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Molecular Mechanism of Cadmium Accumulation in Rice

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Cadmium Toxicity

Abstract

Rice (Oryza sativa L.) is a major dietary source of cadmium (Cd) intake, which accounts for about 50% of total Cd intake for populations consuming rice as the staple food. Therefore, it is a very important issue to reduce transfer of Cd from soil to rice grains for human health. Recently, great progresses have been made in understanding the molecular mechanisms of Cd accumulation in rice. OsNramp5, a member of Nramp (natural resistance-associated macrophage protein) transporter family, is a major transporter for Cd uptake in rice, which is localized at the distal side of both root exodermis and endodermis. On the other hand, OsHMA3 belonging to heavy metal ATPase family is responsible for sequestration of Cd into the root vacuoles. Subsequent translocation of Cd from the roots to the shoots is mediated by OsHMA2 localized at the pericycle cells in the roots. At least two transporters (OsHMA2 and OsLCT1) localized in the nodes are involved in distribution of Cd to the rice grains. In addition, several QTL for Cd accumulation, by using wide genotypic variation in Cd accumulation, have been detected although the responsible genes remain to be identified in the future. Further identification of useful alleles for Cd accumulation will contribute to breeding rice cultivars with low Cd accumulation.

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References

  1. Shimo H, Ishimaru Y, An G, Yamakawa T, Nakanishi H, Nishizawa NK. Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot. 2011;62:5727–34. https://doi.org/10.1093/jxb/err300.

    Article  CAS  Google Scholar 

  2. Horiguchi H, Aoshima K, Oguma E, Sasaki S, Miyamoto K, Hosoi Y, et al. Latest status of cadmium accumulation and its effects on kidneys, bone, and erythropoiesis in inhabitants of the formerly cadmium-polluted Jinzu River Basin in Toyama, Japan, after restoration of rice paddies. Int Arch Occup Environ Health. 2010;83:953–70. https://doi.org/10.1007/s00420-010-0510-x.

    Article  CAS  PubMed  Google Scholar 

  3. Zhang CH, Yin XM, Gao KH, Ge Y, Cheng WD. Non-protein thiols and glutathione S-transferase alleviate Cd stress and reduce root-to-shoot translocation of Cd in rice. J Plant Nutr Soil Sci. 2013;176:626–33. https://doi.org/10.1002/jpln.201100276.

    Article  CAS  Google Scholar 

  4. Liu JG, Qu P, Zhang W, Dong Y, Li L, Wang MX. Variations among rice cultivars in subcellular distribution of Cd: the relationship between translocation and grain accumulation. Environ Exp Bot. 2014;107:25–31. https://doi.org/10.1016/j.envexpbot.2014.05.004.

    Article  CAS  Google Scholar 

  5. Clemens S, Ma JF. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol. 2016;67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301.

    Article  CAS  PubMed  Google Scholar 

  6. Sasaki A, Yamaji N, Yokosho K, Ma JF. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell. 2012;24:2155–67. https://doi.org/10.1105/tpc.112.096925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Enstone D, Peterson C, Ma FS. Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul. 2003;21:335–51. https://doi.org/10.1007/s00344-003-0002-2.

    Article  CAS  Google Scholar 

  8. Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, et al. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci U S A. 2012;109:19166–71.

    Article  CAS  Google Scholar 

  9. Yang M, Zhang Y, Zhang L, Hu J, Zhang X, Lu K, et al. OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot. 2014;65:4849–61. https://doi.org/10.1093/jxb/eru259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, et al. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep. 2012;2:286. https://doi.org/10.1038/srep00286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Supek F, Supekova L, Nelson H, Nelson N. A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc Natl Acad Sci U S A. 1996;93:5105–10.

    Article  CAS  Google Scholar 

  12. Supek F, Supekova L, Nelson H, Nelson N. Function of metal-ion homeostasis in the cell division cycle, mitochondrial protein processing, sensitivity to mycobacterial infection and brain function. J Exp Biol. 1997;200:321–30.

    CAS  PubMed  Google Scholar 

  13. Liu XF, Supek F, Nelson N, Culotta VC. Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem. 1997;272:11763–9.

    Article  CAS  Google Scholar 

  14. Chen XZ, Peng JB, Cohen A, Nelson H, Nelson N, Hediger MA. Yeast SMF1 mediates H+-coupled iron uptake with concomitant uncoupled cation currents. J Biol Chem. 1999;274:35089–94.

