Organic self-organization: tissue symmetry breaking through the irreducible coupling of cell and supracellular structures

The use of the term ‘self-organization’ in the context of developmental biology has increased markedly in the last decade, reflecting a growing recognition that frameworks relying solely on codes or blueprints that “program” or puppeteer collective cell behavior have natural limits in capturing the full complexity and robustness of developmental processes. Our recent experimental work focusing on the emergence of patterns of adjacent cartilage and soft tissue from a field of limb progenitors has revealed the conceptual need to elaborate and clarify the particular ways organic systems self-organize that may be fundamentally distinct from physical self-organization. Physical self-organization, borrowing from studies of non-living systems, focuses on the local interaction of components that lead to higher-order patterns. In contrast, “organic” self-organization involves reciprocal or mutually constituting causal interactions between the parts (cell) and the whole (supracellular structure). This particular form of reciprocity between levels of organization provides an explanation for how tissues gain complexity that does not rely on established frameworks such as graded molecular control by secreted signals (e.g. morphogens). 

Recent publications:

Pfeifer CR, Shyer AE, Rodrigues AR. 2024. Creative processes during vertebrate organ morphogenesis: Biophysical self-organization at the supracellular scale. Curr Opin Cell Biol. 86: 102305.

Yang S, Palmquist KH, Nathan L, Pfeifer CR, Schultheiss PJ, Sharma A, Kam LC, Miller PW, Shyer AE, Rodrigues AR. 2023. Morphogens enable interacting supracellular phases that generate organ architecture. Science. 382: eadg5579.

Palmquist KH, Tiemann SF, Ezzeddine FL, Yang S, Pfeifer CR, Erzberger A, Rodrigues AR, Shyer AE. 2022. Reciprocal cell-ECM dynamics generate supracellular fluidity underlying spontaneous follicle patterning. Cell. 185: 1960–1973.