SpringerLink
Log in

Differences of cadmium uptake and accumulation in roots of two maize varieties (Zea mays L.)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Different maize varieties respond differentially to cadmium (Cd) stress. As the first organ in contact with the soil, the response of the root is particularly important. However, the physiological mechanisms that determine the response are not well defined. Here, we compared the differences in Cd-induced related gene expression, ionic homeostasis, and ultrastructural changes in roots of Cd-tolerant maize variety (XR57) and Cd-sensitive maize variety (LY296), and assessed their effects on Cd uptake and accumulation. Our findings indicate that XR57 absorbed a significantly lower Cd than LY296 did, and that the expression levels of genes related to Cd uptake (ZmNRAMP5 and ZmZIP4) and efflux (ZmABCG4) in the root were consistent with the Cd absorption at the physiological levels. Compared with LY296, the lower Cd concentration in the roots of XR57 caused less interference with the ion balance. Transmission electron microscope images revealed that the roots from XR57 exposed to Cd had developed thicker cell walls than LY296. In addition, the large increase ZmABCC1 and ZmABCC2 expression levels in XR57 mediated the appearance of numerous electron-dense granules in the vacuoles present in the roots. As a result, the high Cd tolerance of XR57 is the result of a multi-level response that involves increased resistance to Cd uptake, a stronger capacity for vacuolar regionalization, and the formation of thicker cell walls. These findings may provide a theoretical basis for maize cultivation in Cd-contaminated areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Andosch A, Affenzeller MJ, Lütz C, Lütz-Meindl U (2012) A freshwater green alga under cadmium stress: ameliorating calcium effects on ultrastructure and photosynthesis in the unicellular model Micrasterias. J Plant Physiol 169:1489–1500

    CAS  Google Scholar 

  • Chen XH, Ouyang Y, Fan YC, Qiu BY, Zhang GP, Zeng FR (2018) The pathway of transmembrane cadmium influx via calcium-permeable channels and its spatial characteristics along rice root. J Exp Bot 69:5279–5291

    CAS  Google Scholar 

  • Cui JH, Liu TX, Li YD, Li FB (2018) Selenium reduces cadmium uptake into rice suspension cells by regulating the expression of lignin synthesis and cadmium-related genes. Sci Total Environ 644:602–610

    CAS  Google Scholar 

  • Daud MK, Sun YQ, Dawood M, Hayat Y, Variath MT, Wu YX, Raziuddin MU, Salahuddin NU, Zhu SJ (2009) Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463–473

    CAS  Google Scholar 

  • Fioroto AM, Albuquerque LGR, Carvalho AAC, Oliveira AP, Rodrigues F, Oliveira PV (2020) Hydroponic growth test of maize sprouts to evaluate As, Cd, Cr and Pb translocation from mineral fertilizer and As and Cr speciation. Environ Pollut 262:114216–114225

    CAS  Google Scholar 

  • Ge W, Jiao YQ, Sun BL, Qin R, Jiang WS, Liu DH (2012) Cadmium-mediated oxidative stress and ultrastructural changes in root cells of poplar cultivars. S Afr J Bot 83:98–108

    CAS  Google Scholar 

  • Gupta P, Seth CS (2022) 24-Epibrassinolide regulates functional components of nitric oxide signalling and antioxidant defense pathways to alleviate salinity stress in Brassica juncea L. cv. Varuna. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10884-

    Article  Google Scholar 

  • Han MX, Ullah H, Yang H, Yu G, You SH, Liu J, Chen BL, Shahab A, Antoniadis V, Shaheen SM, Rinklebe J (2023) Cadmium uptake and membrane transport in roots of hyperaccumulator Amaranthus hypochondriacus L. Environ Pollut 331:121846–121853

    CAS  Google Scholar 

  • Huang HL, Li M, Rizwan M, Dai ZH, Yuan Y, Hossain MM, Cao MH, **ong SL, Tu SX (2021a) Synergistic effect of silicon and selenium on the alleviation of cadmium toxicity in rice plants. J Hazard Mater 401:123393–123403

    CAS  Google Scholar 

  • Huang YF, Chen JH, Zhang DR, Fang B, Yang JT, Zou JW, Chen YH, Su NN, Cui J (2021b) Enhanced vacuole compartmentalization of cadmium in root cells contributes to glutathione-induced reduction of cadmium translocation from roots to shoots in pakchoi (Brassica chinensis L.). Ecotox Environ Safe 208:111616–111625

    CAS  Google Scholar 

  • Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Nati Acad Sci USA 109:19166–19171

