Abstract
The synthesized α-MoO3 and MoS2 NPs had nanosheet and nanoflower-like structures with crystallite size of 21.34 nm and 4.32 nm, respectively. The uptake, bioaccumulation, and impact of these two Mo-NPs were studied in rice (Oryza sativa L) cv. HUR 3022 seedlings exposed to 100, 500, and 1000 ppm concentrations in hydroponics for 10 days in the growth medium. The uptake of α-MoO3 and MoS2 NPs by rice exposed to 100 ppm concentrations of NPs led to the accumulation of 7.32 ppm/4.55 ppm and 1.84 ppm/1.19 ppm in roots/shoots, respectively, as compared to controls. Unlike MoO3, more accumulation of MoS2 in roots reflect less translocation of this NP from roots to shoots. Results suggest tissue-specific distribution of NPs in rice seedlings. The increased growth and elevated protein levels in rice seedlings at 100 ppm concentrations of nanoparticles imply a stimulation in the repair mechanism at low doses indicating hormesis. MoS2 NPs treatments led to increased chlorophyll a levels suggesting it to be non-compromising with photosynthetic process in rice. The high malondialdehyde levels and altered activities of antioxidant enzymes GPX, APX, and CAT in rice seedlings exposed to α-MoO3 or MoS2 NPs indicate oxidative imbalance. Between α-MoO3 and MoS2 NPs, the former shows toxic effects as reflected from the decreased levels of photosynthetic pigments at all concentrations; however, an activation of chloroplast ROS detoxification is evident in the presence of MoS2 NPs. The BCF > 1 for both α-MoO3 and MoS2 NPs and TF of 0.6–2.0 and 0.42–0.65 suggest the latter to be more environmentally safe. In conclusion, a100 ppm MoS2 NPs concentration has low translocation and less accumulation with no significant impact on growth of rice cv. HUR 3022 seedlings and appears to be environmentally safe for future applications.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aebi H (1974) Catalase. In: methods of enzymatic analysis vol 2. Ed: H. U. Bergmeyer, Academic Press, NY, pp 673-684
Agarwala SC (1978) Effect of molybdenum deficiency on the growth and metabolism of corn plants raised in sand culture. Can J Bat 56:1905–1908
Arnon DI (1949) Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Arnot JA, Gobas FA (2006) A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environmental Reviews 14:257–297
Aslani F, Bagheri S, Muhd Julkapli N, Juraimi AS, Hashemi FS, Baghdadi A (2014) Effects of engineered nanomaterials on plants growth: an overview. The Scientific World J 2014:1–28
Aziz N, Faraz M, Pandey R, Shakir M, Fatma T, Varma A, Barman I, Prasad R (2015) Facile algae-derived route to biogenic silver nanoparticles: synthesis, antibacterial, and photocatalytic properties. Langmuir 31:11605–11612
Balk J, Lobréaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends in Plant Sci 10:324–331
Barker AV, Pilbeam DJ (2015a) Handbook of plant nutrition, Second edn. CRC press, Boca Raton
Barker AV, Pilbeam DJ (2015b) Handbook of plant nutrition. CRC press, Boca Raton
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem 44:276–287
Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLOS One 7:e34783
Cairns ALP, Kritzinger JH (1992) The effect of molybdenum on seed dormancy in wheat. Plant Soil 145:295–297
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Chen G, Ma C, Mukherjee A, Musante C, Zhang J, White JC, Dhankher OP, Xing B (2016) Tannic acid alleviates bulk and nanoparticle Nd2O3 toxicity in pumpkin: a physiological and molecular response. Nanotoxicology 10:1243–1253
Chen S, Wang L, Shao R, Zou J, Cai R, Lin J et al (2018) Atomic structure and migration dynamics of MoS2/LixMoS2 interface. Nano energy 48:560–568
