Abstract
Se (Selenium) has been reported to be an important protective agent to decreases Cd (Cadmium) induced toxic in plants. However, it remains unclear how Se mitigates the uptake of Cd and increased the resistance to Cd toxicity. Hydroponic experiments were arranged to investigate the changes of physiological properties, root cell membrane integrity and Cd-related transporter genes in rape seedlings. Comparison of the biomass between the addition of Se and the absence of Se under Cd exposure showed that the Cd-induced growth inhibition of rape seedlings was alleviated by Se. Cd decreased the photosynthetic rate (Pn), stomatal conductance (Gs) and photosynthetic pigment content including chlorophyll a, chlorophyll b and carotenoid. However, all these parameters were all significantly improved by Se addition. Moreover, exposure to Se resulted in a decrease in Cd concentration in both shoot and root, ranging from 4.28 to 27.2%. Notably, the application of Se at a concentration of 1 µmol L− 1 exhibited the best performance. Furthermore, Se enhanced cell membrane integrity and reduced superoxide anion levels, thereby contributing to the alleviation of cadmium toxicity in plants. More critically, Se decreased the expression levels of root Cd-related transporter genes BnIRT1, BnHMA2 and BnHMA4 under Cd stress, which are responsible for Cd transport and translocation. These results are important to increase crop growth and reduce Cd load in the food chain from metal toxicity management and agronomical point of view.
Similar content being viewed by others
References
Alves LR, dos Reis R, Prado A, Lavres ER, Pompeu J, Azevedo GB, R. A., Gratão PL (2019) New insights into cadmium stressful-conditions: role of ethylene on selenium-mediated antioxidant enzymes. Ecotoxicol Environ Saf 186:109747. https://doi.org/10.1016/j.ecoenv.2019.109747
Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212(5):696–709. https://doi.org/10.1007/s004250000439
Chauhan R, Awasthi S, Srivastava S, Dwivedi S, Pilon-Smits EAH, Dhankher OP, Tripathi RD (2019) Understanding selenium metabolism in plants and its role as a beneficial element. Crit Rev Environ Sci Technol 49(21):1937–1958. https://doi.org/10.1080/10643389.2019.1598240
Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99. https://doi.org/10.1016/j.tplants.2012.08.003
Cui J, Liu T, Li Y, Li F (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. https://doi.org/10.1016/j.scitotenv.2018.07.002
Dai Z-H, Guan D-X, Bundschuh J, Ma LQ (2022) Roles of phytohormones in mitigating abiotic stress in plants induced by metal(loid)s as, cd, cr, hg, and Pb. Crit Rev Environ Sci Technol 1–21. https://doi.org/10.1080/10643389.2022.2134694
Ding Y, Feng R, Wang R, Guo J, Zheng X (2014) A dual effect of Se on Cd toxicity: evidence from plant growth, root morphology and responses of the antioxidative systems of paddy rice. Plant Soil 375(1):289–301. https://doi.org/10.1007/s11104-013-1966-8
El Rasafi T, Oukarroum A, Haddioui A, Song H, Kwon EE, Bolan N, Tack FMG, Sebastian A, Prasad MNV, Rinklebe J (2022) Cadmium stress in plants: a critical review of the effects, mechanisms, and tolerance strategies. Crit Rev Environ Sci Technol 52(5):675–726. https://doi.org/10.1080/10643389.2020.1835435
Feng R, Wei C, Tu S (2013) The roles of selenium in protecting plants against abiotic stresses. Environ Exp Bot 87:58–68. https://doi.org/10.1016/j.envexpbot.2012.09.002
Feng R, Wang L, Yang J, Zhao P, Zhu Y, Li Y, Yu Y, Liu H, Rensing C, Wu Z, Ni R, Zheng S (2021) Underlying mechanisms responsible for restriction of uptake and translocation of heavy metals (metalloids) by selenium via root application in plants. J Hazard Mater 402:123570. https://doi.org/10.1016/j.jhazmat.2020.123570
Filek M, Gzyl-Malcher B, Zembala M, Bednarska E, Laggner P, Kriechbaum M (2010a) Effect of selenium on characteristics of rape chloroplasts modified by cadmium. J Plant Physiol 167(1):28–33. https://doi.org/10.1016/j.jplph.2009.07.003
