Soil and Plant Enzymes Responses to Zinc Oxide Nanoparticles in Submerged Rice (Oryza sativa L.) Ecosystem
DOI:
https://doi.org/10.48048/tis.2023.5558Keywords:
Antioxidant enzymes, DTPA extractable Zn, Hydroponic and soil experiment, Plant growth, Oryza sativa, SEM, TEM, UV-visible spectrophotometry, XRD, Zn deficiency, Zinc oxide nanoparticleAbstract
In the present study, the effects of zinc oxide nanoparticles (ZnO NPs) on rice (Oryza sativa L. cv. PB1509) plant growth were assessed in hydroponics (5, 10, 25, 50 mg L−1) and soil microcosm (5, 10, 25 50 mg kg−1) experiments. In both hydroponics and soil experiments, Zinc (Zn) accumulation in plant parts (roots, shoots and grains) was found to increase with increasing doses of ZnO NPs. Grains accumulated 29 mg kg−1 Zn at 50 mg kg−1 ZnO NPs in the soil experiment. In the hydroponics experiment, growth and photosynthetic pigments were induced by ZnO NPs up to 10 mg L−1, while higher doses of 25 and 50 mg L−1 were toxic to plant growth. Antioxidant enzyme activities (SOD, CAT, APX and GPX) were mostly increased or unaffected by all ZnO NPs doses. In soil experiments, acid and alkaline phosphatase activities were increased at 5 mg kg−1 followed by a declining trend. However, a significant decrease occurred only at 50 mg kg−1. Urease activity in soil was significantly increased at all doses of ZnO NPs, while the activity of dehydrogenase did not show any significant change up to 25 mg kg−1. The length of plants and photosynthetic pigments did not show much toxicity except root length beyond 10 mg kg−1; however, the biomass of plants including grains was significantly lower than control beyond 5 mg kg−1 dose. The activity of antioxidant enzymes (GPX, APX and CAT) showed a significant increase at all doses of ZnO NPs. The DTPA extractable Zn concentration in the soil was significantly elevated with increasing exposure concentrations of ZnO NPs. Based on hydroponics and soil experiments, this study suggests a dose of up to 10 mg L−1 or 10 mg kg−1 would be an appropriate dose for augmenting the growth of rice plants and Zn accumulation, and this can be practically utilized for rice plants growing in submerged conditions.
HIGHLIGHTS
- Rice plants exposed to ZnO nanoparticles in hydroponics and soil
- Zinc accumulation increased significantly in roots, shoots and grains
- Lower dose of ZnO NPs (10 mg/L or mg/kg) augmented plant growth
- Antioxidant enzymes showed a significant increase in activity in ZnO NPs treatment
GRAPHICAL ABSTRACT
Downloads
Metrics
References
A Kumar, K Gupta, S Dixit, K Mishra and S Srivastava. A review on positive and negative impacts of nanotechnology in agriculture. Int. J. Environ. Sci. Tech. 2019; 16, 2175-84.
T Farooq, M Adeel, Z He, M Umar, N Shakoor, WD Silva, W Elmer, JC White and Y Rui. Nanotechnology and plant viruses: An emerging disease management approach for resistant pathogens. ACS Nano 2021; 15, 6030-7.
LJ Pang, M Adeel, N Shakoor, KR Guo, DF Ma, MA Ahmad, GQ Lu, MH Zhao, SE Li and YK Rui. Engineered nanomaterials suppress the soft rot disease (Rhizopus stolonifer) and slow down the loss of nutrient in sweet potato. Nanomaterials 2021; 11, 2572.
M Adeel, N Shakoor, T Hussain, I Azeem, P Zhou, P Zhang, Y Hao, J Rinklebe and Y Rui. Bio-interaction of nano and bulk lanthanum and ytterbium oxides in soil system: Biochemical, genetic, and histopathological effects on Eisenia fetida. J. Hazard. Mater. 2021; 415, 125574.
M Adeel, N Shakoor, M Shafiq, A Pavlicek, F Part, C Zafiu, A Raza, MA Ahmad, G Jilani, JC White and EK Ehmoser. A critical review of the environmental impacts of manufactured nano-objects on earthworm species. Environ. Pollut. 2021; 290, 118041.
G Awasthi, V Nagar, S Mandzhieva, T Minkina, MS Sankhla, PP Pandit, V Aseri, KK Awasthi, VD Rajput, T Bauer and S Srivastava. Sustainable amelioration of heavy metals in soil ecosystem: Existing developments to emerging trends. Minerals 2022; 12, 85.
