HMA1 and PAA1, two chloroplast-envelope PIB-ATPases, play distinct roles in chloroplast copper homeostasis

Journal of Experimental Botany

Volumn 65, Issue 6, 2014, Pages 1529-1540

  Boutigny, Sylvain ^a,b,c   Sautron, Emeline ^a,b,c   Finazzi, Giovanni ^a,b,c   Rivasseau, Corinne ^a,b,c   Frelet Barrand, Annie ^a,b,c   Pilon, Marinus ^d   Rolland, Norbert ^a,b,c   Seigneurin Berny, Daphné ^a,b,c  

^a Laboratoire de Physiologie Cellulaire Vegetale Grenoble   (France)

^b UNIV GRENOBLE ALPES   (France)

^c CEA GRENOBLE   (France)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Arabidopsis; Chloroplast; Copper; Envelope transporter; Metal homeostasis; PIB ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARABIDOPSIS PROTEIN; COPPER; HMA1 PROTEIN, ARABIDOPSIS; PAA1 PROTEIN, ARABIDOPSIS; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; ENVELOPE TRANSPORTER; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; METAL HOMEOSTASIS; MUTATION; PHENOTYPE; PHYSIOLOGY; PIB ATPASE.; PLANT LEAF; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; CHLOROPLAST; COPPER; ENVELOPE TRANSPORTER; METAL HOMEOSTASIS; PIB ATPASE.;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLAST PROTON-TRANSLOCATING ATPASES; COPPER; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; MUTATION; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; SEEDLING;

EID: 84897429414     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru020     Document Type: Article

References (43)

