Functional analyses of TaHMA2, a P1B-type ATPase in wheat

Plant Biotechnology Journal

Volumn 11, Issue 4, 2013, Pages 420-431

  Tan, Jinjuan ^a   Wang, Jianwu ^a   Chai, Tuanyao ^a   Zhang, Yuxiu ^b   Feng, Shanshan ^a   Li, Yan ^a   Zhao, Huijun ^a   Liu, Huimin ^a   Chai, Xingping ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b CHINA UNIVERSITY OF MINING AND TECHNOLOGY   (China)

Author keywords

Cadmium; Rice; Seed; TaHMA2; Wheat; Zinc

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CADMIUM; VEGETABLE PROTEIN; ZINC;

ARTICLE; CELL MEMBRANE; ENZYMOLOGY; GENETICS; METABOLISM; RICE; TRANSGENIC PLANT; WHEAT;

ADENOSINE TRIPHOSPHATASES; CADMIUM; CELL MEMBRANE; ORYZA SATIVA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TRITICUM; ZINC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; DICOTYLEDONEAE; LILIOPSIDA; NICOTIANA TABACUM; ORYZA SATIVA; TRITICUM AESTIVUM;

EID: 84876972782     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12027     Document Type: Article

References (49)

1. Becher, M., Talke, I.N., Krall, L. and Krämer, U. (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251-268.
2. Chonan, N., Kawahara, H. and Matsuda, T. (1985) Ultrastructure of elliptical and diffuse bundles in the vegetative nodes of rice. Jpn J. Crop Sci. 54, 393-402.
3. Chvapil, M. (1973) New aspects in the biological role of zinc: a stabilizer of macromolecules and biological membranes. Life Sci. 13, 1041-1049.
4. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
5. Coleman, J.E. (1998) Zinc enzymes. Curr. Opin. Chem. Biol. 2, 222-234.
6. Drakakaki, G., Marcel, S., Glahn, R.P., Lund, E.K., Pariagh, S., Fischer, R., Christou, P. and Stoger, E. (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol. Biol. 59, 869-880.
7. Eren, E. and Argüello, J.M. (2004) Arabidopsis HMA2, a divalent heavy metal-transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol. 136, 3712-3723.
8. 2+-ATPase HMA2. J. Biol. Chem. 281, 33881-33891.
9. Gallois, P. and Marinho, P. (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. Methods Mol. Biol. 49, 39-48.
10. Gravot, A., Lieutaud, A., Verret, F., Auroy, P., Vavasseur, A. and Richaud, P. (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett. 561, 22-28.
11. Hambidge, K.M. and Krebs, N.F. (2007) Zinc deficiency: a special challenge. J. Nutr. 137, 1101-1105.
12. Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D. and Krämer, U. (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature, 453, 391-395.
13. 2+ and regulates ion transport. Proc. Natl Acad. Sci. USA, 98, 11749-11754.
14. Hershfinkel, M., Silverman, W.F. and Sekler, I. (2007) The zinc sensing receptor, a link between zinc and cell signaling. Mol. Med. 13, 331-336.
15. Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F. and Cobbett, C.S. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell, 16, 1327-1339.
16. Ishimaru, Y., Masuda, H., Bashir, K., Inoue, H., Tsukamoto, T., Takahashi, M., Nakanishi, H., Aoki, N., Hirose, T. and Ohsugi, R. (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J. 62, 379-390.
17. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
18. Kawahara, H., Chonan, N. and Matsuda, T. (1974) Studies on morphogenesis in rice plants, 7: the morphology of vascular bundles in the vegetative nodes of the culm. Proc. Crop Sci. Soc. Jpn, 43, 389-401.
19. Lane, T.W., Saito, M.A., George, G.N., Pickering, I.J., Prince, R.C. and Morel, F.M.M. (2005) Biochemistry: a cadmium enzyme from a marine diatom. Nature, 435, 42.
20. Liu, N., Zhang, F., Wang, X., Zhang, Z., Chai, Z., Huang, Y., He, W., Zhao, X., Zuo, A. and Yang, R. (2004) Element distribution in the brain sections of rats measured by synchrotron radiation X-ray fluorescence. Spectrochim. Acta Part B At. Spectrosc. 59, 255-260.
21. MacDonald, R.S. (2000) The role of zinc in growth and cell proliferation. J. Nutr. 130, 1500S-1508S.
22. Maret, W. (2001) Zinc biochemistry, physiology, and homeostasis-recent insights and current trends. Biometals, 14, 187-190.
23. Mills, R.F., Francini, A., Ferreira Da Rocha, P.S.C., Baccarini, P.J., Aylett, M., Krijger, G.C. and Williams, L.E. (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett. 579, 783-791.
