Microbial antagonists: diversity, formulation and applications for management of pest–pathogens
Egyptian Journal of Biological Pest Control volume 33, Article number: 105 (2023)
Agriculture is the backbone of developing countries, which plays an essential role in primary drivers of economy. The increasing use of chemical fertilizers and toxic insecticides endangers the health of human, plant soils, and the environment. Microbial insecticides have been implemented in current scenario for crop protection. Biological agents for pest control have gained more attention in recent year as substitutes for management of pests and pathogens. It provides a sustainable approach to plant health management and assists to minimize the excessive applications of toxic substances. The antagonistic microbes belong to six different phyla including Bacillota, Actinomycetota, Pseudomonadota, Bacteroidota and Mucoromycota. Microbial pesticides have been developed through a number of processes, including extraction of pure culture and screening using effectiveness bioassays under controlled and natural conditions. Biological control agents (BCAs) are recognized to be the most sophisticated technology for environmentally friendly agriculture. The various beneficial BCAs have been reported for the management of plant health, but they required effective acceptance together with the standardization of bioformulation. The present review deals with the recent development of microbial control agents, mechanisms of actions, development of microbial pesticides and their potential applications for agricultural productivity.
The diversity of microbiome is one of the abundant sources exploited for generate a wide range of goods and process with multiple applications in the industrial, medicinal, and agricultural sectors (Yadav et al. 2017). Among all, agriculture is a crucial sector in India, and effective disease management strategies are in high demand. In the agriculture, microbiomes are mostly used as a biocontrol agent to combat pest insects. Although microbial biocontrol of pests have been documented in the middle of the 1990. These chemical pesticides obscure their effects and potential (Gurung et al. 2019). After the “silent spring” researcher erudite that chemicals intensive insect management is detrimental to environment and cannot ensure security of safe food for a growing human population (Gay 2012). Therefore, preventive pest management practices based on different economic, ecological, and human concerns have replaced therapeutic pesticidal control in modern sustainable agriculture techniques (Singh et al. 2020).
Insect pests with high population level are detrimental and destroy agricultural crops and economy as well as decrease the food security for growing human populations (Sharma et al. 2020). To achieve more sustainable agricultural practices, there is a strong push to find substitutes for chemicals in controlling diseases and pests, which have caused significant losses in food production. Now researchers are focusing on potential biological control microbiomes as viable substitutes for managing pests, due to the adverse effect of chemical fertilizers on environment and human health (Ab Rahman et al. 2018). Biotic agents such as harmful insects, pathogens, and parasitic weeds are some of the most important plant pests, which cause serious damages and losses to agricultural products. To ensure quantitative and qualitative food, feed, and fiber production, it is essential to control these plant pests (Heydari and Pessarakli 2010). Bacterial and fungal pathogens can cause plant diseases, leading to losses in agriculture productivity and poor quality of agricultural products. This can result in economic hardships for growers, reduced food supplies, and ultimately high prices (Monte 2001).
The most widely used approach for long-lasting benefits is integrated disease management, while chemicals and numerous biological methods are also employed. Microbiomes often enter plants through naturally occurring wounds, which can occur accidentally due to pests or even human intervention (Lindsey et al. 2020). Understanding the applications of microbiomes for promoting the growth and controlling diseases is crucial. Biofertilizers and biopesticides have been developed as alternative to chemical fertilizers and pesticides, but their success in the field is still inequitable (Ab Rahman et al. 2018). Biological control is managing the plant diseases, which involves the use of beneficial microbiome, including archaea, bacteria and fungi. These microorganisms are specifically selected to attack and control plant pathogens, offering an eco-friendly approach for management of pest and pathogens. By incorporating biological control into physical and cultural controls, limiting chemical usage, it is possible to create an effective integrated pest management (IPM) system (Monte 2001). In recent times, online resources related to medicinal plants, antimicrobial peptides (AMPs), natural products (NPs), and essential oils (EOs) have significantly aided the development of cost-effective and efficient control agents for pests and pathogenic microbes (Jin et al. 2021). The various fungi, bacteria, and viruses are the primary plant pathogens, and the severity of their diseases depends on environmental factors, including temperature, humidity, altitude, and the niches of the pathogens. The present review deals the antagonistic microbes as a biocontrol agent, mechanisms of actions, diversity and their biotechnological applications for agricultural productivity.
Biodiversity of antagonistic microbes
Antagonistic microbe’s importance in the sustainable management practices results in the massive amount of biodiversity study. Due to various ecological services, these microbes have been reported in diverse habitats. These microbes are found in soil, and they are also associated with diverse varieties of plants, nematodes and insects. Various microbes such as fungi and bacteria have been found as an antagonist and they are found to belong to different phylum and genera (Table 1). On a review of diverse finding, antagonistic microbes belong to six different phyla including Bacillota, Actinomycetota, Pseudomonadota, Bacteroidota and Mucoromycota (Fig. 1), in which Pseudomonadota was most dominant phylum followed by Bacillota, whereas Actinomycetota, Bacteroidota and Mucoromycota were least dominant. According to the report, Trichoderma harzianum was sorted out from rhizospheric region of sugarcane. The soil bacterium was found to inhibit the growth of Colletotrichum falcatum (Viswanathan et al. 2003). In a report, Bacillus lentimorbus associated with the weed rhizospheric region was found as an antagonist of Fusarium oxysporum (Kang et al. 2005). In another report, F. oxysporum antagonist Pseudomonas aeruginosa was sorted out from rhizospheric region of banana (Ayyadurai et al. 2006). The soil bacterium, Pseudomonas putida was found to inhibit the growth of Alternaria alternata (Pandey et al. 2006). In a report, Kitasatospora from Fagus sylvatica was found to inhibit the growth of Phytophthora citricola (Haesler et al. 2008). Streptosporangium sp. from Azadirachta indica was reported as Phytophthora sp. growth inhibitor (Verma et al. 2009). In another report, endophytic bacteria, i.e., Acinetobacter rhizosphaere, Pseudomonas reactans, and Rahnella aquatilis in association with wild olive were reported for inhibiting the growth of Verticillium dahlia (Aranda et al. 2011). Similarly, in a report, Fusarium oxysporum from rhizosphere of coffee was found to inhibit the growth of root not pathogen Meloidogyne incognita (Freire et al. 2012). Ma et al. (2013) reported Bacillus sp. isolated from the rhizospheric region of soil was found to inhibit the growth of Rhizoctonia solani.
In a report, Brevibacillus brevis and Streptomyces rochei from rhizosphere of tobacco was found as a biocontrol agent against Ralstonia solanacearum (Liu et al. 2013). An endophytic fungus Trichoderma gamsii from lentil was reported for inhibiting the Pythium afertile growth (Rinu et al. 2014). In another report, Trichoderma harzianum was reported for inhibited the growth of pea pathogen, i.e., Rhizoctonia solani (Akhter et al. 2015). An epiphytic bacterium Bacillus toyonensis from tomato was found to inhibit the blight causing pathogen Alternaria alternata (Pane and Zaccardelli 2015). Ochrobactrum intermedium from tomato rhizosphere was reported as an antagonist of Fusarium oxysporum (Gowtham et al. 2016). In another report, various yeast, i.e., Aureobasidium pullulans, Cyberlindnera sargentensis, and Candida subhashii were isolated from soil and this bacterium inhibiting the growth of Rhizoctonia solani (Hilber-Bodmer et al. 2017). Jeotgalicoccus aerolatus, Moraxella osloensis, Sulftobacter dubius and Staphylococcus epidermidis from Halodule uninervis were reported as antagonists of Pyricularia oryzae, Phytophthora capsici and Pythium ultimum (Bibi et al. 2018). Paenibacillus jamilae from cucumber was reported for inhibiting the growth soilborne pathogen Bipolaris sorokiniana (Wang et al. 2019). In an investigation, Bacillus velezensis from maize was reported inhibiting the pathogenic fungi including Fusarium verticillioides, Penicillium oxalicum, and Talaromyces funiculosus (Yang et al. 2020). Bacillus paralicheniformis and Trichoderma asperellum from rice rhizosphere were reported as growth inhibitors of Xanthomonas oryzae (Kannan et al. 2021). In another report, Lysinabacillus fusiformis and Paenibacillus alvei from Nasutitermes were found to inhibit the growth of Phytophthora capsici (Fitriana et al. 2022). Serratia marcescens from cabbage was reported for inhibiting the growth of pathogen Pythium aphanidermatum (Al-Daghari et al. 2023).
Interkingdom signaling and interconnections of the plant microbiome
It is thought that the numerous signaling molecules used by prokaryotes and eukaryotes to communicate with one another influence both partners' gene expression. The process of interkingdom signaling involves the creation and release of small chemicals by the contacted species, which establishes communication pathways between two kingdoms. The pathogenic or beneficial mirobiomes frequently communicate with their host plants across kingdoms, with variable results depending on the precise chemical-triggered signaling pathways. Major present hurdles in this area include figuring out how it works and decoding the indications or language of this communication between kingdoms. A variety of signaling molecules can be generated by or obtained from bacteria and plants in the processes of the signaling pathways. Instead of eradicating the hazardous bacteria directly, the investigation of such experiments will encourage the creation of methods to enhance plant disease resistance through managing interkingdom communication.
Plant reactions and bacterial QS signals
Bacterial communication known as quorum sensing (QS) organizes bacterial behavior in a population density-dependent way by creating and detecting signal molecules. First discovered in Vibrio fischeri cells, population density dependent phenomena activate light generation when the cell population surpassed a threshold density. N-acyl homoserine lactone (AHL), sometimes known as the first QS signal or autoinducer was discovered in Photobacterium fischeri luciferase (Eberhard et al. 1981). The discovery of QS made it possible to see that, like multicellular creatures, individual microbial cells can coordinate their behavior to better adapt to complicated nutrition or environmental niches. The most extensively researched QS signals to date are AHLs, which are often employed signals by different group of bacteria (Kan et al. 2017). The LuxR and LuxI proteins serve as AHL synthase and signal receptor, respectively, in a typical AHL-QS system (Fuqua et al. 1994).
Cross-kingdom signaling plays a variety of roles in interactions between plants and bacteria and considerably expands the functional spectrum of QS signals. Bacterial AHLs influenced plant growth, immunity, and development (Shrestha et al. 2020). A homoserine lactone (HSL), 3-oxo-C14-HSL from bacterium Sinorhizobium meliloti, via an ethylene-dependent mechanism was shown to significantly increase the nodule counts in Medicago truncatula (Veliz-Vallejos et al. 2014). In barley, glutathione S-transferase and dehydroascorbate reductase were affected by 3-HSLs (C6-, C8-, and C10-HSLs), but these enzymes were unaffected in yam beans, with the exception that C10-HSL treatment resulted in a decrease the amount of content of chlorophyll (Götz-Rösch et al. 2015). The short-chain C4- and C6-HSLs that accumulated in biological films can induce the release of carpospores from the different group of algae (Singh et al. 2015). In Arabidopsis, AHLs containing acyl chains, between 4 and 14C in length, have been reported to influences the growth of the roots. N-decanoyl-HSL (C10-HSL) was the most active AHL in changing the structural makeup of the root system. Although the other evaluated AHLs affected the expression- of genes that control the division and differentiation of cells without requiring auxin signaling (Ortíz‐Castro et al. 2008). C4-HSL treatment caused a brief and quick rise in cytosolic Ca2+ levels, while C6-HSL treatment caused a rise in calmodulin levels (Zhao et al. 2015). The 3-oxo-C6-HSL enhanced cell division in the meristematic zone and cell elongation in the elongation zone in Arabidopsis by activating the transcription factor AtMYB44 and mediating primary root growth through the regulation of cytokinin- and auxin-related genes (Zhao et al. 2016).