K Guo, A Hu, K Wang, L Wang, D Fu, Y Hao, Y Wang, A Ali, M Adeel, Y Rui and W Tan. Effects of spraying nano-materials on the absorption of metal(loid)s in cucumber. IET Nanobiotechnology 2019; 13, 712-9.
PC Srivastava, D Rawat, SP Pachauri and M Shrivastava. Strategies for enhancing zinc efficiency in crop plants. In: A Rakshit, HB Singh and A Sen (Eds.). Nutrient use efficiency: From basics to advances. Springer, New Delhi, India, 2015, p. 87-101.
MR Broadley, PJ White, JP Hammond, I Zelko and A Lux. Zinc in plants. New Phytol. 2007; 173, 677-702.
PC Srivastava, S Kumar, AP Singh, R Singh, V Ramachandran, M Shrivastava and SF D’Souza. Zn fertilizer formulation & process for making it. Indian Patent, Mumbai, India, 2010.
A Singh, SM Prasad and S Singh. Impact of nano ZnO on metabolic attributes and fluorescence kinetics of rice seedlings. Environ. Nanotechnol. Monit. Manag. 2018; 9, 42-9.
CO Dimkpa, U Singh, PS Bindraban, IO Adisa, WH Elmer, JL Gardea-Torresdey and JC White. Addition-omission of zinc, copper, and boron nano and bulk oxide particles demonstrate element and size-specific response of soybean to micronutrients exposure. Sci. Total Environ. 2019; 665, 606-16.
G Yang, H Yuan, H Ji, H Liu, Y Zhang, G Wang, L Chen and Z Guo. Effect of ZnO nanoparticles on the productivity, Zn biofortification, and nutritional quality of rice in a life cycle study. Plant Physiol. Biochem. 2021; 163, 87-94.
V Gupta, S Mohapatra, H Mishra, U Farooq, K Kumar, MJ Ansari, MF Aldawsari, AS Alalaiwe, MA Mirza and Z Iqbal. Nanotechnology in cosmetics and cosmeceuticals - a review of latest advancements. Gels 2022; 8, 173.
EAS Dimapilis, CS Hsu, RMO Mendoza and MC Lu. Zinc oxide nanoparticles for water disinfection. Sustain. Environ. Res. 2018; 28, 47-56.
BP Majee, Bhawna and AK Mishra. Bi-functional ZnO nanoparticles as a reusable SERS substrate for nano-molar detection of organic pollutants. Mater. Res. Express 2020; 6, 1250j1.
A Padmanaban, G Murugadoss, N Venkatesh, S Hazra, MR Kumar, R Tamilselvi and P Sakthivel. Electrochemical determination of harmful catechol and rapid decolorization of textile dyes using ceria and tin doped ZnO nanoparticles. J. Environ. Chem. Eng. 2021; 9, 105976.
AS Prasad. Lessons learned from experimental human model of zinc deficiency. J. Immunol. Res. 2020; 2020, 9207279.
P Ahmad, MN Alyemeni, AA Al-Huqail, MA Alqahtani, L Wijaya, M Ashraf, C Kaya and A Bajguz. Zinc oxide nanoparticles application alleviates arsenic (As) toxicity in soybean plants by restricting the uptake of as and modulating key biochemical attributes, antioxidant enzymes, ascorbate-glutathione cycle and glyoxalase system. Plants 2020; 9, 825.
A Srivastav, D Ganjewala, RK Singhal, VD Rajput, T Minkina, M Voloshina, S Srivastava and M Shrivastava. Effect of ZnO nanoparticles on growth and biochemical responses of wheat and maize. Plants 2021; 10, 2556.
MA Khan, H Yasmin, ZA Shah, J Rinklebe, MN Alyemeni and P Ahmad. Co application of biofertilizer and zinc oxide nanoparticles upregulate protective mechanism culminating improved arsenic resistance in maize. Chemosphere 2022; 294, 133796.
Y Li, Y Rui, B Huang, M Liu, A Muhammad, Z Lu and S Lu. Effects of nanomaterials on plant growth at molecular level. Curr. Mater. Sci. 2022; 15, 21-7.
U Song and S Lee. Phytotoxicity and accumulation of zinc oxide nanoparticles on the aquatic plants Hydrilla verticillata and Phragmites australis: Leaf-type-dependent responses. Environ. Sci. Pollut. Res. Int. 2016; 23, 8539-45.
D Lin and B Xing. Phytotoxicity of nanoparticles: Inhibition of seed germination and root growth. Environ. Pollut. 2007; 150, 243-50.
