Re-vitalizing of endophytic microbes for soil health management and plant protection

Abstract

Soil health management and increase crop productivity are challenging issues for researchers and scientists. Many research publications have given multiple technological solutions for improving soil health and crop productivity but main problem is sustainability of those technologies under field condition and different agro-climatic zone. Due to the random industrialization, deforestation, mining and other environmental factor reduce soil fertility and human health. Many alternative options e.g., crop rotation, green manuring, integrated farming, biofertilizer (plant-growth-promoting microorganism, microbial consortium of rhizosphere soils), and vermicomposting are available for adapting and improving the soil heath and crop productivity by farmers. Recent trends of new research dimension for sustainable agriculture, endophytic microbes and its consortium is one of the better alternative for increasing crop productivity, soil health and fertility management. However, current trends are focuses on the endophytic microbes, which are present mostly in all plant species. Endophytic microbes are isolated from plant parts—root, shoot, leaf, flower and seeds which have very potential ability of plant growth promotion and bio-controlling agent for enhancing plant growth and development. Mostly plant endophytes showed multi-dimensional (synergistic, mutualistic, symbiotic etc.) interactions within the host plants. It promotes the plant growth, protects from pathogen, and induces resistance against biotic and abiotic environmental stresses, and improves the soil fertility. Till date, most of the scientific research has been done on assuming that interaction of plant endophytes with the host is similar like the plant-growth-promoting microorganism (PGPM). It would be very interesting to explore the functional properties of plant endophytes to modulate the essential gene expression during biotic and abiotic stresses. Endophytes have the ability to induce the soil fertility by improving soil essential nutrient, enzymatic activity and influence the other physiochemical property. In this study, we have discussed details about functional properties of plant endophytes and their mechanism for enhancing plant productivity and soil health and fertility management under climate-resilient agricultural practices. Our main objective is to promote and explore the beneficial plant endophytes for enhancing sustainable agricultural productivity.

Introduction

Plants are mega species harboring wide diversity of microbes in their different parts such as seed, root, stems, leaf, pollens and flowers, which altogether is known as the plant microbiome (Zhang et al. 2017; Mukherjee et al. 2020). Plant-associated microbes play critical roles in crop yield and plant health through different direct and indirect mechanisms (Mukherjee et al. 2020; Trivedi et al. 2020b). Endophytes are a unique group of plant microbiome that reside asymptomatically inside plant parts and tissues having a symbiotic relationship (Wilson 1995). The group constitutes bacteria, fungi, and archaea that inhabit the plant tissue as a whole or a part of their lifecycle (Hassan 2017; Harrison and Griffin 2020). The majority of plant endophytes belong to genera of Bacillus, Pseudomonas, Streptomyces, Burkholderia, Klebsiella, Enterobacter, Penicillium, Aspergillus, Alternaria, and Fusarium (Hassan 2017; Khan et al. 2017a, b; Singh et al. 2017a; Mukherjee et al. 2020, 2021). The features of interest of all these endophytic microbial genera are provided in Table 1. However, from newer studies, it has been demonstrated that there is more diversity of plant endophytes which are subject to change according to the host and environmental factors (Kawasaki et al. 2016; Liu et al. 2020). With that being said, some microbial groups are present universally regardless of the environment and are part of the plant’s core microbiome (Hamonts et al. 2018). This core group of microbes has co-evolved with the host plant species and is inherited through generations (Song et al. 2020).

Table 1.

List of major endophytic microbial genera isolated from plants and their features of interest

Endophyte	Host plants	Isolation point(s)	Features of interest	Reference(s)
Alternaria spp.	Salvia miltiorrhiza, Solanum nigrum, and Brassica napus	Root, shoot, and leaf	Increased biomass, chlorophyll content, and secondary metabolite production Abiotic stress tolerance	Khan et al. (2015b) Shi et al. (2017) Zhou et al. (2018)
Aspergillus spp.	Zea mays, Euphorbia indica, Soybean, and Sunflower	Root and leaf	Production of secondary metabolites for plant growth Stress tolerance	Hamayun et al. (2018, 2019) Mehmood et al. (2019)
Bacillus spp.	Zea mays, Saccharum officinarum, Aloe vera, Cucurbits, and Oryza sativa, Cicer arietinum	Seed, root, stem, and leaf	Inhibition of phytopathogens Plant growth promotion	Akinsanya et al. (2015) Gond et al. (2015a) Khalaf and Raizada (2018) Kumar et al. (2020) Mukherjee et al. (2020) Wang et al. (2020b)
Enterobacter spp.	Cicer arietinum, Zea mays, and Sorghum sudanense	Seed	Improved productivity Phyto-stabilization of heavy metals Plant growth promotion	Li et al. (2016) Ullah et al. (2020) Mowafy et al. (2021) Mukherjee et al. (2020)
Fusarium spp.	Brassica napus, Oxalis corniculate, and Glycine max	Root	Abiotic stress tolerance Mineral solubilization Biomass production Secondary metabolite production	Radhakrishnan et al. (2015) Shi et al. (2017) Bilal et al. (2018)
Klebsiella spp.	Zea mays, Saccharum officinarum, and Triticum aestivum	Root	Enhance growth and yield N fixation Stress tolerance	Lin et al. (2015) Zhang et al. (2017) Mowafy et al. (2021)
Penicillium spp.	Triticum aestivum and Capsicum annum	Root	Resistance against abiotic stresses Production of IAA Nutrient mineralization	Ikram et al. (2018) Oses-pedraza et al. (2020)
Pseudomonas spp.	Pisum sativum, Oryza sativa, Achyranthes aspera, Zea mays Brassica napus, and Cicer arietinum	Leaf, root, and seed	Mineral solubilization N fixation Defense against phytopathogens Stress tolerance	Otieno et al. (2015) Devi et al. (2017) Lally et al. (2017) Pham et al. (2017) Sandhya et al. (2017) Mukherjee et al. (2020)
Streptomyces spp.	Solanum lycopersicum, Glycine max, and Sorghum	Root and stem	Plant growth promotion Biocontrol Production of active secondary metabolites	Goudjal et al. (2016) Patel et al. (2018) Liu et al. (2019)

