|
Nicotianamine Chelates Both FeIII and
FeII. Implications for Metal Transport in
Plants1
Nicolaus von Wirén2,
Sukhbinder Klair,
Suhkibar Bansal,
Jean-Francois Briat,
Hicham Khodr,
Takayuki Shioiri,
Roger A. Leigh*, and
Robert C. Hider
Department of Pharmacy, King's College London, Manresa Road,
London SW3 6LX, United Kingdom (N.v.W., S.K., S.B., H.K., R.C.H.); Laboratoire de Biochimie et Physiologie Moléculaire des Plantes,
Institut National de la Recherche Agronomique, Place Viala, F-34060
Montpellier, France (J.-F.B.); Faculty of Pharmaceutical Sciences,
Nagoya City University, Tanabe-dori, Mizuho-ku, Nagoya 467, Japan
(T.S.); and Biochemistry and Physiology Department, IACR-Rothamsted,
Harpenden, Hertfordshire AL5 2JQ, United Kingdom (R.A.L.)
Nicotianamine
(NA) occurs in all plants and chelates metal cations, including
FeII, but reportedly not FeIII. However, a
comparison of the FeII and ZnII affinity
constants of NA and various FeIII-chelating
aminocarboxylates suggested that NA should chelate FeIII.
High-voltage electrophoresis of the FeNA complex formed in the presence
of FeIII showed that the complex had a net charge of 0, consistent with the hexadentate chelation of FeIII.
Measurement of the affinity constant for FeIII yielded a
value of 1020.6, which is greater than that for the
association of NA with FeII (1012.8). However,
capillary electrophoresis showed that in the presence of
FeII and FeIII, NA preferentially chelates
FeII, indicating that the FeIINA complex is
kinetically stable under aerobic conditions. Furthermore, Fe complexes
of NA are relatively poor Fenton reagents, as measured by their ability
to mediate H2O2-dependent oxidation of
deoxyribose. This suggests that NA will have an important role in
scavenging Fe and protecting the cell from oxidative damage. The pH
dependence of metal ion chelation by NA and a typical phytosiderophore,
2 -deoxymugineic acid, indicated that although both have the ability to
chelate Fe, when both are present, 2 -deoxymugineic acid dominates the chelation process at acidic pH values, whereas NA dominates at alkaline
pH values. The consequences for the role of NA in the long-distance
transport of metals in the xylem and phloem are discussed.
1
The work was supported by a grant from the
Biotechnology and Biological Sciences Research Council (BBSRC) of the
United Kingdom and by a short-term fellowship to N.v.W. from the joint
BBSRC/Institut National de la Recherche Agronomique collaboration
scheme. IACR is grant-aided by the BBSRC.
2
Present address: Institut für Allgemeine
Botanik, Universität Tübingen, Morgenstelle 1, D-72076
Tübingen, Germany.
*
Corresponding author; e-mail RL225{at}cam.ac.uk; fax 44-1223-333953.
Copies of the computer program mentioned in the paper are available
from R.C.H. or H.K.
Plant Physiol. (1999) 119: 1107-1114
Copyright Clearance Center: 0032-0889/99/119//08
© 1999 American Society of Plant Physiologists
This article has been cited by other articles:

