingredient. Plant growth promoting rhizobacteria colonized around the rhizosphere of plants induces a positive impact on the host, such as increased plant growth and improved defense against disease-causing pathogens (Fig. 2). The predominant bacterial genera in microbial-based biofertilizers and biocontrol agents are Arthrobacter, Alcaligenes, Azospirillum, Azotobacter, Bacillus, Burkholderia, Enterobacter, Klebsiella, Pseudomonas, Rhizobium, Serratia, and Streptomyces [165]. Microbial-controlling agents are the ultimate replacement for harmful pesticides. These sliving entities, such as microorganisms, provide eco-friendly nonchemical methods for maintaining free of the plant disease [166,167].

The biocontrol of endophytes results in cell wall lyses, iron depletion in the rhizosphere, and increased microbe resistance with the rhizosphere. Endophytes antibiotic-producing mechanism increased the host defense to control microbial diseases, with the potential of antimicrobial enzymes (β1,3-glucanases, chitinases, proteases, and lipases). The biosynthesis of siderophores with low molecular weight helps to chelate the iron content in rhizospheric soil, which blocks the invasion of pathogenic organisms [167,168]. Microbial inoculants increased agricultural promised sustainability, decreased crop loss by diseases, and enhanced the uptake of nutrients. Organic biocontrol microbes built the tolerance for the plants to grow under any conditions. These biopesticides formulation are cost-effective and harmless to the ecosystem when applied to crops [169–171]. The biopesticides improve the performance and yield of the crop. Localizing the bacterial inoculum in the soil will change the temperature and humidity. Soil microbiome interactions with plants improved the yield and productivity of the crop (Table 1).

11. CONCLUSIONS

This review focused on endophytic Streptomyces, the significant contribution ability of these microorganisms to promote plant growth, and their bioactive compounds beneficial to pharmaceuticals, environmental, agricultural, and industrial sectors. The use of eco-friendly microorganisms that reduce pest populations and enhance plant growth forms the foundation of this promise. A potential answer for a more sustainable agricultural future is using consortiums that are developed from two or more compatible strains, biopesticides, or biofertilizers in exemplary formulations. The studies mentioned in this review lend credence to the idea that developing new formulations with cooperative microbes may help improve plant protection and growth in various crops. These studies also emphasize the need for more research on this topic, with an emphasis on endophytic Streptomyces, which have only recently been used as inoculants to improve pristine ecosystems in agricultural soil, agricultural output, and food security.

12. ACKNOWLEDGMENTS

The authors are grateful to the Department of Genetics, Plant Breeding and Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib and Eternal University Funded Project “To establish culture collection of bacteria/fungi/algae/cyanobacteria from hilly areas” Reference number: EU/VCO/72/36 for providing the facilities support, to undertake the investigation.

13. CONFLICT OF INTEREST

The authors report no financial or any other conflicts of interest in this work.

14. CONSENT FOR PUBLICATION

All authors agreed and given their consent for publication.

15. AUTHOR’S CONTRIBUTIONS

All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work. All the authors are eligible to be an author as per the international committee of medical journal editors (ICMJE) requirements/guidelines.

16. ETHICAL APPROVALS

This study does not involve experiments on animals or human subjects.

17. DATA AVAILABILITY

All the data is available with the authors and shall be provided upon request.

18. PUBLISHER’S NOTE

All claims expressed in this article are solely those of the authors and do not necessarily represent those of the publisher, the editors and the reviewers. This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.

19. USE OF ARTIFICIAL INTELLIGENCE (AI)-ASSISTED TECHNOLOGY

The authors declares that they have not used artificial intelligence (AI)-tools for writing and editing of the manuscript, and no images were manipulated using AI.

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