AhNRAMP1 iron transporter is involved in iron acquisition in peanut

Journal of Experimental Botany

Volumn 63, Issue 12, 2012, Pages 4437-4446

  Xiong, Hongchun ^a   Kobayashi, Takanori ^b,c   Kakei, Yusuke ^b   Senoura, Takeshi ^b   Nakazono, Mikio ^b,d   Takahashi, Hirokazu ^b,d   Nakanishi, Hiromi ^b   Shen, Hongyun ^a   Duan, Penggen ^a   Guo, Xiaotong ^a   Nishizawa, Naoko K ^b,c   Zuo, Yuanmei ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF TOKYO   (Japan)

^c ISHIKAWA PREFECTURAL UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

AhNRAMP1; Intercropping; Iron acquisition; Peanut; Tobacco; Transporter

Indexed keywords

CATION TRANSPORT PROTEIN; IRON; MEMBRANE PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; NATURAL RESISTANCE-ASSOCIATED MACROPHAGE PROTEIN 1; VEGETABLE PROTEIN;

ARTICLE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; MAIZE; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PEANUT; PHYLOGENY; PHYSIOLOGY; PLANT EPIDERMIS; PLANT LEAF; PLANT ROOT; PRENATAL DEVELOPMENT; SACCHAROMYCES CEREVISIAE; SEEDLING; TOBACCO; TRANSGENIC PLANT;

ARACHIS HYPOGAEA; BASE SEQUENCE; CATION TRANSPORT PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; IRON; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLANT EPIDERMIS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SACCHAROMYCES CEREVISIAE; SEEDLING; SEQUENCE ANALYSIS, DNA; TOBACCO; ZEA MAYS;

ARACHIS HYPOGAEA; NICOTIANA TABACUM;

EID: 84866655386     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers117     Document Type: Article

References (60)