|
 |

|
 |
 
Y. Kakei, I. Yamaguchi, T. Kobayashi, M. Takahashi, H. Nakanishi, T. Yamakawa, and N. K. Nishizawa
A Highly Sensitive, Quick and Simple Quantification Method for Nicotianamine and 2'-Deoxymugineic Acid from Minimum Samples Using LC/ESI-TOF-MS Achieves Functional Analysis of These Components in Plants
Plant Cell Physiol.,
November 1, 2009;
50(11):
1988 - 1993.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Conte, D. Stevenson, I. Furner, and A. Lloyd
Multiple Antibiotic Resistance in Arabidopsis Is Conferred by Mutations in a Chloroplast-Localized Transport Protein
Plant Physiology,
October 1, 2009;
151(2):
559 - 573.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Mijovilovich, B. Leitenmaier, W. Meyer-Klaucke, P. M.H. Kroneck, B. Gotz, and H. Kupper
Complexation and Toxicity of Copper in Higher Plants. II. Different Mechanisms for Copper versus Cadmium Detoxification in the Copper-Sensitive Cadmium/Zinc Hyperaccumulator Thlaspi caerulescens (Ganges Ecotype)
Plant Physiology,
October 1, 2009;
151(2):
715 - 731.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Dreyfus, D. Lemaire, S. Mari, D. Pignol, and P. Arnoux
Crystallographic snapshots of iterative substrate translocations during nicotianamine synthesis in archaea
PNAS,
September 22, 2009;
106(38):
16180 - 16184.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ravet, B. Touraine, S. A. Kim, F. Cellier, S. Thomine, M. L. Guerinot, J.-F. Briat, and F. Gaymard
Post-Translational Regulation of AtFER2 Ferritin in Response to Intracellular Iron Trafficking during Fruit Development in Arabidopsis
Mol Plant,
September 1, 2009;
2(5):
1095 - 1106.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Lee, J. C. Chiecko, S. A. Kim, E. L. Walker, Y. Lee, M. L. Guerinot, and G. An
Disruption of OsYSL15 Leads to Iron Inefficiency in Rice Plants
Plant Physiology,
June 1, 2009;
150(2):
786 - 800.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Klatte, M. Schuler, M. Wirtz, C. Fink-Straube, R. Hell, and P. Bauer
The Analysis of Arabidopsis Nicotianamine Synthase Mutants Reveals Functions for Nicotianamine in Seed Iron Loading and Iron Deficiency Responses
Plant Physiology,
May 1, 2009;
150(1):
257 - 271.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cassin, S. Mari, C. Curie, J.-F. Briat, and P. Czernic
Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine
J. Exp. Bot.,
March 1, 2009;
60(4):
1249 - 1259.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Inoue, T. Kobayashi, T. Nozoye, M. Takahashi, Y. Kakei, K. Suzuki, M. Nakazono, H. Nakanishi, S. Mori, and N. K. Nishizawa
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
J. Biol. Chem.,
February 6, 2009;
284(6):
3470 - 3479.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Curie, G. Cassin, D. Couch, F. Divol, K. Higuchi, M. Le Jean, J. Misson, A. Schikora, P. Czernic, and S. Mari
Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters
Ann. Bot.,
January 1, 2009;
103(1):
1 - 11.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. Vasconcelos, G. W. Li, M. A. Lubkowitz, and M. A. Grusak
Characterization of the PT Clade of Oligopeptide Transporters in Rice
The Plant Genome,
November 1, 2008;
1(2):
77 - 88.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Cheng, F. Wang, H. Shou, F. Huang, L. Zheng, F. He, J. Li, F.-J. Zhao, D. Ueno, J. F. Ma, et al.
Mutation in Nicotianamine Aminotransferase Stimulated the Fe(II) Acquisition System and Led to Iron Accumulation in Rice
Plant Physiology,
December 1, 2007;
145(4):
1647 - 1657.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. N. Talke, M. Hanikenne, and U. Kramer
Zinc-Dependent Global Transcriptional Control, Transcriptional Deregulation, and Higher Gene Copy Number for Genes in Metal Homeostasis of the Hyperaccumulator Arabidopsis halleri
Plant Physiology,
September 1, 2006;
142(1):
148 - 167.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kim, M. Takahashi, K. Higuchi, K. Tsunoda, H. Nakanishi, E. Yoshimura, S. Mori, and N. K. Nishizawa
Increased Nicotianamine Biosynthesis Confers Enhanced Tolerance of High Levels of Metals, in Particular Nickel, to Plants
Plant Cell Physiol.,
November 1, 2005;
46(11):
1809 - 1818.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schaaf, A. Schikora, J. Haberle, G. Vert, U. Ludewig, J.-F. Briat, C. Curie, and N. von Wiren
A Putative Function for the Arabidopsis Fe-Phytosiderophore Transporter Homolog AtYSL2 in Fe and Zn Homeostasis
Plant Cell Physiol.,
May 1, 2005;
46(5):
762 - 774.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. S. Green and E. E. Rogers
FRD3 Controls Iron Localization in Arabidopsis
Plant Physiology,
September 1, 2004;
136(1):
2523 - 2531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Roberts, A. J. Pierson, Z. Panaviene, and E. L. Walker
Yellow Stripe1. Expanded Roles for the Maize Iron-Phytosiderophore Transporter
Plant Physiology,
May 1, 2004;
135(1):
112 - 120.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schaaf, U. Ludewig, B. E. Erenoglu, S. Mori, T. Kitahara, and N. von Wiren
ZmYS1 Functions as a Proton-coupled Symporter for Phytosiderophore- and Nicotianamine-chelated Metals
J. Biol. Chem.,
March 5, 2004;
279(10):
9091 - 9096.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Mizuno, K. Higuchi, T. Sakamoto, H. Nakanishi, S. Mori, and N. K. Nishizawa
Three Nicotianamine Synthase Genes Isolated from Maize Are Differentially Regulated by Iron Nutritional Status
Plant Physiology,
August 1, 2003;
132(4):
1989 - 1997.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Wang, M. Okamoto, X. Xing, and N. M. Crawford
Microarray Analysis of the Nitrate Response in Arabidopsis Roots and Shoots Reveals over 1,000 Rapidly Responding Genes and New Linkages to Glucose, Trehalose-6-Phosphate, Iron, and Sulfate Metabolism
Plant Physiology,
June 1, 2003;
132(2):
556 - 567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Takahashi, Y. Terada, I. Nakai, H. Nakanishi, E. Yoshimura, S. Mori, and N. K. Nishizawa
Role of Nicotianamine in the Intracellular Delivery of Metals and Plant Reproductive Development
PLANT CELL,
June 1, 2003;
15(6):
1263 - 1280.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. M. Reichman and D. R. Parker
Revisiting the Metal-Binding Chemistry of Nicotianamine and 2'-Deoxymugineic Acid. Implications for Iron Nutrition in Strategy II Plants
Plant Physiology,
August 1, 2002;
129(4):
1435 - 1438.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Kruger, O. Berkowitz, U. W. Stephan, and R. Hell
A Metal-binding Member of the Late Embryogenesis Abundant Protein Family Transports Iron in the Phloem of Ricinus communis L.
J. Biol. Chem.,
July 5, 2002;
277(28):
25062 - 25069.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. M. Ausubel
Summaries of National Science Foundation-Sponsored Arabidopsis 2010 Projects and National Science Foundation-Sponsored Plant Genome Projects That Are Generating Arabidopsis Resources for the Community
Plant Physiology,
June 1, 2002;
129(2):
394 - 437.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Hale, S. P. McGrath, E. Lombi, S. M. Stack, N. Terry, I. J. Pickering, G. N. George, and E. A.H. Pilon-Smits
Molybdenum Sequestration in Brassica Species. A Role for Anthocyanins?
Plant Physiology,
August 1, 2001;
126(4):
1391 - 1402.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|