The endophytic microorganisms have the potential to improve the yield of agricultural crops. They can be used as biological control, plant growth promoter, or bioremediators. The action of endophytes in controlling phytopathogens, insects, and weeds that harm agriculture may be the result of microbial interactions with other organisms or the production of bioactive metabolites. Also, microorganisms can have the ability to favor plant growth and convert toxic compounds present in the soil. The presence of pollutants in the substrate reduces its quality for plant development, so bioremediation also impacts agricultural production. Therefore, prospecting endophytic microorganisms with agronomic potential may provide sustainable alternatives to increase crop yield.
- biological control
- plant growth promoter
In order to apply sustainable solutions to problems related to food production, the biotechnological potential of endophytic microorganisms has been prospected in the agronomic area. The use of beneficial microorganisms in agricultural production aims for pest control, improvement of productivity and plant development, and/or recovery of ecological systems. Endophytes play a role in evolution of plant and in resistance of stresses through the production of bioactive metabolites, changes in enzyme metabolism, and gene expression related to resistance , and those beneficial effects of various endophytic genera may be the combined .
2. Biological control
Biological control of phytopathogens occurs when living microorganisms repress the development of the etiological agent in the plant . Endophytes can act inducing resistance, promoting antibiosis and/or competition in consequence of the mutualistic relation with the plant . These processes can occur independently, but the overlap of mechanisms may also happen , like is observed in the association of
The physiological definition of resistance is the delay or impediment of entry and/or subsequent activity of the pathogen in the plant . Plants have numerous and efficient defense mechanisms naturally triggered when exposed to elicitors  that can be stimulated by the endophytes presence. The plant defense mechanisms are induced after the recognition of molecular patterns associated with pathogens/microbes (PAMPs/MAMPs), or plants’ molecular patterns associated with damage (DAMPs) and effectors, by proteins or by nucleotide-binding leucine-rich repeat (NB-LRR) . Endophyte induces systemic resistance on plants providing an alert state, the priming [10, 11]. Priming plants exhibits faster and stronger responses against pathogen attacks because transcription factors and signaling proteins have already accumulated in cells. This defense induction is a consequence of molecular signaling during the establishment of plant-endophyte symbiosis . An example of the host-induced resistance by endophytes is the frequent isolation of
A reprogrammed genetic transcription occurs in plants associated with endophytes. The
The resistance induction is also related with the activity of defense enzymes, such as phenylalanine ammonia lyase, polyphenol oxidase, superoxide dismutase, peroxidase, ascorbate peroxidase, and guaiacol peroxidase.
The vast majority of endophytes are biotrophic . Therefore, it is important to consider that when colonization of the plant by biotrophic endophytes begins, the salicylic acid (SA) route activates defenses, so endophytes need to be able to suppress this defense by specific effectors. The expression of the Ca2+/calmodulin kinase enzyme is capable to suppress the pathway of SA . In addition, the possibility of recruiting gibberellic acid (GA) reduces the proportion of DELLA proteins, altering the salicylic acid and jasmonic acid (JA) signaling . The suppression of the SA stimulates JA route precursors and genes, which increases resistance to chewing insects and necrotrophic fungi and promotes susceptibility to biotrophics [10, 22]. To ensure plant protection against biotrophic fungi and sucking insects, endophytes have the ability to biosynthesize compounds responsible for antibiosis; besides they can also control these organisms through mycoparasitism and competition.
The endophytes are able to biosynthesize secondary metabolites, which are important for plant colonization processes  and are toxic to insects, pathogens , and algae . These compounds are classified as alkaloids (amines and amides; indole derivatives), steroids, terpenoids (sesquiterpenes, diterpenes, monoterpenes), isocoumarin derivatives, quinones, flavonoids, phenylpropanoids and lignans, peptides, phenol and phenolic acids, aliphatic compounds, and chlorinated metabolites . The antagonistic activity of endophytes associated with antibiosis is described for different cultures, like potato [26, 27] and turmeric rhizome .
Alkaloids are an important group of metabolites produced by endophytes; some characterized classes are ergot alkaloids, diterpene indole, pyrrolizidines, and peramine. These compounds have important biological activity (antitumor, antimicrobial), including the reduction of insect performance [10, 13]. The resistance of chickpeas (
The need for nutritional factors, like carbon, nitrogen, and iron, may also promote biological control. Direct parasitism is a fungus-fungus antagonism, in which one directly attacks another and utilizes its nutrients . This kind of control, independent of a systemic defense response, was observed with the colonization of previously endophyte-free leaves of
Competition and direct parasitism require endophyte-pathogen contact, but those microorganisms have very little to no direct contact with the plant. Because of this, contact mechanisms are not the most important biological control pathway .
