Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis

• Published in: eLife Vol. 12
• Main Authors: Iyer, Krishnan S, Prabhakara, Chaitra, Mayor, Satyajit, Rao, Madan
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications, Ltd 06.03.2023; eLife Sciences Publications Ltd
• Subjects: Animals; Cell Differentiation; cellular compartmentalisation; Cognition; Developmental Biology; Drosophila melanogaster - genetics; Feedback Control; Morphogenesis; Physics of Living Systems; positional inference; receptor promiscuity; Signal Transduction; Feedback Control; morphogenesis; positional inference; cellular compartmentalisation; developmental biology; D. melanogaster; receptor promiscuity; physics of living systems
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/elife.79257

Precise spatial patterning of cell fate during morphogenesis requires accurate inference of cellular position. In making such inferences from morphogen profiles, cells must contend with inherent stochasticity in morphogen production, transport, sensing and signalling. Motivated by the multitude of signalling mechanisms in various developmental contexts, we show how cells may utilise multiple tiers of processing (compartmentalisation) and parallel branches (multiple receptor types), together with feedback control, to bring about fidelity in morphogenetic decoding of their positions within a developing tissue. By simultaneously deploying specific and nonspecific receptors, cells achieve a more accurate and robust inference. We explore these ideas in the patterning of wing imaginal disc by Wingless morphogen signalling, where multiple endocytic pathways participate in decoding the morphogen gradient. The geometry of the inference landscape in the high dimensional space of parameters provides a measure for robustness and delineates and directions. This distributed information processing at the scale of the cell highlights how local cell autonomous control facilitates global tissue scale design.