Antagonism between germ cell-less and Torso receptor regulates transcriptional quiescence underlying germline/soma distinction

Colonnetta, Megan M; Lym, Lauren R; Wilkins, Lillian; Kappes, Gretchen; Castro, Elias A; Ryder, Pearl V.; Schedl, Paul; Lerit, Dorothy A.; Deshpande, Girish

doi:10.7554/elife.54346

Cited by 3 publications

(14 citation statements)

References 51 publications

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“…Instead, they spread into the posterior region of the embryo and are found associated with somatic nuclei. A similar disruption in the proper distribution of pole plasm during PGC cellularization was found when the terminal pathway was upregulated by blocking degradation of Torso, or by a constitutive allele of the downstream MEK kinase [12]. Moreover, as shown here, we find that Vasa is lost from PGCs when the terminal pathway is optogenetically activated at the posterior of the embryo.…”

Section: Discussionsupporting

confidence: 85%

“…Studies by Pae et al (2017) [65] showed that Gcl targets the terminal pathway receptor Torso for proteolytic degradation, thereby shutting down the pathway at the very posterior pole of the embryo. When the terminal signaling cascade is activated at the posterior pole, either in gcl mutants or by gain-of-function mutations in the Torso receptor or its downstream kinases, pole plasm components are not properly incorporated into PGCs when they cellularize [12]. These observations raise the possibility that the BMP pathway might be needed to help suppress the terminal signaling pathway.…”

Section: Bmp Signaling Is Required To Suppress the Functioning Of The Terminal Pathwaymentioning

confidence: 99%

“…This normalization was done for each condition separately. These normalized intensities for individual embryos were plotted and presented in Fig 4 . smFISH was performed as previously described using formaldehyde-fixed embryos [12]. All probe sets were designed using the Stellaris probe designer (20-nucleotide oligonucleotides with 2-nucleotide spacing).…”

Section: Fluorescence In Situ Hybridization (Fish) and Single Molecule Fish (Smfish)mentioning

confidence: 99%

“…In flies, PGCs are formed after the onset of the minor wave of ZGA, which begins at nuclear cycle (NC) 8. During their formation, ongoing transcription is turned off by germ-cell less (gcl) [11,12] while genes activated during the major wave of ZGA (NC14) are kept off by combined action of polar granule component (pgc) [13][14][15] and nanos (nos) [16][17][18]. Broad downregulation of transcription is reflected in the phosphorylation status of the RNA polymerase II CTD domain.…”

Section: Introductionmentioning

confidence: 99%

“…During bud formation, the centrosomes/microtubule network associated with each incoming nucleus triggers the release of localized PGC determinants from the posterior cortical cytoskeleton, and these factors are then incorporated into the newly formed PGCs during cellularization [37,38]. When these factors are not properly sequestered in the newly formed PGCs, PGC specification fails [12,[38][39][40].…”

Section: Introductionmentioning

confidence: 99%

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Preformation and epigenesis converge to specify primordial germ cell fate in the early Drosophila embryo

et al. 2022

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A critical step in animal development is the specification of primordial germ cells (PGCs), the precursors of the germline. Two seemingly mutually exclusive mechanisms are implemented across the animal kingdom: epigenesis and preformation. In epigenesis, PGC specification is non-autonomous and depends on extrinsic signaling pathways. The BMP pathway provides the key PGC specification signals in mammals. Preformation is autonomous and mediated by determinants localized within PGCs. In Drosophila, a classic example of preformation, constituents of the germ plasm localized at the embryonic posterior are thought to be both necessary and sufficient for proper determination of PGCs. Contrary to this longstanding model, here we show that these localized determinants are insufficient by themselves to direct PGC specification in blastoderm stage embryos. Instead, we find that the BMP signaling pathway is required at multiple steps during the specification process and functions in conjunction with components of the germ plasm to orchestrate PGC fate.

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Section: Discussionsupporting

confidence: 85%

Section: Bmp Signaling Is Required To Suppress the Functioning Of The Terminal Pathwaymentioning

confidence: 99%

Section: Fluorescence In Situ Hybridization (Fish) and Single Molecule Fish (Smfish)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Preformation and epigenesis converge to specify primordial germ cell fate in the early Drosophila embryo

et al. 2022

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Finishing the egg

Berg,

Sieber,

Sun

2023

Genetics

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Gamete development is a fundamental process that is highly conserved from early eukaryotes to mammals. As germ cells develop, they must coordinate a dynamic series of cellular processes that support growth, cell specification, patterning, the loading of maternal factors (RNAs, proteins, and nutrients), differentiation of structures to enable fertilization and ensure embryonic survival, and other processes that make a functional oocyte. To achieve these goals, germ cells integrate a complex milieu of environmental and developmental signals to produce fertilizable eggs. Over the past 50 years, Drosophila oogenesis has risen to the forefront as a system to interrogate the sophisticated mechanisms that drive oocyte development. Studies in Drosophila have defined mechanisms in germ cells that control meiosis, protect genome integrity, facilitate mRNA trafficking, and support the maternal loading of nutrients. Work in this system has provided key insights into the mechanisms that establish egg chamber polarity and patterning as well as the mechanisms that drive ovulation and egg activation. Using the power of Drosophila genetics, the field has begun to define the molecular mechanisms that coordinate environmental stresses and nutrient availability with oocyte development. Importantly, the majority of these reproductive mechanisms are highly conserved throughout evolution, and many play critical roles in the development of somatic tissues as well. In this chapter, we summarize the recent progress in several key areas that impact egg chamber development and ovulation. First, we discuss the mechanisms that drive nutrient storage and trafficking during oocyte maturation and vitellogenesis. Second, we examine the processes that regulate follicle cell patterning and how that patterning impacts the construction of the egg shell and the establishment of embryonic polarity. Finally, we examine regulatory factors that control ovulation, egg activation, and successful fertilization.

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Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation

Colonnetta

Schedl

Deshpande

2023

eLife

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In Drosophila melanogaster embryos, somatic versus germline identity is the first cell fate decision. Zygotic genome activation (ZGA) orchestrates regionalized gene expression, imparting specific identity on somatic cells. ZGA begins with a minor wave that commences at nuclear cycle (NC)8 under the guidance of chromatin accessibility factors (Zelda, CLAMP, GAF), followed by the major wave during NC14. By contrast, primordial germ cell (PGC) specification requires maternally deposited and posteriorly anchored germline determinants. This is accomplished by a centrosome coordinated release and sequestration of germ plasm during the precocious cellularization of PGCs in NC10. Here, we report a novel requirement for Zelda and CLAMP during the establishment of the germline/soma distinction. When their activity is compromised, PGC determinants are not properly sequestered, and specification is disrupted. Conversely, the spreading of PGC determinants from the posterior pole adversely influences transcription in the neighboring somatic nuclei. These reciprocal aberrations can be correlated with defects in centrosome duplication/separation that are known to induce inappropriate transmission of the germ plasm. Interestingly, consistent with the ability of bone morphogenetic protein (BMP) signaling to influence specification of embryonic PGCs, reduction in the transcript levels of a BMP family ligand, decapentaplegic (dpp), is exacerbated at the posterior pole.

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Antagonism between germ cell-less and Torso receptor regulates transcriptional quiescence underlying germline/soma distinction

Cited by 3 publications

References 51 publications

Preformation and epigenesis converge to specify primordial germ cell fate in the early Drosophila embryo

Preformation and epigenesis converge to specify primordial germ cell fate in the early Drosophila embryo

Finishing the egg

Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation

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