Abstract
Cadmium (Cd) pollution has become a major threat to crop production and quality globally. The heavy metal P1B-ATPases (HMAs) play a crucial role in metal transport in plants. In the present study, we investigated the interaction in metal transport by HMAs between Cd and mineral elements in rice plants. Rice seedlings were treated with cadmium nitrate either in the nutrient solution (“Cd+M”) or in the ultrapure water (“Cd-M”). Result showed that phytotoxicity of Cd to rice seedlings was evident from both Cd treatments, judged by relative growth rate (RGR), where more severe repression (p < 0.05) of RGR was observed in the “Cd-M” treatments than the “Cd+M” treatments. More Cd (p < 0.05) was accumulated in rice tissues from the “Cd-M” treatments than the “Cd+M” treatments, while there is a significant difference (p < 0.05) in distribution and translocation of mineral elements in rice tissues between the “Cd+M” and the “Cd-M” treatments. RT-qPCR analysis displayed that the expression patterns of HMAs related genes were quite different between “Cd+M” and “Cd-M” treatments, suggesting their different regulatory effects during the transport of Cd and mineral elements within rice plants. The competition in metal transport by HMAs mainly occurs between Cd and micro-elements of Zn and Cu in rice tissues during Cd exposure. Overall, this study provides new evidence to clarify the different translocation mechanisms of HMAs in metal transport between Cd and mineral elements in rice seedlings during Cd exposure.
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References
Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251
Bao T, Sun LN, Sun TH (2010) Evaluation of iron on cadmium uptake by tomato, morel and leaf red beet in hydroponic culture. J Plant Nutr 33:713–723
Binder BM, Rodríguez FI, Bleecker AB (2010) The copper transporter RAN1 is essential for biogenesis of ethylene receptors in Arabidopsis. J Biol Chem 285:37263–37270
Caemmerer SV, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336:1671–1672
Cong WX, Miao YL, Xu L, Zhang YH, Yuan CL, Wang JM, Zhuang TT, Lin XY, Wang NN, Ma J, Sanguinet KA, Liu B, Ou XF (2019) Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol 19:1–14
Deng FL, Yamaji N, Xia JX, Ma JF (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol 163:1353–1362
Dong J, Wu FB, Zhang GP (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666
Feng YX, Yu XZ, Mo CH, Lu CJ (2019) Regulation network of sucrose metabolism in response to trivalent and hexavalent chromium in Oryza sativa. J Agric Food Chem 67:9738–9748
Gourdon P, Liu XY, Skjørringe T, Morth JP, Møller LB, Pedersen BP, Nissen P (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–64
Gratão PL, Monteiro CC, Rossi ML, Martinelli AP, Peres LE, Medici LO, Lea PJ, Azevedo RA (2009) Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ Exp Bot 67:387–394
Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2007) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17:505–512
Haider FU, Cai LQ, Coulter JA, Cheema SA, Wu J, Zhang RZ, Ma WJ, Farooq M (2021) Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887–111909
Huang XY, Deng FL, Yamaji N, Pinson SRM, Fujii-Kashino M, Danku J, Douglas A, Guerinot ML, Salt DE, Ma JF (2016) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:1–13
Gonçalves JF, Antes FG, Maldaner J, Pereira LB, Tabaldi LA, Rauber R, Rossato LV, Bisognin DA, Dressler VL, Flores EMM, Nicoloso FT (2009) Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiol Biochem 47:814–821
Jinadasa N, Collins D, Holford P, Milham PJ, Conroy JP (2016) Reactions to cadmium stress in a cadmium-tolerant variety of cabbage (Brassica oleracea L.): is cadmium tolerance necessarily desirable in food crops? Environ Sci Pollut Res 23:5296–5306
Kashem MA, Kawai S (2007) Alleviation of cadmium phytotoxicity by magnesium in Japanese mustard spinach. Soil Sci Plant Nutr 53:246–251
Kim YY, Choi H, Segami S, Cho HT, Martinoia E, Maeshima M, Lee Y (2009) AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. Plant J 58:737–753
Kinay A (2018) Effects of cadmium on nicotine, reducing sugars and phenolic contents of Basma tobacco variety. Fresenius Environ Bull 27:9195–9202
Kobayashi Y, Kuroda K, Kimura K, Southron-Francis JL, Furuzawa A, Kimura K, Iuchi S, Kobayashi M, Taylor GJ, Koyama H (2008) Amino acid polymorphisms in strictly conserved domains of a P-type ATPase HMA5 are involved in the mechanism of copper tolerance variation in Arabidopsis. Plant Physiol 148:969–980
Kumar S, Kumar S, Mohapatra T (2021) Interaction between macro-and micro-nutrients in plants. Front Plant Sci 12:753–762
Lee S, Kim YY, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol 145:831–842
Li ZM, Liang Y, Hu HW, Shaheen SM, Zhong H, Tack FM, Wu MJ, Li YF, Gao YX, Rinklebe J, Zhao JT (2021) Speciation, transportation, and pathways of cadmium in soil-rice systems: a review on the environmental implications and remediation approaches for food safety. Environ Int 156:106749–106762
Lin YJ, Feng YX, Yu XZ (2022) The importance of utilizing nitrate (NO3−) over ammonium (NH4+) as nitrogen source during detoxification of exogenous thiocyanate (SCN-) in Oryza sativa. Environ Sci Pollut Res 29:5622–5633
Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178
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 P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199
Mohammad A, Moheman A (2010) The effects of cadmium and zinc interactions on the accumulation and tissue distribution of cadmium and zinc in tomato (Lycopersicon esculentum Mill.). Arch Agron Soil Sci 56:551–561