Cornelis G, Hund-Rinke K, Kuhlbusch T, Van den Brink N, Nickel C (2014) Fate and bioavailability of engineered nanoparticles in soils: AReview. Crit Rev Env Sci Tec 44:2720–2764
Da Costa MVJ, Sharma PK (2016) Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica 54:110–119
Darlington TK, Neigh AM, Spencer MT, Guyen OT, Oldenburg SJ (2009) Nanoparticle characteristics affecting environmental fate and transport through soil. Environ Toxicol Chem 28:1191–1199
Etxeberria E, Gonzalez P, Pozueta J (2009) Evidence for two endocytic transport pathways in plant cells. Plant Science 177:341–348
Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA, Hegazy AK, Musarrat J (2013) Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J Hazard Mater 250:318–332
Gardea-Torresdey JL, Rico CM, White JC (2014) Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environments. Environ Sci Technol 48:2526–2540
Ghosh M, Singh SP (2005) A comparative study of cadmium phytoextraction by accumulator and weed species. Environ Pollut 133:365–371
Hajra A, Mondal NK (2017) Effects of ZnO and TiO2 nanoparticles on germination, biochemical and morphoanatomical attributes of Cicer arietinum L. Energy. Ecol Environ 2:77–288
Hawthorne J, De la Torre Roche R, Xing B, Newman LA, Ma X, Majumdar S, Gardea-Torresdey J, White JC (2014) Particle-size dependent accumulation and trophic transfer of cerium oxide through a terrestrial food chain. Environ Sci Technol 48:13102–13109
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185
Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:32
Iversen TG, Skotland T, Sandvig K (2011) Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano today 6:176–185
Jacquot JP, Lancelin JM, Meyer Y (1997) Thioredoxins: structure and function in plant cells. New Phytol. 136:543–570
Judy JD (2013) Bioavailability of manufactured nanomaterials in terrestrial ecosystems. Theses, University of Kentucky
Khodakovskaya M, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, Biris AS (2009) Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 3:3221–3227
Khodakovskaya MV, de Silva K, Nedosekin DA, Dervishi E, Biris AS, Shashkov EV, Galanzha EI, Zharov VP (2011) Complex genetic, photothermal, and photoacoustic analysis of nanoparticle-plant interactions. Proc Natl Acad Sci 108:1028–1033
Kumar R, Khan MA, Haq N (2014) Application of carbon nanotubes in heavy metals remediation. Crit Rev Env Sci Tec 44:1000–1035
Kumar N, George BPA, Abrahamse H, Parashar V, Ngila JC (2017) Sustainable one-step synthesis of hierarchical microspheres of PEGylated MoS2 nanosheets and MoO3 nanorods: their cytotoxicity towards lung and breast cancer cells. Appl Surf Sci 396:8–18
Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675
Levard C, Hotze EM, Lowry GV, Brown GE Jr (2012) Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol 46:6900–6914
Li Y, Jin Q, Yang D, Cui J (2018) Molybdenum sulfide induce growth enhancement effect of rice (Oryza sativa L.) through regulating the synthesis of chlorophyll and the expression of aquaporin gene. J. Agri Food Chem 66:4013–4021
Lowry OH, Roenbrough NJ, Farr AL, Randal EJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Lv J, Christie P, Zhang S (2019) Uptake, translocation, and transformation of metal-based nanoparticles in plants: recent advances and methodological challenges. Environ Sci: Nano 6:41–59
Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061
Ma C, Chhikara S, Minocha R, Long S, Musante C, White JC, Xing B, Dhankher OP (2015a) Reduced silver nanoparticle phytotoxicity in Crambe abyssinica with enhanced glutathione production by overexpressing bacterial γ-glutamylcysteine synthase. Environ Sci Technol 49:10117–10126
