Abstract
Rice consumption is a key Cd exposure pathway, which poses a health risk to humans. Reducing cadmium (Cd) concentrations in rice remains challenging. In this study, a pot experiment was conducted to examine the effects of foliar spray of Zn combined with organic matters (including Zn–lysine (Zn-Lys), Zn–fulvic acid (Zn-FA), Zn–amino acid (Zn-AA), and Zn combined with glutathione (Zn + GSH)) on Cd accumulation in rice grains. Compared with the control group, all treatment groups exhibited reduced Cd concentration in rice grains, while improving plant growth, and reducing Cd transport from other tissues to the grains. Zn–FA was found to be the most effective fertilizer, which considerably reduced Cd concentrations in grains from 0.77 ± 0.068 to 0.14 ± 0.021 mg/kg and yielded reductions of up to 81%, which is within the Chinese food maximum tolerable limit of 0.2 mg/kg. Furthermore, the analysis of the chemical forms of Cd of rice tissues indicated that the treatment groups had increased proportions of integrated with pectates and protein in the stems. Except for the group treated with Zn–Lys spray, the percentages of undissolved Cd phosphate in the leaves were increased in all treatment groups, which reduced Cd toxicity to rice plants. The foliar application of Zn combined with organic matters may be a promising strategy to decrease Cd concentration in rice grains cultivated in severely Cd-contaminated agricultural soil, particularly in the karst area in southwest China with limited available cultivable agricultural land.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are available from the corresponding author on reasonable request.
References
Ali S, Bani Mfarrej MF, Hussain A, Akram NA, Rizwan M, Wang X, Maqbool A, Nafees M, Ali B (2022) Zinc fortification and alleviation of cadmium stress by application of lysine chelated zinc on different varieties of wheat and rice in cadmium stressed soil. Chemosphere 295:133829
Anjum SA, Wang L, Farooq M, XueAli LS (2011) Fulvic acid application improves the maize performance under well-watered and drought conditions. J Agron Crop Sci 197:409–417
Anwar Z, Basharat Z, Hafeez MB, Khan S, Zahra N, Rafique Z, Maqsood M (2021) Biofortification of maize with zinc and iron not only enhances crop growth but also improves grain quality. Asian J Agric Biol 2:202102079
Bocanegra MP, Lobartini JC, Orioli GA (2006) Plant uptake of iron chelated by humic acids of different molecular weights. Commun Soil Sci Plant Anal 37(1–2):239–248
Boonchuay P, Cakmak I, Rerkasem B, Prom-U-Thai C (2013) Effect of different foliar zinc application at different growth stages on seed zinc concentration and its impact on seedling vigor in rice. Soil Sci Plant Nutr 59:180–188
Braziene Z, Paltanavicius V, Avizienytė D (2021) The influence of fulvic acid on spring cereals and sugar beets seed germination and plant productivity. Environ Res 195:110824
Chen X, Zhang X, Chen H, Xu X (2022) Physiology and proteomics reveal fulvic acid mitigates cadmium adverse effects on growth and photosynthetic properties of lettuce. Plant Sci 323:111418
Dolev N, Katz Z, Ludmer Z, Ullmann A, Brauner N, Goikhman R (2020) Natural amino acids as potential chelators for soil remediation. Environ Res 183:109140
Drissi S, Houssa AA, Bamouh A, Benbella M (2015) Corn silage (Zea mays L.) response to zinc foliar spray concentration when grown on sandy soil. J Agr Sci 7(2):68
Du B, Zhou J, Lu B, Zhang C, Li D, Zhou J, Jiao S, Zhao K, Zhang H (2020) Environmental and human health risks from cadmium exposure near an active lead-zinc mine and a copper smelter. China Sci Total Environ 720:137585
