Abstract
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.
Keywords
- endophyte
- agriculture
- biological control
- plant growth promoter
- inoculant
- bioremediator
1. Introduction
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 [1], and those beneficial effects of various endophytic genera may be the combined [2].
2. Biological control
Biological control of phytopathogens occurs when living microorganisms repress the development of the etiological agent in the plant [3]. Endophytes can act inducing resistance, promoting antibiosis and/or competition in consequence of the mutualistic relation with the plant [4]. These processes can occur independently, but the overlap of mechanisms may also happen [5], 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 [7]. Plants have numerous and efficient defense mechanisms naturally triggered when exposed to elicitors [8] 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) [9]. 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 [10]. 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 [22]. 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 [23]. In addition, the possibility of recruiting gibberellic acid (GA) reduces the proportion of DELLA proteins, altering the salicylic acid and jasmonic acid (JA) signaling [24]. 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 [2] and are toxic to insects, pathogens [10], and algae [25]. 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 [25]. The antagonistic activity of endophytes associated with antibiosis is described for different cultures, like potato [26, 27] and turmeric rhizome [28].
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 [31]. 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 [4].
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 [47]. 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 [57]. 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 [58]. 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 [59]. They can also increase the availability of phosphorus in the soil by secreting acid phosphatase, which can mineralize organic phosphorus [60]. Furthermore, endophytic bacteria can prevent phosphate adsorption and fixation under phosphate-limiting conditions and assimilate solubilized phosphorus [61]. 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 [65].
Iron is a component of proteins that control physiological processes such as respiration and transpiration [66]. 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 [69], and on tomato development in hydroponic crops [70].
The ability to promote plant growth by endophytic bacteria may be influenced by host genotype [71]. However, many endophytic bacteria can have a wide range of hosts, such as
4. Bioremediators
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 [77]. 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 [82] 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 [83].
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 [84]. 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
5. Conclusion
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.
Acknowledgments
The authors would like to acknowledge CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), Brazil.
References
- 1.
Yuan Z, Zhang C, Lin F. Role of diverse non-systemic fungal endophytes in plant performance and response to stress: Progress and approaches. Journal of Plant Growth Regulation. 2010; 29 :116-126. DOI: 10.1007/s00344-009-9112-9 - 2.
Rosenblueth M, Martínez-Romero E. Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions. 2006; 19 :827-837. DOI: 10.1094/MPMI-19-0827 - 3.
Heimpel GE, Mills N, editors. Biological Control—Ecology and Applications. 1st ed. Cambridge: Cambridge University Press; 2017. DOI: 10.1017/9781139029117 - 4.
Card S, Johnson L, Teasdale S, Caradus J. Deciphering endophyte behaviour: The link between endophyte biology and efficacious biological control agents. FEMS Microbiology Ecology. 2016; 92 (8):1-19. DOI: 10.1093/femsec/fiw114 - 5.
Latz MAC, Jensen B, Collinge DB, Jørgensen HJL. Endophytic fungi as biocontrol agents: Elucidating mechanisms in disease suppression. Plant Ecology & Diversity. 2018; 11 :555-567. DOI: 10.1080/17550874.2018.1534146 - 6.
Jaber LR, Alananbeh KM. Fungal entomopathogens as endophytes reduce several species of Fusarium causing crown and root rot in sweet pepper (Capsicum annuum L.). Biological Control. 2018;126 :117-126. DOI: 10.1016/j.biocontrol.2018.08.007 - 7.
Walters D, Newton A, Lyon G. Induced Resistance for Plant Defence—A Sustainable Approach to Crop Protection. Oxford: Blackwell Publishing; 2007. p. 272 - 8.
Agrios GN. Plant Pathology. 5th ed. San Diego: Elsevier Academic Press; 2005. p. 952 - 9.
Jones JDG, Dangl JL. The plant immune system. Nature. 2006; 444 :323-329. DOI: nature05286 - 10.
Bastias DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE. Epichloë fungal endophytes and plant defenses: Not just alkaloids. Trend in Plant Science. 2017; 22 (11):939-948. DOI: 10.1016/j.tplants.2017.08.005 - 11.
Iason GR, Taylor J, Helfer S. Community-based biotic effects as determinants of tree resistance to pests and pathogens. Forest Ecology and Management. 2018; 417 :301-312. DOI: 10.1016/j.foreco.2018.01.037 - 12.
Araújo WL, Marcon J, Maccheroni W Jr, Van Elsas JD, Van Vuurde JW, Azevedo JL. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Applied and Environmental Microbiology. 2002;68 :4906-4914. DOI: 10.1128/aem.68.10.4906-4914.2002 - 13.
Bastias DA, Ueno AC, Assefh CRM, Alvarez AE, Young CA, Gundel PE. Metabolism or behavior: Explaining the performance of aphids on alkaloid-producing fungal endophytes in annual ryegrass ( Lolium multiflorum ). Oecologia. 2017;185 :245-256. DOI: 10.1007/s00442-017-3940-2 - 14.
Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, et al. Systemic and local modulation of plant responses by Piriformospora indica and relatedSebacinales species. Journal of Plant Physiology. 2008;165 :60-70. DOI: 10.1016/j.jplph.2007.05.017 - 15.
Yedidia I, Benhamou N, Kapulnik Y, Chet I. Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiology and Biochemistry. 2000;38 :863-873. DOI: 10.1016/S0981-9428(00)01198-0 - 16.
Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, et al. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology. 2014; 5 :479. DOI: 10.3389/fmicb.2014.00479 - 17.
Ji SH, Gururani MA, Chun SC. Expression Analysis of Rice Pathogenesis-related Proteins Involved in Stress Response and Endophytic Colonization Properties of gfp-tagged Bacillus subtilis CB-R05. Applied Biochemistry and Biotechnology. 2014;174 :231-341. DOI: 10.1007/s12010-014-1047-3 - 18.
Liu D, Chen L, Zhu X, Wang Y, Xuan Y, Liu X, et al. Klebsiella pneumoniae SnebYK mediates resistance againstHeterodera glycines and promotes soybean growth. Frontiers in Microbiology. 2018;9 :1134. DOI: 10.3389/fmicb.2018.01134 - 19.
Martinuz A, Schouten A, Sikora RA. Systemically induced resistance and microbial competitive exclusion: Implications on biological control. Phytopathology. 2012; 102 :260-266. DOI: 10.1094/PHYTO-04-11-0120 - 20.
Cabanás CGL, Schilirò E, Valverde-Corredor A, Mercado-Blanco J. The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Frontiers in Microbiology. 2014;5 . DOI: 10.3389/fmicb.2014.00427 - 21.
Siddiqui IA, Shaukat SS. Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: Importance of bacterial secondary metabolite, 2,4-diacetylpholoroglucinol. Soil Biology and Biochemistry. 2003;35 :1615-1623. DOI: 10.1016/j.soilbio.2003.08.006 - 22.
Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, et al. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungusPiriformospora indica . Plant Physiology. 2011;156 :726-740. DOI: 10.1104/pp.111.176446 - 23.
Molitor A, Kogel KH. Induced resistance triggered by Piriformospora indica . Plant Signaling and Behavior. 2009;4 :215-216. DOI: 10.4161/psb.4.3.7814 - 24.
Cosme M, Lu J, Erb M, Stout MJ, Franken P, Wurst S. A fungal endophytes helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling. New Phytologist. 2016; 211 :1065-1076. DOI: 10.1111/nph.13957 - 25.
Tan RX, Zou WX. Endophytes: A rich source of functional metabolites. Natural Products Reports. 2001; 18 :448-459. DOI: 10.1039/b100918o - 26.
Sessitsch A, Reitter B, Berg G. Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Canadian Journal of Microbiology. 2004; 50 :239-249. DOI: 10.1139/w03-118 - 27.
Sturz AV, Kimpinski J. Endoroot bacteria derived from marigolds ( Tagetes spp.) can decrease soil population densities of root-lesion nematodes in the potato root zone. Plant and Soil. 2004;262 :241-249. DOI: 10.1023/B:PLSO.0000037046.86670.a3 - 28.
Vinayarani G, Prakash HS. Fungal endophytes of turmeric ( Curcuma longa L.) and their biocontrol potential against pathogensPythium aphanidermatum andRhizoctonia solani . World Journal of Microbiology and Biotechnology. 2018;34 :9-17. DOI: 10.1007/s11274-018-2431-x - 29.
Singh SP, Gaur R. Endophytic Streptomyces spp. underscore induction of defense regulatory genes and confers resistance againstSclerotium rolfsii in Chickpea. Biological Control. 2017;104 :44-56. DOI: 10.1016/j.biocontrol.2016.10.011 - 30.
