Ancient default activators of terminal photoreceptor differentiation in the pancrustacean compound eye: the homeodomain transcription factors Otd and Pph13

Friedrich, Markus; Cook, Tiffany; Zelhof, Andrew C.

doi:10.1016/j.cois.2015.10.006

Cited by 8 publications

(7 citation statements)

References 69 publications

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“…We propose that the Rh gene duplications also included the promoter region, whose mutation generated novel cis -regulatory motifs for specific trans -acting factors that partition the spatially distinct Rh patterns. Taking both the phylogenetic relationships of the Rh coding sequences [ 22 , 23 ] as well as shared cis -regulatory motifs in their promoters into account, we suggest the following model for the evolution of the Rh cis -regulatory signatures ( Fig 11 ): In agreement with previous models [ 19 , 22 , 27 ], the ancestral Rh was probably broadly expressed by the ancient pan-PR activator Pph13 [ 28 ] through Q 50 motifs in the distal promoter region and within a palindromic P3-type RCSI motif in the proximal region ( Fig 11 ). Such a palindromic P3-type motif, composed of Q 50 motifs and lacking repressor motifs ( Fig 11 ), closely resembles the palindromic P3 motifs in the contemporary Pph13-dependent phototransduction genes that are also broadly expressed in all PRs [ 6 , 19 ].…”

Section: Discussionsupporting

confidence: 85%

A combinatorial cis-regulatory logic restricts color-sensing Rhodopsins to specific photoreceptor subsets in Drosophila

et al. 2021

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Color vision in Drosophila melanogaster is based on the expression of five different color-sensing Rhodopsin proteins in distinct subtypes of photoreceptor neurons. Promoter regions of less than 300 base pairs are sufficient to reproduce the unique, photoreceptor subtype-specific rhodopsin expression patterns. The underlying cis-regulatory logic remains poorly understood, but it has been proposed that the rhodopsin promoters have a bipartite structure: the distal promoter region directs the highly restricted expression in a specific photoreceptor subtype, while the proximal core promoter region provides general activation in all photoreceptors. Here, we investigate whether the rhodopsin promoters exhibit a strict specialization of their distal (subtype specificity) and proximal (general activation) promoter regions, or if both promoter regions contribute to generating the photoreceptor subtype-specific expression pattern. To distinguish between these two models, we analyze the expression patterns of a set of hybrid promoters that combine the distal promoter region of one rhodopsin with the proximal core promoter region of another rhodopsin. We find that the function of the proximal core promoter regions extends beyond providing general activation: these regions play a previously underappreciated role in generating the non-overlapping expression patterns of the different rhodopsins. Therefore, cis-regulatory motifs in both the distal and the proximal core promoter regions recruit transcription factors that generate the unique rhodopsin patterns in a combinatorial manner. We compare this combinatorial regulatory logic to the regulatory logic of olfactory receptor genes and discuss potential implications for the evolution of rhodopsins.

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Section: Discussionsupporting

confidence: 85%

A combinatorial cis-regulatory logic restricts color-sensing Rhodopsins to specific photoreceptor subsets in Drosophila

et al. 2021

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“…Thus further research on these protostomes will reveal whether Glass-Pph13 interplay acts as an evolutionary ancient transcriptional motif between the morphogenesis of various eye structures and the ensuing differentiation of rhabdomeric photoreceptor neurons. Second, it has been postulated that Otd, another shared transcriptional regulator for rhabdomere differentiation among Pancrustaceans, represents the ancestral state for development and function of the prototype photoreceptor and Pph13 joined the regulatory network during the acquisition of a more sophisticated rhabdomere organization at a later stage (Friedrich et al, 2016). This hypothesis is supported by the fact that Otx/Otd homologs are instrumental in directing both rhabdomeric and ciliary photoreceptor differentiation and deuterostomes appear to lack Pph13 homologs (Friedrich et al, 2016; Mahato et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Second, it has been postulated that Otd, another shared transcriptional regulator for rhabdomere differentiation among Pancrustaceans, represents the ancestral state for development and function of the prototype photoreceptor and Pph13 joined the regulatory network during the acquisition of a more sophisticated rhabdomere organization at a later stage (Friedrich et al, 2016). This hypothesis is supported by the fact that Otx/Otd homologs are instrumental in directing both rhabdomeric and ciliary photoreceptor differentiation and deuterostomes appear to lack Pph13 homologs (Friedrich et al, 2016; Mahato et al, 2014). As Pph13 expression requires Glass, and if it is true that the Glass-Pph13 interaction represented an ancestral regulatory mechanism during the evolution of rhabdomeric photoreceptors, the lack of Pph13 orthologs outside protostomes can be partially explained by the absence of glass orthologs.…”

