Axis Patterning by BMPs: Cnidarian Network Reveals Evolutionary Constraints

• Published in: Cell reports (Cambridge) 2015-03, Vol.10 (10), p.1646-1654
• Main Authors: Genikhovich, Grigory, Fried, Patrick, Prünster, M. Mandela, Schinko, Johannes B., Gilles, Anna F., Fredman, David, Meier, Karin, Iber, Dagmar, Technau, Ulrich
• Format: Article
• Language: English
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2015.02.035

BMP signaling plays a crucial role in the establishment of the dorso-ventral body axis in bilaterally symmetric animals. However, the topologies of the bone morphogenetic protein (BMP) signaling networks vary drastically in different animal groups, raising questions about the evolutionary constraints and evolvability of BMP signaling systems. Using loss-of-function analysis and mathematical modeling, we show that two signaling centers expressing different BMPs and BMP antagonists maintain the secondary axis of the sea anemone Nematostella. We demonstrate that BMP signaling is required for asymmetric Hox gene expression and mesentery formation. Computational analysis reveals that network parameters related to BMP4 and Chordin are constrained both in Nematostella and Xenopus, while those describing the BMP signaling modulators can vary significantly. Notably, only chordin, but not bmp4 expression needs to be spatially restricted for robust signaling gradient formation. Our data provide an explanation of the evolvability of BMP signaling systems in axis formation throughout Eumetazoa. [Display omitted] •A gradient of BMP signaling maintains the directive axis in Nematostella•BMP signaling regulates Nematostella Hox genes and patterns the endoderm•BMP network topology is similar in Nematostella and Xenopus•Constraint analysis reveals the evolvability of BMP network components Similar to Bilateria, anthozoans possess a secondary directive body axis. Genikhovich et al. examine the bone morphogenetic protein (BMP) signaling network required to compartmentalize the directive axis and regulate staggered Hox gene expression in a sea anemone. Mathematical modeling reveals the constraints guiding the evolution of the axis-forming BMP networks in animals.