Skip to main content
Log in

The regulatory role of root in cadmium accumulation in a high cadmium-accumulating rice line (Oryza sativa L.)

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

Abstract

There are some key processes that regulate cadmium (Cd) accumulation in rice. Understanding the characteristics and mechanisms of Cd accumulation in high Cd-accumulating rice lines benefits for excavating relevant genes. Cd accumulation and distribution in roots of Lu527-8, a high Cd-accumulating rice line, were investigated by a hydroponic experiment, with a control of a normal rice line (Lu527-4). Lu527-8 showed significantly higher Cd concentrations in roots than Lu527-4. More than 81% of Cd in roots of two rice lines is distributed in soluble fraction and cell wall. In soluble fraction, there were more organic acids, amino acids, and phytochelatins in Lu527-8, benefiting Cd accumulation. Pectin and hemicellulose 1 (HC1), especially pectin, were main polysaccharides in cell wall. Lu527-8 showed more pectin and HC1 along with higher pectin methylesterase (PME) activity compared with Lu527-4, promoting Cd accumulation. Besides, Lu527-8 showed higher Cd translocation from root to shoot due to more amounts of ethanol-extractable Cd in roots than Lu527-4. In conclusion, specific characteristics of Cd chemical forms and subcellular distribution in roots of high Cd-accumulating rice line are important for Cd accumulation and translocation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data and materials will be available on request.

Abbreviations

Cd:

cadmium

PME:

pectin methylesterase

HC1:

hemicellulose 1

HC2:

hemicellulose 2

TF:

translocation factor

References

  • Chebli Y, Geitmann A (2017) Cellular growth in plants requires regulation of cell wall biochemistry. Curr Opin Cell Biol 44:28–35

    Article  CAS  Google Scholar 

  • Chen GC, Liu YQ, Wang RM, Zhang JF, Owens G (2013) Cadmium adsorption by willow root: the role of cell walls and their subfractions. Environ Sci Pollut Res 20:5665–5672

    Article  CAS  Google Scholar 

  • Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicol Environ Saf 66:204–209

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  Google Scholar 

  • Degola F, De Benedictis M, Petraglia A, Massimi A, Fattorini L, Sorbo S, Basile A, di Toppi LS (2014) A Cd/Fe/Zn-responsive phytochelatin synthase is constitutively present in the ancient liverwort Lunularia cruciata (L.) Dumort. Plant Cell Physiol 55:1884–1891

    Article  CAS  Google Scholar 

  • Feng JJ, Jia WT, Lv SL, Bao HXGDL, Miao FF, Zhang X, Wang JH, Li JH, Li DS, Zhu C, Li SZ, Li YX (2017) Comparative transcriptome combined with morpho-physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes. Plant Biotechnol J 16:558–571

    Article  Google Scholar 

  • Fu HJ, Yu HY, Li TX, Wu Y (2019) Effect of cadmium stress on inorganic and organic components in xylem sap of high cadmium accumulating rice line (Oryza sativa L.). Ecotoxicol Environ Saf 168:330–337

    Article  CAS  Google Scholar 

  • Fu HJ, Yu HY, Li TX, Zhang XZ (2018) Influence of cadmium stress on root exudates of high cadmium accumulating rice line (Oryza sativa L.). Ecotoxicol Environ Saf 150:168–175

    Article  CAS  Google Scholar 

  • Fu X, Dou C, Chen Y, Chen X, Shi J, Yu M, Xu T (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J Hazard Mater 186:103–107

    Article  CAS  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unraveling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Guan MY, Zhang HH, Pan W, Jin CW, Lin XY (2018) Sulfide alleviates cadmium toxicity in Arabidopsis plants by altering the chemical form and the subcellular distribution of cadmium. Sci Total Environ 627:663–670

    Article  CAS  Google Scholar 

  • Gutsch A, Sergeant K, Keunen E, Prinsen E, Guerriero G, Renaut J, Hausman JF, Cuypers A (2019) Does long-term cadmium exposure influence the composition of pectic polysaccharides in the cell wall of Medicago sativa stems? BMC Plant Biol 19:271

    Article  Google Scholar 

  • Hazama K, Nagata S, Fujimori T, Yanagisawa S, Yoneyama T (2015) Concentrations of metals and potential metal-binding compounds and speciation of Cd, Zn and Cu in phloem and xylem saps from castor bean plants (Ricinus communis) treated with four levels of cadmium. Physiol Plant 154:243–255

    Article  CAS  Google Scholar 

  • He SY, He ZL, Yang XE, Stoffella PJ, Baligar VC (2015) Chapter Four - Soil biogeochemistry, plant physiology, and phytoremediation of cadmium-contaminated soils. Adv Agron 134:135–225

    Article  Google Scholar 

  • He X, Zhang J, Ren Y, Sun C, Deng X, Qian M, Hu Z, Li R, Chen Y, Shen Z, Xia Y (2019) Polyaspartate and liquid amino acid fertilizer are appropriate alternatives for promoting the phytoextraction of cadmium and lead in Solanum nigrum L. Chemosphere 237:124,483

