Binary Cell Fate Decisions and Fate Transformation in the Drosophila Larval Eye

Abstract

The functionality of sensory neurons is defined by the expression of specific sensory receptor genes. During the development of the Drosophila larval eye, photoreceptor neurons (PRs) make a binary choice to express either the blue-sensitive Rhodopsin 5 (Rh5) or the green-sensitive Rhodopsin 6 (Rh6). Later during metamorphosis, ecdysone signaling induces a cell fate and sensory receptor switch: Rh5-PRs are re-programmed to express Rh6 and become the eyelet, a small group of extraretinal PRs involved in circadian entrainment. However, the genetic and molecular mechanisms of how the binary cell fate decisions are made and switched remain poorly understood. We show that interplay of two transcription factors Senseless (Sens) and Hazy control cell fate decisions, terminal differentiation of the larval eye and its transformation into eyelet. During initial differentiation, a pulse of Sens expression in primary precursors regulates their differentiation into Rh5-PRs and repression of an alternative Rh6-cell fate. Later, during the transformation of the larval eye into the adult eyelet, Sens serves as an anti-apoptotic factor in Rh5-PRs, which helps in promoting survival of Rh5-PRs during metamorphosis and is subsequently required for Rh6 expression. Comparably, during PR differentiation Hazy functions in initiation and maintenance of rhodopsin expression. Hazy represses Sens specifically in the Rh6-PRs, allowing them to die during metamorphosis. Our findings show that the same transcription factors regulate diverse aspects of larval and adult PR development at different stages and in a context-dependent manner.

Organization of the Drosophila larval visual circuit

“…Moreover, the mode of development of Drosophila larval and adult eyes reinforces similarities between Rh5-PRs with an inner-PR type and Rh6-PRs with an outer-PR type: in the adult, R8-PR precursors are formed first to recruit outer PRs, likewise in the larva, Rh5-PR precursors develop first and then recruit the Rh6-PRs, in both cases via the EGFR pathway ( Sprecher et al, 2007 ). Also, development of both inner PRs and Rh5-PRs depend on the transcription factors senseless and spalt ( Sprecher et al, 2007 ; Sprecher and Desplan, 2008 ; Mishra et al, 2013 ). Finally, the inputs from serotonergic and octopaminergic/tyraminergic neurons onto the LON are also a shared feature with the adult visual system where serotonin has been linked to circadian rhythmicity ( Yuan et al, 2005 ) and where visual cues during flight are modulated by octopaminergic inputs ( Suver et al, 2012 ; Wasserman et al, 2015 ).…”

Actinomycetes bioactive compounds: Biological control of fungi and phytopathogenic insect

“…Some species of Aspergillus are highly aflatoxigenic, particularly in tropical and subtropical countries, secreting high level of aflatoxins. Furthermore, aflatoxin is classified as group 1 human carcinogen by the International Agency for Research on Cancer (Mishra et al, 2013).…”

Serial electron microscopic reconstruction of the drosophila larval eye: Photoreceptors with a rudimentary rhabdomere of microvillar-like processes

“…Drosophila larval vision, mediated by the BO, has been the focus of several recent functional studies, including (Essen et al, 2011;Humberg et al, 2018;Humberg and Sprecher, 2017;Justice et al, 2012;Kane et al, 2013;Keene et al, 2011). The BO, due to its simplicity in terms of cell types and rapid development during the embryonic period, has also a rich source for developmental genetic analysis (Sprecher et al, 2007;Sprecher and Desplan, 2008;Vasiliauskas et al, 2011;Mishra et al, 2013Mishra et al, , 2016Zhou et al, 2017). To further aid in these studies a more detailed understanding of the ultrastructural details of the BO photoreceptor membrane specializations is required.…”