Ma C, White JC, Dhankher OP, Xing B (2015b) Metal-based nanotoxicity and detoxification pathways in higher plants. Environ Sci Technol. 49:7109–7122
Majumdar S, Almeida IC, Arigi EA, Choi H, VerBerkmoes NC, Trujillo-Reyes J, Flores-Margez JP, White JC, Peralta-Videa JR, Gardea-Torresdey JL (2015) Environmental effects of nanoceria on seed production of common bean (Phaseolus vulgaris): a proteomic analysis. Environ Sci Technol 49:13283–13293
Marschner H (2012) Marschner's Mineral Nutrition of higher plants 3rd Edition, Academic Press, London
McGrath SP, Micó C, Zhao FJ, Stroud JL, Zhang H, Fozard S (2010) Predicting molybdenum toxicity to higher plants: estimation of toxicity threshold values. Environ Polln 158:3085–3094
Miralles P, Church TL, Harris AT (2012) Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol 46:9224–9239
Mirzajani F, Askari H, Hamzelou S, Farzaneh M, Ghassempour A (2013) Effect of silver nanoparticles on Oryza sativa L. and its rhizosphere bacteria. Ecotoxicol Environ Saf 88:48–54
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19
Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radical Research 28:659–671
Mukherjee A, Peralta-Videa JR, Bandyopadhyay S, Rico CM, Zhao L, Gardea-Torresdey JL (2014) Physiological effects of nanoparticulate ZnO in green peas (Pisum sativum L.) cultivated in soil. Metallomics. 6:132–138
Nahakpam S, Shah K (2011) Expression of key antioxidant enzymes under combined effect of heat and cadmium toxicity in growing rice seedlings. Plant Growth Regulation 63:23–35
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Noori A, White JC, Newman LA (2017) Mycorrhizal fungi influence on silver uptake and membrane protein gene expression following silver nanoparticle exposure. J Nanopart Res 19:66
Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377-400
Onelli E, Prescianotto-Baschong C, Caccianiga M, Moscatelli A (2008) Clathrin-dependent and independent endocytic pathways in tobacco protoplasts revealed by labelling with charged nanogold. J Exp Bot 59:3051–3068
Pagano L, Servin AD, De La Torre-Roche R, Mukherjee A, Majumdar S, Hawthorne J, Marmiroli M, Maestri E, Marra RE, Isch SM, Dhankher OP (2016) Molecular response of crop plants to engineered nanomaterials. Environ Sci Technol 50:7198–7207
Pérez-de-Luque A (2017) Interaction of nanomaterials with plants: what do we need for real applications in agriculture? Front in Environ Sci 5:12
Pradhan S, Mailapalli DR (2017) Interaction of engineered nanoparticles with the agri-environment. J Agri Food Chem 65:8279–8294
Prasad R, Pandey R, Barman I (2016) Engineering tailored nanoparticles with microbes: quo vadis? Wiley Interdiscip Rev Nanomed Nanobiotechnol 8:316–330
Rana K, Kumari M, Mishra A, Pudake RN (2019) Engineered nanoparticles for increasing micronutrient use efficiency. In: Pudake R, Chauhan N, Kole C (eds) Nanoscience for Sustainable Agriculture. Springer, Cham, pp 25–49
Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J. Agric. Food Chem. 59:3485–3498
Rico CM, Hong J, Morales MI, Zhao L, Barrios AC, Zhang JY, Peralta-Videa JR, Gardea-Torresdey JL (2013a) Effect of cerium oxide nanoparticles on rice: a study involving the antioxidant defense system and in vivo fluorescence imaging. Environ Sci Technol 47:5635–5642
Rico CM, Morales MI, McCreary R, Castillo-Michel H, Barrios AC, Hong J, Tafoya A, Lee WY, Varela-Ramirez A, Peralta-Videa JR, Gardea-Torresdey JL (2013b) Cerium oxide nanoparticles modify the antioxidative stress enzyme activities and macromolecule composition in rice seedlings. Environ Sci Technol 47:14110–14118
