Ion-beam Irradiation, Gene Identification, and Marker-assisted Breeding in the Development of Low-cadmium Rice

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2012 Nov 8

PMID 23132948

Citations 122

Authors

Satoru Ishikawa

Yasuhiro Ishimaru

Masato Igura

Masato Kuramata

Tadashi Abe

Takeshi Senoura

Yoshihiro Hase

Tomohito Arao

Naoko K Nishizawa

Hiromi Nakanishi

Affiliations

Soon will be listed here.

Abstract

Rice (Oryza sativa L.) grain is a major dietary source of cadmium (Cd), which is toxic to humans, but no practical technique exists to substantially reduce Cd contamination. Carbon ion-beam irradiation produced three rice mutants with <0.05 mg Cd⋅kg(-1) in the grain compared with a mean of 1.73 mg Cd⋅kg(-1) in the parent, Koshihikari. We identified the gene responsible for reduced Cd uptake and developed a strategy for marker-assisted selection of low-Cd cultivars. Sequence analysis revealed that these mutants have different mutations of the same gene (OsNRAMP5), which encodes a natural resistance-associated macrophage protein. Functional analysis revealed that the defective transporter protein encoded by the mutant osnramp5 greatly decreases Cd uptake by roots, resulting in decreased Cd in the straw and grain. In addition, we developed DNA markers to facilitate marker-assisted selection of cultivars carrying osnramp5. When grown in Cd-contaminated paddy fields, the mutants have nearly undetectable Cd in their grains and exhibit no agriculturally or economically adverse traits. Because mutants produced by ion-beam radiation are not transgenic plants, they are likely to be accepted by consumers and thus represent a practical choice for rice production worldwide.

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References

Kazama Y, Hirano T, Saito H, Liu Y, Ohbu S, Hayashi Y . Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biol. 2011; 11:161. PMC: 3261129. DOI: 10.1186/1471-2229-11-161. View

Ishikawa S, Ae N, Yano M . Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol. 2005; 168(2):345-50. DOI: 10.1111/j.1469-8137.2005.01516.x. View

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(3):223-33. DOI: 10.1269/jrr.09143. View

Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T . OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 2010; 189(1):190-9. DOI: 10.1111/j.1469-8137.2010.03459.x. View

Tsuchiya K . Epidemiological studies on cadmium in the environment in Japan: etiology of itai-itai disease. Fed Proc. 1976; 35(12):2412-8. View

Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K . Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2011; 53(1):213-24. DOI: 10.1093/pcp/pcr166. View

Pinner E, Gruenheid S, Raymond M, Gros P . Functional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family. J Biol Chem. 1997; 272(46):28933-8. DOI: 10.1074/jbc.272.46.28933. View

Uraguchi S, Fujiwara T . Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice (N Y). 2014; 5(1):5. PMC: 3834507. DOI: 10.1186/1939-8433-5-5. View

Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, K Nishizawa N . The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ. 2012; 35(11):1948-57. DOI: 10.1111/j.1365-3040.2012.02527.x. View

10.

Ueno D, Yamaji N, Kono I, Huang C, Ando T, Yano M . Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A. 2010; 107(38):16500-5. PMC: 2944702. DOI: 10.1073/pnas.1005396107. View

11.

Sasaki A, Yamaji N, Yokosho K, Ma J . Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell. 2012; 24(5):2155-67. PMC: 3442593. DOI: 10.1105/tpc.112.096925. View

12.

Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K . Characterizing the role of rice NRAMP5 in Manganese, Iron and Cadmium Transport. Sci Rep. 2012; 2:286. PMC: 3285952. DOI: 10.1038/srep00286. View

13.

Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T . 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. 2009; 61(3):923-34. PMC: 2814118. DOI: 10.1093/jxb/erp360. View

14.

Lidon F, Barreiro M, Ramalho J . Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol. 2004; 161(11):1235-44. DOI: 10.1016/j.jplph.2004.02.003. View

15.

Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T . The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot. 2011; 62(14):4843-50. PMC: 3192999. DOI: 10.1093/jxb/err136. View

16.

Kikuchi K, Terauchi K, Wada M, Hirano H . The plant MITE mPing is mobilized in anther culture. Nature. 2003; 421(6919):167-70. DOI: 10.1038/nature01218. View

17.

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(9):2677-88. PMC: 2692013. DOI: 10.1093/jxb/erp119. View

18.

Curie C, Alonso J, Le Jean M, Ecker J, Briat J . Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J. 2000; 347 Pt 3:749-55. PMC: 1221012. View

19.

Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y . Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci U S A. 2011; 108(52):20959-64. PMC: 3248505. DOI: 10.1073/pnas.1116531109. View