|
Plant Physiol, April 2000, Vol. 122, pp. 1249-1260
The Arabidopsis HKT1 Gene Homolog Mediates Inward
Na+ Currents in Xenopus laevis Oocytes and
Na+ Uptake in Saccharomyces
cerevisiae1
Nobuyuki
Uozumi,
Eugene J.
Kim,
Francisco
Rubio,2
Takao
Yamaguchi,
Shoshi
Muto,
Akio
Tsuboi,
Evert P.
Bakker,
Tatsunosuke
Nakamura, and
Julian I.
Schroeder
Bioscience Center, Nagoya University, Nagoya, 464-8601,
Japan (N.U., S.M.); Department of Biology and Center for Molecular
Genetics, University of California at San Diego, La Jolla, California
92093-0116 (N.U., E.J.K., F.R., J.I.S.); Graduate School of
Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan
(N.U., T.Y., S.M.); Department of Biophysics and Biochemistry, Graduate
School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo
113, Japan (A.T.); Abteilung Mikrobiologie, Universität
Osnabrück, Barbarastrasse 11, D-49076 Osnabrück, Germany
(E.P.B.); and Faculty of Pharmaceutical Sciences, Chiba University,
1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan (T.N.)
The
Na+-K+ co-transporter HKT1, first isolated from
wheat, mediates high-affinity K+ uptake. The function of
HKT1 in plants, however, remains to be elucidated, and the isolation of
HKT1 homologs from Arabidopsis would further studies of the roles of
HKT1 genes in plants. We report here the isolation of a cDNA homologous
to HKT1 from Arabidopsis (AtHKT1) and the
characterization of its mode of ion transport in heterologous systems.
The deduced amino acid sequence of AtHKT1 is 41% identical to that of
HKT1, and the hydropathy profiles are very similar.
AtHKT1 is expressed in roots and, to a lesser extent, in
other tissues. Interestingly, we found that the ion transport
properties of AtHKT1 are significantly different from the wheat
counterpart. As detected by electrophysiological measurements, AtHKT1
functioned as a selective Na+ uptake transporter in
Xenopus laevis oocytes, and the presence of external
K+ did not affect the AtHKT1-mediated ion conductance
(unlike that of HKT1). When expressed in Saccharomyces
cerevisiae, AtHKT1 inhibited growth of the yeast in a medium
containing high levels of Na+, which correlates to the
large inward Na+ currents found in the oocytes.
Furthermore, in contrast to HKT1, AtHKT1 did not complement the growth
of yeast cells deficient in K+ uptake when cultured in
K+-limiting medium. However, expression of
AtHKT1 did rescue Escherichia coli
mutants carrying deletions in K+ transporters. The rescue
was associated with a less than 2-fold stimulation of K+
uptake into K+-depleted cells. These data demonstrate that
AtHKT1 differs in its transport properties from the wheat HKT1,
and that AtHKT1 can mediate Na+ and, to a small degree,
K+ transport in heterologous expression systems.
1
This work was supported by the U.S. Department
of Agriculture (grant no. 98-3504-6684 to J.I.S.), by Grants-in-Aid
for Scientific Research from the Ministry of Education, Science, Sports
and Culture of Japan (nos. 11660082 and 11132227 to N.U.), and by the
Salt Science Research Foundation Grant. This work was also supported in
part by a U.S. Department of Agriculture Postdoctoral Fellowship (no.
9801009 to E.J.K.), by the Deutshe Forschungsgemeinschaft (no. SFB431
to E.P.B), and by the Fonds der Chemischen Industrie (to E.P.B.).
2
Present address: Departemento de Biotecnologia,
Escuela Tecnica Superior de Ingenierous Agronomos, 28040 Madrid, Spain.
© 2000 American Society of Plant Physiologists
This article has been cited by other articles:
|
|
|
|
 
M. Jabnoune, S. Espeout, D. Mieulet, C. Fizames, J.-L. Verdeil, G. Conejero, A. Rodriguez-Navarro, H. Sentenac, E. Guiderdoni, C. Abdelly, et al.