3. Plant growth promoters
Endophytic bacteria promote plant growth directly or indirectly: directly, producing phytohormones or enzymes [37, 38] and indirectly, contributing to plant nutrient uptake through nitrogen fixation, phosphate solubilization, or iron transformation [39, 40]. For this, the inoculant competes with an adapted indigenous microbiota; therefore, for the colonization of plant, some bacterial characteristics are important, such as motility and polysaccharide production [41, 42, 43, 44].
Ethylene and indole-3-acetic acid (IAA) are phytohormones that are involved in almost all aspects of plant growth and development, from seed germination to shoot growth, and they control the response of the plant to stress [45, 46]. Plant growth is promoted by reducing ethylene levels and increasing IAA. Biotic and abiotic stresses result in increased ethylene production in plants, leading to inhibition of root elongation, lateral root development, and root hair formation. Plant-associated microorganisms can increase root growth and budding of plants by reducing ethylene levels . The endophytic bacteria can produce an enzyme called 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which hydrolyzes ACC, an ethylene immediate precursor, relieving stress and improving the growth of plants under disturbed conditions [42, 48, 49]. An inoculum from
Endophytic bacteria can benefit the host by producing cytokines and gibberellins. Corn endophytic bacteria,
Nitrogen is the most important nutrient for plant growth and productivity. Although abundant in the atmosphere, it is not available to plants. For this, it requires to be transformed by a biological nitrogen fixation (BNF) process in which N2 is converted to NH3 by bacteria expressing nitrogenase, such as
Phosphorus is an important micronutrient for the enzymatic reactions of plant physiological processes . Although present in large quantities, most of the soil phosphorus is insoluble and therefore unavailable to the plant. In addition, almost 75% of phosphorus applied as fertilizer forms complexes in the soil, which prevents its absorption by the vegetable . The endophytic bacteria can increase soil phosphorus availability to plants by solubilizing precipitated phosphates through mechanisms of acidification, chelation, ion exchange, and the production of organic acids . They can also increase the availability of phosphorus in the soil by secreting acid phosphatase, which can mineralize organic phosphorus . Furthermore, endophytic bacteria can prevent phosphate adsorption and fixation under phosphate-limiting conditions and assimilate solubilized phosphorus . Studies show that endophytic populations of cactus, strawberry, sunflower, soybean, and other legumes have the ability to solubilize phosphate [62, 63, 64]. A study examined the role of phosphate-solubilizing endophytic bacteria in cactus cultivation and observed that inoculated plants grew well without added nutrients and that their growth was comparable to fertilized plants. This indicates that endophytic bacteria provide the limiting nutrient to seedlings .
Iron is a component of proteins that control physiological processes such as respiration and transpiration . Generally, it occurs in the ferric insoluble form, unavailable to the plants. The endophytic bacteria produce iron chelators called siderophores that may bind to insoluble ferric ions allowing this nutrient uptake by plants [66, 67, 68]. The action of bacterial-produced siderophores has already been correlated with the growth of cultivars such as corn, including shoot and root biomass , and on tomato development in hydroponic crops .
The ability to promote plant growth by endophytic bacteria may be influenced by host genotype . However, many endophytic bacteria can have a wide range of hosts, such as
The prompt development of agriculture has made it possible to increase the food supply all over the world. However, the intensification of agricultural activities brought serious environmental impacts, which not only affect food security but also have impacts on socioeconomic aspects. These impacts comprise contribution to air pollution, impacts on land, waste of water, loss of biological and ecological diversity, and perturbation of global biogeochemical cycles. The pollutants generated by agricultural activities can affect the global or local scale. An example of global-scale agro-environmental problem is the increase in atmospheric concentrations of the greenhouse gasses (GHG) and carbon dioxide (CO2) through deforestation and nitrous oxide (N2O) arising from crop production. Agriculture is the largest water consumer and the main source of nitrate, ammonia, and phosphate pollution. These pollutants affect the local scale; some examples are the salinization of irrigated lands and the buildup of nitrate fertilizer residues in groundwater and surface water [77, 78, 79, 80, 81].