As a result of local induction by microorganisms, plants can develop strengthened defense mechanism against an assortment of pathogens known as induced systemic resistance (Pieterse et al. 2014). In addition, number AHLs bacterial factors are also involved in triggering ISR (Kan et al. 2017). Using rhizobacteria that produce AHL to prime plants for systemic resistance is one method of biocontrol. ISR became activated in AHL-producing plants and protected against infections when S. marcescens AHL-producing and degrading genes were introduced in tobacco (Nicotiana tabacum) plants, whereas due to a lack of ISR, the AHL-degrading plant was unable to provide a defense mechanism against pathogen invasion (Ryu et al. 2013). According to study, treatment with oxo-C14-HSL also caused physiological changes in plant, such as oxylipin levels, phenolic compound accumulation, cellulose deposition, cell wall lignification, and SA-induced stomatal closure in response to P. syringae infection (Schenk et al. 2014). S. meliloti generated oxo-C14-HSL, was used to inoculate host plants, and these plants displayed improved resistance to fungi (Hernández‐Reyes et al. 2014). The bryophyte moss Physcomitrella patens, an example of the first plants to grow on land, exhibits altered spore germination in response to AHLs, showing that number of bacteria change spore germination in the environment via the generation of AHL signal molecules (Vesty et al. 2020). Therefore, one potential crop protection method would be to use bacteria that produce AHL to enhance plant resistance and reduce production losses.
Another distinctive QS signal is the diffusible signal factor (DSF), which has been recognized as cis-11-methyl-2-dodecenoic acid. First discovered in the phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc), this new unsaturated fatty acid has been linked to bacterial virulence, toxin tolerance and biological film formation (He et al. 2006). Glucose is the substrate which supplies carbon and carbon drives the production of the DSF-family signals in Xcc (Deng et al. 2015). However, structurally comparable compounds have been discovered in two unrelated bacteria, Burkholderia cenocepacia and P. aeruginosa, indicating that DSF synthesis is not just limited to Xanthomonads (Deng et al. 2010). More than one type of DSF-family signal can be produced by a single bacterial strain, and many bacteria can each produce a single type of signal (He et al. 2010). In interspecies and interkingdom signaling, DSF-family signals have a role (Ryan et al. 2015). P. aeruginosa's production of cis-2-decenoic acid caused C. albicans and other microorganisms to disperse from biofilms that they had formed together (Jennings et al. 2012). It has also been demonstrated that the DSF-family signals influence plant immunity. However, it was found that in certain plants, the opposite effect that elicits innate immunity (Kakkar et al. 2015).
Many Proteobacteria include unpaired QS LuxRs (called LuxR solos or orphans) that lack matching LuxI homologs (Kan et al. 2017). The LuxR solos’ modular design is identical to that of a standard LuxR protein, featuring a DNA-binding helix-turn-helix (HTH) domain at the C-terminus and an AHL-binding domain at the N-terminus. LuxR soloists, however, substitute a few preserved residues within the AHL-binding domain (González and Venturi 2013). The regulating repertory of the usual LuxI/LuxR QS systems is widened by these LuxR solos. Using “eavesdropping” on signals generated by nearby bacteria or eukaryotic signals created via interkingdom signaling, they react to endogenous or exogenous AHLs (Kan et al. 2017). In contrast to AHLs, a subfamily of LuxR solos in plant-associated bacteria (Palazzini et al.) act to low molecular weight compounds generated by plants. These bacteria are important in biocontrol, symbiosis and virulence in plants (Patel et al. 2013). Interkingdom signaling that is mediated by LuxR alone has received a lot of interest, particularly with regard to understanding the communications' chemical code.
In plant-associated Proteobacteria, like Pseudomonas, Dickeya, and Xanthomonas from the α-proteobacteria group and Rhizobium, Agrobacterium, Sinorhizobium, Citreicella, and Rhodospirillum from the γ-proteobacteria group, LuxR solos were common (González and Venturi 2013). Quorum quenching, an interference with QS signaling, hinders the QS-controlled mechanisms that are frequently essential for fruitful bacterial-host interactions. There are numerous methods for quenching QS. For instance, to stop the expression of bacterial target genes, plants synthesize and secrete a variety of natural chemicals that imitate QS signal. Therefore, symbiosis and pathogenicity are influenced by interkingdom signaling between plants and bacteria, with bacterial QS playing a role. AHLs and DSFs impact plant development and immunology. Both plants and bacteria live in the same environment, with low molecular weight compounds influencing their processes. LuxRs, including LuxR solos, use conserved DNA binding and auto-inducer domains as signal switches, responding more specifically to specific plants than classical QS ligands. Understanding the intra- and inter-communication between microorganisms and plants is therefore urgently needed.
Mode of action of antagonistic microbes for the management of pest–pathogens
Microorganisms offer promise as a biocontrol agent because they may eliminate phytopathogens without threatening the environment or other organisms that are not target. Compared to synthetic pesticides, this is unquestionably advantageous (Khamna et al. 2009). The studies of antagonistic microbiomes are gaining attention in order to manage plant diseases attracting more focus. Biological control agents (BCAs) typically increases the growth of plants via antibiosis, hyperparasitism, enzyme synthesis, competition for vital space and nutrients, plant resistance mechanisms, and production of plant resistance mechanisms (Babbal et al. 2017).
The search for alternative pest control techniques was sparked by rising anxiety and awareness regarding the increasing use of pesticides and their negative effects on the human being and environment, biological accumulation in food chain, insect resistance, and the ongoing presence of harmful chemicals in the environment. Hydrolytic enzymes are essential biochemical elements of insect metabolism and life cycles and include chitinases, lipases, proteases, cellulases, and glucanases, have emerged as a novel tool for management of pest. There have been reports of numerous entomopathogenic fungi, bacteria, and viruses releasing hydrolytic enzymes to kill pests. The potential usage of hydrolytic enzymes, as well as their mode of action and virulence, could therefore be useful for creating insecticides that are stronger and safer. The control of pests and the achievement of IPM objectives will be aided by a thorough understanding of the chemistry, regulation, and metabolism of chitin, a part of the insect pest that is more vulnerable to extra-cellular hydrolytic enzymes, as well as insect stages and life cycle.
Chitin is an insoluble linear homopolymer of N-acetylglucosamine (GlcNAc) that is hydrolyzed by chitinases (Berini et al. 2018). The N-acetylglucosamine polymer, that makes up chitin is the second most common polysaccharide on the planet, and it is connected by β-(1,4) linkages (Adrangi and Faramarzi 2013). It is widely distributed in nature and serves as functions polysaccharide in the exoskeleton of arthropods, the cell wall of fungi, the shells of crustaceans, and the cuticle of nematodes. Chitin is found in three polymorphic forms and is arranged in an antiparallel manner: α-, β-, and γ-chitins (Dahiya et al. 2006). The primary type of chitin found in nature is –chitin, which is primarily used as a structural component in invertebrate exoskeletons and fungal cell walls (Van Dyken and Locksley 2018). These are the primary chitin degraders in nature and participate in the hydrolysis-based recycling of nitrogen and carbon (Hartl et al. 2012). Plants, insects, and animals all produce these enzymes for various reasons, including morphogenesis, nourishment, and defense (Adrangi and Faramarzi 2013).
Large families of chitinases with specific roles in digestion, cell differentiation, and cuticle turnover are found in bacteria, plants, and insects. However, many animals, plants, and insects also express genes that produce lectins that resemble chitinases, but do not contain the catalytic site (Arakane and Muthukrishnan 2010). They retain the capacity to bind chitin despite lacking chitinolytic activity (Adrangi and Faramarzi 2013). Endochitinases (126.96.36.199) and exochitinases (188.8.131.52) are two categories of chitinolytic enzymes based on how they function (Van Dyken and Locksley 2018). The glycosyl hydrolase family (GH) can be used to classify chitinases on the basis of similarities in their amino acid sequences (Khoushab and Yamabhai 2010). Exochitinases are found in GH families 3, 18, 20, and 84, whereas endochitinases are primarily found in GH families 18, 19, 23, and 48 (Khan and Ahmad 2019).
According to Farag et al. (2016), the Aspergillus terreus purified chitinolytic enzyme has the ability to inhibit the growth of A. niger, A. oryzae, Penicillium oxysporium, Rhizoctonia solani, Candida albicans, and Fusarium solani. Streptomyces rimosus purified chitinase shown antifungal activity against Fusarium solani and Alternaria alternata in vitro (Brzezinska et al. 2013). Paenibacillus sp. D1, a high chitinase producer, was discovered by Singh et al. to be effective in the management of Helicoverpa armigera. This strain caused 40% mortality rate in the larvae, and when it was paired with the insecticide acephate, a synergistic effect was seen (Singh et al. 2016).
Though chemical pesticides will continue to be utilized for a very long time, it is imperative that it was find environmentally acceptable solutions if it want to prevent additional harm to the Earth's ecosystems. As they are already a part of the earth's soil and endophytic microbiome and would therefore only slightly modify the environment, chitinolytic bacteria are a potential substitute for these chemicals. In numerous different situations, they have also been shown to offer protection against diseases, and in other cases, simply adding chitin to the soil causes the pathogen population to drop. Although the results so far are encouraging, this line of study continues to be not adequately developed, so further research in this area should be conducted in order to gather enough information to effectively address the issues affecting food production and harvest.
Cellulolytic enzymes are classified primarily into three main groups: endoglucanases (EC 184.108.40.206) (1,4-β-d-glucan-4-glucanohydrolase or carboxymethyl cellulose), exoglucanases [Cellobiohydrolase (EC 220.127.116.11) cellodextrinase (EC 18.104.22.168)], and β-glucosidases (EC 22.214.171.124.1) (Hasunuma et al. 2013). According to the classification of the CAZy database, the three cellulase groups are made up of individuals from different GH families (Lombard et al. 2014). The targeting substrate's depolymerization stage determines how cellulases are categorized. Endoglucanases randomly hydrolyze the glycosidic linkages found in crystalline and amorphous cellulose, producing oligomers with different levels of polymerization (Sharma et al. 2016). The lytic enzyme, including cellulases, chitinases, chitosanases, glucanases, and proteases produced by the antagonists, disintegrate the fungal cell wall, which is made up of chitin and glucan in addition to wall proteins, and this contributes to the biocontrol activity (Spadaro and Droby 2016). The β-1,3-glucanase isolated from T. harzianum CECT 2413 has been reported to cause morphological changes in plants such as cytoplasm leakage, hyphal tip swelling, formation of numerous septae, as well as inhibition of plant disease by preventing the development of pathogenic Rhizopus solani and Fusarium sp. (Behera et al. 2017). Pythium is a plant pathogen that affected cucumber seedlings, was said to be less harmful in hypercellulolytic T. longibrachiatum mutants because they produced more β-1,4-endoglucanase than the wild type (Chet et al. 1998). Cellulase could therefore be employed as a biocontrol agent to shield seeds and plants from plant diseases (Bahera et al. 2017).
Proteases (EC. 3.4) are hydrolytic enzymes that break down proteins into smaller chains of peptides and amino acid groups (E.C. 3.4). Exopeptidases (EC 3.4.11–19), which cleave peptide bonds close to the amino or carboxy termini of the substrate, and endopeptidases (EC 3.4.21–25), which rupture peptide bonds far from the termini of the substrate, are the two primary categories into which proteases are commonly categorized (Rao et al. 1998). Proteases are further divided into four functional group found at the active site: aspartic, cysteine, serine, and metallo proteases (Khan and Ahmad 2019). These enzymes, which are physiologically essential for living and can be found in a variety of sources including microbes animals and plants, play numerous roles in literally all cellular processes (Yadav et al. 2016). Due to their metabolic diversity, quick development, and genetic modification susceptibility, which are all desired properties for biotechnological applications, microbes make an ideal source of proteases (Khan and Ahmad 2019). Insects are poisonous to proteases from a various species, such as fungi, bacteria, plants, insects, and viruses. Since proteins make up between 55 and 80 percent of an insect’s cuticle, the activity of chitinases and lipases follows a protease attack (Petrisor and Stoian 2017). The two most important proteins found in cuticle are collagen and the elastic tissue known as resilin that is peculiar to invertebrates (Khan and Ahmad 2019).
