Cadmium Toxicity pp 139-150 | Cite as
Development of Low-Cadmium-Accumulating Rice
Abstract
Cadmium (Cd) has an important impact on agriculture, and the excessive consumption of Cd from contaminated food crops can lead to toxicity in humans. Rice (Oryza sativa L.) is the greatest source of dietary intake of Cd for populations that consume rice as a staple food. However, there is currently no practical technique designed to substantially reduce the Cd contamination of rice. Here, we report a new rice cultivar, Koshihikari Kan No. 1, which does not accumulate Cd in the grains. Koshihikari Kan No. 1 is a mutant produced from ion-beam irradiation. This cultivar has a single-nucleotide deletion in OsNRAMP5, which encodes a manganese transporter that incidentally transports Cd into rice; this deletion results in a decreased root Cd uptake. In Cd-contaminated paddy fields, Koshihikari Kan No. 1 showed nearly undetectable Cd concentrations in the grains and exhibited no economically adverse traits. A DNA marker, which detects the mutated region of OsNRAMP5, has been developed to facilitate marker-assisted breeding of cultivars with low-Cd traits. Our findings will help to greatly reduce Cd levels in paddy rice.
Keywords
Cadmium Ion beam Marker-assisted breeding OsNRAMP5 transporter Rice mutantReferences
- 1.Alloway BJ, Steinnes E. Anthropogenic additions of cadmium to soils. In: McLaughlin MJ, Singh BR, editors. Cadmium in soils and plants. The Netherlands: Kluwer Academic Publishers; 1999. p. 97–123.CrossRefGoogle Scholar
- 2.Tsuchiya K. Epidemiological-studies on cadmium in environment in Japan - etiology of itai-itai disease. Fed Proc. 1976;35:2412–8.PubMedGoogle Scholar
- 3.FAO/WHO. Joint FAO/WHO Expert Committee on Food Additives, Seventy-third Meeting, Geneva, 8–17 June 2010. Summary and Conclusions; 2010. http://www.who.int/foodsafety/publications/chem/summary73.pdf.
- 4.CODEX STAN 193-1995. Codex general standard for contaminants and toxins in foods and feed; 2008. www.fao.org/fileadmin/user_upload/agns/pdf/CXS_193e.pdf.
- 5.IRRI. World Production and Consumption of Domestic Milled Rice; 2011. http://ricestat.irri.org/vis/wrs_quickCharts.php
- 6.Arao T, Ishikawa S, Murakami M, Abe K, Maejima Y, Makino T. Heavy metal contamination of agricultural soil and countermeasures in Japan. Paddy Water Environ. 2010;8:247–57.CrossRefGoogle Scholar
- 7.Grant CA, Clarke JM, Duguid S, Chaney RL. Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ. 2008;390:301–10.CrossRefGoogle Scholar
- 8.Arao T, Ae N. Genotypic variations in cadmium levels of rice grain. Soil Sci Plant Nutr. 2003;49:473–9.CrossRefGoogle Scholar
- 9.Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot. 2009;60:2677–88.CrossRefGoogle Scholar
- 10.Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M. A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot. 2010;61:923–34.CrossRefGoogle Scholar
- 11.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.CrossRefGoogle Scholar
- 12.Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H. 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.CrossRefGoogle Scholar
- 13.Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep. 2012;2:286.CrossRefGoogle Scholar
- 14.Nakanishi H, Ogawa I, 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.CrossRefGoogle Scholar
- 15.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.CrossRefGoogle Scholar
- 16.Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot. 2011;62:4843–50.CrossRefGoogle Scholar
- 17.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. OsHMA3, a P-1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 2011;189:190–9.CrossRefGoogle Scholar
- 18.Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF. Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A. 2010;107:16500–5.CrossRefGoogle Scholar
- 19.Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H. Mutations in Rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2012;53:213–24.CrossRefGoogle Scholar
- 20.Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci U S A. 2011;108:20959–64.CrossRefGoogle Scholar
- 21.Yamaji N, Xia JX, 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. 2013b;162:927–39.CrossRefGoogle Scholar
- 22.Kazama Y, Hirano T, Saito H, Liu Y, Ohbu S, Hayashi Y, Abe T. Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biol. 2011;11:161.CrossRefGoogle Scholar
- 23.Tanaka A, Shikazono N, Hase Y. Studies on biological effects of ion beams on lethality, molecular nature of mutation, mutation rate, and spectrum of mutation phenotype for mutation breeding in higher plants. J Radiat Res. 2010;51:223–33.CrossRefGoogle Scholar
- 24.Takeuchi Y, Hori K, Suzuki K, Nonoue Y, Takemoto-Kuno Y, Maeda H, Sato H, Hirabayashi H, Ohta H, Ishii T, Kato H, Nemoto H, Imbe T, Ohtsubo K, Yano M, Ando I. Major QTLs for eating quality of an elite Japanese rice cultivar, Koshihikari, on the short arm of chromosome 3. Breed Sci. 2008;58:437–45.CrossRefGoogle Scholar
- 25.Ishikawa S, Makino T, Ito M, Harada K, Nakada H, Nishida I, Nishimura M, Tokunaga T, Shirao K, Yoshizawa C, Matsuyama M, Abe T, Arao T. Low-cadmium rice (Oryza sativa L.) cultivar can simultaneously reduce arsenic and cadmium concentrations in rice grains. Soil Sci Plant Nutr. 2016;62:327–39.CrossRefGoogle Scholar
- 26.Yamaji N, Sasaki A, Xia JX, Yokosho K, Ma JF. A node-based switch for preferential distribution of manganese in rice. Nat Commun. 2013a;4:2442.CrossRefGoogle Scholar
- 27.Honma T, Shiratori Y, Ohba H, Tsuchida T, Makino T, Abe T, Ishikawa S. Concentrations of nutrient content in rice variety KoshihikariKan no.1 and risk estimation of incidence of brown spot disease in different paddy fields. Jpn J Soil Sci Plant Nutr. 2017;88:213–20. (Japanense with English summary)Google Scholar
- 28.Junior LAZ, Rodrigues FA, Fontes RL, Korndorfer GH, Neves JC. Rice resistance to Brown spot mediated by silicon and its interaction with manganese. J Phytopathol. 2009;157:73–8.CrossRefGoogle Scholar