Maternal expression and early zygotic regulation of the Hox3/zen gene in the grasshopper Schistocerca gregaria

In insects, a key step in the early patterning of the egg is to distinguish the primordium of the embryo proper from those regions that will form extr a-embryonic membranes. In Drosophila, where these processes are well unders tood, the structure of the extra-embryonic membranes is highly derived. The distinct amnion and serosa typical of lower insects is replaced by a singl e. fused, and much reduced membrane, the amnioserosa, which never secretes an embryonic cuticle. We have used the Zen gene as a marker to study the formation of the extra-e mbryonic membranes, and other aspects of early embryonic patterning, in the grasshopper Schistocerca gregaria (African Plague Locust). Zen genes are d erived from Hox genes, but in Drosophila they appear to have lost any role in patterning the AIP axis of the embryo; instead, they are involved in D/V patterning and the specification of the extra-embryonic membranes. We show that the Schistocerca ten gene is expressed during embryogenesis in three distinct phases. The first of these is during cleavage, when Sgzen i s transiently expressed in all energids that reach the cell surface. The se cond phase of expression initiates in a ring of "necklace cells" that surro und the forming embryo, and demarcate the boundary between the amnion and s erosa. This leads to expression throughout the serosa. The final phase of e xpression is in the amnion, after this has separated from the serosa. This complex pattern implies that the role of Sgzen in Schistocerca is not limit ed solely to the specification of cell identity in the extra-embryonic memb ranes. We also report that the Schistocerca ten gene is expressed maternally, unli ke its Drosophila and Tribolium counterparts. A distinct maternal transcrip t, and maternal Zen protein, accumulate in the developing oocyte from early post-meiotic stages. They remain uniformly distributed in the oocyte cytop lasm until late vitellogenic stages, when the protein and RNA become somewh at concentrated at the egg cortex and in the posterior polar cap of the ooc yte, probably by passive exclusion from the yolk. The cytoplasmic localizat ion of Sgzen protein in the oocyte, and at some stages during embryogenesis , implies that nuclear exclusion of this transcription factor is specifical ly controlled.