Previously, we reported that OsNRAMP5 functions as a manganese, iron, and cadmium (Cd) transporter. The shoot Cd content in OsNRAMP5 RNAi plants was higher than that in wild-type (WT) plants, whereas the total Cd content (roots plus shoots) was lower. For efficient Cd phytoremediation, we produced OsNRAMP5 RNAi plants using the natural high Cd-accumulating cultivar Anjana Dhan (A5i). Using a positron-emitting tracer imaging system, we assessed the time-course of Cd absorption and accumulation in A5i plants. Enhanced 107Cd translocation from the roots to the shoots was observed in A5i plants. To evaluate the phytoremediation capability of A5i plants, we performed a field experiment in a Cd-contaminated paddy field. The biomass of the A5i plants was unchanged by the suppression of OsNRAMP5 expression; the A5i plants accumulated twice as much Cd in their shoots as WT plants. Thus, A5i plants could be used for rapid Cd extraction and the efficient phytoremediation of Cd from paddy fields, leading to safer food production.
References
[1]
World Health Organization (WHO), International Agency for Research on Cancer (IARC). (2012) Monographs on the evaluation of carcinogenic risks to humans: Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry. Summary of data reported and evaluation. http://monographs.iarc.fr/ENG/Monographs？/vol58/volume58.pdf.
[2]
Moon C-S, Paik J-M, Choi C-S, Kim D-H, Ikeda M (2003) Lead and cadmium levels in daily foods, blood and urine in children and their mothers in Korea. Int Arch Occup Environ Health 76: 282–288.
[3]
Watanabe T, Shimbo S, Nakatsuka H, Koizumi A, Higashikawa K, et al. (2004) Gender-related difference, geographical variation and time trend in dietary cadmium intake in Japan. Sci Total Environ 329: 17–27. doi: 10.1016/j.scitotenv.2004.03.010
[4]
Cheng F, Zhao N, Xu H, Li Y, Zhang W, et al. (2006) Cadmium and lead contamination in japonica rice grains and its variation among the different locations in southeast China. Sci Total Environ 359: 156–166. doi: 10.1016/j.scitotenv.2005.05.005
[5]
Fujimaki S, Suzuki N, Ishioka NS, Kawachi N, Ito S, et al. (2010) 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 152: 1796–1806. doi: 10.1104/pp.109.151035
[6]
Ishikawa S, Suzui N, Ito-Tanabata S, Ishii S, Igura M, et al. (2011) Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positoron-emitting 107Cd tracer. BMC Plant Biol 11: 172. doi: 10.1186/1471-2229-11-172
[7]
Ishikawa S, Ae N, Murakami M, Wagatsuma T (2006) Is Brassica juncea a suitable plant for phytoremediation of cadmium in soils with moderately low cadmium contamination? – Possibility of using other plant species for Cd-phytoextraction. Soil Sci Plant Nutr 52: 32–42. doi: 10.1111/j.1747-0765.2006.00008.x
[8]
Arao T, Ae N (2003) Genotypic variations in cadmium levels of rice grain. Soil Sci Plant Nutr 49: 473–479. doi: 10.1080/00380768.2003.10410035
[9]
Ishikawa S, Ae N, Sugiyama M, Murakami M, Arao T (2005) Genotypic variation in shoot cadmium concentration in rice and soybean in soils with different levels of cadmium contamination. Soil Sci Plant Nutr 51: 101–108. doi: 10.1111/j.1747-0765.2005.tb00012.x
[10]
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, et al. (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60: 2677–2688. doi: 10.1093/jxb/erp119
[11]
Ibaraki T, Kuroyanagi N, Murakami M (2009) Practical phytoextraction in cadmium-polluted paddy fields using a high cadmium accumulating rice plant cultured by early drainage of irrigation water. Soil Sci Plant Nutr 55: 421–427. doi: 10.1111/j.1747-0765.2009.00367.x
[12]
Murakami M, Nakagawa F, Ae N, Ito M, Arao T (2009) Phytoextraction by rice capable of accumulating Cd at high levels: Reduction of Cd content of rice grain. Environ Sci Technol 43: 5878–5883. doi: 10.1021/es8036687
[13]
Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochim Biophys Acta 1763: 609–620. doi: 10.1016/j.bbamcr.2006.05.007
[14]
Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. PNAS 97: 4991–4996. doi: 10.1073/pnas.97.9.4991
[15]
Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P (2003) Differential regulation of nramp and irt metal transporter genes in wild type and iron uptake mutants of tomato. J Biol Chem 278: 24697–24704. doi: 10.1074/jbc.m301365200
[16]
Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, et al. (2003) The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. Plant J 35: 295–304. doi: 10.1046/j.1365-313x.2003.01802.x
[17]
Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, et al. (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiol Biochem 43: 793–801. doi: 10.1016/j.plaphy.2005.07.006
