Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect

Elife. 2015 May 12:4:e05502. doi: 10.7554/eLife.05502.

Abstract

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.

Keywords: Nasonia; Oncopeltus; Tribolium; axis formation; developmental biology; evolutionary biology; gene regulatory networks; genomics; oncopeltus fasciatus; pattern formation; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Evolution
  • Body Patterning / genetics*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / classification
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Embryo, Nonmammalian
  • Gene Expression Regulation, Developmental*
  • Heteroptera / classification
  • Heteroptera / cytology
  • Heteroptera / embryology
  • Heteroptera / genetics*
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Models, Biological
  • Phylogeny
  • Signal Transduction / genetics*
  • Toll-Like Receptors / genetics*
  • Toll-Like Receptors / metabolism
  • Twist-Related Protein 1 / genetics
  • Twist-Related Protein 1 / metabolism
  • Zygote / cytology
  • Zygote / growth & development
  • Zygote / metabolism

Substances

  • Drosophila Proteins
  • Insect Proteins
  • Toll-Like Receptors
  • Twi protein, Drosophila
  • Twist-Related Protein 1
  • dpp protein, Drosophila
  • sog protein, Drosophila

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.