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Science (New York, N.Y.) Sep 2022In most organisms, reproduction is correlated with shorter life span. However, the reproductive queen in eusocial insects exhibits a much longer life span than that of...
In most organisms, reproduction is correlated with shorter life span. However, the reproductive queen in eusocial insects exhibits a much longer life span than that of workers. In ants, when the queen dies, workers can undergo an adult caste switch to reproductive pseudo-queens (gamergates), exhibiting a five-times prolonged life span. To explore the relation between reproduction and longevity, we compared gene expression during caste switching. Insulin expression is increased in the gamergate brain that correlates with increased lipid synthesis and production of vitellogenin in the fat body, both transported to the egg. This results from activation of the mitogen-activated protein kinase (MAPK) branch of the insulin signaling pathway. By contrast, the production in the gamergate developing ovary of anti-insulin Imp-L2 leads to decreased signaling of the AKT/forkhead box O (FOXO) branch in the fat body, which is consistent with their extended longevity.
Topics: Animals; Ants; Female; Insulin; Longevity; Mitogen-Activated Protein Kinase Kinases; Ovary; Reproduction; Signal Transduction; Vitellogenins
PubMed: 36048960
DOI: 10.1126/science.abm8767 -
MBio Feb 2023Integration between animal reproduction and symbiont inheritance is fundamental in symbiosis biology, but the underlying molecular mechanisms are largely unknown....
Integration between animal reproduction and symbiont inheritance is fundamental in symbiosis biology, but the underlying molecular mechanisms are largely unknown. Vitellogenin (Vg) is critical for oogenesis, and it is also a pathogen pattern recognition molecule in some animals. Previous studies have shown that Vg is involved in the regulation of symbiont abundance and transmission. However, the mechanisms by which an insect and its symbiont contribute to the function of Vg and how Vg impacts the persistence of insect-microbe symbiosis remain largely unclear. Symbionts are transovarially transmitted via maternal inheritance of the bacteriocytes in the whitefly Bemisia tabaci. Surprisingly, Vg is localized in bacteriocytes of whiteflies. Vg could be synthesized in whitefly bacteriocytes by the gene expressed in these cells or exported into bacteriocytes from hemolymph via the Vg receptor. We further found that the juvenile hormone and " Portiera aleyrodidarum" (here termed ) control the level and localization of Vg in whiteflies. Immunocapture PCR revealed interactions between Vg and . Suppressing Vg expression reduced abundance as well as whitefly oogenesis and fecundity. Thus, we reveal that Vg facilitated the persistence of whitefly-bacteriocyte symbiont associations. This study will provide insight into the key role of Vg in the coevolution of insect reproduction and symbiont inheritance. Intracellular heritable symbionts have been incorporated into insect reproductive and developmental biology by various mechanisms. All Bemisia tabaci species harbor the obligate symbiont in specialized insect cells called bacteriocytes. We report that the whitefly juvenile hormone and determined vitellogenin (Vg) localization in bacteriocytes of whiteflies. In turn, Vg affected whitefly fecundity as well as fitness and transmission of the symbiont. Our findings show that Vg, a multifunctional protein, is indispensable for symbiont integration into the reproduction and development of insects. This reflects the outcome of long-term coevolution of the insect-microbe symbiosis.
Topics: Animals; Vitellogenins; Hemiptera; Symbiosis; Polymerase Chain Reaction
PubMed: 36692332
DOI: 10.1128/mbio.02990-22 -
Nutrients Oct 2015Vitellogenin (Vtg), the major egg yolk precursor protein, is traditionally thought to provide protein- and lipid-rich nutrients for developing embryos and larvae.... (Review)
Review
Vitellogenin (Vtg), the major egg yolk precursor protein, is traditionally thought to provide protein- and lipid-rich nutrients for developing embryos and larvae. However, the roles of Vtg as well as its derived yolk proteins lipovitellin (Lv) and phosvitin (Pv) extend beyond nutritional functions. Accumulating data have demonstrated that Vtg, Lv and Pv participate in host innate immune defense with multifaceted functions. They can all act as multivalent pattern recognition receptors capable of identifying invading microbes. Vtg and Pv can also act as immune effectors capable of killing bacteria and virus. Moreover, Vtg and Lv are shown to possess phagocytosis-promoting activity as opsonins. In addition to these immune-relevant functions, Vtg and Pv are found to have antioxidant activity, which is able to protect the host from oxidant stress. These non-nutritional functions clearly deepen our understanding of the physiological roles of the molecules, and at the same time, provide a sound basis for potential application of the molecules in human health.