Kang W, Zhu X, Wang Y, Chen L, Duan Y. Transcriptomic and metabolomic analyses reveal that bacteria promote plant defense during infection of soybean cyst nematode in soybean. BMC Plant Biology. 2018; 18 :86. DOI: 10.1186/s12870-018-1302-9 - 31.
Viterbo A, Horwitz BA. Mycoparasitism. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular of Filamentous Fungi. Washington: ASM Press; 2010. pp. 676-677. DOI: 10.1128/9781555816636.ch42 - 32.
Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, et al. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences. 2003; 100 :15649-15654. DOI: 10.1073/pnas.2533483100 - 33.
Souza JT, Bailey BA, Pomella AWV, Erbe EF, Murphy CA, Bae G, et al. Colonization of cacao seedlings by Trichoderma stromaticum , a mycoparasite of the witches’ broom pathogen, and its influence on plant growth and resistance. Biological Control. 2008;46 :36-45. DOI: 10.1016/j.biocontrol.2008.01.010 - 34.
Amira MB, Lopez D, Mohamed AT, Khouaja A, Chaar H, Fumanal B, et al. Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrollingFusarium solani causal agent of root rot disease in olive trees. Biological Control. 2017;110 :70-78. DOI: 10.1016/j.biocontrol.2017.04.008 - 35.
Preto G, Martins F, Pereira JA, Baptista P. Fungal community in olive fruits of cultivars with different susceptibilities to anthracnose and selection of isolates to be used as biocontrol agents. Biological Control. 2017; 110 :1-9. DOI: 10.1016/j.biocontrol.2017.03.011 - 36.
Ribeiro AS, Polonio JC, Costa AT, Santos CM, Rhoden SA, Azevedo JL, et al. Bioprospection of culturable endophytic fungi associated with the ornamental plant Pachystachys lutea . Current Microbiology. 2018;75 :588-596. DOI: 10.1007/s00284-017-1421-9 - 37.
Glick BR. The enhancement of plant growth by free living bacteria. Canadian Journal of Microbiology. 1995; 41 :109-117. DOI: 10.1139/m95-015 - 38.
Madhaiyan M, Suresh Reddy BV, Anandham R, et al. Plant growth–promoting Methylobacterium induces defense responses in groundnut (Arachis hypogaea L.) compared with rot pathogens. Current Microbiology. 2006;53 :270. DOI: 10.1007/s00284-005-0452-9 - 39.
Wakelin SA, Warren RA, Harvey PR, et al. Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biology and Fertility of Soils. 2004;40 :36-43. DOI: 10.1007/s00374-004-0750-6 - 40.
Rasouli-Sadaghiani M, Malakouti MJ, Khavazi K, Miransari M. Siderophore efficacy of fluorescent pseudomonades affecting labeled iron (59Fe) uptake by wheat ( Triticum aestivum L.) genotypes differing in Fe efficiency. In: Miransari M, editor. Use of Microbes for the Alleviation of Soil Stresses. New York: Springer; 2014. pp. 121-132. DOI: 10.1007/978-1-4939-0721-2_7 - 41.
Berninger T, Mitter B, Preininger C. The smaller, the better? The size effect of alginate beads carrying plant growth-promoting bacteria for seed coating. Journal of Microencapsulation. 2016; 33 :127-136. DOI: 10.3109/02652048.2015.1134690 - 42.
Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR. Plant growth-promoting bacterial endophytes. Microbiological Research. 2016; 183 :92-99. DOI: 10.1016/j.micres.2015.11.008 - 43.
Shahzad R, Khan AL, Bilal S, Asaf S, Lee IJ. Plant growth-promoting endophytic bacteria versus pathogenic infections: An example of Bacillus amyloliquefaciens RWL-1 andFusarium oxysporum f. sp.lycopersici in tomato. PeerJ. 2017;5 :e3107. DOI: 10.7717/peerj.3107 - 44.
Liffourrena AS, Lucchesi GI. Alginate-perlite encapsulated Pseudomonas putida A (ATCC 12633) cells: Preparation, characterization and potential use as plant inoculants. Journal of Biotechnology. 2018;278 :28-33. DOI: 10.1016/j.jbiotec.2018.04.019 - 45.
Woodward AW, Bartel B. Auxin: Regulation, action, and interaction. Annals of Botany. 2005; 95 :707-735. DOI: 10.1093/aob/mci083 - 46.
