Research articleAluminum oxide nanoparticles affect the cell wall structure and lignin composition slightly altering the soybean growth
Graphical abstract
Introduction
Nanoparticles (NPs) are materials having one of their dimensions ranging from 1 to 100 nm (Amist et al., 2017; Dayem et al., 2017). They have a high surface to volume ratio, which gives them special properties, such as increased chemical reactivity, conductivity, ductility, toughness, and strength (Amist et al., 2017). These properties have enabled their use in a wide range applications (Singh et al., 2017), especially in industry, medicine, and agriculture (Marchiol, 2018). Due to this, current studies on NPs have been intensified. In fact, about 239,000 papers are found in PubMed website using the term “nanoparticles”, 50% of which have been published in the last 5 years.
With annual world production estimated to reach 100,000 tons in 2020, Al2O3 NPs are among the most widely utilized (Asztemborska, 2018). Their unique physicochemical properties allow their application in drug delivery, chemical synthesis, catalysis, energy storage, hydrogen production, rocket propellants, explosives, high performance ceramics, sunscreens, packaging materials, cutting tools, plastics, and others (Martin et al., 2018; Shabnam and Kim, 2018; Yanık and Vardar, 2015). Undoubtedly, the largest employment sector that uses Al2O3 NPs is the production of paints and coatings (Asztemborska, 2018). However, all these advantages have a cost, and, unfortunately, Al2O3 NPs can reach the soil, water, and air during their production, transport, storage, or disposal (Srikanth et al., 2015). Therefore, studies aiming to investigate their toxicity to living organisms and the environment are imperative.
Whether Al2O3 NPs are phytotoxic or not to plants is still a controversial issue, since positive, negative, and negligible effects have all been reported. Factors that may affect the results of toxicity studies are the sizes and concentrations of the NPs, as well as the methods of plant cultivation and treatment (Asztemborska, 2018). Positive effects of Al2O3 NPs on growth have been reported in Lemna minor (Juhel et al., 2011) and Glycine max under flooding (Yasmeen et al., 2016). These NPs were able to induce the transcription of several genes involved in the growth and nutrient uptake without affecting the photosynthesis and growth of Arabidopsis thaliana (Jin et al., 2017). In turn, Nicotiana tabacum exposed to Al2O3 NPs showed changes in microRNA levels, chlorosis, and had decreased leaf area and root weight (Burklew et al., 2012). Inhibitory effects on growth of Triticum aestivum, Zea mays, Cucumis sativus, Brassica oleracea, and Daucus carota exposed to Al2O3 NPs have also been reported (Yang and Watts, 2005; Yanık and Vardar, 2015). Finally, Vigna radiata growth was not affected by Al2O3 NPs (Shabnam and Kim 2018).
Plant cell wall is a complex and dynamic structure consisting of many different polysaccharides, aromatic compounds, and proteins (Carpita et al., 2015). Cellulose is the main structural component, whose microfibrils are cross-linked by hemicelluloses. Lignin is a heteropolymer of simple phenolic acids that confers rigidity and mechanical resistance to the plant cell wall (Boerjan et al., 2003; Marchiosi et al., 2020). Hydroxycinnamic acids such as p-coumaric and ferulic acids, produced in the phenylpropanoid pathway, covalently bind lignin to proteins and polysaccharides, and act as connectors between cell wall polymers (de Oliveira et al., 2015). Although apparently rigid, the plant cell wall architecture and composition can be modified in response to several biotic and abiotic stresses (Loix et al., 2017; Parrotta et al., 2015). For instance, increased lignification occurs in response to low temperatures, water deficit, salt stress, light, mineral nutrition, and heavy metals (Moura et al., 2010). It has recently been shown that increased lignin deposition produces a physical barrier able to restrict the uptake of heavy metals such as cadmium and, later, its phytotoxicity (Loix et al., 2017; Parrotta et al., 2015). Similarly, the involvement of lignification in plant responses to NPs needs to be investigated.
Some works have revealed increased lignification in a variety of plant species exposed to silica, silver, iron oxide, copper oxide, and zinc oxide NPs (Asgari et al., 2018; Bernard et al., 2015; Lopes et al., 2018; Nazaralian et al., 2017; Prakash and Chung, 2016). However, studies focusing on lignification responses to Al2O3 NPs exposure are scarce. In this work, we evaluated the effects of Al2O3 NPs on the growth and lignin metabolism and composition of soybean plants. Impacts of Al2O3 NPs on the morphology and ultrastructure of roots were analyzed using scanning electron microscopy (SEM) and transmission electron microscopy (TEM). The contents of lignin and its monomeric composition, total phenolics, cell-wall-esterified hydroxycinnamic acids, and activities of soluble and cell wall-bound peroxidases (POD) in addition to phenylalanine ammonia-lyase (PAL) were determined to evaluate the effects at structural and metabolic levels.
Section snippets
Characterization of Al2O3 NPs
The Al2O3 NPs (particle size 30–60 nm (TEM), product number 642991), were purchased from Sigma-Aldrich® (St. Louis, MO, USA). The shapes, sizes, and agglomeration of the NPs were determined by transmission electron microscopy (TEM) and dynamic light scattering (DSL). For TEM analysis, 15 mg L−1 of Al2O3 NPs were suspended in distilled water and sonicated for 15 min. Then, 10 μL of the NP suspension were added to a Formvar-coated copper grid, drained with a filter paper, and examined under the
Characterization of Al2O3 NPs
The TEM micrographs showed that Al2O3 NPs exhibit an irregular morphology and average size of 20–60 nm (Fig. 1A–D). The hydrodynamic diameter and zeta potential of Al2O3 NPs suspended in deionized water were 221.5 ± 11.34 nm and −26.58 ± 1.574 mV, respectively. In turn, when suspended in a full-strength Hoagland nutrient solution, the zeta potential of NPs was −11.4 ± 0.488 mV, which was 57% lower than it was in water.
