Abstract
In order to study the mechanism of cadmium (Cd) uptake by the roots of Celosia argentea Linn. (Amaranthaceae), the effects of various inhibitors, ion channel blockers, and hydroponic conditions on Cd2+ fluxes in the roots were characterized using non-invasive micro-test technology (NMT). The net Cd2+ flux (72.5 pmol∙cm−2∙s−1) in roots that had been pretreated with Mn was significantly higher than that in non-pretreated roots (58.1 pmol∙cm−2∙s−1), indicating that Mn pretreatment enhanced Cd uptake by the roots. This finding may be explained by the fact that the addition of Mn significantly increased the expression of the transporter gene and thus promoted Cd uptake and transport. In addition, Mn pretreatment resulted in an increase in root growth, which may in turn promote root vigor. The uncoupler 2,4-dinitrophenol (DNP) caused a significant reduction in net Cd2+ fluxes in the roots, by 70.5% and 41.4% when exposed to Mn and Cd stress, respectively. In contrast, a P-type ATPase inhibitor (Na3VO4) had only a small effect on net Cd2+ fluxes to the plant roots, indicating that ATP has a relatively minor role in Cd uptake by roots. La3+ (a Ca channel inhibitor) had a more significant inhibitory effect on net Cd2+ fluxes than did TEA (a K channel inhibitor). Therefore, Cd uptake by plant roots may occur mainly through Ca channels rather than K channels. In summary, uptake of Cd by the roots of C. argentea appears to occur via several types of ion channels, and Mn can promote Cd uptake.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Cataldo DA, Garlnd TR, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848
Chen ZH, Yumi FJ, Naoki Y, Sakine M, Yuma T, Takehiro K, Yusufujiang Y, Kozo I, Shin-ichiro K, Masayoshi M, Feng MJ, Daisei U (2013) Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J Exp Bot 64(14):4357–4387
Farrell RE, McArthur DFE, Van Rees KCJ (2005) Net Cd2+ flux at the root surface of durum wheat (Triticum turgidum L. var. durum) cultivars in relation to cultivar differences in Cd accumulation. Can J Plant Sci 85:103–107
Fathi S, Sabet MS, Lohrasebi T, Razavi K, Karimzadeh G, Malekroudi MG (2016) Effect of root morphological traits on zinc efficiency in Iranian bread wheat genotypes. Acta Agr Scand B-S P 66(7):575–582
Fu JX (2019) Effects of Zinc/Manganese on cadmium uptake, transport and physico-biochemical properties of rice (Oryza sativa L.) under cadmium stress [D]. Taiyuan University of Technology
Ge J, Tian SK, Yu HY, Zhao JQ (2021) Exogenous application of Mn significantly increased Cd accumulation in the Cd/Zn hyperaccumulator Sedum alfredii. Environ Pollut 278:116837
He CQ, Zhao YP, Wang FF, Oh K, Zhao ZZ, Wu CL, Zhang XY, Chen XP, Liu XY (2020) Phytoremediation of soil heavy metals (Cd and Zn) by castor seedlings: tolerance, accumulation and subcellular distribution. Chemosphere 252:126471
Koren’kov V, Park S, Cheng NH, Sreevidya C, Lachmansingh J, Morris J, Hirschi K, Wagner GJ (2007) Enhanced Cd2+-selected root-tonoplast in tobaccos expressing Arabidopsis cation exchangers. Planta 225:403–411
Kopec KT, Friermuth C, Maynard S, Beuhler M (2018) Dinitrophenol (DNP) farality associated with a falsely elevated salicylate level: a case report with verification of laboratory cross reactivity. J Med Toxicol 14(4):323–326
Lan XY, He QS, Yang B, Yan YY, Li XY, Xu FL (2020) Influence of Cd exposure on H+ and Cd2+ fluxes in the leaf, stem and root of a novel aquatic hyperaccumulator- Microsorum pteropus. Chemosphere 249:126552
Li LZ, Yu SY, Peijnenburg WJGM, Luo YM (2017a) Determining the fluxes of ions (Pb2+, Cu2+ and Cd2+) at the root surface of wetland plants using the scanning ion-selective electrode technique. Plant Soil 414(1/2):1–12
Li ZZ, Tu C, Peijnenburg WJGM, Luo YM (2017b) Characteristics of cadmium uptake and membrane transport in roots of intact wheat (Triticum arstivum L.) seedlings. Environ Pollut 221:351–358
Lindberg S, Landberg T, Greger M (2004) A new method to detect cadmium uptake in protoplasts. Planta 219:526–532
Liu J, Duan CQ, Zhang XH, Zhu YN, Hu C (2011) Characteristics of chromium (III) uptake in hyperaccumulator Leersia hexandra Swartz. Environ Exp Bot 74:122–126