Plants in natural communities preserve their symbiotic associations with endophytes that help in growth promotion and protection against different stresses (Rodriguez et al. 2009; Johnston-Monje et al. 2016; Trivedi et al. 2020b). The actinorhizal and rhizobial endophytes enhance nutrient availability especially nitrogen through the process of biological nitrogen fixation (BNF) (Pawlowski and Demchenko 2012) in specialized root structures called nodules (Coba de la Peña et al. 2017). The mycorrhizal endophytic fungal families also help in nutrient acquisition to plant especially phosphorous. Many of the endophytes produce siderophores which increase iron availability to plants (Mukherjee et al. 2020). The enzymatic activities of endophytes mobilize the soil nutrients making them readily available to plants (Behie and Bidochaka 2013; White et al. 2019). In a fashion similar to human gut microbes, the endophytes improve plant health by protecting against phytopathogens. They have the ability to induce systemic resistance and upregulate defense gene expression in the host plant and suppress the growth and fitness of phytopathogens (Hardoim et al. 2015; Irizarry and White 2017; White et al. 2018). Endophytes start modulation of defense gene in host plant right from the seedling stage to maturation (Ongena and Jacques 2008; Gond et al. 2015a, b). Systemic resistance is induced against a broad spectrum of phytopathogen through jasmonic acid, salicylic acid, and ethylene pathways and the production of pathogenesis-related proteins (Bastias et al. 2017). The growth suppression of phytopathogen by endophytes is through the production of antimicrobial compounds such as pyrrolnitrin, pyoleutirin, 2, 4-diacetylphloroglucinol, phenazine-1-carboxylic acid, and hydrogen cyanide (Mousa et al. 2016; Bastias et al. 2017). The different underlying mechanisms of plant endophytes in the improvement of plant and soil health are represented in Fig. 1.

Fig. 1.

Diagrammatic representation of plant endophytes’ mechanisms involved in improvement of plant and soil health

Soil is a mystic resource on this planet harboring both biological and chemical entities. Agricultural soil in particular linked to human health, production economics, water and soil quality, and food safety and security either directly and/or indirectly (Karlen et al. 2019). Healthy soils are the backbone of agricultural productivity as it provides support to healthy plant growth and development. The quantity and quality of about 95% of our food depend on soil functional properties (Kemper and Lal 2017; Brevik et al. 2018, 2020) which indirectly dictates human and animal nourishment as nutrient deficiency of food grains cause many human diseases. It has been known through various studies that the application of organic fertilizers improves soil quality and health by stimulating microbial population and diversity in the soil (Jannoura et al. 2014; Verma et al. 2014; Mukherjee et al. 2019). However, both organic and inorganic fertilizers are applied in common agricultural practices for better crop production (Naab et al. 2017; Mukherjee et al. 2021), in which the proportion of the latter is quite higher. Inorganic fertilizers can be replaced with the use of endophytes as a sustainable approach in modern agricultural practices (Kumar et al. 2020). Endophytes possess the ability to solubilize micro and macronutrients in soil without hampering the natural properties and microbial community of the soil. They also play an important role in soil mineral cycling and the removal of pollutants from soil (He et al. 2020; Liu et al. 2020), due to which they are deemed to be a better alternative. Hence, our main aim of this review is to present the functional properties of endophytes keeping in view the current demand of their application as bioinoculants for improvement of soil health, plant productivity, and protection against phytopathogens under a sustainable approach.