Al2O3 NPs slightly affected soybean growth
In general, exposure to Al2O3 NPs did not affect root and stem development (
Discussion
Overall, our data revealed that Al2O3 NPs slightly affect soybean growth, although they promoted notable structural alterations in the cell wall and lignin composition. These findings were associated with the behavior of the NPs in the nutrient solution, the structural changes in the cell wall, and the metabolic responses related to lignification.
When dissolved in water, Al2O3 NPs revealed a high degree of stability, since zeta potential was −26.58 ± 1.574 mV. This value is close to that
Conclusion
Our results indicate that up to 1000 mg L−1, Al2O3 NPs slightly affect the growth of soybean plants. However, at the microscopic level, NPs disorganize the tissues and cause cracks in roots due to their internalization. Changes in cell wall structure may play an important role in reducing the radial movement of NPs within the roots without significantly affecting soybean growth. In this way, increases in lignin content, with modulation of this monomeric composition followed by changes in
Funding
This work was funding by grants from National Council for Scientific and Technological Development – CNPq (nº 407791/2018-3).
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Rogério Marchiosi and Osvaldo Ferrarese-Filho are research fellows of National Council for Scientific and Technological Development (CNPq). This study was financed in part by the Coordination of Enhancement of Higher Education Personal - Brazil (CAPES) - Finance Code 001. The authors thank César Armando Contreras Lancheros by the aid provided in the microscopy analyzes, and Professor Chris Exley (Keele University, Staffordshire, UK) for their careful reading of the manuscript and constructive
References (69)
- et al.
Spectrophotometric determination of aluminium by morin
Talanta
(1995) - et al.
Comparative studies of Al3+ ions and Al2O3 nanoparticles on growth and metabolism of cabbage seedlings
J. Biotechnol.
(2017) - et al.
Effects of silicon nanoparticles on molecular, chemical, structural and ultrastructural characteristics of oat (Avena sativa L.)
Plant Physiol. Biochem.
(2018) - et al.
Exogenous caffeic acid inhibits the growth and enhances the lignification of the roots of soybean (Glycine max)
J. Plant Physiol.
(2011) - et al.
Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f.sp. cubense
Phytochemistry
(2003) - et al.
Nano-aluminum: transport through sand columns and environmental effects on plants and soil communities
Environ. Res.
(2008) - et al.
An integrated approach to highlight biological responses of Pisum sativum root to nano-TiO2 exposure in biosolid-amended agricultural soil
Sci. Total Environ.
(2019) - et al.
Comparative impacts of iron oxide nanoparticles and ferric ions on the growth of Citrus maxima
Environ. Pollut.
(2017) - et al.
Distinct physiological and molecular responses in Arabidopsis thaliana exposed to aluminum oxide nanoparticles and ionic aluminum
Environ. Pollut.
(2017) - et al.
Alumina nanoparticles enhance growth of Lemna minor
Aquat. Toxicol.
(2011)
Role of nanomaterials in plants under challenging environments
Plant Physiol. Biochem.
Lignification and related parameters in copper-exposed Matricaria chamomilla roots: role of H2O2 and NO in this process
Plant Sci.
Phytotoxicity of nanoparticles: inhibition of seed germination and root growth
Environ. Pollut.
Aluminum nanopowder: a substance to be handled with care
J. Hazard Mater.
Designer lignins: harnessing the plasticity of lignification
Curr. Opin. Biotechnol.
Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.)
Ecotoxicol. Environ. Saf.
Comparison of silicon nanoparticles and silicate treatments in fenugreek
Plant Physiol. Biochem.
Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants
Toxicology
Ecotoxicology and environmental safety non-toxicity of nano alumina: a case on mung bean seedlings
Ecotoxicol. Environ. Saf.
Aluminium long-term stress differently affects photosynthesis in rye genotypes
Plant Physiol. Biochem.
Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis
J. Biotechnol.
Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles
Toxicol. Lett.
Quantitative proteomic analysis of post-flooding recovery in soybean root exposed to aluminum oxide nanoparticles
J. Proteomics
Soybean root growth inhibition and lignification induced by p-coumaric acid
Environ. Exp. Bot.
Alumina nanoparticles and plants: environmental transformation, bioaccumulation, and phytotoxicity
Nanoparticle uptake in plants: gold nanomaterial localized in roots of Arabidopsis thaliana by X-ray computed nanotomography and hyperspectral imaging
Characterization of silver nanoparticles internalized by Arabidopsis plants using single particle ICP-MS analysis
Front. Plant Sci.
The effect of colloidal silver nanoparticles on the level of lignification and hyperhydricity syndrome in Thymus daenensis vitro shoots: a possible involvement of bonded polyamines
Vitro Cell Dev. Biol. Plant
No evidence for cerium dioxide nanoparticle translocation in maize plants
Environ. Sci. Technol.
Lignin biosynthesis
Annu. Rev. Plant Biol.
Aluminum speciation using morin: I. Morin and its complexes with aluminum
J. Envirom. Qual.
Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum)
PLoS One
The cell wall
The role of reactive oxygen species (ROS) in the biological activities of metallic nanoparticles
Int. J. Mol. Sci.
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