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Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)

SIMPLE SUMMARY: The tobacco cutworm, Spodoptera litura (F.), exemplifies strong reproductive capacities and damages many agricultural crops. The insulin signaling pathway is known as a key determinant of female reproduction in insects. However, the detailed molecular mechanisms in these processes ar...

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Autores principales: Pan, Xue, Pei, Yanfang, Zhang, Cuici, Huang, Yaling, Chen, Ling, Wei, Liqiong, Li, Chuanren, Dong, Xiaolin, Chen, Xiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409390/
https://www.ncbi.nlm.nih.gov/pubmed/36005325
http://dx.doi.org/10.3390/insects13080701
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author Pan, Xue
Pei, Yanfang
Zhang, Cuici
Huang, Yaling
Chen, Ling
Wei, Liqiong
Li, Chuanren
Dong, Xiaolin
Chen, Xiang
author_facet Pan, Xue
Pei, Yanfang
Zhang, Cuici
Huang, Yaling
Chen, Ling
Wei, Liqiong
Li, Chuanren
Dong, Xiaolin
Chen, Xiang
author_sort Pan, Xue
collection PubMed
description SIMPLE SUMMARY: The tobacco cutworm, Spodoptera litura (F.), exemplifies strong reproductive capacities and damages many agricultural crops. The insulin signaling pathway is known as a key determinant of female reproduction in insects. However, the detailed molecular mechanisms in these processes are poorly studied. Here, we injected bovine insulin into the newly emerged moth, resulting in gene expression changes in the insulin pathway, while knockdown of SlInR caused an inverse gene expression change involved in the insulin pathway. Further studies indicated that the content of JH-III, Vg, total proteins and triacylgycerol could be suppressed by SlInR dsRNA injection. Furthermore, stunted ovaries and lower fecundity were observed by RNAi. Our studies indicated that SlInR plays a key role in JH-III synthesis and the ovarian development in S. litura. ABSTRACT: Insulin signaling can regulate various physiological functions, such as energy metabolism and reproduction and so on, in many insects, including mosquito and locust. However, the molecular mechanism of this physiological process remains elusive. The tobacco cutworm, Spodoptera litura, is one of the most important pests of agricultural crops around the world. In this study, phosphoinositide 3-kinase (SlPI3K), protein kinase B (SlAKT), target of rapamycin (SlTOR), ribosomal protein S6 kinase (SlS6K) and transcription factor cAMP-response element binding protein (SlCREB) genes, except transcription factor forkhead box class O (SlFoxO), can be activated by bovine insulin injection. Then, we studied the influence of the insulin receptor gene (SlInR) on the reproduction of S. litura using RNA interference technology. qRT-PCR analysis revealed that SlInR was most abundant in the head. The SlPI3K, SlAKT, SlTOR, SlS6K and SlCREB genes were decreased, except SlFoxO, after the SlInR gene knockdown. Further studies revealed that the expression of vitellogenin mRNA and protein, Methoprene-tolerant gene (SlMet), could be down-regulated by the injection of dsRNA of SlInR significantly. Furthermore, a depletion in the insulin receptor by RNAi significantly decreased the content of juvenile hormone III (JH-III), total proteins and triacylgycerol. These changes indicated that a lack of SlInR could impair ovarian development and decrease fecundity in S. litura. Our studies contribute to a comprehensive insight into reproduction, regulated by insulin and the juvenile hormone signaling pathway through nutrition, and a provide theoretical basis for the reproduction process in pest insects.
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spelling pubmed-94093902022-08-26 Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.) Pan, Xue Pei, Yanfang Zhang, Cuici Huang, Yaling Chen, Ling Wei, Liqiong Li, Chuanren Dong, Xiaolin Chen, Xiang Insects Article SIMPLE SUMMARY: The tobacco cutworm, Spodoptera litura (F.), exemplifies strong reproductive capacities and damages many agricultural crops. The insulin signaling pathway is known as a key determinant of female reproduction in insects. However, the detailed molecular mechanisms in these processes are poorly studied. Here, we injected bovine insulin into the newly emerged moth, resulting in gene expression changes in the insulin pathway, while knockdown of SlInR caused an inverse gene expression change involved in the insulin pathway. Further studies indicated that the content of JH-III, Vg, total proteins and triacylgycerol could be suppressed by SlInR dsRNA injection. Furthermore, stunted ovaries and lower fecundity were observed by RNAi. Our studies indicated that SlInR plays a key role in JH-III synthesis and the ovarian development in S. litura. ABSTRACT: Insulin signaling can regulate various physiological functions, such as energy metabolism and reproduction and so on, in many insects, including mosquito and locust. However, the molecular mechanism of this physiological process remains elusive. The tobacco cutworm, Spodoptera litura, is one of the most important pests of agricultural crops around the world. In this study, phosphoinositide 3-kinase (SlPI3K), protein kinase B (SlAKT), target of rapamycin (SlTOR), ribosomal protein S6 kinase (SlS6K) and transcription factor cAMP-response element binding protein (SlCREB) genes, except transcription factor forkhead box class O (SlFoxO), can be activated by bovine insulin injection. Then, we studied the influence of the insulin receptor gene (SlInR) on the reproduction of S. litura using RNA interference technology. qRT-PCR analysis revealed that SlInR was most abundant in the head. The SlPI3K, SlAKT, SlTOR, SlS6K and SlCREB genes were decreased, except SlFoxO, after the SlInR gene knockdown. Further studies revealed that the expression of vitellogenin mRNA and protein, Methoprene-tolerant gene (SlMet), could be down-regulated by the injection of dsRNA of SlInR significantly. Furthermore, a depletion in the insulin receptor by RNAi significantly decreased the content of juvenile hormone III (JH-III), total proteins and triacylgycerol. These changes indicated that a lack of SlInR could impair ovarian development and decrease fecundity in S. litura. Our studies contribute to a comprehensive insight into reproduction, regulated by insulin and the juvenile hormone signaling pathway through nutrition, and a provide theoretical basis for the reproduction process in pest insects. MDPI 2022-08-04 /pmc/articles/PMC9409390/ /pubmed/36005325 http://dx.doi.org/10.3390/insects13080701 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Pan, Xue
Pei, Yanfang
Zhang, Cuici
Huang, Yaling
Chen, Ling
Wei, Liqiong
Li, Chuanren
Dong, Xiaolin
Chen, Xiang
Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title_full Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title_fullStr Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title_full_unstemmed Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title_short Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)
title_sort effect of insulin receptor on juvenile hormone signal and fecundity in spodoptera litura (f.)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409390/
https://www.ncbi.nlm.nih.gov/pubmed/36005325
http://dx.doi.org/10.3390/insects13080701
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