1. Abdel-Ghany SE. 2009. Contribution of plastocyanin isoforms to photosynthesis and Cu homeostasis in Arabidopsis thaliana grown at different Cu regimes. Planta 229, 767-779.
2. Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T. 2005. Two P-type ATPases are required for Cu delivery in Arabidopsis thaliana chloroplasts. The Plant Cell 17, 1233-1251.
3. Andrés-Colás N, Sancenon V, Rodriguez-Navarro S, Mayo S, Thiele DJ, Ecker JR, Puig S, Pe'arrubia L. 2006. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in Cu detoxification of roots. The Plant Journal 45, 225-236.
4. Arguëllo JM. 2003. Identification of ion-selectivity determinants in heavy metal transport P1B-ATPases. Journal of Membrane Biology 195, 93-108.
5. Bensmihen S, To A, Lambert G, Kroj T, Giraudat J, Parcy F. 2004. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Letters 561, 127-131.
6. Bruinsma J. 1961. A comment on the spectrophotometric determination of chlorophyll. Biochimica and Biophysica Acta 52, 576-578.
7. Burkhead JL, Abdel-Ghany SE, Morrill JM, Pilon-Smits EA, Pilon M. 2003. The Arabidopsis thaliana CUTA gene encodes an evolutionarily conserved Cu binding chloroplast protein. The Plant Journal 34, 856-867.
8. Burkhead JL, Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M. 2009. Cu homeostasis. New Phytologist 182, 799-816.
9. Catty P, Boutigny S, Miras R, Joyard J, Rolland N, Seigneurin- Berny D. 2011. Biochemical characterization of AtHMA6/PAA1, a chloroplast envelope Cu(I)-ATPase. Journal of Biological Chemistry 286, 36188-36197.
10. Chao DY, Silva A, Baxter I, Huang YS, Nordborg M, Danku J, Lahner B, Yakubova E, Salt DE. 2012. Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genetics 8, e1002923.
11. Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL. 2005. A Cu chaperone for superoxide dismutase that confers three types of Cu/ zinc superoxide dismutase activity in Arabidopsis. Plant Physiology 139, 425-436.
12. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
13. Cohu CM, Pilon M. 2007. Regulation of superoxide dismutase expression by copper availability. Physiologia Plantarum 129, 747-755.
14. Dugas DV and Bartel B. 2008. Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Molecular Biology 67, 403-417.
15. Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K. 2007. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. The Plant Cell 19, 986-1006.
16. Hänsch R, Mendel RR. 2009. Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology 12, 259-266.
17. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I and Millar AH. 2007. SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Research 35, 213-218.
18. Himelblau E, Mira H, Lin SJ, Culotta VC, Penarrubia L, Amasino RM. 1998. Identification of a functional homolog of the yeast Cu homeostasis gene ATX1 from Arabidopsis. Plant Physiology 117, 1227-1234.
19. Huang CH, Kuo WY, Weiss C, Jinn TL. 2012. Copper chaperonedependent and -independent activation of three copper-zinc superoxide dismutase homologs localized in different cellular compartments in Arabidopsis. Plant Physiology 158, 737-746.
20. 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. The Plant Cell 16, 1327-1339
21. Kim YY, Choi H, Segami S, Cho HT, Martinoia E, Maeshima M, Lee Y. 2009. AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. The Plant Journal 58, 737-753.
22. Kunst L. 1998. Preparation of physiologically active chloroplasts from Arabidopsis. In: Martinez-Zapater JM, Salinas J, eds, Methods in molecular biology: Arabidopsis Protocols. Totowa NJ: Humana Press, vol. 82, 43-48.
23. Lutsenko S, Gupta A, Burkhead JL, Zuzel V. 2008. Cellular multitasking: the dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance. Archives of Biochemistry and Biophysics 476, 22-32.
24. McCord JM. 1999. Analysis of superoxide dismutase activity. In: Maines MD, ed, Current protocols in toxicology. New York: Wiley, 7.3.1-7.3.9.
25. Mikkelsen MD, Pedas P, Schiller M, et al. 2012. Barley HvHMA1 is a heavy metal pump involved in mobilizing organellar Zn and Cu and plays a role in metal loading into grains. PLoS One 7, e49027.
26. 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. Journal of Biological Chemistry 283, 9633-9641.
27. Pilon M, Abdel-Ghany SE, Cohu CM, Gogolin KA, Ye H. 2006. Cu cofactor delivery in plant cells. Current Opinion in Plant Biology 9, 256-263.
28. Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L. 2007a. Cu and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. The Plant Cell Environment 30, 271-290.
29. Puig S, Mira H, Dorcey E, et al. 2007b. Higher plants possess two different types of ATX1-like Cu chaperones. Biochemical and Biophysical Research Communications 354, 385-390.
30. + transporting P(1B4)-ATPase of Mycobacterium smegmatis. Molecular Microbiology 84, 1139-1149.
31. Ravet K, Pilon M. 2013. Copper and iron homeostasis in plants: the challenges of oxidative stress. Antioxidants and Redox Signaling 19, 919-932.
32. Rosenzweig AC, Argüello JM. 2012. Toward a molecular understanding of metal transport by P(1B)-type ATPases. Current Topics in Membranes 69, 113-136.
33. Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L. 2004. The Arabidopsis Cu transporter COPT1 functions in root elongation and pollen development. Journal of Biological Chemistry 279, 15348-15355.
34. Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L. 2003. Identification of a Cu transporter family in Arabidopsis thaliana. Plant Molecular Biology 51, 577-587.
35. Scherer J, Nies DH. 2009. CzcP is a novel efflux system contributing to transition metal resistance in Cupriavidus metallidurans CH34. Molecular Microbiology 73, 601-621.
36. Seigneurin-Berny D, Gravot A, Auroy P, et al. 2006. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. Journal of Biological Chemistry 281, 2882-2892.
37. Seigneurin-Berny D, Salvi D, Dorne AJ, Joyard J and Rolland N. 2008. Percoll-purified and photosynthetically active chloroplasts from Arabidopsis thaliana leaves. Plant Physiology and Biochemistry 46, 951-955.
38. Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M. 2003. PAA1, a P-type ATPase of Arabidopsis, functions in Cu transport in chloroplasts. The Plant Cell 15, 1333-1346.
39. Tapken W, Ravet K, Pilon M. 2012. Plastocyanin controls the stabilization of the thylakoid Cu-transporting P-type ATPase PAA2/HMA8 in response to low Cu in Arabidopsis. Journal of Biological Chemistry 287, 18544-18550.
40. Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D. 2003. Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. Journal of Biological Chemistry 278, 31286-31289.
41. Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C. 2003. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. Journal of Biological Chemistry 278, 47644-47653.
42. Wintz H, Vulpe C. 2002. Plant Cu chaperones. Biochemical Society Transactions 30, 732-735.
43. Zhu C, Ding Y, Liu H. 2011. MiR398 and plant stress responses Physiologia Plantarum 143, 1-9.