Fig 2 - available via license: Creative Commons Attribution 4.0 International
Content may be subject to copyright.
Previtellogenesis. Early stages of follicular epithelium differentiation. a Part of germarium:zones III and IV. Clusters of cystocytes (Cc) are surrounded by dividing follicular cells (arrows). In the basal part of zone III, a group of degenerating cells (dc) is visible. os, ovariole sheath. Semithin section after methylene blue. Scale bar = 40 μm. b Anterior part of vitellarium after DAPI staining. mbFC, main body follicular cells; nNC, nurse cells nuclei; os, ovariole sheath; stFC, stretched follicular cells. Arrows indicate dividing follicular cells. Fluorescence microscope, whole mount preparation. Scale bar = 50 μm. c, d Early previtellogenic egg chamber. mbFC, main body follicular cells; ms, muscles covering the ovariolar sheath; NC, nurse cells; Oo, oocyte; pFC, posterior follicular cells; stFC, stretched follicular cells. Cystocytes within the clusters remain interconnected by intercellular bridges (dotted arrows). Confocal microscope, whole mount preparation after DAPI/ phalloidin-conjugated rhodamine (c), only phalloidin-conjugated
Source publication
Lepidoptera together with its sister group Trichoptera belongs to the superorder Amphiesmenoptera, which is closely related to the Antliophora, comprising Diptera, Siphonaptera, and Mecoptera. In the lepidopteran Pieris napi, a representative of the family Pieridae, the ovaries typical of butterflies are polytrophic and consist of structural ovaria...
Contexts in source publication
Context 1
... of the paired ovaries of Pieris napi is composed of four long ovarioles of meroistic polytrophic type (Fig.1a). Individual ovarioles are covered by a relatively thick ovariolar sheath and a layer of muscles (Fig. 2a, ce). Each ovariole is built of four linearly arranged parts: terminal filament, germarium, vitellarium, and ovariolar stalk. Terminal filaments join up with each other and form a ligament that attaches the gonad to the body ...
Context 2
... undifferentiated germ cell clusters (groups of interconnected cystocytes) arise (not shown). Zone III, called a Bcontrol zone,^ is filled with numerous cells that undergo degeneration (apoptotic cells) (usually whole germ cell cluster) (Figs.1b and 2a). In zone IV, the distalmost region of the germarium, the germ cell clusters are fully formed (Fig. 2a). The cystocytes of the cluster are interconnected by cytoplasmic bridges (ring canals) and arranged like the elements of a rosette. All of them enter the first meiotic prophase (Fig. 1b) as indicates the presence of synaptonemal complexes (not ...
Context 3
... cells differentiate from prefollicular cells located in the germarium, at the border of zones III and IV and close to the wall of the ovariole. Each germ cell cluster comes to be encased by a simple follicular epithelium in which intensely dividing follicular cells have been observed (Fig. 2a). As a result, completely formed egg chambers appear in the most posterior region of zone IV. Less numerous dividing follicular cells have been observed in the vitellarium during previtellogenic growth of the oocyte (Fig. 2b). When the germ cells of the clusters start to differentiate into the oocyte and nurse cells, the initially ...
Context 4
... comes to be encased by a simple follicular epithelium in which intensely dividing follicular cells have been observed (Fig. 2a). As a result, completely formed egg chambers appear in the most posterior region of zone IV. Less numerous dividing follicular cells have been observed in the vitellarium during previtellogenic growth of the oocyte (Fig. 2b). When the germ cells of the clusters start to differentiate into the oocyte and nurse cells, the initially uniform population of the follicular cells becomes progressively diversified into specialized subgroups. The process of follicular cell diversification occurs in several steps, and finally, in the advanced vitellogenic egg ...