Topics: Animals; Antioxidants; Bacteria; Egg Proteins; Fishes; Phosvitin; Receptors, Pattern Recognition; Viruses; Vitellogenins
PubMed: 26506386
DOI: 10.3390/nu7105432 -
PloS One 2016Vitellogenin (Vg) plays vital role in oocytes and embryo development in insects. Vg is synthesized in the fat body, moves through haemolymph and accumulates in oocytes....
Vitellogenin (Vg) plays vital role in oocytes and embryo development in insects. Vg is synthesized in the fat body, moves through haemolymph and accumulates in oocytes. Vitellogenin receptors (VgR) present on the surface of oocytes, are responsible for Vg transportation from haemolymph to oocytes. Here, we cloned and characterized these genes from Bemisia tabaci Asia1 (BtA1) species. The cloned BtA1Vg and BtA1VgR genes consisted of 6,330 and 5,430 bp long open reading frames, which encoded 2,109 and 1,809 amino acid (AA) residues long protein. The BtA1Vg protein comprised LPD_N, DUF1943 and VWFD domains, typical R/KXXR/K, DGXR and GL/ICG motifs, and polyserine tracts. BtA1VgR protein contained 12 LDLa, 10 LDLb and 7 EGF domains, and a trans-membrane and cytoplasmic region at C-terminus. Phylogenetic analyses indicated evolutionary association of BtA1Vg and BtA1VgR with the homologous proteins from various insect species. Silencing of BtA1VgR by siRNA did not affect the transcript level of BtA1Vg. However, BtA1Vg protein accumulation in oocytes was directly influenced with the expression level of BtA1VgR. Further, BtA1VgR silencing caused significant mortality and reduced fecundity in adult whiteflies. The results established the role of BtA1VgR in transportation of BtA1Vg in oocytes. Further, these proteins are essential for fecundity, and therefore these can be potential RNAi targets for insect control in crop plants.
Topics: Amino Acid Sequence; Animals; Data Mining; Diptera; Egg Proteins; Phylogeny; Receptors, Cell Surface; Sequence Homology, Amino Acid; Vitellogenins
PubMed: 27159161
DOI: 10.1371/journal.pone.0155306 -
Frontiers in Cellular and Infection... 2022The protozoan parasite spp. invades into tick oocytes and remains in the offspring. The transovarial transmission phenomenon of in ticks has been demonstrated...
The protozoan parasite spp. invades into tick oocytes and remains in the offspring. The transovarial transmission phenomenon of in ticks has been demonstrated experimentally, but the molecular mechanisms remain unclear. invasion into oocytes occurs along with the progression of oogenesis. In the present study, to find the key tick factor(s) for transmission, we focused on molecules involved in yolk protein precursor (vitellogenin, Vg) synthesis and Vg uptake, which are crucial events in tick oogenesis. With a tick- experimental model, the expression profiles of , , , , and , Vg synthesis-related genes, and Vg receptor () and autophagy-related gene 6 (), Vg uptake-related genes, were analyzed using real-time PCR using tissues collected during the preovipositional period in -infected ticks. The expression levels of () and decreased in the fat body of -infected ticks 1 day after engorgement. In the ovary, mRNA expression was significantly higher in -infected ticks than in uninfected ticks 1 and 2 days after engorgement and decreased 3 days after engorgement. expression was significantly lower in -infected ticks than in uninfected ticks 2 and 4 days after engorgement. had a lower gene expression in -infected ticks compared to uninfected ticks 2 days after engorgement. Additionally, western blot analysis using protein extracts from each collected tissue revealed that Vg-2 (HlVg-2) accumulate in the fat body and hemolymph of -infected ticks. These results suggest that Vg uptake from the hemolymph to the ovary was suppressed in the presence of . Moreover, knockdown ticks had a lower detection rate of DNA in the ovary and a significant reduction of DNA in the hemolymph compared with control ticks. Taken together, our results suggest that accumulated HlVg-2 is associated with infection or transmission in the tick body. These findings, besides previous reports on VgR, provide important information to elucidate the transovarial transmission mechanisms of pathogens in tick vectors.
