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Hydrodynamic stress and phenotypic plasticity of the zebrafish regenerating fin


Dagenais, Paule; Blanchoud, Simon; Pury, David; Pfefferli, Catherine; Aegerter-Wilmsen, Tinri; Aegerter, Christof M; Jaźwińska, Anna (2021). Hydrodynamic stress and phenotypic plasticity of the zebrafish regenerating fin. Journal of Experimental Biology, 224(15):jeb242309.

Abstract

Understanding how extrinsic factors modulate genetically encoded information to produce a specific phenotype is of prime scientific interest. In particular, the feedback mechanism between abiotic forces and locomotory organs during morphogenesis to achieve efficient movement is a highly relevant example of such modulation. The study of this developmental process can provide unique insights on the transduction of cues at the interface between physics and biology. Here, we take advantage of the natural ability of adult zebrafish to regenerate their amputated fins to assess its morphogenic plasticity upon external modulations. Using a variety of surgical and chemical treatments, we could induce phenotypic responses to the structure of the fin. Through the ablation of specific rays in regenerating caudal fins, we generated artificially narrowed appendages in which the fin cleft depth and the positioning of rays bifurcations were perturbed compared with normal regenerates. To dissect the role of mechanotransduction in this process, we investigated the patterns of hydrodynamic forces acting on the surface of a zebrafish fin during regeneration by using particle tracking velocimetry on a range of biomimetic hydrofoils. This experimental approach enabled us to quantitatively compare hydrodynamic stress distributions over flapping fins of varying sizes and shapes. As a result, viscous shear stress acting on the distal margin of regenerating fins and the resulting internal tension are proposed as suitable signals for guiding the regulation of ray growth dynamics and branching pattern. Our findings suggest that mechanical forces are involved in the fine-tuning of the locomotory organ during fin morphogenesis.

Abstract

Understanding how extrinsic factors modulate genetically encoded information to produce a specific phenotype is of prime scientific interest. In particular, the feedback mechanism between abiotic forces and locomotory organs during morphogenesis to achieve efficient movement is a highly relevant example of such modulation. The study of this developmental process can provide unique insights on the transduction of cues at the interface between physics and biology. Here, we take advantage of the natural ability of adult zebrafish to regenerate their amputated fins to assess its morphogenic plasticity upon external modulations. Using a variety of surgical and chemical treatments, we could induce phenotypic responses to the structure of the fin. Through the ablation of specific rays in regenerating caudal fins, we generated artificially narrowed appendages in which the fin cleft depth and the positioning of rays bifurcations were perturbed compared with normal regenerates. To dissect the role of mechanotransduction in this process, we investigated the patterns of hydrodynamic forces acting on the surface of a zebrafish fin during regeneration by using particle tracking velocimetry on a range of biomimetic hydrofoils. This experimental approach enabled us to quantitatively compare hydrodynamic stress distributions over flapping fins of varying sizes and shapes. As a result, viscous shear stress acting on the distal margin of regenerating fins and the resulting internal tension are proposed as suitable signals for guiding the regulation of ray growth dynamics and branching pattern. Our findings suggest that mechanical forces are involved in the fine-tuning of the locomotory organ during fin morphogenesis.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Physics Institute
Dewey Decimal Classification:530 Physics
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Life Sciences > Physiology
Life Sciences > Aquatic Science
Life Sciences > Animal Science and Zoology
Life Sciences > Molecular Biology
Life Sciences > Insect Science
Uncontrolled Keywords:Insect Science, Molecular Biology, Animal Science and Zoology, Aquatic Science, Physiology, Ecology, Evolution, Behavior and Systematics
Language:English
Date:1 August 2021
Deposited On:20 Dec 2021 11:18
Last Modified:16 Jun 2024 03:48
Publisher:Company of Biologists
ISSN:0022-0949
OA Status:Green
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1242/jeb.242309
Project Information:
  • : FunderSNSF
  • : Grant IDCRSII3_147675
  • : Project TitleFunctional plasticity: the role of hydrodynamics in ray branching during fin development and regeneration in zebrafish
  • : FunderSNSF
  • : Grant IDPZ00P3_173981
  • : Project TitleWhole-body regeneration in Botrylloides leachii
  • : FunderSNSF
  • : Grant ID310030_179213
  • : Project TitleRegenerative biology of zebrafish
  • : FunderNovartis Foundation
  • : Grant ID
  • : Project Title
  • : FunderForschungskredit, University of Zurich
  • : Grant ID
  • : Project Title
  • Content: Published Version