Abstract
IntroductionEstablishment of distinct follicle cell fates at the early stages of Drosophila oogenesis is crucial for achieving proper morphology of individual egg chambers. In Drosophila oogenesis, Notch-signaling controls proliferation and differentiation of follicular cells, which eventually results in the polarization of the anterior-posterior axis of the oocyte. Here we analyzed the functions of Tribolium Notch-signaling factors during telotrophic oogenesis, which differs fundamentally from the polytrophic ovary of Drosophila.ResultsWe found Notch-signaling to be required for maintaining the mitotic cycle of somatic follicle cells. Upon Delta RNAi, follicle cells enter endocycle prematurely, which affects egg-chamber formation and patterning. Interestingly, our results indicate that Delta RNAi phenotypes are not solely due to the premature termination of cell proliferation. Therefore, we monitored the terminal/stalk cell precursor lineage by molecular markers. We observed that upon Delta RNAi terminal and stalk cell populations were absent, suggesting that Notch-signaling is also required for the specification of follicle cell populations, including terminal and stalk precursor cells.ConclusionsWe demonstrate that with respect to mitotic cycle/endocycle switch Notch-signaling in Tribolium and Drosophila has opposing effects. While in Drosophila a Delta-signal brings about the follicle cells to leave mitosis, Notch-signaling in Triboliumis necessary to retain telotrophic egg-chambers in an “immature” state. In most instances, Notch-signaling is involved in maintaining undifferentiated (or preventing specialized) cell fates. Hence, the role of Notch in Tribolium may reflectthe ancestral function of Notch-signaling in insect oogenesis.The functions of Notch-signaling in patterning the follicle cell epithelium suggest that Tribolium oogenesis may - analogous to Drosophila - involve the stepwise determination of different follicle cell populations. Moreover, our results imply that Notch-signaling may contribute at least to some aspects of oocyte polarization and AP axis also in telotrophic oogenesis.
Highlights
Establishment of distinct follicle cell fates at the early stages of Drosophila oogenesis is crucial for achieving proper morphology of individual egg chambers
While Serrate is not expressed during Tribolium oogenesis, we found Delta expression to be restricted to the germ line (Additional file 1: Figure S1)
Expression of Tribolium Delta resembles the situation in Drosophila, where Delta signals from the germ line to induce distinct follicle cell fates, and later controls the transition from proliferation to endoreplication
Summary
Establishment of distinct follicle cell fates at the early stages of Drosophila oogenesis is crucial for achieving proper morphology of individual egg chambers. The Notch family of receptors plays a central role in an evolutionarily conserved signaling pathway that regulates several cell fate decisions in many organisms [1]. Notch encodes a large transmembrane receptor for the ligands Delta (Dl), Serrate (Ser), which are transmembrane proteins with large extracellular domains, and signaling requires direct cell-cell contact. Insect oogenesis is one such example, where Notch-signaling regulates cell fate decisions of various cell types [1]. Three distinct follicle cell populations are eventually defined: polar cells, which serve as key signaling centers, stalk cells, which will form the short bridge that connects neighboring egg chambers, and main-body follicle cells, which form an epithelium overlying the germline cyst. Polar cell fate is induced in a restricted subset of this population by the Notch ligand Delta (Dl), which is produced in germline cells. Notch is required throughout the follicle cell epithelium to switch the main body cells from mitotic cell divisions to endoreplication [5,6]
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