Route and regulation of zinc, cadmium, and iron transport in rice plants (Oryza sativa L.) during vegetative growth and grain filling: Metal transporters, metal speciation, grain Cd reduction and Zn and Fe biofortification

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 19111-19129

  Yoneyama, Tadakatsu ^a   Ishikawa, Satoru ^b   Fujimaki, Shu ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

^c JAPAN ATOMIC ENERGY AGENCY   (Japan)

Author keywords

Cadmium; Iron; Metal speciation; Metal transporter; Metals in grains; Rice (Oryza sativa L.); Xylem to phloem transport; Zinc

Indexed keywords

CADMIUM; IRON; METAL; ZINC; 2'-DEOXYMUGINEIC ACID; AZETIDINE 2 CARBOXYLIC ACID; NICOTIANAMINE;

ARABIDOPSIS; CAPILLARY ELECTROPHORESIS; GRAIN FILLING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IRON TRANSPORT; MINERALIZATION; PHLOEM; REVIEW; RICE; TIME OF FLIGHT MASS SPECTROMETRY; VEGETATIVE GROWTH; XYLEM; ANALOGS AND DERIVATIVES; CHEMISTRY; FOOD GRAIN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ORYZA SATIVA;

AZETIDINECARBOXYLIC ACID; BIOLOGICAL TRANSPORT; CADMIUM; EDIBLE GRAIN; IRON; ORYZA; PHLOEM; PLANT ROOTS; XYLEM; ZINC;

EID: 84939220232     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160819111     Document Type: Review

References (77)