    Article  CAS  Google Scholar 

  15. Nevo Y, Nelson N. The mutation F227I increases the coupling of metal ion transport in DCT1. J Biol Chem. 2004;279:53056–61. https://doi.org/10.1074/jbc.M408398200.

    Article  CAS  PubMed  Google Scholar 

  16. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J. 2000;347:749–55.

    Article  CAS  Google Scholar 

  17. Cailliatte R, Schikora A, Briat JF, Mari S, Curie C. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell. 2010;22:904–17. https://doi.org/10.1105/tpc.109.073023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, et al. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 2005;24:4041–51.

    Article  CAS  Google Scholar 

  19. Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J. 2009;422:217–28. https://doi.org/10.1042/BJ20090655.

    Article  CAS  PubMed  Google Scholar 

  20. Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, et al. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot. 2011;62:4843–50. https://doi.org/10.1093/jxb/err136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xia JX, Yamaji N, Kasai T, Ma JF. Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci U S A. 2010;107:18381–5.

    Article  CAS  Google Scholar 

  22. Nakanishi H, Ogawa L, Ishimaru Y, Mori S, Nishizawa NK. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr. 2006;52:464–9. https://doi.org/10.1111/j.1747-0765.2006.00055.x.

    Article  CAS  Google Scholar 

  23. Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK. Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav. 2011;6:1813–6. https://doi.org/10.4161/psb.6.11.17587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yang Y, Xiong J, Chen R, Fu G, Chen T, Tao L. Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1 in rice (Oryza sativa). Environ Exp Bot. 2016;122:141–9. https://doi.org/10.1016/j.envexpbot.2015.10.001.

    Article  CAS  Google Scholar 

  25. Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y, Takemoto Y, et al. A polarly localized transporter for efficient manganese uptake in rice. Nat Plants. 2015;1:15170. https://doi.org/10.1038/NPLANTS.2015.170.

    Article  CAS  PubMed  Google Scholar 

  26. Ueno D, Koyama E, Kono L, Ando T, Yano M, Ma JF. Identification of a novel major quantitative trait locus controlling distribution of Cd between roots and shoots in rice. Plant Cell Physiol. 2009;50:2223–33. https://doi.org/10.1093/pcp/pcp160.

    Article  CAS  PubMed  Google Scholar 

  27. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, et al. Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A. 2010;107:16500–5.

    Article  CAS  Google Scholar 

  28. Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, et al. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 2011;189:190–9. https://doi.org/10.1111/j.1469-8137.2010.03459.x.

    Article  CAS  PubMed  Google Scholar 

  29. Sasaki A, Yamaji N, Ma JF. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot. 2014;65:6013–21. https://doi.org/10.1093/jxb/eru340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Yan J, Wang P, Yang M, Lian X, Tang Z, Huang CF, et al. A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ. 2016;39:1941–54. https://doi.org/10.1111/pce.12747.

    Article  CAS  PubMed  Google Scholar 

  31. Shao JF, Fujii-Kashino M, Yamaji N, Fukuoka S, Shen RF, Ma JF. Isolation and characterization of a rice line with high Cd accumulation for potential use in phytoremediation. Plant Soil. 2017;410:357–68. https://doi.org/10.1007/s11104-016-3014-y.

    Article  CAS  Google Scholar 

  32. Kumagai S, Suzuki T, Tezuka K, Satoh-Nagasawa N, Takahashi H, Sakurai K, et al. Functional analysis of the C-terminal region of the vacuolar cadmium-transporting rice OsHMA3. FEBS Lett. 2014;588:789–94. https://doi.org/10.1016/j.febslet.2014.01.037.

    Article  CAS  PubMed  Google Scholar 

  33. Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Ma JF. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 2013;162:927–39. https://doi.org/10.1104/pp.113.216564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, et al. Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2012;53:213–24. https://doi.org/10.1093/pcp/pcr166.

    Article  CAS  PubMed  Google Scholar 

  35. Yamaji N, Ma JF. The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci. 2014;19:556–63. https://doi.org/10.1016/j.tplants.2014.05.007.

    Article  CAS  PubMed  Google Scholar 

  36. Yamaji N, Ma JF. Node-controlled allocation of mineral elements in Poaceae. Curr Opin Plant Biol. 2017;39:18–24. https://doi.org/10.1016/j.pbi.2017.05.002.