Diversity in Expression Patterns and Functional Properties in the Rice HKT Transporter Family
Plant Physiology,
August 1, 2009;
150(4):
1955 - 1971.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. S. Moller, M. Gilliham, D. Jha, G. M. Mayo, S. J. Roy, J. C. Coates, J. Haseloff, and M. Tester
Shoot Na+ Exclusion and Increased Salinity Tolerance Engineered by Cell Type-Specific Alteration of Na+ Transport in Arabidopsis
PLANT CELL,
July 1, 2009;
21(7):
2163 - 2178.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. J. Kronzucker, M. W. Szczerba, L. M. Schulze, and D. T. Britto
Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.)
J. Exp. Bot.,
July 1, 2008;
59(10):
2793 - 2801.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Huang, W. Spielmeyer, E. S. Lagudah, and R. Munns
Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance
J. Exp. Bot.,
March 5, 2008;
(2008)
ern033v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Takahashi, S. Liu, and T. Takano
Cloning and functional comparison of a high-affinity K+ transporter gene PhaHKT1 of salt-tolerant and salt-sensitive reed plants
J. Exp. Bot.,
December 1, 2007;
58(15-16):
4387 - 4395.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S.-M. Wang, J.-L. Zhang, and T. J. Flowers
Low-Affinity Na+ Uptake in the Halophyte Suaeda maritima
Plant Physiology,
October 1, 2007;
145(2):
559 - 571.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Corratge, S. Zimmermann, R. Lambilliotte, C. Plassard, R. Marmeisse, J.-B. Thibaud, B. Lacombe, and H. Sentenac
Molecular and Functional Characterization of a Na+-K+ Transporter from the Trk Family in the Ectomycorrhizal Fungus Hebeloma cylindrosporum
J. Biol. Chem.,
September 7, 2007;
282(36):
26057 - 26066.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. S. Byrt, J. D. Platten, W. Spielmeyer, R. A. James, E. S. Lagudah, E. S. Dennis, M. Tester, and R. Munns
HKT1;5-Like Cation Transporters Linked to Na+ Exclusion Loci in Wheat, Nax2 and Kna1
Plant Physiology,
April 1, 2007;
143(4):
1918 - 1928.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Md. A. Kader, T. Seidel, D. Golldack, and S. Lindberg
Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars
J. Exp. Bot.,
December 1, 2006;
57(15):
4257 - 4268.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Huang, W. Spielmeyer, E. S. Lagudah, R. A. James, J. D. Platten, E. S. Dennis, and R. Munns
A Sodium Transporter (HKT7) Is a Candidate for Nax1, a Gene for Salt Tolerance in Durum Wheat
Plant Physiology,
December 1, 2006;
142(4):
1718 - 1727.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Horie, R. Horie, W.-Y. Chan, H.-Y. Leung, and J. I. Schroeder
Calcium Regulation of Sodium Hypersensitivities of sos3 and athkt1 Mutants
Plant Cell Physiol.,
May 1, 2006;
47(5):
622 - 633.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Rodriguez-Navarro and F. Rubio
High-affinity potassium and sodium transport systems in plants
J. Exp. Bot.,
March 1, 2006;
57(5):
1149 - 1160.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Tholema, M. V. d. Bruggen, P. Maser, T. Nakamura, J. I. Schroeder, H. Kobayashi, N. Uozumi, and E. P. Bakker
All Four Putative Selectivity Filter Glycine Residues in KtrB Are Essential for High Affinity and Selective K+ Uptake by the KtrAB System from Vibrio alginolyticus
J. Biol. Chem.,
December 16, 2005;
280(50):
41146 - 41154.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Md. A. Kader and S. Lindberg
Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI
J. Exp. Bot.,
December 1, 2005;
56(422):
3149 - 3158.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Zhu, D. Schraut, W. Hartung, and A. R. Schaffner
Differential responses of maize MIP genes to salt stress and ABA
J. Exp. Bot.,
November 1, 2005;
56(421):
2971 - 2981.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Vera-Estrella, B. J. Barkla, L. Garcia-Ramirez, and O. Pantoja
Salt Stress in Thellungiella halophila Activates Na+ Transport Mechanisms Required for Salinity Tolerance
Plant Physiology,
November 1, 2005;
139(3):
1507 - 1517.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Sheng, C. J. Perry, O. B. Kashlan, and T. R. Kleyman