Screening and molecular characterization of endophytic microbes from plant material

Before going for screening and molecular characterization, one should have to attain a pure culture of endophytic microbe. Endophytes can be isolated by different plating methods in respective culture media from different plant parts (root, shoot, leaf, flower, fruits, and seeds) after sterilization of that particular part with 1% sodium hypochlorite solution for 1 min and 70% ethanol followed by washing two to three times with sterilized distilled water (Mukherjee et al. 2020). Pure culture of the respective isolated endophyte can be then done by single spore culture for fungi and single colony culture for bacteria. DNA should be extracted from this pure culture of isolated bacteria and fungi as the next step for molecular characterization using polymerase chain reaction (PCR) amplification of conserved regions namely: 16S rRNA or 18S rRNA for bacterial endophytes and ITS for fungal endophytes followed by sequencing. The sequence obtained must be aligned using the Basic Local Alignment Search Tool (BLAST) in National Center for Biotechnology Information (NCBI) for obtaining a similarity index to match the microbial organism from the database. For screening of biochemical and plant growth promotion properties, pure culture of microbes should be grown in respective liquid media. A diagrammatic representation of isolation, identification, and characterization of endophytes from different plant parts is given in Fig. 2. These screening results should be used for the development of potential single inoculants and consortiums. The endophytic microbial consortium is, however, more effective plant-growth-promoting and biocontrol agent for enabling better plant growth under abiotic and biotic stresses (Singh et al. 2018).

Fig. 2.

Flowchart of isolation, identification, and characterization of plant endophytes from different parts

Endophytes for agricultural soil health

Almost all the plants have their world of endophytic microbes which are non-aggressive and ubiquitous (Schulz and Boyle 2006). Once colonized, endophytes stimulate the growth and physiology of host plants and properties of soil through various direct and indirect mechanisms (Singh et al. 2018; Mukherjee et al. 2020; Chouhan et al. 2021). Nitrogen fixation, phosphate solubilization, siderophore production, exopolysaccharide (EPS) secretion, exoenzymes’ production, and biocontrol activities are some of the functional properties of endophytes (Jasim et al. 2014; Mukherjee et al. 2019, 2020) that aid restoration of soil health and fertility. The exoenzymes produced by endophytes specifically have the capacity of solubilizing essential plant nutrients from their insoluble for to soluble ones (Puri et al. 2020). These exoenzymes also constitute organic acids which lead to lowering of soil pH (Verma et al. 2017). The changes in pH additionally inhibit the activities of phytopathogenic microbes and also alter the growth of some invasive plants thereby increasing nutrient availability (Shahrtash and Brown 2021). Many endophytes synthesize soil invertase, urease, and soil alkaline phosphatases which directly modulate soil organic carbon (SOC), soil nitrogen, and microbial biomass (Hou et al. 2020). Endophytes also degrade plant debris present in soil having macromolecules like lignin, pectin, oligosaccharides, cellulose, hemicellulose, lipids, and proteins with the help of exoenzymes (Wang and Dai 2011; Uzma et al. 2016) into their simpler forms. This adds to the nutrient status of soil, enhancing soil quality, nutrient cycling, and soil micro-environment. Puente et al. (2009) reported in a study on endophytic bacteria associated with Pachycereus pringlei produces organic acids which help in weathering and transformation of minerals under in vitro conditions.

Plant–microbe interaction is a complex system that involves a vast array of microbes, the plant, and the soil. The interaction not only affects the physiology of plant but also regulate soil flora and fauna, soil microbial respiration rate, soil health, and nutrient cycling (Chaparro et al. 2012). Plants communicate with the soil microbial community through chemical signals constituting proteins, fatty acids, flavonoids, sugars, aliphatic acids, and amino acids which create a unique environment for the survival of soil microbes. These secreted chemical signals establish interaction with endophytes and neighboring plants leading to the formation of soil aggregates which improves soil porosity by designing the soil structure (Miller and Jastrow 2000). A wide range of endophytic bacteria and fungi viz. Bacillus, Arthrobacter, Enterobacter, Clostridium, Pseudomonas, Microbacterium, Mucor, Microsphaeropsis, Phoma, Alternaria, Steganosporium, and Aspergillus have been reported resistant to metals (Guo et al. 2010; Li et al. 2012). These endophytes can thus be helpful in removing heavy metal toxicity from the soil. Moreover, different studies have suggested that endophytes play a crucial role in the phytoremediation of organic contaminants such as hydrocarbons as well. Most of the soil contaminants are toxic for plants and cannot be degraded by them alone. This problem can be alleviated through plant–endophytes interaction (Li et al. 2012). Endophytes reduce phytotoxicity due to soil contaminants by increasing their immobilization, chelation, and degradation. For this, they secrete organic acids of low molecular weight, siderophores, and enzymes. Siderophores can bind efficiently with iron (Fe), zinc (Zn), cadmium (Cd), gallium (Ga), aluminum (Al), and lead (Pb) to form a stable complex which increases their soluble concentration (Rajkumar et al. 2010).

