Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana - the role in zinc tolerance

New Phytologist

Volumn 190, Issue 1, 2011, Pages 125-137

  Shanmugam, Varanavasiappan ^a,b   Lo, Jing Chi ^a,c   Wu, Chia Lin ^a   Wang, Shan Li ^b   Lai, Chong Cheong ^a   Connolly, Erin L ^d   Huang, Jing Ling ^a   Yeh, Kuo Chen ^a,b  

^a AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Arabidopsis halleri; Hyperaccumulator; Iron homeostasis; IRT1; Zinc tolerance

Indexed keywords

ENZYME ACTIVITY; GENE EXPRESSION; HERB; HOMEOSTASIS; HYPERACCUMULATION; IRON; PHENOTYPE; SHOOT; SOIL TYPE; SPECIES DIVERSITY; TOLERANCE; TOXICITY; ZINC;

ARABIDOPSIS; ARABIDOPSIS HALLERI; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CARRIER PROTEIN; CATION TRANSPORT PROTEIN; FERRIC CITRATE IRON REDUCTASE; FIT1 PROTEIN, ARABIDOPSIS; FLAVINE MONONUCLEOTIDE REDUCTASE; IRON; IRT1 PROTEIN, ARABIDOPSIS; IRT2 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN; ZINC;

ADAPTATION; ARABIDOPSIS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PLANT; PLANT GENE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOXICITY;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CATION TRANSPORT PROTEINS; FMN REDUCTASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; IRON; MEMBRANE TRANSPORT PROTEINS; PLANT PROTEINS; PLANT ROOTS; PLANT SHOOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL; ZINC;

EID: 79951997891     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03606.x     Document Type: Article

References (67)

