AtCCX3 Is an Arabidopsis Endomembrane H+-Dependent K+ Transporter1[W][OA]
The Arabidopsis ( Arabidopsis thaliana ) cation calcium exchangers (CCXs) were recently identified as a subfamily of cation transporters; however, no plant CCX s have been functionally characterized. Here, we show that Arabidopsis AtCCX3 (At3g14070) and AtCCX4 (At1g54115) can suppress yeast mutants...
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| Published in | Plant physiology (Bethesda) Vol. 148; no. 3; pp. 1474 - 1486 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
American Society of Plant Biologists
01.11.2008
|
| Online Access | Get full text |
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| Abstract | The Arabidopsis (
Arabidopsis thaliana
) cation calcium exchangers (CCXs) were recently identified as a subfamily of cation transporters; however, no plant
CCX
s have been functionally characterized. Here, we show that Arabidopsis AtCCX3 (At3g14070) and AtCCX4 (At1g54115) can suppress yeast mutants defective in Na
+
, K
+
, and Mn
2+
transport. We also report high-capacity uptake of
86
Rb
+
in tonoplast-enriched vesicles from yeast expressing
AtCCX3
. Cation competition studies showed inhibition of
86
Rb
+
uptake in
AtCCX3
cells by excess Na
+
, K
+
, and Mn
2+
. Functional epitope-tagged AtCCX3 fusion proteins were localized to endomembranes in plants and yeast. In Arabidopsis,
AtCCX3
is primarily expressed in flowers, while
AtCCX4
is expressed throughout the plant. Quantitative polymerase chain reaction showed that expression of
AtCCX3
increased in plants treated with NaCl, KCl, and MnCl
2
. Insertional mutant lines of
AtCCX3
and
AtCCX4
displayed no apparent growth defects; however, overexpression of
AtCCX3
caused increased Na
+
accumulation and increased
86
Rb
+
transport. Uptake of
86
Rb
+
increased in tonoplast-enriched membranes isolated from Arabidopsis lines expressing CCX3 driven by the cauliflower mosaic virus 35S promoter. Overexpression of
AtCCX3
in tobacco (
Nicotiana tabacum
) produced lesions in the leaves, stunted growth, and resulted in the accumulation of higher levels of numerous cations. In summary, these findings suggest that AtCCX3 is an endomembrane-localized H
+
-dependent K
+
transporter with apparent Na
+
and Mn
2+
transport properties distinct from those of previously characterized plant transporters. |
|---|---|
| AbstractList | The Arabidopsis (
Arabidopsis thaliana
) cation calcium exchangers (CCXs) were recently identified as a subfamily of cation transporters; however, no plant
CCX
s have been functionally characterized. Here, we show that Arabidopsis AtCCX3 (At3g14070) and AtCCX4 (At1g54115) can suppress yeast mutants defective in Na
+
, K
+
, and Mn
2+
transport. We also report high-capacity uptake of
86
Rb
+
in tonoplast-enriched vesicles from yeast expressing
AtCCX3
. Cation competition studies showed inhibition of
86
Rb
+
uptake in
AtCCX3
cells by excess Na
+
, K
+
, and Mn
2+
. Functional epitope-tagged AtCCX3 fusion proteins were localized to endomembranes in plants and yeast. In Arabidopsis,
AtCCX3
is primarily expressed in flowers, while
AtCCX4
is expressed throughout the plant. Quantitative polymerase chain reaction showed that expression of
AtCCX3
increased in plants treated with NaCl, KCl, and MnCl
2
. Insertional mutant lines of
AtCCX3
and
AtCCX4
displayed no apparent growth defects; however, overexpression of
AtCCX3
caused increased Na
+
accumulation and increased
86
Rb
+
transport. Uptake of
86
Rb
+
increased in tonoplast-enriched membranes isolated from Arabidopsis lines expressing CCX3 driven by the cauliflower mosaic virus 35S promoter. Overexpression of
AtCCX3
in tobacco (
Nicotiana tabacum
) produced lesions in the leaves, stunted growth, and resulted in the accumulation of higher levels of numerous cations. In summary, these findings suggest that AtCCX3 is an endomembrane-localized H
+
-dependent K
+
transporter with apparent Na
+
and Mn
2+
transport properties distinct from those of previously characterized plant transporters. |
| Author | Sreevidya, Coimbatore S. Park, Sunghun Hirschi, Kendal D. Morris, Jay Tian, Hui Ward, John M. |
| AuthorAffiliation | Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) |
| AuthorAffiliation_xml | – name: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) |
| Author_xml | – sequence: 1 givenname: Jay surname: Morris fullname: Morris, Jay organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) – sequence: 2 givenname: Hui surname: Tian fullname: Tian, Hui organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) – sequence: 3 givenname: Sunghun surname: Park fullname: Park, Sunghun organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) – sequence: 4 givenname: Coimbatore S. surname: Sreevidya fullname: Sreevidya, Coimbatore S. organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) – sequence: 5 givenname: John M. surname: Ward fullname: Ward, John M. organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) – sequence: 6 givenname: Kendal D. surname: Hirschi fullname: Hirschi, Kendal D. email: kendalh@bcm.tmc.edu organization: Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (J.M., S.P., K.D.H.); Plant Physiology Group, United States Department of Agriculture/Agriculture Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030 (J.M., K.D.H.); Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 (H.T., J.M.W.); and Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 (C.S.S.) |
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| Notes | This work was supported by the U.S. Department of Agriculture/Agricultural Research Service (Cooperative Agreement no. 58–62650–6001), the National Science Foundation (grant nos. NSF 0344350 and NSF 020977), and the U.S. Department of Agriculture Cooperative State Research, Education, and Extension Service (grant no. 2005–34402–17121 to K.D.H.). The National Science Foundation (grant no. 0209792) funded work in the laboratory of J.M.W. Corresponding author; e-mail kendalh@bcm.tmc.edu. www.plantphysiol.org/cgi/doi/10.1104/pp.108.118810 The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Kendal D. Hirschi (kendalh@bcm.tmc.edu). The online version of this article contains Web-only data. Open Access articles can be viewed online without a subscription. |
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| Snippet | The Arabidopsis (
Arabidopsis thaliana
) cation calcium exchangers (CCXs) were recently identified as a subfamily of cation transporters; however, no plant
CCX... |
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| Title | AtCCX3 Is an Arabidopsis Endomembrane H+-Dependent K+ Transporter1[W][OA] |
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