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PLoS One. 2014 Apr 28;9(4):e95670. doi: 10.1371/journal.pone.0095670. eCollection 2014.

Biomechanics and the thermotolerance of development.

Author information

1
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America; Duke University Marine Laboratory, Beaufort, North Carolina, United States of America.
2
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
3
Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America; Department of Developmental Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America; Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.

Abstract

Successful completion of development requires coordination of patterning events with morphogenetic movements. Environmental variability challenges this coordination. For example, developing organisms encounter varying environmental temperatures that can strongly influence developmental rates. We hypothesized that the mechanics of morphogenesis would have to be finely adjusted to allow for normal morphogenesis across a wide range of developmental rates. We formulated our hypothesis as a simple model incorporating time-dependent application of force to a viscoelastic tissue. This model suggested that the capacity to maintain normal morphogenesis across a range of temperatures would depend on how both tissue viscoelasticity and the forces that drive deformation vary with temperature. To test this model we investigated how the mechanical behavior of embryonic tissue (Xenopus laevis) changed with temperature; we used a combination of micropipette aspiration to measure viscoelasticity, electrically induced contractions to measure cellular force generation, and confocal microscopy to measure endogenous contractility. Contrary to expectations, the viscoelasticity of the tissues and peak contractile tension proved invariant with temperature even as rates of force generation and gastrulation movements varied three-fold. Furthermore, the relative rates of different gastrulation movements varied with temperature: the speed of blastopore closure increased more slowly with temperature than the speed of the dorsal-to-ventral progression of involution. The changes in the relative rates of different tissue movements can be explained by the viscoelastic deformation model given observed viscoelastic properties, but only if morphogenetic forces increase slowly rather than all at once.

PMID:
24776615
PMCID:
PMC4002435
DOI:
10.1371/journal.pone.0095670
[Indexed for MEDLINE]
Free PMC Article

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