Context 5
... of the whole mounts in the confocal microscope after DAPI and rhodamine-conjugated phalloidin staining showed that at this stage of oogenesis, two subpopulations of the follicular cells are discernable: the main body follicular cells and the stretched cells (Fig. 2b, c). The main body follicular cells (mbFC) are high and columnar, and closely adjacent to each other. The stretched cells (stFC) are slightly lower and wider (cuboidal) in comparison to the mbFC (Fig. 2c). During previtellogenesis, the activity and volume of the trophocytes increase, and in their cytoplasm numerous organelles (mostly ...
Context 6
... at this stage of oogenesis, two subpopulations of the follicular cells are discernable: the main body follicular cells and the stretched cells (Fig. 2b, c). The main body follicular cells (mbFC) are high and columnar, and closely adjacent to each other. The stretched cells (stFC) are slightly lower and wider (cuboidal) in comparison to the mbFC (Fig. 2c). During previtellogenesis, the activity and volume of the trophocytes increase, and in their cytoplasm numerous organelles (mostly mitochondria and ribosomes) accumulate. As a result, the stretched cells become more flattened (Fig. 2d). In the cytoplasm of both follicle cell subpopulations, a few mitochondria and cisterns of ...
Context 7
... to each other. The stretched cells (stFC) are slightly lower and wider (cuboidal) in comparison to the mbFC (Fig. 2c). During previtellogenesis, the activity and volume of the trophocytes increase, and in their cytoplasm numerous organelles (mostly mitochondria and ribosomes) accumulate. As a result, the stretched cells become more flattened (Fig. 2d). In the cytoplasm of both follicle cell subpopulations, a few mitochondria and cisterns of endoplasmic reticulum are visible (Fig 4a, c). In the progress of early previtellogenic growth, some of the main body follicular cells form projections that surround the posterior pole of the oocyte. In consequence, the posterior pole of the ...
Context 8
... are visible (Fig 4a, c). In the progress of early previtellogenic growth, some of the main body follicular cells form projections that surround the posterior pole of the oocyte. In consequence, the posterior pole of the oocyte becomes ensheathted by the third subpopulation of the follicular cells termed the posterior terminal cells (pFC) (Fig. 2c, d). The number of follicular cells associated with the posterior pole of the oocyte increases as a result of mitotic ...
Context 9
... It suggests that its position within ooplasm is not fixed. In advanced previtellogenesis, the mbFC occasionally divide, and so their number slightly rises. Some of the mbFC located close to the nurse cells start to migrate between the oocyte and the nurse cell compartments, giving rise to the next FC subpopulation termed centripetal cells (cpFC) (Figs. 2e, f and 3a-d). Most of the centripetal cells during their movement detach from the basal lamina and reach the intercellular bridges grouped at the apical part of the oocyte (Figs. 2f and 3a-d). Those cells surround intercellular bridges connecting the oocyte and the nurse cells in a rosette-like pattern (Fig. 2f). Some of the centripetal cells, ...
Context 10
... close to the nurse cells start to migrate between the oocyte and the nurse cell compartments, giving rise to the next FC subpopulation termed centripetal cells (cpFC) (Figs. 2e, f and 3a-d). Most of the centripetal cells during their movement detach from the basal lamina and reach the intercellular bridges grouped at the apical part of the oocyte (Figs. 2f and 3a-d). Those cells surround intercellular bridges connecting the oocyte and the nurse cells in a rosette-like pattern (Fig. 2f). Some of the centripetal cells, located exactly at the border of nurse cells and the oocyte compartments, still contact the basal lamina and form protrusions toward the anterior pole of the oocyte (Figs. 2f and ...
Context 11
... termed centripetal cells (cpFC) (Figs. 2e, f and 3a-d). Most of the centripetal cells during their movement detach from the basal lamina and reach the intercellular bridges grouped at the apical part of the oocyte (Figs. 2f and 3a-d). Those cells surround intercellular bridges connecting the oocyte and the nurse cells in a rosette-like pattern (Fig. 2f). Some of the centripetal cells, located exactly at the border of nurse cells and the oocyte compartments, still contact the basal lamina and form protrusions toward the anterior pole of the oocyte (Figs. 2f and ...