    Article  CAS  Google Scholar 

  • Ibaraki T, Kuroyanagi N, Murakami M (2009) Practical phytoextraction in cadmium-polluted paddy fields using a high cadmium accumulating rice plant cultured by early drainage of irrigation water. Soil Sci Plant Nutr 55:421–427

    Article  CAS  Google Scholar 

  • Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    Article  Google Scholar 

  • Krzesłowska M, Rabęda I, Basińska A, Lewandowski M, Mellerowicz EJ, Napieralska A, Samardakiewicz S, Woźny A (2016) Pectinous cell wall thickenings formation - A common defense strategy of plants to cope with Pb. Environ Pollut 214:354–361

    Article  Google Scholar 

  • Lai HY (2015) Subcellular distribution and chemical forms of cadmium in Impatiens walleriana in relation to its phytoextraction potential. Chemosphere 138:370–376

    Article  CAS  Google Scholar 

  • Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190

    Article  CAS  Google Scholar 

  • Li T, Tao Q, Shohag MJI, Yang X, Sparks DL, Liang Y (2015) Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant Soil 389:387–399

    Article  CAS  Google Scholar 

  • Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867

    Article  Google Scholar 

  • Lu HP, Li ZA, Wu JT, Shen Y, Li YW, Zou B, Tang YT, Zhuang P (2017) Influences of calcium silicate on chemical forms and subcellular distribution of cadmium in Amaranthus hypochondriacus L. Sci Rep 7:40,583

    Article  CAS  Google Scholar 

  • 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. Ecotoxicol Environ Saf 183:109,590

    Article  CAS  Google Scholar 

  • Mwamba TM, Li L, Gill RA, Islam F, Nawaz A, Ali B, Farooq MA, Lwalaba JL, Zhou W (2016) Differential subcellular distribution and chemical forms of cadmium and copper in Brassica napus. Ecotoxicol Environ Saf 134:239–249

    Article  CAS  Google Scholar 

  • Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34:994–1008

    Article  CAS  Google Scholar 

  • Nocito FF, Espen L, Crema B, Cocucci M, Sacchi GA (2008) Cadmium induces acidosis in maize root cells. New Phytol 179:700–711

    Article  Google Scholar 

  • Osmolovskaya N, Dung VV, Kuchaeva L (2018) The role of organic acids in heavy metal tolerance in plants. Bio Comm 63:9–16

    Article  Google Scholar 

  • Ponnamperuma FN (1977) Screening rice for tolerance to mineral stresses. Int Rice Res Inst (IRRI) 25:67–72

    Google Scholar 

  • Ricachenevsky FK, de Araújo Junior AT, Fett JP, Sperotto RA (2018) You shall not pass: root vacuoles as a symplastic checkpoint for metal translocation to shoots and possible application to grain nutritional quality. Front Plant Sci 9:412

    Article  Google Scholar 

  • Sharifi M, Khoshgoftarmanesh AH, Hadadzadeh H (2016) Changes in the chemical properties and swelling coefficient of alfalfa root cell walls in the presence of toluene as a toxic agent. Environ Sci Pollut Res 23:7022–7031

    Article  CAS  Google Scholar 

  • Su CL, Jiang YJ, Li FF, Xu QS (2017) Investigation of subcellular distribution, physiological, and biochemical changes in Spirodela polyrhiza as a function of cadmium exposure. Environ Exp Bot 142:24–33

    Article  CAS  Google Scholar 

  • Su Y, Liu JL, Lu ZW, Wang XM, Zhang Z, Shi GR (2014) Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. Environ Exp Bot 97:40–48

    Article  CAS  Google Scholar 

  • Tang H (2016) Cadmium accumulation and tolerance characteristics in high cadmium accumulating rice. Sichuan agricultural university (In Chinese)

  • Tang H, Li TX, Yu HY, Zhang XZ (2016) Cadmium accumulation characteristics and removal potentials of high cadmium accumulating rice line grown in cadmium contaminated soils. Environ Sci Pollut Res 23:15,351–15,357

    Article  CAS  Google Scholar 

  • Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Cell Biol 16:328–334

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wang J, Yuan J, Yang Z, Huang B, Zhou Y, Xin J, Gong Y, Yu H (2009) Variation in cadmium accumulation among 30 cultivars and cadmium subcellular distribution in 2 selected cultivars of water spinach (Ipomoea aquatica Forsk.). J Agric Food Chem 57:8942–8949

    Article  CAS  Google Scholar 

  • Wang JB, Su LY, Yang JZ, Yuan JG, Yin AG, Qiu Q, Zhang K, Yang ZY (2015) Comparisons of cadmium subcellular distribution and chemical forms between low-Cd and high-Cd accumulation genotypes of watercress (Nasturtium officinale L. R. Br.). Plant Soil 396:325–337

