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Plant Physiol, August 2001, Vol. 126, pp. 1646-1667
Phylogenetic Relationships within Cation Transporter
Families of Arabidopsis1
Pascal
Mäser,2
Sébastien
Thomine,2
Julian I.
Schroeder,2
John M.
Ward,3
Kendal
Hirschi,3
Heven
Sze,3
Ina N.
Talke,4
Anna
Amtmann,4
Frans J.M.
Maathuis,4
Dale
Sanders,4
Jeff F.
Harper,5
Jason
Tchieu,5
Michael
Gribskov,5
Michael W.
Persans,6
David E.
Salt,67*
Sun A
Kim,8 and
Mary Lou
Guerinot8
Division of Biology, Cell and Developmental Biology Section
and Center for Molecular Genetics (P.M., J.I.S.) and San Diego Super
Computer Center (J.T., M.G.), University of California, San Diego, La
Jolla, California 92093-0116; Institut des Sciences du
Végétal, Centre National de la Recherche
Scientifique, Avenue de la Terrasse, 91198 Gif-sur-Yvette cedex,
France (S.T.); Department of Plant Biology, University of Minnesota,
St. Paul, Minnesota 55108-1095 (J.M.W.); Plant Physiology Group,
Baylor College of Medicine Children's Nutrition Research Center,
Houston, Texas 77030 (K.H.); Department of Cell Biology and Molecular
Genetics, University of Maryland, College Park, Maryland 20742-5815
(H.S.); The Plant Laboratory, Department of Biology, University of
York, York YO10 5YW, United Kingdom (I.N.T., A.A., F.J.M.M.,
D.S.); Department of Cell Biology, The Scripps Research Institute, La
Jolla, California 92037 (J.F.H.); Department of Chemistry, Northern
Arizona University, Flagstaff, Arizona 86011 (M.W.P., D.E.S.); and
Department of Biological Science, Dartmouth College, Hanover, New
Hampshire 03755 (S.A.K., M.L.G.)
Uptake and translocation of cationic nutrients play
essential roles in physiological processes including plant growth,
nutrition, signal transduction, and development. Approximately 5% of
the Arabidopsis genome appears to encode membrane transport proteins. These proteins are classified in 46 unique families containing approximately 880 members. In addition, several hundred putative transporters have not yet been assigned to families. In this paper, we
have analyzed the phylogenetic relationships of over 150 cation transport proteins. This analysis has focused on cation transporter gene families for which initial characterizations have been achieved for individual members, including potassium transporters and channels, sodium transporters, calcium antiporters, cyclic nucleotide-gated channels, cation diffusion facilitator proteins, natural
resistance-associated macrophage proteins (NRAMP), and Zn-regulated
transporter Fe-regulated transporter-like proteins. Phylogenetic trees
of each family define the evolutionary relationships of the members to
each other. These families contain numerous members, indicating diverse
functions in vivo. Closely related isoforms and separate subfamilies
exist within many of these gene families, indicating possible
redundancies and specialized functions. To facilitate their further
study, the PlantsT database (http://plantst.sdsc.edu) has been created that includes alignments of the analyzed cation transporters and their
chromosomal locations.
1
This research was supported by the National
Science Foundation (grant no. DBI-0077378 to M.L.G., D.E.S., J.I.S.,
J.F.H., and M.G.), by The Human Frontiers Science Program fellowship
program (support to P.M.), and by AstraZeneca (studentship to I.N.T.). The PlantsT database is partially supported by the resources of the
National Biomedical Computation Resource (grant no. NIH/NCRR P41
RR-08605).
2
These authors were responsible for potassium
transporter and NRAMP families.
3
These authors were responsible for the
cation/H+ antiporter family.
4
These authors were responsible for the CNGC transporter family.
5
These authors were responsible for the bioinformatics
and Web site development.
6
These authors were responsible for the CDF metal
transporter family.
7
Present address: Department of Horticulture and
Landscape Architecture, Purdue University, West Lafayette, IN
47907-1165.
8
These authors were responsible for the ZIP metal
transporter family.
*
Corresponding author; e-mail salt{at}hort.purdue.edu; fax
765-494-0391.
© 2001 American Society of Plant Physiologists
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C.-P. Song, Y. Guo, Q. Qiu, G. Lambert, D. W. Galbraith, A. Jagendorf, and J.-K. Zhu
A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana
PNAS,
July 6, 2004;
101(27):
10211 - 10216.
[Abstract]
[Full Text]
[PDF]
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R. Shin and D. P. Schachtman
Hydrogen peroxide mediates plant root cell response to nutrient deprivation
PNAS,
June 8, 2004;
101(23):
8827 - 8832.
[Abstract]
[Full Text]
[PDF]
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D. Hussain, M. J. Haydon, Y. Wang, E. Wong, S. M. Sherson, J. Young, J. Camakaris, J. F. Harper, and C. S. Cobbett
P-Type ATPase Heavy Metal Transporters with Roles in Essential Zinc Homeostasis in Arabidopsis
PLANT CELL,
May 1, 2004;
16(5):
1327 - 1339.