Fahad S, Hussain S, Khan F, Wu C, Saud S, Hassan S, Ahmad N, Gang D, Ullah A, Huang J (2015) Effects of tire rubber ash and zinc sulfate on crop productivity and cadmium accumulation in five rice cultivars under field conditions. Environ Sci Pollut Res 22:12424–12434
Feng D, Huang C, Xu W, Qin Y, Li Y, Li T, Yang M, He Z (2020) Difference of cadmium bioaccumulation and transportation in two ryegrass varieties and the correlation between plant cadmium concentration and soil cadmium chemical forms. Wirel Pers Commun 110:291–307
Fu X, Dou C, Chen Y, Chen X, Shi J, Yu M, Xu J (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J Hazard Mater 186:103–107
Ghasemi S, Khoshgoftarmanesh AH, Afyuni M, Hadadzadeh H (2013) The effectiveness of foliar applications of synthesized zinc-amino acid chelates in comparison with zinc sulfate to increase yield and grain nutritional quality of wheat. Eur J Agron 45:68–74
Golden BR, Orlowski JM, Bond JA (2016) Corn injury from foliar zinc application does not affect grain yield. Agron J 108:2071–2075
Han X, Ren X, Wang P, Huang Y, Zhang C, Liu Z (2019) Effects of foliar application with zinc on the characteristics of cadmium accumulation in organs of rice plants. J of Agro-Environ Sci 38:1809–1817 (in Chinese)
Hussain B, Umer MJ, Li J, Ma Y, Abbas Y, Ashraf MN, Tahir N, Ullah A, Gogoi N, Farooq M (2021) Strategies for reducing cadmium accumulation in rice grains. J Clean Prod 286:125557
Ilyas N, Akhtar N Yasmin H, Sahreen S, Hasnain Z, Kaushik P, Ahmad A, Ahmad P (2022) Efficacy of citric acid chelate and Bacillus sp in amelioration of cadmium and chromium toxicity in wheat. Chemosphere 290:133342
Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208
Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ Pollut 147:750–756
Justi M, Morais EG, Silva CA (2019) Fulvic acid in foliar spray is more effective than humic acid via soil in improving coffee seedlings growth. Arch Agron Soil Sci 65:1969–1983
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol Plant 168:345–360
Khan MA, Castro-Guerrero N, Mendoza-Cozatl DG (2014) Moving toward a precise nutrition: preferential loading of seeds with essential nutrients over non-essential toxic elements. Front in Plant Sci 5:51
Kumar D, Dhankher OP, Tripathi RD, Seth CS (2023) Titanium dioxide nanoparticles potentially regulate the mechanism(s) for photosynthetic attributes, genotoxicity, antioxidants defense machinery, and phytochelatins synthesis in relation to hexavalent chromium toxicity in Helianthus annuus L. J Hazard Mater 454:131418
Li X (2019) Technical solutions for the safe utilization of heavy metal-contaminated farmland in China: a critical review. Land Degrad Dev 30:1773–1784
Lu Q, Xu Z, Xu X, Liu L, Liang L, Chen Z, Dong X, Li C, Wang Y, Qiu G (2019) Cadmium contamination in a soil-rice system and the associated health risk: an addressing concern caused by barium mining. Ecotox Environ Safe 183:109590
Lu D, Zhang C, Zhou Z, Huang D, Qin C, Nong Z, Ling C, Zhu Y, Chai X (2023) Pollution characteristics and source identification of farmland soils in Pb–Zn mining areas through an integrated approach. Environ Geochem Health 45:2533–2547
Luo N, Li X, Chen AY, Zhang LJ, Zhao HM, Xiang L, Cai QY, Mo CH, Wong MH, Li H (2017) Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Sci Total Environ 599:1564–1572
Lv G, Wang H, Xu C, Shuai H, Luo Z, Zhan Q, Zhu H, Wang S, Zhu Q, Zhang Y, Huang D (2019) Effectiveness of simultaneous foliar application of Zn and Mn or P to reduce Cd concentration in rice grains: a field study. Environ Sci Pollut Res 26:9305–9313
