A translational block to HSPG synthesis permits BMP signaling in the early Drosophila embryo

AbstractIn a developing animal, morphogen gradients act to pattern tissues into distinct domains of cell types. However, despite their prevalence in development, morphogen gradient formation is a matter of debate. In our recent publication, we showed that the Dorsal/NF-κB morphogen gradient, which patterns the DV axis of the early Drosophila embryo, is partially established by a mechanism of facilitated diffusion. This mechanism, also known as “shuttling,” occurs when a binding partner of the morphogen facilitates the diffusion of the morphogen, allowing it to accumulate at a given site. In this case, the inhibitor Cactus/IκB facilitates the diffusion of Dorsal/NF-κB. In the fly embryo, we used computation and experiment to not only show that shuttling occurs in the embryo, but also that it enables the viability of embryos that inherit only one copy of dorsal maternally. Here we further discuss our evidence behind the shuttling mechanism, the previous literature data explained by the mechanism, and how it may also be critical for robustness of development. Finally, we describe an interaction between Dorsal and BMP signaling that is likely affected by shuttling.

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Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen

Development ◽

10.1242/dev.109.4.811 ◽

1990 ◽

Vol 109 (4) ◽

pp. 811-820 ◽

Cited By ~ 16

Author(s):

W. Driever ◽

V. Siegel ◽

C. Nusslein-Volhard

Keyword(s):

Drosophila Embryo ◽

Beta Globin ◽

P Transformation ◽

Early Drosophila Embryo ◽

Maternal Effect Genes ◽

Translational Block ◽

Maternal Gene ◽

Anterior Posterior

A small number of maternal effect genes determine anterior-posterior pattern in the Drosophila embryo. Embryos from females mutant for the maternal gene bicoid lack head and thorax. bcd mRNA becomes localized to the anterior tip of the egg during oogenesis and is the source for the morphogen gradient of bcd protein. Here we show that in vitro transcribed bicoid mRNA that has its own leader sequences substituted by the Xenopus beta-globin 5′ untranslated sequences is translated more efficiently than bicoid mRNA with the natural 5′ mRNA leader when tested in vitro and in Drosophila Schneider cells. When injected into bicoid mutant embryos, only the bcd mRNA with the beta-globin leader sequence, substituted for the natural leader, is able to induce anterior development. We used P-transformation to show that sequences in the 5′ leader are neither necessary for localization of the transcript nor for the translational block of the bcd mRNA during oogenesis. For our injection experiments, we used only one of the identified splicing forms of bcd mRNA. The bcd protein species derived from this mRNA is able to induce anterior development at any position along the anterior-posterior axis. Thus bicoid protein can induce development of head and thorax independent of any other specifically localized morphogenetic factor. Our findings further support the notion that the concentration gradient of bcd protein, and not the existence of different forms of bcd protein, is responsible for specifying subregions of the embryo.

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

PLoS Genetics ◽

10.1371/journal.pgen.1010002 ◽

2022 ◽

Vol 18 (1) ◽

pp. e1010002

Author(s):

Megan M. Colonnetta ◽

Yogesh Goyal ◽

Heath E. Johnson ◽

Sapna Syal ◽

Paul Schedl ◽

...

Keyword(s):

Cell Fate ◽

Germ Plasm ◽

Primordial Germ Cells ◽

Primordial Germ Cell ◽

Bmp Signaling ◽

Drosophila Embryo ◽

Animal Development ◽

Early Drosophila Embryo ◽

Bmp Pathway ◽

Necessary And Sufficient

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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