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Vitellogenesis in insects and other groups: a review

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Abstract

The eggs from oviparous organisms contain large amounts of vitellus, or yolk, which are utilized by the growing embryo. Vitellogenesis is the process of vitellus accumulation and involves massive heterosynthetic synthesis of the protein vitellogenin (Vg) and its deposition in the oocyte. This work summarizes data on Vg structure, synthesis, uptake by oocytes and its fate during embryogenesis. The hormonal control of vitellogenesis and its tissue, sex and temporal regulation are also discussed. Where it is available, data on structure and expression of Vg-coding genes are reviewed. Insect vitellogenesis is priorized although other oviparous animal groups outside insects are also treated.
... Indeed, insects mostly secrete their vitellogenin from fat bodies and are directed to haemolymph for oocyte development by receptormediated endocytosis (Hagedorn et al., 1998;Sappington and Raikhel, 1998). The fat bodies are modulated by endocrine effectors and its complex homeostatic pattern for the formation of vitellogenin (Engelmann, 1983;Valle, 1993). While earlier pupal in the Bombyx mori, the expressions and actions of three matrix metalloproteinases (Mmps) involve differential changes in tissue subsequently with the cell dissociation in the fat bodies (Jia et al., 2018). ...
... Insect fat body is a synthetic organ for various proteins, which is also a particular region for vitellogenin production in most of the insects (Valle, 1993;Bownes, 1980;Zongza and Dimitriadis, 1988;Peferoen and Deloof, 1986).During vitellogenesis, fat body cells perform dramatic changes and produce proteins in a relatively short time (keeley, 1985). Most of higher Diptera (Dacus oleae, Musca domestica, Calliphora vicinia, Calliphora erythrocephala, Sarcophaga argyostoma, Drosophila melanogaster) vitellogenesis occurs both in ovaries and as well as in fat body (Valle,1993;Rousset and Bitsch,1993;Martinez and Bownes, 1996). ...
Article
The present study aims to focus on the site of fat bodies involved in the differential expression of vitellogenin protein in Bombyx mori L which is not yet fully understood. Culturing fat bodies and analyzing in in vitro and in vivo approaches made it useful to study this pattern. In Bombyx mori, L. The vitellogenin protein is 200-205 kDa and resolves at two molecular weight regions that are at 180 kDa and 42 kDa. We subject dorsal perivisceral (DPV) and ventral perivisceral fat body (VPV), haemolymph for this radio labeling cell culture and incorporation experiment. Based on our in vitro and in vivo experiments of S 35 methionine fluorography, Scanning densito-metric, Western blot analysis and RT-PCR expression studies had strongly proven that the ventral perivisceral fat body is the significant and exclusive site of differential vitellogenin expression in silkworm, Bombyx mori but not in dorsal peripheral fat body tissues, haemolymph by radiolabeling studies. The present paper describes an experimental setup based on the incubation of ventral perivisceral and dorsal perivisceral fat bodies and the measurement of vitellogenin with S 35 protein labeling incorporation method. These findings from our lab were the first report proved by in vitro and in vivo labeling experiments.
... Synthesis of yolk proteins is a vital process for the growth of the egg. In this time, quick growth of oocyte arises owing to yolk substance accumulation [13]. Vitellogenesis, is synthesizing a cluster of proteins creating outside the ovary, is the chief constituent of the yolk and deposited as vitellin in oocytes [14]. ...
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The ovarian development of Musca domestica, was examined under light microscope. There are two ovaries in the adult female of fly. Each ovary was formed of about 60-70 polytrophic ovarioles. The ovariole in cross sections organized in several circles. From cytological observations, ovary development and oogenesis could be divided in to 6 stages; ovaries with no noticeable follicle cells existing were characterized as (stage1), the follicle-growing stages considered as (stage2, 3), the vitellogenen in stages (stages4, 5(and mature egg stage (stage6). The oocyte initiated development at first stages of oogenesis; the nurse cells and follicle epithelial cells were considered to fulfill important functions with regard to the growth of the oocyte.