Many of the endophytic bacteria and fungi are antagonistic and are drawing special attention as an alternative for the management of soil-borne diseases with minimal environmental impact and soil pollution. These antagonistic endophytes control the population of soil-borne phytopathogens through different mechanisms namely: parasitism, competition, production of lytic enzymes, and antibiosis (De Silva et al. 2019). EPS produced by endophytes plays important role in plant–endophyte interactions and also exhibit many biological functions. EPS of endophytic origin have antioxidative, antiallergic, and prebiotic properties (Liu et al. 2017) along with metal complexation ability (Liu et al. 2021). Thus, EPS can be helpful in regulating the population of soil phytopathogens and reducing the bioaccessibility of heavy metals. From the above-presented statements, it can be very well concluded that augmentation of soil with specific endophyte or endophytic consortium can be significantly supportive in restoring soil health. A list of identified endophytes that have studied in the management of soil health, their host plant(s), and features of interest is provided in Table 2.

Table 2.

Endophytes in improvement of soil health

Endophytes	Host plant	Features of interest in soil health management	Reference(s)
Neotyphodium coenophialum	Festuca arundinacea	Enhancement of soil carbon and nitrogen	Franzluebbers et al. (1999)
Neotyphodium occultans	Lolium multiflorum	Modulation of soil catabolic activity Enhancement of soil microbial (fungal) population and their activities	Casas et al. (2011)
Bacillus spp.	Solanum nigrum	Hyperaccumulation of metal (Cu, Cd, and Cr) in soil	Guo et al. (2010)
Burkholderia cepacia	Zea mays	Phytoremediation of organic contaminants (toluene and phenols)	Wang et al. (2010)
Phomopsis liquidambari	Bischofia polycarpam	Promotion of litter mass degradation Alleviation of soil nitrogen concentration	Chen et al. (2013)
Phialocephala fortinii	Asparagus officinalis	Degradation of organic compounds Improvement of nutrient cycling in the soil	Narisawa (2017)
	Chamaecyparis obtusa and Rubus spp.		Surono and Narisawa (2017)
Enterobacter spp., Microbacterium arborescens, and Pantoea stewartii	Leptochloa fusca and Brachiaria mutica	Enhancement in the uptake, translocation, accumulation, and phyto-stabilization of heavy metal (Cr) in contaminated soil	Ahsan et al. (2018)
Phomopsis liquidambari	Oryza sativa	Increment in decomposition of straw and total soil nitrogen	Sun et al. (2019)
Epichloë gansuensis	Achnatherum inebrians	Improvement of soil fertility and soil nutrients availability by inducing soil enzyme activity such as invertase, alkaline phosphatase and urease	Hou et al. (2020)
Serratia spp., and Arthrobacter spp.	Brassica juncea	Improvement in organic matter content of soil Phytoremediation of vanadium contaminated soil Improvement of plant growth and soil health	Wang et al. (2020a)
Phomopsis liquidambaris	Acharis hypogaea	Alleviation of soil health through improved root exudation Improvement of soil carbon metabolism Increment of rhizospheric bacterial community	Xie et al. (2020)
Acrocalymma vagum and Paraboeremia putaminum	Glycyrrhiza uralensis	Ensure plant growth under drought stress conditions by structuring soil microbiome and maintaining soil water content, soil organic matter, and nutrient availability	He et al. (2021)

Endophytes for sustainable plant protection and its stress management

Many appreciative efforts have been made to study the role of endophytes in a plant’s defense system against different stresses. Application of different endophytes can assist in the adjustment of plant’s tolerance to various abiotic and biotic stresses (Wani et al. 2015). Biofertilization, biocontrol, and phytostimulation are the three mechanisms through which endophytes help plants in combating unfavorable conditions. It is a well established fact that plants regulate their defense system through phytohormonal signaling and its crosstalk. The phytohormones induce innate immunity in a plant for protection against different phytopathogens. As per Waqas et al. (2015), endophytic fungus Penicillium citrinum provided protection to Sclerotium rolfsii (phytopathogen) by increasing the level of jasmonic acid (JA) and salicylic acid (SA)-mediated hormone signaling. In addition, they also reported that another endophytic species of the same fungus, P. formosus, increased plant growth by lowering the level of phytohormones associated with stress signaling namely abscisic acid (ABA) and JA during heat stress. They also regulated other phytohormones levels and produced different secondary metabolites for alleviating the same stress. Similarly in another study, endophytic Aspergillus niger increased the level of gibberellins and auxin to promote plant growth under stress (Lubna et al. 2018). During stress conditions, the level of ethylene increases in plants causing inhibition in root length, root hair, and lateral root development. During such instances, endophytes produce an enzyme known as 1-aminocyclopropane-1-carboxylate (ACC) deaminase which functions in lowering ethylene levels and promoting plant growth (Santoyo et al. 2016). Sun et al. (2009), compared ACC deaminase production capacity in mutated and wild type endophytic Burkholderia phytofirmans and their impact in canola. They observed that the mutated strain was unable to promote the growth of canola seedlings while the wild type strain showed remarkable growth promotion. The result ascertains that endophytes affect the growth and development of plants through ACC deaminase enzyme production.