1. Nouet, C.; Motte, P.; Hanikenne, M. Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci. 2011, 16, 395-404.
2. Palmer, C.M.; Guerinot, M.L. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat. Chem. Biol. 2009, 5, 333-340.
3. Palmgren, M.G.; Clemens, S.; Williams, L.E.; Krämer, U.; Borg, S.; Schjørring, J.K.; Sanders, D. Zinc biofortification of cereals: Problems and solutions. Trends Plant Sci. 2008, 13, 464-473.
4. White, P.J.; Broadley, M.R. Physiological limits to zinc biofortification of edible crops. Front. Plant Sci. 2011, 2, 80.
5. Clemens, S.; Aarts, M.G.M.; Thomine, S.; Verbruggen, N. Plant science: The key to preventing slow cadmium poisoning. Trends Plant Sci. 2012, 18, 92-99.
6. Zimmermann, M.B.; Hurrell, R.F. Improving iron, zinc, vitamin A nutrition through plant biotechnology. Curr. Opin. Biotechnol. 2002, 13, 142-145.
7. Dijkhuizen, M.A.; Wieringa, F.T.; West, C.E. Zinc plus β-carotene supplementation of pregnant women is superior to β-carotene supplementation alone in improving vitamin A status in both mothers and infants. Am. J. Clin. Nutr. 2004, 80, 1299-1307.
8. Fukushima, M.; Ishizaki, A.; Sakamoto, M.; Kobayashi, E. Cadmium concentration in rice eaten by famers in the Jinzu River Basin. Jpn. J. Hyg. 1973, 28, 406-415. (In Japanese)
9. Khoshgoftarmanesh, A.H.; Schulin, R.; Chaney, R.L.; Daneshbakhsh, B.; Afyuni, M. Micronutrient-efficient genotypes for crop yield and nutritional quality in sustainable agriculture. A review. Agron. Sustain. Dev. 2010, 30, 83-107.
10. Simmons, R.W.; Pongsakul, P.; Chaney, R.L.; Saiyasitpanich, D.; Klinphoklap, S.; Nobuntou, W. The relative exclusion of zinc and iron from rice grain in relation to rice grain cadmium as compared to soybean: Implications for human health. Plant Soil 2003, 257, 163-170.
11. Wissuwa, M.; Ismail, A.M.; Graham, R.D. Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. Plant Soil 2008, 306, 37-48.
12. Ito, H.; Iimura, K. Absorption of zinc and cadmium by rice plants and their influence on its growth. II. Effect of cadmium. Jpn. J. Soil Sci. Plant Nutr. 1976, 47, 44-48.
13. Ito, H.; Iimura, K. Absorption of zinc and cadmium by rice plants and their influence on its growth. I. Effect of zinc. Jpn. J. Soil Sci. Plant Nutr. 1976, 47, 39-43.
14. Jiang, W.; Struik, P.C.; van Keulen, H.; Zhao, M.; Jin, L.N.; Stomph, T.J. Does increased zinc uptake enhance grain zinc mass concentration in rice? Ann. Appl. Biol. 2008, 153, 135-147.
15. Shiratori, K.; Suzuki, T.; Miyoshi, H. Chemical forms of soil zinc in the salt-rich reclaimed fields, where zinc-deficiency symptoms were observed in rice plants. Jpn. J. Soil Sci. Plant Nutr. 1972, 43, 291-296.
16. Khaokaew S.; Chaney, R.L.; Landrot, G.; Ginder-Vogel, M.; Sparks, D.L. Speciation and release kinetics of cadmium in an alkaline paddy soil under various flooding periods and draining conditions. Environ. Sci. Technol. 2011, 45, 4249-4255.
17. Hashimoto, Y.; Yamaguchi, N. Chemical speciation of cadmium and sulfur K-edge XANES spectroscopy in flooded paddy soils amended with zerovalent iron. Soil Sci. Soc. Am. J. 2013, 77, 1189-1198.
18. Lee, S.; An, G. Over-expression of OsIRT1 leads to iron and zinc accumulations in rice. Plant Cell Environ. 2009, 32, 408-416.
19. Ishikawa, S.; Ishimaru, Y.; Igura, M.; Kuramata, M.; Abe, T.; Senoura, T.; Hase, Y.; Arao, T.; Nishizawa, N.K.; Nakanishi, H. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc. Natl. Acad. Sci. USA 2012, 109, 19166-19171.
20. Sasaki, A.; Yamaji, N.; Yokosho, K.; Ma, J.F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 2012, 24, 2155-2167.