... Although most Vg are typically expressed in females, particularly during reproductive stages, some species exhibit low-level expression in males, such as P. pseudoannulata, Sarcophaga bullata, and Tenebrio molitor (Lamy 1984;Valle 1993;Guo et al. 2018). The expression of Vg genes in phytoseiid mites follows a similar pattern: high expression in female mites and low expression in male mites of M. occidentalis, N. barkeri, A. eharai, and N. cucumeris (Zhao et al. 2014;Pomerantz & Hoy 2015;Ding et al. 2018;Jiang et al. 2020;Wang et al. 2020). ...
Article
Neoseiulus californicus is a key natural predator of spider mites and small arthropod pests. Although vitellogenin (Vg) and vitellogenin receptor (VgR) genes are important regulators of oocyte maturation, egg formation, and embryonic development in spider mites and ticks, their role in phytoseiid mites is less understood. Investigating the reproductive mechanism of predatory mites is crucial for understanding their reproduction and evolution. In this study, three Vg genes and one VgR gene were identified, cloned, and characterized in N. californicus. Vg1, Vg2, Vg3, and VgR mRNAs were 6066, 5728, 4515, and 5331 bp long, encoding proteins comprising 1851, 1849, 1471, and 1722 amino acids, respectively. Temporal expression analysis revealed elevated Vg1, Vg2, and VgR levels in fertilized female adult mites, whereas Vg3 exhibited peak expression during the developmental stage. RNA interference–mediated suppression of Vg1 and Vg2 resulted in 14.66% and 11.59% decreases in fecundity, respectively. Vg1 silencing notably reduced egg hatching rate and female offspring ratio. In contrast, Vg3 and VgR silencing had no significant impact on fecundity and egg hatching rate. These findings provide insights into the regulatory roles of Vg and VgR in predatory mite reproduction, offering a theoretical foundation for understanding their evolution and reproductive strategies.
... The uptake of a blood meal triggers several physiological processes including vitellogenesis. Vitellogenesis, the accumulation of yolk (vitellus) in the developing oocytes, starts with the synthesis of yolk protein precursors (YPPs) [9][10][11]. YPPs are synthesized exclusively by the mosquito's fat body. ...
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Increasing levels of insecticide resistance in disease-transmitting mosquitoes highlight the need for alternative strategies to control vector mosquito populations. RNA interference-based strategies have strong potential to become a major component of integrated vector management. To implement dsRNA-based insecticides, effective target genes need to be identified whose knockdown causes death or sterility in mosquitoes. Here, we show that the ribosomal protein P1 is a promising candidate as a target for mosquito birth control using RNA interference.
... As for the ovaries, the abdominal fat body of HiC samples presented signs of degeneration and necrosis. The insect fat body, together with the midgut and haemolymph, plays an essential role in detoxification (Dubovskiy et al., 2011;Enayati et al., 2005;Keeley, 1985) and in the synthesis of yolk protein precursors (e.g., vitellogenin), which determine correct development of the oocyte and of the egg (Pan et al., 1969;Sun et al., 1991;Valle, 1993). Therefore, alterations of the throphocytes imply not only modification of energy metabolism but could also impair correct functioning of detoxification and reproductive activity. ...
Article
Most of the heavy metals in urban environments derives from road traffic, particularly from tyres and brake wear (non-exhaust emission sources). These pollutants contaminate the soil, where several organisms have a primary ecosystem role (e.g., springtails, ants, earthworms). Springtails (Collembola) are soil-dwelling animals regulating soil fertility, flow of energy through above- and below-ground food webs, and they contribute to soil microbial community dispersion and biodiversity maintenance. In this study we investigated the ecotoxicological effects of oral exposure to particles emitted from brake pads and cast-iron brake discs in the euedaphic collembola species Orthonychiurus folsomi under laboratory conditions. Our results showed that chronic exposure to brake wear particles can have sub-lethal effects both at low and high concentrations and it can cause histological alterations. Here, SEM-EDX was applied to observe the particulate and we found its chemical markers in the gut and faeces of collembola, while histological analysis detected alterations of the digestive and reproductive systems and of the abdominal fat body at high concentrations.
... Vitellogenin is a precursor of proteins synthesised and deposited in the oocytes during the vitellogenesis process and utilised by the growing embryos. Vitellogenin plays a significant role in ovary development (Valle, 1993). Two anaesthesia with CO 2 stimulate vitellogenin synthesis in unmated queens (Engels et al., 1976;Thompson et al., 2007). ...
