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Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia

Abstract

The Bicoid (Bcd) gradient in Drosophila has long been a model for the action of a morphogen in establishing embryonic polarity1. However, it is now clear that bcd is a unique feature of higher Diptera2,3. An evolutionarily ancient gene, orthodenticle (otd), has a bcd-like role in the beetle Tribolium4. Unlike the Bcd gradient, which arises by diffusion of protein from an anteriorly localized messenger RNA1,5, the Tribolium Otd gradient forms by translational repression of otd mRNA by a posteriorly localized factor. These differences in gradient formation are correlated with differences in modes of embryonic patterning. Drosophila uses long germ embryogenesis, where the embryo derives from the entire anterior–posterior axis, and all segments are patterned at the blastoderm stage, before gastrulation. In contrast, Tribolium undergoes short germ embryogenesis: the embryo arises from cells in the posterior of the egg, and only anterior segments are patterned at the blastoderm stage, with the remaining segments arising after gastrulation from a growth zone. Here we describe the role of otd in the long germband embryo of the wasp Nasonia vitripennis. We show that Nasonia otd maternal mRNA is localized at both poles of the embryo, and resulting protein gradients pattern both poles. Thus, localized Nasonia otd has two major roles that allow long germ development. It activates anterior targets at the anterior of the egg in a manner reminiscent of the Bcd gradient, and it is required for pre-gastrulation expression of posterior gap genes.

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Figure 1: otd1 expression and localization.
Figure 2: Effects of otd1 RNAi.
Figure 3: Models for patterning the blastoderm of insect model systems.

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Acknowledgements

We would like to thank the Desplan and Small laboratories for support during this work, and J. Blau, E. Mazzoni, E. Olesnicky, M. Siegal, S. Small, J. Treisman, D. Vasiliauskas and E. Wimmer for critical reading of this manuscript. This work was supported by a NIH grant to C.D; J.A.L. was supported by a NIH Training Grant and a Dean Dissertation Fellowship from NYU. This investigation was conducted in a facility constructed with support from a Research Facilities Improvement grant from NCRR, NIH. Author Contributions J.A.L. and C.D. conceived and designed the experiments. J.A.L. performed the experiments and generated data for the figures. A.E.B. cloned Nasonia giant and provided the probe. M.A.P. and D.S.L. cloned Nasonia hunchback, provided valuable reagents and were instrumental in initiating the project. J.A.L. and C.D. wrote the paper.

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Correspondence to Claude Desplan.

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The sequences reported here are deposited in GenBank under the following accession numbers: otd1, AY684810; ems, AY684808; giant, DQ250085. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1 and 2. Supplementary Figure 1 details the variable knockdown of Otd1 protein expression in otd1 RNAi. Supplementary Figure 2 details otd1 and hb RNAi synergy. (PDF 817 kb)

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This file contains text to accompany the above Supplementary Figures. (DOC 24 kb)

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Lynch, J., Brent, A., Leaf, D. et al. Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439, 728–732 (2006). https://doi.org/10.1038/nature04445

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