Cell wall dynamics stabilize tip growth in a filamentous fungus.
Hyphal tip growth allows filamentous fungi to colonize space, reproduce, or infect. It features remarkable morphogenetic plasticity including unusually fast elongation rates, tip turning, branching, or bulging. These shape changes are all driven from the expansion of a protective cell wall (CW) secr...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-01-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001981 |
| _version_ | 1797894840694865920 |
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| author | Louis Chevalier Mario Pinar Rémi Le Borgne Catherine Durieu Miguel A Peñalva Arezki Boudaoud Nicolas Minc |
| author_facet | Louis Chevalier Mario Pinar Rémi Le Borgne Catherine Durieu Miguel A Peñalva Arezki Boudaoud Nicolas Minc |
| author_sort | Louis Chevalier |
| collection | DOAJ |
| description | Hyphal tip growth allows filamentous fungi to colonize space, reproduce, or infect. It features remarkable morphogenetic plasticity including unusually fast elongation rates, tip turning, branching, or bulging. These shape changes are all driven from the expansion of a protective cell wall (CW) secreted from apical pools of exocytic vesicles. How CW secretion, remodeling, and deformation are modulated in concert to support rapid tip growth and morphogenesis while ensuring surface integrity remains poorly understood. We implemented subresolution imaging to map the dynamics of CW thickness and secretory vesicles in Aspergillus nidulans. We found that tip growth is associated with balanced rates of CW secretion and expansion, which limit temporal fluctuations in CW thickness, elongation speed, and vesicle amount, to less than 10% to 20%. Affecting this balance through modulations of growth or trafficking yield to near-immediate changes in CW thickness, mechanics, and shape. We developed a model with mechanical feedback that accounts for steady states of hyphal growth as well as rapid adaptation of CW mechanics and vesicle recruitment to different perturbations. These data provide unprecedented details on how CW dynamics emerges from material secretion and expansion, to stabilize fungal tip growth as well as promote its morphogenetic plasticity. |
| first_indexed | 2024-04-10T07:16:54Z |
| format | Article |
| id | doaj.art-06b690b00b0641b9b384db7cae5547c7 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-10T07:16:54Z |
| publishDate | 2023-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-06b690b00b0641b9b384db7cae5547c72023-02-25T05:30:55ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-01-01211e300198110.1371/journal.pbio.3001981Cell wall dynamics stabilize tip growth in a filamentous fungus.Louis ChevalierMario PinarRémi Le BorgneCatherine DurieuMiguel A PeñalvaArezki BoudaoudNicolas MincHyphal tip growth allows filamentous fungi to colonize space, reproduce, or infect. It features remarkable morphogenetic plasticity including unusually fast elongation rates, tip turning, branching, or bulging. These shape changes are all driven from the expansion of a protective cell wall (CW) secreted from apical pools of exocytic vesicles. How CW secretion, remodeling, and deformation are modulated in concert to support rapid tip growth and morphogenesis while ensuring surface integrity remains poorly understood. We implemented subresolution imaging to map the dynamics of CW thickness and secretory vesicles in Aspergillus nidulans. We found that tip growth is associated with balanced rates of CW secretion and expansion, which limit temporal fluctuations in CW thickness, elongation speed, and vesicle amount, to less than 10% to 20%. Affecting this balance through modulations of growth or trafficking yield to near-immediate changes in CW thickness, mechanics, and shape. We developed a model with mechanical feedback that accounts for steady states of hyphal growth as well as rapid adaptation of CW mechanics and vesicle recruitment to different perturbations. These data provide unprecedented details on how CW dynamics emerges from material secretion and expansion, to stabilize fungal tip growth as well as promote its morphogenetic plasticity.https://doi.org/10.1371/journal.pbio.3001981 |
| spellingShingle | Louis Chevalier Mario Pinar Rémi Le Borgne Catherine Durieu Miguel A Peñalva Arezki Boudaoud Nicolas Minc Cell wall dynamics stabilize tip growth in a filamentous fungus. PLoS Biology |
| title | Cell wall dynamics stabilize tip growth in a filamentous fungus. |
| title_full | Cell wall dynamics stabilize tip growth in a filamentous fungus. |
| title_fullStr | Cell wall dynamics stabilize tip growth in a filamentous fungus. |
| title_full_unstemmed | Cell wall dynamics stabilize tip growth in a filamentous fungus. |
| title_short | Cell wall dynamics stabilize tip growth in a filamentous fungus. |
| title_sort | cell wall dynamics stabilize tip growth in a filamentous fungus |
| url | https://doi.org/10.1371/journal.pbio.3001981 |
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