Topics: Animals; Babesia; DNA; Fat Body; Female; Hemolymph; Ixodidae; Vitellogenins
PubMed: 35800383
DOI: 10.3389/fcimb.2022.908142 -
Microbiology Spectrum Aug 2022Liberibacter solanacearum (CLso) haplotype D, transmitted by the carrot psyllid , is a major constraint for carrot production in Israel. Unveiling the molecular...
Liberibacter solanacearum (CLso) haplotype D, transmitted by the carrot psyllid , is a major constraint for carrot production in Israel. Unveiling the molecular interactions between the psyllid vector and CLso can facilitate the development of nonchemical approaches for controlling the disease caused by CLso. Bacterial surface proteins are often known to be involved in adhesion and virulence; however, interactions of CLso with carrot psyllid proteins that have a role in the transmission process has remained unexplored. In this study, we used CLso outer membrane protein (OmpA) and flagellin as baits to screen for psyllid interacting proteins in a yeast two-hybrid system assay. We identified psyllid vitellogenin (Vg) to interact with both OmpA and flagellin of CLso. As Vg and autophagy are often tightly linked, we also studied the expression of autophagy-related genes to further elucidate this interaction. We used the juvenile hormone (JH-III) to induce the expression of Vg, thapsigargin for suppressing autophagy, and rapamycin for inducing autophagy. The results revealed that Vg negatively regulates autophagy. Induced Vg expression significantly suppressed autophagy-related gene expression and the levels of CLso significantly increased, resulting in a significant mortality of the insect. Although the specific role of Vg remains obscure, the findings presented here identify Vg as an important component in the insect immune responses against CLso and may help in understanding the initial molecular response in the vector against Liberibacter. Pathogen transmission by vectors involves multiple levels of interactions, and for the transmission of liberibacter species by psyllid vectors, much of these interactions are yet to be explored. Liberibacter solanacearum (CLso) haplotype D inflicts severe economic losses to the carrot industry. Understanding the specific interactions at different stages of infection is hence fundamental and could lead to the development of better management strategies to disrupt the transmission of the bacteria to new host plants. Here, we show that two liberibacter membrane proteins interact with psyllid vitellogenin and also induce autophagy. Altering vitellogenin expression directly influences autophagy and CLso abundance in the psyllid vector. Although the exact mechanism underlying this interaction remains unclear, this study highlights the importance of immune responses in the transmission of this disease agent.
Topics: Animals; Autophagy; Flagellin; Hemiptera; Liberibacter; Plant Diseases; Rhizobiaceae; Vitellogenins
PubMed: 35863005
DOI: 10.1128/spectrum.01577-22 -
Journal of Insect Science (Online) Nov 2020Oviposition-related genes have remained a consistent focus of insect molecular biology. Previous research has gradually clarified our mechanistic understanding of... (Review)
Review
Oviposition-related genes have remained a consistent focus of insect molecular biology. Previous research has gradually clarified our mechanistic understanding of oviposition-related genes, including those related to oviposition-gland-related genes, oogenesis-related genes, oviposition-site-selection-related genes, and genes related to ovulation and hatching. Moreover, some of this research has revealed how the expression of single oviposition-related genes affects the expression of related genes, and more importantly, how individual node genes function to link the expression of upstream and downstream genes. However, the research to date is not sufficient to completely explain the overall interactions among the genes of the insect oviposition system. Through a literature review of a large number of studies, this review provides references for future research on oviposition-related genes in insects and the use of RNAi or CRISPR/Cas9 technology to verify the functions of oviposition-related genes and to prevent and control harmful insects.
Topics: Animals; CRISPR-Cas Systems; Egg Proteins; Female; Gene Expression; Genes, Insect; Insect Control; Insecta; Oogenesis; Oviposition; RNA Interference; Receptors, Cell Surface; Vitellogenins
PubMed: 33367730
DOI: 10.1093/jisesa/ieaa137 -
Biology Open May 2022Vitellogenin is an essential protein involved in ovary maturation in many animals. Detection of this protein correlated with reproductive capacity may be important if...