Sun L, Wang X, Li Y. Increased plant growth and copper uptake of host and non-host plants by metal-resistant and plant growth-promoting endophytic bactéria. International Journal of Phytoremediation. 2016; 18 :494-501. DOI: 10.1080/15226514.2015.1115962 - 47.
Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B. Promotion of plant growth by bacterial ACC deaminase. Critical Reviews in Plant Sciences. 2007; 26 :227-242. DOI: 10.1080/07352680701572966 - 48.
Sun Y, Cheng Z, Glick BR. The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiology Letters. 2009;296 :131-136. DOI: 10.1111/j.1574-6968.2009.01625.x - 49.
Nikolic B, Schwab H, Sessitsch A. Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene ( acdS ) operon of an uncultured bacterial endophyte colonizingSolanum tuberosum L. Archives of Microbiology. 2011;193 :665. DOI: 10.1007/s00203-011-0703-z - 50.
Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews. 2007; 31 :425-448. DOI: 10.1111/j.1574-6976.2007.00072.x - 51.
Cohena AC, Travaglia CN, Bottini R, Piccoli PN. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany. 2009;87 :462-487. DOI: 10.1139/B09-023 - 52.
Bhore SJ, Ravichantar N, Loh SY. Screening of endophytic bacteria isolated from leaves of Sambung Nyawa Gynura procumbens Lour Merr. for cytokinin-like compounds. Bioinformation. 2010;5 :191-197. DOI: 10.6026/97320630005191 - 53.
Scherling C, Ulrich K, Ewald D, Weckwerth W. A metabolic signature of the beneficial interaction of the endophyte Paenibacillus sp. isolate and in vitro–grown poplar plants revealed by metabolomics. APS Publications. 2009;22 :1032-1037. DOI: 10.1094/MPMI-22-8-1032 - 54.
Singh A. Soil salinization and waterlogging: A threat to environment and agricultural sustainability. Ecological Indicators. 2015; 57 :128-130. DOI: 10.1016/j.ecolind.2015.04.027 - 55.
Ivleva NB, Groat J, Staub JM, Stephens M. Expression of active subunit of nitrogenase via integration into plant organelle genome. PLoS One. 2016; 11 (8):e0160951. DOI: 10.1371/journal.pone.0160951 - 56.
Hurek T, Reinhold-Hurek B. Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. Journal of Biotechnology. 2003;106 :169-178. DOI: 10.1016/j.jbiotec.2003.07.010 - 57.
Ahemad M. Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: A review. 3 Biotech. 2015; 5 :111-121. DOI: 10.1007/s13205-014-0206-0 - 58.
Ezawa T, Smith SE, Smith FA. P metabolism and transport in AM fungi. Plant and Soil. 2002; 224 :221-230. DOI: 10.1023/A:102025832 - 59.
Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D. Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiology Letters. 2000; 182 :291-296. DOI: 10.1111/j.1574-6968.2000.tb08910.x - 60.
Van Der Heijden MG, Bardgett RD, Van Straalen NM. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters. 2008; 11 :296-310. DOI: 10.1111/j.1461-0248.2007.01139.x - 61.
Khan KS, Joergensen RG. Changes in microbial biomass and P fractions in biogenic household waste compost amended with inorganic P fertilizers. Bioresource Technology. 2009; 100 :303-309. DOI: 10.1016/j.biortech.2008.06.002 - 62.
Kuklinsky-Sobral J, Araújo WL, Mendes R, et al. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Plant and Soil. 2005; 273 :91-99. DOI: 10.1007/s11104-004-6894-1 - 63.
Dias AC, Costa FE, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, et al. Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World Journal of Microbiology and Biotechnology. 2009; 25 :189-195. DOI: 10.1007/s11274-008-9878-0 - 64.
Puente ME, Li CY, Bashan Y. Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environmental and Experimental Botany. 2009; 66 :402-408. DOI: 10.1016/j.envexpbot.2009.04.007 - 65.
Puente ME, Li CY, Bashan Y. Rock-degrading endophytic bacteria in cacti. Environmental and Experimental Botany. 2009; 66 :389-401. DOI: 10.1016/j.envexpbot.2009.04.010 - 66.
Ma Y, Rajkumar M, Zhang C, Freitas H. Beneficial role of bacterial endophytes in heavy metal phytoremediation. Journal of Environmental Management. 2016; 174 :14-25. DOI: 10.1016/j.jenvman.2016.02.047 - 67.
