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Perturbation analysis of a multi-morphogen Turing reaction-diffusion stripe patterning system reveals key regulatory interactions.

ABSTRACT: Periodic patterning is widespread in development and can be modelled by reaction-diffusion (RD) processes. However, minimal two-component RD descriptions are vastly simpler than the multi-molecular events that actually occur and are often hard to relate to real interactions measured experimentally. Addressing these issues, we investigated the periodic striped patterning of the rugae (transverse ridges) in the mammalian oral palate, focusing on multiple previously implicated pathways: FGF, Hh, Wnt and BMP. For each, we experimentally identified spatial patterns of activity and distinct responses of the system to inhibition. Through numerical and analytical approaches, we were able to constrain substantially the number of network structures consistent with the data. Determination of the dynamics of pattern appearance further revealed its initiation by 'activators' FGF and Wnt, and 'inhibitor' Hh, whereas BMP and mesenchyme-specific-FGF signalling were incorporated once stripes were formed. This further limited the number of possible networks. Experimental constraint thus limited the number of possible minimal networks to 154, just 0.004% of the number of possible diffusion-driven instability networks. Together, these studies articulate the principles of multi-morphogen RD patterning and demonstrate the utility of perturbation analysis for constraining RD systems.This article has an associated 'The people behind the papers' interview.

SUBMITTER: Economou AD

PROVIDER: S-EPMC7648603 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Perturbation analysis of a multi-morphogen Turing reaction-diffusion stripe patterning system reveals key regulatory interactions.

Economou Andrew D AD Monk Nicholas A M NAM Green Jeremy B A JBA

Development (Cambridge, England) 20201029 20

Periodic patterning is widespread in development and can be modelled by reaction-diffusion (RD) processes. However, minimal two-component RD descriptions are vastly simpler than the multi-molecular events that actually occur and are often hard to relate to real interactions measured experimentally. Addressing these issues, we investigated the periodic striped patterning of the rugae (transverse ridges) in the mammalian oral palate, focusing on multiple previously implicated pathways: FGF, Hh, Wn ...[more]

PMID: 33033117

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Project description:Vascular tissue in plants provides a resource distribution network for water and nutrients that exhibits remarkable diversity in patterning among different species. In many succulent plants, the vascular network includes longitudinally-oriented supplemental vascular bundles (SVBs) in the central core of the succulent stems and roots in addition to the more typical zone of vascular tissue development (vascular cambium) in a cylinder at the periphery of the succulent organ. Plant SVBs evolved in over 38 plant families often in tandem with evolutionary increases in stem and root parenchyma storage tissue, so it is of interest to understand the evolutionary-developmental processes responsible for their recurrent evolution and patterning. Previous mathematical models have successfully recreated the two-dimensional vascular patterns in stem and root cross sections, but such models have yet to recreate three-dimensional vascular patterning. Here, a stochastic reaction-diffusion model of plant vascular bundle patterning is developed in an effort to highlight a potential mechanism of three dimensional patterning-Turing pattern formation coupled with longitudinal efflux of a regulatory molecule. A relatively simple model of four or five molecules recreated empirical SVB patterns and many other common vascular arrangements. SVBs failed to develop below a threshold width of parenchymatous tissues, suggesting a mechanism of evolutionary character loss due to changes in the spatial context in which development takes place. Altered diffusion rates of the modeled activator and substrate molecules affected the number and size of the simulated SVBs. This work provides a first mathematical model employing a stochastic Turing-type mechanism that recreates three dimensional vascular patterns seen in plant stems. The model offers predictions that can be tested using molecular-genetic approaches. Evolutionary-developmental ramifications concerning evolution of diffusion rates, organ size and geometry are discussed.

Dataset Information

Perturbation analysis of a multi-morphogen Turing reaction-diffusion stripe patterning system reveals key regulatory interactions.

Publications

Perturbation analysis of a multi-morphogen Turing reaction-diffusion stripe patterning system reveals key regulatory interactions.

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