HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana

New Phytologist

Volumn 181, Issue 1, 2009, Pages 71-78

  Wong, Chong Kum Edwin ^a   Cobbett, Christopher S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

cad1; HMA2; HMA4; Phytochelatins; Root to shoot Cd translocation; Zn Cd ATPases

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARABIDOPSIS PROTEIN; CADMIUM; HMA2 PROTEIN, ARABIDOPSIS; HMA4 PROTEIN, ARABIDOPSIS; PHYTOCHELATIN;

ANGIOSPERM; CADMIUM; DETOXIFICATION; ENZYME ACTIVITY; ROOT; SEQUESTRATION (CHEMISTRY); SHOOT; TRANSLOCATION; ZINC;

ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENETICS; GENOTYPE; METABOLISM; PHYSIOLOGY; PLANT; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CADMIUM; GENOTYPE; PHYTOCHELATINS; PLANT ROOTS; PLANT SHOOTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 57449106181     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02638.x     Document Type: Article

References (31)

1. Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T. 2005. Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17 : 1233 1251.
2. Andres-Colas N, Sancenon V, Rodriguez-Navarro S, Mayo S, Thiele DJ, Ecker JR, Puig S, Penarrubia L. 2006. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant Journal 45 : 225 236.
3. Arrivault S, Senger T, Kramer U. 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant Journal 46 : 861 879.
4. Chen A, Komives EA, Schroeder JI. 2006. An improved grafting technique for mature arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiology 141 : 108 120.
5. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N. 2007. A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology 144 : 1052 1065.
6. Desbrosses-Fonrouge A-G, Voigt K, Schroder A, Arrivault S, Thomine S, Kramer U. 2005. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Letters 579 : 4165.
7. 2+ homeostasis. Plant Physiology 136 : 3712 3723.
8. Gong JM, Lee DA, Schroeder JI. 2003. Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proceedings of the National Academy of Sciences, USA 100 : 10118 10123.
9. Grotz N, Guerinot ML. 2006. Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta 1763 : 595 608.
10. Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O'Connell MJ, Goldsbrough PB, Cobbett CS. 1999. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11 : 1153 1164.
11. Hall JL, Williams LE. 2003. Transition metal transporters in plants. Journal of Experimental Botany 54 : 2601 2613.
12. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U. 2008. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453 : 391 395.
13. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR. 1999. RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97 : 383 393.
14. Howden R, Cobbett CS. 1992. Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiology 100 : 100 107.
15. Howden R, Goldsbrough PB, Andersen CR, Cobbett CS. 1995. Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiology 107 : 1059 1066.
16. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS. 2004. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 : 1327 1339.
17. Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M. 2004. Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant and Cell Physiology 45 : 1749 1758.
18. Larsson EH, Asp H, Bornman JF. 2002. Influence of prior Cd(2+) exposure on the uptake of Cd(2+) and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana. Journal of Experimental Botany 53 : 447 453.
19. Mendoza-Cozatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI. 2008. Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant Journal 54 : 249 259.
20. Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE. 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 Letters 579 : 783 791.
21. Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE. 2003. Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant Journal 35 : 164 176.
22. Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR. 2008. AtHMA1 is a thapsigargin sensitive Ca2+/heavy metal pump. The Journal of Biological Chemistry 283 : 9633 9641.
23. Rensing C, Fan B, Sharma R, Mitra B, Rosen BP. 2000. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proceedings of the National Academy of Sciences, USA 97 : 652 656.
24. Rensing C, Sun Y, Mitra B, Rosen BP. 1998. Pb(II)-translocating P-type ATPases. The Journal of Biological Chemistry 273 : 32614 32617.
25. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J et al. 2006. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. The Journal of Biological Chemistry 281 : 2882 2892.
26. 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. Proceedings of the National Academy of Sciences, USA 97 : 4991 4996.
27. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P. 2004. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Letters 576 : 306 312.
28. Verret F, Gravot A, Auroy P, Preveral S, Forestier C, Vavasseur A, Richaud P. 2005. Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Letters 579 : 1515 1522.
29. Voskoboinik I, Mar J, Strausak D, Camakaris J. 2001. The regulation of catalytic activity of the menkes copper-translocating P-type ATPase. Role of high affinity copper-binding sites. The Journal of Biological Chemistry 276 : 28620 28627.
30. Williams LE, Pittman JK, Hall JL. 2000. Emerging mechanisms for heavy metal transport in plants. Biochimica et Biophysica Acta 1465 : 104 126.
31. Woeste KE, Kieber JJ. 2000. A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12 : 443 455.