    CAS  Google Scholar 

  • Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286–293

    Google Scholar 

  • Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11:255–277

    CAS  Google Scholar 

  • Javed MT, Akram MS, Tanwir K, Chaudhary HJ, Qasim A, Stoltz E, Lindberg S (2017) Cadmium spiked soil modulates root organic acids exudation and ionic contents of two differentially Cd tolerant maize (Zea mays L.) cultivars. Ecotox Environ Safe 141:216–225

    CAS  Google Scholar 

  • Khan MD, Mei L, Ali B, Chen Y, Cheng X, Zhu SJ (2013) Cadmium-induced upregulation of lipid peroxidation and reactive oxygen species caused physiological, biochemical, and ultrastructural changes in upland cotton seedlings. BioMed Res Int 2013:374063–374072

    Google Scholar 

  • Khan ZS, Rizwan M, Hafeez M, Ali S, Javed MR, Adrees M (2019) The accumulation of cadmium in wheat (Triticum aestivum) as influenced by zinc oxide nanoparticles and soil moisture conditions. Environ Sci Pollut Res 26:19859–19870

    CAS  Google Scholar 

  • Kim DY, Bovet L, Masayoshi M, Enrico M, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50:207–218

    CAS  Google Scholar 

  • Kollárováa K, Kamenickáb V, Vatehováa Z, Lišková D (2018) Impact of galactoglucomannan oligosaccharides and Cd stress on maize root growth parameters, morphology, and structure. J Plant Physiol 222:59–66

    Google Scholar 

  • 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 454:131418–131430

    CAS  Google Scholar 

  • Lavres J, Rabêlo FHS, Capaldi FR, Reis AR, Rosssi ML, Franco MR, Azevedo RA, Abreu-Junior CH, Nogueir NL (2019) Investigation into the relationship among Cd bioaccumulation, nutrient composition, ultrastructural changes and antioxidative metabolism in lettuce genotypes under Cd stress. Ecotox Environ Safe 170:578–589

    CAS  Google Scholar 

  • Li C, Liu Y, Tian J, Tian J, Zhu YS, Fan JJ (2020) Changes in sucrose metabolism in maize varieties with different cadmium sensitivities under cadmium stress. PLoS 15:1–16

    CAS  Google Scholar 

  • Liu HY, Liao BH, Lu SQ (2004) Toxicity of surfactant, acid rain and Cd2+ combined pollution to the nucleus of Vicia faba root tip cells. Chinese J Applied Environm Biol 15:493–496

    CAS  Google Scholar 

  • Liu JJ, Wei Z, Li JH (2014) Effects of copper on leaf membrane structure and root activity of maize seedling. Bot Stud 55:47–52

    Google Scholar 

  • Lux A, Martinka M, Vaculí M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    CAS  Google Scholar 

  • Ma JF, Shen RF, Shao JF (2021) Transport of cadmium from soil to grain in cereal crops: a review. Pedosphere 31:3–10

    CAS  Google Scholar 

  • Mclaughlin MJ, Smolders E, Zhao FJ, Grant C, Montalvo D (2020) Managing cadmium in agricultural systems. Adv Agron 166:1–129

    Google Scholar 

  • Muneer S, Jeong BR, Kim TH, Lee JH, Soundararajan P (2014) Transcriptional and physiological changes in relation to Fe uptake under conditions of Fe-deficiency and Cd-toxicity in roots of Vigna radiata L. J Plant Res 127:731–742

    CAS  Google Scholar 

  • Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32:73–86

    Google Scholar 

  • Pang KY, Li YJ, Liu MH, Meng ZD, Yu YL (2013) Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526:411–428

    CAS  Google Scholar 

  • Park JY, Song WY, Ko D, Eom YJ, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee YS (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288

    CAS  Google Scholar 

  • Qi WZ, Liu HH, Liu P, Dong ST, Zhao BQ, So HB, Li G, Liu HD, Zhang JW, Zhao B (2012) Morphological and physiological characteristics of corn (Zea mays L.) roots from cultivars with different yield potentials. Eur J Agron 38:54–63

    Google Scholar 

  • Qin SY, Xu YF, Nie ZJ, Liu HE, Gao W, Li C, Wang L, Zhao P (2022) Effect of boron on cadmium uptake and expression of Cd transport genes at different growth stages of wheat (Triticum aestivum L.). Ecotox Environ Safe 241:113834–113842

