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PLoS Genetics Aug 2022The decision to engage in courtship depends on external cues from potential mates and internal cues related to maturation, health, and experience. Hormones allow for...
The decision to engage in courtship depends on external cues from potential mates and internal cues related to maturation, health, and experience. Hormones allow for coordinated conveyance of such information to peripheral tissues. Here, we show Ecdysis-Triggering Hormone (ETH) is critical for courtship inhibition after completion of copulation in Drosophila melanogaster. ETH deficiency relieves post-copulation courtship inhibition (PCCI) and increases male-male courtship. ETH appears to modulate perception and attractiveness of potential mates by direct action on primary chemosensory neurons. Knockdown of ETH receptor (ETHR) expression in GR32A-expressing neurons leads to reduced ligand sensitivity and elevated male-male courtship. We find OR67D also is critical for normal levels of PCCI after mating. ETHR knockdown in OR67D-expressing neurons or GR32A-expressing neurons relieves PCCI. Finally, ETHR silencing in the corpus allatum (CA), the sole source of juvenile hormone, also relieves PCCI; treatment with the juvenile hormone analog methoprene partially restores normal post-mating behavior. We find that ETH, a stress-sensitive reproductive hormone, appears to coordinate multiple sensory modalities to guide Drosophila male courtship behaviors, especially after mating.
Topics: Animals; Courtship; Drosophila; Drosophila Proteins; Drosophila melanogaster; Juvenile Hormones; Male; Neurons; Sexual Behavior, Animal
PubMed: 35998183
DOI: 10.1371/journal.pgen.1010357 -
PLoS Genetics Sep 2023TAIMAN (TAI), the only insect ortholog of mammalian Steroid Receptor Coactivators (SRCs), is a critical modulator of ecdysone and juvenile hormone (JH) signaling...
TAIMAN (TAI), the only insect ortholog of mammalian Steroid Receptor Coactivators (SRCs), is a critical modulator of ecdysone and juvenile hormone (JH) signaling pathways, which govern insect development and reproduction. The modulatory effect is mediated by JH-dependent TAI's heterodimerization with JH receptor Methoprene-tolerant and association with the Ecdysone Receptor complex. Insect hormones regulate insect physiology and development in concert with abiotic cues, such as photo- and thermoperiod. Here we tested the effects of JH and ecdysone signaling on the circadian clock by a combination of microsurgical operations, application of hormones and hormone mimics, and gene knockdowns in the linden bug Pyrrhocoris apterus males. Silencing taiman by each of three non-overlapping double-strand RNA fragments dramatically slowed the free-running period (FRP) to 27-29 hours, contrasting to 24 hours in controls. To further corroborate TAIMAN's clock modulatory function in the insect circadian clock, we performed taiman knockdown in the cockroach Blattella germanica. Although Blattella and Pyrrhocoris lineages separated ~380 mya, B. germanica taiman silencing slowed the FRP by more than 2 hours, suggesting a conserved TAI clock function in (at least) some insect groups. Interestingly, the pace of the linden bug circadian clock was neither changed by blocking JH and ecdysone synthesis, by application of the hormones or their mimics nor by the knockdown of corresponding hormone receptors. Our results promote TAI as a new circadian clock modulator, a role described for the first time in insects. We speculate that TAI participation in the clock is congruent with the mammalian SRC-2 role in orchestrating metabolism and circadian rhythms, and that TAI/SRCs might be conserved components of the circadian clock in animals.
Topics: Animals; Male; Circadian Clocks; Ecdysone; Insecta; Circadian Rhythm; Cell Membrane; Juvenile Hormones; Mammals
PubMed: 37683015
DOI: 10.1371/journal.pgen.1010924 -
ELife May 2023For at least two centuries, scientists have been enthralled by the "zombie" behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases...
For at least two centuries, scientists have been enthralled by the "zombie" behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the - "zombie fly" system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the "zombie fly" brain by cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly's hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
Topics: Animals; Drosophila; Drosophila melanogaster; Parasites; Corpora Allata; Juvenile Hormones
PubMed: 37184212
DOI: 10.7554/eLife.85410 -
PloS One 2022The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), a primary pest of soybean, poses a severe threat to soybean production. In this study, the 4th instar...