Mariyam S, Upadhyay SK, Chakraborty K, Verma KK, Duhan JS, Muneer S, Meena M, Sharma RK, Ghodake G, Seth CS (2024) Nanotechnology, a frontier in agricultural science, a novel approach in abiotic stress management and convergence with new age medicine-a review. Sci Total Environ 912:169097
Mei Q, Tian C, Zhou Q, Wu M, Zhang W, Tian X (2022) Effects of spraying zinc chelate fertilizer on the grain yield, zinc content and quality of rice. Hubei Agric Sci 61:27–31 (in Chinese)
Meng D, Xu P, Dong Q, Wang S, Wang Z (2017) Comparison of foliar and root application of potassium dihydrogen phosphate in regulating cadmium translocation and accumulation in tall fescue (Festuca arundinacea). Water Air Soil Pollut 228:1–8
Ministry of Ecology and Environment of People’s Republic of China (MEE) (2018) Soil Environmental Quality Risk Control Standard for Soil Contamination of Agricultural Land (GB 15618–2018). Beijing, China, pp 1–7. (in Chinese)
Nakamura S-I, Wongkaew A, Nakai Y, Rai H, Ohkama-Ohtsu N (2019) Foliar-applied glutathione activates zinc transport from roots to shoots in oilseed rape. Plant Sci 283:424–434
National Health Commission of the People’s Republic of China (NHC) (2017) Food safety standards, limits of contaminants in food (GB2762–2017). Beijing, China, pp. 1–18. (in Chinese)
Qin S, Liu H, Nie Z, Rengel Z, Gao W, Li C, Zhao P (2020) Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: a review. Pedosphere 30:168–180
Rehman MZU, Rizwan M, Rauf A, Ayub MA, Ali S, Qayyum MF, Waris AA, Naeem A, Sanaullah M (2019) Split application of silicon in cadmium (Cd) spiked alkaline soil plays a vital role in decreasing Cd accumulation in rice (Oryza sativa L.) grains. Chemosphere 226:454–462
Schroeder WH, Breuer U, Stelzer R, Gierth M (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149:167–192
Schwartz GG, Reis IM (2000) Is cadmium a cause of human pancreatic cancer? Cancer Epidem Biomark 9:139–145
Song J, Hui Y, Yu C, Zhang Q, Zhou Y, Li Y, Liu X, Zhu L, Hui D, Wan S (2017) Carbon balance under four double-season cropping systems in North China Plain. Plant Soil 421:319–336
Sui F-Q, Chang J-D, Tang Z, Liu W-J, Huang X-Y, Zhao F-J (2018) Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize. Plant Soil 433:377–389
The Ministry of Agriculture of the People’s Republic of China (2007) Determination of pH in soil. NY/T 1377–2007. (in Chinese)
Tian S, Liang S, Qiao K, Wang F, Zhang Y, Chai T (2019) Co-expression of multiple heavy metal transporters changes the translocation, accumulation, and potential oxidative stress of Cd and Zn in rice (Oryza sativa L.). J Hazard Mater 380: 120853
Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol 16:328–334
Wang Y, Yang R, Zheng J, Shen Z, Xu X (2019) Exogenous foliar application of fulvic acid alleviate cadmium toxicity in lettuce (Lactuca sativa L.). Ecotox Environ Safe 167:10–19
Wang S, Tian X, Liu Q (2020a) The effectiveness of foliar applications of zinc and biostimulants to increase zinc concentration and bioavailability of wheat grain. Agron 10:178
Wang Z, Wang H, Xu C, Lv G, Luo Z, Zhu H, Wang S, Zhu Q, Huang D, Li B (2020b) Foliar application of Zn-EDTA at early filling stage to increase grain Zn and Fe, and reduce grain Cd, Pb and grain yield in rice (Oryza sativa L.). B Environ Contam Tox 105:428–432
Wu FB, Dong J, Qian QQ, Zhang GP (2005) Subcellular distribution and chemical form of Cd and Cd-Zn interaction in different barley genotypes. Chemosphere 60:1437–1446
Wu Q, Magnus JH, Hentz JG (2010) Urinary cadmium, osteopenia, and osteoporosis in the US population. Osteoporosis Int 21:1449–1454
Xu XD (1986) The effect of foliar application of fulvic acid on water use, nutrient uptake and yield in wheat. Aust J Agric Res 37:343–350
