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Lanthanum reduces the cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in wheat

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Abstract

Background and aims

Lanthanum (La) is attracting increasing attention due to its effects in enhancing yields and reducing cadmium (Cd) accumulation in crops. Although a few transporter genes are reportedly involved in regulating the Cd accumulation in plants, the mechanisms of La-decreased Cd accumulation in plants remain poorly understood. Therefore, this study aimed to 1) investigate the effects of La on Cd accumulation and growth of wheat and 2) determine whether La regulates the Cd accumulation in wheat correlating with the expression of TaNramp5, TaHMA2 and TaHMA3.

Methods

Hydroponics and pot experiments were conducted under Cd stressed conditions in the presence or absence of La, with special emphasis on the accumulation of Cd, the expression of TaNramp5, TaHMA2 and TaHMA3, and the growth of wheat.

Results

La supplementation decreased Cd accumulation in wheat, which resulted in better plant growth. Pre-treatment with La also decreased Cd accumulation in both roots and shoots. La supply resulted in a decreased Cd concentration in the root cell sap, cell wall and xylem sap, respectively. Furthermore, in the pot experiment, La application also reduced Cd accumulation in all tissues of wheat under Cd exposure, and the concentration of Cd in grains decreased by 35.0%. The expression levels of TaNramp5 and TaHMA2 were down-regulated by La supplementation.

Conclusions

La could efficiently limit Cd accumulation in wheat. The La-decreased Cd accumulation in wheat is probably a consequence of both decreased Cd uptake due to the down-regulation of TaNramp5, and reduced root-to-shoot by the down-regulation of TaHMA2.

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References

  • Agathokleous E, Kitao M, Calabrese EJ (2018) Environmental hormesis and its fundamental biological basis: rewriting the history of toxicology. Environ Res 165:274–278

    Article  CAS  PubMed  Google Scholar 

  • Åkesson A, Barregard L, Bergdahl IA, Nordberg GF, Nordberg M, Skerfving S (2014) Non-renal effects and the risk assessment of environmental cadmium exposure. Environ Health Perspect 122:431–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arduini I, Masoni A, Mariotti M, Pampana S, Ercoli L (2014) Cadmium uptake and translocation in durum wheat varieties differing in grain-cd accumulation. Plant Soil Environ 60:43–49

    Article  CAS  Google Scholar 

  • Berkelaar E, Hale B (2000) The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can J Bot 78:381–387

    CAS  Google Scholar 

  • Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Che J, Yamaji N, Shao JF, Ma JF, Shen RF (2016) Silicon decreases both uptake and root-to-shoot translocation of manganese in rice. J Exp Bot 67:1535–1544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WJ, Tao Y, Gu YH, Zhao GW (2001) Effect of lanthanide chloride on photosynthesis and dry matter accumulation in tobacco seedlings. Biol Trace Elem Res 79:169–176

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Codex Alimentarius Commission of Food and Agriculture Organization (2006) Report of the twenty-ninth session of the Codex Alimentarius Commission

  • d’Aquino L, de Pinto MC, Nardi L, Morgana M, Tommasi F (2009) Effect of some light rare earth elements on seed germination, seedling growth and antioxidant metabolism in Triticum durum. Chemosphere 75:900–905

    Article  CAS  PubMed  Google Scholar 

  • Dai H, Shan C, Zhao H, Jia G, Chen D (2017) Lanthanum improves the cadmium tolerance of Zea mays seedlings by the regulation of ascorbate and glutathione metabolism. Biol Plant 61:551–556

    Article  CAS  Google Scholar 

  • de Oliveira C, Ramos SJ, Siqueira JO, Faquin V, de Castro EM, Amaral DC, Techio VH, Coelho LC, e Silva PH, Schnug E (2015) Bioaccumulation and effects of lanthanum on growth and mitotic index in soybean plants. Ecotoxicol Environ Saf 122:136–144

    Article  CAS  PubMed  Google Scholar 

  • Edington SC, Gonzalez A, Middendorf TR, Halling DB, Aldrich RW, Baiz CR (2018) Coordination to lanthanide ions distorts binding site conformation in calmodulin. Proc Natl Acad Sci 115:3126–3134

    Article  CAS  Google Scholar 

  • Evens NP, Buchner P, Williams LE, Hawkesford MJ (2017) The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum). Plant J 92:291–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2012) ProdStat. Core Production Data Base, Core production data base, Electronic resource under http://faostat.fao.org/

