Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis

The Bicaudal-D (Bic-D) gene is required early in Drosophila oogenesis for the differentiation of an oocyte from one of a cluster of 16 interconnected germarial cells. To analyze the role of Bic-D later in oogenesis, we have constructed Drosophila lines in which Bic-D expression is under the control of the hsp70 promoter. In these flies, Bic-D activity can be induced early in oogenesis, allowing an oocyte to be made. Then, by shifting females to non-inducing conditions, Bic-D levels are depleted for the remainder of oogenesis. Using this system, we find that Bic-D is indeed required in the later stages of oogenesis. In ovaries from mutant females, oocyte growth is reduced, apparently due to defects in nurse-cell-to-oocyte transport. Smaller oocyte size results in the misalignment of follicle cells and the underlying germ line, leading to ventralization of dorsal follicle cells and to defects in centripetal cell migration. In addition, we show that Bic-D is required for the localization of specific mRNAs at both the anterior and posterior of the oocyte.

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The TGF-beta signaling pathway is essential for Drosophila oogenesis

Development ◽

10.1242/dev.122.5.1555 ◽

1996 ◽

Vol 122 (5) ◽

pp. 1555-1565 ◽

Cited By ~ 29

Author(s):

V. Twombly ◽

R.K. Blackman ◽

H. Jin ◽

J.M. Graff ◽

R.W. Padgett ◽

...

Keyword(s):

Family Member ◽

Signaling Pathway ◽

Expression Pattern ◽

Nurse Cell ◽

Follicle Cells ◽

Tgf Beta ◽

Drosophila Oogenesis ◽

Egg Chamber

We examine roles of signaling by secreted ligands of the TGF-beta family during Drosophila oogenesis. One family member, the DPP ligand encoded by the decapentaplegic (dpp) gene, is required for patterning of anterior eggshell structures. This requirement presumably reflects the expression pattern of dpp in an anterior subset of somatic follicle cells: the centripetally migrating and the nurse cell-associated follicle cells. Similar requirements are also revealed by mutations in the saxophone (sax)-encoded receptor, consistent with the idea that DPP signaling is, at least in part, mediated by the SAX receptor. A loss of germline sax function results in a block in oogenesis associated with egg chamber degeneration and a failure of the transfer of nurse cell contents to the oocyte, indicating that TGF-beta signaling is required for these events. Some phenotypes of sax mutations during oogenesis suggest that SAX responds to at least one other TGF-beta ligand as well in the posterior follicle cells.

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Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras

Development ◽

10.1242/dev.119.4.1359 ◽

1993 ◽

Vol 119 (4) ◽

pp. 1359-1369 ◽

Cited By ~ 41

Author(s):

T.B. Chou ◽

E. Noll ◽

N. Perrimon

Keyword(s):

Tissue Specificity ◽

Germ Line ◽

Egg Laying ◽

P Element ◽

Follicle Cells ◽

Gtpase Activating Protein ◽

Lethal Mutations ◽

Sterile Technique ◽

Dominant Female ◽

Polarity Determination

The ‘dominant female-sterile’ technique used to generate germ-line mosaics in Drosophila is a powerful tool to determine the tissue specificity (germ line versus somatic) of recessive female-sterile mutations as well as to analyze the maternal effect of recessive zygotic lethal mutations. This technique requires the availability of germ-line-dependent, dominant female-sterile (DFS) mutations that block egg laying but do not affect viability. To date only one X-linked mutation, ovoD1 has been isolated that completely fulfills these criteria. Thus the ‘DFS technique’ has been largely limited to the X-chromosome. To extend this technique to the autosomes, we have cloned the ovoD1 mutation into a P-element vector and recovered fully expressed P[ovoD1] insertions on each autosomal arm. We describe the generation of these P[ovoD1] strains as well as demonstrate their use in generating germ-line chimeras. Specifically, we show that the Gap1 gene, which encodes a Drosophila homologue of mammalian GTPase-activating protein, is required in somatic follicle cells for embryonic dorsoventral polarity determination.