According to the report, Metarhizium anisopliae has been extensively explored as a model study, in pathogenicity and virulence processes against insect pests (Rosas-García et al. 2014). In similar report, Beauveria bassiana, an entomopathogenic fungus, has demonstrated potential as a biological pest management agent (Valero-Jiménez et al. 2016). Galleria mellonella produces proteinase inhibitors and antifungal peptides, which Metarhizium robertsii can detect and respond to by selectively expressing metalloproteases and proteases that target and degrade the insect defense molecules (Mukherjee and Vilcinskas 2018). An extracellular cuticle-degrading protease released by the soil-isolated Saccharomonospora viridis displayed exceptional nematotoxic action against Panagrellus redivivus (Darwesh et al. 2019).
In terms of a collection of varied and mostly unknown agents for the control of pests pathogens proteases stand out. Target specificity is a crucial concern before such proteases are widely used for pest management. The pest specificity is highly desired for reduced risk allied with any pest control approach. The future development of insect resistant transgenic plants shows special potential with the applications of proteases in plant defense against herbivory. The identification of potential proteases for use in pest management may be made easier in the genomes and transcriptomics era with a more efficiently understanding of the biology of virulence factors.
The most prevalent class of polysaccharides is β-glucans and made by microbes and higher plants as extracellular compounds, storage substances, and structural elements of the cell wall. Various microbes produce enzymes that can hydrolyze β-glucans (Bielecki and Galas 1991). Four different β-glucanases have been identified that catalyze the hydrolysis of β-glucan: lichenase (EC 126.96.36.199), cellulase (EC 188.8.131.52), laminarinase (EC 184.108.40.206), and β-1, 3(4)-glucanase (EC 220.127.116.11) (Luo et al. 2010).
In plant tissues, β-glucanases take role in the breakdown of glucans like callose, which is one of the wall changes implicated in resistance responses. Although investigations of β-glucanase I deficient mutants made via antisense transformation reveal that these enzymes play a critical role in viral pathogenesis, antifungal β-glucanase I appears to be optimized for defense against fungi, according to previous research (Prasannath 2017). While the exotype β-1,3-glucanase is involved in the further hydrolysis of released oligosaccharides, the endotype β-1,3-glucanase enzyme appears to be more crucial for the breakdown of the callosic walls. According to one theory, these glucanohydrolases function in at least two separate ways: directly by destroying the pathogen’s cell walls and indirectly by encouraging the release of substances produced from the pathogen’s cell walls that can trigger immune responses (Prasannath 2017; Veliz et al. 2017).
The anti-pathogenic effects of Trichoderma asperellum were sorted out from plantations damaged by banana wilt, by number of mechanisms. One of them is antibiosis, a pathogenic fungus from the Fusarium genus that is utilized by T. asperellum which inhibits spore germination by 30–75% and reduces phytopathogen development by 65–74%. The mycolytic enzymes β-1,3 glucanase and chitinase that T. asperellum releases may also be able to demolish phytopathogen cell walls. Enzymes β-1,3 glucanase and chitinase both had significantly increased transcript accumulation and enzymatic activity in pathogen-induced cells (Win et al. 2021). The genes were induced by chitinase and glucanase activity, while genes encoding antioxidant enzymes were regulated, when the plant immune system was stimulated by biocontrol fungal communities against RKNs, ET- and SA-responsive (Molinari and Leonetti 2019).
In mangoes infected with Colletotrichum gloeosporioides, the yeast Debaryomyces nepalensis generated β-1,3-glucanases. This hydrolytic enzyme’s production, along with the creation of other beneficial substances such volatile chemicals, assisted in controlling the spread of the fungus infection (Zhou et al. 2018). An intriguing BCA against Magnaporthe oryzae, the rice blast, is Paenibacillus terrae NK3-4. It was claimed that the 1,3-β-glucanase this bacterium produces may be almost liable for its antagonistic action (Yu et al. 2019). Promising BCAs for pepper grey mold, which is brought on by Botrytis cinerea, include the Bacillus velezensis strains 5YN8 and DSN012. According to the report, these strains of bacillus produced significant levels of glucanases enzymes (Jiang et al. 2018). It is interesting to note that plants' β-1,3 can be activated by volatile substances produced by bacteria. In another report, tobacco leaves harmed by R. solani and the oomycete Phytophthora nicotianae, volatiles of Bacillus sp. JS led to the up-regulation of PR-2 encoding β-1,3-glucanase (Kim et al. 2015).
Small substances known as plant hormones play a substantial role in a numerous physiological functions throughout stress and growth responses (Ma and Ma 2016). Through the manipulation of plant hormonal pathways, pathogens can also gain an advantage through two different mechanisms: firstly they can inhibit defense responses controlled by “stress” hormones in order to colonize plant tissues; and then they can interfere with nutrient allocation and plant development processes controlled by “growth” hormones in order to promote long-lasting colonization and dissemination. The “classical five”—commonly recognized classes of Phytohormones including abscisic acid, auxins, cytokinins, ethylene and gibberellins. Brassinosteroid, oligosaccharides, bioamines, salicylates-salicylic acid, and jasmonic acid are a few more new phytohormones or hormone-like compounds that have been identified (Tsavkelova et al. 2006).
A good example of this in pest–pathogen management is the ability of the bacterium P. fluorescens G20-18 to produce plant hormones (cytokinins), which improve the defenses of plants or crops against bacterial infections. On cultivated thale cress (Arabidopsis thaliana), this effect has been successfully proven (Großkinsky et al. 2016). In a report, virulent sugarcane aphid can initially start feeding on seedlings of both lines, according to a comparison of the two sorghum genotypes BTx623 and, Tx2783 but only Tx2783 showed to be resistant and able to protect against SCA. A complex molecular defense system like phytohormone-mediated defense is one of many internal defenses that resistant plants have to withstand unanticipated attacks (Huang et al. 2022). Therefore, metabolomic technique used to evaluate phytohormone expression profiles in plants with aphid infestations revealed that seven phytohormones expressed differently in resistant and vulnerable plants, supporting the critical function of phytohormones jasmonic acid, salicylic acid, and Auxin in sugarcane plant defense.
Durum wheat is more prone to Fusarium head blight. Antagonizing microbes can stimulate the biosynthesis of phytohormones, which are essential components of the plant defense system. The inoculation of B. velezensis RC 218 and S. albidoflavus RC 87B increase the level of salicylic acid (SA) and jasmonic acid (JA) under green house condition to control Fusarium blight infection in durum wheat increases the likelihood that these BCAs will become commercially successful products (Palazzini et al. 2018). The biocontrol of the anthracnose disease and better sorghum plant development have both been linked to T. harzianum's generation of IAA (Saber et al. 2017). Thus, a deeper understanding of the mechanism and action of phytohormones will help to uncover new strategies for managing pest pathogens.
Secondary metabolites production
Antibiotics, anticancer drugs, growth hormones, pigments, and other microbial secondary metabolites are necessary for the development and growth of microorganisms, but they showed a great deal of potential for improving the well-being of humans, plants and animals (Ruiz et al. 2010). A numerous bioactive molecules produced by microbes, including Actinobacteria, and fungi among the microorganisms that create the aforementioned chemicals have a great potential for use in various fields (O’Brien and Wright 2011). Accordingly, the expression of these clusters would be useful in taking advantage of the biodiversity of microbes. These bioactive molecules are mostly created by the activation of cryptic gene clusters, which are inactive under normal circumstances (Xu et al. 2019).
Crop protection has become a necessity in modern agriculture in order to maintain production. Chemical pesticides are thought to be a great solution for any pest issue, but using them excessively led to other environmental issues in addition to the fact that resistance developed, rendering them worthless. Microbial pest–pathogen management had at this point become a viable alternative technique because of its high ecological safety and target specificity. Although many different microorganisms including, bacteria, fungi, and nematodes are commercially accessible and being developed as well, their metabolites actually cause pathogenicity and host killing. It follows that choosing a particular strain of microbe for pest management depends on the pesticide metabolites, it produce and their bioactivity against target pest (Subbanna et al. 2020).
There are numerous secondary metabolites that have been shown to have pesticidal activity in field usage. These include the fungicides like kasugamycin, strobilurin A and B, validamycin, mildiomycin, blasticidin S, and polyoxin, the miticide as tetranactin, and the insecticides as avermectin and spinosyn (Maharana et al. 2022). Numerous investigations have recently revealed novel bioactive compounds from a wide range of microbial agents in pest management (Maharana et al. 2022). Sphaeropsidins belong to class of natural compound pimarane diterpene produced by fungi Diplodia spp. exhibit antibacterial antimycotic, and insecticidal activity (Ingels et al. 2017). Photorhabdus luminescens and Xenorhabdus nematophila produces secondary metabolites like p-hydroxyphenylpropionic acid (PHPP), Benzylideneacetone (BZA), 2-oxindole, acetylated phenylalanine-glycine- valine (Ac-FGV), 4-hydroxyphenylacetic acid (HPA), proline tyrosine (PY), cyclo-proline tyrosine (cPY) against insect pest that Inhibited phospholipase A2 (PLA2) and shut down eicosanoid biosynthesis (Mollah et al. 2020). P. chlororaphis, P. fluorescens, and P. aeruginosa produces Phenazine-1-carboxylate that has broad antifungal and antibacterial activity against plant pathogens (Shahid et al. 2017).
The majority of investigations used traditional activity monitoring and additional characterization utilizing fundamental molecular methods to examine the metabolites from known and established microbial pathogens. Additionally, the use of various media, fermentation methods, and screening approaches may result in a significant amount of bioactive secondary metabolites. Purification of products and the commercialization of powerful metabolites benefit greatly from developments in organic and synthetic chemistry. Additionally, conventional genetic techniques like recombination and mutation can be used to enhance the bioactivity and efficacy of metabolites. Thus, microbial pest–pathogen management has become a viable alternative to chemical pesticides due to its high ecological safety and target specificity. The commercial availability of biological pesticides with metabolites of microbial origin has been made possible by the isolation and characterization of secondary metabolites genes and their products of microbial origin.
Microbial pesticides in the new scenario of crop protection
The microbial pesticides are also known as biological control agent. In this group, the active substance is microbiomes that are either occur naturally or is genetically modified (Nega 2014). The bio based pesticides offer the advantages of high accuracy and no harmful effect in comparison to chemical pesticides (Hernandez et al. 2005). The biopesticides contain living organism (bacteria, fungus, virus, protozoan or alga, rickettsia, Mycoplasma and nematodes) which are toxic for the targeted pest including, Bacillus thuringiensis, bioherbicides (phytophthora) and biofungicides (Trichoderma, Pseudomonas, and Bacillus) (Gupta and Dikshit 2010). They suppress pest and pathogen by causing disease, producing pathogenic metabolites and preventing by other microorganism through numerous mode of action (Clemson 2007).
Bacteria are unicellular, prokaryotic microorganism varied from less than 1 μm to divergent length. Most of the pathogenic microbes belong to family Enterobacteriaceae, Micrococcaceae, Pseudomonadaceae, Streptococcaceae and Bacillaceae, in which member of Bacillaceae particularly Bacillus spp. showed maximum recognition as biocontrol agent (Kachhawa 2017). Bacteria biopesticides are used for the management to control the growth of harmful pathogenic bacteria. They are generally specific to the individual species of butterflies and moths or species of mosquitoes, flies and beetles (Kausar 2018). In insect, bacteria disrupt the digestive system by colonize the interior part of plant and producing endotoxin that is constantly specific to targeted insect pest (O’Brien et al. 2009). The most commonly used biopesticides are strain of Bacillus thuringiensis (Bt), accounting around 90% of the biopesticides in the market of USA (Chattopadhyay et al. 2004). Bt has been most widely used to control insect pest and pathogen in agriculture, medicine and forestry (Mazid et al. 2011). During synthesis of Bt sporulation of crystalline containing Cry protein showed insecticidal properties (Federici et al. 2006). Although their high attentiveness and security in the environment, Bt and Cry protein are effective, safe and sustainable substitute to chemical pesticides for management of insect pest (Kumar et al. 2008).