T Bai, P Zhang, Z Guo, AJ Chetwynd, M Zhang, M Adeel, M Li, K Guo, R Gao, J Li, Y Hao and Y Rui. Different physiological responses of C3 and C4 plants to nanomaterials. Environ. Sci. Pollut. Res. 2021; 28, 25542-51.
N Milani, GM Hettiarachchi, JK Kirby, DG Beak, SP Stacey and MJ McLaughlin. Fate of zinc oxide nanoparticles coated onto macronutrient fertilizers in an alkaline calcareous soil. PLos One 2015; 10, e0126275.
J Xu, X Luo, Y Wang and Y Feng. Evaluation of zinc oxide nanoparticles on lettuce (Lactuca sativa L.) growth and soil bacterial community. Environ. Sci. Pollut. Res. Int. 2018; 25, 6026-35.
WH Elmer and JC White. The use of metallic oxide nanoparticles to enhance growth of tomatoes and eggplants in disease infested soil or soilless medium. Environ. Sci. Nano 2016; 3, 1072-9.
MS Sheteiwy, Y Fu, Q Hu, A Nawaz, Y Guan, Z Li, Y Huang and J Hu. Seed priming with polyethylene glycol induces antioxidative defense and metabolic regulation of rice under nano-ZnO stress. Environ. Sci. Pollut. Res. Int. 2016; 23, 19989-20002.
H Zhang, R Wang, Z Chen, P Cui, H Lu, Y Yang and H Zhang. The effect of Zinc oxide nanoparticles for enhancing rice (Oryza sativa L.) yield and quality. Agriculture 2021; 11, 1247.
M Faizan, S Sehar, VD Rajput, A Faraz, S Afzal, T Minkina, S Sushkova, MF Adil, F Yu, AA Alatar, F Akhter and M Faisal. Modulation of cellular redox status and antioxidant defense system after synergistic application of zinc oxide nanoparticles and salicylic acid in rice (Oryza sativa) plant under arsenic stress. Plants 2021; 10, 2254.
Z Yang, J Chen, R Dou, X Gao, C Mao and L Wang. Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (Zea mays L.) and rice (Oryza sativa L.). Int. J. Environ. Res. Publ. Health 2015; 12, 15100-9.
MW Mazhar, M Ishtiaq, I Hussain, A Parveen, KH Bhatti, M Azeem, S Thind, M Ajaib, M Maqbool, T Sardar, K Muzammil and N Nasir. Seed nano-priming with zinc oxide nanoparticles in rice mitigates drought and enhances agronomic profile. PLos One 2022; 17, e0264967.
N Akhtar, S Khan, SU Rehman, ES Rha and M Jamil. Combined effect of zinc oxide nanoparticles and bacteria on osmolytes and antioxidative parameters of rice (Oryza sativa L.) plant grown in heavy metal-contaminated water. Adsorption Sci. Tech. 2022; 2022, 4148765.
United States Department of Agriculture (USDA), Available at: http://www.World agricultural production.com/crops/rice.aspx, accessed June 2022.
N Kumar, RS Chhokar, RP Meena, AS Kharub, SC Gill, SC Tripathi, OP Gupta, SK Mangrauthia, RM Sundaram, CP Sawant, A Gupta, A Naorem, M Kumar and GP Singh. Challenges and opportunities in productivity and sustainability of rice cultivation system: a critical review in Indian perspective. Cereal Res. Comm. 2022; 50, 573-601.
N Tyagi, R Raghuvanshi, MK Upadhyay, AK Srivastava, P Suprasanna and S Srivastava. Elemental (As, Zn, Fe and Cu) analysis and health risk assessment of rice grains and rice based food products collected from markets from different cities of Gangetic basin, India. J. Food Compos. Anal. 2020; 93, 103612.
A Kumar, K Gupta, Dixit, K Mishra and S Srivastava. A review on positive and negative impacts of nanotechnology in agriculture. Int. J. Environ. Sci. Tech. 2019; 16, 2175-84.
P Arunachalam, K Pandian, P Gnanasekaran and M Govindaraj. Zinc deficiency in Indian soils with special focus to enrich zinc in peanut. Afr. J. Agr. Res. 2013; 8, 6681-8.
F Wu, Q Fang, S Yan, L Pan, X Tang and W Ye. Effects of zinc oxide nanoparticles on arsenic stress in rice (Oryza sativa L.): Germination, early growth, and arsenic uptake. Environ. Sci. Pollut. Res. 2020; 27, 26974-81.
CO Dimkpa, U Singh, PS Bindraban, WH Elmer, JL Gardea-Torresdey and JC White. Zinc oxide nanoparticles alleviate drought-induced alterations in sorghum performance, nutrient acquisition, and grain fortification. Sci. Total Environ. 2019; 688, 926-34.
