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      Are Fungal Endophytes Merely Mycorrhizal Copycats? The Role of Fungal Endophytes in the Adaptation of Plants to Metal Toxicity

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          Abstract

          The contamination of soil with toxic metals is a worldwide problem, resulting in the disruption of plant vegetation and subsequent crop production. Thus, remediation techniques for contaminated soil and water remain a constant interest of researchers. Phytoremediation, which utilizes plants to remove or stabilize contaminants, is perceived to be a promising strategy. However, phytoremediation’s use to date is limited because of constraints associated with such factors as slow plant growth rates or metal toxicity. Microbial-assisted phytoremediation serves as an alternative solution, since the impact of the microbial symbionts on plant growth and stress tolerance has frequently been described. Endophytic fungi occur in almost every plant in the natural environment and contribute to plant growth and tolerance to environmental stress conditions. Although this group of symbiotic fungi was found to form association with a wide range of hosts, including the non-mycorrhizal Brassicaceae metallophytes, their role in the response of plants to metal toxicity has not been thoroughly elucidated to date. This review summarizes the current knowledge regarding the role of endophytic fungi in the tolerance of plants to toxic metals and highlights the similarities and differences between this group of symbiotic fungi and mycorrhizal associations in terms of the survival of the plant during heavy metal stress.

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          Fungal endophytes: diversity and functional roles.

          All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.
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            The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress.

            Plants exposed to heavy metals accumulate an array of metabolites, some to high millimolar concentrations. This review deals with N-containing metabolites frequently preferentially synthesized under heavy metal stress such as Cd, Cu, Ni, and Zn. Special focus is given to proline, but certain other amino acids and oligopeptides, as well as betaine, polyamines, and nicotianamine are also addressed. Particularly for proline a large body of data suggests significant beneficial functions under metal stress. In general, the molecules have three major functions, namely metal binding, antioxidant defence, and signalling. Strong correlative and mechanistic experimental evidence, including work with transgenic plants and algae, has been provided that indicates the involvement of metal-induced proline in metal stress defence. Histidine, other amino acids and particularly phytochelatins and glutathione play a role in metal binding, while polyamines function as signalling molecules and antioxidants. Their accumulation needs to be considered as active response and not as consequence of metabolic dys-regulation.
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              Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions.

              Development and application of new types of fertilizers using innovative nanotechnology are one of the potentially effective options of significantly enhancing the global agricultural productions needed to meet the future demands of the growing population. Indeed, the review of available literature indicates that some engineered nanomaterials can enhance plant-growth in certain concentration ranges and could be used as nanofertilizers in agriculture to increase agronomic yields of crops and/or minimize environmental pollution. This article summarizes this type of nanomaterials under four categories: macronutrient nanofertilizers, micronutrient nanofertilizers, nutrient-loaded nanofertilizers, and plant-growth-enhancing nanomaterials. Each category is discussed respectively with reference to nanomaterials' chemical composition, particle size, concentrations applied, benefited plant species, plant incubation methods, and plant-growth enhancement aspects and the rates. The importance, research directions, and research requirements of each nanofertilizer category for achieving sustainable agriculture are also specifically examined. Finally, this review suggests that development of N and P macronutrient nanofertilizers is a high research and development priority both for food production and environmental protection.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                15 March 2019
                2019
                : 10
                : 371
                Affiliations
                [1] 1 Institute of Environmental Sciences, Jagiellonian University , Kraków, Poland
                [2] 2 Malopolska Centre of Biotechnology, Jagiellonian University , Kraków, Poland
                Author notes

                Edited by: Raul Antonio Sperotto, University of Taquari Valley, Brazil

                Reviewed by: Joséli Schwambach, University of Caxias do Sul, Brazil; Nuria Ferrol, Spanish National Research Council (CSIC), Spain

                *Correspondence: Piotr Rozpaądek, piotr.rozpadek@ 123456uj.edu.pl

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00371
                6428775
                30930857
                46ba81f2-5ece-4473-82ac-1cea922ca850
                Copyright © 2019 Domka, Rozpaądek and Turnau.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 November 2018
                : 12 February 2019
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 197, Pages: 16, Words: 15110
                Funding
                Funded by: Polish National Centre for Research and Development
                Award ID: FACCE SURPLUS/I/AGRONICKEL/02/2016
                Funded by: National Science Center
                Award ID: 2017/27/B/NZ8/01199
                Categories
                Microbiology
                Review

                Microbiology & Virology
                fungal endophytes,toxic metals,mycorrhiza,phytoremediation,phytomining
                Microbiology & Virology
                fungal endophytes, toxic metals, mycorrhiza, phytoremediation, phytomining

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