The selector genes midline and H15 control ventral leg pattern by both inhibiting Dpp signaling and specifying ventral fate

Svendsen, Pia; Phillips, Lindsay A.; Deshwar, Ashish R.; Ryu, Jae-Ryeon; Najand, Nima; Brook, William J.

doi:10.1016/j.ydbio.2019.05.012

Cited by 9 publications

(29 citation statements)

References 56 publications

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“…Therefore, functional studies targeting a single Wnt gene, as performed in Oncopeltus [ 1 ], could easily overlook the involvement of Wnt-patterning in ventral vs dorsal appendage development. To circumvent problems caused by redundant function(s) of multiple Wnts in studying arthropod limb development, known downstream targets of Wnt, such as the T-box encoding transcription factor H15 / midline, could instead be addressed by means of e.g., RNAi-mediated knockdown [ 38 , 71 , 86 , 87 ]. Another transcription factor that is expressed along the ventral sector of all appendages in all arthropods and even an onychophoran is the forkhead-box encoding gene FoxB .…”

Section: Discussionmentioning

confidence: 99%

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

Janßen

Pechmann

Turetzek

2021

EvoDevo

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The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution.

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Section: Discussionmentioning

confidence: 99%

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

Janßen

Pechmann

Turetzek

2021

EvoDevo

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“…Our previous work showed that the eh1 repressor binding domain was required for Mid selector gene function. We also showed that Mid acted by antagonizing Dpp signaling, reducing the levels of pMad accumulation in the ventral domain of the fly leg (Svendsen et al, 2019).…”

Section: Mid Blocks Dpp Activation Of Dad13 Reporter Expressionmentioning

confidence: 61%

“…While Dpp does not contribute to ventral patterning, 3 double mutant analysis shows mid H15 mutant clones blocked for Dpp signaling are rescued in some regions of the leg, indicating an inhibitory effect of mid on Dpp signaling that is necessary for ventral patterning. This is further demonstrated by the inhibition of pMad accumulation by mid (Svendsen et al, 2019). Additionally, mid-expressing clones repress the Dpp-target genes Dad, Upd3, and mid itself in an eh1-dependent manner, and using chromatinimmunoprecipitation (ChIP) assays, Mid has been shown to localize to enhancers for these genes (Svendsen et al, 2019).…”

Section: Introductionmentioning

confidence: 94%

“…This is further demonstrated by the inhibition of pMad accumulation by mid (Svendsen et al, 2019). Additionally, mid-expressing clones repress the Dpp-target genes Dad, Upd3, and mid itself in an eh1-dependent manner, and using chromatinimmunoprecipitation (ChIP) assays, Mid has been shown to localize to enhancers for these genes (Svendsen et al, 2019).…”

Section: Introductionmentioning

confidence: 94%

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midline represses Dpp signaling and target gene expression in Drosophila ventral leg development

Phillips

Atienza

Ryu

et al. 2021

Preprint

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Ventral leg patterning in Drosophila is controlled by the expression of the redundant T-box Transcription factors midline (mid) and H15. Here we show that mid represses the Dpp-activated gene Daughters against decapentaplegic (Dad) through a consensus TBE site in the minimal enhancer, Dad13. Mutating the Dad13 DNA sequence results in an increased and broadening of Dad expression. We further demonstrate that the engrailed-homology-1 domain of Mid is critical for regulating the levels of phospho-Mad, a transducer of Dpp-signaling. However, we find that mid does not affect all Dpp-target genes as we demonstrate that brinker (brk) expression is unresponsive to mid. This study further illuminates the interplay between mechanisms involved in determination of cellular fate and the varied roles of mid.Summary statementVentral patterning is controlled in part by the T-box Transcription factor midline blocking Dpp signaling and Dpp-activated genes, though midline does not affect the Dpp-repressed gene brk.

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“…In the ventral domain of the leg, Wg activates while Dpp represses the expression of the redundant genes H15 and midline (mid) that act as selector genes for ventral fates, promoting the acquisition of ventral identity. Accordingly, mutants for H15/mid lack ventral leg structures or these are transformed to dorsal, whereas when ectopically expressed in the dorsal domain, H15/mid induce ventral fates (Svendsen et al, 2009(Svendsen et al, , 2019. In the dorsal domain, the expression of the T-box genes optomotor-blind (omb) and the Dorsocross (Doc) 1, 2, and 3 are able to repress ventral genes (Maves and Schubiger, 1998;Reim et al, 2003;Svendsen et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Role of the Forkhead Transcription Factors Fd4 and Fd5 During Drosophila Leg Development

Ruiz-Losada

Pérez-Reyes

Estella

2021

Front. Cell Dev. Biol.

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Appendage development requires the coordinated function of signaling pathways and transcription factors to pattern the leg along the three main axes: the antero-posterior (AP), proximo-distal (PD), and dorso-ventral (DV). The Drosophila leg DV axis is organized by two morphogens, Decapentaplegic (Dpp), and Wingless (Wg), which direct dorsal and ventral cell fates, respectively. However, how these signals regulate the differential expression of its target genes is mostly unknown. In this work, we found that two members of the Drosophila forkhead family of transcription factors, Fd4 and Fd5 (also known as fd96Ca and fd96Cb), are identically expressed in the ventro-lateral domain of the leg imaginal disc in response to Dpp signaling. Here, we analyze the expression regulation and function of these genes during leg development. We have generated specific mutant alleles for each gene and a double fd4/fd5 mutant chromosome to study their function during development. We highlight the redundant role of the fd4/fd5 genes during the formation of the sex comb, a male specific structure that appears in the ventro-lateral domain of the prothoracic leg.

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The selector genes midline and H15 control ventral leg pattern by both inhibiting Dpp signaling and specifying ventral fate

Cited by 9 publications

References 56 publications

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

midline represses Dpp signaling and target gene expression in Drosophila ventral leg development

Role of the Forkhead Transcription Factors Fd4 and Fd5 During Drosophila Leg Development

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