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Proc Natl Acad Sci U S A. 2014 May 20;111(20):7480-5. doi: 10.1073/pnas.1323899111. Epub 2014 May 2.

Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis.

Author information

1
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;
2
Department of Botany II, University of Cologne, 50674 Cologne, Germany;
3
Department of Biological and Environmental Sciences, University of Gothenburg, 40530 Gothenburg, Sweden; and.
4
Department of Energy Plant Research, Michigan State University, East Lansing, MI 48824-1312.
5
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.

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.

PMID:
24794527
PMCID:
PMC4034250
DOI:
10.1073/pnas.1323899111
[Indexed for MEDLINE]
Free PMC Article

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