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Badyaev, A. V.

Publications and source records attributed to Badyaev, A. V..

4 recordsLinked to original sources

Subcellular compartmentalization expands the regulatory repertoire of a conserved developmental network

How can a conserved network orchestrate precise local outcomes across a wide array of developmental and ecological contexts during evolution? Flexible subcellular compartmentalization of multivalent proteins is a powerful, but understudied, driver of dynamic modularity in regulatory networks, defining an architecture in which context-sensing bridges between distributed subnetworks allow simultaneous access to alternative regulatory states. Here we construct one of the most complete atlases of avian beak morphogenesis and examine how subcellular compartmentalization modulates regulatory repertoire of the conserved protein network across hundreds of developmental contexts. We find that, in both jaws, the network is comprised of a hub of autoregulatory, context-sensing proteins whose links to a context-invariant core depends on subcellular colocalization. We show that proteins in this hub more than double the networks regulatory repertoire by unlocking latent coexpression states allowing concurrent tissue divergence. We demonstrate that in this architecture, specialization does not interfere with changeability, enabling a compact network to achieve remarkable tissue diversification and developmental expansion. The regulatory autonomy of the hub proteins and their ability to convert a wide range of inputs underpin robustness of developmental systems. Ultimately, such organization can reconcile ecological precision with the evolutionary lability evident in avian beak diversification.

evolutionary biology↗

Spatial and temporal coordination of signaling pathways in tissue differentiation: developmental atlas of protein expression during zebra finch beak maturation

BackgroundMorphogenesis depends on spatial and temporal coordination of signaling pathways, yet the colocalization of proteins across pathways remains poorly understood. Here we examine cellular and histological localization of regulatory proteins forming core craniofacial developmental pathways during beak morphogenesis of the zebra finch (Taeniopygia guttata). ResultsWe present an atlas of spatiotemporal coexpression of {beta}-catenin, Bmp4, CaM, Dkk3, Fgf8, Ihh, Tgf{beta}2, and Wnt4 across embryonic stages HH29-42 revealing both established and novel patterns of expression. Overall, in the earliest stages (HH29-32), most proteins show broad and overlapping expression across epithelial and mesenchymal tissues. By stage HH36, expression becomes increasingly compartmentalized, with pronounced differentiation among tissue types. Notably, at later stages, proteins showed tissue-specific distributions in boundary versus core regions of chondrogenic and osteogenic domains indicating coordinated cross-pathway patterning during cartilage and bone formation. ConclusionsOsteogenesis in the zebra finch beak is organized by coordinated signaling between boundary-associated cells and differentiating cores, with cross-pathway feedback establishing bone and cartilage differentiation while maintaining boundaries. Our results corroborated core elements of craniofacial signaling dynamics, while revealing unexpected subcellular localization for several proteins that showed regulatory complexity not captured by prior transcript-level maps. This atlas provides a protein-level baseline for comparative and mechanistic studies of beak morphogenesis.

developmental biology↗

Ultimate paths of least resistance: Intrinsically disordered links as developmental resets in regulatory protein networks

Development and evolution require both stability and adaptability, yet how these opposite properties are reconciled is unclear. Here, we show that intrinsically disordered proteins (IDPs) act as reset mechanisms in conserved regulatory networks facilitating developmental transitions by integrating physical processes with genetic regulation. By tracing the ontogeny of mesenchymal cells in avian beak primordia, we demonstrate that mechanosensitive IDPs mediate shifts between physical cell states via dosage-dependent binding plasticity, converting stochastic protein variation into discreet regulatory networks. The disorder-enabled connectivity in these proteins resets their regulatory specialization and promotes population divergence. Comparative analyses across avian proteomes confirm that binding plasticity in transcriptional IDPs drives their diverse regulatory associations and accelerates their evolution. By resetting specialized states in conserved regulatory networks, IDPs flexibly regulate developmental pathways and reconcile precision with evolvability.

evolutionary biology↗

Cell jamming transitions shape regulatory protein gradients and prime evolutionary divergence

A long-standing goal of evolutionary developmental biology is to identify the mechanisms underlying criticality of developmental transitions that allow processes governing individual cells scale up to the organism-level patterning. The viscoelastic properties of embryonic tissues imply collective cell behaviors, leading to the expectation that signaling networks should capitalize on the material properties of tissues, structuring morphogenesis around the spatial and temporal transitions that they induce. Here, we show that this interaction is evident even prior to tissue differentiation and is traceable to behavior of individual cells. In avian beak primordia, we find that fields of mesenchymal cells undergo cycles of local jamming dynamically modulating coordination of cell shape and movement. These cycles progressively alter the spatial reach of regulatory proteins, strongly expanding or restricting their gradients based on tissue mechanical state. Tissue-level gradients of proteins most sensitive to local cell jamming transitions also diverge the most across populations, priming tissue compartmentalization. These findings suggest that the material state transition is an effective interface for integration of stochastic physical processes and genetic regulation and is well placed to underlie criticality of developmental systems allowing local rules governing cell-state transitions scale up to tissue-level patterning. More broadly, our findings reveal how transient material transitions reset developmental trajectories and promote diversification while preserving robustness.

evolutionary biology↗