Context 12
... oocyte (Figs. 2f and 3a-d). Those cells surround intercellular bridges connecting the oocyte and the nurse cells in a rosette-like pattern (Fig. 2f). Some of the centripetal cells, located exactly at the border of nurse cells and the oocyte compartments, still contact the basal lamina and form protrusions toward the anterior pole of the oocyte (Figs. 2f and ...
Context 13
... the progress of previtellogenesis, neighboring egg chambers become separated by the interfollicular stalk cells (IFS) (Figs. 2f and 3a, d). Initially, these cells are arranged irregularly, and the stalks take the whole width of the ovariole (Fig. 3a). During later stages, when the number of the interfollicular stalk cells significantly increases, the interfollicular stalks noticeably elongate and the arrangement of stalk cells changes from irregular to radial (Fig. 3d). ...
Context 14
... increases, the interfollicular stalks noticeably elongate and the arrangement of stalk cells changes from irregular to radial (Fig. 3d). Some of the interfollicular stalk cells directly adhere to the pFC and stFC, and thus, the follicular cells surrounding the anterior and posterior poles of the egg chambers have no contact with the basal lamina (Figs. 2f and ...
Citations
... Simple examples of four cell cysts (n = 2) are found in two types of clam shrimp, Cyzicus tetracerus and Lynceus brachyurus of different orders (Spinicaudata and Laevicaudata, respectively) [91], the scorpion fly Panorpa communis [92], and the bark lice Peripsocus phaeopterus and Stenopsocus stigmaticus [93]. Extending one round of division further are the whirligig beetles Gyrinus natator [94] and Dineutus nigrior [95], sheep ked Melophagus ovinus [96], and the majority of moths and butterflies in the order Lepidoptera [97][98][99][100][101][102]. A large portion of characterized cell cyst shapes in this class are those that contain 16 Figure 2. Zoology of germline CLT topologies across species. ...
Small cell clusters exhibit numerous phenomena typically associated with complex systems, such as division of labour and programmed cell death. A conserved class of such clusters occurs during oogenesis in the form of germline cysts that give rise to oocytes. Germline cysts form through cell divisions with incomplete cytokinesis, leaving cells intimately connected through intercellular bridges that facilitate cyst generation, cell fate determination and collective growth dynamics. Using the well-characterized Drosophila melanogaster female germline cyst as a foundation, we present mathematical models rooted in the dynamics of cell cycle proteins and their interactions to explain the generation of germline cell lineage trees (CLTs) and highlight the diversity of observed CLT sizes and topologies across species. We analyse competing models of symmetry breaking in CLTs to rationalize the observed dynamics and robustness of oocyte fate specification, and highlight remaining gaps in knowledge. We also explore how CLT topology affects cell cycle dynamics and synchronization and highlight mechanisms of intercellular coupling that underlie the observed collective growth patterns during oogenesis. Throughout, we point to similarities across organisms that warrant further investigation and comment on the extent to which experimental and theoretical findings made in model systems extend to other species.
... Most studies have explored the role of follicular epithelial cells in vitellogenesis and eggshell formation. In this study, the definition and location of follicular epithelial cells of M. separata were determined with reference to the internal morphology of other lepidopteran insects, such as B. mori (Stanley and Kirkland 1968;Yamauchi and Yoshitake 1984), Diatraea saccharalis (Santos and Gregorio 2002), Diatraea saccharalis Fabricius (Santos and Gregorio 2006), Spodoptera frugiperda (Alves et al. 2014), Pieris napi (Mazurkiewicz-Kania et al. 2019), and also based on the follicular cell development of D. melanogaster (Michael 1974;Büning 1994) and mosquitoes (Mazurkiewicz and Kubrakiewicz 2008). ...