[Abstract]
[Full Text]
[PDF]
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S. J. Ahn, R. Shin, and D. P. Schachtman
Expression of KT/KUP Genes in Arabidopsis and the Role of Root Hairs in K+ Uptake
Plant Physiology,
March 1, 2004;
134(3):
1135 - 1145.
[Abstract]
[Full Text]
[PDF]
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R. Waditee, G. S. Hossain, Y. Tanaka, T. Nakamura, M. Shikata, J. Takano, T. Takabe, and T. Takabe
Isolation and Functional Characterization of Ca2+/H+ Antiporters from Cyanobacteria
J. Biol. Chem.,
February 6, 2004;
279(6):
4330 - 4338.
[Abstract]
[Full Text]
[PDF]
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N.-H. Cheng, J. K. Pittman, J.-K. Zhu, and K. D. Hirschi
The Protein Kinase SOS2 Activates the Arabidopsis H+/Ca2+ Antiporter CAX1 to Integrate Calcium Transport and Salt Tolerance
J. Biol. Chem.,
January 23, 2004;
279(4):
2922 - 2926.
[Abstract]
[Full Text]
[PDF]
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J. L. Hall and L. E. Williams
Transition metal transporters in plants
J. Exp. Bot.,
December 1, 2003;
54(393):
2601 - 2613.
[Abstract]
[Full Text]
[PDF]
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R. Catala, E. Santos, J. M. Alonso, J. R. Ecker, J. M. Martinez-Zapater, and J. Salinas
Mutations in the Ca2+/H+ Transporter CAX1 Increase CBF/DREB1 Expression and the Cold-Acclimation Response in Arabidopsis
PLANT CELL,
December 1, 2003;
15(12):
2940 - 2951.
[Abstract]
[Full Text]
[PDF]
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D. Blaudez, A. Kohler, F. Martin, D. Sanders, and M. Chalot
Poplar Metal Tolerance Protein 1 Confers Zinc Tolerance and Is an Oligomeric Vacuolar Zinc Transporter with an Essential Leucine Zipper Motif
PLANT CELL,
December 1, 2003;
15(12):
2911 - 2928.
[Abstract]
[Full Text]
[PDF]
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H. Wintz, T. Fox, Y.-Y. Wu, V. Feng, W. Chen, H.-S. Chang, T. Zhu, and C. Vulpe
Expression Profiles of Arabidopsis thaliana in Mineral Deficiencies Reveal Novel Transporters Involved in Metal Homeostasis
J. Biol. Chem.,
November 28, 2003;
278(48):
47644 - 47653.
[Abstract]
[Full Text]
[PDF]
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S. SHABALA
Regulation of Potassium Transport in Leaves: from Molecular to Tissue Level
Ann. Bot.,
November 1, 2003;
92(5):
627 - 634.
[Abstract]
[Full Text]
[PDF]
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T. Yamaguchi, M. P. Apse, H. Shi, and E. Blumwald
Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity
PNAS,
October 14, 2003;
100(21):
12510 - 12515.
[Abstract]
[Full Text]
[PDF]
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J. D. Becker, L. C. Boavida, J. Carneiro, M. Haury, and J. A. Feijo
Transcriptional Profiling of Arabidopsis Tissues Reveals the Unique Characteristics of the Pollen Transcriptome
Plant Physiology,
October 1, 2003;
133(2):
713 - 725.
[Abstract]
[Full Text]
[PDF]
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S. A. Ramesh, R. Shin, D. J. Eide, and D. P. Schachtman
Differential Metal Selectivity and Gene Expression of Two Zinc Transporters from Rice
Plant Physiology,
September 1, 2003;
133(1):
126 - 134.
[Abstract]
[Full Text]
[PDF]
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B.-G. Hua, R. W. Mercier, Q. Leng, and G. A. Berkowitz
Plants Do It Differently. A New Basis for Potassium/Sodium Selectivity in the Pore of an Ion Channel
Plant Physiology,
July 1, 2003;
132(3):
1353 - 1361.
[Abstract]
[Full Text]
[PDF]
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K. Philippar, K. Buchsenschutz, M. Abshagen, I. Fuchs, D. Geiger, B. Lacombe, and R. Hedrich
The K+ Channel KZM1 Mediates Potassium Uptake into the Phloem and Guard Cells of the C4 Grass Zea mays
J. Biol. Chem.,
May 2, 2003;
278(19):
16973 - 16981.
[Abstract]
[Full Text]
[PDF]
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E. Delhaize, T. Kataoka, D. M. Hebb, R. G. White, and P. R. Ryan
Genes Encoding Proteins of the Cation Diffusion Facilitator Family That Confer Manganese Tolerance
PLANT CELL,
May 1, 2003;
15(5):
1131 - 1142.
