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Cell state switching factors and dynamical patterning modules: complementary mediators of plasticity in development and evolution

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Abstract

Ancient metazoan organisms arose from unicellular eukaryotes that had billions of years of genetic evolution behind them. The transcription factor networks present in single-celled ancestors at the origin of the Metazoa (multicellular animals) were already capable of mediating the switching of the unicellular phenotype among alternative states of gene activity in response to environmental conditions. Cell differentiation, therefore, had its roots in phenotypic plasticity, with the ancient regulatory proteins acquiring new targets over time and evolving into the “developmental transcription factors” (DTFs) of the “developmental-genetic toolkit.” In contrast, the emergence of pattern formation and morphogenesis in the Metazoa had a different trajectory. Aggregation of unicellular metazoan ancestors changed the organisms’ spatial scale, leading to the first “dynamical patterning module” (DPM): cell-cell adhesion. Following this, other DPMs (defined as physical forces and processes pertinent to the scale of the aggregates mobilized by a set of toolkit gene products distinct from the DTFs), transformed simple cell aggregates into hollow, multilayered, segmented, differentiated and additional complex structures, with minimal evolution of constituent genes. Like cell differentiation, therefore, metazoan morphologies also originated from plastic responses of cells and tissues. Here we describe examples of DTFs and most of the important DPMs, discussing their complementary roles in the evolution of developmental mechanisms. We also provide recently characterized examples of DTFs in cell type switching and DPMs in morphogenesis of avian limb bud mesenchyme, an embryo-derived tissue that retains a high degree of developmental plasticity.

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Abbreviations

DPMs:

dynamical patterning modules

DTFs:

developmental transcription factors

ECM:

extracellular matrix

GRNs:

gene regulatory networks

PCP:

planar cell polarity

PPARγ:

Peroxisome proliferator-activated receptor gamma

UCP1:

uncoupling protein 1

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  1. Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY, 10595, USA

    Stuart A. Newman, Ramray Bhat & Nadejda V. Mezentseva

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  1. Stuart A. Newman
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Correspondence to Stuart A. Newman.

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This article, designated JBEP-1, is published in affiliation with the Embryo Projects ( http://embryo.asu.edu/index.php ), an international consortium of biologists, historians and philosophers of science that examines the changing scientific understanding of embryos.

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Newman, S.A., Bhat, R. & Mezentseva, N.V. Cell state switching factors and dynamical patterning modules: complementary mediators of plasticity in development and evolution. J Biosci 34, 553–572 (2009). https://doi.org/10.1007/s12038-009-0074-7

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