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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [4];  [3];  [1]
  1. Univ. of California, San Diego, La Jolla, CA (United States)
  2. Univ. of Cologne (Germany)
  3. Univ. of Gothenburg (Sweden)
  4. Michigan State Univ., East Lansing, MI (United States)
+ Show Author Affiliations

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. In this paper, 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.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF); National Institute of Environmental Health Sciences (NIEHS)
Grant/Contract Number:
FG02-91ER20021; FG02-03ER15449; MCB0918220; P42ES010337
OSTI ID:
1602746
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, Issue 20; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 190 works
Citation information provided by
Web of Science

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Cited By (40)

Ion antiport accelerates photosynthetic acclimation in fluctuating light environments journal November 2014
Ion and metabolite transport in the chloroplast of algae: lessons from land plants journal March 2018
DAY-LENGTH-DEPENDENT DELAYED-GREENING1, the Arabidopsis Homolog of the Cyanobacterial H+-Extrusion Protein, Is Essential for Chloroplast pH Regulation and Optimization of Non-Photochemical Quenching journal October 2019
Leaf photosynthetic capacity is regulated by the interaction of nitrogen and potassium through coordination of CO 2 diffusion and carboxylation journal March 2019
RNA Sequencing Analysis of the msl2msl3, crl, and ggps1 Mutants Indicates that Diverse Sources of Plastid Dysfunction Do Not Alter Leaf Morphology Through a Common Signaling Pathway journal December 2015
A Grapevine TTG2-Like WRKY Transcription Factor Is Involved in Regulating Vacuolar Transport and Flavonoid Biosynthesis journal January 2017
A bestrophin-like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis : Involvement of AtBest in fine-tuning of photosynthesis journal April 2016
Genomic and Transcriptomic Compilation of Chloroplast Ionic Transporters of Physcomitrella patens. Study of NHAD Transporters in Na+ and K+ Homeostasis journal October 2017
Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM journal December 2019
Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I journal May 2017
Photoprotective strategies in the motile cryptophyte alga Rhodomonas salina—role of non-photochemical quenching, ions, photoinhibition, and cell motility journal July 2019
Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes journal May 2017
The topology of plastid inner envelope potassium cation efflux antiporter KEA1 provides new insights into its regulatory features journal December 2019
Regulation and Levels of the Thylakoid K + /H + Antiporter KEA3 Shape the Dynamic Response of Photosynthesis in Fluctuating Light journal May 2016
Rapid hyperosmotic-induced Ca 2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters journal August 2016
A voltage-dependent chloride channel fine-tunes photosynthesis in plants journal May 2016
In-Depth Genomic and Transcriptomic Analysis of Five K+ Transporter Gene Families in Soybean Confirm Their Differential Expression for Nodulation journal May 2017
The plastid NAD(P)H dehydrogenase-like complex: structure, function and evolutionary dynamics journal October 2019
Chloroplast‐localized BICAT proteins shape stromal calcium signals and are required for efficient photosynthesis journal August 2018
Roles and Transport of Sodium and Potassium in Plants book January 2016
Ion Channels in Native Chloroplast Membranes: Challenges and Potential for Direct Patch-Clamp Studies journal December 2015
Proteomic Insight into the Response of Arabidopsis Chloroplasts to Darkness journal May 2016
Salt-Enhanced Reproductive Development of Suaeda salsa L. Coincided With Ion Transporter Gene Upregulation in Flowers and Increased Pollen K+ Content journal March 2019
Evidence for potassium transport activity of Arabidopsis KEA1-KEA6 journal July 2019
Genomic novelty versus convergence in the basis of adaptation to whole genome duplication posted_content June 2020
Proton Gradients and Proton-Dependent Transport Processes in the Chloroplast journal February 2016
Golgi-localized cation/proton exchangers regulate ionic homeostasis and skotomorphogenesis in Arabidopsis: Golgi-Localized KEAs Regulate Ionic Homeostasis journal November 2018
Potassium: A Vital Regulator of Plant Responses and Tolerance to Abiotic Stresses journal March 2018
K+ and Cl− channels/transporters independently fine-tune photosynthesis in plants journal June 2019
The Arabidopsis Thylakoid Chloride Channel AtCLCe Functions in Chloride Homeostasis and Regulation of Photosynthetic Electron Transport journal February 2016
The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth journal September 2015
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Molecular Evolution and Interaction of Membrane Transport and Photoreception in Plants journal October 2019
Salinity Response in Chloroplasts: Insights from Gene Characterization journal May 2017
Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH
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  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730 https://doi.org/10.1098/rstb.2016.0381
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Increasing cyclic electron flow is related to Na + sequestration into vacuoles for salt tolerance in soybean journal August 2015
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Potassium: A Vital Regulator of Plant Responses and Tolerance to Abiotic Stresses journal January 2018

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