Following a long course of coexistence, endophytes have developed the ability to mimic host plant metabolism and produce effective bioactive compounds similar to their host in vitro as a result of close contact and horizontal gene transfer (Wang et al. 2010). Endophytes produce a vast array of secondary metabolites constituting antibiotics, hydrolytic enzymes, toxins, and volatile organic compounds (VOCs) that play a significant role in alleviating a plant’s defense system for mitigation of stresses (Afzal et al. 2019). Hence, endophytes are also considered as an emerging source of novel bioactive compounds (Singh et al. 2017a). Endophytic Streptomyces spp. provides resistance in chickpea by enhancing the level of defense-related compounds such as phenols and flavonoids (Singh and Gaur 2017). Kang et al. (2018) observed an increased level of nematicidal compounds such as 4-vinyl phenol, L-methionine, palmitic acid, and piperine in plants colonized by Bacillus simplex, inhibited soybean cyst nematode. Co-inoculation of endophytic fungi Beauveria bassiana and mycorrhizae increases terpenoids levels in tomato plant leaves, reducing the foliar feeding by herbivores (Shrivastava et al. 2015). Endophytes also activate the defense pathway by modulating systemic acquired resistance in the plant. Endophyte actinobacteria isolated from the wheat plant induced the genes of SAR such as PR-1 and PR-5 genes and PDF-1.2 and Hel genes to regulate JA and ethylene pathway and confers resistance against several fungal phytopathogens in A. thaliana (Conn et al. 2008). A similar study was also reported by Gond et al. (2015a), that endophytic bacteria, Bacillus amyloliquefaciens activate JA-dependent defense pathway by increasing the expression of PR-1 and PR-10 genes against the attack of fungal pathogens and enhanced the growth and development of maize plant. Endophytes also protect plants from oxidation through excessive pesticidal application by producing antioxidants (Jan et al. 2020).

Quorum sensing (QS) is responsible for communication between host and pathogenic microbes as well as other bacterial symbionts via signaling molecules like N-acyl-homoserine lactone (AHL). Quorum sensing is a density-dependent gene expression in bacteria. As the density increases, the signaling also increases and all cells act somewhat like multicellular organisms (Rosenblueth and Martínez-Romero 2006). The regulation of gene expression in phytopathogenic bacteria needs to produce antibiotics, virulence factors, and exoenzymes to degrade cell walls and to infect plants (Von Bodman et al. 2003). Plant under stress conditions produce signal molecules or mimic the bacterial QS to manipulate the QS-regulated behavior of phytopathogenic bacteria (Bauer and Mathesius 2004). Endophytic bacteria isolated from Cannabis sativa were investigated to disrupt cell-to-cell quorum sensing signals in Chromobacterium violaceum and were proved to act as biocontrol agents for bacterial phytopathogens (Kusari et al. 2014). In the same way, endophytic isolates of phylum Actinobacteria isolated from Phaseolus vulgaris provide resistance from phytopathogenic Gram-positive bacteria disruption of QS (Lopes et al. 2015). A detailed list of endophytes that have been studied in plant protection and stress management and their respective features of interest is provided in Table 3.

Table 3.

