Methoprene-tolerant (Met) knockdown in the adult female cockroach, Diploptera punctata completely inhibits ovarian development
Independent of the design of the life cycle of any insect, their growth and reproduction are highly choreographed through the action of two versatile hormones: ecdysteroids and juvenile hormones (JH). However, the means by which JH can target tissues and exert its pleiotropic physiological effects i...
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Published in | PloS one Vol. 9; no. 9; p. e106737 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
08.09.2014
Public Library of Science (PLoS) |
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Abstract | Independent of the design of the life cycle of any insect, their growth and reproduction are highly choreographed through the action of two versatile hormones: ecdysteroids and juvenile hormones (JH). However, the means by which JH can target tissues and exert its pleiotropic physiological effects is currently still not completely elucidated. Although the identity of the one JH receptor is currently still elusive, recent evidence seems to point to the product of the Methoprene-tolerant gene (Met) as the most likely contender in transducing the action of JH. Studies on the role of this transcription factor have mostly been focused on immature insect stages. In this study we used the viviparous cockroach Diploptera punctata, a favorite model in studying JH endocrinology, to examine the role of Met during reproduction. A tissue distribution and developmental profile of transcript levels was determined for Met and its downstream partners during the first gonadotropic cycle of this cockroach. Using RNA interference, our study shows that silencing Met results in an arrest of basal oocyte development; vitellogenin is no longer transcribed in the fat body and no longer taken up by the ovary. Patency is not induced in these animals which fail to produce the characteristic profile of JH biosynthesis typical of the first gonadotropic cycle. Moreover, the ultrastructure of the follicle cells showed conspicuous whorls of rough endoplasmic reticulum and a failure to form chorion. Our study describes the role of Met on a cellular and physiological level during insect reproduction, and confirms the role of Met as a key factor in the JH signaling pathway. |
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AbstractList | Independent of the design of the life cycle of any insect, their growth and reproduction are highly choreographed through the action of two versatile hormones: ecdysteroids and juvenile hormones (JH). However, the means by which JH can target tissues and exert its pleiotropic physiological effects is currently still not completely elucidated. Although the identity of the one JH receptor is currently still elusive, recent evidence seems to point to the product of the Methoprene-tolerant gene (Met) as the most likely contender in transducing the action of JH. Studies on the role of this transcription factor have mostly been focused on immature insect stages. In this study we used the viviparous cockroach Diploptera punctata, a favorite model in studying JH endocrinology, to examine the role of Met during reproduction. A tissue distribution and developmental profile of transcript levels was determined for Met and its downstream partners during the first gonadotropic cycle of this cockroach. Using RNA interference, our study shows that silencing Met results in an arrest of basal oocyte development; vitellogenin is no longer transcribed in the fat body and no longer taken up by the ovary. Patency is not induced in these animals which fail to produce the characteristic profile of JH biosynthesis typical of the first gonadotropic cycle. Moreover, the ultrastructure of the follicle cells showed conspicuous whorls of rough endoplasmic reticulum and a failure to form chorion. Our study describes the role of Met on a cellular and physiological level during insect reproduction, and confirms the role of Met as a key factor in the JH signaling pathway. Independent of the design of the life cycle of any insect, their growth and reproduction are highly choreographed through the action of two versatile hormones: ecdysteroids and juvenile hormones (JH). However, the means by which JH can target tissues and exert its pleiotropic physiological effects is currently still not completely elucidated. Although the identity of the one JH receptor is currently still elusive, recent evidence seems to point to the product of the Methoprene-tolerant gene (Met) as the most likely contender in transducing the action of JH. Studies on the role of this transcription factor have mostly been focused on immature insect stages. In this study we used the viviparous cockroach Diploptera punctata , a favorite