Abstract
Iron (Fe) fertilizer can reduce cadmium (Cd) uptake and toxicity in rice, but the underlying mechanisms of Cd mitigation by different fertilizers are poorly understood. Here, pot experiments in rice were conducted to characterize the effects of four types of foliar-applied Fe fertilizer (chelated ferrous Fe, ferric Fe, ionic ferrous Fe, and ferric Fe) at three doses (20, 50, and 100 mg L−1) on photosynthetic capacity, antioxidant ability, yield, and Cd accumulation in Cd-contaminated soil. The results showed that foliar Fe application increased the net photosynthesis rate by 19.3%, peroxidase (POD) by 18.2%, superoxide dismutase (SOD) by 26.9%, and catalase (CAT) by 19.6%, and led to a 7.2% increase in grain yield compared with the control. Moreover, foliar Fe application significantly reduced Cd accumulation by 15.9% in brown rice and decreased the translocation of Cd from roots to other plant tissues. Overall, application of moderate doses (50 mg L−1) of chelated ferrous Fe was the most effective method for reducing Cd uptake (decreasing the Cd concentration in brown rice by 29.0%) and toxicity in rice (decreasing malondialdehyde by 23.2% and increasing POD, SOD, and CAT by 54.4%, 51.6%, and 45.7%, respectively), which may stem from the fact that chelated ferrous Fe was a more stable and bioavailable source of Fe for rice. The Cd concentration in rice had negative relationship with Fe concentration, and the translocation of Cd from root to the other tissues was reduced by the higher Fe nutrition status in leaf, suggesting that a high Fe supply may decrease Cd content by inhibiting the expression of the Fe transport system. These results indicate that foliar application of chelated ferrous Fe provides a promising alternative approach for enhancing growth and controlling Cd accumulation in rice plants. Furthermore, these results advance our understanding of the associations between plant Fe nutrition status and Cd accumulation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbas T, Rizwan M, Ali S, Zia-ur-Rehman M, Farooq Qayyum M, Abbas F, Hannan F, Rinklebe J, Sik Ok Y (2017) Effect of biochar on cadmium bioavailability and uptake in wheat (Triticum aestivum L.) grown in a soil with aged contamination. Ecotoxicol Environ Saf 140:37–47. https://doi.org/10.1016/j.ecoenv.2017.02.028
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Alidoust D, Isoda A (2013) Effect of γFe2O3 nanoparticles on photosynthetic characteristic of soybean (Glycine max (L.) Merr.): foliar spray versus soil amendment. Acta Physiol Plant 35:3365–3375. https://doi.org/10.1007/s11738-013-1369-8
Bashir K, Ishimaru Y, Nishizawa NK (2010) Iron uptake and loading into rice grains. Rice 3:122–130. https://doi.org/10.1007/s12284-010-9042-y
Bashir A, Rizwan M, Ali S, Zia ur Rehman M, Ishaque W, Atif Riaz M, Maqbool A (2018) Effect of foliar applied iron complexed with lysine on growth and cadmium (Cd) uptake in rice under Cd stress. Environ Sci Pollut Res 25:20691–20699. https://doi.org/10.1007/s11356-018-2042-y
Bolan N, Adriano DC, Duraisamy P et al (2003) Immobilization and phytoavailability of cadmium in variable charge soils. I. Effect of phosphate addition. Plant Soil 250:83–94. https://doi.org/10.1023/a:1022826014841
Chen Z, Tang YT, Yao AJ, Cao J, Wu ZH, Peng ZR, Wang SZ, Xiao S, Baker AJM, Qiu RL (2017a) Mitigation of Cd accumulation in paddy rice (Oryza sativa L.) by Fe fertilization. Environ Pollut 231:549–559. https://doi.org/10.1016/j.envpol.2017.08.055
Chen Z, Tang YT, Zhou C, Xie ST, Xiao S, Baker AJM, Qiu RL (2017b) Mechanisms of Fe biofortification and mitigation of Cd accumulation in rice (Oryza sativa L.) grown hydroponically with Fe chelate fertilization. Chemosphere 175:275–285. https://doi.org/10.1016/j.chemosphere.2017.02.053
Chen J, Zou W, Meng L, Fan X, Xu G, Ye G (2019) Advances in the uptake and transport mechanisms and QTLs mapping of cadmium in rice. Int J Mol Sci 20:3417. https://doi.org/10.3390/ijms20143417
Choppala G, Saifullah BN et al (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391. https://doi.org/10.1080/07352689.2014.903747
Duan MM, Wang S, Huang DY, Zhu QH, Liu SL, Zhang Q, Zhu HH, Xu C (2018) Effectiveness of simultaneous applications of lime and zinc/iron foliar sprays to minimize cadmium accumulation in rice. Ecotoxicol Environ Saf 165:510–515. https://doi.org/10.1016/j.ecoenv.2018.09.037