1. Belouchi A, Kwan T, Gros P. 1997. Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Molecular Biology 33, 1085-1092.
2. Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P. 2003. Differential regulation of nramp and irt metal transporter genes in wild type and iron uptake mutants of tomato. Journal of Biological Chemistry 278, 24697-24704.
3. Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C. 2009. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochemical Journal 422, 217-228.
4. Cailliatte R, Schikora A, Briat JF, Mari S, Curie C. 2010. Highaffinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. The Plant Cell 22, 904-917.
5. 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. The Plant Cell 14, 1347-1357.
6. 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.
7. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL. 2001. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346-349.
8. Diatchenko L, Lau YF, Campbell AP, et al. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences, USA 93, 6025-6030.
9. Ding H, Duan L, Li J, Yan H, Zhao M, Zhang F, Li WX. 2010. Cloning and functional analysis of the peanut iron transporter AhIRT1 during iron deficiency stress and intercropping with maize. Journal of Plant Physiology 167, 996-1002.
10. Ding H, Duan L, Wu H, Yang R, Ling H, Li WX, Zhang F. 2009. Regulation of AhFRO1, an Fe(III)-chelate reductase of peanut, during iron deficiency stress and intercropping with maize. Physiologia Plantarum 136, 274-283.
11. Dix DR, Bridgham JT, Broderius MA, Byersdorfer CA, Eide DJ. 1994. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. Journal of Biological Chemistry 269, 26092-26099.
12. Eide D, Broderius M, Fett J, Guerinot ML. 1996. A novel ironregulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences, USA 93, 5624-5628.
13. Fleming MD, Romano MA, Su MA, Garrick LM, Garrick MD, Andrews NC. 1998. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proceedings of the National Academy of Sciences, USA 95, 1148-1153.
14. Fleming MD, Trenor CC, Su MA, Foernzler D, Beier DR, Dietrich WF, Andrews NC. 1997. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nature Genetics 16, 383-386.
15. Gietz RD, Schiestl RH. 1995. Transforming yeast with DNA. Methods in Molecular and Cellular Biology 5, 255-269.
16. Guerinot ML, Yi Y. 1994. Iron: nutritious, noxious, and not readily available. Plant Physiology 104, 815-820.
17. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA. 1997. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488.
18. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95-98.
19. Helmer G, Casadaban M, Bevan M, Kayes L, Chilton MD. 1984. A new chimeric gene as a marker for plant transformation: the expression of Escherichia coli [beta]-galactosidase in sunflower and tobacco cells. Nature Biotechnology 2, 520-527.
20. Hiei Y, Ohta S, Komari T, Kumashiro T. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271-282.
21. Inal A, Gunes A, Zhang F, Cakmak I. 2007. Peanut/maize intercropping induced changes in rhizosphere and nutrient concentrations in shoots. Plant Physiology and Biochemistry 45, 350-356.
22. Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK. 2009. Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. Journal of Biological Chemistry 284, 3470-3479.
23. Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2005. OsZIP4, a novel zinc-regulated zinc transporter in rice. Journal of Experimental Botany 56, 3207-3214.
24. Ishimaru Y, Suzuki M, Tsukamoto T, et al. 2006. Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. The Plant Journal 45, 335-346.
25. Ishimaru Y, Takahashi R, Bashir K, et al. 2012. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Scientific Reports 2, 286.
26. Kaiser BN, Moreau S, Castelli J, Thomson R, Lambert A, Bogliolo S, Puppo A, Day DA. 2003. The soybean NRAMP homologue, GmDMT1, is a symbiotic divalent metal transporter capable of ferrous iron transport. The Plant Journal 35, 295-304.
27. Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK. 2003. Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants. The Plant Journal 36, 780-793.
28. Kobayashi T, Nakayama Y, Takahashi M, Inoue H, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK. 2004. Construction of artificial promoters highly responsive to iron deficiency. Soil Science and Plant Nutrition 50, 1167-1175.
29. Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB. 1999. The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Molecular Biology 40, 37-44.
30. Lanquar V, Lelievre F, Bolte S, et al. 2005. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. The EMBO Journal 24, 4041-4051.
31. Lanquar V, Ramos MS, Lelièvre F, Barbier-Brygoo H, Krieger- Liszkay A, Krämer U, Thomine S. 2010. Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiology 152, 1986-1999.
32. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G. 2009. Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiology 150, 786-800.
33. Luo M, Dang P, Bausher MG, Holbrook CC, Lee RD, Lynch RE, Guo BZ. 2005. Identification of transcripts involved in resistance responses to leaf spot disease caused by Cercosporidium personatum in peanut (Arachis hypogaea). Phytopathology 95, 381-387.
34. Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF. 2000. Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Molecular Microbiology 35, 1065-1078.
35. Mizuno D, Higuchi K, Sakamoto T, Nakanishi H, Mori S, Nishizawa NK. 2003. Three nicotianamine synthase genes isolated from maize are differentially regulated by iron nutritional status. Plant Physiology 132, 1989-1997.
36. Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H. 2005. Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiology and Biochemistry 43, 793-801.
37. Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T. 2006. A specific transporter for iron(III)-phytosiderophore in barley roots. The Plant Journal 46, 563-572.
38. Nevo Y, Nelson N. 2006. The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta 1763, 609-620.
39. Oomen RJFJ, Wu J, Lelièvre F, Blanchet S, Richaud P, Barbier- Brygoo H, Aarts MGM, Thomine S. 2009. Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytologist 181, 637-650.
40. Portnoy ME, Liu XF, Culotta VC. 2000. Saccharomyces cerevisiae expresses three functionally distinct homologues of the Nramp family of metal transporters. Molecular and Cellular Biology 20, 7893-7902.
41. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397, 694-697.
42. 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.
43. Römheld V, Marschner H. 1986. Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiology 80, 175-180.
44. Schaaf G, Schikora A, Häberle J, Vert G, Ludewig U, Briat JF, Curie C, von Wiré n N. 2005. A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant and Cell Physiology 46, 762-774.
45. Takagi S. 1976. Naturally occurring iron-chelating compounds in oatand rice-root washing. I. Activity measurement and preliminary characterization. Soil Science and Plant Nutrition 22, 423-433.
46. Takahashi H, Kamakura H, Sato Y, Shiono K, Abiko T, Tsutsumi N, Nagamura Y, Nishizawa N, Nakazono M. 2010. A method for obtaining high quality RNA from paraffin sections of plant tissues by laser microdissection. Journal of Plant Research 123, 807-813.
47. Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK. 2011. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. Journal of Experimental Botany. 62, 4843-4850.
48. Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier- Brygoo H. 2003. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. The Plant Journal 34, 685-695.
49. 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.
50. Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T. 2011. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proceedings of the National Academy of Sciences, USA 108, 20959-20964.
51. Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D. 2002. The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. The Plant Journal 31, 589-599.
52. Vert G, Grotz N, Dédaldéchamp 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. The Plant Cell 14, 1223-1233.
53. Wei W, Chai T, Zhang Y, Han L, Xu J, Guan Z. 2009. The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport. Molecular Biotechnology 41, 15-21.
54. Williams LE, Pittman JK, Hall JL. 2000. Emerging mechanisms for heavy metal transport in plants. Biochimica et Biophysica Acta 1465, 104-126.
55. Xia J, Yamaji N, Kasai T, Ma JF. 2010. Plasma membrane-localized transporter for aluminum in rice. Proceedings of the National Academy of Sciences, USA 107, 18381-18385.
56. Xiao H, Yin L, Xu X, Li T, Han Z. 2008. The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Annals of Botany 102, 881-889.
57. Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F. 2006. Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Reports 25, 365-373.
58. Zuo Y, Zhang F. 2008. Effect of peanut mixed cropping with gramineous species on micronutrient concentrations and iron chlorosis of peanut plants grown in a calcareous soil. Plant and Soil 306, 23-36.
59. Zuo Y, Zhang F. 2009. Iron and zinc biofortification strategies in dicot plants by intercropping with gramineous species. A review. Agronomy for Sustainable Development 29, 63-71.
60. Zuo Y, Zhang F, Li X, Cao Y. 2000. Studies on the improvement in iron nutrition of peanut by intercropping with maize on a calcareous soil. Plant and Soil 220, 13-25.