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Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression

Despite the vital roles of jasmonoyl-isoleucine (JA-Ile) in governing plant growth and environmental acclimation, it remains unclear what intracellular processes lead to its induction. Here, we provide compelling genetic evidence that mechanical and osmotic regulation of turgor pressure represents a...

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Autores principales: Mielke, Stefan, Zimmer, Marlene, Meena, Mukesh Kumar, Dreos, René, Stellmach, Hagen, Hause, Bettina, Voiniciuc, Cătălin, Gasperini, Debora
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/PMC7875531/
https://www.ncbi.nlm.nih.gov/pubmed/33568489
http://dx.doi.org/10.1126/sciadv.abf0356
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author Mielke, Stefan
Zimmer, Marlene
Meena, Mukesh Kumar
Dreos, René
Stellmach, Hagen
Hause, Bettina
Voiniciuc, Cătălin
Gasperini, Debora
author_facet Mielke, Stefan
Zimmer, Marlene
Meena, Mukesh Kumar
Dreos, René
Stellmach, Hagen
Hause, Bettina
Voiniciuc, Cătălin
Gasperini, Debora
author_sort Mielke, Stefan
collection PubMed
description Despite the vital roles of jasmonoyl-isoleucine (JA-Ile) in governing plant growth and environmental acclimation, it remains unclear what intracellular processes lead to its induction. Here, we provide compelling genetic evidence that mechanical and osmotic regulation of turgor pressure represents a key elicitor of JA-Ile biosynthesis. After identifying cell wall mutant alleles in KORRIGAN1 (KOR1) with elevated JA-Ile in seedling roots, we found that ectopic JA-Ile resulted from cell nonautonomous signals deriving from enlarged cortex cells compressing inner tissues and stimulating JA-Ile production. Restoring cortex cell size by cell type–specific KOR1 complementation, by isolating a genetic kor1 suppressor, and by lowering turgor pressure with hyperosmotic treatments abolished JA-Ile signaling. Conversely, hypoosmotic treatment activated JA-Ile signaling in wild-type plants. Furthermore, constitutive JA-Ile levels guided mutant roots toward greater water availability. Collectively, these findings enhance our understanding on JA-Ile biosynthesis initiation and reveal a previously undescribed role of JA-Ile in orchestrating environmental resilience.
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spelling pubmed-78755312021-02-19 Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression Mielke, Stefan Zimmer, Marlene Meena, Mukesh Kumar Dreos, René Stellmach, Hagen Hause, Bettina Voiniciuc, Cătălin Gasperini, Debora Sci Adv Research Articles Despite the vital roles of jasmonoyl-isoleucine (JA-Ile) in governing plant growth and environmental acclimation, it remains unclear what intracellular processes lead to its induction. Here, we provide compelling genetic evidence that mechanical and osmotic regulation of turgor pressure represents a key elicitor of JA-Ile biosynthesis. After identifying cell wall mutant alleles in KORRIGAN1 (KOR1) with elevated JA-Ile in seedling roots, we found that ectopic JA-Ile resulted from cell nonautonomous signals deriving from enlarged cortex cells compressing inner tissues and stimulating JA-Ile production. Restoring cortex cell size by cell type–specific KOR1 complementation, by isolating a genetic kor1 suppressor, and by lowering turgor pressure with hyperosmotic treatments abolished JA-Ile signaling. Conversely, hypoosmotic treatment activated JA-Ile signaling in wild-type plants. Furthermore, constitutive JA-Ile levels guided mutant roots toward greater water availability. Collectively, these findings enhance our understanding on JA-Ile biosynthesis initiation and reveal a previously undescribed role of JA-Ile in orchestrating environmental resilience. American Association for the Advancement of Science 2021-02-10 /pmc/articles/PMC7875531/ /pubmed/33568489 http://dx.doi.org/10.1126/sciadv.abf0356 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/ 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 Research Articles
Mielke, Stefan
Zimmer, Marlene
Meena, Mukesh Kumar
Dreos, René
Stellmach, Hagen
Hause, Bettina
Voiniciuc, Cătălin
Gasperini, Debora
Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title_full Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title_fullStr Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title_full_unstemmed Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title_short Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
title_sort jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875531/
https://www.ncbi.nlm.nih.gov/pubmed/33568489
http://dx.doi.org/10.1126/sciadv.abf0356
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