The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), a primary pest of soybean, poses a severe threat to soybean production. In this study, the 4th instar nymphs were exposed to the LC50 and LC30 of imidacloprid and thiamethoxam from F0 to F4 generations to evaluate the activities of peroxidase, pyruvate kinase, and trehalase using microassay. We found that peroxidase and pyruvate kinase activities in soybean aphids increased rapidly, first to peak and then decreased slowly generation by generation under imidacloprid and thiamethoxam stress. In contrast, the trehalase activity was significantly decreased in F1 to F5 generations when treated with the LC50 and LC30 and imidacloprid and thiamethoxam compared to control. In addition, the Enzyme-Linked Immunosorbent Assay (ELISA) was used to monitor the changes in molting and juvenile hormone expressions of the soybean aphids in each generation (F1-F5). The expression of juvenile hormone in soybean aphids was increased significantly in each generation under continuous stress of imidacloprid and thiamethoxam LC50 imidacloprid and LC50 thiamethoxam inhibited the expression of molting hormones in soybean aphids of each generation. LC30 imidacloprid or LC30 thiamethoxam significantly stimulated the expression of molting hormone in the 1st and 2nd instar nymphs in each generation. In this paper, the differences in antioxidant regulation, energy metabolism intensity, and hormone expression of multi-generation soybean aphids were monitored under continuous stress of imidacloprid and thiamethoxam. Our results revealed the effects of continuous insecticide stress on the main endogenous substances. Further, they clarified the regulation rules of resistance in soybean aphids, providing a reference for efficient control with imidacloprid and thiamethoxam.
Topics: Animals; Aphids; Juvenile Hormones; Neonicotinoids; Nitro Compounds; Nymph; Peroxidases; Pyruvate Kinase; Glycine max; Thiamethoxam; Trehalase
PubMed: 35802579
DOI: 10.1371/journal.pone.0271069 -
BMC Evolutionary Biology Mar 2014The genetic and physiological pathways regulating behavior in solitary species are hypothesized to have been co-opted to regulate social behavior in social species. One...
BACKGROUND
The genetic and physiological pathways regulating behavior in solitary species are hypothesized to have been co-opted to regulate social behavior in social species. One classic example is the interaction between vitellogenin (an egg-yolk and storage protein) and juvenile hormone, which are positively correlated in most insect species but have modified interactions in highly eusocial insects. In some of these species (including some termites, ants, and the honey bee), juvenile hormone and vitellogenin levels are negatively correlated and juvenile hormone has shifted its role from a gonadotropin to a regulator of maturation and division of labor in the primarily sterile workers. The function of vitellogenin also seems to have broadened to encompass similar roles. Thus, the functions and molecular interactions of juvenile hormone and vitellogenin are hypothesized to have undergone changes during the evolution of eusociality, but the mechanisms underlying these changes are unknown.Bumble bees offer an excellent model system for testing how the relationship between juvenile hormone and vitellogenin evolved from solitary to social species. Bumble bee colonies are primitively eusocial and comprised of a single reproductive queen and facultatively sterile workers. In Bombus terrestris, juvenile hormone retains its ancestral role as a gonadotropin and is also hypothesized to regulate aggressive behavior. However, the function of vitellogenin and its interactions with juvenile hormone have not yet been characterized.
RESULTS
By characterizing vitellogenin RNA expression levels (vg) in B. terrestris we show that vg is not associated with task and only partially associated with worker age, queen presence, and caste (queen vs worker). The correlations of vg with ovarian activation were not consistent across experiments, but both vg and ovarian activation were significantly associated with levels of aggression experienced by workers. Treatment with juvenile hormone did not affect vg levels in queenless groups.
CONCLUSIONS
We suggest that social interactions affect vg levels more strongly than a worker's reproductive physiological state, and that juvenile hormone and vg are uncoupled in this species. Thus, although juvenile hormone maintains its traditional role as gonadotropin in B. terrestris, vg has already been co-opted into a novel role, consistent with the model that Bombus represents an intermediate stage in the evolution of eusociality.
