Unsupervised spatiotemporal classification of deformation patterns of embryonic tissues matches their fate map
David Pastor-Escuredo,
Benoît Lombardot,
Thierry Savy,
Adeline Boyreau,
René Doursat,
Jose M. Goicolea,
Andrés Santos,
Paul Bourgine,
Juan C. del Álamo,
María J. Ledesma- Carbayo,
Nadine Peyriéras
Affiliations
David Pastor-Escuredo
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France; Biomedical Image Technologies, ETSIT, Universidad Politécnica de Madrid, 28040 Madrid, Spain; Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain; Corresponding author
Benoît Lombardot
UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
Thierry Savy
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France; UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France; Matières et Systèmes Complexes (MSC) UMR7057, CNRS, Université Paris Cité, 10 rue Alice Domon et Léonie Duquet, 75013 Paris, France
Adeline Boyreau
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France
René Doursat
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France; UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France
Jose M. Goicolea
Computational Mechanics Group, Universidad Politécnica de Madrid, 28040 Madrid, Spain
Andrés Santos
Biomedical Image Technologies, ETSIT, Universidad Politécnica de Madrid, 28040 Madrid, Spain; Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain
Paul Bourgine
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France; UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France; Matières et Systèmes Complexes (MSC) UMR7057, CNRS, Université Paris Cité, 10 rue Alice Domon et Léonie Duquet, 75013 Paris, France
Juan C. del Álamo
Mechanical and Aerospace Engineering Department, University of California San Diego, La Jolla, CA 92093, USA; Mechanical Engineering Department, University of Washington, Seattle, WA 98195, USA; Center for Cardiovascular Biology, University of Washington, Seattle, WA 98109, USA
María J. Ledesma- Carbayo
Biomedical Image Technologies, ETSIT, Universidad Politécnica de Madrid, 28040 Madrid, Spain; Biomedical Research Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain; Corresponding author
Nadine Peyriéras
USR3695/FRE2039 BioEmergences, CNRS, Paris-Saclay University, Gif-sur-Yvette, France; UPS3611 Complex Systems Institute Paris Ile-de-France (ISC-PIF), CNRS, Paris, France; Matières et Systèmes Complexes (MSC) UMR7057, CNRS, Université Paris Cité, 10 rue Alice Domon et Léonie Duquet, 75013 Paris, France; Corresponding author
Summary: During morphogenesis, embryonic tissues display fluid-like behavior with fluctuating strain rates. Digital cell lineages reconstructed from 4D images of developing zebrafish embryos are used to infer representative tissue deformation patterns and their association with developmental events. Finite deformation analysis along cell trajectories and unsupervised machine learning are applied to obtain reduced-order models condensing the collective cell motions, delineating tissue domains with distinct 4D biomechanical behavior. This reduced-order kinematic description is reproducible across specimens and matches fate maps of the zebrafish brain in wild-type and nodal pathway mutants (zoeptz57/tz57), shedding light into the morphogenetic defects causing these mutants’ cyclopia. Furthermore, the inferred kinematic maps also match expression maps of the gene transcription factor goosecoid (gsc). In summary, this work introduces an objective analytical framework to systematically unravel the complex spatiotemporal patterns of embryonic tissue deformations and couple them with cell fate and gene expression maps.