Effects of Silver Nanoparticles on Physiological and Proteomic Responses of Tobacco (Nicotiana tabacum) Seedlings Are Coating-Dependent

Abstract

The harmful effects of silver nanoparticles (AgNPs) have been confirmed in many organisms, but the mechanism of their toxicity is not yet fully understood. In biological systems, AgNPs tend to aggregate and dissolve, so they are often stabilized by coatings that influence their physico-chemical properties. In this study, the effects of AgNPs with different coatings [polyvinylpyrrolidone (PVP) and cetyltrimethylammonium bromide (CTAB)] on oxidative stress appearance and proteome changes in tobacco (Nicotiana tabacum) seedlings have been examined. To discriminate between the nanoparticulate Ag form from the ionic one, the treatments with AgNO3, a source of Ag+ ions, were also included. Ag uptake and accumulation were found to be similarly effective upon exposure to all treatment types, although positively charged AgNP-CTAB showed less stability and a generally stronger impact on the investigated parameters in comparison with more stable and negatively charged AgNP-PVP and ionic silver (AgNO3). Both AgNP treatments induced reactive oxygen species (ROS) formation and increased the expression of proteins involved in antioxidant defense, confirming oxidative stress as an important mechanism of AgNP phytotoxicity. However, the mechanism of seedling responses differed depending on the type of AgNP used. The highest AgNP-CTAB concentration and CTAB coating resulted in increased H2O2 content and significant damage to lipids, proteins and DNA molecules, as well as a strong activation of antioxidant enzymes, especially CAT and APX. On the other hand, AgNP-PVP and AgNO3 treatments induced the nonenzymatic antioxidants by significantly increasing the proline and GSH content. Exposure to AgNP-CTAB also resulted in more noticeable changes in the expression of proteins belonging to the defense and stress response, carbohydrate and energy metabolism and storage protein categories in comparison to AgNP-PVP and AgNO3. Cysteine addition significantly reduced the effects of AgNP-PVP and AgNO3 for the majority of investigated parameters, indicating that AgNP-PVP toxicity mostly derives from released Ag+ ions. AgNP-CTAB effects, however, were not alleviated by cysteine addition, suggesting that their toxicity derives from the intrinsic properties of the nanoparticles and the coating itself.

Attenuation of photosynthesis in nanosilver-treated Arabidopsis thaliana is inherently linked to the particulate nature of silver

“…This suggested a significant up-regulation of ascorbate synthesis, a key scavenger of hydrogen peroxide in the apoplast and the chloroplast. This is in agreement with commonly reported observations that AgNPs cause a shift in the redox balance toward oxidative conditions, as documented by experimental measurements of an increase in reactive oxygen species (ROS) [ 9 , 12 , 13 , 37 , 41 , 43 , 44 ]. In qPCR-based gene expression measurements, Qian et al [ 26 ] and Nair and Chung [ 9 ] documented the up-regulation of catalase and several members of the superoxide dismutase and ascorbate peroxidase gene families in Arabidopsis and rice, respectively.…”

“…Our results are in agreement with data generated from broad range of plants including Arabidopsis [ 10 ], tobacco [ 44 ], mustard [ 11 ], arugula [ 51 ], kiwifruit [ 12 ], trumpetweed [ 52 ], pokeweed [ 52 ] and O. alismoides [ 39 ]. Notable exceptions are to this are the duckweed species Lemna minor [ 25 ] and Spirodela polyrhiza [ 13 ] in which AgNO3 was reported to cause a more severe toxic impact than AgNPs.…”

“…These data indicated that the phytotoxicity of AgNPs is influenced by medium pH, likely through the modified physicochemical properties of the particles. This is supported by recent data from Biba et al [ 44 ] who used AgNPs with polyvinylpyrrolidone (PVP) and cetyltrimethylammonium bromide (CTAB) coating and found a greater impact of the latter on the rise of ROS, the activation of antioxidant response and the abundance of proteins involved in stress-response and energy metabolism in tobacco. Stefanic et al [ 27 ] studied AgNPs coated with CTAB, PVP, and citrate, and found that citrate-coated AgNPs had the least impact on the chlorophyll and carotenoid content of and photosynthetic efficiency in tobacco.…”

The Occurrence of Oxidative Stress Induced by Silver Nanoparticles in Chlorella vulgaris Depends on the Surface-Stabilizing Agent

“…The influence of the physical and chemical properties of AgNPs on their stability and subsequent biological interactions has been confirmed in several studies, especially highlighting the size of AgNPs as a crucial factor for their phytotoxicity [ 15 , 49 , 73 , 74 ]. However, the number of studies investigating the effects of differently coated AgNPs on living organisms is increasing [ 11 , 17 , 25 , 27 , 33 , 75 ]. Stabilizing agents can alter AgNP surfaces and thus affect their behavior and transformation in the exposure medium [ 22 ].…”

Unraveling the mysteries of silver nanoparticles: synthesis, characterization, antimicrobial effects and uptake translocation in plant—a review

“…Superoxide dismutase (SOD) and other enzymatic antioxidants are essential for shielding plant cells from oxidative damage brought on by exposure to AgNP (Rajput et al, 2020). Research has indicated that the Nicotiana tabacum plant may experience oxidative damage as a result of AgNP exposure, which would raise SOD activity (Biba et al 2022 ). Furthermore, studies have shown that plant leaf biosynthesis can function as a supplemental mechanism to the root pathway for AgNP absorption (Xu et al 2020 ).…”