Embryonic development of the nervous system in the planarian Schmidtea polychroa

Abstract

The development of a nervous system is a key innovation in the evolution of metazoans, which is illustrated by the presence of a common developmental toolkit for the formation of this organ system. Neurogenesis in the Spiralia, in particular the Platyhelminthes, is, however, poorly understood when compared with other animal groups. Here, we characterize embryonic neurogenesis in the freshwater flatworm Schmidtea polychroa and analyze the expression of soxB and a set of proneural bHLH genes, which are gene families with a well-established role in metazoan early neural development. We show that the nervous system is fully de novo assembled after the early embryo ingests the maternal nutrients. At early stages of neurogenesis, soxB1 genes are expressed in putative neural progenitor cells, whereas soxB2 and neural bHLH genes (achaete-scute, neuroD and beta3) are associated with late neurogenesis and the specification of neural subpopulations of the central and peripheral nervous system. Our findings are consistent with the role of proneural genes in other bilaterians, suggesting that the ancestral neural-specific gene regulatory network is conserved in triclads, despite exhibiting a divergent mode of development.

Nervous system development and regeneration in freshwater planarians

“…Some of these blastomeres are thought to differentiate into putative transient structures that include an epidermis and an embryonic pharynx for ingestion of the nutrient‐providing yolk cells . Within these early‐stage embryos, a primordial nervous system is generated that exhibits expression of conserved genes required for neurogenesis in other developmental model organisms . The primordial nervous system is speculated to be required for modulation of feeding behaviors essential for the early embryo to digest yolk cells, and is likely similar to the function of serotonergic neurons described in the pond snail embryo .…”

“…This time period also marks the emergence of the definitive CNS. Finally, during Stages 7 and 8 (days 10–15 development), the embryo acquires a body plan that resembles that of the adult organism, including a CNS with all of its basic components …”

“…By Stage 7 (just prior to hatching), a defined brain, ventral nerve cords, and the nerve net of the definitive pharynx are visible. (Modified and reprinted with permission from Ref . Copyright 2015 Elsevier)…”

Localization of planarian β-CATENIN-1 reveals multiple roles during anterior-posterior regeneration and organogenesis

“…To further investigate the distribution of β-CATENIN-1 during organogenesis, we characterized its localization in stage 5 embryos, which corresponds to the onset of de novo cell differentiation and early organogenesis during planarian embryonic development (Martín-Durán and Romero, 2011;Monjo and Romero, 2015). We detected a widespread distribution of β-CATENIN-1 throughout the entire embryo, and in particular in the presumptive anlagen of the definitive pharynx and brain, which at this stage appear as an anterior bilobed cluster of cells that are already positive for neural markers (Martín-Durán and Romero, 2011;Monjo and Romero, 2015) (Fig. 4C; Fig.…”

Diversification and biogeographic history of the Western Palearctic freshwater flatworm genusSchmidtea(Tricladida: Dugesiidae), with a redescription ofSchmidtea nova

“…It should be noted that occurrence of S. polychroa in North America is the result of human‐mediated dispersal (Ball, ; Benazzi & Benazzi‐Lentati, ). The species S. mediterranea is a model organism in regeneration research (Reddien & Alvarado, ; Rink, ) with a fully sequenced genome (Robb, Ross, & Alvarado, ; Grohme et al, ), while S. polychroa has been used as a model organism in studies on embryogenesis (Cardona, Hartenstein, & Romero, ; Monjo & Romero, ) and reproduction (D'Souza & Michiels, ; Pongratz, Storhas, Carranza, & Michiels, ). In comparison with these two model species, S. lugubris and S. nova are poorly studied.…”