Liu J, Mo LY, Zhang XH, Yao SY, Wang YX (2018) Simultaneous hyperaccumulation of cadmium and manganese in Celosia argentea Linn. Int J Phytoremediat 20(11):1106–1112
Liu J, Yu G, Jiang PP, Zhang XF, Meng DJ, Chen Z, Baker AJM, Qiu RL (2020a) Interaction of Mn and Cd during their uptake in Celosia argentea differs between hydroponic and soil systems. Plant Soil 450:323–336
Liu YK, Yao Q, Guo XY, Luo JP, Li JX, Liang YC, Li TQ (2020) Low calcium-induced delay in development of root apoplastic barriers enhances Cd uptake and accumulation in Sedum alfredii. Sci Total Environ 723(25):137810
Page V, Feller U (2005) Selective transport of zinc, manganese, nickel, cobalt and cadmium in the root system and transfer to the leaves in young wheat plants. Ann Bot-London 96:25–434
Pedas P, Hebbern CA, Schjoerring JK, Holm PE, Husted S (2005) Differential capacity for high-affinity manganese uptake contributes to differences between barley genotypes in tolerance to low manganese availability. Plant Physiol 139:1411–1420
Piñeros MA, Shaff JE, Kochian LV (1998) Cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi Species and wheat. Plant Physiol 116:1393–1401
Quinn CJ, Mohammad A, Macfie SM (2011) Accumulation of cadmium in near-isogenic lines of durum wheat (Triticum turgidum L. var durum): the role of transpiration. Physiol Mol Biol Pla 17(4):317–325
Rasafi TE, Bouda S, Hamdali H, Haddioui A (2021) Seed germination and early seedling growth of fenugreek (Trigonella foenum-gracium L.) under Cu, Ni and As stress. Acta Ecological Sinica 41(3):223–227
Sasaki A, Yamaji N, **a JX, Ma JF (2011) OsYSL6 is involved in the detoxification of excess manganese in rice. Plant Physiol 157:1832–1840
Shao JF, Yamaji N, Shen RF, Ma JF (2017) The key to Mn homeostasis in plants: regulation of Mn transporters. Trends Plant Sci 22(3):215–224
Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci 5:106
Sun J, Wang RG, Liu ZQ, Ding YZ, Li TQ (2013) Non-invasive microelectrode cadmium flux measurements reveal the spatial characteristics and real-time kinetics of cadmium transport in hyperaccumulator and nonhyperaccumulator ecotypes of Sedum alfredii. J Plant Physiol 170:355–359
Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotechnol-Nar 22(1):19–25
Tao Q, Liu YK, Li M, Li JX, Luo JP, Lux A, Kováč J, Yuan S, Li B, Li QQ, Li HX, Li TQ, Wang CQ (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 243:125290
Van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58(11):2939–2947
Wu SB, Shi KL, Hu CX, Guo JL, Tan QL, Sun XC (2019) Non-invasive microeletrode cadmium measurements reveal the decrease of cadmium uptake by zinc supply in pakchoi root (Brassica chinensis L.). Ecotox Environ Safe 168:363–368
**n XP, Zhao FL, Rho JY, Goodirch SL, Sumerlin BS, He ZL (2020) Use of polymeric nanoparticles to improve seed germination and plant growth under copper stress. Sci Total Environ 745(25):141055
Xu J, Sun JH, Du LG, Liu XJ (2012) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124
Yu G, Jiang PP, Fu XF, Liu J, Sunahara IG, Chen Z, **ao H, Lin FY, Wang XS (2020) Phytoextraction of cadmium-contaminated soil by Celosia argentea Linn: a long-term field study. Environ Pollut 266:155408
Yang CM, Juang KW (2015) Alleviation effects of calcium and potassium on cadmium rhizotoxicity and absorption by soybean and wheat roots. J Plant Nutr Soil Sci 178:748–754
Funding
This research was sponsored by the Natural Science Foundation of China (41867022), the Natural Science Foundation of Guangxi (2020GXNSFDA297018), the Special Funds of Guangxi Distinguished Experts, and the Program for High Level Innovation Team and Outstanding Scholar of Universities in Guangxi (GuiCaiJiaoHan[2018]319).
Author information
Authors and Affiliations
Contributions
P. Jiang and J. Liu: conceived the study.
Y. Zheng and P. Jiang: collected data and prepared the data for analysis.
G. Yu and F. Lin: performed statistical analyses and literature review.
P. Jiang: wrote the main manuscript text.
G. Yu and J. Liu: improved the draft.
All authors contributed to the interpretation of results and revised the manuscript critically.
All authors approved the final manuscript.