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

Volumn 7, Issue 11, 2012, Pages

  Mikkelsen, Maria Dalgaard ^a,b   Pedas, Pai ^b   Schiller, Michaela ^b   Vincze, Eva ^c   Mills, Rebecca F ^d   Borg, Søren ^c   Møller, Annette ^a,b   Schjoerring, Jan K ^b   Williams, Lorraine E ^d   Baekgaard, Lone ^a,b   Holm, Preben Bach ^c   Palmgren, Michael G ^a,b  

^a DANISH NATIONAL RESEARCH FOUNDATION   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CADMIUM; CALCIUM; COBALT; COPPER; HEAVY METAL; IRON; MAGNESIUM; MANGANESE; PROTEIN HMA1; THAPSIGARGIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ZINC;

ALEURONE; ARABIDOPSIS; ARTICLE; BARLEY; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELLULAR DISTRIBUTION; CHEMOSENSITIVITY; CHLOROPLAST; CONTROLLED STUDY; DOWN REGULATION; ENZYME SPECIFICITY; FUNGAL STRAIN; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHYTOTOXICITY; PLANT CELL; PLANT LEAF; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE; ZINC DEFICIENCY;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; COPPER; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; HORDEUM; ZINC;

ARABIDOPSIS THALIANA; HORDEUM;

EID: 84869099802     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049027     Document Type: Article

References (69)

1. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A, (2007) Zinc in plants. New Phytol 173: 677-702.
2. Grusak M, Cakmak I (2005) Methods to improve the crop-delivery of minerals to humans and livestock. In: Plant Nutritional Genomics (Broadley MR, White PJ, Eds.), Blackwell, pp. 265-286.
3. Pilon M, Abdel-Ghany SE, Cohu CM, Gogolin KA, Ye H, (2006) Copper cofactor delivery in plant cells. Curr Opin Plant Biol 9: 256-263.
4. Welch RM, Graham RD, (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55: 353-364.
5. White PJ, Broadley MR, (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10: 586-593.
6. Andreini C, Banci L, Bertini I, Rosato A, (2006) Zinc through the three domains of life. J Proteome Res 5: 3173-3178.
7. Marschner H (1995) Mineral nutrition of higher plants. 2nd edn., Academic Press, London.
8. Berg JM, Shi Y, (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271: 1081-1085.
9. Rhodes D, Klug A, (1993) Zinc fingers. Sci Am 268: 56-59, 62-55.
10. Bowler C, Van Camp W, Van Montagu M, Inze D, (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13: 199-199.
11. Plesnicar M, Bendall DS, (1970) The plastocyanin content of chloroplasts from some higher plants estimated by a sensitive enzymatic assay. Biochim Biophys Acta 216: 192-199.
12. Maret W, Sandstead HH, (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Bio 20: 3-18.
13. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV, (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284: 805-808.
14. Yamasaki H, Pilon M, Shikanai T, (2008) How do plants respond to copper deficiency? Plant Signal Behav 3: 231-232.
15. Andrés-Colás N, Sancenón V, Rodríguez-Navarro S, Mayo S, Thiele DJ, et al. (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45: 225-36.
16. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, et al. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16: 1327-1339.
17. Palmgren MG, Clemens S, Williams LE, Kramer U, Borg S, et al. (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13: 464-473.
18. Brinch-Pedersen H, Borg S, Tauris B, Holm PB, (2007) Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J Cereal Sci 46: 308-326.
19. Hegelund JN, Pedas P, Husted S, Schiller M, Schjoerring JK, (2012) Zinc fluxes into developing barley grains: use of stable Zn isotopes to separate root uptake from remobilization in plants with contrasting Zn status. Plant Soil DOI: 10.1007/s11104-012-1272.
20. Uauy C, Brevis JC, Dubcovsky J, (2006) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57: 2785-2794.
21. Ozturk L, Yazici MA, Yucel C, Torun A, Cekic C, et al. (2006) Concentration and localization of zinc during seed development and germination in wheat. Physiol Plant 128: 144-152.
22. Mazzolini AP, Pallaghy CK, Legge GJF, (1985) Quantitative microanalysis of Mn, Zn and other elements in mature wheat seed. New Phytol 100: 483-509.
23. Lombi E, Smith E, Hansen TH, Paterson D, de Jonge MD, et al. (2011) Megapixel imaging of (micro)nutrients in mature barley grains. J Exp Bot 62: 273-282.
24. Patrick JW, Offler CE, (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52: 551-564.
25. Zhang WH, Zhou YC, Dibley KE, Tyerman SD, Furbank RT, et al. (2007) Nutrient loading of developing seeds. Funct Plant Biol 34: 314-331.
26. Axelsen KB, Palmgren MG, (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 461: 84-101.
27. Palmgren MG, Axelsen KB, (1998) Evolution of P-type ATPases. Biochim Biophys Acta 1365: 37-45.
28. Poulsen LR, Lopez-Marques RL, Palmgren MG, (2008) Flippases: still more questions than answers. Cell Mol Life Sci 65: 3119-3125.
29. Williams LE, Mills RF, (2005) P1B-ATPases- an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10: 491-502.
30. Arguello JM, Eren E, Gonzalez-Guerrero M, (2007) The structure and function of heavy metal transport P1B-ATPases. Biometals 20: 233-248.
31. Baekgaard L, Mikkelsen MD, Soerensen DM, Hegelund JN, Persson DP, et al. (2010) A combined Zn/Cd sensor and Zn/Cd export regulator in a heavy metal pump. J Biol Chem 285: 31243-31252.
32. Mana-Capelli S, Mandal AK, Arguello JM, (2003) Archaeoglobus fulgidus CopB is a thermophilic Cu2+-ATPase: functional role of its histidine-rich-N-terminal metal binding domain. J Biol Chem 278: 40534-40541.
33. Mandal AK, Arguello JM, (2003) Functional roles of metal binding domains of the Archaeoglobus fulgidus Cu+-ATPase CopA. Biochemistry 42: 11040-11047.
34. Verret F, Gravot A, Auroy P, Preveral S, Forestier C, et al. (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett 579: 1515-1522.
35. Mills RF, Valdes B, Duke M, Peaston KA, Lahner B, et al. (2010) Functional significance of AtHMA4 C-terminal domain in planta. PLoS ONE 5: e13388.
36. Axelsen KB, Palmgren MG, (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126: 696-706.
37. Wong CK, Jarvis RS, Sherson SM, Cobbett CS, (2009) Functional analysis of the heavy metal binding domains of the Zn/Cd-transporting ATPase, HMA2, in Arabidopsis thaliana. New Phytol 181: 79-88.
38. Mills RF, Kerry AP, Runions J, Williams LE, (2012) HvHMA2, a P1B-ATPase from Barley, Is Highly Conserved among Cereals and Functions in Zn and Cd Transport. PLoS ONE 7: e42640.
39. Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, et al. (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97: 383-393.
40. 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.
41. 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.
42. Shikanai T, Muller-Moule P, Munekage Y, Niyogi KK, Pilon M, (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15: 1333-1346.
43. Kim YY, Choi H, Segami S, Cho HT, Martinoia E, et al. (2009) AtHMA1 contributes to the detoxification of excess Zn(II) in Arabidopsis. Plant J 58: 737-753.
44. Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, et al. (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281: 2882-2892.
45. Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, et al. (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283: 9633-9641.
46. Higuchi M, Ozaki H, Matsui M, Sonoike K, (2009) A T-DNA insertion mutant of AtHMA1 gene encoding a Cu transporting ATPase in Arabidopsis thaliana has a defect in the water-water cycle of photosynthesis. J Photoch Photobio B 94: 205-213.
47. Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, et al. (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiololy 148: 455-466.
48. Regenberg B, Villalba JM, Lanfermeijer FC, Palmgren MG, (1995) C-terminal deletion analysis of plant plasma membrane H+-ATPase: yeast as a model system for solute transport across the plant plasma membrane. Plant Cell 7: 1655-1666.
49. Curtis M, Grossniklaus U, (2003) A Gateway cloning vector set for high-throughput functional analysis of genes in plants. Plant Physiology 133: 462-469.
50. Lange M, Vincze E, Møller MG, Holm PB, (2006) Molecular analysis of transgene and vector backbone integration into the barley genome following Agrobacterium-mediated transformation. Plant Cell Rep 25: 815-820.
51. Tingay S, McElroy D, Kalla R, Fieg S, Wang MB, et al. (1997) Agrobacterium tumefaciens-mediated barley transformation. Plant J 11: 1369-1376.
52. Matthews PR, Wang M-B, Waterhouse PM, Thornton S, Fieg SJ, et al. (2001) Marker gene elimination from transgenic barley, using co-transformation with adjacent 'twin T-DNAs' on a standard Agrobacterium transformation vector. Mol Breeding 73: 195-202.
53. Carciofi M, Shaik SS, Jensen SL, Blennow PGA, Svensson JT, et al. (2011) Hyperphosphorylation of cereal starch. J Cereal Sci 54: 339-346.
54. Lazo GR, Stein PA, Ludwig RA, (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology 9: 963-967.
55. Pedas P, Hebbern CA, Schjoerring JK, Holm PB, Husted S, (2005) Differential capacity for high-affinity manganese uptake contributes to differences between barley genotypes in tolerance to low manganese availability. Plant Physiol 139: 1411-1420.
56. Murashige T, Skoog F, (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15: 473-497.
57. Mills RF, Doherty ML, Lopez-Marques RL, Weimar T, Dupree P, et al. (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol 146: 116-128.
58. Tauris B, Borg S, Gregersen PL, Holm PB, (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.
59. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
60. Veierskov B, Ferguson IB, (1991) Conjugation of ubiquitin to proteins from green plant tissues. Plant Physiol 96: 4-9.
61. Hansen TH, Laursen KH, Persson DP, Pedas P, Husted S, et al. (2009) Micro-scaled high-throughput digestion of plant tissue samples for multi-elemental analysis. Plant Methods 5DOI: 10.1186/1746-4811-5-12.
62. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
63. Moran R, (1982) Formulae for determination of chlorophyllous pigments extracted with n,n-dimethylformamide. Plant Physiol 69: 1376-1381.
64. Toyoshima C, Nakasako M, Nomura H, Ogawa H, (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2 6 A resolution. Nature 405: 647-655.
65. Zhang Z, Sumbilla C, Lewis D, Inesi G, (1993) High sensitivity to site directed mutagenesis of the peptide segment connecting phosphorylation and Ca2+ binding domains in the Ca2+ transport ATPase. FEBS Lett 335: 261-264.
66. Zhong L, Inesi G, (1998) Role of the S3 stalk segment in the thapsigargin concentration dependence of sarco-endoplasmic reticulum Ca2+ ATPase inhibition. J Biol Chem 273: 12994-12998.
67. Eren E, Kennedy DC, Maroney MJ, Arguello JM, (2006) A novel regulatory metal binding domain is present in the C terminus of Arabidopsis Zn2+-ATPase HMA2. J Biol Chem 281: 33881-33891.
68. Bechtel DB, Gaines RL, Pomeranz Y, (1982) Early stages in wheat endosperm formation and protein body initiation. Ann Bot 50: 507-518.
69. Treiman M, Caspersen C, Christensen SB, (1998) A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca2+-ATPases. Trends Pharmacol Sci 19: 131-135.