The analysis of body axis formation in the common house spider Parasteatoda tepidariorum

• Applicant: Dr. Matthias Pechmann
• Subject Area: Evolutionary Cell and Developmental Biology (Zoology) ; Developmental Biology
• Term: from 2012 to 2018
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 226588632

• Final Report Year: 2019

Final Report Abstract

Chelicerates are basally branching arthropods and belong to the second most species rich group of animals on this planet. The phylum includes horseshoe crabs, sea spiders and arachnids like spiders and scorpions. The best-established chelicerate model system for studying embryonic development is the common house spider "Parasteatoda tepidariorum". A crucial event during early chelicerate embryogenesis is the establishment of a radially symmetric disc shaped embryo, the germ-disc. While the rim of this disc will develop into anterior structures of the embryo, the centre of the disc will give rise to the posterior of the pider embryo. Chelicerates have evolved a specialized group of cells, the cumulus, which is required to break the radial symmetry of the early embryo. The cumulus functions as an organizing centre, and induces the formation of the dorsoventral body axis by secreting the ligand for the BMP receptor, Decapentaplegic. Also in vertebrate embryos like the frog, the BMP signaling pathway is involved in setting up the dorsoventral body axis and the cumulus of chelicerates can be considered as being analogous to the vertebrate organizer (e.g. Spemann organizer of amphibian embryos). One main goal of the project was to get a better understanding of germ-disc and cumulus formation in general. More specific, the project was intended to identify genes that are involved in setting up the main body axes in the spider and to identify genes that regulate cumulus specific gene expression. The combined use of inhibitors that prevent translation or interfere with the actin or microtubule cytoskeleton together with cell membrane markers revealed that the germ-disc forms from a regular blastoderm and that germ-disc and cumulus formation depend on the onset of zygotic transcription. Furthermore, we used next generation transcriptome sequencing and were able to identify novel genes that are involved in cumulus maintenance and migration. We found that the transcription factor Pt-Ets4 is required to keep cumulus cells in a cluster and is involved in activating the cumulus specific expression of genes like hunchback and twist. Finally, the overexpression of Pt-Ets4 is sufficient to drive cell delamination and cell migration in spider embryos.

Publications

• Formation of the germ-disc in spider embryos by a condensation-like mechanism. Front Zool. 2016;13:35
  Pechmann M
  
• Toll Genes Have an Ancestral Role in Axis Elongation. Curr Biol. 2016 Jun 20;26(12):1609–15
  Benton MA, Pechmann M, Frey N, Stappert D, Conrads KH, Chen Y-T, et al.
  
• A novel role for Ets4 in axis specification and cell migration in the spider Parasteatoda tepidariorum. Elife. 2017 Aug 29;6
  Pechmann M, Benton MA, Kenny NJ, Posnien N, Roth S
  
• Expression and function of the zinc finger transcription factor Sp6–9 in the spider Parasteatoda tepidariorum. Dev Genes Evol. 2017 Nov 7;1–12
  Königsmann T, Turetzek N, Pechmann M, Prpic N-M
  
• Molecular control of gut formation in the spider Parasteatoda tepidariorum. Genesis. 2017 May;55(5)
  Feitosa NM, Pechmann M, Schwager EE, Tobias-Santos V, McGregor AP, Damen WGM, et al.