Section: Discussionmentioning

confidence: 99%

Two temporal functions of Glass: Ommatidium patterning and photoreceptor differentiation

Liang

Mahato

Hemmerich

et al. 2016

Developmental Biology

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Much progress has been made in elucidating the molecular networks required for specifying retinal cells, including photoreceptors, but the downstream mechanisms that maintain identity and regulate differentiation remain poorly understood. Here, we report that the transcription factor Glass has a dual role in establishing a functional Drosophila eye. Utilizing conditional rescue approaches, we confirm that persistent defects in ommatidium patterning combined with cell death correlate with the overall disruption of eye morphology in glass mutants. In addition, we reveal that Glass exhibits a separable role in regulating photoreceptor differentiation. In particular, we demonstrate the apparent loss of glass mutant photoreceptors is not only due to cell death but also a failure of the surviving photoreceptors to complete differentiation. Moreover, the late reintroduction of Glass in these developmentally stalled photoreceptors is capable of restoring differentiation in the absence of correct ommatidium patterning. Mechanistically, transcription profiling at the time of differentiation reveals that Glass is necessary for the expression of many genes implicated in differentiation, i.e. rhabdomere morphogenesis, phototransduction, and synaptogenesis. Specifically, we show Glass directly regulates the expression of Pph13, which encodes a transcription factor necessary for opsin expression and rhabdomere morphogenesis. Finally, we demonstrate the ability of Glass to choreograph photoreceptor differentiation is conserved between Drosophila and Tribolium, two holometabolous insects. Altogether, our work identifies a fundamental regulatory mechanism to generate the full complement of cells required for a functional rhabdomeric visual system and provides a critical framework to investigate the basis of differentiation and maintenance of photoreceptor identity.

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“…The last gene to mention here is orthodenticle (otd), which in Drosophila is essential for the proper development of photoreceptors (McDonald et al, 2010;Terrell et al, 2012). This gene is also predicted to be part of the ancestral regulatory network (Friedrich, 2006;Friedrich et al, 2016). Interestingly, orthologs have been identified in the secondary but not principal eyes of C. salei (Samadi et al, 2015) and, rather curiously, in the principal but not secondary eyes of P. tepidariorum (Schomburg et al, 2015).…”

Section: Sparse But Definitive Overlap In Patterns Of Gene Expressionmentioning

confidence: 99%

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

Morehouse

Buschbeck

Zurek

et al. 2017

The Biological Bulletin

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Spiders are among the world's most species-rich animal lineages, and their visual systems are likewise highly diverse. These modular visual systems, composed of four pairs of image-forming "camera" eyes, have taken on a huge variety of forms, exhibiting variation in eye size, eye placement, image resolution, and field of view, as well as sensitivity to color, polarization, light levels, and motion cues. However, despite this conspicuous diversity, our understanding of the genetic underpinnings of these visual systems remains shallow. Here, we review the current literature, analyze publicly available transcriptomic data, and discuss hypotheses about the origins and development of spider eyes. Our efforts highlight that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages. For example, many (but not all) of the genes that appear important for early eye development in spiders are familiar players known from the developmental networks of other model systems (e.g., Drosophila). Similarly, our analyses of opsins and related phototransduction genes suggest that spider photoreceptors employ many of the same genes and molecular mechanisms known from other arthropods, with a hypothesized ancestral spider set of four visual and four nonvisual opsins. This deep homology provides a number of useful footholds into new work on spider vision and the molecular basis of its extant variety. We therefore discuss what some of these first steps might be in the hopes of convincing others to join us in studying the vision of these fascinating creatures.

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Ancient default activators of terminal photoreceptor differentiation in the pancrustacean compound eye: the homeodomain transcription factors Otd and Pph13

Cited by 8 publications

References 69 publications

A combinatorial cis-regulatory logic restricts color-sensing Rhodopsins to specific photoreceptor subsets in Drosophila

A combinatorial cis-regulatory logic restricts color-sensing Rhodopsins to specific photoreceptor subsets in Drosophila

Two temporal functions of Glass: Ommatidium patterning and photoreceptor differentiation

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

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