Development and Evolution of the Drosophila Bolwig’s Organ: A Compound Eye Relict

Friedrich, Markus

doi:10.1007/978-1-4614-8232-1_12

Cited by 7 publications

(6 citation statements)

References 124 publications

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“…The BO thus represents the most recent of the three sense organs of the Drosophila visual system and is more closely related to the CE than to the OC (Fig. 6C) (Friedrich, 2013). …”

Section: Discussionmentioning

confidence: 97%

“…The origin of OC and CE from a singleton precursor visual organ predates the diversification of arthropods begun at least 500 Mya. The larval eye evolved later (~350 Mya) through subfunctionalization of part of the ancestral insect CE during the evolution of the larval stage in Holometabola (indirect developing insects) (Friedrich, 2013). The BO thus represents the most recent of the three sense organs of the Drosophila visual system and is more closely related to the CE than to the OC (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Within this phylogenetic framework, the use of direct transcriptional activation by So emerges as an ancestral and evolutionarily conserved feature of the ato BO cis -element; whereas, the dispensability of Pax6 in BO development and ato expression represents an outcome of regressive evolution at the gene regulatory level (Porter and Crandall, 2003; Friedrich, 2011 and 2013). Both conclusions have intriguing implications.…”

Section: Discussionmentioning

confidence: 99%

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Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Zhou

Friedrich

et al. 2017

Developmental Biology

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Drosophila has three types of visual organs, the larval eyes or Bolwig’s organs (BO), the ocelli (OC) and the compound eyes (CE). In all, the bHLH protein Atonal (Ato) functions as the proneural factor for photoreceptors and effects the transition from progenitor cells to differentiating neurons. In this work, we investigate the regulation of ato expression in the BO primordium (BOP). Surprisingly, we find that ato transcription in the BOP is entirely independent of the shared regulatory DNA for the developing CE and OC. The core enhancer for BOP expression, atoBO, lies ~6 kb upstream of the ato gene, in contrast to the downstream location of CE and OC regulatory elements. Moreover, maintenance of ato expression in the neuronal precursors through autoregulation-a common and ancient feature of ato expression that is well-documented in eyes, ocelli and chordotonal organs-does not occur in the BO. We also show that the atoBO enhancer contains two binding sites for the transcription factor Sine oculis (So), a core component of the progenitor specification network in all three visual organs. These binding sites function in vivo and are specifically bound by So in vitro. Taken together, our findings reveal that the control of ato transcription in the evolutionarily derived BO has diverged considerably from ato regulation in the more ancestral compound eyes and ocelli, to the extent of acquiring what appears to be a distinct and evolutionarily novel cis-regulatory module.

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“…The BO thus represents the most recent of the three sense organs of the Drosophila visual system and is more closely related to the CE than to the OC (Fig. 6C) (Friedrich, 2013). …”

Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Zhou

Friedrich

et al. 2017

Developmental Biology

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“…Lampel et al [ 59 ] speculated on the circadian role of invertebrate non-visual opsins, and in at least one vertebrate, blind cavefish, point mutations (stop codons) in both melanopsin and teleost multiple tissue opsin are implicated in the de-activation of diurnal circadian rhythm [ 32 ]. The retention (‘recycling’) of larval-stage visual organs in adults of some endopterygote insects are also implicated in deep-brain circadian entrainment (notably Drosophila, Tribolium and Thermonectus —reviewed in [ 60 , 61 ]), suggesting ontogenesis of these insect visual systems is complex and deserving of considerable attention.…”

Section: Discussionmentioning

confidence: 99%

Opsin transcripts of predatory diving beetles: a comparison of surface and subterranean photic niches

et al. 2015

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The regressive evolution of eyes has long intrigued biologists yet the genetic underpinnings remain opaque. A system of discrete aquifers in arid Australia provides a powerful comparative means to explore trait regression at the genomic level. Multiple surface ancestors from two tribes of diving beetles (Dytiscidae) repeatedly invaded these calcrete aquifers and convergently evolved eye-less phenotypes. We use this system to assess transcription of opsin photoreceptor genes among the transcriptomes of two surface and three subterranean dytiscid species and test whether these genes have evolved under neutral predictions. Transcripts for UV, long-wavelength and ciliary-type opsins were identified from the surface beetle transcriptomes. Two subterranean beetles showed parallel loss of all opsin transcription, as expected under ‘neutral’ regressive evolution. The third species Limbodessus palmulaoides retained transcription of a long-wavelength opsin (lwop) orthologue, albeit in an aphotic environment. Tests of selection on lwop indicated no significant differences between transcripts derived from surface and subterranean habitats, with strong evidence for purifying selection acting on L. palmulaoides lwop. Retention of sequence integrity and the lack of evidence for neutral evolution raise the question of whether we have identified a novel pleiotropic role for lwop, or an incipient phase of pseudogene development.

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“…Where do the microvillar-like processes of Drosophila larval PRCs fall into the wide spectrum of apical membrane processes observed among different animal phyla? According to the existing developmental and genetic evidence, larval stemmata observed in holometabolous insects, including Drosophila, are homologous to the ommatidia of adult compound eyes, a proposition that has been well documented and discussed in previous works (Paulus, 1986(Paulus, , 1989Melzer and Paulus, 1989;Friedrich, 2013;Buschbeck, 2014). Microvilli of ommatidial rhabdomeres, including those of larval stemmata described for other species, are of extremely uniform diameter, orientation and high packing density, with neighboring microvilli stacked right next to each other (Arikawa et al, 1990;Hardie and Raghu, 2001;Fain et al, 2010).…”

Section: Photoreceptor Membrane Stacking: Microvilli and Microvillar-mentioning

confidence: 88%

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

Hartenstein

Yuan

Younossi-Hartenstein

et al. 2019

Developmental Biology

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Photoreceptor cells (PRCs) across the animal kingdom are characterized by a stacking of apical membranes to accommodate the high abundance of photopigment. In arthropods and many other invertebrate phyla PRC membrane stacks adopt the shape of densely packed microvilli that form a structure called rhabdomere. PRCs and surrounding accessory cells, including pigment cells and lens-forming cells, are grouped in stereotyped units, the ommatidia. In larvae of holometabolan insects, eyes (called stemmata) are reduced in terms of number and composition of ommatidia. The stemma of Drosophila (Bolwig organ) is reduced to a bilateral cluster of subepidermal PRCs, lacking all other cell types. In the present paper we have analyzed the development and fine structure of the Drosophila larval PRCs. Shortly after their appearance in the embryonic head ectoderm, PRC precursors delaminate and lose expression of apical markers of epithelial cells, including Crumbs and several centrosome-associated proteins. In the early first instar larva, PRCs show an expanded, irregularly shaped apical surface that is folded into multiple horizontal microvillar-like processes (MLPs). Apical PRC membranes and MLPs are covered with a layer of extracellular matrix. MLPs are predominantly aligned along an axis that extends ventro-anteriorly to dorso-posteriorly, but vary in length, diameter, and spacing. Individual MLPs present a "beaded" shape, with thick segments (0.2-0.3 μm diameter) alternating with thin segments (>0.1 μm). We show that loss of the glycoprotein Chaoptin, which is absolutely essential for rhabdomere formation in the adult PRCs, does not lead to severe abnormalities in larval PRCs.

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Development and Evolution of the Drosophila Bolwig’s Organ: A Compound Eye Relict

Cited by 7 publications

References 124 publications

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Distinct regulation of atonal in a visual organ of Drosophila : Organ-specific enhancer and lack of autoregulation in the larval eye

Opsin transcripts of predatory diving beetles: a comparison of surface and subterranean photic niches

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

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