    Article  CAS  Google Scholar 

  • Wang QY, Liu JS, Hu B (2016) Integration of copper subcellular distribution and chemical forms to understand copper toxicity in apple trees. Environ Exp Bot 123:125–131

    Article  CAS  Google Scholar 

  • Wang X, Liu YG, Zeng GM, Chai LY, Song XC, Min ZY, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Gaud. Environ Exp Bot 62:389–395

    Article  CAS  Google Scholar 

  • Wu Y, Wang WX (2011) Accumulation, subcellular distribution and toxicity of inorganic mercury and methylmercury in marine phytoplankton. Environ Pollut 159:3097–3105

    Article  CAS  Google Scholar 

  • Xin J, Huang B, Yang Z, Yuan J, Zhang Y (2013) Comparison of cadmium subcellular distribution in different organs of two water spinach (Ipomoea aquatica Forsk.) cultivars. Plant Soil 372:431–444

    Article  CAS  Google Scholar 

  • Xin J, Zhao XH, Tan QL, Sun XC, Hu CX (2017) Comparison of cadmium absorption, translocation, subcellular distribution and chemical forms between two radish cultivars (Raphanus sativus L.). Ecotoxicol Environ Saf 145:258–265

    Article  CAS  Google Scholar 

  • Xiong J, An LY, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  CAS  Google Scholar 

  • Xue WJ, Zhang CB, Wang PP, Wang CR, Huang YC, Zhang X, Liu ZQ (2019) Rice vegetative organs alleviate cadmium toxicity by altering the chemical forms of cadmium and increasing the ratio of calcium to manganese. Ecotoxicol Environ Saf 184:109640

    Article  CAS  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  CAS  Google Scholar 

  • Yang LP, Zhu J, Wang P, Zeng J, Tan R, Yang YZ, Liu ZM (2018) Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicol Environ Saf 160:10–18

    Article  CAS  Google Scholar 

  • Zhang HZ, Guo QJ, Yang JX, Shen JX, Chen TB, Zhu GX, Chen H, Shao CY (2015) Subcellular cadmium distribution and antioxidant enzymatic activities in the leaves of two castor (Ricinus communis L.) cultivars exhibit differences in Cd accumulation. Ecotoxicol Environ Saf 120:184–192

    Article  CAS  Google Scholar 

  • Zhang SJ, Li TX, Huang HG, Zou TJ, Zhang XZ, Yu HY, Zheng ZC, Wang YD (2012) Cd accumulation and phytostabilization potential of dominant plants surrounding mining tailings. Environ Sci Pollut Res 19:3879–3888

    Article  CAS  Google Scholar 

  • Zhao YF, Wu JF, Shang DR, Ning JS, Zhai YX, Sheng XF, Ding HY (2015) Subcellular distribution and chemical forms of cadmium in the edible seaweed, Porphyra yezoensis. Food Chem Toxicol 168:48–54

    Article  CAS  Google Scholar 

  • Zhou JT, Wan HX, He JL, Lyu D, Li HF (2017) Integration of cadmium accumulation, subcellular distribution, and physiological responses to understand cadmium tolerance in apple rootstocks. Front Plant Sci 8:1–16

    Article  Google Scholar 

  • Zhu G, Xiao H, Guo Q, Zhang Z, Zhao J, Yang D (2018) Effects of cadmium stress on growth and amino acid metabolism in two Compositae plants. Ecotoxicol Environ Saf 158:300–308

    Article  CAS  Google Scholar 

  • Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012) Cell wall polysaccharides are involved in P-deficiency induced Cd exclusion in Arabidopsis thaliana. Planta 236:989–997

    Article  CAS  Google Scholar 

  • Zhu XF, Wang ZW, Dong F, Lei GJ, Shi YZ, Li GX, Zheng SJ (2013) Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater 263:398–403

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by Major Science and Technology Project of Sichuan Province (2018SZDZX0029), National Key Research and Development Program of China (2018YFC1802605), and National Natural Science Foundation of China (41807147).

Author information

Authors and Affiliations

Authors

Contributions

Haiying Yu has contributed to conceptualization and writing (reviewing and editing). Keji Wang has contributed to formal analysis, visualization, and writing (original draft). Huagang Huang has contributed to methodology and software. Xizhou Zhang has contributed to supervision and validation. Tingxuan Li has contributed to supervision, resources, and writing (reviewing and editing). All authors read and approved the final manuscript.

Corresponding author

Correspondence to Tingxuan Li.

Ethics declarations

Competing interests

The authors declare that they have 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.

A.Supplementary information

ESM 1

(DOCX 80 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, H., Wang, K., Huang, H. et al. The regulatory role of root in cadmium accumulation in a high cadmium-accumulating rice line (Oryza sativa L.). Environ Sci Pollut Res 28, 25432–25441 (2021). https://doi.org/10.1007/s11356-021-12373-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12373-3

Keywords

Navigation