model in studying JH endocrinology, to examine the role of Met during reproduction. A tissue distribution and developmental profile of transcript levels was determined for Met and its downstream partners during the first gonadotropic cycle of this cockroach. Using RNA interference, our study shows that silencing Met results in an arrest of basal oocyte development; vitellogenin is no longer transcribed in the fat body and no longer taken up by the ovary. Patency is not induced in these animals which fail to produce the characteristic profile of JH biosynthesis typical of the first gonadotropic cycle. Moreover, the ultrastructure of the follicle cells showed conspicuous whorls of rough endoplasmic reticulum and a failure to form chorion. Our study describes the role of Met on a cellular and physiological level during insect reproduction, and confirms the role of Met as a key factor in the JH signaling pathway. |
Author | Marchal, Elisabeth Stay, Barbara Hult, Ekaterina F Pang, Zhenguo Tobe, Stephen S Huang, Juan |
AuthorAffiliation | University of Cincinnati, United States of America 1 Department of Cell and Systems Biology, University of Toronto, Toronto, Canada 2 Department of Biology, University of Iowa, Iowa City, Iowa, United States of America |
AuthorAffiliation_xml | – name: 1 Department of Cell and Systems Biology, University of Toronto, Toronto, Canada – name: University of Cincinnati, United States of America – name: 2 Department of Biology, University of Iowa, Iowa City, Iowa, United States of America |
Author_xml | – sequence: 1 givenname: Elisabeth surname: Marchal fullname: Marchal, Elisabeth organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada – sequence: 2 givenname: Ekaterina F surname: Hult fullname: Hult, Ekaterina F organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada – sequence: 3 givenname: Juan surname: Huang fullname: Huang, Juan organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada – sequence: 4 givenname: Zhenguo surname: Pang fullname: Pang, Zhenguo organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada – sequence: 5 givenname: Barbara surname: Stay fullname: Stay, Barbara organization: Department of Biology, University of Iowa, Iowa City, Iowa, United States of America – sequence: 6 givenname: Stephen S surname: Tobe fullname: Tobe, Stephen S organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25197795$$D View this record in MEDLINE/PubMed |
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Copyright | 2014 Marchal et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2014 Marchal et al 2014 Marchal et al |
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DocumentTitleAlternate | Role of Met in Cockroach Ovarian Development |
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Editor | Benoit, Joshua B. |
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Notes | Conceived and designed the experiments: EM EFH SST. Performed the experiments: EM EFH JH ZP. Analyzed the data: EM EFH JH BS SST. Contributed reagents/materials/analysis tools: SST. Contributed to the writing of the manuscript: EM EFH BS SST. Competing Interests: The authors have declared that no competing interests exist. Current address: Research group of Molecular Developmental Physiology and Signal Transduction, Department of Biology, Katholieke Universiteit Leuven, Leuven, Belgium |
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Snippet | Independent of the design of the life cycle of any insect, their growth and reproduction are highly choreographed through the action of two versatile hormones:... |
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StartPage | e106737 |
SubjectTerms | Animal behavior Animals Biology Biology and life sciences Biosynthesis Blattella germanica Chorion Cockroaches Cockroaches - drug effects Diploptera punctata Drosophila Ecdysteroids Endocrinology Endoplasmic reticulum Fat body Female Females Hormones Insects Insulin Juvenile hormones Life cycle engineering Life cycles Methoprene Methoprene - toxicity Ovary - drug effects Physiological effects Physiology Pituitary (anterior) Real-Time Polymerase Chain Reaction Reproduction Ribonucleic acid RNA RNA Interference RNA-mediated interference Signal Transduction Signaling Tissues Transcription factors Tribolium castaneum Ultrastructure Vitellogenin |
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Title | Methoprene-tolerant (Met) knockdown in the adult female cockroach, Diploptera punctata completely inhibits ovarian development |
URI | https://www.ncbi.nlm.nih.gov/pubmed/25197795 https://www.proquest.com/docview/1560821708 https://pubmed.ncbi.nlm.nih.gov/PMC4157775 https://doaj.org/article/f7d01d23dd0e4cb695231f8f7938cab1 http://dx.doi.org/10.1371/journal.pone.0106737 |
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