    Article  CAS  PubMed  Google Scholar 

  37. Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, et al. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci U S A. 2011;108:20959–64. https://doi.org/10.1073/pnas.1116531109.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sasaki A, Yamaji N, Mitani-Ueno N, Kashino M, Ma JF. A node-localized transporter OsZIP3 is responsible for the preferential distribution of Zn to developing tissues in rice. Plant J. 2015;84:374–84. https://doi.org/10.1111/tpj.13005.

    Article  CAS  PubMed  Google Scholar 

  39. Yamaji N, Sasaki A, Xia JX, Yokosho K, Ma JF. A node-based switch for preferential distribution of manganese in rice. Nat Commun. 2013;4:2442. https://doi.org/10.1038/ncomms3442.

    Article  CAS  PubMed  Google Scholar 

  40. Zheng L, Yamaji N, Yokosho K, Ma JF. YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell. 2012;24:3767–82. https://doi.org/10.1105/tpc.112.103820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Deng F, Yamaji N, Xia J, Ma JF. A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol. 2013;163:1353–62. https://doi.org/10.1104/pp.113.226225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Yamaji N, Takemoto Y, Miyaji T, Mitani-Ueno N, Yoshida KT, Ma JF. Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature. 2017;541:92–5. https://doi.org/10.1038/nature20610.

    Article  CAS  PubMed  Google Scholar 

  43. Uraguchi S, Kamiya T, Clemens S, Fujiwara T. Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiol Plant. 2014;151:339–47. https://doi.org/10.1111/ppl.12189.

    Article  CAS  PubMed  Google Scholar 

  44. Uraguchi S, Tanaka N, Hofmann C, Abiko K, Ohkama-Ohtsu N, Weber M, et al. Phytochelatin synthase has contrasting effects on cadmium and arsenic accumulation in rice grains. Plant Cell Physiol. 2017;58:1730–42. https://doi.org/10.1093/pcp/pcx114/4082758.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hayashi S, Kuramata M, Abe T, Takagi H, Ozawa K, Ishikawa S. Phytochelatin synthase OsPCS1 plays a crucial role in reducing arsenic levels in rice grains. Plant J. 2017;91:840–8. https://doi.org/10.1111/tpj.13612.

    Article  CAS  PubMed  Google Scholar 

  46. Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF. A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol. 2009;182:644–53. https://doi.org/10.1111/j.1469-8137.2009.02784.x.

    Article  CAS  PubMed  Google Scholar 

  47. Ishikawa S, Ae N, Sugiyama M, Murakami M, Arao T. Genotypic variation in shoot cadmium concentration in rice and soybean in soils with different levels of cadmium contamination. Soil Sci Plant Nutr. 2005;51:101–8.

    Article  CAS  Google Scholar 

  48. Liu JG, Zhu QS, Zhang ZJ, Xu JK, Yang JC, Wong MH. Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agr. 2005;85:147–53. https://doi.org/10.1002/jsfa.1973.

    Article  CAS  Google Scholar 

  49. Arao T, Ishikawa S. Genotypic differences in cadmium concentration and distribution of soybean and rice. JARQ. 2006;40:21–30.

    Article  CAS  Google Scholar 

  50. He JY, Zhu C, Ren YF, Yan YP, Jiang D. Genotypic variation in grain cadmium concentration of lowland rice. J Plant Nutr Soil Sci. 2006;169:711–6. https://doi.org/10.1002/jpln.200525101.

    Article  CAS  Google Scholar 

  51. Ishikawa S, Ae N, Yano M. Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol. 2005;168:345–50. https://doi.org/10.1111/j.1469-8137.2005.01516.x.

    Article  CAS  PubMed  Google Scholar 

  52. Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K. Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol. 2009;9:8. https://doi.org/10.1186/1471-2229-9-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by a Grant-in-Aid for Specially Promoted Research (JSPS KAKENHI grant 16H06296 to J.F.M.).

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Correspondence to Jian Feng Ma .

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Wang, W., Yamaji, N., Ma, J.F. (2019). Molecular Mechanism of Cadmium Accumulation in Rice. In: Himeno, S., Aoshima, K. (eds) Cadmium Toxicity. Current Topics in Environmental Health and Preventive Medicine. Springer, Singapore. https://doi.org/10.1007/978-981-13-3630-0_9

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