Entomopathogenic fungi play an important role as biocontrol agent of insect population (Sharma and Malik 2012). A diverse group of fungal species is found in various infected insect and infecting capability including, facultative and obligate pathogens (Pucheta et al. 2016). In 1980s, the first insect pathogenicity was carried out and their main focus was to detect the method of disease management of silkworm (Steinhaus 1975). A diverse group of fungi belongs to phylum Ascomycota, Chytridiomycota, Deuteromycota, Oomycota and Zygomycota (Samson et al. 1988). The entrance point of entomopathogen is through integument and they also infect the insect by through wounds or trachea or ingestion method (Holder and Keyhani 2005). The entomopathogenic fungi had the most relevant biocontrol agent, as they represent a group with approx 750 species and when disseminate in the environment and produce fungal infection in insect community. They begin their infective process when the spore of fungi is employ on integument surface, where the formation of germinative tube inaugurates. The fungi also produce enzyme such as chitinases, lipoxygenases, proteases, Upases and quitobiases (Vaghasiya et al. 2021). These enzymes deteriorate the insect cuticle and help in penetration by mechanical pressure that is begin by appressorium (Zhang et al. 2010). After that fungi flourish as hyphal bodies that promulgate hemocoel and infect diverse group of fatty bodies, malpighian tubes, muscle tissues, hemocytes and mitochondria, cause the death of insect after 3 to 14 days of infection (Woldemelak 2020). Once the insect dies a large number of nutrient are consume, fungi start micelles growth and occupy the entire organ in the host cell. Ultimately, hyphae penetrate the cuticle in interior of insect and make an appearance at the surface where they start spore formation under the adequate environmental conditions (Henrik et al. 2023).
Insect virus are considered as beneficial and environmentally friendly which may contribute to attain sustainable agriculture through providing an appropriate replacement of chemical pesticides which have negative impact on the environment (Riyaz et al. 2022). A virus is an assembly of one or more nucleic acid template molecules that are generally covered in a protein or lipoprotein protective shell and are able to coordinate their own replication in specific kinds of host cells. The virus has been sorted out from more than 1000 species of insect from nearly 13 different insect orders (Käfer et al. 2019). Entomogenous viruses are categories into two, viz. inclusion viruses producing insertion bodies in the host cell and another is non-inclusion viruses, which do not produce insertion bodies. The insect virus belonging to the family of Baculoviridae was considered for the development and commercialization of viral biopesticides (Moore et al. 1987). Baculoviruses contain enveloped viruses that only infect insects. They have circular, supercoiled double-stranded DNA genomes that range in size from 80 to 180 kbp (Chambers et al. 2018). A large number of baculoviruses have been sorted out from butterflies, moths, sawflies and mosquitoes (Blissard et al. 2000).
The name baculovirus are derived from Latin, which are approximately 230–385 nm in length and 40–60 nm in diameter. These viruses are transmissible by mouth and reveal via horizontal transmission. When the occlusion bodies (OBs) are digested by insect and release the virions particles into the lumen (Derksen and Granados 1988). These virions entered into nucleus, at the point in which virus replicate within the nucleus of susceptible tissue and tissue susceptibility varied between virus and nuclear polyhedrosis viruses being capable of infecting all the tissue and granulosis viruses (GVs) being specific for tissue replication (Adams and McClintock 1991). The budded virus starts infection to other tissue such as hemocytes, nerve cells and fat bodies. However, cell infected in the second round of virus replicate in the insect larva and produce budded virus but particles of occlude virus within polyhedral in the nucleus (Godfray et al. 1997). The accretion of polyhedral within the insect profits until the host incorporates almost completely of a bag of virus. At the last stage of infection insect liquefies and release polyhedral, which can infect other insect and targeted pest killed 3–7 days but when the condition is not ideal the death may take 3–4 weeks (Kalha et al. 2014). The viruses are used as biopesticides against insect pest, but the main drawback is the requirement for in vivo conditions and this high sensitivity to ultraviolet radiation.
Development and commercialization of microbial pesticides
The use of pesticides to protect plants from viruses, pests, and weeds has steadily evolved from a therapeutic strategy to a pragmatic one those priorities protecting human health and the environment over any form of productivity or commercialization. Currently, number of beneficial microbiomes are among the vigorous ingredients in a new generation of bacterial pesticides or serve as the basis for numerous naturally occurring chemicals obtained by microbial extraction. The development of microbial pesticides involves number of steps such as the isolation of pure culture in form of single distinct archaea, bacteria, fungi, and screening of isolated microbes for biocontrol attributes (Fig. 2). To be commercially delivered, a microbial pesticide, industrial-scale production is important, followed by preservation and formulation with biocompatible additives to enhance the survival and improving applications and stability of the final product (Montesinos 2003).
Formulation and production
India has the greatest potential for microbial-based insecticide because agriculture is foundation of our economy. The researchers should look into all of the limitations and popularization prospects in this emerging field. Excessive and incorrect use of insecticide has led to the emergence of secondary pests, the rise of pesticide resistance to main classes of pesticides, high levels of pesticide residue in product, and the extinction of natural enemies. The excessive utilization of the pesticides has led to the adverse effect on humans and the environment. Biopesticides are an environmental friendly alternative to the biopesticides. Biopesticides have been categorized into microbial, biochemical, and plant-incorporated protectants (PIPs). The most commonly utilized biological pesticides are microbes which possess a pathogenic effect on pest of interest. These consist of bioinsecticides which include Bacillus thuringiensis and Bacillus sphaericus; biofungicides including Trichoderma; bioherbicides including Phytophthora.
Antinsectan compounds such as thiolutin, aminolevulinic acid, thuringiensin, xenorhabdins, actinomycin A, aplasmomycin, citromycin, piericidins, spinosyns and nikkomycin derived from actinomycetes, fungi and non-filamentous bacteria are well known to produce toxic effects and are able to act as antifeedants, growth inhibitors and physiological disrupters against the pests (Kirst 2010). Some of these compounds such as spinosyns and avermectins have been commercialized. The superior characteristics of microbial pesticides have gained much attention and also have made them a hot spot of research in biotechnology and numerous companies.
Fermentation provides a source of bioactivity against agriculturally important target organisms. The development of a biopesticide is a lengthy process with several stages such as discovery, product, production, efficacy testing, development, registration, and finally commercialization. Formulation technology must be account at all stages from concept to final action on the target. The method of production frequently dictates subsequent formulation activities, which may result in changes to the production process. The method of manufacturing frequently dictates subsequent formulation activities, which may changes in production process. Formulation serves four main function: stabilizing the organism during production, distribution, and storage; assisting with product handling and application so that it can be delivered to the target easily; protecting the agent from harmful environmental factors at the target site; and enhancing the activity of the organism at the location of the target through boosting its activity, development, connection, and interaction with the target (Jones and Burges 1998).
Microbial pesticides can be found in a number of formulations, including suspensions, wettable powders, oil suspensions, suspended seed coatings, and water dispersible granules. Microbial pesticide production is a complex and complicated process as compared to the chemical pesticides. Microbial pesticides are more susceptible to external environmental factors during the process of preparation (Lin et al. 2023). Microorganisms directly affected physical properties of pesticide preparations such as wettability, suspension, and dispersibility. Microbial pesticides are produced using adjuvants, which are primarily divided into transporters, protecting agents, surfactants, and nutritive adjuvants. Surfactants play an essential role for enhancing the potency, efficiency, and cost-effectiveness of the synthesis of microbial pesticides as well as conserving energy and raw materials. They improve biological functions and maintain physical stability of the product (Castro et al. 2014). The main function of a carrier is to encapsulate or dilute the active components of microbial pesticides. (Borger et al. 2013). Attapulgite, bentonite, diatomite, and silica are examples of carriers that can be employed to create wettable powders, granules, or high concentration powders (Kashyap et al. 2015).
Microbial pesticides are passivation degraded, or damaged by UV radiation (Jarzębski et al. 2019). The majority of UV protection compounds employed in the formation of microbial pesticides grouped into two categories UV ray absorption materials and antioxidant UV protection substances. UV ray absorbers can absorb the UV ray and fluorescent light sources without changing itself (Jadhav et al. 2022). Strong antioxidant properties of anti-oxidative UV protection compounds assist in the prevention of microbial pesticides being easily oxidized and converted into additional compounds that are useless against potentially dangerous organisms when exposed to UV radiation. Protective substances can extend the shelf lives and enhance the control effect of microbial pesticides when used in the field (Pershakova et al. 2021). The dietary requirements of the microbes in microbial pesticides are met by nutritional adjuvants, which improved their ability to reproduce and encourage their proliferation and expansion in the field.
The active ingredient used in bio-pesticide formulations is the most important factor in their production. The active compound influences the composition of bio-pesticides. The microbial formulation technique is governed by the active ingredient, which differs in each of them. In the case of microbial bio-based pesticides, the active ingredient is microbiomes that are useful in controlling crop damage which is caused by insect pests. In order to make this formulation, these microorganisms must be utilized in a specific method. The microorganisms are biogenetically altered in a way that restricts the range of applications for their action spectrum (Meena and Mishra 2020).
Microbial pesticides contain active ingredients that are specific to their target pests (Kawalekar 2013). These pesticides are therefore safe for non-target beneficial pests and maintained ecological balance. The use of bio-pesticides is increasing at a rate of about 10% per year (Bailey and Mupondwa 2006). However, due to increased resistance of pest to chemical pesticides and increasing awareness about the use of non-toxic and safe substances in agriculture, this rate has been increasing in recent years. The USA uses the biopesticides (45%), followed by the European Union (20%) and the rest by other countries (Bailey et al. 2010). Depending on the preparation and retention of the microorganisms, the shelf life of bacterial pesticides might range from a few days to several months.
Currently, the biopesticides market enjoys an annual expansion of 15%, and the prospect for growth seems bright. But, efforts are still required to achieve a successful commercialization. It is crucial to focus on customer satisfaction based on sustained product performance in respect to prices and usability. There are number of factors that determine success or failure of a product. In 1938, France, with Sporeine, a living organism, was used commercially for the first time in agriculture. Bt was used as a biopesticide for controlling the caterpillars. Products based on nematodes fungi, and bacteria gradually entered the market at beginning in the 1960s, and the range of pest and disease control products has grown ever since. Today, the worldwide turnover of bio-based pesticides is approximately 1.8 billion US$. Annual growth for the last decade has been approximately 15% (Ravensberg 2015).
Microbial biopesticides are the most common broad-spectrum biopesticides used today, accounting for the majority of pest-specific bio-pesticides. At the least 1500 naturally occurring insect specific microorganisms exist, with 100 of them being insecticidal. Over 200 microbial biopesticides are available in 30 Organizations for Economic Cooperation and Development member countries (OECD). There are 22 registered microbial biopesticides in Canada, 53 in USA and 21 in the European Union. Overall microbial biopesticides registration are increased globally, the expansion of numerous technology has increased the scope of more product and the trends toward development of microbial product is definitely changed (Opender Koul 2012).
The development and use of microbial pesticides is gradually replacing the highly harmful and chemical pesticides in the market. The production of microbial-based pesticides increases at the rate of 20% annually, while the production of chemical-based pesticides has declined by 2% every year (Cheng et al. 2010). Pest Management Regulatory Agency accepted registration of 24 microbial active substances in 83 formulations in Canada in 1972–2008 (Bailey et al. 2010). The majority of the registrations (55/83) occurred up to 2000, and in 2008 alone, there were ten new products under regulatory evaluation. Commercially, there are some biopesticides available to farmers. There are about 175 registered bio-based pesticides globally, with 700 active substances available for use.
In India, 194 compounds have been registered as chemical pesticides and 12 biopesticides by the year 2006. The number of newly created and approved microbial pesticides is rising at a rate of 4% annually, but the overall market share of biopesticides has increased to 30% (Gupta 2006). Presently, about 75% of biopesticide use consists of Bt-based products. Bt has been used to control lepidopteran, dipteran and coleopteran insects for more than three decades. As an effective microbial pesticide, mostly biochemical biopesticides worldwide are the purified toxin from this strain. Metabolites from Photorhabdus luminescens are a promising alternative to synthetic fungicides. They are effective against pecan scab because of the bioactive compound trans-cinnamic acid that showed antifungal (Bock et al. 2014). Beauveria bassiana can be used as a biopesticide in the management of crop pests (Samada and Tambunan 2020).
