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Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots

Wound healing in plant tissues, consisting of rigid cell wall-encapsulated cells, represents a considerable challenge and occurs through largely unknown mechanisms distinct from those in animals. Owing to their inability to migrate, plant cells rely on targeted cell division and expansion to regener...

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Autores principales: Hoermayer, Lukas, Montesinos, Juan Carlos, Marhava, Petra, Benková, Eva, Yoshida, Saiko, Friml, Jiří
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7334516/
https://www.ncbi.nlm.nih.gov/pubmed/32541049
http://dx.doi.org/10.1073/pnas.2003346117
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author Hoermayer, Lukas
Montesinos, Juan Carlos
Marhava, Petra
Benková, Eva
Yoshida, Saiko
Friml, Jiří
author_facet Hoermayer, Lukas
Montesinos, Juan Carlos
Marhava, Petra
Benková, Eva
Yoshida, Saiko
Friml, Jiří
author_sort Hoermayer, Lukas
collection PubMed
description Wound healing in plant tissues, consisting of rigid cell wall-encapsulated cells, represents a considerable challenge and occurs through largely unknown mechanisms distinct from those in animals. Owing to their inability to migrate, plant cells rely on targeted cell division and expansion to regenerate wounds. Strict coordination of these wound-induced responses is essential to ensure efficient, spatially restricted wound healing. Single-cell tracking by live imaging allowed us to gain mechanistic insight into the wound perception and coordination of wound responses after laser-based wounding in Arabidopsis root. We revealed a crucial contribution of the collapse of damaged cells in wound perception and detected an auxin increase specific to cells immediately adjacent to the wound. This localized auxin increase balances wound-induced cell expansion and restorative division rates in a dose-dependent manner, leading to tumorous overproliferation when the canonical TIR1 auxin signaling is disrupted. Auxin and wound-induced turgor pressure changes together also spatially define the activation of key components of regeneration, such as the transcription regulator ERF115. Our observations suggest that the wound signaling involves the sensing of collapse of damaged cells and a local auxin signaling activation to coordinate the downstream transcriptional responses in the immediate wound vicinity.
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spelling pubmed-73345162020-07-15 Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots Hoermayer, Lukas Montesinos, Juan Carlos Marhava, Petra Benková, Eva Yoshida, Saiko Friml, Jiří Proc Natl Acad Sci U S A Biological Sciences Wound healing in plant tissues, consisting of rigid cell wall-encapsulated cells, represents a considerable challenge and occurs through largely unknown mechanisms distinct from those in animals. Owing to their inability to migrate, plant cells rely on targeted cell division and expansion to regenerate wounds. Strict coordination of these wound-induced responses is essential to ensure efficient, spatially restricted wound healing. Single-cell tracking by live imaging allowed us to gain mechanistic insight into the wound perception and coordination of wound responses after laser-based wounding in Arabidopsis root. We revealed a crucial contribution of the collapse of damaged cells in wound perception and detected an auxin increase specific to cells immediately adjacent to the wound. This localized auxin increase balances wound-induced cell expansion and restorative division rates in a dose-dependent manner, leading to tumorous overproliferation when the canonical TIR1 auxin signaling is disrupted. Auxin and wound-induced turgor pressure changes together also spatially define the activation of key components of regeneration, such as the transcription regulator ERF115. Our observations suggest that the wound signaling involves the sensing of collapse of damaged cells and a local auxin signaling activation to coordinate the downstream transcriptional responses in the immediate wound vicinity. National Academy of Sciences 2020-06-30 2020-06-15 /pmc/articles/PMC7334516/ /pubmed/32541049 http://dx.doi.org/10.1073/pnas.2003346117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Hoermayer, Lukas
Montesinos, Juan Carlos
Marhava, Petra
Benková, Eva
Yoshida, Saiko
Friml, Jiří
Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title_full Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title_fullStr Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title_full_unstemmed Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title_short Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
title_sort wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7334516/
https://www.ncbi.nlm.nih.gov/pubmed/32541049
http://dx.doi.org/10.1073/pnas.2003346117
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