Roy A, Bhattacharya T, Kumari M (2020) Air pollution tolerance, metal accumulation and dust capturing capacity of common tropical trees in commercial and industrial sites. Sci Total Environ 722:137622
Østerberg JT, Palmgren M (2018) Heavy metal pumps in plants: structure, function and origin. Adv Bot Res 87:57–89
Rascio N, Vecchia DF, La-Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278
Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang DCW, Zia-ur-Rehman M, Zahir ZA, Rinklebed J, Tack FMG, Ok YS (2017) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105
Sarwar N, Saifullah MSS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937
Sebastian A, Prasad MNV (2015) Iron-and manganese-assisted cadmium tolerance in Oryza sativa L.: lowering of rhizotoxicity next to functional photosynthesis. Planta 241:1519–1528
Shao JF, Xia JX, Yamaji N, Shen RF, Ma JF (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. J Exp Bot 69:2743–2752
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143–1179
Song WE, Chen SB, Liu JF, Chen L, Song NN, Li N, Liu B (2015) Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J Integr Agric 14:1845–1854
Sterckeman T, Thomine S (2020) Mechanisms of cadmium accumulation in plants. Crit Rev Plant Sci 39:322–359
Sun CJ, Yang M, Li Y, Tian JJ, Zhang YY, Liang LM, Liu ZH, Chen K, Li YT, Lv K, Li XM (2019) Comprehensive analysis of variation of cadmium accumulation in rice and detection of a new weak allele of OsHMA3. J Exp Bot 70:6389–6400
Suzuki M, Bashir K, Inoue H, Takahashi M, Nakanishi H, Nishizawa NK (2012) Accumulation of starch in Zn-deficient rice. Rice 5:1–8
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 35:1948–1957
Tezuka K, Miyadate H, Katou K, Kodama I, Matsumoto S, Kawamoto T, Masaki S, Satoh H, Yamaguchi M, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2010) A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor Appl Genet 120:1175–1182
Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13
Trotta A, Falaschi P, Cornara L, Minganti V, Fusconi A, Drava G, Berta G (2006) Arbuscular mycorrhizae increase the arsenic translocation factor in the As hyperaccumulating fern Pteris vittata L. Chemosphere 65:74–81
Ueno D, Koyama E, Yamaji N, Ma JF (2011) Physiological, genetic, and molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan. J Exp Bot 62:2265–2272
Wong CKE, Jarvis RS, Sherson SM, Cobbett CS (2009) Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytol 181:79–88
Wu JW, Li RJ, Lu Y, Bai ZQ (2021) Sustainable management of cadmium-contaminated soils as affected by exogenous application of nutrients: A review. J Environ Manag 295:113081–113095
Wu FB, Zhang GP, Yu JS (2003) Interaction of cadmium and four microelements for uptake and translocation in different barley genotypes. Commun Soil Sci Plant Anal 34:2003–2020
Yan JL, Wang PT, Wang P, Yang M, Lian XM, Huang CF, Tang Z, Salt DE, Zhao FJ (2016) A loss of function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ 39:1941–1954
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
Yang JX, Wang LQ, Wei DP, Chen SB, Ma YB (2011) Foliar spraying and seed soaking of zinc fertilizers decreased cadmium accumulation in cucumbers grown in Cd-contaminated soils. Soil Sediment Contam 20:400–410
Yang Z, Yang F, Liu JL, Wu HT, Yang H, Shi Y, Liu J, Zhang YF, Luo YR, Chen KM (2022) Heavy metal transporters: Functional mechanisms, regulation, and application in phytoremediation. Sci Total Environ 809:151099–1510120
Yang L, Feng YX, Lin YJ, Yu XZ (2021) Comparative effects of sodium hydrosulfide and proline on functional repair in rice chloroplast through the D1 protein and thioredoxin system under simulated thiocyanate pollution. Chemosphere. 284:131389
Zhang FG, Liu MH, Li Y, Che YY, Xiao Y (2019) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158
Zhang Q, Feng YX, Lin YJ, Yu XZ (2021) Indigenous proline is a two-dimensional safety-relief valve in balancing specific amino acids in rice under hexavalent chromium stress. J Agric Food Chem 69:11185–11195
Zhao AQ, Tian XH, Lu WH, Gale WJ, Lu XC, Cao YX (2011) Effect of zinc on cadmium toxicity in winter wheat. J Plant Nutr 34:1372–1385
Zielazinski EL, González-Guerrero M, Subramanian P, Stemmler TL, Argüello JM, Rosenzweig AC (2013) Sinorhizobium meliloti Nia is a P1B-5-ATPase expressed in the nodule during plant symbiosis and is involved in Ni and Fe transport. Metallomics 5:1614–1623
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This work is financially supported by the Natural Science Foundation of Guangxi (No. 2018GXNSFDA281024).
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Conceptualization, Methodology, supervision, writing-reviewing and editing, and funding acquisition: Xiao-Zhang Yu. Investigation, data analysis, and visualization: Peng Tian. Writing original draft preparation and visualization: Yu-Xi Feng. Investigation: Cheng-Zhi Li. Investigation, Ping Zhang. All of the authors contributed to the final review of the manuscript.
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Tian, P., Feng, YX., Li, CZ. et al. Transcriptional analysis of heavy metal P1B-ATPases (HMAs) elucidates competitive interaction in metal transport between cadmium and mineral elements in rice plants. Environ Sci Pollut Res 30, 287–297 (2023). https://doi.org/10.1007/s11356-022-22243-1
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DOI: https://doi.org/10.1007/s11356-022-22243-1