Filek M, Kościelniak J, Łabanowska M, Bednarska E, Bidzińska E (2010b) Selenium-induced protection of photosynthesis activity in rape (Brassica napus) seedlings subjected to cadmium stress. Fluorescence and EPR measurements. Photosynth Res 105(1):27–37. https://doi.org/10.1007/s11120-010-9551-y
Guo Y, Mao K, Cao H, Ali W, Lei D, Teng D, Chang C, Yang X, Yang Q, Niazi NK (2021) Exogenous selenium (cadmium) inhibits the absorption and transportation of cadmium (selenium) in rice. Environ Pollut 268:115829. https://doi.org/10.1016/j.envpol.2020.115829
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Huang B, Xin J, Dai H, Zhou W (2017) Effects of Interaction between Cadmium (cd) and selenium (Se) on Grain Yield and Cd and Se Accumulation in a Hybrid Rice (Oryza sativa) system. J Agric Food Chem 65(43):9537–9546. https://doi.org/10.1021/acs.jafc.7b03316
Huang G, Ding C, Li Y, Zhang T, Wang X (2020) Selenium enhances iron plaque formation by elevating the radial oxygen loss of roots to reduce cadmium accumulation in rice (Oryza sativa L). J Hazard Mater 398:122860. https://doi.org/10.1016/j.jhazmat.2020.122860
Huang H, Li M, Rizwan M, Dai Z, Yuan Y, Hossain MM, Cao M, Xiong S, Tu S (2021) Synergistic effect of silicon and selenium on the alleviation of cadmium toxicity in rice plants. J Hazard Mater 401:123393. https://doi.org/10.1016/j.jhazmat.2020.123393
Khan N, Samiullah, Singh S, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193(6):435–444. https://doi.org/10.1111/j.1439-037X.2007.00272.x
Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2014) Histochemical detection of superoxide and H2O2 accumulation in Brassica juncea seedlings. Bio-protocol 4(8):e1108–e1108
Lehotai N, Kolbert Z, Pető A, Feigl G, Ördög A, Kumar D, Tari I, Erdei L (2012) Selenite-induced hormonal and signalling mechanisms during root growth of Arabidopsis thaliana L. J Exp Bot 63(15):5677–5687. https://doi.org/10.1093/jxb/ers222
Li Q, Wang G, Wang Y, Dan Y, Guan C, Ji J (2019) Foliar application of salicylic acid alleviate the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicol Environ Saf 172:317–325. https://doi.org/10.1016/j.ecoenv.2019.01.078
Lin L, Zhou W, Dai H, Cao F, Zhang G, Wu F (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235–236:343–351. https://doi.org/10.1016/j.jhazmat.2012.08.012
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37. https://doi.org/10.1093/jxb/erq281
Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164(5):601–610. https://doi.org/10.1016/j.jplph.2006.03.003
Mroczek-Zdyrska M, Strubińska J, Hanaka A (2017) Selenium improves physiological parameters and alleviates oxidative stress in shoots of lead-exposed Vicia faba L. minor plants grown under phosphorus-deficient conditions. J Plant Growth Regul 36(1):186–199. https://doi.org/10.1007/s00344-016-9629-7
Qi W-Y, Li Q, Chen H, Liu J, Xing S-F, Xu M, Yan Z, Song C, Wang S-G (2021) Selenium nanoparticles ameliorate Brassica napus L. cadmium toxicity by inhibiting the respiratory burst and scavenging reactive oxygen species. J Hazard Mater 417:125900. https://doi.org/10.1016/j.jhazmat.2021.125900
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(2):168–180. https://doi.org/10.1016/S1002-0160(20)60002-9
Qing X, Zhao X, Hu C, Wang P, Zhang Y, Zhang X, Wang P, Shi H, Jia F, Qu C (2015) Selenium alleviates chromium toxicity by preventing oxidative stress in cabbage (Brassica campestris L. ssp. Pekinensis) leaves. Ecotoxicol Environ Saf 114:179–189. https://doi.org/10.1016/j.ecoenv.2015.01.026
Schiavon M, Pilon-Smits EA (2017) The fascinating facets of plant selenium accumulation–biochemistry, physiology, evolution and ecology. New Phytol 213(4):1582–1596. https://doi.org/10.1111/nph.14378
Sun H, Dai H, Wang X, Wang G (2016) Physiological and proteomic analysis of selenium-mediated tolerance to cd stress in cucumber (Cucumis sativus L). Ecotoxicol Environ Saf 133:114–126. https://doi.org/10.1016/j.ecoenv.2016.07.003
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to‐shoot translocation of Zn and Cd in rice. Plant Cell Environ 35(11):1948–1957. https://doi.org/10.1111/j.1365-3040.2012.02527.x
Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. Chemosphere 84(1):63–69. https://doi.org/10.1016/j.chemosphere.2011.02.054
Ulhassan Z, Gill RA, Ali S, Mwamba TM, Ali B, Wang J, Huang Q, Aziz R, Zhou W (2019) Dual behavior of selenium: insights into physio-biochemical, anatomical and molecular analyses of four Brassica napus cultivars. Chemosphere 225:329–341. https://doi.org/10.1016/j.chemosphere.2019.03.028
Wan Y, Yu Y, Wang Q, Qiao Y, Li H (2016) Cadmium uptake dynamics and translocation in rice seedling: influence of different forms of selenium. Ecotoxicol Environ Saf 133:127–134. https://doi.org/10.1016/j.ecoenv.2016.07.001
Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root‐to‐shoot cd translocation in Arabidopsis thaliana. New Phytol 181(1):71–78. https://doi.org/10.1111/j.1469-8137.2008.02638.x
Wu Z, Zhao X, Sun X, Tan Q, Tang Y, Nie Z, Hu C (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. https://doi.org/10.1016/j.chemosphere.2014.09.099
Wu S, Hu C, Tan Q, Xu S, Sun X (2017) Nitric oxide mediates Molybdenum-Induced antioxidant defense in wheat under Drought stress [Original Research]. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01085
Yang Z, Yang F, Liu J-L, Wu H-T, Yang H, Shi Y, Liu J, Zhang Y-F, Luo Y-R, Chen K-M (2021) Heavy metal transporters: functional mechanisms, regulation, and application in phytoremediation. Sci Total Environ 151099. https://doi.org/10.1016/j.scitotenv.2021.151099
Zembala M, Filek M, Walas S, Mrowiec H, Kornaś A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329(1):457–468. https://doi.org/10.1007/s11104-009-0171-2
Zhang M, Tang S, Huang X, Zhang F, Pang Y, Huang Q, Yi Q (2014) Selenium uptake, dynamic changes in selenium content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa L). Environ Exp Bot 107:39–45. https://doi.org/10.1016/j.envexpbot.2014.05.005
Zhang Z-H, Zhou T, Tang T-J, Song H-X, Guan C-Y, Huang J-Y, Hua Y-P (2019) A multiomics approach reveals the pivotal role of subcellular reallocation in determining rapeseed resistance to cadmium toxicity. J Exp Bot 70(19):5437–5455. https://doi.org/10.1093/jxb/erz2951
Zhao Y, Hu C, Wang X, Qing X, Wang P, Zhang Y, Zhang X, Zhao X (2019a) Selenium alleviated chromium stress in chinese cabbage (Brassica campestris L. ssp. Pekinensis) by regulating root morphology and metal element uptake. Ecotoxicol Environ Saf 173:314–321. https://doi.org/10.1016/j.ecoenv.2019.01.090
Zhao Y, Hu C, Wu Z, Liu X, Cai M, Jia W, Zhao X (2019b) Selenium reduces cadmium accumulation in seed by increasing cadmium retention in root of oilseed rape (Brassica napus L). Environ Exp Bot 158:161–170. https://doi.org/10.1016/j.envexpbot.2018.11.017
Acknowledgements
This work is funded by Fujian Provincial Key Lab of Coastal Basin Environment (Fujian Polytechnic Normal University) (S1-KF2110), the Opening Project of Fujian Provincial Key Laboratory of Resources and Environment Monitoring & Sustainable Management and Utilization (ZD202101), Program for Innovative Research Team in Science and Technology in Fujian Province University (KC190002), the Opening Project of Key Laboratory of Risk Assessment for Agro-product Quality and Safety, Guangdong Province (SZKF202101).
Author information
Authors and Affiliations
Contributions
Yuanyuan Zhao and Yanni Tang conceived the experiment, performed the main experiments and data analysis, and wrote the manuscript. Yingjie Zhou, Shiqian Li, Chihhung Wu, Guangyu Shi and Chengxiao Hu assisted in the implementation of the experiment and data analysis. Xiaohu Zhao conceived the experiment and revised the manuscript. All authors have approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no competing financial interest.
Additional information
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
Tang, Y., Zhao, Y., Zhou, Y. et al. Se Ameliorates Cd Toxicity in Oilseed rape (Brassica napus L.) Seedlings by Inhibiting Cd Transporter Genes and Maintaining root Plasma Membrane Integrity. Bull Environ Contam Toxicol 111, 42 (2023). https://doi.org/10.1007/s00128-023-03804-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00128-023-03804-7