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Periodic spatial patterning with a single morphogen

Wang, Sheng and Garcia-Ojalvo, Jordi and Elowitz, Michael B. (2022) Periodic spatial patterning with a single morphogen. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20220328-182609385

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Abstract

Multicellular development employs periodic spatial patterning to generate repetitive structures such as digits, vertebrae, and teeth. Turing patterning has long provided a key paradigm for understanding such systems. The simplest Turing systems are believed to require at least two signals, or morphogens, that diffuse and react to spontaneously generate periodic patterns. Here, using mathematical modeling, we show that a minimal circuit comprising an intracellular positive feedback loop and a single diffusible morphogen is sufficient to generate stable, long-range spatially periodic cellular patterns. The model considers cells as discrete entities as a key feature, and incorporates transient boundary conditions. Linear stability analysis reveals that this single-morphogen Turing circuit can support a broad range of spatial wavelengths, including fine-grain patterns similar to those generated by classic lateral inhibition systems. Further, signals emanating from a boundary can initiate and stabilize propagating modes with a well-defined spatial wavelength. Once formed, patterns are self-sustaining and robust to noise. Finally, while noise can disrupt patterning in pre-patterned regions, its disruptive effect can be overcome by a bistable intracellular circuit loop, or by considering patterning in the context of growing tissue. Together, these results show that a single morphogen can be sufficient for robust spatial pattern formation, and should provide a foundation for engineering pattern formation in the emerging field of synthetic developmental biology.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2022.03.21.484932DOIDiscussion Paper
https://doi.org/10.22002/D1.20060DOICode
ORCID:
AuthorORCID
Garcia-Ojalvo, Jordi0000-0002-3716-7520
Elowitz, Michael B.0000-0002-1221-0967
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This version posted March 22, 2022. MBE is a Howard Hughes Medical Institute Investigator. This research was supported by the Allen Discovery Center program under Award No. UWSC10142, a Paul G. Allen Frontiers Group advised program of the Paul G. Allen Family Foundation. J.G.O. was supported by the Spanish Ministry of Science and Innovation and FEDER, under project PGC2018-101251-B-I00, by the “Maria de Maeztu” Programme for Units of Excellence in R&D (grant CEX2018-000792-M), and by the Generalitat de Catalunya (ICREA Academia programme). We acknowledge insightful feedback from Elowitz lab members. The authors have declared that no competing interests exist. Author contributions: Conceptualization and Investigation: S.W., J.G-O, M.B.E.; Formal Analysis, Software, and Visualization: S.W.; Writing: S.W., J.G-O, M.B.E. Code reporting: Simulation code and data is accessible from CaltechDATA. Wang, S., García-Ojalvo, J., & Elowitz, M. B. (2022). Periodic spatial patterning with a single morphogen (Version 1.0) [Data set]. CaltechDATA. https://doi.org/10.22002/D1.20060
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Paul G. Allen Frontiers GroupUWSC10142
Paul G. Allen Family FoundationUNSPECIFIED
Ministerio de Ciencia e Innovación (MCINN)PGC2018-101251-B-I00
Fondo Europeo de Desarrollo Regional (FEDER)UNSPECIFIED
Maria de MaeztuCEX2018-000792-M
Generalitat de CatalunyaUNSPECIFIED
DOI:10.1101/2022.03.21.484932
Record Number:CaltechAUTHORS:20220328-182609385
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220328-182609385
Official Citation:Periodic spatial patterning with a single morphogen. Sheng Wang, Jordi Garcia-Ojalvo, Michael B. Elowitz. bioRxiv 2022.03.21.484932; doi: https://doi.org/10.1101/2022.03.21.484932
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114102
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:28 Mar 2022 21:23
Last Modified:28 Mar 2022 21:23

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