24. Mills, R.F., Peaston, K.A., Runions, J. and Williams, L.E. (2012) HvHMA2, a P1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS One, 7, e42640.
25. Miyadate, H., Adachi, S., Hiraizumi, A., Tezuka, K., Nakazawa, N., Kawamoto, T., Katou, K., Kodama, I., Sakurai, K. and Takahashi, H. (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 189, 190-199.
26. Morel, M., Crouzet, J., Gravot, A., Auroy, P., Leonhardt, N., Vavasseur, A. and Richaud, P. (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol. 149, 894-904.
27. Nocito, F.F., Lancilli, C., Dendena, B., Lucchini, G. and Sacchi, G.A. (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ. 34, 994-1008.
28. Ogawa, I., Nakanishi, H., Mori, S. and Nishizawa, N.K. (2009) Time course analysis of gene regulation under cadmium stress in rice. Plant Soil, 325, 97-108.
29. Papoyan, A. and Kochian, L.V. (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 136, 3814-3823.
30. Rensing, C., Ghosh, M. and Rosen, B.P. (1999) Families of soft-metal-ion-transporting ATPases. J. Bacteriol. 181, 5891-5897.
31. Rogers, E.E., Eide, D.J. and Guerinot, M.L. (2000) Altered selectivity in an Arabidopsis metal transporter. Proc. Natl Acad. Sci. USA, 97, 12356-12360.
32. Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., Takahashi, H., Watanabe, A. and Akagi, H. (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 53, 213-224.
33. Scofield, G.N., Hirose, T., Aoki, N. and Furbank, R.T. (2007) Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J. Exp. Bot. 58, 3155-3169.
34. Sun, T., Zhang, Y. and Chai, T. (2011) Cloning, characterization, and expression of the BjEXPA1 gene and its promoter region from Brassica juncea L. Plant Growth Regul. 64, 39-51.
35. Suzuki, M. and Yagi, N. (1994) DNA recognition code of transcription factors in the helix-turn-helix, probe helix, hormone receptor, and zinc finger families. Proc. Natl Acad. Sci. USA, 91, 12357-12361.
36. Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizawa, N.K. and Nakanishi, H. (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ. 35, 1948-1957.
37. Tauris, B., Borg, S., Gregersen, P.L. and Holm, P.B. (2009) A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J. Exp. Bot. 60, 1333-1347.
38. Truong-Tran, A.Q., Carter, J., Ruffin, R.E. and Zalewski, P.D. (2001) The role of zinc in caspase activation and apoptotic cell death. Biometals, 14, 315-330.
39. Ueno, D., Yamaji, N., Kono, I., Huang, C.F., Ando, T., Yano, M. and Ma, J.F. (2010) Gene limiting cadmium accumulation in rice. Proc. Natl Acad. Sci. USA, 107, 16500-16505.
40. Ueno, D., Milner, M.J., Yamaji, N., Yokosho, K., Koyama, E., Clemencia Zambrano, M., Kaskie, M., Ebbs, S., Kochian, L.V. and Ma, J.F. (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J. 66, 852-862.
41. Verret, F., Gravot, A., Auroy, P., Leonhardt, N., David, P., Nussaume, L., Vavasseur, A. and Richaud, P. (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett. 576, 306-312.
42. Waters, B.M. and Sankaran, R.P. (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci. 180, 562-574.
43. WHO (World Health Organization). (2002) The World Health Report 2002: Reducing Risks, Promoting Healthy Life. Geneva, Switzerland: World Health Organization, pp. 1-230.
44. Wirth, J., Poletti, S., Aeschlimann, B., Yakandawala, N., Drosse, B., Osorio, S., Tohge, T., Fernie, A.R., Günther, D. and Gruissem, W. (2009) Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7, 631-644.
45. Wong, C.K.E., Jarvis, R.S., Sherson, S.M. and Cobbett, C.S. (2009) Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytol. 181, 79-88.
46. Yoshida, S., Forno, D., Cock, J. and Gomez, K. (1976) Routine procedure for growing rice plants in culture solution. In Laboratory Manual for Physiological Studies of Rice, pp. 61-66. Los Baños, Laguna, Philippines: The International Rice Research Institute (IRRI).
47. Zhang, Y., Song, Q., Yan, J., Tang, J., Zhao, R., He, Z., Zou, C. and Ortiz-Monasterio, I. (2010) Mineral element concentrations in grains of Chinese wheat cultivars. Euphytica, 174, 303-313.
48. Zhao, F.J. and McGrath, S.P. (2009) Biofortification and phytoremediation. Curr. Opin. Plant Biol. 12, 373-380.
49. 1B-ATPases appears to be structured according to the botanical families. C. R. Biol. 334, 863-871.