  • Guo B, Xu LL, Guan ZJ, Wei YH (2012) Effect of lanthanum on rooting of in vitro regenerated shoots of Saussurea involucrata Kar. Et Kir. Biol Trace Elem Res 147:334–340

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–396

    Article  CAS  PubMed  Google Scholar 

  • He J, Li H, Luo J, Ma C, Li S, Qu L, Gai Y, Jiang X, Janz D, Polle A, Tyree M, Luo Z (2013) A transcriptomic network underlies microstructural and physiological responses to cadmium in populus ×canescens1[C][W]. Plant Physiol 162:424–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong F, Wang L, Liu C (2003) Study of lanthanum on seed germination and growth of rice. Biol Trace Elem Res 94:273–286

    Article  CAS  Google Scholar 

  • Hu Z, Richter H, Sparovek G, Schnug E (2004) Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review. J Plant Nutr 27:183–220

    Article  CAS  Google Scholar 

  • Hu Y, Cheng H, Tao S (2016) The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environ Int 92-93:515–532

    Article  CAS  PubMed  Google Scholar 

  • Huang GQ, Wang DF (2016) Effects of lanthanum on the cadmium uptake of pacific oyster Crassostrea gigas. Indian J Geo-Mar Sci 45:653–657

    Google Scholar 

  • Huang X, Zhou Q (2006) Alleviation effect of lanthanum on cadmium stress in seedling hydroponic culture of kidney bean and corn. J Rare Earths 24:248–252

    Article  Google Scholar 

  • 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 7:12138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IUPAC (2005) In: Connelly N, Damhus T, Harshorn RM (eds) Nomenclature of inorganic chemistry, IUPAC recommendations (the “red book”). RSC Publishing, Cambridge, UK

    Google Scholar 

  • Kubo K, Watanabe Y, Matsunaka H, Seki M, Fujita M, Kawada N, Hatta K, Nakajima T (2011) Differences in cadmium accumulation and root morphology in seedlings of Japanese wheat varieties with distinctive grain cadmium concentration. Plant Production Sci 14:148–155

    Article  CAS  Google Scholar 

  • Liedschulte V, Laparra H, Battey James Nicolas D, Schwaar Joanne D, Broye H, Mark R, Klein M, Goepfert S, Bovet L (2016) Impairing both HMA4 homeologs is required for cadmium reduction in tobacco. Plant Cell Environ 40:364–377

    Article  CAS  Google Scholar 

  • Liu D, Lin Y, Wang X (2012) Effects of lanthanum on growth, element uptake, and oxidative stress in rice seedlings. J Plant Nutr Soil Sci 175:907–911

    Article  CAS  Google Scholar 

  • Liu D, Wang X, Zhang X, Gao Z (2013) Effects of lanthanum on growth and accumulation in roots of rice seedlings. Plant Soil Environ 59:196–200

    Article  CAS  Google Scholar 

  • Liu D, Zheng S, Wang X (2016) Lanthanum regulates the reactive oxygen species in the roots of rice seedlings. Sci Rep 6:31860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo JS, Huang J, Zeng DL, Peng JS, Zhang GB, Ma HL, Guan Y, Yi HY, Fu YL, Han B, Lin HX, Qian Q, Gong JM (2018) A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9:645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Cai H, He C, Zhang W, Wang L (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206:1063–1074

    Article  CAS  PubMed  Google Scholar 

  • Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 (2010) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199

    Article  CAS  PubMed  Google Scholar 

  • Nagahashi G, Thomson WW, Leonard RT (1974) The Casparian strip as a barrier to the movement of lanthanum in corn roots. Science 183:670–671

    Article  CAS  PubMed  Google Scholar 

  • Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ran J, Wang D, Wang C, Zhang G, Zhang H (2016) Heavy metal contents, distribution, and prediction in a regional soil–wheat system. Sci Total Environ 544:422–431

    Article  CAS  PubMed  Google Scholar 

  • Rezanka T, Kaineder K, Mezricky D, Rezanka M, Bisova K, Zachleder V, Vitova M (2016) The effect of lanthanides on photosynthesis, growth, and chlorophyll profile of the green alga Desmodesmus quadricauda. Photosynth Res 130:335–346

    Article  CAS  PubMed  Google Scholar 

  • Rizwan M, Ali S, Abbas T, Zia-Ur-Rehman M, Hannan F, Keller C, Al-Wabel MI, Ok YS (2016) Cadmium minimization in wheat: a critical review. Ecotoxicol Environ Saf 130:43–53

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2012) Mutations in Rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224

