Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect
Lena Sachs,
Yen-Ta Chen,
Axel Drechsler,
Jeremy A Lynch,
Kristen A Panfilio,
Michael Lässig,
Johannes Berg,
Siegfried Roth
Affiliations
Lena Sachs
Institute for Developmental Biology, University of Cologne, Köln, Germany
Yen-Ta Chen
Institute for Developmental Biology, University of Cologne, Köln, Germany
Axel Drechsler
Institute for Developmental Biology, University of Cologne, Köln, Germany; Bundesministerium für Umwelt, Naturschutz, Bau und Reaktorsicherheit, Bonn, Germany
Jeremy A Lynch
Institute for Developmental Biology, University of Cologne, Köln, Germany; Department of Biological Sciences, University of Illinois at Chicago, Chicago, United States
Kristen A Panfilio
Institute for Developmental Biology, University of Cologne, Köln, Germany
Michael Lässig
Institute for Theoretical Physics, University of Cologne, Cologne, Germany
Johannes Berg
Institute for Theoretical Physics, University of Cologne, Cologne, Germany
Siegfried Roth
Institute for Developmental Biology, University of Cologne, Köln, Germany
Toll-dependent patterning of the dorsoventral axis in Drosophila represents one of the best understood gene regulatory networks. However, its evolutionary origin has remained elusive. Outside the insects Toll is not known for a patterning function, but rather for a role in pathogen defense. Here, we show that in the milkweed bug Oncopeltus fasciatus, whose lineage split from Drosophila's more than 350 million years ago, Toll is only required to polarize a dynamic BMP signaling network. A theoretical model reveals that this network has self-regulatory properties and that shallow Toll signaling gradients are sufficient to initiate axis formation. Such gradients can account for the experimentally observed twinning of insect embryos upon egg fragmentation and might have evolved from a state of uniform Toll activity associated with protecting insect eggs against pathogens.