    CAS  Google Scholar 

  • Qin XM, Nie ZJ, Liu HE, Zhao P, Qin SY, Shi ZW (2018) Influence of selenium on root morphology and photosynthetic characteristics of winter wheat under cadmium stress. Environ Exp Bot 150:232–239

    CAS  Google Scholar 

  • Ramos I, Esteban E, Lucena JJ, Garate A (2002) Cadmium uptake and subcellular distribution in plants of Lactuca sp. Cd-Mn interaction. Plant Sci 162:761–767

    CAS  Google Scholar 

  • Riaz M, Kamran M, Fang YZ, Yang GL, Rizwan M, Ali S, Zhou YY, Wang QQ, Deng LL, Wang YJ, Wang XR (2021) Boron supply alleviates cadmium toxicity in rice (Oryza sativa L.) by enhancing cadmium adsorption on cell wall and triggering antioxidant defense system in roots. Chemosphere 266:128938–128950

    CAS  Google Scholar 

  • Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing azotobacter chroococcum. Ecotoxicol Environ Safe 157:9–20

    CAS  Google Scholar 

  • Rodda MS, Li G, Rj R (2011) The timing of grain Cd accumulation in rice plants: the relative importance of remobilisation within the plant and root Cd uptake post-flowering. Plant Soil 347:105–114

    CAS  Google Scholar 

  • Romè C, Huang XY, Danku J, Salt DE, Sebastiani L (2016) Expression of specific genes involved in Cd uptake, translocation, vacuolar compartmentalisation and recycling in Populus alba Villafranca clone. J Plant Physiol 202:83–91

    Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    CAS  Google Scholar 

  • Sun GY, Meng Y, Wang Y, Zhao M, Wei S, Gu WR (2021) Exogenous hemin optimized maize leaf photosynthesis, root development, grain filling, and resource utilization on alleviating cadmium stress under field condition. J Soil Sci Plant Nut 22:631–646

    Google Scholar 

  • Tang RJ, Luan S (2017) Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr Opin Plant Biol 39:97–105

    CAS  Google Scholar 

  • Tao Q, Liu YK, Li M, Li JX, Luo JP, Lux A, Yuan S, Li B, Li QQ, Li HX, Li TQ (2020) Cd-induced difference in root characteristics along root apex contributes to variation in Cd uptake and accumulation between two contrasting ecotypes of Sedum alfredii. Chemosphere 243:1–11

    Google Scholar 

  • Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, Clemencia Zambrano M, Kaskie M, Ebbs S, Kochian LV, Ma JF (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862

    CAS  Google Scholar 

  • Wang HQ, Xuan W, Huang XY, Mao CZ, Zhao FJ (2021) Cadmium inhibits lateral root emergence in rice by disrupting OsPIN-mediated auxin distribution and the protective effect of OsHMA3. Plant Cell Physiol 62:166–177

    CAS  Google Scholar 

  • Wang L, Zou R, Cai JH, Liu GH, Jiang Y, Chai GQ, Qin S, Fan CW (2023) Effect of Cd toxicity on root morphology, ultrastructure, Cd uptake and accumulation of wheat under intercrop** with Solanum nigrum L. Heliyon 9:16270–16278

    Google Scholar 

  • Wang YT, Björn LO (2014) Heavy metal pollution in Guangdong Province, China, and the strategies to manage the situation. Front Environ Sci 2:1–12

    Google Scholar 

  • Wei W, Peng H, **e YH, Wang X, Huang R, Chen HY, Ji XH (2021) The role of silicon in cadmium alleviation by rice root cell wall retention and vacuole compartmentalization under different durations of Cd exposure. Ecotox Environ Safe 226:112810–112819

    CAS  Google Scholar 

  • Wu XW, Tian H, Li L, Wang XQ (2021) Polyaspartic acid alleviates cadmium toxicity in rapeseed leaves by affecting cadmium translocation and cell wall fixation of cadmium. Ecotox Environ Safe 224:112685–112692

    CAS  Google Scholar 

  • Wu ZC, Zhao XH, Sun XC, Tan QL, Tang YF, Nie ZJ, Hu CX (2015) Xylem transport and gene expression play decisive roles in cadmium accumulation in shoots of two oilseed rape cultivars (Brassica napus). Chemosphere 119:1217–1223

    CAS  Google Scholar 

  • **ao AW, Chen DT, Li WC, Ye ZH (2021) Root morphology and anatomy affect cadmium translocation and accumulation in rice. Rice Sci 28:594–604

    Google Scholar 

  • Xu XH, Liu CY, Zhao XY, Li RY, Deng WJ (2014) Involvement of an antioxidant defense system in the adaptive response to cadmium in maize seedlings (Zea mays L.). B Environ Contam Tox 93:618–624