Rajkumar M, Ae N, Freitas H. Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere. 2009; 77 :153-160. DOI: 10.1016/j.chemosphere.2009.06.047 - 68.
Crowley DE, Römheld V, Marschner H, et al. Root-microbial effects on plant iron uptake from siderophores and phytosiderophores. Plant and Soil. 1992; 142 :1-7. DOI: 10.1007/BF00010169 - 69.
Marques AP, Pires C, Moreira H, Rangel AO, Castro PM. Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biology and Biochemistry. 2010;42 :1229-1235. DOI: 10.1016/j.soilbio.2010.04.014 - 70.
Radzki W, Mañero FG, Algar E, García JL, García-Villaraco A, Solano BR. Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek. 2013; 104 :321-330. DOI: 10.1007/s10482-013-9954-9 - 71.
Long HH, Schmidt DD, Baldwin IT. Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS One. 2008; 3 :e2702. DOI: 10.1371/journal.pone.0002702 - 72.
Pillay V, Nowak J. Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato ( Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Canadian Journal of Microbiology. 1997;43 :354-361. DOI: 10.1139/m97-049 - 73.
Sessitsch A, Coenye T, Sturz A, Vandamme P, Barka EA, Salles J, et al. Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. International Journal of Systematic and Evolutionary Microbiology. 2005;55 :1187-1192. DOI: 10.1099/ijs.0.63149-0 - 74.
Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B. Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. MBio. 2015;6 :e00621-e00615. DOI: 10.1128/mBio.00621-15 - 75.
Trognitz F, Scherwinski K, Fekete A, Schmidt S, Eberl L, Rodewald J, et al. Interaction between potato and the endophyte Burkholderia phytofirmans . In: Abwehrstrategien gegen biotische Schaderreger Züchtung von Hackfrüchten und Sonderkulturen. Tagungsband der 59. Jahrestagung der Vereinigung der Pflanzenzüchter und Saatgutkaufleute Österreichs; 25-27 November 2008; Raumberg-Gumpenstein. Austria. 2008. pp. 63-66 - 76.
Dong Z, Canny MJ, McCully ME, Roboredo MR, Cabadilla CF, Ortega E, et al. A nitrogen-fixing endophyte of sugarcane stems (a new role for the apoplast). Plant Physiology. 1994; 105 :1139-1147. DOI: 10.1104/pp.105.4.1139 - 77.
Bruinsma J. World Agriculture: Towards 2015/2030. London: Routledge; 2003 - 78.
Henis Y. Bioremediation in agriculture: Dream or reality? In: Rosen D, Tel-Or E, Hadar Y, Chen Y, editors. Modern Agriculture and the Environment: Proceedings of an International Conference, held in Rehovot, Israel, 2-6 October 1994, under the auspices of the Faculty of Agriculture, the Hebrew University of Jerusalem. Dordrecht: Springer Netherlands; 1997. pp. 481-489 - 79.
Parris K. Impact of agriculture on water pollution in OECD countries: Recent trends and future prospects. International Journal of Water Resources Development. 2011; 27 :33-52. DOI: 10.1080/07900627.2010.531898 - 80.
Tilman D. Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proceedings of the National Academy of Sciences. 1999; 96 :5995-6000. DOI: 10.1073/pnas.96.11.5995 - 81.
Yu J, Wu J. The Sustainability of agricultural development in China: The agriculture–environment nexus. Sustainability. 2018; 10 :1776. DOI: 10.3390/su10061776 - 82.
Atlas RM, Pramer D. Focus on bioremediatison. ASM News. 1990; 56 :352-354 - 83.
Sim CSF, Chen SH, Ting ASY. Endophytes: Emerging tools for the bioremediation of pollutants. In: Bharagava RN, Chowdhary P, editors. Emerging and Eco-Friendly Approaches for Waste Management. Singapore: Springer Singapore; 2019. pp. 189-217 - 84.
Zaccaria M, Dawson W, Cristiglio V, Reverberi M, Ratcliff LE, Nakajima T, et al. Designing a bioremediator: Mechanistic models guide cellular and molecular specialization. Current Opinion in Biotechnology. 2020; 62 :98-105. DOI: 10.1016/j.copbio.2019.09.006 - 85.
