Cell wall dynamics stabilize tip growth in a filamentous fungus

PLoS Biol. 2023 Jan 17;21(1):e3001981. doi: 10.1371/journal.pbio.3001981. eCollection 2023 Jan.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aspergillus nidulans* / metabolism
  • Cell Wall
  • Hyphae*
  • Secretory Vesicles / metabolism

Grants and funding

This work was supported by grants from the "Fondation de la Recherche Médicale" (n°13171) to L.C., the "Spain’s Ministerio de Ciencia e Innovación" (grant RTI2018-093344-B100) and the "Comunidad de Madrid and he European Regional Development and European Social Funds" (grant S2017/BMD-3691) to M.A.P, the "La Ligue Contre le Cancer" (EL2021.LNCC/ NiM) and the "European Research Council" (ERC CoG “Forcaster” no. 647073) to N.M., as well as the "Agence Nationale pour la Recherche" (ANR, “CellWallSense” no. ANR-20-CE13-0003-02) to N.M. and A.B. "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript."