Abstract
Soil cadmium (Cd) contamination poses adverse impacts on crop yield and quality. Maize is a widely cultivated cereal throughout the world. In this study, field and hydroponic experiments were conducted to investigate the genotypic difference in Cd accumulation and tolerance in maize. There were significant genotypic differences in grain Cd concentrations among 95 genotypes. From these 95 genotypes, L42 which showed a higher grain Cd concentration and L63 which showed a lower grain Cd concentration was selected for further study. Under Cd stress, L63 showed much less reduction in plant growth than L42 compared with the control. Seedlings of L63 recorded higher Cd concentration in roots, but lower in shoots L42, indicating that the low grain Cd concentration in L63 is mainly due to the low rate of transportation of Cd from roots to shoots. Most Cd accumulated in epidermis and xylem vessels of L63, while the green fluorescent was found across almost the entire cross-section of root in L42. Obvious ultrastructural damage was observed in L42 under Cd stress, especially in mesophyll cells, while L63 was less affected. These findings could contribute to developing low Cd accumulation and high tolerance maize cultivars.
Similar content being viewed by others
Data availability
All data can be found in the manuscript.
References
Cai Y, Cao FB, Wei K, Zhang GP, Wu FB (2011) Genotypic dependent effect of exogenous glutathione on Cd-induced changes in proteins, ultrastructure and antioxidant defense enzymes in rice seedlings. J Hazard Mater 192:1056–1066. https://doi.org/10.1016/j.jhazmat.2011.06.011
Cao FB, Wang RF, Cheng WD, Zeng FR, Ahmed IM, Hu XN, Zhang GP, Wu FB (2014a) Genotypic and environmental variation in cadmium, chromium, lead and copper in rice and approaches for reducing the accumulation. Sci Total Environ 496:275–281. https://doi.org/10.1016/j.scitotenv.2014.07.064
Cao FB, Chen F, Sun HY, Zhang GP, Chen ZH, Wu FB (2014b) Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics 15:611. https://doi.org/10.1186/1471-2164-15-611
Cao FB, Dai HX, Hao PF, Wu FB (2020) Silicon regulates the expression of vacuolar H+-pyrophosphatase 1 and decreases cadmium accumulation in rice (Oryza sativa L.). Chemosphere 240:124907. https://doi.org/10.1016/j.chemosphere.2019.124907
Catav SS, Genc TO, Oktay MK, Kucukakyuz K (2020) Cadmium toxicity in wheat: impacts on element contents, antioxidant enzyme activities, oxidative stress, and genotoxicity. Bull Environ Contam Toxicol 104:71–77. https://doi.org/10.1007/s00128-019-02745-4
Cheng K, Tian HZ, Zhao D, Lu L, Wang Y, Chen J, Liu XG, Jia WX, Huang Z (2014) Atmospheric emission inventory of cadmium from anthropogenic sources. Int J Environ Sci Technol 11:605–616. https://doi.org/10.1007/s13762-013-0206-3
de Araujo RP, de Almeida AAF, Pereira LS, Mangabeira PAO, Souza JO, Pirovani CP, Ahnert D, Baligar VC (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotox Environ Safe 144:148–157. https://doi.org/10.1016/j.ecoenv.2017.06.006
Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Goncalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289. https://doi.org/10.1007/s11738-012-1167-8
Duan GL, Shao GS, Tang Z, Chen HP, Wang BX, Tang Z, Yang YP, Liu YC, Zhao FJ (2017) Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars. Rice 10:9. https://doi.org/10.1186/s12284-017-0149-2
Harris NS, Taylor GJ (2013) Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biol 13. https://doi.org/10.1186/1471-2229-13-103
Kanu AS, Ashraf U, Mo ZW, Fuseini I, Mansaray LR, Duan MY, Pan SG, Tang XR (2017) Cadmium uptake and distribution in fragrant rice genotypes and related consequences on yield and grain quality traits. J Chem 2017:1405878. https://doi.org/10.1155/2017/1405878
Kaya C, Okant M, Ugurlar F, Alyemeni MN, Ashraf M, Ahmad P (2019) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere 225:627–638. https://doi.org/10.1016/j.chemosphere.2019.03.026
Khan A, Khan S, Khan MA, Qamar Z, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res 22:13772–13799. https://doi.org/10.1007/s11356-015-4881-0
Khan S, Munir S, Sajjad M, Li G (2016) Urban park soil contamination by potentially harmful elements and human health risk in Peshawar City, Khyber Pakhtunkhwa, Pakistan. J Geochem Explor 165:102–110. https://doi.org/10.1016/j.gexplo.2016.03.007
Kollarova K, Kamenicka V, Vatehova Z, Liskova D (2018) Impact of galactoglucomannan oligosaccharides and Cd stress on maize root growth parameters, morphology, and structure. J Plant Physiol 222:59–66. https://doi.org/10.1016/j.jplph.2017.12.017
Lekeux G, Crowet JM, Nouet C, Joris M, Jadoul A, Bosman B, Carnol M, Motte P, Lins L, Galleni M, Hanikenne M (2019) Homology modeling and in vivo functional characterization of the zinc permeation pathway in a heavy metal P-type ATPase. J Exp Bot 70:329–341. https://doi.org/10.1093/jxb/ery353
Li M, Hao PF, Cao FB (2017a) Glutathione-induced alleviation of cadmium toxicity in Zea mays. Plant Physiol Biochem 119:240–249. https://doi.org/10.1016/j.plaphy.2017.09.005