Rico CM, Peralta-Videa JR, Gardea-Torresdey JL (2015) Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants. In: Siddiqui M, Al-Whaibi M, Mohammad F (eds) Nanotechnology and Plant Sciences. Springer, Cham, pp 1–17
Roco MC (2005) International perspective on government nanotechnology funding in 2005. J Nanoparticle Res 7:707–712
Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T, Zhu S (2016) Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci 7:815
Sahle-Demessie E, Han C, Zhao A, Hahn B, Grecsek H (2016) Interaction of engineered nanomaterials with hydrophobic organic pollutants. Nanotechnology 27:284003
Santos AR, Miguel AS, Tomaz L, Malhó R, Maycock C, Patto MC, Fevereiro P, Oliva A (2010) The impact of CdSe/ZnS quantum dots in cells of Medicago sativa in suspension culture. J Nanobiotechnol 8:24
Scheffer F, Schachtschabel P (2002) Textbook of Soil Science. Auflage Spektrum Akademischer Verlag, Heidelberg, 15, p 593 (In German)
Serag MF, Kaji N, Gaillard C, Okamoto Y, Terasaka K, Jabasini M, Tokeshi M, Mizukami H, Bianco A, Baba Y (2011) Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. ACS nano 5:493–499
Servin AD, Morales MI, Castillo-Michel H, Hernandez-Viezcas JA, Munoz B, Zhao L, Nunez JE, Peralta-Videa JR, Gardea-Torresdey JL (2013) Synchrotron verification of TiO2 accumulation in cucumber fruit: a possible pathway of TiO2 nanoparticle transfer from soil into the food chain. Environ Sci Technol 47:11592–11598
Servin AD, Pagano L, Castillo-Michel H, De la Torre-Roche R, Hawthorne J, Hernandez-Viezcas JA, Loredo-Portales R, Majumdar S, Gardea-Torresday J, Dhankher OP, White JC (2017) Weathering in soil increases nanoparticle CuO bioaccumulation within a terrestrial food chain. Nanotoxicology 11:98–111
Shah K, Singh P, Nahakpam S (2013) Effect of cadmium uptake and heat stress on root ultrastructure, membrane damage and antioxidative response in rice seedlings. J Plant Biochem Biotechnol 22:103–112
Shah K, Nahakpam S, Chaturvedi V, Singh P (2019) Cadmium-induced anatomical abnormalities in plants. In: Prasad MNV, Fujita M (eds) In: Hasanuzzaman M. Academic Press, Cadmium Toxicity and Tolerance in Plants, pp 111–139
Sharma PK, Raghubanshi AS, Shah K (2020) Examining dye degradation and antibacterial properties of organically induced a-MoO3 nanoparticles, their uptake and phytotoxicity in rice seedlings. Environ Nanotechnol Monit Manag 14:1–10
Singh P, Shah K (2014) An update on effects of nitric oxide under abiotic stresses in higher plants. In: Hemantaranjan A (ed) Advances in Plant Physiology, vol. 15. Scientific Publishers, India, p 283
Tripathi DK, Singh VP, Swati S, Prasad SM, Chauhan DK, Dubey NK (2016) Silicon nanoparticles more efficiently alleviate arsenate toxicity than silicon in maize cultiver and hybrid differing in arsenate tolerance. Front. Environ. Sci. 4:46
Tripathi DK, Singh S, Singh S, Pandey R, Singh VP, Sharma NC, Prasad SM, Dubey NK, Chauhan DK (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol Biochem 110:2–12
Van Dongen JT, Ammerlaan AMH, Wouterlood M, Van Aelst AC, Borstlap AC (2003) Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann. Bot. 91:729–737
Vieira RF, Vieira C, Cardoso EJBN, Mosquim PR (1998) Foliar application of molybdenum in common bean. II. Nitrogenase and nitrate reductase activities in a soil of low fertility. J Plant Nutrition 21:2141–2151
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51
Wang X, Guo Y, Yang L, Han M, Zhao J, Cheng X (2012) Nanomaterials as sorbents to remove heavy metal ions in wastewater treatment. J Environ Anal Toxicol 2:154–158
