Gonadulin: A newly discovered insulin-like peptide involved in ovulation and oviposition in Rhodnius prolixus, a vector of Chagas disease

Leyria, Jimena; Philip, Riya; Orchard, Ian; Lange, Angela B.

doi:10.1016/j.ibmb.2022.103848

Cited by 8 publications

(7 citation statements)

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“…The function of dilp7 is intriguing, as both ligand and receptor are well conserved in many animal species, but the data reported here do no contribute any insights as what its function might be. As in other arthropods (Veenstra et al, 2021;Leyria et al, 2022) the expression of gonadulin seems to be particularly abundant in the female reproductive system of the lower termites, but this signaling system was lost in higher termites. The expression of termite IGF suggests that it is likely a growth hormone as in other insect species.…”

Section: Plausible Functions Of Termite Ilpsmentioning

confidence: 50%

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Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Veenstra

2023

Preprint

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Background. Insulin-like growth factor (IGF) and other Insulin-like peptides (ilps) are important hormones regulating growth and development in animals. Whereas most animals have a single female and male adult phenotype, in some insect species the same genome may lead to different final forms. Perhaps the best known example is the honeybee where females can either develop into queens or workers. More extreme forms of such polyphenism occur in termites, where queens, kings, workers and soldiers coexist. Both juvenile hormone and insulin-like peptides are known to regulate growth and reproduction as well as polyphenism. In termites the role of juvenile hormone in reproduction and the induction of the soldier caste is well known, but the role of IGF and other ilps in these processes remains largely unknown. Here the various termite ilps are identified and hypotheses regarding their functions suggested. Methods. Genome assemblies and transcriptome short read archives (SRAs) were used to identify insulin-like peptides and neuropeptides in termites and to determine their expression in different species, tissues and castes. Results and Discussion. Termites have seven different ilps, i.e. gonadulin, IGF and an ortholog of Drosophila insulin-like peptide 7 (dilp7), which are commonly present in insects, and four smaller peptides, that have collectively been called short IGF-related peptides (sirps) and individually atirpin, birpin, cirpin and brovirpin. Gonadulin is lost from the higher termites which have however amplified the brovirpin gene, of which they often have two or three paralogs. Based on differential expression of these genes it seems likely that IGF is a growth hormone and atirpin an autocrine tissue factor that is released when a tissue faces metabolic stress. Birpin seems to be responsible for growth and in the absence of juvenile hormone this may lead to reproductive adults or, when juvenile hormone is present, to soldiers. Brovirpin is expressed both by the brain and the ovary and likely stimulates vitellogenesis, while the function of cirpin is less clear.

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Section: Plausible Functions Of Termite Ilpsmentioning

confidence: 50%

“…Males of the latter species show lower expression levels. This suggests that in these species the major tissue that expresses gonadulin is likely the female reproductive system, as in other insect species (Liao & Nässel, 2020;Veenstra, 2020a;Veenstra et al, 2021;Leyria et al, 2022).…”

Section: Expression and Functional Relevance Of Gonadulin And Dilp7 O...mentioning

confidence: 86%

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Veenstra

2023

Preprint

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“…Males of the latter species show lower expression levels. This suggests that in these species the major tissue that expresses gonadulin is likely the female reproductive system, as in other insect species ( Liao & Nässel, 2020 ; Veenstra, 2020 ; Veenstra et al, 2021 ; Leyria et al, 2022 ). However, as mentioned above, in several termites the gonadulin signaling pathway has been lost.…”

