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Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis.
Proc Natl Acad Sci U S A. 2014 May 20; 111(20):7480-5.PN

Abstract

Multiple K(+) transporters and channels and the corresponding mutants have been described and studied in the plasma membrane and organelle membranes of plant cells. However, knowledge about the molecular identity of chloroplast K(+) transporters is limited. Potassium transport and a well-balanced K(+) homeostasis were suggested to play important roles in chloroplast function. Because no loss-of-function mutants have been identified, the importance of K(+) transporters for chloroplast function and photosynthesis remains to be determined. Here, we report single and higher-order loss-of-function mutants in members of the cation/proton antiporters-2 antiporter superfamily KEA1, KEA2, and KEA3. KEA1 and KEA2 proteins are targeted to the inner envelope membrane of chloroplasts, whereas KEA3 is targeted to the thylakoid membrane. Higher-order but not single mutants showed increasingly impaired photosynthesis along with pale green leaves and severely stunted growth. The pH component of the proton motive force across the thylakoid membrane was significantly decreased in the kea1kea2 mutants, but increased in the kea3 mutant, indicating an altered chloroplast pH homeostasis. Electron microscopy of kea1kea2 leaf cells revealed dramatically swollen chloroplasts with disrupted envelope membranes and reduced thylakoid membrane density. Unexpectedly, exogenous NaCl application reversed the observed phenotypes. Furthermore, the kea1kea2 background enables genetic analyses of the functional significance of other chloroplast transporters as exemplified here in kea1kea2Na(+)/H(+) antiporter1 (nhd1) triple mutants. Taken together, the presented data demonstrate a fundamental role of inner envelope KEA1 and KEA2 and thylakoid KEA3 transporters in chloroplast osmoregulation, integrity, and ion and pH homeostasis.

Authors+Show Affiliations

Division of Biological Sciences, Section of Cell and Developmental Biology, Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093-0116;Department of Botany II, University of Cologne, 50674 Cologne, Germany;Department of Biological and Environmental Sciences, University of Gothenburg, 40530 Gothenburg, Sweden; and.Department of Energy Plant Research, Michigan State University, East Lansing, MI 48824-1312.Department of Energy Plant Research, Michigan State University, East Lansing, MI 48824-1312.Department of Biological and Environmental Sciences, University of Gothenburg, 40530 Gothenburg, Sweden; and.Division of Biological Sciences, Section of Cell and Developmental Biology, Center for Food and Fuel for the 21st Century, University of California, San Diego, La Jolla, CA 92093-0116; jischroeder@ucsd.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

24794527

Citation

Kunz, Hans-Henning, et al. "Plastidial Transporters KEA1, -2, and -3 Are Essential for Chloroplast Osmoregulation, Integrity, and pH Regulation in Arabidopsis." Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 20, 2014, pp. 7480-5.
Kunz HH, Gierth M, Herdean A, et al. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc Natl Acad Sci U S A. 2014;111(20):7480-5.
Kunz, H. H., Gierth, M., Herdean, A., Satoh-Cruz, M., Kramer, D. M., Spetea, C., & Schroeder, J. I. (2014). Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 111(20), 7480-5. https://doi.org/10.1073/pnas.1323899111
Kunz HH, et al. Plastidial Transporters KEA1, -2, and -3 Are Essential for Chloroplast Osmoregulation, Integrity, and pH Regulation in Arabidopsis. Proc Natl Acad Sci U S A. 2014 May 20;111(20):7480-5. PubMed PMID: 24794527.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. AU - Kunz,Hans-Henning, AU - Gierth,Markus, AU - Herdean,Andrei, AU - Satoh-Cruz,Mio, AU - Kramer,David M, AU - Spetea,Cornelia, AU - Schroeder,Julian I, Y1 - 2014/05/02/ PY - 2014/5/6/entrez PY - 2014/5/6/pubmed PY - 2014/7/16/medline SP - 7480 EP - 5 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 111 IS - 20 N2 - Multiple K(+) transporters and channels and the corresponding mutants have been described and studied in the plasma membrane and organelle membranes of plant cells. However, knowledge about the molecular identity of chloroplast K(+) transporters is limited. Potassium transport and a well-balanced K(+) homeostasis were suggested to play important roles in chloroplast function. Because no loss-of-function mutants have been identified, the importance of K(+) transporters for chloroplast function and photosynthesis remains to be determined. Here, we report single and higher-order loss-of-function mutants in members of the cation/proton antiporters-2 antiporter superfamily KEA1, KEA2, and KEA3. KEA1 and KEA2 proteins are targeted to the inner envelope membrane of chloroplasts, whereas KEA3 is targeted to the thylakoid membrane. Higher-order but not single mutants showed increasingly impaired photosynthesis along with pale green leaves and severely stunted growth. The pH component of the proton motive force across the thylakoid membrane was significantly decreased in the kea1kea2 mutants, but increased in the kea3 mutant, indicating an altered chloroplast pH homeostasis. Electron microscopy of kea1kea2 leaf cells revealed dramatically swollen chloroplasts with disrupted envelope membranes and reduced thylakoid membrane density. Unexpectedly, exogenous NaCl application reversed the observed phenotypes. Furthermore, the kea1kea2 background enables genetic analyses of the functional significance of other chloroplast transporters as exemplified here in kea1kea2Na(+)/H(+) antiporter1 (nhd1) triple mutants. Taken together, the presented data demonstrate a fundamental role of inner envelope KEA1 and KEA2 and thylakoid KEA3 transporters in chloroplast osmoregulation, integrity, and ion and pH homeostasis. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/24794527/Plastidial_transporters_KEA1__2_and__3_are_essential_for_chloroplast_osmoregulation_integrity_and_pH_regulation_in_Arabidopsis_ DB - PRIME DP - Unbound Medicine ER -