Wang P, Lombi E, Zhao FJ, Kopittke PM (2016a) Nanotechnology: a new opportunity in plant sciences. Trends in Plant Science 21(8):699–712
Wang F, Liu X, Shi Z, Tong R, Adams CA, Shi X (2016b) Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants–a soil microcosm experiment. Chemosphere 147:88–97
Yang K, Xing B (2010) Adsorption of organic compounds by carbon nanomaterials in aqueous phase: Polanyi theory and its application. Chem Rev 110:5989–6008
Yue L, Ma C, Zhan X, White JC, Xing B (2017) Molecular mechanisms of maize seedling response to La2O3 NP exposure: water uptake, aquaporin gene expression and signal transduction. Environ Sci Nano 4:843–855
Zahra Z, Arshad M, Rafique R, Mahmood A, Habib A, Qazi IA, Khan SA (2015) Metallic nanoparticle (TiO2 and Fe3O4) application modifies rhizosphere phosphorus availability and uptake by Lactuca sativa. J Agric Food Chem 63:6876–6882
Zakikhani H, Yusop MK, Anuar AR, Radziah O, Soltangheisi A (2014) Effects of different levels of molybdenum on uptake of nutrients in rice cultivars. Asian J Crop Sci 6(3):236–244
Zhang YC, Yao L, Zhang G, Dionysiou DD, Li J, Du X (2014) One-step hydrothermal synthesis of high-performance visible-light-driven SnS2/SnO2 nano heterojunction photocatalyst for the reduction of aqueous Cr (VI). Applied Catalysis B: Environmental 144:730–738
Zhao L, Peralta-Videa JR, Varela-Ramirez A, Castillo-Michel H, Li C, Zhang J, Aguilera RJ, Keller AA, Gardea-Torresdey JL (2012a) Effect of surface coating and organic matter on the uptake of CeO2 NPs by corn plants grown in soil: Insight into the uptake mechanism. J Hazard Mater 225:131–138
Zhao L, Peng B, Hernandez-Viezcas JA, Rico C, Sun Y, Peralta-Videa JR, Tang X, Niu G, Jin L, Varela-Ramirez A, Zhang JY (2012b) Stress response and tolerance of Zea mays to CeO2 nanoparticles: cross talk among H2O2, heat shock protein, and lipid peroxidation. ACS Nano 6:9615–9622
Zhao L, Sun Y, Hernandez-Viezcas JA, Hong J, Majumdar S, Niu G, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2015) Monitoring the environmental effects of CeO2 and ZnO nanoparticles through the life cycle of corn (Zea mays) plants and in situ μ-XRF mapping of nutrients in kernels. Environ Sci Technol 49:2921–2928
Zhao Y, Le X, Yan J, Yan W, Wu C, Lian J, Huang Y, Bao J, Qiu J, Xu L, Xu Y, Xu H, Li H (2017) Facile preparation of NiFe2O4/MoS2 composite material with synergistic effect for high performance supercapacitor. J Alloy Comp 726:608–617
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The support from IIT Delhi, Jamia Milia Islamia, New Delhi, NEERI, Nagpur and Institute of Science, BHU, Varanasi for various analysis is thankfully acknowledged. Ms. Chitra Pokharia is thankfully acknowledged for her help in the editing of the MS.
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The authors are grateful to the University Grants Commission, New Delhi, for the fellowship to PKS and the Design Innovation Centre, IIT BHU, for the financial support.
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Sharma P and Shah K: conceptualization and methodology. Shah K: data curation and writing—original draft preparation. Sharma P: visualization and investigation. Shah K and Raghubanshi A: supervision. Sharma P: writing. Shah K: reviewing and editing.
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Sharma, P.K., Raghubanshi, A.S. & Shah, K. Examining the uptake and bioaccumulation of molybdenum nanoparticles and their effect on antioxidant activities in growing rice seedlings. Environ Sci Pollut Res 28, 13439–13453 (2021). https://doi.org/10.1007/s11356-020-11511-7
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DOI: https://doi.org/10.1007/s11356-020-11511-7