D Singh and A Kumar. Quantification of metal uptake in Spinacia oleracea irrigated with water containing a mixture of CuO and ZnO nanoparticles. Chemosphere 2020; 243, 125239.
PN Takkar, MV Singh and AN Ganeshmurthy. A critical review of plant nutrient supply needs, efficiency and policy issues for Indian agriculture for the year 2000: Micronutrients and trace elements. In: JS Kanwar and JC Katyal (Eds.). Plant nutrient, supply efficiency and policy issues: 2000 - 2025. National Academy of Agricultural Sciences, New Delhi, India, 1997, p. 238-64.
BJ Alloway. Zinc in soils and crop nutrition. IZA and IFA Brussels, France, 2008.
ML Jackson. Soil chemical analysis: Advanced course. University of Wisconsin-Madison Libraries Parallel Press, Madison, Wisconsin, 1979.
A Walkley and IA Black. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934; 37, 29-38.
BV Subbiah and GL Asija. A rapid procedure for the determination of available nitrogen in soils. Curr. Sci. 1956; 25, 259-60.
SR Olsen, CV Cole, FS Watanabe and LA Dean. Estimation of available phosphorus in soils by extraction with NaHCO3. United States Department of Agriculture, Washington, 1954.
WL Lindsay and WA Norvell. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci. Soc. Am. J. 1978; 42, 421-8.
MA Tabatabai and JM Bremner. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1969; 1, 301-7.
JM Bremner and LA Douglas. Inhibition of urease activity in soils. Soil Biol. Biochem. 1971; 3, 297-307.
DA Klein, TC Loh and RL Goulding. A rapid procedure to evaluate the dehydrogenase activity of soils low in organic matter. Soil Biol. Biochem. 1971; 3, 385-7.
D Salaskar, M Shrivastava and SP Kale. Bioremediation potential of spinach (Spinacia oleracea L.) for decontamination of cadmium in soil. Curr. Sci. 2011; 101, 1359-63.
DI Arnon. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 1949; 24, 1-15.
FAC Duxbury and CS Yentsch. Plankton pigment nomographs. J. Mar. Res. 1956; 15, 92-101.
DP Singh, V Singh, VK Gupta, R Shukla, R Prabha, BK Sarma and JS Patel. Microbial inoculation in rice regulates antioxidative reactions and defence related genes to mitigate drought stress. Sci. Rep. 2020; 10, 4818.
R Hoshmand. Experimental research design and analysis: A practical approach for agricultural and natural sciences. CRC Press, Boca Raton, Florida, 1993.
S Talam, SR Karumuri and N Gunnam. Synthesis, characterization, and spectroscopic properties of ZnO nanoparticles. Int. Sch. Res. Not. 2012; 2012, 372505.
DH Zhang, ZY Xue and QP Wang. Formation of ZnO nanoparticles by the reaction of zinc metal with aliphatic alcohols. J. Phys. D 2002; 35, 2837-40.
CO Dimkpa, DE Latta, JE McLean, DW Britt, MI Boyanov and AJ Anderson. Fate of CuO and ZnO nano-and microparticles in the plant environment. Environ. Sci. Tech. 2013; 47, 4734-42.
ML López-Moreno, GDL Rosa, JA Hernández-Viezcas, H Castillo-Michel, CE Botez, JR Peralta-Videa and JL Gardea-Torresdey. Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants. Environ. Sci. Tech. 2010; 44, 7315-20.
S Yan, F Wu, S Zhou, J Yang, X Tang and W Ye. Zinc oxide nanoparticles alleviate the arsenic toxicity and decrease the accumulation of arsenic in rice (Oryza sativa L.). BMC Plant Biol. 2021; 21, 150.
M Wissuwa, AB Ismail and RD Graham. Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. Plant Soil 2008; 306, 37-48.
RG Burns, JL DeForest, J Marxsen, RL Sinsabaugh, ME Stromberger, MD Wallenstein, MN Weintraub and A Zoppini. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol. Biochem. 2013; 58, 216-34.
K Liu, C Li, S Tang, G Shang, F Yu and Y Li. Heavy metal concentration, potential ecological risk assessment and enzyme activity in soils affected by a lead-zinc tailing spill in Guangxi, China. Chemosphere 2020; 251, 126415.
AS Karthikeyan, DK Varadarajan, UT Mukatira, MP D’Urzo, B Damsz and KG Raghothama. Regulated expression of Arabidopsis phosphate transporters. Plant Physiol. 2002; 130, 221-33.