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Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis

Development ◽

10.1242/dev.125.15.2837 ◽

1998 ◽

Vol 125 (15) ◽

pp. 2837-2846 ◽

Cited By ~ 13

Author(s):

A. Gonzalez-Reyes ◽

D. St Johnston

Keyword(s):

Follicle Cell ◽

Cell Types ◽

Follicle Cells ◽

Follicular Epithelium ◽

Axis Formation ◽

Main Body ◽

Drosophila Oogenesis ◽

Egfr Mutant ◽

Anterior Posterior ◽

Anterior Posterior Axis

Gurken signals from the oocyte to the adjacent follicle cells twice during Drosophila oogenesis; first to induce posterior fate, thereby polarising the anterior-posterior axis of the future embryo and then to induce dorsal fate and polarise the dorsal-ventral axis. Here we show that Gurken induces two different follicle cell fates because the follicle cells at the termini of the egg chamber differ in their competence to respond to Gurken from the main-body follicle cells in between. By removing the putative Gurken receptor, Egfr, in clones of cells, we show that Gurken signals directly to induce posterior fate in about 200 cells, defining a terminal competence domain that extends 10–11 cell diameters from the pole. Furthermore, small clones of Egfr mutant cells at the posterior interpret their position with respect to the pole and differentiate as the appropriate anterior cell type. Thus, the two terminal follicle cell populations contain a symmetric prepattern that is independent of Gurken signalling. These results suggest a three-step model for the anterior-posterior patterning of the follicular epithelium that subdivides this axis into at least five distinct cell types. Finally, we show that Notch plays a role in both the specification and patterning of the terminal follicle cells, providing a possible explanation for the defect in anterior-posterior axis formation caused by Notch and Delta mutants.

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Infection of the germ line by retroviral particles produced in the follicle cells: a possible mechanism for the mobilization of the gypsy retroelement of Drosophila

Development ◽

10.1242/dev.124.14.2789 ◽

1997 ◽

Vol 124 (14) ◽

pp. 2789-2798 ◽

Cited By ~ 2

Author(s):

S.U. Song ◽

M. Kurkulos ◽

J.D. Boeke ◽

V.G. Corces

Keyword(s):

High Frequency ◽

Cytoplasmic Membrane ◽

De Novo ◽

Germ Line ◽

High Rate ◽

Follicle Cells ◽

Nurse Cells ◽

Perivitelline Space ◽

Viral Particles ◽

Secretory Apparatus

The gypsy retroelement of Drosophila moves at high frequency in the germ line of the progeny of females carrying a mutation in the flamenco (flam) gene. This high rate of de novo insertion correlates with elevated accumulation of full-length gypsy RNA in the ovaries of these females, as well as the presence of an env-specific RNA. We have prepared monoclonal antibodies against the gypsy Pol and Env products and found that these proteins are expressed in the ovaries of flam females and processed in the manner characteristic of vertebrate retroviruses. The Pol proteins are expressed in both follicle and nurse cells, but they do not accumulate at detectable levels in the oocyte. The Env proteins are expressed exclusively in the follicle cells starting at stage 9 of oogenesis, where they accumulate in the secretory apparatus of the endoplasmic reticulum. They then migrate to the inner side of the cytoplasmic membrane where they assemble into viral particles. These particles can be observed in the perivitelline space starting at stage 10 by immunoelectron microscopy using anti-Env antibodies. We propose a model to explain flamenco-mediated induction of gypsy mobilization that involves the synthesis of gypsy viral particles in the follicle cells, from where they leave and infect the oocyte, thus explaining gypsy insertion into the germ line of the subsequent generation.

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Drosophila YBX1 homolog YPS promotes ovarian germ line stem cell development by preferentially recognizing 5-methylcytosine RNAs

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1910862117 ◽

2020 ◽

Vol 117 (7) ◽

pp. 3603-3609 ◽

Cited By ~ 9

Author(s):

Fan Zou ◽

Renjun Tu ◽

Bo Duan ◽

Zhenlin Yang ◽

Zhaohua Ping ◽

...

