Biology

The anti-neural role of BMP signaling is a consequence of its ancestral function in dorsoventral patterning

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This study challenges the established view that BMP signaling universally suppresses nervous system formation. Using transgenic reporters in the sea anemone Nematostella, jellyfish species, and the chaetognath Spadella, the researchers demonstrate that BMP signaling is active in neuronal populations across cnidarians and some bilaterians, and functions as a positive regulator of neuronal genes, including the neural progenitor marker soxB(2). The authors propose that BMP signaling ancestrally promoted neurogenesis, and that its well-documented "anti-neural" role in vertebrates and arthropods is a derived consequence of its broader function in dorsoventral ectodermal patterning.


Reframing the ancestral role of BMP signaling in nervous system development has implications for understanding how centralized nervous systems evolved across animal lineages, and may inform research on neural development and regenerative biology.


by Paul Knabl, June F. Ordoñez, Juan Daniel Montenegro Cabrera, Daniel Abed-Navandi, Roland Halbauer, Oliver Link, Tim Wollesen, Grigory Genikhovich

In Bilateria with centralized nervous systems (e.g., in vertebrates or arthropods), the minimum of the BMP signaling activity gradient defines the position of the central nervous system. BMP-dependent patterning of the secondary body axis is ancestral for Bilateria and possibly also for the bilaterian sister clade Cnidaria. However, the variety of levels of centralization of the nervous systems in Bilateria—from diffuse to fully centralized—as well as the lack of centralization of the nervous system in Cnidaria, suggest that BMP signaling cannot be perceived as a universally “anti-neural” signal. Here we use transgenic reporter lines in the anthozoan cnidarian Nematostella to show that BMP signaling is active in distinct neuronal populations. Moreover, attenuation of BMP signaling followed by RNA-Seq shows that BMP signaling is a positive regulator of many neuronal genes, including the top-tier neural progenitor marker soxB(2). Furthermore, we analyze BMP signaling activity in the cubozoan jellyfish Tripedalia and the scyphozoan jellyfish Stomolophus and prove that BMP signaling in parts of the diffuse nervous system is not an anthozoan but an ancestral cnidarian feature, shared by anthozoans and medusozoans. Finally, we show that the highly centralized ventral nervous system of the nonmodel spiralian, the chaetognath Spadella, forms out of paired BMP signaling-positive domains on the lateral sides of the embryo. Together, our data suggest that one of the ancestral roles of BMP signaling may have been in promoting neurogenesis. We propose that the “anti-neural” function of BMP signaling in vertebrates and arthropods is a consequence of its global role in the dorsoventral patterning of the ectoderm.

Source: The anti-neural role of BMP signaling is a consequence of its ancestral function in dorsoventral patterning