A complete temporal transcription factor series in the fly visual system

Κωνσταντινίδης, Νικόλαος; Holguera, Isabel; Rossi, Anthony; Escobar, Aristides; Dudragne, Liébaut; Chen, Yen‐Chung; Tran, Tony; Jaimes, Azalia M Martínez; Özel, Mehmet Neset; Simon, Félix; Shao, Zhiping; Tsankova, Nadejda M.; Fullard, John F.; Walldorf, Uwe; Roussos, Panos; Desplan, Claude

doi:10.1038/s41586-022-04564-w

Cited by 82 publications

(106 citation statements)

References 48 publications

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“…The heavily rearranged genome architecture of cephalopods with the fusion of multiple ancestral linkage groups might have not only promoted duplication hotspots, but also permitted the acquisition of more complex gene regulatory processes that could have promoted a cell type specific expression of duplicated genes as seen, for example, in vertebrates (Albertin et al, 2022a;Marlétaz et al, 2018). We hope that our single-cell atlas coupled with the model capabilities of the E. berryi will promote further studies to decipher the underpinnings and evolutionary origin of cephalopod nervous systems and detect distinct subtypes as has been the case for Drosophila and vertebrate models (Konstantinides et al, 2022;Sanes and Zipursky, 2020;. (C-F) Heatmaps displaying AUROC scores or "Reciprocal_top_hit" match types are identified as cell type pairs comparisons between E. berryi retina and chicken retina cell types (Yamagata et al, 2021) (C), E. berryi adult optic lobe comparisons to (D-F) to mouse dorsal lateral geniculate nucleus (Allen Brain Atlas, D) , to mouse visual cortex (Tasic et al, 2016) (E) and to adult Drosophila optic lobes (Özel et al, 2021)…”

Section: Discussionmentioning

confidence: 92%

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Gavriouchkina

Tan

Ziadi-Künzli

et al. 2022

Preprint

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Although the camera-type eyes of cephalopods and vertebrates are a canonical example of convergent morphological evolution, the cellular and molecular mechanisms underlying this convergence remain obscure. We used genomics and single cell transcriptomics to study these mechanisms in the visual system of the bobtail squid Euprymna berryi, an emerging cephalopod model. Analysis of 98,537 cellular transcriptomes from the squid visual and nervous system identified dozens of cell types that cannot be placed in simple correspondence with those of vertebrate or fly visual systems, as proposed by Ramón y Cajal and J.Z. Young. Instead, we find an unexpected diversity of neural types, dominated by dopamine, and previously uncharacterized glial cells. Surprisingly, we observe changes in cell populations and neurotransmitter usage during maturation and growth of the visual systems from hatchling to adult. Together these genomic and cellular findings shed new light on the parallel evolution of visual system complexity in cephalopods and vertebrates.

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Section: Discussionmentioning

confidence: 92%

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Gavriouchkina

Tan

Ziadi-Künzli

et al. 2022

Preprint

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“…The tTF Slp1 regulates the widely expressed selectors Toy and Sox102F, and the tTF D regulates Ets65A 11, 70 , which is a common selector of Mi15 and Dm2 (among others). tTF Hbn also regulates Toy, and other selectors including Tj and Otd; and the tTF Opa regulates TfAP-2 10 , a selector TF shared by all four Tm neurons we studied here. Finally, all Notch ON neurons express the selector TF Ap 11 , which is required for the cholinergic identity of most of those neurons 68 .…”

Section: Discussionmentioning

confidence: 86%

Coordinated control of neuronal differentiation and wiring by a sustained code of transcription factors

Özel

Gibbs

Holguera

et al. 2022

Preprint

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The enormous diversity of cell types in nervous systems presents a challenge in identifying the genetic mechanisms that encode it. Here, we report that nearly 200 distinct neurons in the Drosophila visual system can each be defined by unique combinations of ∼10 transcription factors that are continuously expressed by them. We show that targeted modifications of this ‘selector’ code induce predictable conversions of cell fates between neurons in vivo. These conversions appear morphologically and transcriptionally complete, arguing for a conserved gene regulatory program that jointly instructs both the type-specific development and the terminal features of neurons. Cis-regulatory sequence analysis of open chromatin links one of these selectors to an upstream patterning gene in stem cells that specifies neuronal fates. Experimentally validated network models show that selectors interact with ecdysone signaling to regulate downstream effectors controlling brain wiring. Our results provide a generalizable framework of how specific fates are initiated and maintained in postmitotic neurons.

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“…Several scRNA-seq analyses have been performed in the OL, revealing gene expression profiles in a large number of neurons [ 22–26 , 63 ]. In addition, scRNA-seq analysis has been performed focusing on the developing OL, which has led to a better understanding of the temporal patterning of neurogenesis [ 27 , 29 ]. As a result, many TTFs were newly identified in medulla NBs, and their regulatory network was revealed.…”

Section: Temporal Patterning Following the Proneural Wave In The Larv...mentioning

confidence: 99%

“…Hbn and Scro were found to be expressed in the regions of Ey- and Slp-positive NBs. They promote the transition from Ey- to Slp-positive NBs [ 27 , 29 ]. These TTFs have been identified as target genes of Ey by TaDa analysis using the Ey-Dam fusion protein [ 50 ].…”

Section: Temporal Patterning Following the Proneural Wave In The Larv...mentioning

confidence: 99%

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Cutting edge technologies expose the temporal regulation of neurogenesis in the Drosophila nervous system

Sato

Suzuki

2022

Fly

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During the development of the central nervous system (CNS), extremely large numbers of neurons are produced in a regular fashion to form precise neural circuits. During this process, neural progenitor cells produce different neurons over time due to their intrinsic gene regulatory mechanisms as well as extrinsic mechanisms. The Drosophila CNS has played an important role in elucidating the temporal mechanisms that control neurogenesis over time. It has been shown that a series of temporal transcription factors are sequentially expressed in neural progenitor cells and regulate the temporal specification of neurons in the embryonic CNS. Additionally, similar mechanisms are found in the developing optic lobe and central brain in the larval CNS. However, it is difficult to elucidate the function of numerous molecules in many different cell types solely by molecular genetic approaches. Recently, omics analysis using single-cell RNA-seq and other methods has been used to study the Drosophila nervous system on a large scale and is making a significant contribution to the understanding of the temporal mechanisms of neurogenesis. In this article, recent findings on the temporal patterning of neurogenesis and the contributions of cutting-edge technologies will be reviewed.

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A complete temporal transcription factor series in the fly visual system

Cited by 82 publications

References 48 publications

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Coordinated control of neuronal differentiation and wiring by a sustained code of transcription factors

Cutting edge technologies expose the temporal regulation of neurogenesis in the Drosophila nervous system

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