New microbial insecticides containing pathogenic or inhibiting microorganisms must follow guidelines for safety testing and registration. These guidelines provide interested businesses and government agencies. They are the outcome of recent, vigorous involvement with this field and more than a decade of experience. The identity, biological characteristics, production, formulation, quality control, application, and efficacy of the novel bacteria are all necessary for the registration of a new microbial product. The current recommendations include a list of required tests for new bacterial pesticides. The standards for registering a novel bacterial pesticide should generally be the same, although guidelines may differ according to the national pesticide registration protocols of other nations (Burges et al. 1982).
Role of microbial pesticides in agriculture
Environmental challenges and threats to sustainable agriculture are presently causing an increasing amount of concern (Gomiero et al. 2011). The famers are increasing used chemical pesticides to control the pest and pathogen for improvement of crop production. Chemical pesticides are made from chemical such as polymer which is specific to targeted host (Rakhimol et al. 2020). The over application of pesticides and excess discharge into water bodies during rainfall can cause death of fishes and other marine life. The consumption of fishes by human may cause disease including cardiovascular, diabetes, kidney failure, skin, cancer, liver dysfunction, eczema and neurological destruction (Manfo et al. 2020). In agriculture use of chemical pesticides harm beneficial soil microbes, plant and soil texture (Riedo et al. 2021). In light of all of these considerations, using biopesticides over the long run appears to be more cost-effective, environmentally friendly, productive, and accessible to marginal and small farmers than chemical insecticides. This makes crops more susceptible to insect pest attacks, which severely decreases crop yield. Natural product is eco-friendly in nature and also easily biodegradable. In response to the demand for food grown organically and changing consumer tastes and preferences, biopesticides are appropriate substitutes for synthetic pesticides (Okunlola and Akinrinnola 2014). As a result of their short pre-harvest intervals, biopesticides are safe to use on fresh fruits and vegetables (Khater 2012). They are efficient in small amounts, and their use stimulates viable pest control, which helps contribute to sustainable agriculture (Nawaz et al. 2016). In order to reduce the amount of chemical pesticides used in the management of crop pests, biopesticides can therefore be effectively included into integrated pest management (IPM) (Sesan et al. 2015). Additionally, biopesticides have been used for cleaning up agricultural soils by introducing significant microbial populations (Javaid et al. 2016).
Limitations and challenges
Although microbial inoculants offer a potential alternative to chemical fertilizers, there are a number of restrictions and difficulties that come with their use as biopesticides. They only have a short shelf life, and if they are not utilized promptly or stored properly, they may lose their potency (Qiu et al. 2019). New biotechnological techniques should be developed in order to provide formulations with extended shelf life. Additionally, there are certain restrictions on the usage of microbial inoculants, such as the need to monitor their consistency, consistency of their quality, application methods, compatibility with chemical fertilizers, and environmental conditions including temperature, moisture, and pH (Shahwar et al. 2023). The ability to enhance or protect yield is the most crucial component for a successful product. In addition to the other aspects, this is undoubtedly the most crucial and essential factor for the success of the entire product. However, success in the laboratory or greenhouse does not always equate to success in the field. The use of an inoculants or biocontrol product by both the manufacturer and the consumer is a crucial component in determining its success. The product should ideally have a low adoption barrier and be compatible with the farmer's equipment and production practices (Parnell et al. 2016).
The challenge of pest control for sustainable agriculture has been of great concern. Efficient, low-risk and eco-friendly pest control solutions to meet manufacturer, consumer and regulatory needs are of major importance. The research on microbes-based biopesticides is emerging as an important alternative for chemicals used for pest control for many years. Biopesticides control the plant pathogens, pests and weeds by diverse mechanisms. In fact, the biopesticides are becoming an integral part of pest management systems due to their advantages of environmental safety, biodegradability, effectiveness and suitability in the integrated pest management (IPM) programs. Further research on biopesticides and their development is important on priority basis. It is important to make awareness and educate general people, farmers, agriculturists, government agencies and policy makers about the use and handling of microbial pesticides. The popularization of the biopesticides is another challenge which can be met with through training programs on production and quality control to manufacturers. The adoption of this technology also requires organizational training to extension workers and farmers. The search for new biocontrol agents for future use in different habitats and climates should continue. Development of novel methods for manufacturing, formulation, storage and utilization to improve efficiency and cost effectiveness will also open way for adoption of microbes-based biopesticides. Changes in political and social attitudes have though increased the opportunities for microbial pesticides still further research on pest pathogen ecology and exploration of diversity is required. All this will lead to a more comprehensive understanding of the benefits of biopesticides as a green and sustainable alternative.
Availability of data and material
N-acyl homoserine lactone
Biological control agents
Diffusible signal factor
Integrated pest management
Ab Rahman SFS, Singh E, Pieterse CM, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111. https://doi.org/10.1016/j.plantsci.2017.11.012
Adams JR, McClintock JT (1991) Baculoviridae. Nuclear polyhedrosis viruses. Part 1. Nuclear polyhedrosis viruses of insects. In: Adams JR, Bonami JR (eds) Atlas of invertebrate viruses. CRC Press, Boca Raton, pp 89–204
Akhter W, Bhuiyan MKA, Sultana F, Hossain MM (2015) Integrated effect of microbial antagonist, organic amendment and fungicide in controlling seedling mortality (Rhizoctonia solani) and improving yield in pea (Pisum sativum L.). CR Biol 338(1):21–28. https://doi.org/10.1016/j.crvi.2014.10.003
Al-Daghari DSS, Al-Sadi AM, Al-Mahmooli IH, Janke R, Velazhahan R (2023) Biological control efficacy of indigenous antagonistic bacteria isolated from the rhizosphere of cabbage grown in biofumigated soil against Pythium aphanidermatum damping-off of cucumber. Agriculture 13(3):626. https://doi.org/10.3390/agriculture13030626
Al-Ghamdi A, Al-Abbadi AA, Khan KA, Ghramh HA, Ahmed AM, Ansari MJ (2020) In vitro antagonistic potential of gut bacteria isolated from indigenous honey bee race of Saudi Arabia against Paenibacillus larvae. J Apic Res 59(5):825–833. https://doi.org/10.1080/00218839.2019.1706912
Arakane Y, Muthukrishnan S (2010) Insect chitinase and chitinase-like proteins. Cell Mol Life Sci 67:201–216. https://doi.org/10.1007/s00018-009-0161-9
Aranda S, Montes-Borrego M, Jiménez-Díaz RM, Landa BB (2011) Microbial communities associated with the root system of wild olives (Olea europaea L. subsp. europaea var. sylvestris) are good reservoirs of bacteria with antagonistic potential against Verticillium dahliae. Plant Soil 343(1):329–345. https://doi.org/10.1007/s11104-011-0721-2
Ayyadurai N, Ravindra Naik P, Sreehari Rao M, Sunish Kumar R, Samrat SK, Manohar M, Sakthivel N (2006) Isolation and characterization of a novel banana rhizosphere bacterium as fungal antagonist and microbial adjuvant in micropropagation of banana. J Appl Microbiol 100(5):926–937. https://doi.org/10.1111/j.1365-2672.2006.02863.x
Babbal, Adivitiya, Khasa YP (2017) Microbes as biocontrol agents. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and plant health. Springer, Singapore. https://doi.org/10.1007/978-981-10-3473-2_24
Bailey K, Boyetchko S, Längle T (2010) Social and economic drivers shaping the future of biological control: a Canadian perspective on the factors affecting the development and use of microbial biopesticides. Biol Control 52(3):221–229. https://doi.org/10.1016/j.biocontrol.2009.05.003
Bailey KL, Mupondwa EK (2006) Developing microbial weed control products: commercialization, biological, and technological considerations. In: Singh HP, Batish DR, Kohli RK, Binghamton NY (eds) Handbook of sustainable weed management. The Haworth Press, Binghamton, pp 431–473
Bahera BC, Sethi BK, Mishra RR, Dutta SK, Thatoi HN (2017) Microbial cellulases—diversity and biotechnology with reference to mangrove environment: a review. J Genet Eng Biotech 15(1):197–210. https://doi.org/10.1016/j.jgeb.2016.12.001
Berini F, Katz C, Gruzdev N, Casartelli M, Tettamanti G, Marinelli F (2018) Microbial and viral chitinases: attractive biopesticides for integrated pest management. Biotechnol Adv 36(3):818–838. https://doi.org/10.1016/j.biotechadv.2018.01.002
Bibi F, Naseer MI, Hassan AM, Yasir M, Al-Ghamdi AAK, Azhar EI (2018) Diversity and antagonistic potential of bacteria isolated from marine grass Halodule uninervis. 3 Biotech 8(1):48. https://doi.org/10.1007/s13205-017-1066-1
Bielecki S, Galas E (1991) Microbial β-glucanases different from cellulases. Crit Rev Biotechnol 10(4):275–304. https://doi.org/10.3109/07388559109038212
Blissard G, Black B, Crook N, Keddie B, Possee R, Rohrmann G, Theilmann D, Volkman L (2000) Family Baculoviridae. In: van Regenmoertel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB (eds) Virus Taxonomy—seventh report of the international committee on taxonomy of viruses. Academic Press San Diego, pp 195–202
Bock CH, Shapiro-Ilan DI, Wedge DE, Cantrell CL (2014) Identification of the antifungal compound, trans-cinnamic acid, produced by Photorhabdus luminescens, a potential biopesticide against Pecan scab. J Pest Sci 87:155–162. https://doi.org/10.1007/s10340-013-0519-5
Borger CP, Riethmuller GP, Ashworth M, Minkey D, Hashem A, Powles SB (2013) Increased carrier volume improves preemergence control of rigid ryegrass (Lolium rigidum) in zero-tillage seeding systems. Weed Technol 27(4):649–655. https://doi.org/10.1614/WT-D-12-00117
Brzezinska MS, Jankiewicz U, Walczak M (2013) Biodegradation of chitinous substances and chitinase production by the soil actinomycete Streptomyces rimosus. Int Biodeterior Biodegrad 84:104–110. https://doi.org/10.1016/j.ibiod.2012.05.038
Burges HD, Krieg A, Lüthy P, de Barjac H (1982) Guidelines for safety tests and registration of bacterial pesticides. Entomophaga 27(3):225–235. https://doi.org/10.1007/BF02374807