[Abstract]
[Full Text]
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N.-H. Cheng and K. D. Hirschi
Cloning and Characterization of CXIP1, a Novel PICOT Domain-containing Arabidopsis Protein That Associates with CAX1
J. Biol. Chem.,
February 14, 2003;
278(8):
6503 - 6509.
[Abstract]
[Full Text]
[PDF]
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T. Shigaki, J. K. Pittman, and K. D. Hirschi
Manganese Specificity Determinants in the Arabidopsis Metal/H+ Antiporter CAX2
J. Biol. Chem.,
February 14, 2003;
278(8):
6610 - 6617.
[Abstract]
[Full Text]
[PDF]
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N.-H. Cheng, J. K. Pittman, B. J. Barkla, T. Shigaki, and K. D. Hirschi
The Arabidopsis cax1 Mutant Exhibits Impaired Ion Homeostasis, Development, and Hormonal Responses and Reveals Interplay among Vacuolar Transporters
PLANT CELL,
February 1, 2003;
15(2):
347 - 364.
[Abstract]
[Full Text]
[PDF]
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C. Balague, B. Lin, C. Alcon, G. Flottes, S. Malmstrom, C. Kohler, G. Neuhaus, G. Pelletier, F. Gaymard, and D. Roby
HLM1, an Essential Signaling Component in the Hypersensitive Response, Is a Member of the Cyclic Nucleotide-Gated Channel Ion Channel Family
PLANT CELL,
February 1, 2003;
15(2):
365 - 379.
[Abstract]
[Full Text]
[PDF]
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R. Schwacke, A. Schneider, E. van der Graaff, K. Fischer, E. Catoni, M. Desimone, W. B. Frommer, U.-I. Flugge, and R. Kunze
ARAMEMNON, a Novel Database for Arabidopsis Integral Membrane Proteins
Plant Physiology,
January 1, 2003;
131(1):
16 - 26.
[Abstract]
[Full Text]
[PDF]
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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]
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J. K. Pittman, C. S. Sreevidya, T. Shigaki, H. Ueoka-Nakanishi, and K. D. Hirschi
Distinct N-Terminal Regulatory Domains of Ca2+/H+ Antiporters
Plant Physiology,
October 1, 2002;
130(2):
1054 - 1062.
[Abstract]
[Full Text]
[PDF]
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D. Geiger, D. Becker, B. Lacombe, and R. Hedrich
Outer Pore Residues Control the H+ and K+ Sensitivity of the Arabidopsis Potassium Channel AKT3
PLANT CELL,
August 1, 2002;
14(8):
1859 - 1868.
[Abstract]
[Full Text]
[PDF]
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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]
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J. K. Pittman, T. Shigaki, N.-H. Cheng, and K. D. Hirschi
Mechanism of N-terminal Autoinhibition in the Arabidopsis Ca2+/H+ Antiporter CAX1
J. Biol. Chem.,
July 12, 2002;
277(29):
26452 - 26459.
[Abstract]
[Full Text]
[PDF]
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R. A. Gaxiola, G. R. Fink, and K. D. Hirschi
Genetic Manipulation of Vacuolar Proton Pumps and Transporters
Plant Physiology,
July 1, 2002;
129(3):
967 - 973.
[Full Text]
[PDF]
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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]
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D. Sanders, J. Pelloux, C. Brownlee, and J. F. Harper
Calcium at the Crossroads of Signaling
PLANT CELL,
May 1, 2002;
14(90001):
S401 - 417.
[Full Text]
[PDF]
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V. S. Reddy, G. S. Ali, and A. S. N. Reddy
Genes Encoding Calmodulin-binding Proteins in the Arabidopsis Genome
J. Biol. Chem.,
March 15, 2002;
277(12):
9840 - 9852.
[Abstract]
[Full Text]
[PDF]
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K. Mouline, A.-A. Very, F. Gaymard, J. Boucherez, G. Pilot, M. Devic, D. Bouchez, J.-B. Thibaud, and H. Sentenac
Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis
Genes & Dev.,
February 1, 2002;
16(3):
339 - 350.
[Abstract]
[Full Text]
[PDF]
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Q. Leng, R. W. Mercier, B.-G. Hua, H. Fromm, and G. A. Berkowitz
Electrophysiological Analysis of Cloned Cyclic Nucleotide-Gated Ion Channels
Plant Physiology,
February 1, 2002;
128(2):
400 - 410.
[Abstract]
[Full Text]
[PDF]
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F. J.M. Maathuis and D. Sanders
Sodium Uptake in Arabidopsis Roots Is Regulated by Cyclic Nucleotides
Plant Physiology,
December 1, 2001;
127(4):
1617 - 1625.
[Abstract]
[Full Text]
[PDF]
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T. Shigaki, N.-h. Cheng, J. K. Pittman, and K. Hirschi
Structural Determinants of Ca2+ Transport in the Arabidopsis H+/Ca2+ Antiporter CAX1
J. Biol. Chem.,
November 9, 2001;
276(46):
43152 - 43159.
[Abstract]
[Full Text]
[PDF]
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