Topics: Animals; Bees; Biological Evolution; Female; Insect Proteins; Juvenile Hormones; Male; Models, Biological; RNA, Messenger; Reproduction; Social Behavior; Vitellogenins
PubMed: 24618396
DOI: 10.1186/1471-2148-14-45 -
PloS One 2021In the highly eusocial wasp, Vespula vulgaris, queens produce honest signals to alert their subordinate workers of their fertility status, and therefore they are...
In the highly eusocial wasp, Vespula vulgaris, queens produce honest signals to alert their subordinate workers of their fertility status, and therefore they are reproductively suppressed and help in the colony. The honesty of the queen signals is likely maintained due to hormonal regulation, which affects fertility and fertility cue expression. Here, we tested if hormonal pleiotropy could support the hypothesis that juvenile hormone controls fertility and fertility signaling in workers. In addition, we aimed to check oocyte size as a proxy of fertility. To do that, we treated V. vulgaris workers with synthetic versions of juvenile hormone (JH) analogue and a JH inhibitor, methoprene and precocene, respectively. We dissected the treated females to check ovary activation and analyzed their chemical profile. Our results showed that juvenile hormone has an influence on the abundance of fertility linked compounds produced by workers, and it also showed to increase oocyte size in workers. Our results corroborate the hypothesis that juvenile hormone controls fertility and fertility signaling in workers, whereby workers are unable to reproduce without alerting other colony members of their fertility. This provides supports the hypothesis that hormonal pleiotropy contributes to keeping the queen fertility signals honest.
Topics: Animals; Female; Fertility; Juvenile Hormones; Reproduction; Signal Transduction; Wasps
PubMed: 33999926
DOI: 10.1371/journal.pone.0250720 -
Frontiers in Immunology 2022Cry toxins produced by (Bt) are well known for their insecticidal activities against Lepidopteran, Dipteran, and Coleopteran species. In our previous work, we showed...
Cry toxins produced by (Bt) are well known for their insecticidal activities against Lepidopteran, Dipteran, and Coleopteran species. In our previous work, we showed that trypsin-digested full-length Cry7Ab4 protoxin did not have insecticidal activity against larvae but strongly inhibited their growth. In this paper, we expressed and purified recombinant active Cry7Ab4 toxic core from for bioassay and identified its binding proteins. Interestingly, Cry7Ab4 toxic core exhibited activity to delay the pupation of larvae. Using protein pull-down assay, several proteins, including basic juvenile hormone-suppressible protein 1-like (BJSP-1), were identified from the midgut juice of larvae as putative Cry7Ab4-binding proteins. We showed that feeding larval Cry7Ab4 toxic core upregulated the level of BJSP-1 mRNA in the hemocytes and fat body and decreased the free juvenile hormone (JH) level in larvae. BJSP-1 interacted with Cry7Ab4 and bound to free JH . A possible mechanism of Cry7Ab4 in delaying the pupation of larvae was proposed.
Topics: Animals; Bacterial Proteins; Insect Proteins; Insecticides; Juvenile Hormones; Larva; Moths; RNA, Messenger; Trypsin
PubMed: 36159828
DOI: 10.3389/fimmu.2022.849620 -
Scientific Reports Oct 2021In recent years, there has been a rise in the emergence of arboviruses of public health importance, including Zika, chikungunya, dengue, and yellow fever viruses....
In recent years, there has been a rise in the emergence of arboviruses of public health importance, including Zika, chikungunya, dengue, and yellow fever viruses. Insecticide-based mosquito control has been the primary method for mitigating transmission of arboviruses. The consequences for the application of insecticides include both lethal and sublethal effects, and associated development of insecticide resistance. However, little is known about the influence on arboviral transmission. Mosquitoes with phenotypes that exhibit insecticide resistance or experience sublethal effects may be associated with altered susceptibility to arbovirus infection and transmission. Juvenile hormone analogs (JHAs) are insecticides that prevent pupa to adult molting of mosquitoes by mimicking the action of their natural juvenile hormone. Here, we examined whether the JHA pyriproxyfen interacts with ambient temperature (20 °C and 30 °C) during juvenile stages to influence life-history traits, population growth (λ'), and Zika virus (ZIKV) infection in Aedes aegypti. Development time of females was lengthened at 20 °C and in the presence of JHA. Prevention of pupa to adult molting by JHA was differentially higher at elevated temperature than low temperature. Size of females was larger at 20 °C and smaller at 30 °C. Infection, disseminated infection, and transmission of ZIKV in females were enhanced by JHA at both 20 °C and 30 °C relative to the controls. These results demonstrate that mosquito life-history and vector competence parameters are strongly influenced by interactive effects of JHA and temperature. The JHA-induced enhancement of ZIKV infection in females should be a consideration when implementing JHA in vector control strategies.
