Temporal integration of auxin information for the regulation of patterning

Positional information is essential for coordinating the development of multicellular organisms. In plants, positional information provided by the hormone auxin regulates rhythmic organ production at the shoot apex, but the spatio-temporal dynamics of auxin gradients is unknown. We used quantitative...

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Main Authors: Carlos S Galvan-Ampudia, Guillaume Cerutti, Jonathan Legrand, Géraldine Brunoud, Raquel Martin-Arevalillo, Romain Azais, Vincent Bayle, Steven Moussu, Christian Wenzl, Yvon Jaillais, Jan U Lohmann, Christophe Godin, Teva Vernoux
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-05-01
Series:eLife
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Online Access:https://elifesciences.org/articles/55832
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author Carlos S Galvan-Ampudia
Guillaume Cerutti
Jonathan Legrand
Géraldine Brunoud
Raquel Martin-Arevalillo
Romain Azais
Vincent Bayle
Steven Moussu
Christian Wenzl
Yvon Jaillais
Jan U Lohmann
Christophe Godin
Teva Vernoux
author_facet Carlos S Galvan-Ampudia
Guillaume Cerutti
Jonathan Legrand
Géraldine Brunoud
Raquel Martin-Arevalillo
Romain Azais
Vincent Bayle
Steven Moussu
Christian Wenzl
Yvon Jaillais
Jan U Lohmann
Christophe Godin
Teva Vernoux
author_sort Carlos S Galvan-Ampudia
collection DOAJ
description Positional information is essential for coordinating the development of multicellular organisms. In plants, positional information provided by the hormone auxin regulates rhythmic organ production at the shoot apex, but the spatio-temporal dynamics of auxin gradients is unknown. We used quantitative imaging to demonstrate that auxin carries high-definition graded information not only in space but also in time. We show that, during organogenesis, temporal patterns of auxin arise from rhythmic centrifugal waves of high auxin travelling through the tissue faster than growth. We further demonstrate that temporal integration of auxin concentration is required to trigger the auxin-dependent transcription associated with organogenesis. This provides a mechanism to temporally differentiate sites of organ initiation and exemplifies how spatio-temporal positional information can be used to create rhythmicity.
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spelling doaj.art-ec0ffbe557104faea3398566965c68dc2022-12-22T02:05:11ZengeLife Sciences Publications LtdeLife2050-084X2020-05-01910.7554/eLife.55832Temporal integration of auxin information for the regulation of patterningCarlos S Galvan-Ampudia0https://orcid.org/0000-0002-4779-3568Guillaume Cerutti1https://orcid.org/0000-0003-2003-9335Jonathan Legrand2Géraldine Brunoud3Raquel Martin-Arevalillo4Romain Azais5Vincent Bayle6Steven Moussu7Christian Wenzl8Yvon Jaillais9https://orcid.org/0000-0003-4923-883XJan U Lohmann10https://orcid.org/0000-0003-3667-187XChristophe Godin11https://orcid.org/0000-0002-1202-8460Teva Vernoux12https://orcid.org/0000-0002-8257-4088Laboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceDepartment of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, GermanyLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceDepartment of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, GermanyLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRAE, Inria, Lyon, FrancePositional information is essential for coordinating the development of multicellular organisms. In plants, positional information provided by the hormone auxin regulates rhythmic organ production at the shoot apex, but the spatio-temporal dynamics of auxin gradients is unknown. We used quantitative imaging to demonstrate that auxin carries high-definition graded information not only in space but also in time. We show that, during organogenesis, temporal patterns of auxin arise from rhythmic centrifugal waves of high auxin travelling through the tissue faster than growth. We further demonstrate that temporal integration of auxin concentration is required to trigger the auxin-dependent transcription associated with organogenesis. This provides a mechanism to temporally differentiate sites of organ initiation and exemplifies how spatio-temporal positional information can be used to create rhythmicity.https://elifesciences.org/articles/55832shoot apical meristemplant biologyAuxin
spellingShingle Carlos S Galvan-Ampudia
Guillaume Cerutti
Jonathan Legrand
Géraldine Brunoud
Raquel Martin-Arevalillo
Romain Azais
Vincent Bayle
Steven Moussu
Christian Wenzl
Yvon Jaillais
Jan U Lohmann
Christophe Godin
Teva Vernoux
Temporal integration of auxin information for the regulation of patterning
eLife
shoot apical meristem
plant biology
Auxin
title Temporal integration of auxin information for the regulation of patterning
title_full Temporal integration of auxin information for the regulation of patterning
title_fullStr Temporal integration of auxin information for the regulation of patterning
title_full_unstemmed Temporal integration of auxin information for the regulation of patterning
title_short Temporal integration of auxin information for the regulation of patterning
title_sort temporal integration of auxin information for the regulation of patterning
topic shoot apical meristem
plant biology
Auxin
url https://elifesciences.org/articles/55832
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