21. Nakanishi, H.; Ogawa, I.; Ishimaru, Y.; Mori, S.; Nishizawa, N.K. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci. Plant Nutr. 2006, 52, 464-469.
22. Inoue, H.; Kobayashi, T.; Nozoye, T.; Takahashi, M.; Kakei, Y.; Suzuki, K.; Nakazono, M.; Nakanishi, H.; Mori, S.; Nishizawa, N.K. Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J. Biol. Chem. 2009, 284, 3470-3479.
23. Ishimaru, Y.; Suzuki, M.; Tsukamoto, T.; Suzuki, K.; Nakazono, M.; Kobayashi, T.; Wada, Y.; Watanabe, S.; Matsuhashi, S.; Takahashi, M. et al. Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J. 2006, 45, 335-346.
24. Haydon, M.J.; Kawachi, M.; Wirtz, M.; Hillmer, S.; Hell, R.; Krämer, U. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 2012, 24, 724-737.
25. Ueno, D.; Yamaji, N.; Kono, I.; Huang, C.F.; Ando, T.; Yano, M.; Ma, J.F. Gene limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. USA 2010, 107, 16500-16505.
26. Nocito, F.F.; Lancilli, C.; Dendena, B.; Lucchini, G.; Sacchi, G.A. Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ. 2011, 34, 994-1008
27. Takahashi, R.; Ishimaru, Y.; Shimo, H.; Ogo, Y.; Senoura, T.; Nishizawa, N.K.; Nakanishi, H. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ. 2012, 35, 1948-1957.
28. Yamaji, N.; Xia, J.; Mitani-Ueno, N.; Yokosho, K.; Ma, J.F. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 2013, 162, 927-939.
29. Kakei, Y.; Ishimaru, Y.; Kobayashi, T.; Yamakawa, T.; Nakanshi, H.; Nishizawa, N.K. OsYSL16 plays a role in the allocation of iron. Plant Mol. Biol. 2012, 79, 583-594.
30. Lee, S.; Chiecko, J.C.; Kim, S.A.; Walker, E.L.; Lee, Y.; Guerinot, M.L.; An, G. Disruption of OsYSL15 leads to inefficiency in rice plants. Plant Physiol. 2009, 150, 786-800.
31. Aoyama, T.; Kobayashi, T.; Takahashi, M.; Nagasaka, S.; Usuda, K.; Kakei, Y.; Ishimaru, Y.; Nakanishi, H.; Mori, S.; Nishizawa, N.K. OsYSL18 is a rice iron(III)-deoxymugineic acid transporter specifically expressed in reproductive organs and phloem of lamina joints. Plant Mol. Biol. 2009, 70, 681-692.
32. Widodo Broadley, M.R.; Rose, T.; Frei, M.; Pariasca-Tanaka, J.; Yoshihashi, T.; Thomson, M.; Hammond, J.P.; Aprile, A.; Close, T.J. et al. Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rate, and not by zinc-transport activity. New Phytol. 2010, 186, 400-414.
33. Takagi, S.; Nomoto, K.; Takemoto, S. Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J. Plant Nutr. 1984, 7, 469-477.
34. Nozoye, T.; Nagasaka, S.; Kobayashi, T.; Takahashi, M.; Sato, Y.; Uozumi, N.; Nakanishi, H.; Nishizawa, N.K. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 2011, 286, 5446-5454.
35. Weber, G.; von Wiren, N.; Hayen, H. Investigation of ascorbate-mediated iron release from ferric phytosiderophores in the presence of nicotianamine. Biometals 2008, 21, 503-513.
36. Ariga, T.; Hazama, K.; Yanagisawa, S.; Yoneyama, T. Chemical forms of iron in xylem sap from graminaceous and non-graminaceous plants. Soil Sci. Plant Nutr. 2014, 60, 460-469.
37. Park, J.; Song, W.-Y.; Ko, D.; Eom, Y.; Hansen, T.H.; Schiller, M.; Lee, T.G.; Martinoia, E.; Lee, Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012, 69, 278-288.
38. Ishikawa, S.; Suzui, N.; Ito-Tanabata, S.; Ishii, S.; Igura, M.; Abe, T.; Kuramata, M,; Kawachi, N.; Fujimaki, S. Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting 107Cd trace. BMC Plant Biol. 2011, 11, 172.
39. Yokosho, K.; Yamaji, N.; Ueno, D.; Mitani, N.; Ma, J.F. OsFRDL1 is a citrate transporter required for efficient transformation of iron in rice. Plant Physiol. 2009, 149, 297-305.
40. Kawabe, S.; Fukumorita, T.; Chino, M. Collection of rice phloem sap from stylets of homopterous insects severed by YAG laser. Plant Cell Physiol. 1980, 21, 1319-1327.
