Abstract
Drosophila melanogaster head development represents a valuable process to study the developmental control of various organs, such as the antennae, the dorsal ocelli and the compound eyes from a common precursor, the eye-antennal imaginal disc. While the gene regulatory network underlying compound eye development has been extensively studied, the key transcription factors regulating the formation of other head structures from the same imaginal disc are largely unknown. We obtained the developmental transcriptome of the eye-antennal discs covering late patterning processes at the late 2nd larval instar stage to the onset and progression of differentiation at the end of larval development. We revealed the expression profiles of all genes expressed during eye-antennal disc development and we determined temporally co-expressed genes by hierarchical clustering. Since co-expressed genes may be regulated by common transcriptional regulators, we combined our transcriptome dataset with publicly available ChIP-seq data to identify central transcription factors that co-regulate genes during head development. Besides the identification of already known and well-described transcription factors, we show that the transcription factor Hunchback (Hb) regulates a significant number of genes that are expressed during late differentiation stages. We confirm that hb is expressed in two polyploid subperineurial glia cells (carpet cells) and a thorough functional analysis shows that loss of Hb function results in a loss of carpet cells in the eye-antennal disc. Additionally, we provide for the first time functional data indicating that carpet cells are an integral part of the blood-brain barrier. Eventually, we combined our expression data with a de novo Hb motif search to reveal stage specific putative target genes of which we find a significant number indeed expressed in carpet cells.
Highlights
The development of complex organs is often accompanied by extensive cell- and tissue rearrangements
To identify the genes expressed during D. melanogaster eye-antennal disc development and their expression dynamics, we performed RNA-seq on this tissue at three larval stages covering the process of retinal differentiation that is marked by the progression of the morphogenetic furrow
In a Gene Ontology (GO) term analysis, we only found two terms associated with the search term “sex”, namely “sex differentiation” (GO:0007548; padj = 5.35e-5; 47 genes) and “dosage compensation” (GO:0007549; padj = 2.61e-3; 15 genes) among those genes that were higher expressed at 96h AEL
Summary
The development of complex organs is often accompanied by extensive cell- and tissue rearrangements. Simple cells undergo profound morphological changes such as extensive cell fusions of muscle precursor cells to form syncytial muscle fibers [1] or the formation of highly polarized neurons from initially uniform neuroectodermal cells [2,3] Other cell types, such as germ cells, first migrate long distances before coming to rest in the developing gonads [4]. The adult D. melanogaster head is composed of the compound eyes (the main visual system), the three dorsal ocelli, the antennae, the ventral mouthparts and the head capsule that connects these organs and encloses the brain [11] Most of these structures develop during larval stages from eye-antennal imaginal discs, which originate from about 20 cells that are specified at embryonic stages [12,13,14]. At the same time when the retinal part of the disc and the antennal region separate during the early L2 stage, the maxillary palp is defined in the ventral portion of the antennal part [25,26,27]
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