Keyword(s):

Stem Cell ◽

Rna Binding ◽

Germ Line ◽

Adult Stem Cell ◽

Cell Development ◽

Rna Modification ◽

Proliferation And Differentiation ◽

Germ Line Stem Cell ◽

Rna Complex

5-Methylcytosine (m5C) is a RNA modification that exists in tRNAs and rRNAs and was recently found in mRNAs. Although it has been suggested to regulate diverse biological functions, whether m5C RNA modification influences adult stem cell development remains undetermined. In this study, we show that Ypsilon schachtel (YPS), a homolog of human Y box binding protein 1 (YBX1), promotes germ line stem cell (GSC) maintenance, proliferation, and differentiation in the Drosophila ovary by preferentially binding to m5C-containing RNAs. YPS is genetically demonstrated to function intrinsically for GSC maintenance, proliferation, and progeny differentiation in the Drosophila ovary, and human YBX1 can functionally replace YPS to support normal GSC development. Highly conserved cold-shock domains (CSDs) of YPS and YBX1 preferentially bind to m5C RNA in vitro. Moreover, YPS also preferentially binds to m5C-containing RNAs, including mRNAs, in germ cells. The crystal structure of the YBX1 CSD-RNA complex reveals that both hydrophobic stacking and hydrogen bonds are critical for m5C binding. Overexpression of RNA-binding–defective YPS and YBX1 proteins disrupts GSC development. Taken together, our findings show that m5C RNA modification plays an important role in adult stem cell development.

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Tissue Tropisms and Transstadial Transmission of a Rickettsia Endosymbiont in the Highland Midge, Culicoides impunctatus (Diptera: Ceratopogonidae)

Applied and Environmental Microbiology ◽

10.1128/aem.01492-20 ◽

2020 ◽

Vol 86 (20) ◽

Author(s):

Jack Pilgrim ◽

Stefanos Siozios ◽

Matthew Baylis ◽

Gregory D. D. Hurst

Keyword(s):

Vertical Transmission ◽

Fat Body ◽

Germ Line ◽

Horizontal Transmission ◽

Follicle Cells ◽

Biting Midges ◽

Diverse Range ◽

Suspensory Ligament ◽

Transstadial Transmission ◽

Tissue Tropisms

ABSTRACT Rickettsia is a genus of intracellular bacteria which can manipulate host reproduction and alter sensitivity to natural enemy attack in a diverse range of arthropods. The maintenance of Rickettsia endosymbionts in insect populations can be achieved through both vertical and horizontal transmission routes. For example, the presence of the symbiont in the follicle cells and salivary glands of Bemisia whiteflies allows Belli group Rickettsia transmission via the germ line and plants, respectively. However, the transmission routes of other Rickettsia bacteria, such as those in the Torix group of the genus, remain underexplored. Through fluorescence in situ hybridization (FISH) and transmission electron microscopy (TEM) screening, this study describes the pattern of Torix Rickettsia tissue tropisms in the highland midge, Culicoides impunctatus (Diptera: Ceratopogonidae). Of note is the high intensity of infection of the ovarian suspensory ligament, suggestive of a novel germ line targeting strategy. Additionally, localization of the symbiont in tissues of several developmental stages suggests transstadial transmission is a major route for ensuring maintenance of Rickettsia within C. impunctatus populations. Aside from providing insights into transmission strategies, the presence of Rickettsia bacteria in the fat body of larvae indicates potential host fitness and vector capacity impacts to be investigated in the future. IMPORTANCE Microbial symbionts of disease vectors have garnered recent attention due to their ability to alter vectorial capacity. Their consideration as a means of arbovirus control depends on symbiont vertical transmission, which leads to spread of the bacteria through a population. Previous work has identified a Rickettsia symbiont present in several species of biting midges (Culicoides spp.), which transmit bluetongue and Schmallenberg arboviruses. However, symbiont transmission strategies and host effects remain underexplored. In this study, we describe the presence of Rickettsia in the ovarian suspensory ligament of Culicoides impunctatus. Infection of this organ suggests the connective tissue surrounding developing eggs is important for ensuring vertical transmission of the symbiont in midges and possibly other insects. Additionally, our results indicate Rickettsia localization in the fat body of Culicoides impunctatus. As the arboviruses spread by midges often replicate in the fat body, this location implies possible symbiont-virus interactions to be further investigated.