41. Nishiyama, R. Zinc Transport via Phloem in Rice Plants. Master thesis, Graduate School of Agricultural and Life Sciences, the University of Tokyo, Tokyo, Japan, 2006.
42. Kato, M. The University of Tokyo, Tokyo, Unpublished work, 2006.
43. Nishiyama, R.; Kato, M.; Nagata, S.; Yanagisawa, S.; Yoneyama, T. Identification of Zn-nicotianamine and Fe-2′-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.). Plant Cell Physiol. 2012, 53, 381-390.
44. Kato, M.; Ishikawa, S.; Inagaki, K.; Chiba, K.; Hayashi, H.; Yanagisawa, S.; Yoneyama, T. 2010: Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants (Oryza sativa L.). Soil Sci. Plant Nutr. 2010, 56, 839-847.
45. Álvarez-Fernández, A.; Díaz-Benito, P.; Abadía, A.; Lopez-Millán, A.-F.; Abadía, J. 2014: Metal species involved in long distance metal transport in plants. Front. Plant Sci. 2014, 5, 105.
46. Ando, Y.; Nagata, S.; Yanagisawa, S.; Yoneyama, T. Copper in xylem and phloem from rice (Oryza sativa): The effect of moderate copper concentrations in the growth medium on the accumulation of five essential metals and a speciation analysis of copper-containing compounds. Funct. Plant Biol. 2013, 40, 89-100.
47. Obata, H.; Kitagishi, K. Longitudinal distribution pattern of zinc and manganese in leaf with special reference to aging. Jpn. J. Soil Sci. Plant Nutr. 1980, 51, 285-291.
48. Kitagishi, K.; Obata, H.; Kondo, T. Effect of zinc deficiency on 80S ribosome content of meristematic tissues of rice plant. Soil Sci. Plant Nutr. 1987, 33, 423-429.
49. Obata, H.; Kitagishi, K. Accumulation and retranslocation of zinc in a leaf of rice plant with reference to aging. Jpn. J. Soil Sci. Plant Nutr. 1982, 53, 235-240.
50. Kitagishi, K.; Obata, H. Retrieval of zinc from transpiration stream in the nodes of rice plants as affected by the concentration of zinc in culture solution. Rep. Environ. Sci. Mie Univ. 1982, 7, 91-97.
51. Yamaguchi, N.; Ishikawa, S.; Abe, T.; Baba, K.; Arao, T.; Terada, Y. Role of the node in controlling traffic of cadmium, zinc, and manganese in rice. J. Exp. Bot. 2012, 63, 2729-2737.
52. Kitagishi, K.; Obata, H. Distribution of 115mCd in rice plants absorbed by roots at vegetative stage. Rep. Environ. Sci. Mie Univ. 1979, 4, 59-65.
53. Kobayashi, N.I.: Tanoi, K.; Hirose, A.; Nakanishi, T.M. Characterization of rapid intervascular transport of cadmium in rice stem by radioisotope imaging. J. Exp. Bot. 2013, 64, 507-517.
54. Tsukamoto, T.; Nakanishi, H.; Uchida, H.; Watanabe, S.; Matsuhashi, S.; Mori, S.; Nishizawa, N.K. 2009: 52Fe translocation in barley as monitored by a positron emitting tracer imaging system (PETIS): Evidence for the direct translocation of Fe from roots to young leaves via phloem. Plant Cell Physiol. 2009, 50, 48-57.
55. Yoneyama, T.; Gosho, T.; Kato, M.; Goto, S.; Hayashi, H. Xylem and phloem transport of Cd, Zn and Fe into the grains of rice plants (Oryza sativa L.) grown in continuously flooded Cd-contaminated soil. Soil Sci. Plant Nutr. 2010, 56, 445-453.
56. Zee, S.-Y. Transfer cells and vascular tissue distribution in the vegetative nodes of rice. Aust. J. Bot. 1972, 20, 41-48.
57. Kawahara, H.; Chonan, N.; Matsuda, T. Studies on morphogenesis in rice plants. 7. The morphology of vascular bundles in the vegetative nodes of the culm. Proc. Crop Sci. Soc. Jpn. 1974, 43, 389-401.
58. Chonan, N.; Kawahara, H.; Matsuda, T. Ultrastructure of elliptical and diffuse bundles in the vegetative nodes of rice. Jpn. J. Crop Sci. 1984, 54, 393-402.
59. Wu, C.-Y.; Lu, L.-L.; Yang, X.-E.; Feng, Y.; Wei, Y.-Y.; Hao, H.-L.; Stoffella, P.J.; He, Z.-L. Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J. Agric. Food Chem. 2010, 58, 6767-6773.
