The brown algal mode of tip growth: Keeping stress under control
| Autor: | Bernard Billoud, Sophie Le Panse, Bénédicte Charrier, Hervé Rabillé, Elodie Rolland, Benoit Tesson |
|---|---|
| Přispěvatelé: | Reproduction et développement des plantes (RDP), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), University of California [San Diego] (UC San Diego), University of California (UC), Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Fédération de recherche de Roscoff (FR2424), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), University of California, Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-École normale supérieure - Lyon (ENS Lyon) |
| Jazyk: | angličtina |
| Rok vydání: | 2019 |
| Předmět: |
0301 basic medicine
Plant Science Pollen Tube [SDV.BC.BC]Life Sciences [q-bio]/Cellular Biology/Subcellular Processes [q-bio.SC] Plant Roots 0302 clinical medicine Cell Wall Electron Microscopy Biology (General) Microscopy biology Organic Compounds General Neuroscience Plant Anatomy Physics Eukaryota Light Microscopy Ectocarpus [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics Plants Chemistry Physical Sciences Pollen Pollen tube Cellular Structures and Organelles Plant Cell Walls Cellular Types General Agricultural and Biological Sciences Research Article Algae QH301-705.5 Fluorescence Recovery after Photobleaching [PHYS.PHYS.PHYS-BIO-PH]Physics [physics]/Physics [physics]/Biological Physics [physics.bio-ph] Plant Cell Biology Morphogenesis Biophysics Apical cell Root hair Research and Analysis Methods Phaeophyta Models Biological General Biochemistry Genetics and Molecular Biology Cell wall 03 medical and health sciences Cell Walls Plant Cells Tip growth Cellulose Cell Shape General Immunology and Microbiology Indoleacetic Acids Organic Chemistry Organisms Chemical Compounds Fluorescence recovery after photobleaching Biology and Life Sciences [SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis Cell Biology biology.organism_classification 030104 developmental biology Transmission Electron Microscopy 030217 neurology & neurosurgery |
| Zdroj: | PLoS Biology PLoS Biology, 2019, 17 (1), pp.e2005258. ⟨10.1371/journal.pbio.2005258⟩ PLoS Biology, Vol 17, Iss 1, p e2005258 (2019) PLoS Biology, Public Library of Science, 2019, 17 (1), pp.e2005258. ⟨10.1371/journal.pbio.2005258⟩ |
| ISSN: | 1544-9173 1545-7885 |
| DOI: | 10.1371/journal.pbio.2005258⟩ |
| Popis: | 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. Author summary Tip growth is known in organisms with filament-like structures, such as fungi (e.g., hyphae), plants (e.g., root hairs, moss protonemata), and algae (e.g., filamentous thalli). The driving force for growth in these organisms is the difference in osmotic pressure (turgor) between the inside of the cell and the external medium, a force contained by the cell wall. Physical laws imply that the higher the curvature of the cell, the lower the pressure (stress) perceived by the cell wall. Paradoxically, growth takes place at the dome-shaped cell apex, which has high curvature. Tip-growing cells studied so far (mainly plants) compensate the low wall stress in the apex by chemically loosening their cell wall. We studied Ectocarpus, which is a representative of brown algae, a eukaryotic branch very divergent from land plants, fungi, and green algae. We carried out a series of quantitative measurements at the cellular level and showed that the cell wall is thinner at the tip (36 nm) than on the shanks (170 to 500 nm). Using a viscoplastic model of cell wall expansion, we showed that the cell wall thickness gradient, together with dome curvature, generates sufficient wall stress to account for the observed growth pattern. |
| Databáze: | OpenAIRE |
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