Article
Treating instrumentally inseminated honey bee queens with carbon dioxide accelerates egg laying. This treatment also activates the ovaries of virgins. The aim of the study was to compare the effect of three different treatments: (1) anaesthesia with carbon dioxide, (2) anaesthesia with nitrogen, and (3) oxygen deprivation by submersion in water, on the onset of oviposition in virgin queens. The effect of the number and duration of CO2 treatments was also investigated. No significant differences were found in the onset of egg laying in queens treated with CO2, or N2, or water. The beginning of oviposition after the CO2 treatment for 0.1, 1, 2, and 10 min, did not differ significantly. Whether a CO2 treatment was performed twice or three times, the effect was the same, but oviposition was accelerated compared to when only one anaesthesia treatment was used. I speculate that ovary activation in queens is not the effect of CO2 or any other gases but rather the effect of a lack of oxygen, i.e., anoxia.
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While CRISPR-Cas9 technology has demonstrated remarkable promise as a gene editing tool, its application in certain insects, such as the jewel wasp, Nasonia vitripennis, has been hindered by a lack of a tractable method for reagent delivery. Direct Parental-CRISPR (DIPA-CRISPR) recently emerged as a facile way to induce gene lesions because it involves adult injection with commercially available Cas9-sgRNA with no helper reagent. However, DIPA-CRISPR has so far been tested in only a few insects. Here, we have assessed the viability of DIPA-CRISPR in N. vitripennis by targeting two eye-pigmentation genes, cinnabar and vermilion, which function in the ommochrome pathway. Successful generation of lesions in both genes demonstrated the functionality of DIPA-CRISPR in N. vitripennis and its potential application to other genes, thereby expanding the range of insects suitable for this method. We varied two parameters, Cas9-sgRNA concentration and injection volume, to determine optimal injection conditions. We found that the larger injection volume coupled with either higher or lower concentration was needed for consistent mutation production. However, DIPA-CRISPR yields an overall low mutation rate in N. vitripennis when compared to other tested insects, a characteristic that may be attributed to a proportionally low vitellogenic import efficiency in the jewel wasp. We discuss different factors that may be considered in determining when DIPA-CRISPR may be preferable over other reagent delivery methods.
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Conogethes punctiferalis is a serious pest in China affecting a wide variety of field crops, fruits, and forest trees. Many insects require supplemental nutrients after emergence to compensate for insufficient nutrients at the larval stage. In this study, to better understand the determinants of C. punctiferalis survival and reproduction, the impact of supplemental nutrition was examined. In particular, the effects of 11 treatments (5% sucrose, 10% sucrose, 15% sucrose, 5% sophora honey, 10% sophora honey, 15% sophora honey, 5% wild honey, 10% wild honey, 15% wild honey, distilled water, and blank control) on adult longevity and oviposition were evaluated, with detailed morphological analyses of ovarian development in the 10% sucrose, distilled water, and blank control groups. Conogethes punctiferalis required supplementary nutrition after emergence. Supplementary nutrition improved fecundity (number of eggs laid) and longevity, and 10% sucrose water had the greatest effects. The preoviposition period and oviposition period of C. punctiferalis females were longer, and the numbers of eggs in female ovarian tubes and eggs laid by females were higher in the 10% sucrose water group than in other groups. Females supplemented with distilled water laid a small number of eggs. Without nutrient supplementation, females did not lay eggs. In conclusion, supplemental nutrition was beneficial for ovarian development in female moths, prolonging the oviposition period and lifespan, and was an important factor affecting population dynamics. These results lay a foundation for further analyses of the nutritional requirements for C. punctiferalis in the field and provide a reference for indoor population feeding.
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Vitellogenin is the generic name for a unique group of proteins that are synthesized extraovarially and become the major egg yolk protein, vitellin. Similar proteins are found in all animals with yolky eggs. Because of their high concentration in the egg, and the relative ease with which they can be purified, these proteins are excellent material for the study of the regulation of their synthesis from the molecular, developmental, and physiological points of view. This review covers the synthesis, uptake, and physical and chemical properties of vitellogenins and vitellins in insects.