Castro MJ, Ojeda C, Cirelli AF (2014) Advances in surfactants for agrochemicals. Environ Chem Lett 12:85–95. https://doi.org/10.1007/s10311-013-0432-4
Caulier S, Gillis A, Colau G, Licciardi F, Liépin M, Desoignies N, Bragard C (2018) Versatile antagonistic activities of soil-borne Bacillus spp. and Pseudomonas spp. against Phytophthora infestans and other potato pathogens. Front Microbiol 9:143. https://doi.org/10.3389/fmicb.2018.00143
Chambers AC, Aksular M, Graves LP, Irons SL, Possee RD, King LA (2018) Overview of the baculovirus expression system. Curr Protoc Protein Sci 91:541–546. https://doi.org/10.1002/cpps.47
Chandra H, Kumari P, Bisht R, Prasad R, Yadav S (2020) Plant growth promoting Pseudomonas aeruginosa from Valeriana wallichii displays antagonistic potential against three phytopathogenic fungi. Mol Biol Rep 47(8):6015–6026. https://doi.org/10.1007/s11033-020-05676-0
Chattopadhyay A, Bhatnagar N, Bhatnagar R (2004) Bacterial insecticidal toxins. Crit Rev Microbiol 30(1):33–54. https://doi.org/10.1080/10408410490270712
Cheng XL, Liu CJ, Yao JW (2010) The current status, development trend and strategy of the bio-pesticide industry in China. Hubei Agric Sci 49:2287–2290
Chowhan LB, Mir MI, Sabra MA, El-Habbab AA, Kumar BK (2023) Plant growth promoting and antagonistic traits of bacteria isolated from forest soil samples. Iran J Microbiol 15(2):278. https://doi.org/10.18502/ijm.v15i2.12480
Clemson HG (2007) Organic pesticides and biopesticides, Clemson extension, home and garden information center. Clemson University, Clemson
Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71:773–782. https://doi.org/10.1007/s00253-005-0183-7
Damodaran T, Rajan S, Manoharan Muthukumar RG, Yadav K, Kumar S, Ahmad I, Jha SK (2020) Biological management of banana Fusarium wilt caused by Fusarium oxysporum f. sp. cubense tropical race 4 using antagonistic fungal isolate CSR-T-3 (Trichoderma reesei). Front Microbiol 11:595845. https://doi.org/10.3389/fmicb.2020.595845
Darwesh OM, El-Hawary AS, El Kelany US, El-Sherbiny GM (2019) Nematicidal activity of thermostable alkaline protease produced by Saccharomonospora viridis strain Hw G550. Biotechnol Rep 24:e00386. https://doi.org/10.1016/j.btre.2019.e00386
Deng Y, Je Wu, Eberl L, Zhang L-H (2010) Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl Environ Microbiol 76(14):4675–4683. https://doi.org/10.1128/AEM.00480-10
Deng Y, Liu X, Je Wu, Lee J, Chen S, Cheng Y, Zhang C, Zhang L-H (2015) The host plant metabolite glucose is the precursor of diffusible signal factor (DSF) family signals in Xanthomonas campestris. Appl Environ Microbiol 81(8):2861–2868. https://doi.org/10.1128/AEM.03813-14
Derksen AC, Granados RR (1988) Alteration of a lepidopteran peritrophic membrane by baculoviruses and enhancement of viral infectivity. Virology 167(1):242–250. https://doi.org/10.1016/0042-6822(88)90074-8
DiLegge MJ, Manter DK, Vivanco JM (2019) A novel approach to determine generalist nematophagous microbes reveals Mortierella globalpina as a new biocontrol agent against Meloidogyne spp. nematodes. Sci Rep 9(1):7521. https://doi.org/10.1038/s41598-019-44010-y
Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer N (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20(9):2444–2449. https://doi.org/10.1021/bi00512a013
Federici BA, Park HW, Sakano Y (2006) Insecticidal protein crystals of Bacillus thuringiensis. In: Shively JM (ed) Inclusions in Prokaryotes. Springer, Berlin-Heidelberg, pp 195–235. https://doi.org/10.1007/3-540-33774-1_8
Fitriana Y, Tampubolon DAT, Suharjo R, Lestari P, Swibawa IG (2022) Lysinabacillus fusiformis and Paenibacillus alvei obtained from the internal of nasutitermes termites revealed their ability as antagonist of plant pathogenic fungi. Plant Pathol J 38(5):449. https://doi.org/10.5423/PPJ.OA.03.2022.0031
Freire E, Campos V, Pinho R, Oliveira D, Faria M, Pohlit A, Noberto N, Rezende E, Pfenning L, Silva J (2012) Volatile substances produced by Fusarium oxysporum from coffee rhizosphere and other microbes affect Meloidogyne incognita and Arthrobotrys conoides. J Nematol 44(4):321
Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269–275
Gay H (2012) Before and after Silent Spring: from chemical pesticides to biological control and integrated pest management—Britain, 1945–1980. Ambix 59(2):88–108. https://doi.org/10.1179/174582312X13345259995930
Godfray H, O’reilly D, Briggs C (1997) A model of Nucleopolyhedrovirus (NPV) population genetics applied to co–occlusion and the spread of the few Polyhedra (FP) phenotype. Proc R Soc Lond Series B: Biol Sci 264(1380):315–322. https://doi.org/10.1098/rspb.1997.0045
Gomiero T, Pimentel D, Paoletti MG (2011) Is there a need for a more sustainable agriculture? Crit Rev Plant Sci 30(1–2):6–23. https://doi.org/10.1080/07352689.2011.553515
Götz-Rösch C, Sieper T, Fekete A, Schmitt-Kopplin P, Hartmann A, Schröder P (2015) Influence of bacterial N-acyl-homoserine lactones on growth parameters, pigments, antioxidative capacities and the xenobiotic phase II detoxification enzymes in barley and yam bean. Front Plant Sci 6:205. https://doi.org/10.3389/fpls.2015.00205
Gowtham HG, Hariprasad P, Nayak SC, Niranjana SR (2016) Application of rhizobacteria antagonistic to Fusarium oxysporum f. sp. lycopersici for the management of Fusarium wilt in tomato. Rhizosphere 2:72–74. https://doi.org/10.1016/j.rhisph.2016.07.008
Großkinsky DK, Tafner R, Moreno MV, Stenglein SA, García de Salamone IE, Nelson LM, Novák O, Strnad M, Van der Graaff E, Roitsch T (2016) Cytokinin production by Pseudomonas fluorescens G20–18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci Rep 6(1):1–11. https://doi.org/10.1038/srep23310
Gupta PK (2006) Status of biopesticides-Indian scene. Toxicol Lett 13:65–73. https://doi.org/10.1016/j.toxlet.2006.06.085
Gupta S, Dikshit A (2010) Biopesticides: An ecofriendly approach for pest control. J Biopestic 3(1):186–188
Gurung K, Wertheim B, Salles JF (2019) The microbiome of pest insects: it is not just bacteria. Entomol Experim Appl 167:156–170. https://doi.org/10.1111/eea.12768
Haesler F, Hagn A, Frommberger M, Hertkorn N, Schmitt-Kopplin P, Munch JC, Schloter M (2008) In vitro antagonism of an actinobacterial Kitasatospora isolate against the plant pathogen Phytophthora citricola as elucidated with ultrahigh resolution mass spectrometry. J Microbiol Methods 75(2):188–195. https://doi.org/10.1016/j.mimet.2008.05.028
Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93:533–543. https://doi.org/10.1007/s00253-011-3723-3
Hasunuma T, Okazaki F, Okai N, Hara KY, Ishii J, Kondo A (2013) A review of enzymes and microbes for lignocellulosic biorefinery and the possibility of their application to consolidated bioprocessing technology. Bioresour Technol 135:513–522. https://doi.org/10.1016/j.biortech.2012.10.047
He YW, Xu M, Lin K, Ng YJA, Wen CM, Wang LH, Liu ZD, Zhang HB, Dong YH, Dow JM (2006) Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell–cell communication-dependent genes and functions. Mol Microbiol 59(2):610–622. https://doi.org/10.1111/j.1365-2958.2005.04961.x
He Y-W, Je Wu, Cha J-S, Zhang L-H (2010) Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:1–9. https://doi.org/10.1186/1471-2180-10-187
Henrik H, Edwards S, Elya C, Henrik H (2023) Evolutionary ecology of an obligate and behaviorally manipulating insect-pathogenic fungus, Entomophthora muscae. https://doi.org/10.22541/au.167778641.14505987/v1
Hernández-Reyes C, Schenk ST, Neumann C, Kogel KH, Schikora A (2014) N-acyl-homoserine lactones-producing bacteria protect plants against plant and human pathogens. Microb Biotechnol 7(6):580–588. https://doi.org/10.1111/1751-7915.12177
Hernandez F, Sancho J, Pozo O (2005) Critical review of the application of liquid chromatography/mass spectrometry to the determination of pesticide residues in biological samples. Anal Bioanal Chem 382:934–946. https://doi.org/10.1007/s00216-005-3185-5
Heydari A, Pessarakli M (2010) A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci 10(4):273–290. https://doi.org/10.3923/jbs.2010.273.290
Hilber-Bodmer M, Schmid M, Ahrens CH, Freimoser FM (2017) Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi. BMC Microbiol 17(1):4. https://doi.org/10.1186/s12866-016-0908-z
Holder DJ, Keyhani NO (2005) Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Appl Environ Microbiol 71(9):5260–5266. https://doi.org/10.1128/AEM.71.9.5260-5266.2005
Hong CE, Jo SH, Moon JY, Lee J-S, Kwon S-Y, Park JM (2015) Isolation of novel leaf-inhabiting endophytic bacteria in Arabidopsis thaliana and their antagonistic effects on phytophathogens. Plant Biotechnol Rep 9(6):451–458. https://doi.org/10.1007/s11816-015-0372-5
Huang J, Shrestha K, Huang Y (2022) Revealing differential expression of phytohormones in sorghum in response to aphid attack using the metabolomics approach. Int J Mol Sci 23(22):13782. https://doi.org/10.3390/ijms232213782
Ingels A, Dinhof C, Garg AD, Maddau L, Masi M, Evidente A, Berger W, Dejaegher B, Mathieu V (2017) Computed determination of the in vitro optimal chemocombinations of sphaeropsidin A with chemotherapeutic agents to combat melanomas. Cancer Chemother Pharmacol 79:971–983. https://doi.org/10.1007/s00280-017-3293-x
Jadhav N, Pantwalawalkar J, Sawant R, Attar A, Lohar D, Kadane P, Ghadage K (2022) Development of progesterone oily suspension using Moringa oil and Neusilin US2. J Pharm Innov 17:534–545. https://doi.org/10.1007/s12247-020-09529-y
Jarzębski M, Smułek W, Siejak P, Kobus-Cisowska J, Pieczyrak D, Baranowska HM, Jakubowicz J, Sopata M, Białopiotrowicz T, Kaczorek E (2019) Aesculus hippocastanum L. extract as a potential emulsion stabilizer. Food Hydrocoll 97:105237. https://doi.org/10.1016/j.foodhyd.2019.105237
Javaid MK, Ashiq M, Tahir M (2016) Potential of biological agents in decontamination of agricultural soil. Scientifica. https://doi.org/10.1155/2016/1598325
Jennings JA, Courtney HS, Haggard WO (2012) Cis-2-decenoic acid inhibits S. aureus growth and biofilm In vitro: a pilot study. Clin Orthop Relat Res 470:2663–2670. https://doi.org/10.1007/s11999-012-2388-2
Jiang C-H, Liao M-J, Wang H-K, Zheng M-Z, Xu J-J, Guo J-H (2018) Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinerea. Biol Control 126:147–157. https://doi.org/10.1016/j.biocontrol.2018.07.017
Jin F, Ding Y, Ding W, Reddy MS, Fernando WGD, Du B (2011) Genetic diversity and phylogeny of antagonistic bacteria against Phytophthora nicotianae isolated from tobacco rhizosphere. Int J Mol Sci 12(5):3055–3071. https://doi.org/10.3390/ijms12053055
Jin Y, Wang Z, Dong A-Y, Huang Y-Q, Hao G-F, Song B-A (2021) Web repositories of natural agents promote pests and pathogenic microbes management. Brief Bioinform 22(6):bbab205. https://doi.org/10.1093/bib/bbab205
Jing R, Li N, Wang W, Liu Y (2020) An endophytic strain JK of genus Bacillus isolated from the seeds of super hybrid rice (Oryza sativa L. Shenliangyou 5814) has antagonistic activity against rice blast pathogen. Microb Pathog 147:104422. https://doi.org/10.1016/j.micpath.2020.104422
Jones KA, Burges HD (eds). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. Kluwer Academic, Dordrecht, Springer, The Netherlands; 1998. p. 411.