Topics: Aedes; Animals; Female; Insecticides; Juvenile Hormones; Zika Virus; Zika Virus Infection
PubMed: 34702871
DOI: 10.1038/s41598-021-00432-1 -
BMC Biology Dec 2022In insects, an interplay between the activities of distinct hormones, such as juvenile hormone (JH) and 20-hydroxyecdysone (20E), regulates the progression through...
BACKGROUND
In insects, an interplay between the activities of distinct hormones, such as juvenile hormone (JH) and 20-hydroxyecdysone (20E), regulates the progression through numerous life history hallmarks. As a crucial endocrine factor, JH is mainly synthesized in the corpora allata (CA) to regulate multiple physiological and developmental processes, including molting, metamorphosis, and reproduction. During the last century, significant progress has been achieved in elucidating the JH signal transduction pathway, while less progress has been made in dissecting the regulatory mechanism of JH biosynthesis. Previous work has shown that receptor tyrosine kinase (RTK) signaling regulates hormone biosynthesis in both insects and mammals. Here, we performed a systematic RNA interference (RNAi) screening to identify RTKs involved in regulating JH biosynthesis in the CA of adult Blattella germanica females.
RESULTS
We found that the epidermal growth factor receptor (Egfr) is required for promoting JH biosynthesis in the CA of adult females. The Egf ligands Vein and Spitz activate Egfr, followed by Ras/Raf/ERK signaling, and finally activation of the downstream transcription factor Pointed (Pnt). Importantly, Pnt induces the transcriptional expression of two key enzyme-encoding genes in the JH biosynthesis pathway: juvenile hormone acid methyltransferase (JHAMT) and methyl farnesoate epoxidase (CYP15A1). Dual-luciferase reporter assay shows that Pnt is able to activate a promoter region of Jhamt. In addition, electrophoretic mobility shift assay confirms that Pnt directly binds to the - 941~ - 886 nt region of the Jhamt promoter.
CONCLUSIONS
This study reveals the detailed molecular mechanism of Egfr signaling in promoting JH biosynthesis in the German cockroach, shedding light on the intricate regulation of JH biosynthesis during insect development.
Topics: Animals; Female; Blattellidae; Corpora Allata; Juvenile Hormones; Metamorphosis, Biological; Signal Transduction; Mammals
PubMed: 36514097
DOI: 10.1186/s12915-022-01484-z -
Scientific Reports Sep 2017Hormones play essential roles during development and maintaining homeostasis in adult organisms, regulating a plethora of biological processes. Generally, hormones are...
Hormones play essential roles during development and maintaining homeostasis in adult organisms, regulating a plethora of biological processes. Generally, hormones are secreted by glands and perform a systemic action. Here we show that Juvenile Hormones (JHs), insect sesquiterpenoids synthesized by the corpora allata, are also synthesized by the adult Drosophila gut. This local, gut specific JH activity, is synthesized by and acts on the intestinal stem cell and enteroblast populations, regulating their survival and cellular growth through the JH receptors Gce/Met and the coactivator Tai. Furthermore, we show that this local JH activity is important for damage response and is necessary for intestinal tumor growth driven by activating mutations in Wnt and EGFR/Ras pathways. Together, our results identify JHs as key hormonal regulators of gut homeostasis and open the possibility that analogous hormones may play a similar role in maintaining vertebrate adult intestinal stem cell population and sustaining tumor growth.
Topics: Animals; Cell Proliferation; Drosophila; Gastrointestinal Tract; Homeostasis; Intestinal Neoplasms; Juvenile Hormones; Stem Cells
PubMed: 28916802
DOI: 10.1038/s41598-017-11199-9