An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian

Ayyar, Savita; Negre, Bàrbara; Simpson, Patricia; Stollewerk, Angelika

doi:10.1186/1741-7007-8-127

Cited by 24 publications

(36 citation statements)

References 44 publications

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“…For this process, the SOPE, a very ancient regulatory element that predates the Diptera (Ayyar et al, 2010), is the only cis-regulatory element of ac-sc that would be required. Factors that act through the SOPE could be co-opted to modulate the temporal activity of ac-sc.…”

Section: Research Articlementioning

confidence: 99%

The kinase Sgg modulates temporal development of macrochaetes inDrosophilaby phosphorylation of Scute and Pannier

2012

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SUMMARYEvolution of novel structures is often made possible by changes in the timing or spatial expression of genes regulating development. Macrochaetes, large sensory bristles arranged into species-specific stereotypical patterns, are an evolutionary novelty of cyclorraphous flies and are associated with changes in both the temporal and spatial expression of the proneural genes achaete (ac) and scute (sc). Changes in spatial expression are associated with the evolution of cis-regulatory sequences, but it is not known how temporal regulation is achieved. One factor required for ac-sc expression, the expression of which coincides temporally with that of ac-sc in the notum, is Wingless (Wg; also known as Wnt). Wingless downregulates the activity of the serine/threonine kinase Shaggy (Sgg; also known as GSK-3). We demonstrate that Scute is phosphorylated by Sgg on a serine residue and that mutation of this residue results in a form of Sc with heightened proneural activity that can rescue the loss of bristles characteristic of wg mutants. We suggest that the phosphorylated form of Sc has reduced transcriptional activity such that sc is unable to autoregulate, an essential function for the segregation of bristle precursors. Sgg also phosphorylates Pannier, a transcriptional activator of ac-sc, the activity of which is similarly dampened when in the phosphorylated state. Furthermore, we show that Wg signalling does not act directly via a cis-regulatory element of the ac-sc genes. We suggest that temporal control of ac-sc activity in cyclorraphous flies is likely to be regulated by permissive factors and might therefore not be encoded at the level of ac-sc gene sequences.

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Section: Research Articlementioning

confidence: 99%

The kinase Sgg modulates temporal development of macrochaetes inDrosophilaby phosphorylation of Scute and Pannier

2012

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“…This was probably facilitated by parallel changes in the regulatory regions of the proneural genes (Ayyar et al, 2010;Eriksson and Stollewerk, 2010). Since the ancestral state of neurogenesis in arthropods is the segregation of neural precursors, we assume that the same mechanism was adopted for neuroblasts in the Tetraconata ancestor.…”

Section: The Role Of Notch Signalling In Binary Cell Fate Decisionsmentioning

confidence: 97%

Unravelling the evolution of neural stem cells in arthropods: Notch signalling in neural stem cell development in the crustacean Daphnia magna

Ungerer

Eriksson

Stollewerk

2012

Developmental Biology

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The genetic regulatory networks controlling major developmental processes seem to be conserved in bilaterians regardless of an independent or a common origin of the structures. This has been explained by the employment of a genetic toolkit that was repeatedly used during bilaterian evolution to build the various forms and body plans. However, it is not clear how genetic networks were incorporated into the formation of novel structures and how homologous genes can regulate the disparate morphological processes. Here we address this question by analysing the role of Notch signalling, which is part of the bilaterian toolkit, in neural stem cell evolution in arthropods. Within arthropods neural stem cells have evolved in the last common ancestor of insects and crustaceans (Tetraconata). We analyse here for the first time the role of Notch signalling in a crustacean, the branchiopod Daphnia magna, and show that it is required in neural stem cells for regulating the time of neural precursor production and for binary cell fate decisions in the ventral neuroectoderm. The function of Notch signalling has diverged in the ventral neuroectoderm of insects and crustaceans accompanied by changes in the morphogenetic processes. In the crustacean, Notch controlled mechanisms of neuroblast regulation have evolved that are surprisingly similar to vertebrates and thus present a remarkable case of parallel evolution. These new data on a representative of crustaceans complete the arthropod data set on Notch signalling in the nervous system and allow for reconstructing how the Notch signalling pathway has been co-opted from pre-existing structures to the development of the evolving neural stem cells in the Tetraconata ancestor.

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“…They influence the AS C expression either by a direct binding to AS C regulatory regions or via post translational interactions with AS C mRNA, which modifies its stability and translation efficiency. It is known that neural potential of the disc cells are pro vided by a low level of NF kB/Rel family proteins in combination with a high level of AS C proteins (Ayyar et al, 2007(Ayyar et al, , 2010. The EGFR signaling pathway plays a considerable part in the bristle patterning.…”

Section: As C Wg Ush Pnrmentioning

confidence: 99%

The mechanisms determining bristle pattern in Drosophila melanogaster

Бухарина

Furman

2015

Russ J Dev Biol

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Macrochaetes (large bristles) are arranged on the drosophila head and notum in a specific bristle pattern. The number and positions of the macrochaetes forming the pattern are important species specific characteristics, which are determined by a strict positioning of the proneural clusters in the in the imaginal disc ectoderm in the third instar larvae and prepupae. In turn, the positioning of proneural clusters depends on the distribution of the so called prepattern factors, responsible for the bristle prepatterning. The current concept identifies the prepattern factors with the transcription factors that initiate the local expression of the achaete scute complex (AS C) genes. Expression of these genes confined to certain regions of the ectoderm is the particular factor that determines the macrochaete pattern on the adult fly body. The review considers and systematizes the data on establishment of the prepatterning as the final stage in the functioning of hier archically organized molecular genetic system resulting in the local expression of AS C genes in the ectoderm of imaginal discs.

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An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian

Cited by 24 publications

References 44 publications

The kinase Sgg modulates temporal development of macrochaetes inDrosophilaby phosphorylation of Scute and Pannier

The kinase Sgg modulates temporal development of macrochaetes inDrosophilaby phosphorylation of Scute and Pannier

Unravelling the evolution of neural stem cells in arthropods: Notch signalling in neural stem cell development in the crustacean Daphnia magna

The mechanisms determining bristle pattern in Drosophila melanogaster

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