Kachhawa D (2017) Microorganisms as a biopesticides. J Entomol Zool Stud 5(3):468–473
Käfer S, Paraskevopoulou S, Zirkel F, Wieseke N, Donath A, Petersen M, Jones TC, Liu S, Zhou X, Middendorf M (2019) Re-assessing the diversity of negative strand RNA viruses in insects. PLoS Pathog 15(12):e1008224. https://doi.org/10.1371/journal.ppat.1008224
Kakkar A, Nizampatnam NR, Kondreddy A, Pradhan BB, Chatterjee S (2015) Xanthomonas campestris cell–cell signalling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. J Exp Bot 66(21):6697–6714. https://doi.org/10.1093/jxb/erv377
Kalha C, Singh P, Kang S, Hunjan M, Gupta V, Sharma R (2014) Entomopathogenic viruses and bacteria for insect-pest control. In: Abrol DP (ed) Integrated pest management: current concepts and ecological perspectives. Academic Press, Elsevier, San Diego, pp 225–244. https://doi.org/10.1016/B978-0-12-398529-3.00013-0
Kan J, Fang R, Jia Y (2017) Interkingdom signaling in plant-microbe interactions. Sci China Life Sci 60:785–796. https://doi.org/10.1007/s11427-017-9092-3
Kang S, Kim J, Joo G (2005) Isolation of antagonistic bacteria against Fusarium oxysporum and physicochemical properties of compost mixed with microbial formulation. Korean J Hortic Sci Technol 23(3):342–350
Kannan C, Mishra D, Rekha G, Maruthi P, Shaik H, Sundaram RM (2021) Diversity analysis of antagonistic microbes against bacterial leaf and fungal sheath blight diseases of rice. Egypt J Biol Pest Control 31(1):115. https://doi.org/10.1186/s41938-021-00462-x
Kashyap PL, Xiang X, Heiden P (2015) Chitosan nanoparticle based delivery systems for sustainable agriculture. Int J Biol Macromol 77:36–51. https://doi.org/10.1016/j.ijbiomac.2015.02.039
Kausar MA (2018) A review on respiratory allergy caused by insects. Bioinformation 14(9):540–553. https://doi.org/10.6026/97320630014540
Kawalekar JS (2013) Role of biofertilizers and biopesticides for sustainable agriculture. J Bio Innov 2(3):73–78
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
Khan MA, Ahmad W (2019) Microbes for sustainable lnsect pest management. Springer
Khater HF (2012) Prospects of botanical biopesticides in insect pest management. Pharmacologia 3(12):641–656
Khoushab F, Yamabhai M (2010) Chitin research revisited. Mar Drugs 8(7):1988–2012. https://doi.org/10.3390/md8071988
Kim J-S, Lee J, Lee C-h, Woo SY, Kang H, Seo S-G, Kim S-H (2015) Activation of pathogenesis-related genes by the rhizobacterium, Bacillus sp. JS which induces systemic resistance in tobacco plants. Plant Pathol J 31(2):195. https://doi.org/10.5423/PPJ.NT.11.2014.0122
Kirst HA (2010) The spinosyn family of insecticides: realizing the potential of natural products research. J Antibiot 63(3):101–111. https://doi.org/10.1038/ja.2010.5
Kumar S, Chandra A, Pandey K (2008) Bacillus thuringiensis (Bt) transgenic crop: an environment friendly insect-pest management strategy. J Environ Biol 29(5):641–653
Lee K, Jung J, Mo Y, Yoon Y, Kim S (2017) Isolation of antagonistic microbes for biological control of ginseng root rot. Planta Med Int Open 4(1):S1–S202. https://doi.org/10.1055/s-0037-1608502
Lin F, Mao Y, Zhao F, Idris AL, Liu Q, Zou S, Guan X, Huang T (2023) Towards sustainable green adjuvants for microbial pesticides: recent progress, upcoming challenges, and future perspectives. Microorganisms 11(2):364. https://doi.org/10.3390/microorganisms11020364
Lindsey APJ, Murugan S, Renitta RE (2020) Microbial disease management in agriculture: current status and future prospects. Biocatal Agric Biotechnol 23:101468. https://doi.org/10.1016/j.bcab.2019.101468
Liu Y, Shi J, Feng Y, Yang X, Li X, Shen Q (2013) Tobacco bacterial wilt can be biologically controlled by the application of antagonistic strains in combination with organic fertilizer. Biol Fertil Soils 49(4):447–464. https://doi.org/10.1007/s00374-012-0740-z
Liu Y, Bai F, Li T, Yan H (2018) An endophytic strain of genus Paenibacillus isolated from the fruits of Noni (Morinda citrifolia L.) has antagonistic activity against a Noni’s pathogenic strain of genus Aspergillus. Microb Pathog 125:158–163. https://doi.org/10.1016/j.micpath.2018.09.018
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42(D1):D490–D495. https://doi.org/10.1093/nar/gkt1178
Luo H, Yang J, Yang P, Li J, Huang H, Shi P, Bai Y, Wang Y, Fan Y, Yao B (2010) Gene cloning and expression of a new acidic family 7 endo-β-1, 3–1, 4-glucanase from the acidophilic fungus Bispora sp. MEY-1. Appl Microbiol Biotechnol 85:1015–1023. https://doi.org/10.1007/s00253-009-2119-0
Ma K-W, Ma W (2016) Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol Biol 91:713–725. https://doi.org/10.1007/s11103-016-0452-0
Ma K, Kwark S, Lee G (2013) Isolation and selection of antagonistic microbes for biological control of zoysiagrass large patch disease. Korean J Hortic Sci Technol 31(6):657–665
Maharana C, Padala VK, Hubballi AB, Nikhil Raj M, Paschapur A, Bhat C, Singh AK, Subbanna A (2022) Secondary metabolites of microbials as potential pesticides. In: Chakrabarti SK, Sharma S, Shah MA (eds) Sustainable management of potato pests and diseases. Springer, Singapore, pp 111–142. https://doi.org/10.1007/978-981-16-7695-6_5
Mamphogoro TP, Kamutando CN, Maboko MM, Aiyegoro OA, Babalola OO (2021) Epiphytic bacteria from sweet pepper antagonistic in vitro to Ralstonia solanacearum bd 261, a causative agent of bacterial wilt. Microorganisms 9(9):1947. https://doi.org/10.3390/microorganisms9091947
Manfo FPT, Mboe SA, Nantia EA, Ngoula F, Telefo PB, Moundipa PF, Cho-Ngwa F (2020) Evaluation of the effects of agro pesticides use on liver and kidney function in farmers from Buea, Cameroon. J Toxicol 2020:1–10. https://doi.org/10.1155/2020/2305764
Mazid S, Kalita JC, Rajkhowa RC (2011) A review on the use of biopesticides in insect pest management. Int J Sci Adv Technol 1(7):169–178
Meena RK, Mishra P (2020) Bio-pesticides for agriculture and environment sustainability. In: Kumar S, Meena RS, Jhariya MK (eds) Resources use efficiency in agriculture. Springer, Singapore, pp 85–107. https://doi.org/10.1007/978-981-15-6953-1_3
Molinari S, Leonetti P (2019) Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes. PLoS ONE 14(12):e0213230. https://doi.org/10.1371/journal.pone.0213230
Mollah MMI, Yeasmin F, Kim Y (2020) Benzylideneacetone and other phenylethylamide bacterial metabolites induce apoptosis to kill insects. J Asia Pac Entomol 23(2):449–457. https://doi.org/10.1016/j.aspen.2020.03.008
Monte E (2001) Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol 4(1):4–7. https://doi.org/10.1007/s101230100001
Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6:245–252. https://doi.org/10.1007/s10123-003-0144-x
Moore N, King L, Possee R (1987) Viruses of insects. Int J Trop Insect Sci 8(3):275–289
Mukherjee K, Vilcinskas A (2018) The entomopathogenic fungus Metarhizium robertsii communicates with the insect host Galleria mellonella during infection. Virulence 9(1):402–413. https://doi.org/10.1080/21505594.2017.1405190
Nawaz M, Mabubu JI, Hua H (2016) Current status and advancement of biopesticides: microbial and botanical pesticides. J Entomol Zool Stud 4(2):241–246
Nega A (2014) Review on concepts in biological control of plant pathogens. J Biol Agric Health 4(27):33–54
O’Brien J, Wright GD (2011) An ecological perspective of microbial secondary metabolism. Curr Opin Biotechnol 22(4):552–558. https://doi.org/10.1016/j.copbio.2011.03.010
O’Brien KP, Franjevic S, Jones J. Green chemistry and sustainable agriculture: the role of biopesticides. Advancing Green Chemistry, Charlottesville, USA; 2009.
Okunlola A, Akinrinnola O (2014) Effectiveness of botanical formulations in vegetable production and bio-diversity preservation in Ondo State, Nigeria. J Hortic for 6(1):6–13
Opender Koul OK (2012) Microbial biopesticides: opportunities and challenges. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 6:1–26. https://doi.org/10.1079/pavsnnr20116056
Ortíz-Castro R, Martínez-Trujillo M, López-bucio J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31(10):1497–1509. https://doi.org/10.1111/j.1365-3040.2008.01863.x
Palazzini J, Roncallo P, Cantoro R, Chiotta M, Yerkovich N, Palacios S, Echenique V, Torres A, Ramirez M, Karlovsky P (2018) Biocontrol of Fusarium graminearum sensu stricto, reduction of deoxynivalenol accumulation and phytohormone induction by two selected antagonists. Toxins 10(2):88. https://doi.org/10.3390/toxins10020088
Pandey A, Trivedi P, Kumar B, Palni LMS (2006) Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the indian central himalaya. Curr Microbiol 53(2):102–107. https://doi.org/10.1007/s00284-006-4590-5
Pane C, Villecco D, Campanile F, Zaccardelli M (2012) Novel strains of Bacillus, isolated from compost and compost-amended soils, as biological control agents against soil-borne phytopathogenic fungi. Biocontrol Sci Technol 22(12):1373–1388. https://doi.org/10.1080/09583157.2012.729143
Pane C, Zaccardelli M (2015) Evaluation of Bacillus strains isolated from solanaceous phylloplane for biocontrol of Alternaria early blight of tomato. Biol Control 84:11–18. https://doi.org/10.1016/j.biocontrol.2015.01.005
Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1110. https://doi.org/10.3389/fpls.2016.01110
Patel HK, Suárez-Moreno ZR, Degrassi G, Subramoni S, González JF, Venturi V (2013) Bacterial LuxR solos have evolved to respond to different molecules including signals from plants. Front Plant Sci 4:447. https://doi.org/10.3389/fpls.2013.00447
Pershakova T, Gorlov S, Lisovoy V, Mikhaylyuta L, Babakina M, Aleshin V (2021) Influence of electromagnetic fields and microbial pesticide Vitaplan on stability of apples during storage. IOP Conf Ser Earth Environ Sci 640:022053
Petrisor C, Stoian G (2017) The role of hydrolytic enzymes produced by entomopathogenic fungi in pathogenesis of insects mini review. Rom J Plant Prot 10:66–72
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
Prasannath K (2017) Plant defence-related enzymes against pathogens: a review. AGRIEAST J Agric Sci 11(1):38–48. https://doi.org/10.4038/agrieast.v11i1.33
Pucheta D, Macias AF, Navarro SR, Mayra D (2016) Mechanism of action of entomopathogenic fungi. Interciencia 156(12):2164–2171
Qiu Z, Egidi E, Liu H, Kaur S, Singh BK (2019) New frontiers in agriculture productivity: optimised microbial inoculants and in situ microbiome engineering. Biotechnol Adv 37(6):11. https://doi.org/10.1016/j.biotechadv.2019.03.010
Rae R, Iatsenko I, Witte H, Sommer RJ (2010) A subset of naturally isolated Bacillus strains show extreme virulence to the free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Environ Microbiol 12(11):3007–3021. https://doi.org/10.1111/j.1462-2920.2010.02278.x
Rakhimol KR, Thomas S, Volova T, Jayachandran K (2020) Controlled release of pesticides for sustainable agriculture. Springer, Switzerland
Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62(3):597–635. https://doi.org/10.1128/mmbr.62.3.597-635.1998
Ravensberg W (2015) Commercialisation of microbes: Present situation and future prospects. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Springer, Cham, pp 309–317. https://doi.org/10.1007/978-3-319-08575-3_32
Riedo J, Wettstein FE, Rösch A, Herzog C, Banerjee S, Büchi L, Charles R, Wächter D, Martin-Laurent F, Bucheli TD (2021) Widespread occurrence of pesticides in organically managed agricultural soils—The ghost of a conventional agricultural past? Environ Sci Technol 55(5):2919–2928. https://doi.org/10.1021/acs.est.0c06405