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Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery

mBio ◽

10.1128/mbio.00532-12 ◽

2013 ◽

Vol 4 (2) ◽

Cited By ~ 53

Author(s):

Jeremy K. Herren ◽

Juan C. Paredes ◽

Fanny Schüpfer ◽

Bruno Lemaitre

Keyword(s):

Vertical Transmission ◽

Fat Body ◽

Germ Line ◽

Ovarian Follicle ◽

Follicle Cells ◽

Content Type ◽

Vector Borne Diseases ◽

Severe Reduction ◽

Female Germ Line ◽

Vector Borne

ABSTRACTSpiroplasmais a diverse bacterial clade that includes many vertically transmitted insect endosymbionts, includingSpiroplasma poulsonii, a natural endosymbiont ofDrosophila melanogaster. These bacteria persist in the hemolymph of their adult host and exhibit efficient vertical transmission from mother to offspring. In this study, we analyzed the mechanism that underlies their vertical transmission, and here we provide strong evidence that these bacteria use the yolk uptake machinery to colonize the germ line. We show thatSpiroplasmareaches the oocyte by passing through the intercellular space surrounding the ovarian follicle cells and is then endocytosed into oocytes within yolk granules during the vitellogenic stages of oogenesis. Mutations that disrupt yolk uptake by oocytes inhibit verticalSpiroplasmatransmission and lead to an accumulation of these bacteria outside the oocyte. Impairment of yolk secretion by the fat body results inSpiroplasmanot reaching the oocyte and a severe reduction of vertical transmission. We propose a model in whichSpiroplasmafirst interacts with yolk in the hemolymph to gain access to the oocyte and then uses the yolk receptor, Yolkless, to be endocytosed into the oocyte. Cooption of the yolk uptake machinery is a powerful strategy for endosymbionts to target the germ line and achieve vertical transmission. This mechanism may apply to other endosymbionts and provides a possible explanation for endosymbiont host specificity.IMPORTANCEMost insect species, including important disease vectors and crop pests, harbor vertically transmitted endosymbiotic bacteria. Studies have shown that many facultative endosymbionts, includingSpiroplasma, confer protection against different classes of parasites on their hosts and therefore are attractive tools for the control of vector-borne diseases. The ability to be efficiently transmitted from females to their offspring is the key feature shaping associations between insects and their inherited endosymbionts, but to date, little is known about the mechanisms involved. In oviparous animals, yolk accumulates in developing eggs and serves to meet the nutritional demands of embryonic development. Here we show thatSpiroplasma coopts the yolk transport and uptake machinery to colonize the germ line and ensure efficient vertical transmission. The uptake of yolk is a female germ line-specific feature and therefore an attractive target for cooption by endosymbionts that need to maintain high-fidelity maternal transmission.

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Requirement for cell-proliferation control genes in Drosophila oogenesis.

Genetics ◽

10.1093/genetics/127.3.525 ◽

1991 ◽

Vol 127 (3) ◽

pp. 525-533

Author(s):

J Szabad ◽

V A Jursnich ◽

P J Bryant

Keyword(s):

Cell Proliferation ◽

Germ Line ◽

Follicle Cell ◽

Mitotic Recombination ◽

Follicle Cells ◽

Egg Development ◽

Proliferation Control ◽

Dominant Female ◽

Female Germ Line ◽

Cell Proliferation Control

Abstract Genes that are required for cell proliferation control in Drosophila imaginal discs were tested for function in the female germ-line and follicle cells. Chimeras and mosaics were produced in which developing oocytes and nurse cells were mutant at one of five imaginal disc overgrowth loci (fat, lgd, lgl, c43 and dco) while the enveloping follicle cells were normal. The chimeras were produced by transplantation of pole cells and the mosaics were produced by X-ray-induced mitotic recombination using the dominant female-sterile technique. The results show that each of the genes tested plays an essential role in the development or function of the female germ line. The fat, lgl and c43 homozygous germ-line clones fail to produce eggs, indicating a germ-line requirement for the corresponding genes. Perdurance of the fat+ gene product in mitotic recombination clones allows the formation of a few infertile eggs from fat homozygous germ-line cells. The lgd homozygous germ-line clones give rise to a few eggs with abnormal chorionic appendages, a defect thought to result from defective cell communication between the mutant germ-line and the nonmutant follicle cells. One allele of dco (dcole88) prevents egg development when homozygous in the germ line, whereas the dco18 allele has no effect on germ-line development. Fs(2)Ugra, a recently described follicle cell-dependent dominant female-sterile mutation, allowed the analysis of egg primordia in which fat, lgd or lgl homozygous mutant follicle cells surrounded normal oocytes. The results show that the fat and lgd genes are not required for follicle cell functions, while absence of lgl function in follicles prevents egg development.(ABSTRACT TRUNCATED AT 250 WORDS)

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