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

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.

Animal egg as evolutionary innovation: a solution to the “embryonic hourglass” puzzle

“…The composition, physics, and developmental roles of DPMs are described in detail in earlier publications (Newman and Bhat, 2008, 2009; Newman et al, 2009). Here, I note two points which are relevant for the proposed solution to the hourglass puzzle: (i) DPMs can organize cell aggregates without the need for any prespecification in the egg, and (ii) a given set of DPMs can produce slight variations on the same basic plan owing to their sensitivity to the initial and boundary conditions.…”

“…Choanozoan genomes also specify functional portions of the morphogen Hedgehog, as well as cell surface and intracellular components of the Notch pathway, which mediates lateral inhibition in metazoan embryos (King et al, 2008; Shalchian‐Tabrizi et al, 2008). Although lateral inhibition is an inherently multicellular function, the Notch pathway may have evolved in single‐celled organisms to perform the related role of influencing the choice between alternative cell states (Newman et al, 2009).…”

The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression

“…Plant and animal development is guided by transcriptional networks that control cell‐fate decisions in conjunction with dynamic patterning modules, such as those that regulate the differential distribution (gradients) of hormones (Davidson and Erwin, 2006; Newman et al , 2009). Establishing the molecular links between such networks and hormone or nutrient distribution is a key for understanding cell patterning.…”

“…Establishing the molecular links between such networks and hormone or nutrient distribution is a key for understanding cell patterning. Our current comprehension of how these two types of processes are linked spatially and temporally in vivo is limited (Newman et al , 2009).…”

Dynamic Paleontology

“…Cell-cell adhesion dynamic patterning modules are essential for animalian multicellularity Newman et al 2009). The expression of cell-cell adhesion (ADH/DAD) dynamical patterning module (DPM) effects decreased over time in the Kiwetinokia lineage.…”