Endophytes in plant health and defense

Endophytes	Host plant	Features of interest	Reference(s)
Neotyphodium coenophialum	Festuca arundinacea	Alteration of root activity and mineral transport from root to shoot under phosphate limited condition	Malinowski et al. (2000)
Penicillium verruculosum RS7PF	Potentilla fulgens L.	Promotion of seed germination in green-gram and chickpea by IAA modulation	Bhagobaty et al. (2010)
Acinetobacter johnsonii	Beta vulgaris	Production of IAA for plant growth and development Production of phosphatase enzyme for enhanced nutrient absorption by host plant	Shi et al. (2011)
Bacillus weihenstephanensis, Serratia marcescens, and Cornyebacterium minutissimum	Solanum lycopersicum and Capsicum annum	Antagonism against wilt-causing bacteria Ralstonia solanacearum Production of secondary metabolites for increased plant growth	Amaresan et al. (2012)
Sporosarcina aquimarina	Avicennia marina	Promotion of plants growth by IAA production Enhancement of nutrient availability by production of siderophore and phosphatase	Janarthine and Eganathan (2012)
Piriformospora indica	Hordeum vulgare L.	Increased grain yield and shoot biomass under low temperature condition	Murphy et al. (2014)
Trichoderma brevicompactum	Allium sativum	Production of bioactive compound (trichodermin) Antifungal activity against fungal phytopathogens	Shentu et al. (2014)
Bacillus spp.	Zea mays	Inhibition of phytopathogens through antifungal lipopeptide Regulation of genes associated to production of pathogenesis-related (PR) proteins	Gond et al. (2015b)
Pantoea spp. and Paenibacillus spp.	Triticum aestivum	Biocontrol activity against F. graminearum by biofilm formation Modulation of plant growth through production of IAA, siderophore, and phosphatase	Herrera et al. (2016)
Pseudomonas aeruginosa, Bacillus spp., Enterobacter spp., Shinella spp.	Saccharum officinarum	Promotion of plant growth by IAA production, phosphorous solubilization, siderophore production, and biocontrol activity	Taulé et al. (2016) Pirhadi et al. (2018)
Bacillus subtilis	Cicer arietinum L.	Improvement in plant growth under salinity condition Protection against root rot causing fungal phytopathogen (F. solani)	Egamberdieva et al. (2017)
Stenotrophomonas maltophilia, Prototheora geniculata, Bacillus amyloliquefaciens, Stenotrophomonas maltophilia, and Bacillus licheniformis	Solanum lycopersicum	Production of IAA and phosphatase for increased plant growth and development	Abdallah et al. (2018)
Hypocrea lixii F3ST1	Allium cepa	Boosting of plant immunity and reducing damage caused by Iris yellow spot virus and its vector Thrips tabaci	Muvea et al. (2018)
Curtobacterium spp., Methylobacterium spp., Microbacterium spp., and Bacillus amyloliquefaciens	Urochloa ramosa L.	Inhibition of fungal phytopathogens by lipopeptide Promotion of seedling growth Regulation of expression of defense-related genes	Verma (2018)
Acinetobacter calcoaceticus, Enterobacter cloacae, and Bacillus cereus	Glycine max	Promotion of plant growth through IAA and siderophore production Fixation of atmospheric nitrogen Phosphate solubilization	Zhao et al. (2018)
Acinetobacter baumannii	Capsicum annum	Induction of secondary metabolites production having antioxidant property	Monowar et al. (2019)
Pseudomonas aeruginosa	Cucumis sativus	Suppression of damping off phytopathogen (Pythium aphanidermatum) Plant growth promotion activity	Priyanka et al. (2019)
Bacillus subtilis, Bacillus pumilus, and Klebsiella pneumoniae	Oryzae sativa	Antagonism against fungal phytopathogens	Kumar et al. (2020)
Enterobacter cloacae, Enterobacter spp., Bacillus subtilis, Pseudomonas aeruginosa, Bacillus subtilis, Enterobacter spp., Enterobacter hormaechei, Staphylococcus equorum, Pantoea spp., and Mixta intestinalis	Cicer arietinum L.	Production of plant growth-promoting components (IAA, mineral solubilization, NH3 production, siderophore production, protease activity) Antagonism against phytopathogens	Mukherjee et al. (2020)

Endophytes for sustainable management of environmental pollution

Detoxification of heavy metals (HMs)

Rapid industrialization and urbanization without proper planning is adversely affecting the environment through contamination or pollution. One such pollution is the increasing deposition of HMs and pesticides in soil which is has a direct impact on crop production and human health. HMs and their isotopes are categorized under elemental pollutants while residual pesticides are categorized under organic pollutants. As per WHO (1996), the maximum permissible limit of HMs is (0.8, 50, 36, 100, 85, and 35 mg kg⁻¹) in soils and (0.02, 0.6, 1, 1.3, 2, and 10 mg kg⁻¹) in plant with respect of Cd, Zn, Cu, Cr, Pb, and Ni. However, the amount of these HMs is ever-increasing in the soil and the plants leading to several fatal human diseases. Endophytes perform the remediation process more effectively than rhizospheric microbes because of their close contact with host plants, since plants growing in HM contaminated soil naturally employ endophytes with HM-degrading genes. Siciliano et al. (2001) support this fact as they reported that endophytes perform degradation of nitroaromatic compounds more effectively than the rhizospheric microbial community. This was due to the presence of nitro-aromatics degradation genes being prevalent in endophytes than other soil microbes. Microbes and/or genetically engineered microbes have the capacity of reducing soil contamination (Pilon Smits et al. 1999). Research studies have reported that endophytes such as A. calcoaceticus, B. cereus, P. putida, Trichoderma spp., Cladosporium spp., P. polymyxa, P. fluorescens, Paecilomyces spp., B. subtilis, Rhizobium spp., E. pisciphila, R. rubrum, P. agglomerans, Aspergillus spp., Mucor spp., Microsphaeropsis spp., Alternaria spp., Phoma spp., Peyronellaea spp., Steganosporium spp., and Azotobacter spp. have the ability to produce different extracellular oxidase enzymes such as manganese peroxidase, laccase, and lithium peroxidase that helps to degrade various phenolics substance and it directly linked to the remediation process (Ongena and Jacques 2008; Nandy et al. 2020). The removal of HMs is mostly done through absorption, transformation, phytoextraction, hyperaccumulation, and translocation. The organic pollutants are mostly removed by the process of mineralization, degradation, and detoxification (Meagher 2000). A list of endophytes studied for HMs detoxification and their respective host(s) is provided in Table 4.