Section: Resultsmentioning

confidence: 84%

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Veenstra

2023

PeerJ

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Background Insulin-like growth factor (IGF) and other insulin-like peptides (ilps) are important hormones regulating growth and development in animals. Whereas most animals have a single female and male adult phenotype, in some insect species the same genome may lead to different final forms. Perhaps the best known example is the honeybee where females can either develop into queens or workers. More extreme forms of such polyphenism occur in termites, where queens, kings, workers and soldiers coexist. Both juvenile hormone and insulin-like peptides are known to regulate growth and reproduction as well as polyphenism. In termites the role of juvenile hormone in reproduction and the induction of the soldier caste is well known, but the role of IGF and other ilps in these processes remains largely unknown. Here the various termite ilps are identified and hypotheses regarding their functions suggested. Methods Genome assemblies and transcriptome short read archives (SRAs) were used to identify insulin-like peptides and neuropeptides in termites and to determine their expression in different species, tissues and castes. Results and Discussion Termites have seven different ilps, i.e. gonadulin, IGF and an ortholog of Drosophila insulin-like peptide 7 (dilp7), which are commonly present in insects, and four smaller peptides, that have collectively been called short IGF-related peptides (sirps) and individually atirpin, birpin, cirpin and brovirpin. Gonadulin is lost from the higher termites which have however amplified the brovirpin gene, of which they often have two or three paralogs. Based on differential expression of these genes it seems likely that IGF is a growth hormone and atirpin an autocrine tissue factor that is released when a tissue faces metabolic stress. Birpin seems to be responsible for growth and in the absence of juvenile hormone this may lead to reproductive adults or, when juvenile hormone is present, to soldiers. Brovirpin is expressed both by the brain and the ovary and likely stimulates vitellogenesis, while the function of cirpin is less clear.

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“…The dIlp8 mutant flies display ovulation defect and reduction of female fecundity ( Liao and Nässel, 2020 ). Orthologs of dIlp8 have been described under the name of gonadulin in several insect species, as RNA sequencing analyses suggest that they are highly expressed in the gonads ( Veenstra, 2020 ; Leyria et al, 2022 ). Knock-down of Ilp8/gonadulin expression by RNAi leads to oocyte growth inhibition in the migratory locust ( Veenstra et al, 2021 ) as well as ovulation defect in the kissing bug ( Leyria et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…Orthologs of dIlp8 have been described under the name of gonadulin in several insect species, as RNA sequencing analyses suggest that they are highly expressed in the gonads ( Veenstra, 2020 ; Leyria et al, 2022 ). Knock-down of Ilp8/gonadulin expression by RNAi leads to oocyte growth inhibition in the migratory locust ( Veenstra et al, 2021 ) as well as ovulation defect in the kissing bug ( Leyria et al, 2022 ). These observations suggest that Ilp8 might be generally involved in regulation of insect metabolism and reproduction, but the underlying mechanisms are not fully understood.…”

Section: Introductionmentioning

confidence: 99%

Insulin-like peptide 8 (Ilp8) regulates female fecundity in flies

Luo

et al. 2023

Front. Cell Dev. Biol.

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Introduction: Insulin-like peptides (Ilps) play crucial roles in nearly all life stages of insects. Ilp8 is involved in developmental stability, stress resistance and female fecundity in several insect species, but the underlying mechanisms are not fully understood. Here we report the functional characterization of Ilp8s in three fly species, including Bactrocera dorsalis, Drosophila mercatorum and Drosophila melanogaster.Methods: Phylogenetic analyses were performed to identify and characterize insect Ilp8s. The amino acid sequences of fly Ilp8s were aligned and the three-dimensional structures of fly Ilp8s were constructed and compared. The tissue specific expression pattern of fly Ilp8s were examined by qRT-PCR. In Bactrocera dorsalis and Drosophila mercatorum, dsRNAs were injected into virgin females to inhibit the expression of Ilp8 and the impacts on female fecundity were examined. In Drosophila melanogaster, the female fecundity of Ilp8 loss-of-function mutant was compared with wild type control flies. The mutant fruit fly strain was also used for sexual behavioral analysis and transcriptomic analysis.Results: Orthologs of Ilp8s are found in major groups of insects except for the lepidopterans and coleopterans, and Ilp8s are found to be well separated from other Ilps in three fly species. The key motif and the predicted three-dimensional structure of fly Ilp8s are well conserved. Ilp8 are specifically expressed in the ovary and are essential for female fecundity in three fly species. Behavior analysis demonstrates that Ilp8 mutation impairs female sexual attractiveness in fruit fly, which results in decreased mating success and is likely the cause of fecundity reduction. Further transcriptomic analysis indicates that Ilp8 might influence metabolism, immune activity, oocyte development as well as hormone homeostasis to collectively regulate female fecundity in the fruit fly.Discussion: Our findings support a universal role of insect Ilp8 in female fecundity, and also provide novel clues for understanding the modes of action of Ilp8.

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Gonadulin: A newly discovered insulin-like peptide involved in ovulation and oviposition in Rhodnius prolixus, a vector of Chagas disease

Cited by 8 publications

References 44 publications

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

Insulin-like peptide 8 (Ilp8) regulates female fecundity in flies

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