Glass promotes the differentiation of neuronal and non-neuronal cell types in the Drosophila eye

Morrison, Carolyn A.; Chen, Hao; Cook, Tiffany; Brown, Stuart M.; Treisman, Jessica E.

doi:10.1371/journal.pgen.1007173

Cited by 18 publications

(17 citation statements)

References 100 publications

(146 reference statements)

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“…PIP82 is not required for specification of photoreceptors but rather is a terminal differentiation gene. Moreover, we demonstrate that PIP82 transcription is regulated by the known transcriptional drivers of photoreceptor differentiation Glass and Pph13 [25][26][27][28] and, functionally, that the loss of PIP82 impacts the morphological differentiation and maintenance of rhabdomere structure. We further show that PIP82 is a post-translational target of aPKC and phosphorylation of PIP82 regulates cortical membrane localization of the protein.…”

Section: Plos Geneticsmentioning

confidence: 80%

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila

et al. 2020

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The Drosophila apical photoreceptor membrane is defined by the presence of two distinct morphological regions, the microvilli-based rhabdomere and the stalk membrane. The subdivision of the apical membrane contributes to the geometrical positioning and the stereotypical morphology of the rhabdomeres in compound eyes with open rhabdoms and neural superposition. Here we describe the characterization of the photoreceptor specific protein PIP82. We found that PIP82's subcellular localization demarcates the rhabdomeric portion of the apical membrane. We further demonstrate that PIP82 is a phosphorylation target of aPKC. PIP82 localization is modulated by phosphorylation, and in vivo, the loss of the aPKC/Crumbs complex results in an expansion of the PIP82 localization domain. The absence of PIP82 in photoreceptors leads to misshapped rhabdomeres as a result of misdirected cellular trafficking of rhabdomere proteins. Comparative analyses reveal that PIP82 originated de novo in the lineage leading to brachyceran Diptera, which is also characterized by the transition from fused to open rhabdoms. Taken together, these findings define a novel factor that delineates and maintains a specific apical membrane domain, and offers new insights into the functional organization and evolutionary history of the Drosophila retina.

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Section: Plos Geneticsmentioning

confidence: 80%

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila

et al. 2020

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“…Glass plays a fundamental role for the differentiation of rhabdomeric PRs in the fruit fly [9, 11, 45, 46]. To investigate if it provides a similar function across metazoans, we first decided to search for Glass homologues in other species.…”

Section: Resultsmentioning

confidence: 99%

Glass confers rhabdomeric photoreceptor identity inDrosophila, but not across all metazoans

Bernardo-Garcia

Syed

Jékely

et al. 2018

Preprint

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Across metazoans, visual systems employ different types of photoreceptor neurons to detect light. These include rhabdomeric PRs, which exist in distantly related phyla and possess an evolutionarily conserved phototransduction cascade. While the development of rhabdomeric PRs has been thoroughly studied in the fruit fly Drosophila melanogaster, we still know very little about how they form in other species. To investigate this question, we tested whether the transcription factor Glass, which is crucial for instructing rhabdomeric PR formation in Drosophila, may play a similar role in other metazoans. Glass homologues exist throughout the animal kingdom, indicating that this protein evolved prior to the metazoan radiation. Interestingly, our work indicates that glass is not expressed in rhabdomeric photoreceptors in the planarian Schmidtea mediterranea nor in the annelid Platynereis dumerilii. Combined with a comparative analysis of the Glass DNA-binding domain, our data suggest that the fate of rhabdomeric PRs is controlled by Glass-dependent and Glass-independent mechanisms in different animal clades.

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“…In addition, intron-retaining mRNA transcripts can remain in the nucleus and be spliced upon requirement providing a source of transcript that could be faster activated than by de novo transcription [26]. Recent RNAseq data suggests that intron 4 is not retained in the glass mRNA [4]. The authors found that expression of either the glass RA+RC or the glass RB transcript from transgenic constructs resulted in production of functional Glass protein, suggesting that in their ectopic expression experiments, intron 4 of the RB transcript was spliced out to produce full-length Glass PA (and PC) protein.…”

Section: Discussionmentioning

confidence: 99%

“…The zinc-finger transcription factor Glass provides a critical link betwee the RDN and terminal differentiaton. Glass is required during eye development for the differentiation of photoreceptor neurons, patterning of the ommatidia, as well as for the differentiation of cone- and pigment-cells [1-4]. glass mutants were first discovered by H.J.…”

Section: Introductionmentioning

confidence: 99%

“…Intrestingly glass acts in conjunction with distinct transcripton factors to coordinate different cell fates during eye formation. For the specification of cone cells glass acts together with d Pax2, eyes absent and lozenge , while for the formation of pigment cells it requires escargot [4]. Thus, dependent on the cellular context Glass is likely to control distinct developmental programs.…”

Section: Introductionmentioning

confidence: 99%

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Multilevel regulation of the glass locus during Drosophila eye development

Fritsch

Bernardo-Garcia

Humberg

et al. 2019

Preprint

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21Development of eye tissue is initiated by a conserved set of transcripton factors 22 development, but may act to buffer Glass expression level. Moreover, we assessed 80 the requirement and functionality of the three Glass protein isoforms by CRISPR-81 mediated genome editing introducing deletions into the glass locus resulting in the 82 loss of one or two of the three isoforms. We analyzed these isoform mutants for the 83 morphology of their eyes, the expression of photoreceptor markers that depend on 84Glass function, photoreceptor activity, and light preference behavior. We found that 85 the short Glass PB isoform is not able to confer normal eye development and 86 function resulting in a glass mutant phenotype, while the Glass PA isoform alone is 87 fully functional. Our results suggest that the expression of glass is tightly regulated as 88 the development of a functional tissue is surprisingly robust resulting in no detectable 89 change in the physiological response or alteration in photoattraction behaviour upon 90 deletion of the smORF. Similarly, only one of the isoforms is critical for eye 91 development, suggesting that the other isoforms may function in a similar way to 92 control levels of the functional protein. Since sequence comparison to closely related 93 species show conservation of these features, such mechanisms may function to fine-94 tune gene expression. 95 96 RESULTS 97 98 An overlapping upstream open reading frame inhibits the expression of a glass 99 reporter 100 In the developing eye, expression of glass is initated at the morphogenetic furrow in 101 the eye-imaginal disc of third instar larvae and is detectable in the nuclei of all cells 102 posterior to the morphogenetic furrow [7]. The same expression pattern is obtained 103 with a reporter construct containing a 5.2 kb DNA fragment upstream of glass [8], 104spaning from -4190 bp to the AUG at +960 (Fig. 1A) [8]. Suprisingly, using this 5.2 kb 105 upstream genomic sequence to drive a GFP reporter we observed GFP expression 106 was barely detectable in the eye imaginal discs (Fig. 1B, B''). By increasing the gain 107 at the confocal microscope, we were able to detect a weak GFP signal posterior to 108 the morphogenetic furrow, barely above background level ( Fig. 1B''', B''''). A closer 109 inspection of our reporter construct revealed the presence of two potential start 110 codons in the 5'UTR of glass, that were also present in the GFP reporter construct, 111 one at position +889 relative to the predicted transcription start, the other at position 112 +955. Translation from the first start codon, if functional, may compete with the GFP 113

show abstract

Glass promotes the differentiation of neuronal and non-neuronal cell types in the Drosophila eye

Cited by 18 publications

References 100 publications

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila

Glass confers rhabdomeric photoreceptor identity inDrosophila, but not across all metazoans

Multilevel regulation of the glass locus during Drosophila eye development

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