Rinu K, Sati P, Pandey A (2014) Trichoderma gamsii (NFCCI 2177): a newly isolated endophytic, psychrotolerant, plant growth promoting, and antagonistic fungal strain. J Basic Microbiol 54(5):408–417. https://doi.org/10.1002/jobm.201200579
Riyaz M, Mathew P, Zuber S, Rather GA (2022) Botanical pesticides for an eco-friendly and sustainable agriculture: new challenges and prospects. In: Bandh SA (ed) sustainable agriculture. Springer, Cham, pp 69–96. https://doi.org/10.1007/978-3-030-83066-3_5
Rosas-García NM, Ávalos-de-León O, Villegas-Mendoza JM, Mireles-Martínez M, Barboza-Corona J, Castañeda-Ramírez J (2014) Correlation between pr1 and pr2 gene content and virulence in Metarhizium anisopliae strains. J Microbiol Biotechnol 24(11):1495–1502. https://doi.org/10.4014/jmb.1404.04044
Ruiz B, Chávez A, Forero A, García-Huante Y, Romero A, Sánchez M, Rocha D, Sánchez B, Rodríguez-Sanoja R, Sánchez S (2010) Production of microbial secondary metabolites: regulation by the carbon source. Crit Rev Microbiol 36(2):146–167. https://doi.org/10.3109/10408410903489576
Ryu C-M, Choi HK, Lee C-H, Murphy JF, Lee J-K, Kloepper JW (2013) Modulation of quorum sensing in acylhomoserine lactone-producing or-degrading tobacco plants leads to alteration of induced systemic resistance elicited by the rhizobacterium Serratia marcescens 90–166. Plant Pathol J 29(2):182. https://doi.org/10.5423/PPJ.SI.11.2012.0173.R2
Saber WI, Ghoneem KM, Rashad YM, Al-Askar AA (2017) Trichoderma harzianum WKY1: an indole acetic acid producer for growth improvement and anthracnose disease control in sorghum. Biocontrol Sci Technol 27(5):654–676. https://doi.org/10.1080/09583157.2017.1321733
Samada LH, Tambunan USF (2020) Biopesticides as promising alternatives to chemical pesticides: a review of their current and future status. Online J Biol Sci 20:66–76
Samson R, Evans H, Latge J (1988) Atlas of entomopathogenic fungi. Springer, Berlin, Heidelberg, pp 1–187
Santamarina MP, Roselló J, Llacer R, Sanchis V (2002) Antagonistic activity of Penicillium oxalicum Corrie and Thom, Penicillium decumbens Thom and Trichoderma harzianum Rifai isolates against fungi, bacteria and insects in vitro. Rev Iberoam Micol 19(2):99–103
Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel K-H (2014) N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26(6):2708–2723. https://doi.org/10.1105/tpc.114.126763
Sesan TE, Enache E, Iacomi BM, Oprea M, Oancea F, Iacomi C (2015) Antifungal activity of some plant extracts against Botrytis cinerea Pers. in the blackcurrant crop (Ribes nigrum L.). Acta Sci Pol Hortorum Cultus 14(1):29–43
Shahid I, Rizwan M, Baig DN, Saleem RS, Malik KA, Mehnaz S (2017) Secondary metabolites production and plant growth promotion by Pseudomonas chlororaphis and P. aurantiaca strains isolated from cactus, cotton, and para grass. J Microbiol Biotechnol 27(3):480–491. https://doi.org/10.4014/jmb.1601.01021
Shahwar D, Mushtaq Z, Mushtaq H, Alqarawi AA, Park Y, Alshahrani TS, Faizan S (2023) Role of microbial inoculants as bio fertilizers for improving crop productivity: a review. 9: e16134
Sharma S, Malik P (2012) Biopesticides: types and applications. Int J Adv Pharm Biol Chem 1(4):508–515
Sharma A, Tewari R, Rana SS, Soni R, Soni SK (2016) Cellulases: classification, methods of determination and industrial applications. Appl Biochem Biotechnol 179:1346–1380. https://doi.org/10.1007/s12010-016-2070-3
Sharma A, Srivastava A, Shukla AK, Srivastava K, Srivastava AK, Saxena AK (2020) Entomopathogenic fungi: a potential source for biological control of insect pests. In: Solanki M, Kashyap P, Kumari B (eds) Phytobiomes: current insights and future vistas. Springer, Singapore, pp 225–250. https://doi.org/10.1007/978-981-15-3151-4_9
Shi J-F, Sun C-Q (2017) Isolation, identification, and biocontrol of antagonistic bacterium against Botrytis cinerea after tomato harvest. Braz J Microbiol 48:706–714. https://doi.org/10.1016/j.bjm.2017.03.002
Shrestha A, Grimm M, Ojiro I, Krumwiede J, Schikora A (2020) Impact of quorum sensing molecules on plant growth and immune system. Front Microbiol 11:1545. https://doi.org/10.3389/fmicb.2020.01545
Singh AK, Singh A, Joshi P (2016) Combined application of chitinolytic bacterium Paenibacillus sp. D1 with low doses of chemical pesticides for better control of Helicoverpa armigera. Int J Pest Manag 62(3):222–227. https://doi.org/10.1080/09670874.2016.1167267
Singh RP, Baghel RS, Reddy C, Jha B (2015) Effect of quorum sensing signals produced by seaweed-associated bacteria on carpospore liberation from Gracilaria dura. Front Plant Sci 6:117. https://doi.org/10.3389/fpls.2015.00117
Singh A, Dhiman N, Kar AK, Singh D, Purohit MP, Ghosh D, Patnaik S (2020) Advances in controlled release pesticide formulations: prospects to safer integrated pest management and sustainable agriculture. J Hazard Mater 385:121525. https://doi.org/10.1016/j.jhazmat.2019.121525
Solanki MK, Solanki AC, Rai S, Srivastava S, Kashyap BK, Divvela PK, Kumar S, Yandigeri MS, Kashyap PL, Shrivastava AK, Ali B, Khan S, Jaremko M, Qureshi KA (2022) Functional interplay between antagonistic bacteria and Rhizoctonia solani in the tomato plant rhizosphere. Front Microbiol. https://doi.org/10.3389/fmicb.2022.990850
Spadaro D, Droby S (2016) Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci Technol 47:39–49. https://doi.org/10.1016/j.tifs.2015.11.003
Steinhaus EA (1975) Disease in a minor chord. Ohio State University Press, Columbus
Tsavkelova E, Klimova SY, Cherdyntseva T, Netrusov A (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126. https://doi.org/10.1134/S0003683806020013
Twizeyimana M, Hammer PE, Gachango E, Craig K, Espejo B, Biggs MB, Kremer J, Ingham DJ (2023) Diverse environmental bacteria displaying activity against Phakopsora pachyrhizi, the cause of soybean rust. Front Plant Sci. https://doi.org/10.3389/fpls.2023.1080116
Vaghasiya MPD, Chouhan BP, Nair A (2021) Evaluation of various parameters in mass multiplication of Beauveria bassiana in modified method. Int J Environ Agric Res 7:29–34
Valero-Jiménez CA, Wiegers H, Zwaan BJ, Koenraadt CJ, van Kan JA (2016) Genes involved in virulence of the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol 133:41–49
Van Dyken SJ, Locksley RM (2018) Chitins and chitinase activity in airway diseases. J Allergy Clin Immunol 142(2):364–369. https://doi.org/10.1016/j.jaci.2018.06.017
Veliz-Vallejos DF, van Noorden GE, Yuan M, Mathesius U (2014) A Sinorhizobium meliloti-specific N-acyl homoserine lactone quorum-sensing signal increases nodule numbers in Medicago truncatula independent of autoregulation. Front Plant Sci 5:551. https://doi.org/10.3389/fpls.2014.00551
Veliz EA, Martínez-Hidalgo P, Hirsch AM (2017) Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiol 3(3):689. https://doi.org/10.3934/microbiol.2017.3.689
Verma VC, Gond SK, Kumar A, Mishra A, Kharwar RN, Gange AC (2009) Endophytic actinomycetes from Azadirachta indica A. Juss.: isolation, diversity, and anti-microbial activity. Microb Ecol 57(4):749–756. https://doi.org/10.1007/s00248-008-9450-3
Vesty EF, Whitbread AL, Needs S, Tanko W, Jones K, Halliday N, Ghaderiardakani F, Liu X, Cámara M, Coates JC (2020) Cross-kingdom signalling regulates spore germination in the moss Physcomitrella patens. Sci Rep 10(1):2614. https://doi.org/10.1038/s41598-020-59467-5
Viswanathan R, Sundar AR, Premkumari SM (2003) Mycolytic effect of extracellular enzymes of antagonistic microbes to Colletotrichum falcatum, red rot pathogen of sugarcane. World J Microbiol Biotechnol 19(9):953–959. https://doi.org/10.1023/B:WIBI.0000007329.68910.e5
Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2013) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49(4):435–446. https://doi.org/10.1007/s00374-012-0739-5
Wang X, Li Q, Sui J, Zhang J, Liu Z, Du J, Xu R, Zhou Y, Liu X (2019) Isolation and characterization of antagonistic bacteria Paenibacillus jamilae HS-26 and their effects on plant growth. Biomed Res Int. https://doi.org/10.1155/2019/3638926
Win TT, Bo B, Malec P, Khan S, Fu P (2021) Newly isolated strain of Trichoderma asperellum from disease suppressive soil is a potential bio-control agent to suppress Fusarium soil borne fungal phytopathogens. J Plant Pathol 103:549–561. https://doi.org/10.1007/s42161-021-00780-x
Woldemelak WA (2020) The major biological approaches in the integrated pest management of onion thrips, Thrips tabaci (Thysanoptera: Thripidae): a review. J Hortic Res 28:13–20
Xu F, Wu Y, Zhang C, Davis KM, Moon K, Bushin LB, Seyedsayamdost MR (2019) A genetics-free method for high-throughput discovery of cryptic microbial metabolites. Nat Chem Biol 15(2):161–168. https://doi.org/10.1038/s41589-018-0193-2
Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauahan VS, Dhaliwal HS, Saxena AK (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57. https://doi.org/10.7324/JABB.2017.50607
Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016) Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307. https://doi.org/10.1002/jobm.201500230
Yadav K, Damodaran T, Dutt K, Singh A, Muthukumar M, Rajan S, Gopal R, Sharma PC (2021) Effective biocontrol of banana fusarium wilt tropical race 4 by a Bacillus rhizobacteria strain with antagonistic secondary metabolites. Rhizosphere 18:100341. https://doi.org/10.1016/j.rhisph.2021.100341
Yang F, Zhang R, Wu X, Xu T, Ahmad S, Zhang X, Zhao J, Liu Y (2020) An endophytic strain of the genus Bacillus isolated from the seeds of maize (Zea mays L.) has antagonistic activity against maize pathogenic strains. Microb Pathog 142:104074. https://doi.org/10.1016/j.micpath.2020.104074
Yu WQ, Zheng GP, Yan FC, Liu WZ, Liu WX (2019) Paenibacillus terrae NK3-4: a potential biocontrol agent that produces β-1, 3-glucanase. Biol Control 129:92–101. https://doi.org/10.1016/j.biocontrol.2018.09.019
Zhang Y, Zhang J, Jiang X, Wang G, Luo Z, Fan Y, Wu Z, Pei Y (2010) Requirement of a mitogen-activated protein kinase for appressorium formation and penetration of insect cuticle by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 76(7):2262–2270. https://doi.org/10.1128/AEM.02246-09
Zhao Q, Zhang C, Jia Z, Huang Y, Li H, Song S (2015) Involvement of calmodulin in regulation of primary root elongation by N-3-oxo-hexanoyl homoserine lactone in Arabidopsis thaliana. Front Plant Sci 5:807. https://doi.org/10.3389/fpls.2014.00807
Zhao Q, Li M, Jia Z, Liu F, Ma H, Huang Y, Song S (2016) AtMYB44 positively regulates the enhanced elongation of primary roots induced by N-3-oxo-hexanoyl-homoserine lactone in Arabidopsis thaliana. Mol Plant Microbe Interact 29(10):774–785. https://doi.org/10.1094/MPMI-03-16-0063-R
Zhou Y, Li W, Zeng J, Shao Y (2018) Mechanisms of action of the yeast Debaryomyces nepalensis for control of the pathogen Colletotrichum gloeosporioides in mango fruit. Biol Control 123:111–119. https://doi.org/10.1016/j.biocontrol.2018.05.014
The authors declare that no funds, grants, or other support was received during the preparation of this manuscript.
Ethics approval and consent to participate
All procedures performed in studies are in accordance with the ethical standards of the institutional and/or national research committee. We further declare that no animal was harmed during this study.
Consent for publication
Informed consent was obtained from all individual participants included in the study.
All authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Negi, R., Sharma, B., Kaur, S. et al. Microbial antagonists: diversity, formulation and applications for management of pest–pathogens. Egypt J Biol Pest Control 33, 105 (2023). https://doi.org/10.1186/s41938-023-00748-2