60. Nishiyama, R.; Tanoi, K.; Yanagisawa, S.; Yoneyama, T. 2013: Quantification of zinc transport to the grain in rice plants (Oryza sativa L.) at early grain-filling by a combination of mathematical modeling and 65Zn tracing. Soil Sci. Plant Nutr. 2013, 59, 750-755.
61. Tanaka, K.; Fujimaki, S.; Fujiwara, T.; Yoneyama, T.; Hayashi, H. Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants (Oryza sativa L.). Soil Sci. Plant Nutr. 2007, 53, 72-77.
62. Rodda, M.S.; Li, G.; Reid, R.J. The timing of grain Cd accumulation in rice plants: The relative importance of remobilization within the plant and root Cd uptake post-flowering. Plant Soil 2011, 347, 105-114.
63. Fujimaki, S.; Suzui, N.; Ishioka, N.S.; Kawachi, N.; Ito, S.; Chino, M.; Nakamura, S. Tracing cadmium from culture to spikelet: Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol. 2010, 152, 1796-1806.
64. Zee, S.-Y. Vascular tissue and transfer cell distribution in the rice spikelet. Aust. J. Biol. Sci. 1972, 25, 411-414.
65. Kawahara, H.; Matsuda, T.; Chonan, N. Studies on morphogenesis in rice plants. 9. On the structure of vascular bundles and phloem transport in the spikelet. Proc. Crop Sci. Soc. Jpn. 1977, 46, 82-90.
66. Herren, T.; Feller, U. Transfer of zinc from xylem to phloem in the peduncle of wheat. J. Plant Nutr. 1994, 17, 1587-1598.
67. Jiang, W.; Struik, P.C.; Lingna, J.; van Keulen, H.; Ming, Z.; Stomph, T.J. Uptake and distribution of root-applied or foliar-applied 65Zn after flowering in aerobic rice. Ann. Appl. Biol. 2007, 150, 383-391.
68. Sperotto, P.A.; Ricachenevsky, F.K.; Waldow, V.A.; Fett, J.P. Iron biofortification in rice: It’s a long way to the top. Plant Sci. 2012, 190, 24-39.
69. Moritsugu, M. A study on combination of glutelin with cadmium in rice grain. Ber. Obara Inst. Landwirtsch. Biol. 1964, 12, 251-260.
70. Schuler, M.; Rellán-Álvarez, R.; Fink-Straube, C.; Abadía, J.; Bauer, P. Nicotianamine functions in the phloem-based transport of iron to sink organs in pollen development and pollen tube growth in Arabidopsis. Plant Cell 2012, 24, 2380-2400.
71. Yuan, L.; Wu, L.; Yang, C.; Lv, Q. Effects of iron and zinc foliar applications on rice plants and their grain accumulation and grain quality. J. Sci. Food Agric. 2012, 93, 254-261.
72. Ishimaru, Y.; Kim, S.; Tsukamoto, T.; Oki, H.; Kobayashi, T.; Watanabe, S.; Matsuhashi, S.; Takahashi, M.; Nakanishi, H.; Mori, S. et al. Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc. Natl. Acad. Sci. USA 2007, 104, 7373-7378.
73. Masuda, H.; Usuda, K.; Kobayashi, T.; Ishimaru, Y.; Kakei, Y.; Takahashi, M.; Higuchi, K.; Nakanishi, H.; Mori, S.; Nishizawa, K.N. Overexpression of the barley nicotianamine synthase gene HvHAS1 increases iron and zinc concentrations in rice grains. Rice 2009, 2, 155-166.
74. Lee, S.; Jeon, U.S.; Lee, S.J.; Kim, Y.-K.; Persson, D.P.; Husted, S.; Schjørring, J.K.; Kakei, Y.; Masuda, H.; Nishizawa, N.K. et al. Iron fortification of rice seeds through activation of the nicotianamine synthase gene. Proc. Nat. Acad. Sci. USA 2009, 106, 22014-22019.
75. Zheng, L.; Cheng, Z.; Ai, C.; Jiang, X.; Bei, X.; Zheng, Y.; Glahn, R.P.; Welch, R.M.; Miller, D.D.; Lei, X.G. et al. Nicotianamine, a novel enhancer of rice iron bioavailability to humans. PLoS ONE 2010, 5, e10190.
76. Reeves, P.G.; Chaney, R.L. Bioavailability as an issue in risk assessment and management of food cadmium: A review. Sci. Total Environ. 2008, 398, 13-19.
77. Codex Alimentarius (2014) CODEX STAN 193-1995, General Standard for Contaminants and Toxins in Food and Feed. Available online: http://www.codexalimentarius.org/download/standards/17/CXS_193e2015.pdf (accessed on 31 March 2015).