Ossification across scales guides emergent multifractal biomineral pattern in the skull

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Mohammadreza Bahadorian - , Max Planck Institute of Molecular Cell Biology and Genetics, Center for Systems Biology Dresden (CSBD) (Author)
  • Johanna Lattner - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Klea Abazaj - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Jacqueline Tabler - , Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Carl D. Modes - , Max Planck Institute of Molecular Cell Biology and Genetics, Center for Systems Biology Dresden (CSBD), Clusters of Excellence PoL: Physics of Life (Author)

Abstract

Cross-scale interactions underlying dynamic pattern formation are found throughout developing biological systems. One hallmark of such patterns is their emergence from conditions at smaller scales. Here, we employ fluctuation analyses and multifractal methods to quantify the contribution of different processes involved in cross-scale patterning of mineralization during flat bone development of the skull. We develop a minimal stochastic generative model capable of accurately recapitulating qualitative features of the imaging data from alizarin red-stained embryos. To provide a quantitative metric of model-generated and in vivo pattern features, we tailored multifractal analyses to frontal bones, focusing on the degree of multifractality and the spatial distribution of singularities causing such multifractality. Our minimal model highlights the crucial role of collagen density in mineral pattern establishment and predicts the existence of a sharp boundary in pattern complexity. To validate our theoretical model, we chemically perturbed collagen fiber organization at the nanoscale. We find a decrease in the variety of singularities that mapped to our imaging data, accompanied by an impaired biomineral pattern at the mesoscale consistent with predictions made by our minimal model. Ultimately, our approach has the potential to help understand complex cross-scale pattern-forming systems in biological contexts and beyond.

Details

Original languageEnglish
Article number100161
JournalNewton
Volume1
Issue number5
Publication statusPublished - 7 Jul 2025
Peer-reviewedYes

Keywords

Keywords

  • biomineralization, collagen, intramembranous bone, mesenchyme, morphogenesis, multifractality, multiscale, multiscale fluctuation analysis, pattern description, wavelet transform