Fang Y, Wang L, Xin Z, Zhao L, An X, Hu Q (2008) Effect of foliar application of zinc, selenium, and iron fertilizers on nutrients concentration and yield of rice grain in China. J Agric Food Chem 56:2079–2084. https://doi.org/10.1021/jf800150z
Fernández V, Ebert G (2005) Foliar iron fertilization: a critical review. J Plant Nutr 28:2113–2124. https://doi.org/10.1080/01904160500320954
Fernández V, Del Río V, Abadía J, Abadía A (2006) Foliar iron fertilization of peach (Prunus persica (L.) Batsch): effects of iron compounds, surfactants and other adjuvants. Plant Soil 289:239–252. https://doi.org/10.1007/s11104-006-9132-1
Gao L, Chang J, Chen R, Li H, Lu H, Tao L, Xiong J (2016) Comparison on cellular mechanisms of iron and cadmium accumulation in rice: prospects for cultivating Fe-rich but Cd-free rice. Rice 9:1–12. https://doi.org/10.1186/s12284-016-0112-7
Grusak MA, Pezeshgi S (1996) Shoot-to-root signal transmission regulates root Fe (III) reductase activity in the dgl mutant of pea. Plant Physiol 110:329–334. https://doi.org/10.1104/pp.110.1.329
Hasegawa H, Rahman MM, Kadohashi K, Takasugi Y, Tate Y, Maki T, Rahman MA (2012) Significance of the concentration of chelating ligands on Fe3+-solubility, bioavailability, and uptake in rice plant. Plant Physiol Biochem 58:205–211. https://doi.org/10.1016/j.plaphy.2012.07.004
He W, Shohag MJI, Wei Y, Feng Y, Yang X (2013) Iron concentration, bioavailability, and nutritional quality of polished rice affected by different forms of foliar iron fertilizer. Food Chem 141:4122–4126. https://doi.org/10.1016/j.foodchem.2013.07.005
Hu Y, Cheng H, Tao S (2016) The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environ Int 92:515–532. https://doi.org/10.1016/j.envint.2016.04.042
Huang Y, Wang L, Wang W, Li T, He Z, Yang X (2019) Current status of agricultural soil pollution by heavy metals in China: a meta-analysis. Sci Total Environ 651:3034–3042. https://doi.org/10.1016/j.scitotenv.2018.10.185
Hussain A, Ali S, Rizwan M, Rehman MZ, Qayyum MF, Wang H, Rinklebe J (2019) Responses of wheat (Triticum aestivum) plants grown in a Cd contaminated soil to the application of iron oxide nanoparticles. Ecotoxicol Environ Saf 173:156–164. https://doi.org/10.1016/j.ecoenv.2019.01.118
Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346. https://doi.org/10.1111/j.1365-313X.2005.02624.x
Khan MA, Ding X, Khan S, Brusseau ML, Khan A, Nawab J (2018) The influence of various organic amendments on the bioavailability and plant uptake of cadmium present in mine-degraded soil. Sci Total Environ 636:810–817. https://doi.org/10.1016/j.scitotenv.2018.04.299
Kobayashi J (1978) Pollution by cadmium and the itai-itai disease in Japan. In: Oehme FW (ed) Toxicity of heavy metals in the environment, part 1. Marcel Dekker, New York
Konate A, He X, Zhang Z, Ma Y, Zhang P, Alugongo G, Rui Y (2017) Magnetic (Fe3O4) nanoparticles reduce heavy metals uptake and mitigate their toxicity in wheat seedling. Sustainability 9:1–16. https://doi.org/10.3390/su9050790
Lei M, Pan Y, Chen C et al (2019) Application of economic plant for remediation of cadmium contaminated soils: three mulberry (Moms alba L.) varieties cultivated in two polluted fields. Chemosphere 236:124379. https://doi.org/10.1016/j.chemosphere.2019.124379
Liu H, Zhang J, Christie P, Zhang F (2008) Influence of iron plaque on uptake and accumulation of Cd by rice (Oryza sativa L.) seedlings grown in soil. Sci Total Environ 394:361–368. https://doi.org/10.1016/j.scitotenv.2008.02.004
Liu H, Zhang C, Wang J, Zhou C, Feng H, Mahajan MD, Han X (2017) Influence and interaction of iron and cadmium on photosynthesis and antioxidative enzymes in two rice cultivars. Chemosphere 171:240–247. https://doi.org/10.1016/j.chemosphere.2016.12.081
Lu C, Zhang L, Tang Z, Huang, et al. (2019) Producing cadmium-free Indica rice by overexpressing OsHMA3. Environ Int 126:619–626. https://doi.org/10.1016/j.envint.2019.03.004
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Science and Plant Nutrition 52:464–469. https://doi.org/10.1111/j.1747-0765.2006.00055.x
Peng JF, Song YH, Yuan P, Cui XY, Qiu GL (2009) The remediation of heavy metals contaminated sediment. J Hazard Mater 161:633–640. https://doi.org/10.1016/j.jhazmat.2008.04.061
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rai PK, Lee SS, Zhang M, Tsang YF, Kim KH (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385. https://doi.org/10.1016/j.envint.2019.01.067
Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879. https://doi.org/10.1007/s11356-016-6436-4
