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 inPloS one Vol. 9; no. 9; p. e106737
Main Authors Marchal, Elisabeth, Hult, Ekaterina F, Huang, Juan, Pang, Zhenguo, Stay, Barbara, Tobe, Stephen S
Format Journal Article
LanguageEnglish
Published United States 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.
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
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  surname: Hult
  fullname: Hult, Ekaterina F
  organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
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  givenname: Juan
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  organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
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  surname: Tobe
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  organization: Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
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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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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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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
Volume 9
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