A caudal mRNA gradient controls posterior development in the wasp Nasonia

Eugenia C. Olesnicky, Ava E. Brent, Lori Tonnes, Megan Walker, Mary Anne Pultz, David Leaf, Claude Desplan

Research output: Contribution to journalArticle

Abstract

One of the earliest steps of embryonic development is the establishment of polarity along the anteroposterior axis. Extensive studies of Drosophila embryonic development have elucidated mechanisms for establishing polarity, while studies with other model systems have found that many of these molecular components are conserved through evolution. One exception is Bicoid, the master organizer of anterior development in Drosophila and higher dipterans, which is not conserved. Thus, the study of anteroposterior patterning in insects that lack Bicoid can provide insight into the evolution of the diversity of body plan patterning networks. To this end, we have established the long germ parasitic wasp Nasonia vitripennis as a model for comparative studies with Drosophila. Here we report that, in Nasonia, a gradient of localized caudal mRNA directs posterior patterning, whereas, in Drosophila, the gradient of maternal Caudal protein is established through translational repression by Bicoid of homogeneous caudal mRNA. Loss of caudal function in Nasonia results in severe segmentation defects. We show that Nasonia caudal is an activator of gap gene expression that acts far towards the anterior of the embryo, placing it atop a cascade of early patterning. By contrast, activation of gap genes in flies relies on redundant functions of Bicoid and Caudal, leading to a lack of dramatic action on gap gene expression: caudal instead plays a limited role as an activator of pair-rule gene expression. These studies, together with studies in short germ insects, suggest that caudal is an ancestral master organizer of patterning, and that its role has been reduced in higher dipterans such as Drosophila.

Original languageEnglish (US)
Pages (from-to)3973-3982
Number of pages10
JournalDevelopment
Volume133
Issue number20
DOIs
StatePublished - Oct 2006

Fingerprint

Wasps
Drosophila
Messenger RNA
Gene Expression
Embryonic Development
Insects
Body Patterning
Diptera
Transcriptional Activation
Embryonic Structures
Mothers
Proteins

Keywords

  • Caudal
  • Nasonia
  • Segmentation

ASJC Scopus subject areas

  • Anatomy
  • Cell Biology

Cite this

Olesnicky, E. C., Brent, A. E., Tonnes, L., Walker, M., Pultz, M. A., Leaf, D., & Desplan, C. (2006). A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development, 133(20), 3973-3982. https://doi.org/10.1242/dev.02576

A caudal mRNA gradient controls posterior development in the wasp Nasonia. / Olesnicky, Eugenia C.; Brent, Ava E.; Tonnes, Lori; Walker, Megan; Pultz, Mary Anne; Leaf, David; Desplan, Claude.

In: Development, Vol. 133, No. 20, 10.2006, p. 3973-3982.

Research output: Contribution to journalArticle

Olesnicky, EC, Brent, AE, Tonnes, L, Walker, M, Pultz, MA, Leaf, D & Desplan, C 2006, 'A caudal mRNA gradient controls posterior development in the wasp Nasonia', Development, vol. 133, no. 20, pp. 3973-3982. https://doi.org/10.1242/dev.02576
Olesnicky EC, Brent AE, Tonnes L, Walker M, Pultz MA, Leaf D et al. A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development. 2006 Oct;133(20):3973-3982. https://doi.org/10.1242/dev.02576
Olesnicky, Eugenia C. ; Brent, Ava E. ; Tonnes, Lori ; Walker, Megan ; Pultz, Mary Anne ; Leaf, David ; Desplan, Claude. / A caudal mRNA gradient controls posterior development in the wasp Nasonia. In: Development. 2006 ; Vol. 133, No. 20. pp. 3973-3982.
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