Table 4.

Endophytes in bioremediation of heavy metals (HMs)

Host plant	Microbes	HMs bioremediated	Reference(s)
Salix variegate Franch	Chromosporium spp., Fusarium spp., and Gonatobotrysi spp.	Cd	An et al. (2015)
Solanum lycopersicum L.	P. janthinellum LK5	Al	Khan et al. (2015a)
Populus spp.	Serenpidita vermifera P04	Cd, Zn, Pb, and Cu	Lacercat-Didier et al. (2016)
Dysphania ambrosioides L.	Plectosphaerella spp., Cladosporium spp., and Verticillium spp.	Pb and Zn	Li et al. (2016)
	Penicillium spp. FT2G59 and P. columnaris FT2G7
Imperata cylindrica L. and Bothriochloa ischaemum L.	Leotiomycetes and Pezizomycetes	Pb and Cd	Tong et al. (2017)
Solanum nigrum L.	Colletotrichum spp., Alternaria spp., and Fusarium spp.	Cd	Khan et al. 2017a, b
	F. tricinctum, and A. alternata	Cd
Brassica napus L.	Fusarium spp., Penicillium spp., and Alternaria spp.	Cd and Pb	Shi et al. (2017)
Zea mays	Westerdykella spp.	Hg	Pietro-Souza et al. (2020)

Detoxification of pesticides

Injudicious use of fertilizers and pesticides has caused many physical and physiological discomforts in plants as well as in animals. Discolouration, necrosis, and deformation are the major physical impact of excessive pesticides on plants (Geetha 2019) which have significant effects on physiological and biochemical processes (Chaudhary et al. 2020; Giménez-Moolhuyzen et al. 2020). The pesticides accumulate in soil mostly through the process of leaching which leads to deterioration of soil fertility and soil microbial community. Endophytic microbes play an important role to minimize and degrade inside the plant body. A study on bark, xylem tissue, and leaves of tea plants showed that there are no significant changes in community structure and number of endophytic colonies in the phyllosphere after pesticide treatment (Win et al. 2021). Seed treatment with pesticides resulted in alteration of rhizosphere fungal and bacterial community in maize plant but leaf fungal endophytic colonies remain unaffected (Nettles et al. 2016). Another study on the community-level effect of different concentrations of pesticide N-(3,5-dichlorophenyl) succinimide on Nicotiana tabacum phyllosphere showed that there was no significant impact on alpha and beta diversity of beneficial endophytic bacterial community, viz., Alphaproteobacteria, Gammaproteobacteria, Sphingomonas, and Pseudomonas (Chen et al. 2021). All these reports suggest that leaf endophytes are more resistant to pesticides and are well-suited candidates for degradation agrochemicals.

There are a number of studies on endophytes revealing that these microbes establish a symbiotic relationship with their host and secrete enzymes to metabolize and detoxify various pesticides. For example, an endophytic Pseudomonas spp. possesses gene encoding organophosphate hydrolase enzyme which is responsible for degradation of 97% of organophosphate pesticide such as chlorpyrifos (Barman et al. 2014a, b). A group of endophytes having a symbiotic relationship with P. fugax (one of the major winter weeds in the oilseed rape field in China) helped to promote resistance from quizalofop-p-ethyl, an acetyl CoA carboxylase-inhibiting herbicide (Liu et al. 2020). In another study, it was shown that endophytic bacteria Pantoea ananatis Sd-1 degrade carbaryl by secreting hydrolytic enzyme carbohydrate esterase (Yao et al. 2020). This enzyme esterase is a major enzyme in hydrolysis of other pesticidal compounds as well namely: organochlorines, pyrethroids, and carbamates (Sharma et al. 2018). Since endophytes exhibit significant growth and multiplication rate within plant tissue, they can be used as a potential tool for the bioremediation of environmental contaminants such as xenobiotics and pesticides (Gupta et al. 2020; Win et al. 2021). Moreover, plant–endophyte interaction not only enhances phytoextraction or phytoremediation of environmental pollutants but they perform an excellent job for plant growth promotion even under biotic and abiotic stress conditions (Waller et al. 2005; Becerra-Castro et al. 2013). A detailed list of endophytes studied in the bioremediation of pesticides and their respective host(s) and properties is provided in Table 5.

Table 5.