1. Allison JD, Brown DS, Novo-Gradac KJ. 1991. n 3.0 user's manual. Washington, DC: United States Environmental Protection Agency, EPA/600/3-91/021.
2. Assuncao AG, Herrero E, Lin YF, Huettel B, Talukdar S, Smaczniak C, Immink RG, van Eldik M, Fiers M, Schat H. 2010. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proceedings of the National Academy of Sciences, USA 107: 10296-10301.
3. Baker AJM, Brooks RR. 1989. Terrestrial higher plants which hyperaccumulate metallic elements - a review of their distribution, ecology and phytochemistry. Biorecovery 1: 81-126.
4. Barabasz A, Kramer U, Hanikenne M, Rudzka J, Antosiewicz DM. 2010. Metal accumulation in tobacco expressing Arabidopsis halleri metal hyperaccumulation gene depends on external supply. Journal of Experimental Botany 61: 3057-3067.
5. Bauer P, Ling HQ, Guerinot ML. 2007. FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis. Plant Physiology and Biochemistry 45: 260-261.
6. Becher M, Talke IN, Krall L, Kramer U. 2004. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant Journal 37: 251-268.
7. Bert V, Bonnin I, Saumitou-Laprade P, de Laguerie P, Petit D. 2002. Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytologist 155: 47-57.
8. Bert V, Macnair MR, de Laguerie P, Saumitou-Laprade P, Petit D. 2000. Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytologist 146: 225-233.
9. Briat JF, Lebrun M. 1999. Plant responses to metal toxicity. Comptes Rendus de l'Academie des Sciences. Serie III, Sciences de la Vie 322: 43-54.
10. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A. 2007. Zinc in plants. New Phytologist 173: 677-702.
11. Cailliatte R, Schikora A, Briat JF, Mari S, Curie C. 2010. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22: 904-917.
12. Cakmak I. 2002. Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant and Soil 247: 3-24.
13. Chaney RL. 1993. Zinc phytotoxicity. In: Robson AD, ed. Zinc in soil and plants. Dordrecht, the Netherlands: Kluwer Academic Publishers, 135-150.
14. Chiang HC, Lo JC, Yeh KC. 2006. Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environmental Science and Technology 40: 6792-6798.
15. Clemens S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719.
16. Colangelo EP, Guerinot ML. 2004. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400-3412.
17. Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML. 2003. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiology 133: 1102-1110.
18. Connolly EL, Fett JP, Guerinot ML. 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14: 1347-1357.
19. Connolly EL, Guerinot M. 2002. Iron stress in plants. Genome Biology 3: Reviews 1024.1-1024.4.
20. Cosio C, Martinoia E, Keller C. 2004. Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology 134: 716-725.
21. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF. 2000. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochemical Journal 347: 749-755.
22. Curie C, Briat JF. 2003. Iron transport and signaling in plants. Annual Review of Plant Biology 54: 183-206.
23. Desbrosses-Fonrouge AG, 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: 4165-4174.
24. Eide D, Broderius M, Fett J, Guerinot ML. 1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences, USA 93: 5624-5628.
25. Ernst WHO. 1974. Schwermetallvegetation der Erde. Stuttgart: G. Fischer Verlag.
26. Ghasemi R, Ghaderian SM, Kramer U. 2009. Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytologist 184: 566-580.
27. Guerinot ML, Eide D. 1999. Zeroing in on zinc uptake in yeast and plants. Current Opinion in Plant Biology 2: 244-249.
28. Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, Salt DE. 2009. MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant Journal 57: 1116-1127.
29. 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.
30. Haydon MJ, Cobbett CS. 2007. A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiology 143: 1705-1719.
31. Hell R, Stephan UW. 2003. Iron uptake, trafficking and homeostasis in plants. Planta 216: 541-551.
32. 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.
33. Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL. 2008. Iron-induced turnover of the Arabidopsis IRON-REGULATED TRANSPORTER1 metal transporter requires lysine residues. Plant Physiology 146: 1964-1973.
34. Kim SA, Guerinot ML. 2007. Mining iron: iron uptake and transport in plants. FEBS Letters 581: 2273-2280.
35. 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.
36. Kramer U. 2010. Metal hyperaccumulation in plants. Annual Review of Plant Biology 61: 517-534.
37. Kubota H, Takenaka C. 2003. Arabis gemmifera is a hyperaccumulator of Cd and Zn. International Journal of Phytoremediation 5: 197-201.
38. Kupper H, Lombi E, Zhao FJ, McGrath SP. 2000. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212: 75-84.
39. Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC, Wu JF, Huang JL, Yeh KC. 2009. Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytologist 182: 392-404.
40. Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. London, UK: Academic Press.
41. Mills RF, Valdes B, Duke M, Peaston KA, Lahner B, Salt DE, Williams LE. 2010. Functional significance of AtHMA4 C-terminal domain in planta. PLoS ONE 5: e13388.
42. Mirouze M, Sels J, Richard O, Czernic P, Loubet S, Jacquier A, Francois IE, Cammue BP, Lebrun M, Berthomieu P et al. 2006. A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant Journal 47: 329-342.
43. van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver Loren van Themaat E, Koornneef M, Aarts MG. 2006. Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 142: 1127-1147.
44. Oomen RJ, Wu J, Lelievre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MG, Thomine S. 2009. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytologist 181: 637-650.
45. Ramesh SA, Choimes S, Schachtman DP. 2004. Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Molecular Biology 54: 373-385.
46. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694-697.
47. Rogers EE, Eide DJ, Guerinot ML. 2000. Altered selectivity in an Arabidopsis metal transporter. Proceedings of the National Academy of Sciences, USA 97: 12356-12360.
48. Schmidt W. 2003. Iron solutions: acquisition strategies and signaling pathways in plants. Trends in Plant Science 8: 188-193.
49. Shahzad Z, Gosti F, Frerot H, Lacombe E, Roosens N, Saumitou-Laprade P, Berthomieu P. 2010. The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genetics 6: e1000911.
50. Talke IN, Hanikenne M, Kramer U. 2006. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology 142: 148-167.
51. Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S. 2009. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiology 149: 938-948.
52. Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H. 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant Journal 34: 685-695.
53. 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.
54. Van Wuytswinkel O, Vansuyt G, Grignon N, Fourcroy P, Briat JF. 1999. Iron homeostasis alteration in transgenic tobacco overexpressing ferritin. Plant Journal 17: 93-97.
55. Verbruggen N, Hermans C, Schat H. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181: 759-776.
56. 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.
57. Vert G, Barberon M, Zelazny E, Seguela M, Briat JF, Curie C. 2009. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229: 1171-1179.
58. Vert G, Briat JF, Curie C. 2001. Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant Journal 26: 181-189.
59. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223-1233.
60. Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S. 2004. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant Journal 37: 269-281.
61. 2 progeny grown on cadmium-contaminated soil. New Phytologist 187: 368-379.
62. Yang TJ, Lin WD, Schmidt W. 2010. Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiology 152: 2130-2141.
63. Yi Y, Guerinot ML. 1996. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant Journal 10: 835-844.
64. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ. 2008. FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Research 18: 385-397.
65. van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JA, Hooykaas PJ. 1999. Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiology 119: 1047-1055.
66. Zhao FJ, Jiang RF, Dunham SJ, McGrath SP. 2006. Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytologist 172: 646-654.
67. Zhao FJ, Lombi E, Breedon T, McGrath SP. 2000. Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant, Cell & Environment 23: 507-514.