Side Chain Orientation of Residues Lining the Selectivity Filter of Epithelial Na+ Channels
J. Biol. Chem.,
March 4, 2005;
280(9):
8513 - 8522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Chinnusamy, A. Jagendorf, and J.-K. Zhu
Understanding and Improving Salt Tolerance in Plants
Crop Sci.,
January 31, 2005;
45(2):
437 - 448.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Matsuda, H. Kobayashi, H. Katoh, T. Ogawa, L. Futatsugi, T. Nakamura, E. P. Bakker, and N. Uozumi
Na+-dependent K+ Uptake Ktr System from the Cyanobacterium Synechocystis sp. PCC 6803 and Its Role in the Early Phases of Cell Adaptation to Hyperosmotic Shock
J. Biol. Chem.,
December 24, 2004;
279(52):
54952 - 54962.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-M. Gong, D. A. Waner, T. Horie, S. L. Li, R. Horie, K. B. Abid, and J. I. Schroeder
Microarray-based rapid cloning of an ion accumulation deletion mutant in Arabidopsis thaliana
PNAS,
October 26, 2004;
101(43):
15404 - 15409.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Horie and J. I. Schroeder
Sodium Transporters in Plants. Diverse Genes and Physiological Functions
Plant Physiology,
September 1, 2004;
136(1):
2457 - 2462.
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Qi and E. P. Spalding
Protection of Plasma Membrane K+ Transport by the Salt Overly Sensitive1 Na+-H+ Antiporter during Salinity Stress
Plant Physiology,
September 1, 2004;
136(1):
2548 - 2555.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Rus, B.-h. Lee, A. Munoz-Mayor, A. Sharkhuu, K. Miura, J.-K. Zhu, R. A. Bressan, and P. M. Hasegawa
AtHKT1 Facilitates Na+ Homeostasis and K+ Nutrition in Planta
Plant Physiology,
September 1, 2004;
136(1):
2500 - 2511.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Bertrand, K. Altendorf, and M. Bramkamp
Amino Acid Substitutions in Putative Selectivity Filter Regions III and IV in KdpA Alter Ion Selectivity of the KdpFABC Complex from Escherichia coli
J. Bacteriol.,
August 15, 2004;
186(16):
5519 - 5522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y.-H. Peng, Y.-F. Zhu, Y.-Q. Mao, S.-M. Wang, W.-A. Su, and Z.-C. Tang
Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+
J. Exp. Bot.,
April 1, 2004;
55(398):
939 - 949.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G.-F. Zeng, M. Pypaert, and C. L. Slayman
Epitope Tagging of the Yeast K+ Carrier Trk2p Demonstrates Folding That Is Consistent with a Channel-like Structure
J. Biol. Chem.,
January 23, 2004;
279(4):
3003 - 3013.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Chinnusamy, K. Schumaker, and J.-K. Zhu
Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants
J. Exp. Bot.,
January 2, 2004;
55(395):
225 - 236.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Nagaoka and T. Takano
Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis
J. Exp. Bot.,
October 1, 2003;
54(391):
2231 - 2237.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. TESTER and R. DAVENPORT
Na+ Tolerance and Na+ Transport in Higher Plants
Ann. Bot.,
April 1, 2003;
91(5):
503 - 527.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Banuelos, B. Garciadeblas, B. Cubero, and A. Rodriguez-Navarro
Inventory and Functional Characterization of the HAK Potassium Transporters of Rice
Plant Physiology,
October 1, 2002;
130(2):
784 - 795.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Su, D. Golldack, C. Zhao, and H. J. Bohnert
The Expression of HAK-Type K+ Transporters Is Regulated in Response to Salinity Stress in Common Ice Plant
Plant Physiology,
August 1, 2002;
129(4):
1482 - 1493.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Shibata, H. Katoh, M. Sonoda, H. Ohkawa, M. Shimoyama, H. Fukuzawa, A. Kaplan, and T. Ogawa
Genes Essential to Sodium-dependent Bicarbonate Transport in Cyanobacteria. FUNCTION AND PHYLOGENETIC ANALYSIS
J. Biol. Chem.,
May 17, 2002;
277(21):
18658 - 18664.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Xiong, K. S. Schumaker, and J.-K. Zhu
Cell Signaling during Cold, Drought, and Salt Stress
PLANT CELL,
May 1, 2002;
14(90001):
S165 - 183.
