Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis

Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpeno...

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Veröffentlicht in:PLoS genetics 2015-03, Vol.11 (3), p.e1005038-e1005038
Hauptverfasser: Wen, Di, Rivera-Perez, Crisalejandra, Abdou, Mohamed, Jia, Qiangqiang, He, Qianyu, Liu, Xi, Zyaan, Ola, Xu, Jingjing, Bendena, William G, Tobe, Stephen S, Noriega, Fernando G, Palli, Subba R, Wang, Jian, Li, Sheng
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container_issue 3
container_start_page e1005038
container_title PLoS genetics
container_volume 11
creator Wen, Di
Rivera-Perez, Crisalejandra
Abdou, Mohamed
Jia, Qiangqiang
He, Qianyu
Liu, Xi
Zyaan, Ola
Xu, Jingjing
Bendena, William G
Tobe, Stephen S
Noriega, Fernando G
Palli, Subba R
Wang, Jian
Li, Sheng
description Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce.
doi_str_mv 10.1371/journal.pgen.1005038
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The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005038</identifier><identifier>PMID: 25774983</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Animals ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Biosynthesis ; Corpora Allata - growth &amp; development ; Corpora Allata - metabolism ; Drosophila ; Drosophila melanogaster - genetics ; Drosophila melanogaster - growth &amp; development ; Drosophila Proteins - biosynthesis ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Enzymes ; Experiments ; Fatty Acids, Monounsaturated - metabolism ; Fatty Acids, Unsaturated - biosynthesis ; Fatty Acids, Unsaturated - genetics ; Fatty Acids, Unsaturated - metabolism ; Genetic aspects ; Hydroxymethylglutaryl CoA Reductases - biosynthesis ; Hydroxymethylglutaryl CoA Reductases - genetics ; Identification and classification ; Insects ; Kruppel-Like Transcription Factors - genetics ; Kruppel-Like Transcription Factors - metabolism ; Larva ; Metamorphosis, Biological - genetics ; Methyltransferases - biosynthesis ; Methyltransferases - genetics ; Physiological aspects ; Protein synthesis ; Pupa ; Terpenoids ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>PLoS genetics, 2015-03, Vol.11 (3), p.e1005038-e1005038</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Wen et al 2015 Wen et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Metamorphosis. 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Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. 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Rivera-Perez, Crisalejandra ; Abdou, Mohamed ; Jia, Qiangqiang ; He, Qianyu ; Liu, Xi ; Zyaan, Ola ; Xu, Jingjing ; Bendena, William G ; Tobe, Stephen S ; Noriega, Fernando G ; Palli, Subba R ; Wang, Jian ; Li, Sheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c764t-3fce51e6fcc3f12b8010c0fcdeb63ac8eb6a3514fb61e9ff8e3200d9636090ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Acids</topic><topic>Animals</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Biosynthesis</topic><topic>Corpora Allata - growth &amp; development</topic><topic>Corpora Allata - metabolism</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - growth &amp; development</topic><topic>Drosophila Proteins - biosynthesis</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Enzymes</topic><topic>Experiments</topic><topic>Fatty Acids, Monounsaturated - metabolism</topic><topic>Fatty Acids, Unsaturated - biosynthesis</topic><topic>Fatty Acids, Unsaturated - genetics</topic><topic>Fatty Acids, Unsaturated - metabolism</topic><topic>Genetic aspects</topic><topic>Hydroxymethylglutaryl CoA Reductases - biosynthesis</topic><topic>Hydroxymethylglutaryl CoA Reductases - genetics</topic><topic>Identification and classification</topic><topic>Insects</topic><topic>Kruppel-Like Transcription Factors - genetics</topic><topic>Kruppel-Like Transcription Factors - metabolism</topic><topic>Larva</topic><topic>Metamorphosis, Biological - genetics</topic><topic>Methyltransferases - biosynthesis</topic><topic>Methyltransferases - genetics</topic><topic>Physiological aspects</topic><topic>Protein synthesis</topic><topic>Pupa</topic><topic>Terpenoids</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wen, Di</creatorcontrib><creatorcontrib>Rivera-Perez, Crisalejandra</creatorcontrib><creatorcontrib>Abdou, Mohamed</creatorcontrib><creatorcontrib>Jia, Qiangqiang</creatorcontrib><creatorcontrib>He, Qianyu</creatorcontrib><creatorcontrib>Liu, Xi</creatorcontrib><creatorcontrib>Zyaan, Ola</creatorcontrib><creatorcontrib>Xu, Jingjing</creatorcontrib><creatorcontrib>Bendena, William G</creatorcontrib><creatorcontrib>Tobe, Stephen S</creatorcontrib><creatorcontrib>Noriega, Fernando G</creatorcontrib><creatorcontrib>Palli, Subba R</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Li, Sheng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wen, Di</au><au>Rivera-Perez, Crisalejandra</au><au>Abdou, Mohamed</au><au>Jia, Qiangqiang</au><au>He, Qianyu</au><au>Liu, Xi</au><au>Zyaan, Ola</au><au>Xu, Jingjing</au><au>Bendena, William G</au><au>Tobe, Stephen S</au><au>Noriega, Fernando G</au><au>Palli, Subba R</au><au>Wang, Jian</au><au>Li, Sheng</au><au>Schoofs, Liliane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>11</volume><issue>3</issue><spage>e1005038</spage><epage>e1005038</epage><pages>e1005038-e1005038</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. 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subjects Acids
Animals
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Biosynthesis
Corpora Allata - growth & development
Corpora Allata - metabolism
Drosophila
Drosophila melanogaster - genetics
Drosophila melanogaster - growth & development
Drosophila Proteins - biosynthesis
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Enzymes
Experiments
Fatty Acids, Monounsaturated - metabolism
Fatty Acids, Unsaturated - biosynthesis
Fatty Acids, Unsaturated - genetics
Fatty Acids, Unsaturated - metabolism
Genetic aspects
Hydroxymethylglutaryl CoA Reductases - biosynthesis
Hydroxymethylglutaryl CoA Reductases - genetics
Identification and classification
Insects
Kruppel-Like Transcription Factors - genetics
Kruppel-Like Transcription Factors - metabolism
Larva
Metamorphosis, Biological - genetics
Methyltransferases - biosynthesis
Methyltransferases - genetics
Physiological aspects
Protein synthesis
Pupa
Terpenoids
Transcription Factors - genetics
Transcription Factors - metabolism
title Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis
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