Yan X, Huang J, Xu X, Chen D, Xie X, Tao Q , et al. Enhanced and complete removal of phenylurea herbicides by combinational transgenic plant-microbe remediation. Applied and Environmental Microbiology. 2018; 84 :e00273-e00218. DOI: 10.1128/AEM.00273-18 - 86.
Anyasi RO, Atagana HI. Endophyte: Understanding the microbes and its applications. Pakistan Journal of Biological Sciences. 2019; 22 :154-167. DOI: 10.3923/pjbs.2019.154.167 - 87.
Manzotti A, Jørgensen HJL, Collinge DB, Jensen B. Phytohormones in plant-endophyte interactions: Investigating the role of these compounds in the recruitment of tomato root fungal endophytes. Plant Biology. 2017; 9 :89-105. DOI: 10.1007/978-3-319-65897-1_6 - 88.
Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, et al. Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal. 2008; 2 :404-416. DOI: 10.1038/ismej.2007.106 - 89.
Tonial F, Maia BHLNS, Gomes-Figueiredo JA, Sobottka AM, Bertol CD, Nepel A, et al. Influence of culturing conditions on bioprospecting and the antimicrobial potential of endophytic fungi from Schinus terebinthifolius . Current Microbiology. 2016;72 :173-183. DOI: 10.1007/s00284-015-0929-0 - 90.
Savi DC, Aluizio R, Glienke C. Brazilian plants: An unexplored source of endophytes as producers of active metabolites. Planta Medica. 2019; 85 :619-636. DOI: 10.1055/a-0847-1532 - 91.
Gadd GM. Geomycology: Biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research. 2007; 111 :3-49. DOI: 10.1016/j.mycres.2006.12.001 - 92.
Krishnamurthy YL, Naik BS. Endophytic fungi bioremediation. In: Endophytes: Crop Productivity and Protection. Switzerland: Springer Nature Switzerland AG; 2017. pp. 47-60 - 93.
Stępniewska Z, Kuźniar A. Endophytic microorganisms—Promising applications in bioremediation of greenhouse gases. Applied Microbiology and Biotechnology. 2013; 97 :9589-9596. DOI: 10.1007/s00253-013-5235-9 - 94.
Dinler BS, Antoniou C, Fotopoulos V. Interplay between GST and nitric oxide in the early response of soybean ( Glycine max L.) plants to salinity stress. Journal of Plant Physiology. 2014;171 :1740-1747. DOI: 10.1016/j.jplph.2014.07.026 - 95.
Hamayun M, Hussain A, Khan SA, Kim H-Y, Khan AL, Waqas M, et al. Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt affected soybean. Frontiers in Microbiology. 2017;8 :686. DOI: 10.3389/fmicb.2017.00686 - 96.
Dixit R, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, et al. Bioremediation of heavy metals from soil and aquatic environment: An overview of principles and criteria of fundamental processes. Sustainability. 2015; 7 :2189-2212. DOI: 10.3390/su7022189 - 97.
Deng Z, Zhang R, Shi Y, La H, Tan H, Cao L. Characterization of Cd-, Pb-, Zn-resistant endophytic Lasiodiplodia sp. MXSF31 from metal accumulatingPortulaca oleracea and its potential in promoting the growth of rape in metal-contaminated soils. Environmental Science and Pollution Research. 2014;21 :2346-2357. DOI: 10.1007/s11356-013-2163-2 - 98.
Sim CSF, Tan WS, Ting ASY. Endophytes from Phragmites for metal removal: Evaluating their metal tolerance, adaptive tolerance behaviour and biosorption efficacy. Desalination and Water Treatment. 2016;57 :6959-6966. DOI: 10.1080/19443994.2015.1013507 - 99.
Fu X-Y, Zhao W, Xiong A-S, Tian Y-S, Zhu B, Peng R-H, et al. Phytoremediation of triphenylmethane dyes by overexpressing a Citrobacter sp. triphenylmethane reductase in transgenic Arabidopsis. Applied Microbiology and Biotechnology. 2013;97 :1799-1806. DOI: 10.1007/s00253-012-4106-0 - 100.
Wang S, Shi X. Molecular mechanisms of metal toxicity and carcinogenesis. In: Shi X, Castranova V, Vallyathan V, Perry WG, editors. Molecular Mechanisms of Metal Toxicity and Carcinogenesis. Boston, MA: Springer US; 2001. pp. 3-9 - 101.
Clemens S, Ma JF. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review of Plant Biology. 2016; 67 :489-512. DOI: 10.1146/annurev-arplant-043015-11230 - 102.