Endophytes in bioremediation of pesticides

Endophytes	Host plant	Pesticide bioremediated	Properties	Reference(s)
Sphingomonas spp.	Cytisus striatus	Hexachlorocyclohexane	Phytoremediation of HCH Enhancement of plant growth	Becerra-Castro et al. (2013)
Pseudomonas spp.	Balloon flower	Chlorpyrifos	Synthesis of organophosphate hydrolase enzyme	Barman et al. (2014a, b)
	Polypogon fugax	Quizalofop-p-ethyl	Degradation of acetyl-CoA carboxylase-inhibiting herbicide	Liu et al. (2020)
Rhizobium leguminosarum	Pisum sativum	Kitazin	Production of plant growth-promoting bioactive compounds to enhance plant growth under pesticide stress condition	Shahid et al. (2018)
Alphaproteobacteria, Gammaproteobacteria, Sphingomonas, and Pseudomonas spp.	Nicotiana tabacum	N-(3,5-Dichlorophenyl) succinimide	Negative responders of broad-spectrum pesticide treatments	Chen et al. (2020)
Pantoea ananatis	Oryza sativa	Carbaryl	Secretion of carbohydrate esterase to hydrolyze carbaryl	Yao et al. (2020)

Endophytes for human health

Endophytes are a very precious source of secondary metabolites of which many are antioxidant, antimicrobial, and anticancerous. They are just like a treasure house of bioactive molecules that needs to be explored. Many of these bioactive molecules can be used for the management of human diseases either directly or after transformation (Devi and Prabakaran 2014; Gouda et al. 2016). The trait of producing bioactive molecules have been incorporated in them through the transfer of genetic information from higher plants during evolution as explained earlier. The classical example of this fact is taxol-producing endophyte Metarhizium anisopliae isolated from the bark of Taxus spp., which is a very important life-saving anticancer agent (Zhang et al. 2009). Going by the classical example, endophytes associated with medicinal plants can be a very eminent source of bioactive molecules and can be utilized for producing natural drugs (Singh and Dubey 2015). Several bioactive compounds constituting vinblastine, paclitaxel, camptothecin, hypericin, etc. are already produced at a commercial scale from the endophytes isolated from their respective plants and are of pharmaceutical importance (Nicoletti and Fiorentino 2015). Endophytes are also gaining the limelight for human health because many studies suggest that novel bioactive molecules produced by them are important for combating antibiotic resistance by human pathogenic microbes (Fadiji and Babalola 2020).

Endophytes are also a good source of antioxidant compounds that are now deemed to be a potential alternative for the prevention and treatment of human diseases linked with reactive oxygen species (ROS). Thus, diseases such as diabetes, hypertension, cancer, Alzheimer, ischemia, and Parkinson can be treated with the help of antioxidants derived from endophytes (Mishra et al. 2014). Many prevalent human deficiency diseases can be overcome by taking that particular nutrient through diet. Plants form a major part of the diet and their biofortification with nutrients can help in providing the deficient nutrient to the human population naturally as a replacement of chemical supplements. Endophytes can be an integral part of this concept as well, since, many of the reports have proved that endophytic microbes associated to crop also helps in biofortification (Singh et al. 2017b; Trivedi et al. 2020a). The underlying mechanisms in crop biofortification by endophytes are improvement of nutrient absorption, direct synthesis and release of micronutrients, and induction of micronutrient synthesis in plants (Ku et al. 2019). The list of potential use of endophytes for human health also continues to grow with the advancements in science.

Conclusions

Excessive use of synthetic fertilizers and pesticides and changing environment has led to unfertile agricultural lands causing a major problem in feeding the growing population. The inevitable concern arising due to this is enhancing the crop productivity under shrinking land and minimization of chemical inputs. Hence, we have provided some critical insights about an emerging alternative of utilizing the plant endophytic microbiome for combating the concern. Endophytes are significantly influential and are providing us with the opportunity to overcome the global problem of agricultural productivity. Augmentation of indigenous and effective beneficial endophytes has the potential to bring consequential positive impacts on the current agriculture scenario by improving soil and yield quality. Endophytes have more potential than other rhizosphere microbes as they can be inoculated in the same plant species from which they are isolated and can easily colonize inside the plant body to provide sustainable crop productivity and food security under different environmental stresses. A consortium of endophytic microbes can be more effective as climate-resilient biofertilizers and biocontrol agents. In addition, the consortium can be a powerful approach for boosting plant growth and productivity along with the maintenance of the soil microbial community. The approach is environment friendly, ecologically sound, and socially acceptable. However, the studies on the effects of endophytic microbial consortium are very limited and should be explored further in combination with plant-growth-promoting microbes (PGPMs) for boosting the productivity in agricultural crops and improvement of soil health under different environmental conditions.

Author contributions

AM contributed to the preparation of the manuscript, its formatting and collection of data for writing and preparing figures. MMR, GKC and JKV contributed to creating figures and editing the manuscript. SB, GKC and SY contributed to the collection of data for preparing the tables. JPV contributed to the design, idea, final editing, and revision of the whole manuscript.

Declarations

Conflict of interest

On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.