[18]
Xiao H, Yin L, Xu X, Li T, Han Z (2008) The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Ann Bot 102: 881–889. doi: 10.1093/aob/mcn178
[19]
Oomen RJFJ, Wu J, Lelievre F, Blanchet S, Richaud P, et al. (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181: 637–650. doi: 10.1111/j.1469-8137.2008.02694.x
[20]
Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. PNAS 107: 18381–18385. doi: 10.1073/pnas.1004949107
[21]
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H (2012) The role of heavy metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav 7: 1799–1801. doi: 10.4161/psb.22454
[22]
Curie C, Alonso JM, Jean ML, Ecker JR, Briat J-F (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347: 749–755. doi: 10.1042/0264-6021:3470749
[23]
Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34: 685–695. doi: 10.1046/j.1365-313x.2003.01760.x
[24]
Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, et al. (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24: 4041–4051. doi: 10.1038/sj.emboj.7600864
[25]
Lanquar V, Ramos MS, Lelievre F, Barbier-Brygoo H, Krieger-Liszkay A, et al. (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol 152: 1986–1999. doi: 10.1104/pp.109.150946
[26]
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. doi: 10.1105/tpc.109.073023
[27]
Cailliatte R, Lapeyre B, Briat J-F, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422: 217–228. doi: 10.1042/bj20090655
[28]
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, et al. (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62: 4843–4850. doi: 10.1093/jxb/err136
[29]
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, et al. (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmiun transport. Sci Rep 2: 286. doi: 10.1038/srep00286
[30]
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. doi: 10.1105/tpc.112.096925
[31]
Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, et al. (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45: 335–346. doi: 10.1111/j.1365-313x.2005.02624.x
[32]
Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, et al. (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. PNAS 104: 7373–7378. doi: 10.1073/pnas.0610555104
[33]
Suzuki M, Takahashi M, Tsukamoto T, Watanabe S, Matsuhashi S, et al. (2006) Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J 48: 85–97. doi: 10.1111/j.1365-313x.2006.02853.x
[34]
Suzuki M, Tsukamoto T, Inoue H, Watanabe S, Matsuhashi S, et al. (2008) Deoxymugineic acid increases Zn translocation in Zn-deficient rice plants. Plant Mol Biol 66: 609–617. doi: 10.1007/s11103-008-9292-x
[35]
Tsukamoto T, Nakanishi H, Kiyomiya S, Watanabe S, Matsuhashi S, et al. (2006) 52Mn translocation in barley monitored using a positron-emitting tracer imaging system. Soil Sci Plant Nutr 52: 717–725. doi: 10.1111/j.1747-0765.2006.00096.x
[36]
Tsukamoto T, Nakanishi H, Uchida H, Watanabe S, Matsuhashi S, et al. (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 50: 48–57. doi: 10.1093/pcp/pcn192
[37]
Nakamura S, Suzui N, Nagasaka T, Komatsu F, Ishioka NS, et al. (2013) Application of glutathione to roots selectively inhibits cadmium transport from roots to shoots in oilseed rape. J Exp Bot 64: 1073–1081. doi: 10.1093/jxb/ers388
[38]
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, et al. (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35: 1948–1957. doi: 10.1111/j.1365-3040.2012.02527.x
[39]
Masuda H, Ishimaru Y, Aung MS, Kobayashi T, Kakei Y, et al. (2012) Iron biofortification in rice by the introduction of multiple genes involved in iron nutrition. Sci Rep 2: 543. doi: 10.1038/srep00543
[40]
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52: 464–469. doi: 10.1111/j.1747-0765.2006.00055.x
[41]
Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK (2011) Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav 6: 1813–1816. doi: 10.4161/psb.6.11.17587
[42]
Ishimaru Y, Bashir K, Nakanishi H, Nishizawa NK (2012) OsNRAMP5, a major player for constitutive iron and manganese uptake in rice. Plant Signal and Behav 7: 763–766. doi: 10.4161/psb.20510
[43]
Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, et al. (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. PNAS 109: 19166–19171. doi: 10.1073/pnas.1211132109
[44]
Cheng L, Wang F, Shou H, Huang F, Zheng L, et al. (2007) Mutation in nicotianamine aminotransferase stimulated the Fe (II) acquisition system and led to iron accumulation in rice. Plant Physiol 145: 1647–1657. doi: 10.1104/pp.107.107912
