A Re-examination of the Selection of the Sensory Organ Precursor of the Bristle Sensilla of Drosophila melanogaster

Abstract

The bristle sensillum of the imago of Drosophila is made of four cells that arise from a sensory organ precursor cell (SOP). This SOP is selected within proneural clusters (PNC) through a mechanism that involves Notch signalling. PNCs are defined through the expression domains of the proneural genes, whose activities enables cells to become SOPs. They encode tissue specific bHLH proteins that form functional heterodimers with the bHLH protein Daughterless (Da). In the prevailing lateral inhibition model for SOP selection, a transcriptional feedback loop that involves the Notch pathway amplifies small differences of proneural activity between cells of the PNC. As a result only one or two cells accumulate sufficient proneural activity to adopt the SOP fate. Most of the experiments that sustained the prevailing lateral inhibition model were performed a decade ago. We here re-examined the selection process using recently available reagents. Our data suggest a different picture of SOP selection. They indicate that a band-like region of proneural activity exists. In this proneural band the activity of the Notch pathway is required in combination with Emc to define the PNCs. We found a sub-group in the PNCs from which a pre-selected SOP arises. Our data indicate that most imaginal disc cells are able to adopt a proneural state from which they can progress to become SOPs. They further show that bristle formation can occur in the absence of the proneural genes if the function of emc is abolished. These results suggest that the tissue specific proneural proteins of Drosophila have a similar function as in the vertebrates, which is to determine the time of emergence and position of the SOP and to stabilise the proneural state.

The Canonical Notch Signaling Pathway: Structural and Biochemical Insights into Shape, Sugar, and Force

“…More recent work by Hunter et al suggests that differences in the level of signaling between SOP and its direct (cells that share apical contact) and indirect neighbors (cells in contact through filopodia) are important for ordered and timely progression of SOP patterning (Hunter et al, 2016). However, a recent paper by Troost et al (Troost et al, 2015) provides evidence against the filopodial model of SOP patterning, showing that only cells adjacent to the SOP receive inhibitory Notch signals. Hence, more direct evidence is needed to resolve this controversy.…”

Selection of cell fate in the organ of Corti involves the integration of Hes/Hey signaling at the Atoh1 promoter

“…*P<0.05. Drosophila notum (Troost et al, 2015). Here, the standard theory holds that small stochastic differences in proneural gene expression in single cells within a proneural cluster are amplified by strong Notch-mediated feedback to select them as SOPs (reviewed by Fortini, 2009).…”

“…Here, the standard theory holds that small stochastic differences in proneural gene expression in single cells within a proneural cluster are amplified by strong Notch-mediated feedback to select them as SOPs (reviewed by Fortini, 2009). However, in their re-evaluation of this system, Troost et al (2015) discovered that, similar to the situation in the cochlea, the proneural genes achaete and scute, which are involved in SOP selection, are first upregulated in a band of cells that crosses the proneural domain and are subsequently repressed in all but the SOP. Thus, although the mechanism by which SOPs are selected remains unknown, this re-evaluation recognizes that it is unlikely to be strictly stochastic.…”

Integration of Drosophila and Human Genetics to Understand Notch Signaling Related Diseases

“…Within the young proneural cluster, the expression level of AS-C, Sens and Notch signaling components are similar among the cells. However, at some time point during development, the equilibrium of Notch-Delta signaling becomes disrupted which is thought to be through a stochastic event[240–242]. When one cell receives less Notch signal, expression of E(spl) within this cell is reduced and Delta expression becomes derepressed.…”