Determining the source of primary cells is conductive to enriching sufficient cells with immortal potential thereby improving the success rate of establishing cell lines. However, most of the existing insect cell lines are established by mixing and fragmentation of explants. At present, the origin of cell lines can only be determined according to the cultured tissues, so it is impossible to determine which cell types they come from. In this study, a new cell line designated IOZCAS-Myse-1 was generated from pupal ovaries of the migratory pest Mythimna separata by explant tissues to derive adherent cultures. This paper mainly shows the further descriptive information on the origin of primary cells in the process of ovarian tissue isolation and culture. Phospho-histone H3 antibody-labeled cells with mitotic activity showed that the rapidly developing somatic cells in vivo gradually stopped proliferation when cultured ex vivo. The primary cells dissociated outside the tissue originated from the lumen cells, rather than the germ cells or the follicular epithelium cells. The results suggest that the newly established cell line IOZCAS-Myse-1 had two possible sources. One is the mutation of lumen cells in the vitellarium, and the other is the stem cells with differentiation potential in the germarium of the ovarioles. Moreover, the newly established cell line is sensitive to the infection of Autographa californica multiple nucleopolyhedrovirus, responds to 20-hydroxyecdysone and has weak encapsulation ability. Therefore, the new cell line can be a useful platform for replication of viral insecticides, screening of hormone-based insecticides and immunology research.
... There is a clear tendency to reduce the number of gonads and/or the ducts and other organs of the reproductive sys tems. For instance, in insects, which commonly have paired ovaries and oviducts (Biliński, 1998;Büning, 1994;Garbiec & Kubrakiewicz, 2012;Mazurkiewicz Kania et al., 2019;Simiczyjew et al., 1998), un paired ovaries and oviducts have been reported in minute collem bolan species (Panina et al., 2019). In small or tiny chelicerates such as pseudoscorpions and some mites, the number of ovarian tubules is also significantly reduced, usually to one, compared to numerous and branched ovarian tubules in giant horseshoe crabs and large scorpions (reviewed in Dunlop, 2019). ...
Chelicerata, the second largest subphylum of Arthropoda, includes invertebrates with a wide range of body size. Pseudoscorpions are among small or miniature chelicer ates which exhibit several morphological, anatomical, and developmental features related to miniaturization, e.g., replacement of book lungs by tracheae, unpaired gonads, and matrotrophic development of the embryos outside the female body, in the brood sac. In this paper, we show the ovary structure of two pseudoscorpion species, Cheiridium museorum and Apocheiridium ferum (Cheiridiidae). Both cheiridiids are one of the smallest pseudoscorpions. The results of our observations conducted in light, transmission electron, and confocal microscopy demonstrate that the ovary of C. museorum and A. ferum, displays a significant structural difference that is unusual for chelicerates. The difference concerns the spatially restricted position of the germarium. We show that such ovary architecture results in a significantly reduced number of growing oocytes and in consequence a reduced number of deposited eggs. A centrally located germarium implies also a modified pattern of ovary development during oocyte growth due to long distance migration of the germline and the accom panying somatic cells. Herein, we postulate that such an ovary structure is related to the pseudoscorpion's small body size and it is a step towards miniaturization in the smaller pseudoscorpions species.
... Ovarian ring canals in bees can reach diameters of up to 4 microns (Ramamurty and Engels 1977;Patricio and Cruz-Landim 2006), while aphids appear have ring canals more similar to those in males (Pyka-Fosciak and Szklarzewicz 2008). Recent work observing ovaries in the butterfly Pieris napi suggests that they have actin rich ring canals in the female germline with diameters of around 10 microns (Mazurkiewicz-Kania et al. 2019). It is possible that differences in size could reflect the presence or absence of a HtsRC homolog. ...
Ring canals in the female germline of Drosophila melanogaster are supported by a robust filamentous actin (F-actin) cytoskeleton, setting them apart from ring canals in other species and tissues. Previous work has identified components required for the expansion of the ring canal actin cytoskeleton but has not identified the proteins responsible for F-actin recruitment or accumulation. Using a combination of CRISPR-Cas9 mediated mutagenesis and UAS-Gal4 overexpression, we show that HtsRC, a component specific to female germline ring canals, is both necessary and sufficient to drive F-actin accumulation. Absence of HtsRC in the germline resulted in ring canals lacking inner rim F-actin, while overexpression of HtsRC led to larger ring canals. HtsRC functions in combination with Filamin to recruit F-actin to ring-canal-like ectopic actin structures in somatic follicle cells. Finally, we present findings which indicate that HtsRC expression and robust female germline ring canal expansion are important for high fecundity in fruit flies but dispensable for their fertility, a result which is consistent with our understanding of HtsRC as a newly evolved gene specific to female germline ring canals.
