A mathematical framework for understanding the spontaneous emergence of complexity applicable to growing multicellular systems.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238922 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7358 (Electronic) Linking ISSN: 1553734X NLM ISO Abbreviation: PLoS Comput Biol Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, [2005]-

Models, Biological* ; Gene Regulatory Networks*/genetics; Animals ; Caenorhabditis elegans/genetics ; Caenorhabditis elegans/embryology ; Caenorhabditis elegans/growth & development ; Cell Division/physiology ; Cell Division/genetics ; Computational Biology ; Embryonic Development/physiology ; Embryonic Development/genetics ; Cell Lineage ; Computer Simulation ; Gene Expression Regulation, Developmental/genetics

In embryonic development and organogenesis, cells sharing identical genetic codes acquire diverse gene expression states in a highly reproducible spatial distribution, crucial for multicellular formation and quantifiable through positional information. To understand the spontaneous growth of complexity, we constructed a one-dimensional division-decision model, simulating the growth of cells with identical genetic networks from a single cell. Our findings highlight the pivotal role of cell division in providing positional cues, escorting the system toward states rich in information. Moreover, we pinpointed lateral inhibition as a critical mechanism translating spatial contacts into gene expression. Our model demonstrates that the spatial arrangement resulting from cell division, combined with cell lineages, imparts positional information, specifying multiple cell states with increased complexity-illustrated through examples in C.elegans. This study constitutes a foundational step in comprehending developmental intricacies, paving the way for future quantitative formulations to construct synthetic multicellular patterns.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

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Date Created: 20240605 Date Completed: 20240617 Latest Revision: 20240619

20240619

PMC11182560

10.1371/journal.pcbi.1011882

38838038