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Abstract
Forming the anterior-posterior (AP) body axis is a fundamental process during embryogenesis. In flies (Diptera), symmetry breaking along the AP axis requires anterior determinants (ADs) that differ between species. In Drosophila melanogaster, localized mRNA of bicoid serves as the AD. Once translated, the Bicoid protein competes with nucleosomes and initiates symmetry-breaking along the AP axis by promoting chromatin accessibility at the lociof segmentation genes that are required to pattern the anterior embryo. The ADs of other dipteran insects are encoded by transcription factor (TF) genes that are unrelated to Bicoid, and little is known about they function and if they act through a shared mechanism. This study uses a de novo assembly and annotation of the genome of the moth fly Clogmia albipunctata to investigate whether the AD of this species initiates symmetry breaking along the AP axis during zygotic genome activation at the level of chromatin accessibility. In Clogmia, a maternally expressed transcript isoform of the pair-rule segmentation gene odd-paired is localized in the anterior egg and has been co-opted as the AD. I first describe the dynamics of chromatin accessibility during the last nuclear cycles before gastrulation. I find that in Clogmia, similar to Drosophila, the chromatin landscape progressively opens throughout development encompassing widespread zygotic transcription. However, following their initial opening, many regions close at earlier nuclear cycles in Clogmia than when such widespread changes occur in Drosophila. I investigate how knockdown of the pioneer factor gene zelda affects the chromatin landscape in Clogmia and find that Clogmia’s zelda homolog is important for both opening and closing chromatin. I then show that maternal odd-paired activity promotes chromatin accessibility and anterior gene expression during the early phase of zygotic genome activation at Clogmia’s homeobrain and sloppy-paired loci. These loci differ from the key targets of Bicoid but given that homologs homeobrain and sloppy-paired have early anterior expression domains and function in head development in Drosophila and other insects, these genes may serve a more widely conserved role in the initiation of anterior pattern formation. I conclude that unrelated dipteran ADs initiate anterior-posterior axis-specification at the level of enhancer accessibility through distinct sets of target genes. My study motivates further investigation into how the network downstream of the primary AD targets converges in different dipteran species to yield the conserved segmented body plan.