A conserved transcriptional network regulates lamina development in the Drosophila visual system

Abstract

The visual system of insects is a multilayered structure composed externally by the compound eye and internally by the three ganglia of the optic lobe: lamina, medulla and the lobula complex. The differentiation of lamina neurons depends heavily on Hedgehog (Hh) signaling, which is delivered by the incoming photoreceptor axons, and occurs in a wave-like fashion. Despite the primary role of lamina neurons in visual perception, it is still unclear how these neurons are specified from neuroepithelial (NE) progenitors. Here we show that a homothorax (hth)-eyes absent (eya)-sine oculis (so)-dachshund (dac) gene regulatory cassette is involved in this specification. Lamina neurons differentiate from NE progenitors that express hth, eya and so. One of the first events in the differentiation of lamina neurons is the upregulation of dac expression in response to Hh signaling. We show that this dac upregulation, which marks the transition from NE progenitors into lamina precursors, also requires Eya/So, the expression of which is locked in by mutual feedback. dac expression is crucial for lamina differentiation because it ensures repression of hth, a negative regulator of single-minded, and thus dac allows further lamina neuron differentiation. Therefore, the specification of lamina neurons is controlled by coupling the cell-autonomous hth-eya-so-dac regulatory cassette to Hh signaling.

Spatio-temporal pattern of neuronal differentiation in the Drosophila visual system: A user’s guide to the dynamic morphology of the developing optic lobe

“…This was shown in several previous studies for the OPC, which gives rise to the neurons of the lamina and medulla in a strict posterior-to-anterior and medial-to-lateral order, respectively (Piñeiro et al, 2014; Ngo et al, 2010; Yasugi et al, 2008; Egger et al, 2007; Meinertzhagen and Hanson, 1993; Hofbauer and Campos-Ortega, 1990). A similar order is observed in the IPCl (Fig.…”

“…The original position of immature neurons in the larval optic lobe primordium is determined by the position of its progenitor, as well as its date of birth (Piñeiro et al, 2014; Li et al, 2013a; Li et al, 2013b; Suzuki et al, 2013; Hasegawa et al, 2011). This relationship has been investigated in detail for the OPC, but, as shown above (see Fig.…”

A Unique Class of Neural Progenitors in the Drosophila Optic Lobe Generates Both Migrating Neurons and Glia

“…It is required for lamina neurogenesis (Chotard et al, 2005). gcm-Gal4 expression overlapped with Eya, which is also strongly expressed in cells in this region (Piñeiro et al, 2014) (Figure S2B). gcm-Gal4 G-trace marked Hth + Eya + cells that could be observed moving away from the lateral neuroepithelium and toward the region of the medulla where Lawfs are located at larval stages (Figure 2G).…”

Pa2G4 is a novel Six1 co-factor that is required for neural crest and otic development

“…SO has been studied in great detail because it is a major player in the formation of the Drosophila visual system (Cheyette et al, 1994; Blanco et al, 2010; Piñeiro et al, 2014; Serikaku and O'Tousa, 1994; Hayashi et al, 2008; Pauli et al, 2005; Pignoni et al, 1997; Yan et al, 2003; Zhang et al, 2006; Zhou et al, 2014). All SO/Six proteins contain a highly conserved Six-type home-odomain, which binds DNA, and an N-terminal domain called the Six domain (SD) (Fig.…”