Bibi S, Hussain A, Hamayun M, Rahman H, Iqbal A, Shah M, et al. Bioremediation of hexavalent chromium by endophytic fungi; safe and improved production of Lactuca sativa L. Chemosphere. 2018;211 :653-663. DOI: 10.1016/j.chemosphere.2018.07.197 - 103.
Zahoor M, Irshad M, Rahman H, Qasim M, Afridi SG, Qadir M, et al. Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophyticMucor sp. MHR-7. Ecotoxicology and Environmental Safety. 2017;142 :139-149. DOI: 10.1016/j.ecoenv.2017.04.005 - 104.
Sun L, Cao X, Li M, Zhang X, Li X, Cui Z. Enhanced bioremediation of lead-contaminated soil by Solanum nigrum L. withMucor circinelloides . Environmental Science and Pollution Research. 2017;24 :9681-9689. DOI: 10.1007/s11356-017-8637-x - 105.
An H, Liu Y, Zhao X, Huang Q , Yuan S, Yang X, et al. Characterization of cadmium-resistant endophytic fungi from Salix variegata Franch in three gorges reservoir region, China. Microbiological Research. 2015;176 :29-37. DOI: 10.1016/j.micres.2015.03.013 - 106.
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metal toxicity and the environment. In: Luch A, editor. Molecular, Clinical and Environmental Toxicology: Volume 3: Environmental Toxicology. Basel: Springer Basel; 2012. pp. 133-164 - 107.
Gill RA, Ali B, Cui P, Shen E, Farooq MA, Islam F, et al. Comparative transcriptome profiling of two Brassica napus cultivars under chromium toxicity and its alleviation by reduced glutathione. BMC Genomics. 2016;17 :885. DOI: 10.1186/s12864-016-3200-6 - 108.
López-Bucio J, Hernández-Madrigal F, Cervantes C, Ortiz-Castro R, Carreón-Abud Y, Martínez-Trujillo M. Phosphate relieves chromium toxicity in Arabidopsis thaliana plants by interfering with chromate uptake. Biometals. 2014;27 :363-370. DOI: 10.1007/s10534-014-9718-7 - 109.
Zhu S-C, Tang J-X, Zeng X-X, Wei B-J, Yang S-D, Huang B. Isolation of Mucor circinelloides Z4 andMucor racemosus Z8 from heavy metal-contaminated soil and their potential in promoting phytoextraction with Guizhou oilseed rap. Journal of Central South University. 2015;22 :88-94. DOI: 10.1007/s11771-015-2498-6 - 110.
Shen M, Liu L, Li D-W, Zhou W-N, Zhou Z-P, Zhang C-F, et al. The effect of endophytic Peyronellaea from heavy metal-contaminated and uncontaminated sites on maize growth, heavy metal absorption and accumulation. Fungal Ecology. 2013;6 :539-645. DOI: 10.1016/j.funeco.2013.08.001 - 111.
Xiao X, Luo S, Zeng G, Wei W, Wan Y, Chen L, et al. Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulatorSolanum nigrum L. Bioresource Technology. 2010;101 :1668-1674. DOI: 10.1016/j.biortech.2009.09.083 - 112.
Pietro-Souza W, de Campos Pereira F, Mello IS, Stachack FFF, Terezo AJ, Cunha CN, et al. Mercury resistance and bioremediation mediated by endophytic fungi. Chemosphere. 2020; 240 :124874. DOI: 10.1016/j.chemosphere.2019.124874 - 113.
Ting ASY, Lee MVJ, Chow YY, Cheong SL. Novel exploration of endophytic Diaporthe sp. for the biosorption and biodegradation of triphenylmethane dyes. Water, Air, & Soil Pollution. 2016;227 :109. DOI: 10.1007/s11270-016-2810-6 - 114.
Przystaś W, Zabłocka-Godlewska E, Grabińska-Sota E. Biological removal of azo and triphenylmethane dyes and toxicity of process by-products. Water, Air, & Soil Pollution. 2012; 223 :1581-1592. DOI: 10.1007/s11270-011-0966-7 - 115.
Gangadevi V, Muthumary J. Isolation of Colletotrichum gloeosporioides , a novel endophytic taxol-producing fungus from the leaves of a medicinal plant,Justicia gendarussa . Mycologia Balcanica. 2008;5 :1-4. DOI: 10.1.1.457.1000