Vitellogenin is an essential protein involved in ovary maturation in many animals. Detection of this protein correlated with reproductive capacity may be important if carried out on marine organisms such as the red spiny lobster Palinurus elephas, a crustacean that is an economically important crop from wild fish catches. Moreover, in recent years, vitellogenin has assumed an important role as a possible biomarker of marine environmental pollution, as its expression levels can be influenced by the presence of similar estrogen pollutants and can affect the reproductive sphere of marine organisms such as crustaceans. The P. elephas vitellogenin protein and its coding gene have never been isolated, so there is little information about its presence in this lobster. The aim of the present study was to develop a molecular strategy to create, for the first time, an antibody for the detection and quantization of vitellogenin in P. elephas.
Topics: Animals; Crustacea; Female; Palinuridae; Peptides; RNA, Messenger; Vitellogenins
PubMed: 35452506
DOI: 10.1242/bio.059019 -
International Journal of Molecular... Oct 2022The fall armyworm is a highly polyphagous invasive pest. The strong reproductive capacity is an important factor in the rapid colonization and expansion of...
The fall armyworm is a highly polyphagous invasive pest. The strong reproductive capacity is an important factor in the rapid colonization and expansion of Vitellogenin (Vg) and vitellogenin receptor (VgR) play important roles in insect reproduction. As the precursor of vitellin (Vn), Vg provides essential nutrition for embryonic development, and VgR mediates the uptake of Vg by oocytes. In this context, we cloned and characterized these two genes of ( and ) and evaluated their expression profiles in different developmental stages and tissues. The RNA interference experiment was used to investigate their function in vitellogenesis. The ORF values of and were 5250 and 5445 bp, encoding 1749 and 1815 amino acid residues, respectively. The qRT-PCR results revealed that both and were highly expressed in female adults; was specifically expressed in the fat body, whereas was highly expressed in the ovary. In addition, the depletion of either or hindered oocyte maturation and ovarian development, leading to a significant decrease in fecundity. The present study reveals the importance of and in the vitellogenesis of , laying a theoretical foundation for the development of pollution-free pest control strategies with and as new targets.
Topics: Amino Acids; Animals; Female; Spodoptera; Vitellins; Vitellogenesis; Vitellogenins
PubMed: 36233286
DOI: 10.3390/ijms231911972 -
PLoS Pathogens Dec 2023Microsporidia are a group of obligate intracellular parasites that infect almost all animals, causing serious human diseases and major economic losses to the farming...
Microsporidia are a group of obligate intracellular parasites that infect almost all animals, causing serious human diseases and major economic losses to the farming industry. Nosema bombycis is a typical microsporidium that infects multiple lepidopteran insects via fecal-oral and transovarial transmission (TOT); however, the underlying TOT processes and mechanisms remain unknown. Here, we characterized the TOT process and identified key factors enabling N. bombycis to invade the ovariole and oocyte of silkworm Bombyx mori. We found that the parasites commenced with TOT at the early pupal stage when ovarioles penetrated the ovary wall and were exposed to the hemolymph. Subsequently, the parasites in hemolymph and hemolymph cells firstly infiltrated the ovariole sheath, from where they invaded the oocyte via two routes: (I) infecting follicular cells, thereby penetrating oocytes after proliferation, and (II) infecting nurse cells, thus entering oocytes following replication. In follicle and nurse cells, the parasites restructured and built large vacuoles to deliver themselves into the oocyte. In the whole process, the parasites were coated with B. mori vitellogenin (BmVg) on their surfaces. To investigate the BmVg effects on TOT, we suppressed its expression and found a dramatic decrease of pathogen load in both ovarioles and eggs, suggesting that BmVg plays a crucial role in the TOT. Thereby, we identified the BmVg domains and parasite spore wall proteins (SWPs) mediating the interaction, and demonstrated that the von Willebrand domain (VWD) interacted with SWP12, SWP26 and SWP30, and the unknown function domain (DUF1943) bound with the SWP30. When disrupting these interactions, we found significant reductions of the pathogen load in both ovarioles and eggs, suggesting that the interplays between BmVg and SWPs were vital for the TOT. In conclusion, our study has elucidated key aspects about the microsporidian TOT and revealed the key factors for understanding the molecular mechanisms underlying this transmission.
Topics: Animals; Humans; Vitellogenins; Spores, Fungal; Nosema; Bombyx
PubMed: 38060601
DOI: 10.1371/journal.ppat.1011859