    CAS  Google Scholar 

  • Yang JL, Li K, Zheng W, Zhang HZ, Cao XD, Lan YX, Yang CP, Li CH (2015) Characterization of early transcriptional responses to cadmium in the root and leaf of Cd-resistant Salix matsudana Koidz. BMC Genom 16:705–720

    Google Scholar 

  • Yue RQ, Lu CX, Qi JS, Han XH, Yan SF, Guo SL, Liu L, Fu XL, Chen NN, Yin HY, Chi HF, Tie SG (2016) Transcriptome analysis of cadmium-treated roots in Maize (Zea mays L.). Front in Plant Sci 7:1298–1308

    Google Scholar 

  • Zeng LH, Zhu T, Gao Y, Wang YT, Ning CJ, Björn LO, Chen D, Li SS (2017) Effects of Ca addition on the uptake, translocation, and distribution of Cd in Arabidopsis thaliana. Ecotox Environ Safe 139:228–237

    CAS  Google Scholar 

  • Zhang LG, Zhang C, Du BY, Lu BX, Zhou DM, Zhou J, Zhou J (2020) Effects of node restriction on cadmium accumulation in eight Chinese wheat (Triticum turgidum) cultivars. Sci Total Environ 725:138358–138365

    CAS  Google Scholar 

  • Zhao YN, Luo LL, Xu JS, **n PY, Guo HY, Wu J, Bai L, Wang GD, Chu JF, Zuo JR, Yu H, Huang X, Li JY (2018) Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana. Cell Res 28:448–461

    CAS  Google Scholar 

  • Zhou J, Du BY, Wang ZW, Zhang WT, Xu L, Fan XJ, Liu XL, Zhou J (2019) Distributions and pools of lead (Pb) in a terrestrial forest ecosystem with highly elevated atmospheric Pb deposition and ecological risks to insects. Sci Total Environ 647:932–941

    CAS  Google Scholar 

  • Zhou J, Zhang C, Du BY, Cui HB, Fan XJ, Zhou DM, Zhou J (2020) Effects of zinc application on cadmium (Cd) accumulation and plant growth through modulation of the antioxidant system and translocation of Cd in low- and high-Cd wheat cultivars. Environ Pollut 265:115045–115054

    CAS  Google Scholar 

  • Zuzana V, Karin K, Anna M, Desana L (2018) Maize shoot cell walls under cadmium stress. Environ Sci Pollut Res 25:22318–22322

    Google Scholar 

Download references

Funding

This work was financially supported by National Natural Science Foundation of China (31771713, 31371576) and Shandong Province Key Agricultural Project for Application Technology Innovation (SDAIT02-08).

Author information

Authors and Affiliations

  1. College of Agronomy, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Mengxue Qu, Jie Song, Hao Ren, Bin Zhao, Jiwang Zhang, Baizhao Ren & Peng Liu

Authors
  1. Mengxue Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hao Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiwang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Baizhao Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Peng Liu: conceptualization, methodology, and resources. Mengxue Qu: investigation, data curation, and writing — original draft. Jie Song: investigation. Jiwang Zhang: supervision. Bin Zhao: supervision. Baizhao Ren: supervision. Hao Ren: supervision and project administration.

Corresponding author

Correspondence to Peng Liu.

Ethics declarations

Ethics approval and consent to participate

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.

Highlights

1. Roots of Cd-sensitive maize varieties accumulate more Cd than those of Cd-tolerant varieties.

2. Cd tolerance is associated with ZmNRAMP5 and ZmZIP4 suppression, as well as ZmABCG4 elevation.

3. Cd-stress-induced upregulation of ZmABCC1 and ZmABCC2 expression boosts vacuolar regionalization.

4. Roots of Cd-tolerant maize varieties respond to Cd stress by develo** thicker cell walls and larger vacuoles.

Novelty statement

We investigated the difference in performance of two maize varieties subjected to Cd stress by combining measurements of the expression levels of genes associated with Cd tolerance with observations of changes in the root ultrastructure. Our study provided us with an in-depth understanding of the mechanisms governing Cd tolerance in Cd-tolerant maize varieties.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 22 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qu, M., Song, J., Ren, H. et al. Differences of cadmium uptake and accumulation in roots of two maize varieties (Zea mays L.). Environ Sci Pollut Res 30, 96993–97004 (2023). https://doi.org/10.1007/s11356-023-29340-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-29340-9

Keywords

Search

Navigation