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Maser, Y. Hosoo, S. Goshima, T. Horie, B. Eckelman, K. Yamada, K. Yoshida, E. P. Bakker, A. Shinmyo, S. Oiki, et al.
Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants
PNAS,
April 30, 2002;
99(9):
6428 - 6433.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Uozumi
Escherichia coli as an expression system for K+ transport systems from plants
Am J Physiol Cell Physiol,
September 1, 2001;
281(3):
C733 - C739.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Liu, D. J. Fairbairn, R. J. Reid, and D. P. Schachtman
Characterization of Two HKT1 Homologues from Eucalyptus camaldulensis That Display Intrinsic Osmosensing Capability
Plant Physiology,
September 1, 2001;
127(1):
283 - 294.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Cushman
Osmoregulation in Plants: Implications for Agriculture
Integr. Comp. Biol.,
August 1, 2001;
41(4):
758 - 769.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Maser, S. Thomine, J. I. Schroeder, J. M. Ward, K. Hirschi, H. Sze, I. N. Talke, A. Amtmann, F. J.M. Maathuis, D. Sanders, et al.
Phylogenetic Relationships within Cation Transporter Families of Arabidopsis
Plant Physiology,
August 1, 2001;
126(4):
1646 - 1667.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Amtmann, M. Fischer, E. L. Marsh, A. Stefanovic, D. Sanders, and D. P. Schachtman
The Wheat cDNA LCT1 Generates Hypersensitivity to Sodium in a Salt-Sensitive Yeast Strain
Plant Physiology,
July 1, 2001;
126(3):
1061 - 1071.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kato, M. Sakaguchi, Y. Mori, K. Saito, T. Nakamura, E. P. Bakker, Y. Sato, S. Goshima, and N. Uozumi
Evidence in support of a four transmembrane-pore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters
PNAS,
May 3, 2001;
(2001)
101556598.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
M. Tester and R. A. Leigh
Partitioning of nutrient transport processes in roots
J. Exp. Bot.,
March 1, 2001;
52(90001):
445 - 457.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
A. Nublat, J. Desplans, F. Casse, and P. Berthomieu
sas1, an Arabidopsis Mutant Overaccumulating Sodium in the Shoot, Shows Deficiency in the Control of the Root Radial Transport of Sodium
PLANT CELL,
January 1, 2001;
13(1):
125 - 137.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
M. E. Senn, F. Rubio, M. A. Banuelos, and A. Rodriguez-Navarro
Comparative Functional Features of Plant Potassium HvHAK1 and HvHAK2 Transporters
J. Biol. Chem.,
November 21, 2001;
276(48):
44563 - 44569.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Maser, Y. Hosoo, S. Goshima, T. Horie, B. Eckelman, K. Yamada, K. Yoshida, E. P. Bakker, A. Shinmyo, S. Oiki, et al.
Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants
PNAS,
April 30, 2002;
99(9):
6428 - 6433.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kato, M. Sakaguchi, Y. Mori, K. Saito, T. Nakamura, E. P. Bakker, Y. Sato, S. Goshima, and N. Uozumi
Evidence in support of a four transmembrane-pore-transmembrane topology model for the Arabidopsis thaliana Na+/K+ translocating AtHKT1 protein, a member of the superfamily of K+ transporters
PNAS,
May 22, 2001;
98(11):
6488 - 6493.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Rus, S. Yokoi, A. Sharkhuu, M. Reddy, B.-h. Lee, T. K. Matsumoto, H. Koiwa, J.-K. Zhu, R. A. Bressan, and P. M. Hasegawa
AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots
PNAS,
November 20, 2001;
98(24):
14150 - 14155.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