Most of the negative environmental impacts generated by the intensification of agricultural activities can be reduced or prevented . The use of new technological approaches, physicochemical- or biological-based, could remove pollutants from nature. Biological-based methods are preferred due to the low cost and because they are less harmful to the environment. Atlas and Pramer  defined the term bioremediation as “the use of biological agents to reclaim soils and waters polluted by substances hazardous to human health and/or the environment.” In other words, bioremediation is a biological-based method involving the use of living organisms, such as plants or microorganisms (bacteria, fungi, and algae), to remove pollutants from the environment .
Degradation of pollutants by a microorganism demands favorable conditions of nutrients, temperature, pH, and oxygen. Bacteria and fungi are commonly used in bioremediation strategies, because they are ubiquitous and capable in withstanding different environmental conditions, so they can be used for a broader range of application. There are two main mechanisms of bioremediation: biosorption and bioaccumulation. Biosorption involves sequestration of pollutants thought binding onto surfaces, such as the cell wall. Bioaccumulation involves transport and accumulation of pollutants in the cells and, in some cases, the transformation of pollutants into less harmful compounds [78, 83]. The degradation of target pollutants can also be achieved by employing nonliving subcellular entities of biological origin as bioremediators . To overcome the instability due to the rapid decline in the inoculated cell amount during its competition with indigenous microorganisms, some authors have proposed solutions. For example, a new strategy for the efficient removal of phenylurea herbicides from contaminated soil uses transgenic plants. Transgenic
Endophytes can remove pollutants by employing either the biosorption or the bioaccumulation mechanisms [83, 86, 87, 88, 89, 90]. They have the ability of decreasing and/or removing contaminants from soil, water, sediments, and air. Endophytic fungi have a great potential to manage toxic pollutants; many studies report those fungi to clean up environmental pollutants, such as white rot fungi like
Heavy metals are one example of pollutants generated by agricultural activity that bioremediators can remove. The use of some pesticides and fertilizers can introduce into the environment copper (Cu), and some insecticide and herbicides can contain lead (Pb). Fungi have emerged as potential biocatalysts to access heavy metals and transform them into less toxic compounds [92, 96]. Endophytic fungi isolated of
Phytoremediation is the process that uses plants associated with microorganisms to remediate contaminants from soil, sludge, sediments, wastewater, and groundwater [92, 96]. Plants naturally harbor endophytes that may have natural tolerance and adaptation toward the pollutants. Studies explored the potential of using endophytes associated with plants for removal of pollutants in this process of phytoremediation [86, 88, 96, 99]. Plants growing in metal-contaminated soils accumulate the pollutant consumed directly or indirectly by humans and animals [100, 101]. Besides the human risk, polluted soil slows plant growth and reduces the biomass accumulation, compromising some crop productivity [102, 103]. Endophytic fungi resistant to different metals, including cadmium, lead, zinc (Zn), chromium, manganese (Mn), and cobalt (Co), are associated with plant species present in contaminated sites, indicating that these microorganisms have metal bioremediation potential [83, 97, 98, 99, 104, 105]. Chromium toxicity influences a number of processes that can lead to low yield. The accumulation of Cr from industrial activities in soil is a serious threat to some crops [106, 107, 108]. To minimize the Cr effects from contaminated soils, it is possible to use plants that harbor endophytic fungi that act as bioremediators. In experiments, strains of
Studies reported the use of
Similar to metal pollutants, triphenylmethane (TPM) dyes are water-soluble organic compounds extensively used in industrial processes and have adverse effects on living organisms. TPM is phytotoxic for several cultivated plants, such as
Endophytic microorganisms are inestimable natural resources for solving problems in different areas such as human health, veterinary, industrial and ecological systems, and agronomy. In contrast to current agricultural practices that degrade systems and produce food with high concentrations of various contaminants, endophytes are a sustainable alternative to increase crop productivity. For this, they can be exploited by the ability to control pests, to promote plant growth, and by the bioremediation potential. This is possible because these microorganisms are able to induce resistance mechanisms in the host, release compounds with biological activity, compete for space and nutrients with pathogens, provide nutritional elements present in the soil, stimulate the production of phytohormones and cytokines, and neutralize the presence of pollutants in the system. Ultimately, bioprospecting and the use of endophytes in agriculture are a viable alternative to the need of increased food production with quality and sustainably.
The authors would like to acknowledge CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), Brazil.