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

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    Evaluation Summary:

    The early differentiation of germ cells, those that will form egg and sperm, is a critical and nearly universal step in animal development. This paper reveals new layers of molecular and cellular regulation that control this process in the fly, and as such be of broad interest to cell and developmental biologists, especially those interested in critical cell fate decisions. The paper contains a wealth of experimental data demonstrating that processes generally thought to be restricted to somatic cells alter the differentiation of germ cells, but provides only limited functional interpretation of the observed phenotypes.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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Abstract

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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  1. Evaluation Summary:

    The early differentiation of germ cells, those that will form egg and sperm, is a critical and nearly universal step in animal development. This paper reveals new layers of molecular and cellular regulation that control this process in the fly, and as such be of broad interest to cell and developmental biologists, especially those interested in critical cell fate decisions. The paper contains a wealth of experimental data demonstrating that processes generally thought to be restricted to somatic cells alter the differentiation of germ cells, but provides only limited functional interpretation of the observed phenotypes.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers …

  2. Reviewer #1 (Public Review):

    Primordial germ cells are formed in the posterior pole of developing Drosophila embryo via taking up of maternally supplied germline determinants (a.k.a., germ plasm). PGC formation occurs approximately at the stage of 10th nuclear division cycle, located between minor and major ZGA waves which take place in somatic nuclei. Zelda and CLAMP are two key factors essential for global zygotic genome activation in soma. Since Zelda mutant retain apparently intact PGCs, Zelda has been thought to be dispensable for PGC formation. However, in this study, the authors identified slight loss of PGC number in both mutants lacking Zelda and CLAMP, which led authors propose a model in which somatic ZGA factors influence PGC specification.

    The authors show that maternal or zygotic RNAi against Zelda or CLAMP caused …

  3. Reviewer #2 (Public Review):

    Colonetta, Schedl, and Deshpande evaluated how loss of regulators of Zygotic Genome Activation (ZGA) impacts the germ-soma decision in early Drosophila embryos. The prevailing view of that decision in fly embryos has been that ZGA regulates the turn-on of somatic genes in the syncytial embryo and that the primordial germ cells or pole cells, which are cellularized at an earlier stage than somatic cells, are not influenced by ZGA. The authors tested that by eliminating 2 ZGA regulators, Zelda and CLAMP, either maternally or zygotically (but see below), and imaging markers of pole cells and markers of somatic cells. They found that loss of ZGA regulators caused pole cells to display some somatic features and caused somatic cells to display some pole cell features. Specific pole cell defects in mutant embryos …