B Byrnes, K Vilsmeier, E Austin and A Amberger. Degradation of the urease inhibitor phenyl phosphorodiamidate in solutions and floodwaters. J. Agr. Food Chem. 1989; 37, 473-7.
JT Trevors. Dehydrogenase activity in soil: A comparison between the INT and TTC assay. Soil Biol. Biochem. 1984; 16, 673-4.
AK Suresh, DA Pelletier and MJ Doktycz. Relating nanomaterial properties and microbial toxicity. Nanoscale 2012; 5, 463-74.
ZX Yang, SQ Lui, DW Zheng and SD Feng. Effect of cadmium, zinc and lead on soil enzyme activities. J. Environ. Sci. 2006; 18, 1135-41.
S Kim, J Kim and I Lee. Effects of Zn and ZnO nanoparticles and Zn2+ on soil enzyme activity and bioaccumulation of Zn in Cucumis sativus. Chem. Ecol. 2011; 27, 49-55.
B Li, Y Chen, WZ Liang, L Mu, WC Bridges, AR Jacobson and CJG Darnault. Influence of cerium oxide nanoparticles on the soil enzyme activities in a soil-grass microcosm system. Geoderma 2017; 299, 54-62.
M Adeel, N Shakoor, MA Ahmad, JC White, G Jilani and Y Rui. Bioavailability and toxicity of nanoscale/bulk rare earth oxides in soil: Physiological and ultrastructural alterations in Eisenia fetida. Environ. Sci. Nano 2021; 8, 1654-66.
S Chaperon and S Sauvé. Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biol. Biochem. 2007; 39, 2329-38.
F Gülser and E Erdoğan. The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ. Monit. Assess. 2008; 145, 127-33.
J Liu, B Dhungana and GP Cobb. Copper oxide nanoparticles and arsenic interact to alter seedling growth of rice (Oryza sativa japonica). Chemosphere 2018; 206, 330-37.
M Rizwan, S Ali, MZU Rehman, M Adrees, M Arshad, MF Qayyum, L Ali, A Hussain, SAS Chatha and M Imran. Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil. Environ. Pollut. 2019; 248, 358-67.
SJ Yoon, JI Kwak, WM Lee, PA Holden and YJ An. Zinc oxide nanoparticles delay soybean development: A standard soil microcosm study. Ecotoxicol. Environ. Saf. 2014; 100, 131-7.
P Mahajan, SK Dhoke and AS Khanna. Effect of nano-ZnO particle suspension on growth of mung (Vigna radiata) and gram (Cicer arietinum) seedlings using plant agar method. J. Nanotechnology 2011; 2011, 696535.
K Guo, A Hu, K Wang, L Wang, D Fu, Y Hao, Y Wang, A Ali, M Adeel, Y Rui and W Tan. Effects of spraying nano-materials on the absorption of metal(loid)s in cucumber. IET Nanobiotechnology 2019; 13, 712-9.
LJ Pang, M Adeel, N Shakoor, KR Guo, DF Ma, MA Ahmad, GQ Lu, MH Zhao, SE Li and YK Rui. Engineered nanomaterials suppress the soft rot disease (Rhizopus stolonifer) and slow down the loss of nutrient in sweet potato. Nanomaterials 2021; 11, 2572.
RJ DiMario, H Clayton, A Mukherjee, M Ludwig and JV Moroney. Plant carbonic anhydrases: Structures, locations, evolution, and physiological roles. Mol. Plant 2017; 10, 30-46.
N Priyanka and P Venkatachalam. Biofabricated zinc oxide nanoparticles coated with phycomolecules as novel micronutrient catalysts for stimulating plant growth of cotton. Adv. Nat. Sci. Nanoscience Nanotechnology 2016; 7, 045018.
YV Ivanov, YV Savochkin and VV Kuznetsov. Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 2 Functioning of antioxidant enzymes in pine seedlings under chronic zinc action. Russ. J. Plant Physiol. 2012; 59, 50-8.
DD Baccio, R Tognetti, L Sebastiani and C Vitagliano. Responses of Populus deltoides × Populus nigra (Populus × euramericana) clone I‐214 to high zinc concentrations. New Phytol. 2003; 159, 443-52.
IA Abreu and DE Cabelli. Superoxide dismutases - a review of the metal-associated mechanistic variations. Biochim. Biophys. Acta 2010; 1804, 263-74.
C Peng, H Tong, C Shen, L Sun, P Yuan, M He and J Shi. Bioavailability and translocation of metal oxide nanoparticles in the soil-rice plant system. Sci. Total Environ. 2020; 713, 136662.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Walailak University
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
