Components of the dorsal-ventral pathway also contribute to anterior-posterior patterning in honeybee embryos (Apis mellifera)

Megan J Wilson,Peter K Dearden,Nathan J Kenny

doi:10.1186/2041-9139-5-11

Megan J Wilson, Peter K Dearden + Show 1 more

Open Access

https://doi.org/10.1186/2041-9139-5-11

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Abstract

BackgroundA key early step in embryogenesis is the establishment of the major body axes; the dorsal-ventral (DV) and anterior-posterior (AP) axes. Determination of these axes in some insects requires the function of different sets of signalling pathways for each axis. Patterning across the DV axis requires interaction between the Toll and Dpp/TGF-β pathways, whereas patterning across the AP axis requires gradients of bicoid/orthodenticle proteins and the actions of a hierarchy of gene transcription factors. We examined the expression and function of Toll and Dpp signalling during honeybee embryogenesis to assess to the role of these genes in DV patterning.ResultsPathway components that are required for dorsal specification in Drosophila are expressed in an AP-restricted pattern in the honeybee embryo, including Dpp and its receptor Tkv. Components of the Toll pathway are expressed in a more conserved pattern along the ventral axis of the embryo. Late-stage embryos from RNA interference (RNAi) knockdown of Toll and Dpp pathways had both DV and AP patterning defects, confirmed by staining with Am-sna, Am-zen, Am-eve, and Am-twi at earlier stages. We also identified two orthologues of dorsal in the honeybee genome, with one being expressed during embryogenesis and having a minor role in axis patterning, as determined by RNAi and the other expressed during oogenesis.ConclusionsWe found that early acting pathways (Toll and Dpp) are involved not only in DV patterning but also AP patterning in honeybee embryogenesis. Changes to the expression patterns and function of these genes may reflect evolutionary changes in the placement of the extra-embryonic membranes during embryogenesis with respect to the AP and DV axes.

Highlights

A key early step in embryogenesis is the establishment of the major body axes; the dorsal-ventral (DV) and anterior-posterior (AP) axes
Using the honeybee (Apis mellifera) model, we previously found that Dpp mRNA was maternally expressed and localized to the dorsal side of the oocyte, rather than the embryo, and the MAD pathway was activated in overlying follicle cells, implying that the Dpp-MAD pathway may pattern the DV axis of the oocyte, rather than the embryo [14]
We have previously shown that Am-Dpp is expressed maternally and that its mRNA is localized to dorsal regions of the oocyte [14], implying a possible early role in DV patterning during oogenesis

Summary

Introduction

A key early step in embryogenesis is the establishment of the major body axes; the dorsal-ventral (DV) and anterior-posterior (AP) axes Determination of these axes in some insects requires the function of different sets of signalling pathways for each axis. A critical early step in establishing the future body plan of any animal is the formation of the major body axes, the anterior-posterior axis (AP), and the dorsal-ventral axis (DV) Determination of these axes is established by an initial, often maternally driven, symmetry-breaking event, and as the process continues it requires precise zygotic control of gene expression across the body axes via cell-signalling pathways. Using the honeybee (Apis mellifera) model, we previously found that Dpp mRNA was maternally expressed and localized to the dorsal side of the oocyte, rather than the embryo, and the MAD pathway was activated in overlying follicle cells, implying that the Dpp-MAD pathway may pattern the DV axis of the oocyte, rather than the embryo [14]

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