Cis-regulatory evolution integrated the Bric-à-brac transcription factors into a novel fruit fly gene regulatory network

Roeske, Maxwell J; Camino, Eric M.; Grover, Sumant; Rebeiz, Mark; Williams, Thomas M.

doi:10.7554/elife.32273

Cited by 40 publications

(56 citation statements)

References 44 publications

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“…For example, broad expression in the abdomen was driven by three fragments from D. melanogaster, six fragments from D. pseudoobscura and six fragments from D. willistoni. Redundant enhancers driving expression throughout the wing blade, in abdominal stripes, and in segments A5 and A6 of D. melanogaster males were especially surprising given that these patterns were previously described as being controlled by a single enhancer module (Wittkopp et al 2002;Gompel et al 2005;Prud'homme et al 2006;Jeong et al 2006;Camino et al 2015;Roeske et al 2018). In the wing blade, expression was driven by three, seven, and seven fragments from D. melanogaster, D. pseudoobscura, and D. willistoni, respectively (Figure 7).…”

Section: Redundant Enhancers Are Common For the Yellow Genementioning

confidence: 87%

“…Expression in all of the other structures scored (i.e., top of head and head circumference, broad abdominal expression, sexually dimorphic A5/A6 expression, thoracic trident expression, and expression in the wing blade and veins) was driven by multiple fragments within each species without any clear patterns of sequence similarity linking these fragments (Figure 7). Of these traits, enhancers driving sexually dimorphic expression have been studied most extensively in prior work, with two transcription factors, Abdominal-B (Abd-B) and Bric-a-brac (Bab) shown to directly regulate a sexually dimorphic enhancer of yellow in D. melanogaster (Jeong et al 2006;Camino et al 2015;Roeske et al 2018). We tested for enrichment of motifs representing binding sites for Abd-B, Bab, or any of ~400 other transcription factors within the 13 fragments that drove sexually dimorphic expression in A5 and A6 relative to the 16 fragments that did not.…”

Section: Conservation and Divergence Of Enhancer Activities Are Not Wmentioning

confidence: 99%

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Redundant and cryptic enhancer activities of the Drosophilayellowgene

Kalay

Lachowiec

Rosas

et al. 2018

Preprint

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cis-regulatory sequences known as enhancers play a key role in regulating gene expression. Evolutionary changes in these DNA sequences contribute to phenotypic evolution. The Drosophila yellow gene, which is required for pigmentation, has emerged as a model system for understanding how cis-regulatory sequences evolve, providing some of the most detailed insights available into how activities of orthologous enhancers have diverged between species. Here, we examine the evolution of yellow cis-regulatory sequences on a broader scale by comparing the distribution and function of yellow enhancer activities throughout the 5' intergenic and intronic sequences of Drosophila melanogaster, Drosophila pseudoobscura, and Drosophila willistoni. We find that cis-regulatory sequences driving expression in a particular tissue are not as modular as previously described, but rather have many redundant and cryptic enhancer activities distributed throughout the regions surveyed. Interestingly, cryptic enhancer activities of sequences from one species often drove patterns of expression observed in other species, suggesting that the frequent evolutionary changes in yellow expression observed among Drosophila species may be facilitated by gaining and losing repression of pre-existing cis-regulatory sequences.

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Section: Redundant Enhancers Are Common For the Yellow Genementioning

confidence: 87%

Section: Conservation and Divergence Of Enhancer Activities Are Not Wmentioning

confidence: 99%

Redundant and cryptic enhancer activities of the Drosophilayellowgene

Kalay

Lachowiec

Rosas

et al. 2018

Preprint

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“…Indeed, for bab1, the bab A128 allele has been shown to be associated with complete loss of Bab1 without affecting Bab2 levels (confirmed in the present study), but no equivalent allele has been characterized for bab2 (Chalvet et al, 2011;Couderc et al, 2002). Two studies have now addressed the question of redundancy between the two bab genes using tissue-specific expression of bab1 and bab2 RNAi constructs, for abdomen pigmentation (Roeske et al, 2018) and the present study for ovarian GSC niche formation. Roeske et al (Roeske et al, 2018) showed that both bab1 and bab2 are necessary for repression of pigmentation of female abdomen segments A5 and A6.…”

Section: Bab 1 and Bab2 Are Redundant In Precursor Niche Cells For Fumentioning

confidence: 99%

“…Two studies have now addressed the question of redundancy between the two bab genes using tissue-specific expression of bab1 and bab2 RNAi constructs, for abdomen pigmentation (Roeske et al, 2018) and the present study for ovarian GSC niche formation. Roeske et al (Roeske et al, 2018) showed that both bab1 and bab2 are necessary for repression of pigmentation of female abdomen segments A5 and A6. However, since depletion of both proteins leads to a much stronger female pigmentation defect than depletion of each one separately, this and other results led the authors to propose that 4 doses of Bab proteins, provided in the wildtype by the presence of the two paralogs, are needed to repress expression of a pigmentation gene, yellow, in the female abdomen.…”

Section: Bab 1 and Bab2 Are Redundant In Precursor Niche Cells For Fumentioning

confidence: 99%

The Bric-à-Brac transcription factors are necessary for formation of functional germline stem cell niches through control ofdppexpression in theDrosophila melanogasterovary