    Article  CAS  PubMed  Google Scholar 

  • Shao JF, Che J, Yamaji N, Shen RF, Ma JF (2017a) Silicon reduces cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in rice. J Exp Bot 68:5641–5651

    Article  CAS  Google Scholar 

  • Shao JF, Yamaji N, Shen RF, Ma JF (2017b) The key to Mn homeostasis in plants: regulation of Mn transporters. Trends Plant Sci 22:215–224

    Article  CAS  PubMed  Google Scholar 

  • Sui FQ, Chang JD, Tang Z, Liu WJ, Huang XY, Zhao FJ (2018) Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize. Plant Soil 433:377–389

    Article  CAS  Google Scholar 

  • Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012a) The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7:1605–1607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012b) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and cd in rice. Plant Cell Environ 35:1948–1957

    Article  CAS  PubMed  Google Scholar 

  • Tan J, Wang J, Chai T, Zhang Y, Feng S, Li Y, Zhao H, Liu H, Chai X (2013) Functional analyses of TaHMA2, a P1B-type ATPase in wheat. Plant Biotechnol J 11:420–431

    Article  CAS  PubMed  Google Scholar 

  • Tang Z, Cai H, Li J, Lv Y, Zhang W, Zhao FJ (2017) Allelic variation of NtNramp5 associated with cultivar variation in cadmium accumulation in tobacco. Plant Cell Physiol 58:1583–1593

    Article  CAS  PubMed  Google Scholar 

  • Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci 107:16500–16505

    Article  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y, Takemoto Y, Moriyama S, Che J, Moriyama Y, Iwasaki K, Ma JF (2015) A polarly localized transporter for efficient manganese uptake in rice. Nature Plants 1:15170

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhang X, Mu Y (2008) Effects of rare-earth fertilizers on the emission of nitrous oxide from agricultural soils in China. Atmos Environ 42:3882–3887

    Article  CAS  Google Scholar 

  • Wang C, Lu X, Tian Y, Cheng T, Hu L, Chen F, Jiang C, Wang X (2011) Lanthanum resulted in unbalance of nutrient elements and disturbance of cell proliferation cycles in V. faba L. seedlings. Biol Trace Elem Res 143:1174–1181

    Article  CAS  PubMed  Google Scholar 

  • Wang CR, Wang QY, Tian Y, Zhang JF, Li ZX, Cao P, Zhu M, Li TT (2014a) Lanthanum ions intervened in enzymatic production and elimination of reactive oxygen species in leaves of rice seedlings under cadmium stress. Environ Toxicol Chem 33:1656–1664

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Li JG, Zhou Q, Yang G, Ding X, Li X, Cai C, Zhang Z, Wei H, Lu T, Deng X, Huang X (2014b) Rare earth elements activate endocytosis in plant cells. Proc Natl Acad Sci 111:12936–12941

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Yu H, Tian C, Sajjad M, Gao C, Tong Y, Wang X, Jiao Y (2017) Transcriptome association identifies regulators of wheat spike architecture. Plant Physiol 175:746–757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016a) The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172:1899–1910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Geilfus C-M, Pitann B, Mühling K-H (2016b) Silicon-enhanced oxalate exudation contributes to alleviation of cadmium toxicity in wheat. Environ Exp Bot 131:10–18

    Article  CAS  Google Scholar 

  • Wu J, Mock H-P, Giehl RFH, Pitann B, Mühling KH (2019) Silicon decreases cadmium concentrations by modulating root endodermal suberin development in wheat plants. J Hazard Mater 364:581–590

    Article  CAS  PubMed  Google Scholar 

  • Xiong SL, Xiong ZT, Chen YC, Huang H (2006) Interactive effects of lanthanum and cadmium on plant growth and mineral element uptake in crisped-leaf mustard under hydroponic conditions. J Plant Nutr 29:1889–1902

    Article  CAS  Google Scholar 

  • Yang GM, Chu YX, Lv XF, Zhou Q, Huang XH (2012) Interaction between La(III) and proteins on the plasma membrane of horseradish. Spectrochim Acta A Mol Biomol Spectrosc 92:42–45

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The work was financed by the National Key Research and Development Program of China (2017YFD0801500). We thank the Jiangxi Academy of Agricultural Sciences for their provision of the wheat seeds.

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Correspondence to Zhiting Xiong.

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Yang, H., Xu, Z., Liu, R. et al. Lanthanum reduces the cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in wheat. Plant Soil 441, 235–252 (2019). https://doi.org/10.1007/s11104-019-04112-y

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