... This intriguing, genetically regulated process leads to the formation of eight morphologically and functionally distinct subpopulations of cells that, after termination of yolk accumulation, participate in the formation of regionally specialized egg coverings (internal vitelline envelope and external chorion) termed collectively the eggshell. Diversification of the follicular cells has been also described in several other holometabolous and hemimetabolous insects, including non-Drosophila dipterans (gnats, snipe flies, and horse flies), lepidopterans (butterflies), neuropterans (lacewings), hymenopterans (parasitic wasps and wasps), mecopterans (scorpionflies), hemipterans (true bugs), mallophagans (bird-lice), and plecopterans (stoneflies), for example, Tworzydlo, Jablonska, Kisiel, and Bilinski (2005), Jaglarz, Krzeminski, and Bilinski (2008), Jaglarz, Kubrakiewicz, and Bilinski (2010), Mazurkiewicz and Kubrakiewicz (2008), Garbiec and Kubrakiewicz (2012), and Mazurkiewicz-Kania, Simiczyjew, and Jedrzejowska (2019). As a rule, the complexity of the eggshell of a given species depends on the number of the subpopulations of the follicular cells. ...
Representatives of the highly specialized earwig family Hemimeridae are epizoic and viviparous. Their embryos develop inside terminal ovarian follicles (termed also embryonic follicles) and rely solely on nutrients transferred from mother tissues. In this report, we present results of ultrastructural and histochemical studies of the initial stage of Hemimerus talpoides development. Our results show that the follicular cells surrounding fully grown oocyte of Hemimerus do not degenerate after initiation of embryogenesis, but transform and gradually form the wall of the incubation chamber in which the embryo develops. We also show that amniotic cells of the early embryo remain in direct contact with transformed follicular cells. In the region of contact, short outgrowths of the amniotic cells associate with irregular surface specializations of the transformed follicular cells. We suggest that extended “postfertilization” activity of hemimerid follicular cells represents an adaptation to viviparity and matrotrophy in this insect lineage.
The insect egg is the single-celled developmental stage, a resource investment in the next generation, an unusually large and complex cell type, and the protective vessel for embryonic development. In this review, I describe the morphological diversity of insect eggs and then identify recent advances in understanding the patterns of their evolution, the cellular mechanisms underlying their development, and notable aspects of their ecology. I also suggest areas for particularly promising future research on insect egg morphology; these topics touch upon such diverse areas as tissue morphogenesis, life history evolution, organismal scaling, cellular secretion, and oviposition ecology.
Ring canals in the female germline of Drosophila melanogaster are supported by a robust filamentous actin (F-actin) cytoskeleton, setting them apart from ring canals in other species and tissues. Previous work has identified components required for the expansion of the ring canal actin cytoskeleton but has not identified the proteins responsible for F-actin recruitment or accumulation. Using a combination of CRISPR-Cas9 mediated mutagenesis and UAS-Gal4 overexpression, we show that HtsRC, a component specific to female germline ring canals, is both necessary and sufficient to drive F-actin accumulation. Absence of HtsRC in the germline resulted in ring canals lacking inner rim F-actin, while overexpression of HtsRC led to larger ring canals. HtsRC functions in combination with Filamin to recruit F-actin to ectopic actin structures in somatic follicle cells. Finally, we present findings which indicate that HtsRC expression and robust female germline ring canal expansion are important for high fecundity in fruit flies but dispensable for their fertility, a result which is consistent with our understanding of HtsRC as a newly evolved gene specific to female germline ring canals.