Saler

Bartoletti

Hauser

et al. 2019

Preprint

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Many studies have focused on the mechanisms of stem cell maintenance via their interaction with a particular niche or microenvironment in adult tissues, but how formation of a functional niche is initiated, including how stem cells within a niche are established, is less well understood. Adult Drosophila melanogaster ovary Germline Stem Cell (GSC) niches are comprised of somatic cells forming a stack called a Terminal Filament (TF) and underlying Cap Cells (CCs) and Escort Cells (ECs), which are in direct contact with GSCs. In the adult, the Engrailed (En) transcription factor is specifically expressed in niche cells where it directly controls expression of the decapentaplegic gene (dpp) encoding a member of the Bone Morphogenetic Protein (BMP) family of secreted signaling molecules, which are key factors for GSC maintenance. In late third instar larval ovaries, in response to BMP signaling from newly-formed niches, adjacent primordial germ cells become GSCs. The bric-àbrac paralogs (bab1 and bab2) encode BTB/POZ-domain containing transcription factors, that are also expressed in developing GSCs niches where they are required for TF formation. Here, we demonstrate that Bab1 and Bab2 display redundant cell autonomous function for TF morphogenesis and we identify a new function for these genes in GSC establishment. Moreover, we show that Bab proteins control dpp expression in otherwise correctly specified CCs, independently of En and its paralog Invected (Inv). In fact, our results also indicate that en/inv function in larval stages are neither essential for TF formation, nor GSC establishment. Finally, when bab2 was overexpressed in ovarian somatic cells outside of the niche, where en/inv were not expressed, ectopic BMP signaling activation was induced in adjacent germ cells of adult ovaries, which formed GSC-like tumors.Together, these results indicate that Bab transcription factors are positive regulators of BMP signaling for acquisition of GSC status.

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“…A y body enhancer, adjacent to the wing enhancer ( Fig. 2a) and that receives indirect inputs from the sex-determination hierarchy, directs this male-specific expression pattern 14 . We compared the reporter activity of the y::mCherry 25kb transgene inserted on the X chromosome in hemizygous males, hetero-and homozygous females (Extended Data Fig.…”

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confidence: 99%

trans-homolog interaction regulates the sex-biased expression of an X-linked gene

Galouzis

Prud’homme

2020

Preprint

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Sex-biased gene expression patterns in animals are generally controlled by the somatic sex-determination hierarchies. How the different tiers of these hierarchies act on sexually dimorphic gene regulation is still poorly understood. In the developing Drosophila biarmipes wing, the X-linked gene yellow is expressed in males in a specific distal spot pattern that prefigures a corresponding adult pigmentation pattern. This yellow expression pattern is controlled by the spot enhancer, but the origin of yellow sexually dimorphic expression is unknown. Here we find that the functional interaction between homologous yellow alleles silences specifically the spot enhancer, which is therefore active in males (XY) but not in females (XX). We show that inserting yellow at homologous positions on autosomes recapitulates, in either sex, the homologousdependent silencing of the spot enhancer. We further find that this silencing requires the yellow intron as well as the architectural protein Mod(mdg4). Finally, we show that Mod(mdg4) is also necessary for the sex-biased expression of some X-linked genes in the brain. Our results demonstrate that regulatory interactions between X-linked homologous alleles promote their sex-biased expression, independently of the canonical sex-determination hierarchy. More generally, they illustrate the biological significance of homologous chromosome pairing and trans-homolog interactions for the sexually dimorphic regulation of X-linked genes.Sexual dimorphism in morphology, physiology and behaviour is pervasive in animals. Sexbiased gene expression patterns, deployed during embryonic or adult development, direct the formation of these phenotypic sex-specific differences 1 . It is well established that the transcriptional regulators of the somatic sex-determination hierarchies directly control sexually dimorphic gene regulation 1-3 . Yet, the different tiers of these hierarchies seem to contribute to this control through a variety of regulatory mechanisms 1-7 . To better understand the molecular mechanisms governing sexually dimorphic gene regulation, we examined the dimorphic regulation of the yellow (y) gene in D. biarmipes, a species that has evolved a male-specific wing pigmentation spot ( Fig. 1a) 8,9 . During late pupal wing development in D.biarmipes males, Yellow spatial distribution prefigures the adult pigmentation spot (Fig. 1b).In females, only a handful of cells produce Yellow, forming a typical dotted, stochastic pattern (Fig. 1d). Accordingly, almost no pigmentation pattern appears in adult females (Fig. 1c). We first examined the contribution of the top tier of the somatic sex-determination hierarchy, which initiates and establishes female identity in a cell-autonomous manner in

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Cis-regulatory evolution integrated the Bric-à-brac transcription factors into a novel fruit fly gene regulatory network

Cited by 40 publications

References 44 publications

Redundant and cryptic enhancer activities of the Drosophilayellowgene

Redundant and cryptic enhancer activities of the Drosophilayellowgene

The Bric-à-Brac transcription factors are necessary for formation of functional germline stem cell niches through control ofdppexpression in theDrosophila melanogasterovary

trans-homolog interaction regulates the sex-biased expression of an X-linked gene

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