Xu P, Wang Z (2013) Physiological mechanism of hypertolerance of cadmium in Kentucky bluegrass and tall fescue: chemical forms and tissue distribution. Environ Exp Bot 96:35–42
Xu W, Shi W, Yan F, Zhang B, Liang J (2011) Mechanisms of cadmium detoxification in cattail (Typha angustifolia L.). Aquat Bot 94:37–43
Yadav M, Gupta P, Seth CS (2022) Foliar application of α-lipoic acid attenuates cadmium toxicity on photosynthetic pigments and nitrogen metabolism in Solanum lycopersicum L. Acta Physiol Plant 44(11). https://doi.org/10.1007/s11738-022-03445-z
Yang X, Wang C, Huang Y, Liu B, Liu Z, Huang Y, Cheng L, Huang Y, Zhang C (2021) Foliar application of the sulfhydryl compound 2,3-dimercaptosuccinic acid inhibits cadmium, lead, and arsenic accumulation in rice grains by promoting heavy metal immobilization in flag leaves. Environ Pollut 285:117355
Yasmin H, Mazher J, Azmat A, Nosheen A, Naz R, Hassan MN, Noureldeen A, Ahmad P (2021) Combined application of zinc oxide nanoparticles and biofertilizer to induce salt resistance in safflower by regulating ion homeostasis and antioxidant defence responses. Ecotoxicol Environ Saf 218:112262
Zhang W, Lin K, Zhou J, Zhang W, Liu L, Zhang Q (2014) Cadmium accumulation, sub-cellular distribution and chemical forms in rice seedling in the presence of sulfur. Environ Toxicol Pharmacol 37:348–353
Zhao Y, Wu J, Shang D, Ning J, Zhai Y, Sheng X, Ding H (2015) Subcellular distribution and chemical forms of cadmium in the edible seaweed, Porphyra yezoensis. Food Chem 168:48–54
Zhen S, Shuai H, Xu C, Lv G, Zhu X, Zhang Q, Zhu Q, Nunez-Delgado A, Conde-Cid M, Zhou Y, Huang D (2021) Foliar application of Zn reduces Cd accumulation in grains of late rice by regulating the antioxidant system, enhancing Cd chelation onto cell wall of leaves, and inhibiting Cd translocation in rice. Sci Total Environ 770:145302
Zheng X, Cheng X, Pan N, Huang W, Shi L, Lu W (2022) Foliar spraying of mannose alleviates cadmium stress by changing the subcellular distribution and chemical forms of cadmium in wheat root. Agron 12:2273
Zhu P, Liang X-X, Wang P, Wang J, Gao Y-H, Hu S-G, Huang Q, Huang R, Jiang Q, Wu S-X, Li Z-X, Ling H-T, Xu Y-H, Wu Y-N, Zou F, Yang X-F (2016) Assessment of dietary cadmium exposure: a cross-sectional study in rural areas of south China. Food Control 62:284–290
Zulfiqar U, Hussain S, Ishfaq M, Matloob A, Ali N, Ahmad M, Alyemeni MN, Ahmad P (2020) Zinc-induced effects on productivity, zinc use efficiency, and grain biofortification of bread wheat under different tillage permutations. Agron 10:1566
Funding
This study was supported by the Science and Technology Planning Program of Guizhou Province (QianKeHe-pillar [2020]1Y123), the Doctoral Scientific Research Foundation of Guizhou Medical University (J [2021]069).
Author information
Authors and Affiliations
Contributions
QL: investigation, writing—original draft, writing—reviewing and editing, funding acquisition; ZX: investigation, methodology, writing—reviewing and editing; ZC: investigation, formal analysis; GQ: supervision, project administration, funding acquisition, writing—reviewing and editing.
Corresponding author
Ethics declarations
Ethics approval
This is not applicable.
Consent for participate
This is not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Elena Maestri
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lu, Q., Xu, Z., Chen, Z. et al. Effects of foliar application of Zn combined with organic matters on Cd accumulation and its chemical forms in rice. Environ Sci Pollut Res 31, 25182–25191 (2024). https://doi.org/10.1007/s11356-024-32808-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-024-32808-x