Evolutionary changes in TGFα distribution underlie morphological diversity in eggshells from <i>Drosophila</i> species

Niepielko, Matthew G.; Yakoby, Nir

doi:10.1242/dev.111898

Cited by 10 publications

(10 citation statements)

References 42 publications

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“…Species with a dorsal ridge exhibit an unusual staining pattern at stage 10 for diphosphorylated ERK (dpERK), a marker for EGFR signaling. In many species, dpERK is confined to the dorsal anterior region, where the midline and appendage cell types will be specified, but in species with a dorsal ridge, dpERK extends more posteriorly, along the dorsal midline (Niepielko and Yakoby, 2014). The dorsal midline is located over the path the nucleus would be expected to traverse as it moves from the posterior of the oocyte, during early oogenesis, to the dorsal anterior, where it resides in mid and late oogenesis.…”

Section: Evolutionmentioning

confidence: 99%

“…Indeed, grk knockdown by RNAi inhibits dorsal ridge formation in D. willistoni , a species that normally produces this structure. Strikingly, expressing the D. willistoni Grk protein (wGRK) in D. melanogaster not only rescues a grk mutant, but it can also cause the formation of a partial dorsal ridge (Niepielko and Yakoby, 2014). These exciting findings raise the question of how differences in Grk between D. willistoni and D. melanogaster control this aspect of morphology; possibilities may include differences in signal strength, or in ligand anchoring or stability (Niepielko and Yakoby, 2014).…”

Section: Evolutionmentioning

confidence: 99%

“…In addition to describing the Grk and Dpp gradients in Drosophila melanogaster, these models have facilitated mechanistic interpretation of quantitative changes in the spatial patterns of Grk and Dpp observed in related fly species (Niepielko et al, 2012; Zartman et al, 2011). For instance, within the framework of reaction-diffusion models, a dramatically elongated pattern of Grk observed in D. willistoni can be explained by quantitative changes in the diffusion and endocytic uptake rates of secreted Grk (Niepielko and Yakoby, 2014). …”

Section: Computational Modeling Of Pattern Formation and Morphogenesismentioning

confidence: 99%

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Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

2017

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Summary Understanding the mechanisms driving tissue and organ formation requires knowledge across scales. How do signaling pathways specify distinct tissue types? How does the patterning system control morphogenesis? How do these processes evolve? The Drosophila egg chamber, where EGF and BMP signaling intersect to specify unique cell types that construct epithelial tubes for specialized eggshell structures, has provided a tractable system to ask these questions. Work there has elucidated connections between scales of development, including across evolutionary scales, and fostered the development of quantitative modeling tools. These tools and general principles can be applied towards understanding other developmental processes across organisms.

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Section: Evolutionmentioning

confidence: 99%

Section: Evolutionmentioning

confidence: 99%

Section: Computational Modeling Of Pattern Formation and Morphogenesismentioning

confidence: 99%

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Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

2017

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“…In other situations, however, ligand concentration, not the identity of the ligand itself, determines the developmental outcome (Austin et al 2014). Previous studies using genomic regions to rescue grk null mutants showed that expression of Drosophila willistoni grk in D. melanogaster can induce an ectopic dorsal ridge structure in eggshells (Niepielko and Yakoby 2014). Unfortunately, the available scaffold in S. lebanonensis (Vicoso and Bachtrog 2015) lacks potentially important upstream and downstream regulatory regions, and we were unable to bridge the gap with the flanking genes predicted by synteny, D12 and AKAP200 .…”

Section: Resultsmentioning

confidence: 99%

Two Drosophilids exhibit distinct EGF pathway patterns in oogenesis

et al. 2017

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Deciphering the evolution of morphological structures is a remaining challenge in the field of developmental biology. The respiratory structures of insect eggshells, called the dorsal appendages, provide an outstanding system for exploring these processes since considerable information is known about their patterning and morphogenesis in Drosophila melanogaster and dorsal appendage number and morphology vary widely across Drosophilid species. We investigated the patterning differences that might facilitate morphogenetic differences between D. melanogaster, which produces two oar-like structures first by wrapping and then elongating the tubes via cell intercalation and cell crawling, and Scaptodrosophila lebanonensis, which produces a variable number of appendages simply by cell intercalation and crawling. Analyses of BMP pathway components thickveins and P-Mad demonstrate that anterior patterning is conserved between these species. In contrast, EGF signaling exhibits significant differences. Transcripts for the ligand encoded by gurken localize similarly in the two species, but this morphogen creates a single dorsolateral primordium in S. lebanonensis as defined by activated MAP kinase and the downstream marker broad. Expression patterns of pointed, argos, and Capicua, early steps in the EGF pathway, exhibit a heterochronic shift in S. lebanonensis relative to those seen in D. melanogaster. We demonstrate that the S. lebanonensis Gurken homolog is active in D. melanogaster but is insufficient to alter downstream patterning responses, indicating that Gurken-EGF receptor interactions do not distinguish the two species' patterning. Altogether, these results differentiate EGF signaling patterns between species and shed light on how changes to the regulation of patterning genes may contribute to different tube-forming mechanisms.

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“…1F) (32,36) In contrast to D. melanogaster, which lacks the dorsal ridge and is patterned by GRK localized around the oocyte nucleus (Fig. 4E), D. willistoni is patterned by the GRK profile that is significantly extended toward the posterior end of the follicular epithelium (45) (Fig. 4F).…”

Section: From D Melanogaster To Other Speciesmentioning

confidence: 97%

Gene regulation during Drosophila eggshell patterning

Pyrowolakis

Veikkolainen

Yakoby

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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A common path to the formation of complex 3D structures starts with an epithelial sheet that is patterned by inductive cues that control the spatiotemporal activities of transcription factors. These activities are then interpreted by the cis-regulatory regions of the genes involved in cell differentiation and tissue morphogenesis. Although this general strategy has been documented in multiple developmental contexts, the range of experimental models in which each of the steps can be examined in detail and evaluated in its effect on the final structure remains very limited. Studies of the Drosophila eggshell patterning provide unique insights into the multiscale mechanisms that connect gene regulation and 3D epithelial morphogenesis. Here we review the current understanding of this system, emphasizing how the recent identification of cis-regulatory regions of genes within the eggshell patterning network enables mechanistic analysis of its spatiotemporal dynamics and evolutionary diversification. It appears that cis-regulatory changes can account for only some aspects of the morphological diversity of Drosophila eggshells, such as the prominent differences in the number of the respiratory dorsal appendages. Other changes, such as the appearance of the respiratory eggshell ridges, are caused by changes in the spatial distribution of inductive signals. Both types of mechanisms are at play in this rapidly evolving system, which provides an excellent model of developmental patterning and morphogenesis.enhancer | network | evolution | signal | dynamics

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Evolutionary changes in TGFα distribution underlie morphological diversity in eggshells from Drosophila species

Cited by 10 publications

References 42 publications

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

Epithelial Patterning, Morphogenesis, and Evolution: Drosophila Eggshell as a Model

Two Drosophilids exhibit distinct EGF pathway patterns in oogenesis

Gene regulation during Drosophila eggshell patterning

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