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Nanomaterials 2020, 10, 1146 12 of 24 4. Mechanisms of Action of Nanoparticles against Phytopathogens Although green synthesized metallic NPs have been studied for their potentials against phytopathogens, the exact mode of actions of NPs is not completely understood [165]. To date, some mechanisms have been reported, such as protein dysfunction (e.g., oxidation of cysteine in Fe-binding site, destruction of Fe–S cluster, exchange of catalytic metal, and exchange of structural metal), production of reactive oxygen species(ROS) and antioxidant depletion, impaired membrane function (e.g., membrane damage, loss of membrane potential), interference with nutrient uptake (e.g., inhibition of Fe (III) transporter gene expression) and genotoxicity (e.g., double-strand breaks) [166]. These mechanisms may not operate individually, but function in combination against various phytopathogens [52,166]. The adhesion of NPs with microbial cell membrane occurs due to the electrostatic attraction between the negatively charged cell membrane of microbes and NPs with positive or low negative charges. The morphological structures of the membrane are disturbed by the NPs and the membrane depolarization causes the disruption of membrane permeability and respiratory actions, and ultimately damages the cell structures, leading to cell death. This disruption of cell structure leads to the leakage of internal cell content including proteins, enzymes, DNA, and metabolites. In addition, the NPs may cause irregular pits on the microbial cell wall that facilitate NPs’ entry into periplasmic space and inside the cells. NP actions on membrane damage and pit formation on the cell surface can be observed by using TEM and SEM [14]. Masum et al. observed the green synthesized AgNPs effects on Acidovorax oryzae strain RS-2 using TEM and showed highly ruptured cell walls, leakage of cytoplasmic and nucleic contents, swollen structure leading to bacterial death [112]. In another study, biosynthesized AgNPs were applied to Fusarium graminearum strain PH-1 and antifungal activities of distortion of hyphae and damaging cell walls were observed by both SEM and TEM [20]. Similar effects of AgNPs on several other phytopathogenic fungi such as Alternaria alternata, Botrytis cinera and Trichosporon asahii were also observed [167]. The toxicity of NPs may be caused by the formation of ROS [143]. Free radicals can damage the cell wall and various biomolecules such as proteins, lipids and DNA. DNA damages, such as mutations, deletions, single-strand breaks, double-strand breaks, and cross-linking with proteins, may occur [168]. Zhang et al. revealed that damaging cell membrane and generating ROS are involved in the antibacterial mechanisms [169]. They observed damage of cell membrane and AgNPs inside Azotobacter vinelandii cells using TEM and revealed AgNP-induced hydroxyl radicals inside bacterial cells using electron spin resonance. 5. Environmental Consequences of Metallic Nanoparticles Several studies have revealed that NPs can be used to manage or control plant pathogens [5,6]. Besides this benefit, there may be some toxic or adverse effects of these NPs on various components of the environments (Figure 3). The NPs that have been used for plant pathogen management may be dispersed from the crop lands to the soil, water and atmosphere. The dispersion may take place through leaching, surface run-off by rain, and transport by air current or trophic transfer [170]. Different studies on this subject have suggested that NPs may be absorbed by microbes in the soils, sediments and plant roots. Later, these NPs are migrated from roots to other parts of the plants, and accumulation occurs [171]. Shifting of NPs from one trophic level to another trophic level takes place as the microbes, plant products or their waste materials are utilized or consumed by various organisms such as protozoa, arthropods, annelids, mollusks, fish, insects, birds and mammals [172,173]. This demonstrates that the adverse effects may be inherited by their offspring [174]. This scenario has also been observed in marine organisms [175] and also in food chains of plant-herbivore-carnivore [172,173,176,177]. Therefore, a standard application of nanomaterials in crop plants is needed for safe and sustainable use of nanotechnology in agriculture. For the management of plant pathogens, the application of NPs should be accompanied with the knowledge of possible risks for direct or indirect application to crop plants, and the ecosystem where the crop plants have interacted with microorganisms, animals orPDF Image | Plant and Microbe-Based Synthesis of Metallic Nanoparticles
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