Li H, Luo N, Li YW, Cai QY, Li HY, Mo CH, Wong MH (2017b) Cadmium in rice: transport mechanisms, influencing factors, and minimizing measures. Environ Pollut 224:622–630. https://doi.org/10.1016/j.envpol.2017.01.087
Liu JG, Qu P, Zhang W, Dong Y, Li L, Wang MX (2014) Variations among rice cultivars in subcellular distribution of Cd: the relationship between translocation and grain accumulation. Environ Exp Bot 107:25–31. https://doi.org/10.1016/j.envexpbot.2014.05.004
Liu Y, Zhang CB, Zhao YL, Sun SJ, Liu ZQ (2017) Effects of growing seasons and genotypes on the accumulation of cadmium and mineral nutrients in rice grown in cadmium contaminated soil. Sci Total Environ 579:1282–1288. https://doi.org/10.1016/j.scitotenv.2016.11.115
Luo JS, Huang J, Zeng DL, Peng JS, Zhang GB, Ma HL, Guan Y, Yi HY, Fu YL, Han B, Lin HX, Qian Q, Gong JM (2018) A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9:645. https://doi.org/10.1038/s41467-018-03088-0
Maccaferri M, Harris NS, Twardziok SO et al (2019) Durum wheat genome highlights past domestication signatures and future improvement targets. Nat Genet 51(5):885. https://doi.org/10.1038/s41588-019-0381-3
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P-1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189(1):190–199. https://doi.org/10.1111/j.1469-8137.2010.03459.x
Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14(5):554–562. https://doi.org/10.1016/j.pbi.2011.07.004
OECD FAO (2019) OECD-FAO Agricultural outlook. OECD agriculture statistics, Paris
Ogawa I, Nakanishi H, Ishimaru Y, Takahashi M, Mori S, Nishizawa NK (2006) Fe-deficiency enhanced Cd uptake and translocation by Fe2+-transporters, OsIRT1 and OsIRT2, in rice. Plant Cell Physiol 47:S231–S231. https://doi.org/10.1111/j.1747-0765.2006.00055.x
Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Rehman MZU, Waris AA (2019) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277. https://doi.org/10.1016/j.chemosphere.2018.09.120
Romero-Puertas MC, Terron-Camero LC, Pelaez-Vico MA, Olmedilla A, Sandalio LM (2019) Reactive oxygen and nitrogen species as key indicators of plant responses to Cd stress. Environ Exp Bot 161:107–119. https://doi.org/10.1016/j.envexpbot.2018.10.012
Sanaeiostovar A, Khoshgoftarmanesh AH, Shariatmadari H, Afyuni M, Schulin R (2012) Combined effect of zinc and cadmium levels on root antioxidative responses in three different zinc-efficient wheat genotypes. J Agron Crop Sci 198(4):276–285. https://doi.org/10.1111/j.1439-037X.2012.00504.x
Song Y, Jin L, Wang XJ (2017) Cadmium absorption and transportation pathways in plants. Int J Phytoremediat 19:133–141. https://doi.org/10.1080/15226514.2016.1207598
Sun HY, Cao FB, Wang NB, Zhang M, Ahmed IM, Zhang GP, Wu FB (2013) Differences in grain ultrastructure, phytochemical and proteomic profiles between the two contrasting grain Cd-accumulation barley genotypes. PLoS ONE 8:11. https://doi.org/10.1371/journal.pone.0079158
Tang QY, Feng M (2010) DPS Data processing system:experimental design, statistical analysis and mining.
Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182:644–653. https://doi.org/10.1111/j.1469-8137.2009.02784.x
Uraguchi S, Kamiya T, Clemens S, Fujiwara T (2014) Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa.). Physiol Plant 151:339–347. https://doi.org/10.1111/ppl.12189
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688. https://doi.org/10.1093/jxb/erp119
Wang P, Chen HP, 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
Wu DZ, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016) The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172:1899–1910. https://doi.org/10.1104/pp.16.01189
Yu Y, Zhou XY, Zhu ZH, Zhou KJ (2019) Sodium hydrosulfide mitigates cadmium toxicity by promoting cadmium retention and inhibiting its translocation from roots to shoots in Brassica napus. Agric Food Chem 67:433–440. https://doi.org/10.1021/acs.jafc.8b04622
Acknowledgements
This work was supported by funding from the National Natural Science Foundation of China (31501233) and the Natural Science Foundation of Zhejiang Province (LY20C130007).
Author information
Authors and Affiliations
Contributions
HD and FC planned and designed the research; KL, DVW, and MZ carried out experiments; DVW and FC analysed data; KL, DVW, HD, and FC drafted the manuscript. IA revised the manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Gangrong Shi
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Kaina Lin and Darron V. Williams contributed equally to this work.
Rights and permissions
About this article
Cite this article
Lin, K., Williams, D.V., Zeng, M. et al. Identification of low grain cadmium accumulation genotypes and its physiological mechanism in maize (Zea mays L.). Environ Sci Pollut Res 29, 20721–20730 (2022). https://doi.org/10.1007/s11356-021-16991-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16991-9