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Vicia faba TPC1, a genetically encoded variant of the vacuole Two Pore Channel 1, is hyperexcitable

View ORCID ProfileJinping Lu, View ORCID ProfileIngo Dreyer, View ORCID ProfileMiles Sasha Dickinson, View ORCID ProfileSabine Panzer, View ORCID ProfileDawid Jaslan, View ORCID ProfileCarlos Navarro-Retamal, View ORCID ProfileDietmar Geiger, View ORCID ProfileUlrich Terpitz, View ORCID ProfileDirk Becker, View ORCID ProfileRobert M. Stroud, View ORCID ProfileIrene Marten, View ORCID ProfileRainer Hedrich
doi: https://doi.org/10.1101/2021.12.22.473873
Jinping Lu
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
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Ingo Dreyer
2Center of Bioinformatics, Simulation and Modeling, Faculty of Engineering, Universidad de Talca, 3460000 Talca, Chile
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Miles Sasha Dickinson
3Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA 94143, U.S.A
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Sabine Panzer
4Theodor-Boveri-Institute, Department of Biotechnology and Biophysics, Biocenter, University of Würzburg, D-97074 Würzburg, Germany
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Dawid Jaslan
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
5Walther Straub Institute of Pharmacology and Toxicology, Faculty of Medicine, Ludwig Maximilians-Universität, 80336 Munich, Germany
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Carlos Navarro-Retamal
2Center of Bioinformatics, Simulation and Modeling, Faculty of Engineering, Universidad de Talca, 3460000 Talca, Chile
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Dietmar Geiger
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
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Ulrich Terpitz
4Theodor-Boveri-Institute, Department of Biotechnology and Biophysics, Biocenter, University of Würzburg, D-97074 Würzburg, Germany
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Dirk Becker
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
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Robert M. Stroud
3Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, CA 94143, U.S.A
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  • For correspondence: marten@botanik.uni-wuerzburg.de
Irene Marten
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
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  • For correspondence: marten@botanik.uni-wuerzburg.de
Rainer Hedrich
1Department of Molecular Plant Physiology and Biophysics, Biocenter, University of Würzburg, D-97082 Würzburg, Germany
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Abstract

To fire action-potential-like electrical signals, the vacuole membrane requires the depolarization-activated two-pore channel TPC1, also called Slowly activating Vacuolar SV channel. The TPC1/SV channel, encoded by the TPC1 gene, functions as a voltage-dependent and Ca2+-regulated potassium channel. TPC1 currents are activated by a rise in cytoplasmic Ca2+ but inhibited by luminal Ca2+. In search for species-dependent functional TPC1 channel variants, we studied polymorphic amino acids contributing to luminal Ca2+ sensitivity. We found that the acidic residues E457, E605 and D606 of the Ca2+-sensitive Arabidopsis AtTPC1 channel were neutralized by either asparagine or alanine in Vicia faba and many other Fabaceae as well. When expressed in the Arabidopsis loss-of-AtTPC1 function background, the wild type VfTPC1 was hypersensitive to vacuole depolarization and insensitive to blocking luminal Ca2+. When AtTPC1 was mutated for the three VfTPC1-homologous polymorphic site residues, the Arabidopsis At-VfTPC1 channel mutant gained VfTPC1-like voltage and luminal Ca2+ insensitivity that together made vacuoles hyperexcitable. These findings indicate that natural TPC1 channel variants in plant families exist which differ in vacuole excitability and very likely respond to changes in environmental settings of their ecological niche.

Significance statement Vacuolar electrical excitability and stress-related Ca2+ signaling depends on the activity of the vacuolar cation channel TPC1. Until now, the regulatory features of AtTPC1 from the model plant Arabidopsis thaliana was believed to apply to the TPC1 channels of other species. However, here we now show that, surprisingly, the VfTPC1 channel of the economic broad bean, in contrast to AtTPC1, proves to be hyperactive and confers hyperexcitability to the vacuole. The different gating behavior is most likely related to an impaired Ca2+ sensor site in the vacuolar pore vestibule, rising the probability to open at more negative membrane voltages. These natural variants of the TPC1 channel could help the plant adapt and respond to environmental challenges.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 04, 2022.
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Vicia faba TPC1, a genetically encoded variant of the vacuole Two Pore Channel 1, is hyperexcitable
Jinping Lu, Ingo Dreyer, Miles Sasha Dickinson, Sabine Panzer, Dawid Jaslan, Carlos Navarro-Retamal, Dietmar Geiger, Ulrich Terpitz, Dirk Becker, Robert M. Stroud, Irene Marten, Rainer Hedrich
bioRxiv 2021.12.22.473873; doi: https://doi.org/10.1101/2021.12.22.473873
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Vicia faba TPC1, a genetically encoded variant of the vacuole Two Pore Channel 1, is hyperexcitable
Jinping Lu, Ingo Dreyer, Miles Sasha Dickinson, Sabine Panzer, Dawid Jaslan, Carlos Navarro-Retamal, Dietmar Geiger, Ulrich Terpitz, Dirk Becker, Robert M. Stroud, Irene Marten, Rainer Hedrich
bioRxiv 2021.12.22.473873; doi: https://doi.org/10.1101/2021.12.22.473873

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