Rizwan M, Ali S, Qayyum MF, Ok YS, Adrees M, Ibrahim M, Zia-ur-Rehman M, Farid M, Abbas F (2017) Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review. J Hazard Mater 322:2–16. https://doi.org/10.1016/j.jhazmat.2016.05.061
Rizwan M, Ali S, Rehman MZ et al (2018) Cadmium phytoremediation potential of Brassica crop species: a review. Sci Total Environ 631–632:1175–1191. https://doi.org/10.1016/j.scitotenv.2018.03.104
Rizwan M, Ali S, ur Rehman MZ et al (2019a) Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil. Environ Pollut 248:358–367. https://doi.org/10.1016/j.envpol.2019.02.031
Rizwan M, Noureen S, Ali S, Anwar S, Rehman MZ, Qayyum MF, Hussain A (2019b) Influence of biochar amendment and foliar application of iron oxide nanoparticles on growth, photosynthesis, and cadmium accumulation in rice biomass. J Soils Sediments 19:1–11. https://doi.org/10.1007/s11368-019-02327-1
Sarwar N, Malhi SS, Zia MH et al (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937. https://doi.org/10.1002/jsfa.3916
Sebastian A, Prasad MNV (2015) Iron- and manganese-assisted cadmium tolerance in Oryza sativa L.: lowering of rhizotoxicity next to functional photosynthesis. Planta 241:1519–1528. https://doi.org/10.1007/s00425-015-2276-6
Shao G, Chen M, Wang W, Mou R, Zhang G (2007) Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regul 53:33–42. https://doi.org/10.1007/s10725-007-9201-3
Shao GS, Chen MX, Wang DY, Xu CM, Mou RX, Cao ZY, Zhang XF (2008) Using iron fertilizer to control Cd accumulation in rice plants: a new promising technology. Sci China Ser C Life Sci 51:245–253. https://doi.org/10.1007/s11427-008-0031-y
Sharma SS, Kaul S, Metwally A, Goyal KC, Finkemeier I, Dietz KJ (2004) Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Sci 166:1287–1295. https://doi.org/10.1016/j.plantsci.2004.01.006
Vert GA, Briat JF, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804. https://doi.org/10.1104/pp.102.016089
Vigani G, Zocchi G, Bashir K, Philippar K, Briat JF (2013) Signals from chloroplasts and mitochondria for iron homeostasis regulation. Trends Plant Sci 18:305–311. https://doi.org/10.1016/j.tplants.2013.01.006
Wang X, Yao H, Wong MH, Ye Z (2013) Dynamic changes in radial oxygen loss and iron plaque formation and their effects on Cd and As accumulation in rice (Oryza sativa L.). Environ Geochem Health 35:779–788. https://doi.org/10.1007/s10653-013-9534-y
Wang Y, Jiang X, Li K, Wu M, Zhang R, Zhang L, Chen G (2014) Photosynthetic responses of Oryza sativa L. seedlings to cadmium stress: physiological, biochemical and ultrastructural analyses. Biometals 27:389–401. https://doi.org/10.1007/s10534-014-9720-0
Wang P, Chen H, Kopittke PM, Zhao FJ (2019) Cadmium contamination in agricultural soils of China and the impact on food safety. Environ Pollut 249:1038–1048. https://doi.org/10.1016/j.envpol.2019.03.063
Yu H, Wang J, Fang W, Yuan J, Yang Z (2006) Cadmium accumulation in different rice cultivars and screening for pollution-safe cultivars of rice. Sci Total Environ 370:302–309. https://doi.org/10.1016/j.scitotenv.2006.06.013
Zacchini M, Pietrini F, Mugnozza GS et al (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut 197:23–34. https://doi.org/10.1007/s11270-008-9788-7
Zhang XZ (1992) The measurement and mechanism of lipid peroxidation and SOD POD and CAT activities in biological system. In: Zhang XZ (ed) Research methodology of crop physiology. Beijing Agriculture Press, Beijing, pp 208–211
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50. https://doi.org/10.1016/j.chemosphere.2006.10.007
Availability of data and materials
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
Funding
The Ministry of Science and Technology of China (2018YFD0800700) and National Natural Science Foundation of China (41671475).
Author information
Authors and Affiliations
Contributions
Xinqi Wang, Sihan Deng and Ming Lei designed research; Xinqi Wang, Sihan Deng, Yimin Zhou, Jiumei Long performed research; Xinqi Wang and Sihan Deng analyzed data; Xinqi Wang wrote the manuscript. All authors revised and reviewed the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Responsible Editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 41.3 kb).
Rights and permissions
About this article
Cite this article
Wang, X., Deng, S., Zhou, Y. et al. Application of different foliar iron fertilizers for enhancing the growth and antioxidant capacity of rice and minimizing cadmium accumulation. Environ Sci Pollut Res 28, 7828–7839 (2021). https://doi.org/10.1007/s11356-020-11056-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-11056-9