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Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling

Glutamate has dual roles in metabolism and signaling; thus, signaling functions must be isolatable and distinct from metabolic fluctuations, as seen in low-glutamate domains at synapses. In plants, wounding triggers electrical and calcium (Ca(2+)) signaling, which involve homologs of mammalian gluta...

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Autores principales: Moe-Lange, Jacob, Gappel, Nicoline M., Machado, Mackenzie, Wudick, Michael M., Sies, Cosima S. A., Schott-Verdugo, Stephan N., Bonus, Michele, Mishra, Swastik, Hartwig, Thomas, Bezrutczyk, Margaret, Basu, Debarati, Farmer, Edward E., Gohlke, Holger, Malkovskiy, Andrey, Haswell, Elizabeth S., Lercher, Martin J., Ehrhardt, David W., Frommer, Wolf B., Kleist, Thomas J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8442888/
https://www.ncbi.nlm.nih.gov/pubmed/34516872
http://dx.doi.org/10.1126/sciadv.abg4298
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author Moe-Lange, Jacob
Gappel, Nicoline M.
Machado, Mackenzie
Wudick, Michael M.
Sies, Cosima S. A.
Schott-Verdugo, Stephan N.
Bonus, Michele
Mishra, Swastik
Hartwig, Thomas
Bezrutczyk, Margaret
Basu, Debarati
Farmer, Edward E.
Gohlke, Holger
Malkovskiy, Andrey
Haswell, Elizabeth S.
Lercher, Martin J.
Ehrhardt, David W.
Frommer, Wolf B.
Kleist, Thomas J.
author_facet Moe-Lange, Jacob
Gappel, Nicoline M.
Machado, Mackenzie
Wudick, Michael M.
Sies, Cosima S. A.
Schott-Verdugo, Stephan N.
Bonus, Michele
Mishra, Swastik
Hartwig, Thomas
Bezrutczyk, Margaret
Basu, Debarati
Farmer, Edward E.
Gohlke, Holger
Malkovskiy, Andrey
Haswell, Elizabeth S.
Lercher, Martin J.
Ehrhardt, David W.
Frommer, Wolf B.
Kleist, Thomas J.
author_sort Moe-Lange, Jacob
collection PubMed
description Glutamate has dual roles in metabolism and signaling; thus, signaling functions must be isolatable and distinct from metabolic fluctuations, as seen in low-glutamate domains at synapses. In plants, wounding triggers electrical and calcium (Ca(2+)) signaling, which involve homologs of mammalian glutamate receptors. The hydraulic dispersal and squeeze-cell hypotheses implicate pressure as a key component of systemic signaling. Here, we identify the stretch-activated anion channel MSL10 as necessary for proper wound-induced electrical and Ca(2+) signaling. Wound gene induction, genetics, and Ca(2+) imaging indicate that MSL10 acts in the same pathway as the glutamate receptor–like proteins (GLRs). Analogous to mammalian NMDA glutamate receptors, GLRs may serve as coincidence detectors gated by the combined requirement for ligand binding and membrane depolarization, here mediated by stretch activation of MSL10. This study provides a molecular genetic basis for a role of mechanical signal perception and the transmission of long-distance electrical and Ca(2+) signals in plants.
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spelling pubmed-84428882021-09-24 Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling Moe-Lange, Jacob Gappel, Nicoline M. Machado, Mackenzie Wudick, Michael M. Sies, Cosima S. A. Schott-Verdugo, Stephan N. Bonus, Michele Mishra, Swastik Hartwig, Thomas Bezrutczyk, Margaret Basu, Debarati Farmer, Edward E. Gohlke, Holger Malkovskiy, Andrey Haswell, Elizabeth S. Lercher, Martin J. Ehrhardt, David W. Frommer, Wolf B. Kleist, Thomas J. Sci Adv Biomedicine and Life Sciences Glutamate has dual roles in metabolism and signaling; thus, signaling functions must be isolatable and distinct from metabolic fluctuations, as seen in low-glutamate domains at synapses. In plants, wounding triggers electrical and calcium (Ca(2+)) signaling, which involve homologs of mammalian glutamate receptors. The hydraulic dispersal and squeeze-cell hypotheses implicate pressure as a key component of systemic signaling. Here, we identify the stretch-activated anion channel MSL10 as necessary for proper wound-induced electrical and Ca(2+) signaling. Wound gene induction, genetics, and Ca(2+) imaging indicate that MSL10 acts in the same pathway as the glutamate receptor–like proteins (GLRs). Analogous to mammalian NMDA glutamate receptors, GLRs may serve as coincidence detectors gated by the combined requirement for ligand binding and membrane depolarization, here mediated by stretch activation of MSL10. This study provides a molecular genetic basis for a role of mechanical signal perception and the transmission of long-distance electrical and Ca(2+) signals in plants. American Association for the Advancement of Science 2021-09-08 /pmc/articles/PMC8442888/ /pubmed/34516872 http://dx.doi.org/10.1126/sciadv.abg4298 Text en Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Moe-Lange, Jacob
Gappel, Nicoline M.
Machado, Mackenzie
Wudick, Michael M.
Sies, Cosima S. A.
Schott-Verdugo, Stephan N.
Bonus, Michele
Mishra, Swastik
Hartwig, Thomas
Bezrutczyk, Margaret
Basu, Debarati
Farmer, Edward E.
Gohlke, Holger
Malkovskiy, Andrey
Haswell, Elizabeth S.
Lercher, Martin J.
Ehrhardt, David W.
Frommer, Wolf B.
Kleist, Thomas J.
Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title_full Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title_fullStr Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title_full_unstemmed Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title_short Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
title_sort interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8442888/
https://www.ncbi.nlm.nih.gov/pubmed/34516872
http://dx.doi.org/10.1126/sciadv.abg4298
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