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The brown algal mode of tip growth: Keeping stress under control

Tip growth has been studied in pollen tubes, root hairs, and fungal and oomycete hyphae and is the most widely distributed unidirectional growth process on the planet. It ensures spatial colonization, nutrient predation, fertilization, and symbiosis with growth speeds of up to 800 μm h(−1). Although...

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Autores principales: Rabillé, Hervé, Billoud, Bernard, Tesson, Benoit, Le Panse, Sophie, Rolland, Élodie, Charrier, Bénédicte
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6347293/
https://www.ncbi.nlm.nih.gov/pubmed/30640903
http://dx.doi.org/10.1371/journal.pbio.2005258
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author Rabillé, Hervé
Billoud, Bernard
Tesson, Benoit
Le Panse, Sophie
Rolland, Élodie
Charrier, Bénédicte
author_facet Rabillé, Hervé
Billoud, Bernard
Tesson, Benoit
Le Panse, Sophie
Rolland, Élodie
Charrier, Bénédicte
author_sort Rabillé, Hervé
collection PubMed
description Tip growth has been studied in pollen tubes, root hairs, and fungal and oomycete hyphae and is the most widely distributed unidirectional growth process on the planet. It ensures spatial colonization, nutrient predation, fertilization, and symbiosis with growth speeds of up to 800 μm h(−1). Although turgor-driven growth is intuitively conceivable, a closer examination of the physical processes at work in tip growth raises a paradox: growth occurs where biophysical forces are low, because of the increase in curvature in the tip. All tip-growing cells studied so far rely on the modulation of cell wall extensibility via the polarized excretion of cell wall–loosening compounds at the tip. Here, we used a series of quantitative measurements at the cellular level and a biophysical simulation approach to show that the brown alga Ectocarpus has an original tip-growth mechanism. In this alga, the establishment of a steep gradient in cell wall thickness can compensate for the variation in tip curvature, thereby modulating wall stress within the tip cell. Bootstrap analyses support the robustness of the process, and experiments with fluorescence recovery after photobleaching (FRAP) confirmed the active vesicle trafficking in the shanks of the apical cell, as inferred from the model. In response to auxin, biophysical measurements change in agreement with the model. Although we cannot strictly exclude the involvement of a gradient in mechanical properties in Ectocarpus morphogenesis, the viscoplastic model of cell wall mechanics strongly suggests that brown algae have evolved an alternative strategy of tip growth. This strategy is largely based on the control of cell wall thickness rather than fluctuations in cell wall mechanical properties.
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spelling pubmed-63472932019-02-01 The brown algal mode of tip growth: Keeping stress under control Rabillé, Hervé Billoud, Bernard Tesson, Benoit Le Panse, Sophie Rolland, Élodie Charrier, Bénédicte PLoS Biol Research Article Tip growth has been studied in pollen tubes, root hairs, and fungal and oomycete hyphae and is the most widely distributed unidirectional growth process on the planet. It ensures spatial colonization, nutrient predation, fertilization, and symbiosis with growth speeds of up to 800 μm h(−1). Although turgor-driven growth is intuitively conceivable, a closer examination of the physical processes at work in tip growth raises a paradox: growth occurs where biophysical forces are low, because of the increase in curvature in the tip. All tip-growing cells studied so far rely on the modulation of cell wall extensibility via the polarized excretion of cell wall–loosening compounds at the tip. Here, we used a series of quantitative measurements at the cellular level and a biophysical simulation approach to show that the brown alga Ectocarpus has an original tip-growth mechanism. In this alga, the establishment of a steep gradient in cell wall thickness can compensate for the variation in tip curvature, thereby modulating wall stress within the tip cell. Bootstrap analyses support the robustness of the process, and experiments with fluorescence recovery after photobleaching (FRAP) confirmed the active vesicle trafficking in the shanks of the apical cell, as inferred from the model. In response to auxin, biophysical measurements change in agreement with the model. Although we cannot strictly exclude the involvement of a gradient in mechanical properties in Ectocarpus morphogenesis, the viscoplastic model of cell wall mechanics strongly suggests that brown algae have evolved an alternative strategy of tip growth. This strategy is largely based on the control of cell wall thickness rather than fluctuations in cell wall mechanical properties. Public Library of Science 2019-01-14 /pmc/articles/PMC6347293/ /pubmed/30640903 http://dx.doi.org/10.1371/journal.pbio.2005258 Text en © 2019 Rabillé et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rabillé, Hervé
Billoud, Bernard
Tesson, Benoit
Le Panse, Sophie
Rolland, Élodie
Charrier, Bénédicte
The brown algal mode of tip growth: Keeping stress under control
title The brown algal mode of tip growth: Keeping stress under control
title_full The brown algal mode of tip growth: Keeping stress under control
title_fullStr The brown algal mode of tip growth: Keeping stress under control
title_full_unstemmed The brown algal mode of tip growth: Keeping stress under control
title_short The brown algal mode of tip growth: Keeping stress under control
title_sort brown algal mode of tip growth: keeping stress under control
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6347293/
https://www.ncbi.nlm.nih.gov/pubmed/30640903
http://dx.doi.org/10.1371/journal.pbio.2005258
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