Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex

Juvenile hormone (JH) regulates insect development by a poorly understood mechanism. Application of JH agonist insecticides to Drosophila melanogaster during the ecdysone-driven onset of metamorphosis results in lethality and specific morphogenetic defects, some of which resemble those in mutants of...

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Veröffentlicht in:Genetics (Austin) 2006-01, Vol.172 (1), p.253-264
Hauptverfasser: Wilson, Thomas G, Yerushalmi, Yoram, Donnell, David M, Restifo, Linda L
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creator Wilson, Thomas G
Yerushalmi, Yoram
Donnell, David M
Restifo, Linda L
description Juvenile hormone (JH) regulates insect development by a poorly understood mechanism. Application of JH agonist insecticides to Drosophila melanogaster during the ecdysone-driven onset of metamorphosis results in lethality and specific morphogenetic defects, some of which resemble those in mutants of the ecdysone-regulated Broad-Complex (BR-C). The Methoprene-tolerant (Met) bHLH-PAS gene mediates JH action, and Met mutations protect against the lethality and defects. To explore relationships among these two genes and JH, double mutants were constructed between Met alleles and alleles of each of the BR-C complementation groups: broad (br), reduced bristles on palpus (rbp), and 2Bc. Defects in viability and oogenesis were consistently more severe in rbp Met or br Met double mutants than would be expected if these genes act independently. Additionally, complementation between BR-C mutant alleles often failed when MET was absent. Patterns of BRC protein accumulation during metamorphosis revealed essentially no difference between wild-type and Met-null individuals. JH agonist treatment did not block accumulation of BRC proteins. We propose that MET and BRC interact to control transcription of one or more downstream effector genes, which can be disrupted either by mutations in Met or BR-C or by application of JH/JH agonist, which alters MET interaction with BRC.
doi_str_mv 10.1534/genetics.105.046631
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Application of JH agonist insecticides to Drosophila melanogaster during the ecdysone-driven onset of metamorphosis results in lethality and specific morphogenetic defects, some of which resemble those in mutants of the ecdysone-regulated Broad-Complex (BR-C). The Methoprene-tolerant (Met) bHLH-PAS gene mediates JH action, and Met mutations protect against the lethality and defects. To explore relationships among these two genes and JH, double mutants were constructed between Met alleles and alleles of each of the BR-C complementation groups: broad (br), reduced bristles on palpus (rbp), and 2Bc. Defects in viability and oogenesis were consistently more severe in rbp Met or br Met double mutants than would be expected if these genes act independently. Additionally, complementation between BR-C mutant alleles often failed when MET was absent. Patterns of BRC protein accumulation during metamorphosis revealed essentially no difference between wild-type and Met-null individuals. JH agonist treatment did not block accumulation of BRC proteins. We propose that MET and BRC interact to control transcription of one or more downstream effector genes, which can be disrupted either by mutations in Met or BR-C or by application of JH/JH agonist, which alters MET interaction with BRC.</description><identifier>ISSN: 0016-6731</identifier><identifier>ISSN: 1943-2631</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.105.046631</identifier><identifier>PMID: 16204218</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Soc America</publisher><subject>Alleles ; Animals ; Animals, Genetically Modified ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Cell Survival - drug effects ; Drosophila melanogaster ; Drosophila melanogaster - genetics ; Drosophila melanogaster - growth &amp; development ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Female ; Gene expression ; Gene Expression Regulation ; Genetic Complementation Test ; Insecticide Resistance ; Insects ; Investigations ; Male ; Metamorphosis, Biological - genetics ; Methoprene - pharmacology ; Mutation ; Oogenesis ; Ovary - drug effects ; Ovary - metabolism ; Proteins ; Signal Transduction ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic ; Zinc Fingers</subject><ispartof>Genetics (Austin), 2006-01, Vol.172 (1), p.253-264</ispartof><rights>Copyright Genetics Society of America Jan 2006</rights><rights>Copyright © 2006 by the Genetics Society of America 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c523t-ebb88aada1b35e84a2879bdcc3e54e37e9043bc29b0cd6e1135fa12dd6129e423</citedby><cites>FETCH-LOGICAL-c523t-ebb88aada1b35e84a2879bdcc3e54e37e9043bc29b0cd6e1135fa12dd6129e423</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27926,27927</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16204218$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wilson, Thomas G</creatorcontrib><creatorcontrib>Yerushalmi, Yoram</creatorcontrib><creatorcontrib>Donnell, David M</creatorcontrib><creatorcontrib>Restifo, Linda L</creatorcontrib><title>Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Juvenile hormone (JH) regulates insect development by a poorly understood mechanism. Application of JH agonist insecticides to Drosophila melanogaster during the ecdysone-driven onset of metamorphosis results in lethality and specific morphogenetic defects, some of which resemble those in mutants of the ecdysone-regulated Broad-Complex (BR-C). The Methoprene-tolerant (Met) bHLH-PAS gene mediates JH action, and Met mutations protect against the lethality and defects. To explore relationships among these two genes and JH, double mutants were constructed between Met alleles and alleles of each of the BR-C complementation groups: broad (br), reduced bristles on palpus (rbp), and 2Bc. Defects in viability and oogenesis were consistently more severe in rbp Met or br Met double mutants than would be expected if these genes act independently. Additionally, complementation between BR-C mutant alleles often failed when MET was absent. Patterns of BRC protein accumulation during metamorphosis revealed essentially no difference between wild-type and Met-null individuals. JH agonist treatment did not block accumulation of BRC proteins. We propose that MET and BRC interact to control transcription of one or more downstream effector genes, which can be disrupted either by mutations in Met or BR-C or by application of JH/JH agonist, which alters MET interaction with BRC.</description><subject>Alleles</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Cell Survival - drug effects</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - growth &amp; development</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Genetic Complementation Test</subject><subject>Insecticide Resistance</subject><subject>Insects</subject><subject>Investigations</subject><subject>Male</subject><subject>Metamorphosis, Biological - genetics</subject><subject>Methoprene - pharmacology</subject><subject>Mutation</subject><subject>Oogenesis</subject><subject>Ovary - drug effects</subject><subject>Ovary - metabolism</subject><subject>Proteins</subject><subject>Signal Transduction</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic</subject><subject>Zinc Fingers</subject><issn>0016-6731</issn><issn>1943-2631</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqFkttu1DAQhiMEokvhCZCQxQV3WTx2nMMNEl2grVQE4nBtOcls4sqxF9vbsM_Cy-LVLhQQUq_G8nzzezzzZ9lToEsQvHg5oMWou7AEKpa0KEsO97IFNAXPWTrfzxaUQpmXFYeT7FEI15TSshH1w-wESkYLBvUi-3FpI3rVRe0sOcM4I1py4fzkrDLksx5S0HYgH1UcZ7ULRFvyxrvgNqM2ikxolHWDCkmEqEA-4Q0qgz1pd-T80B_53wvvMY5u4xORR2dS2kaibE_OvFN9vnLTxuD3x9mDtTIBnxzjafb13dsvq4v86sP55er1Vd4JxmOObVvXSvUKWi6wLhSrq6btu46jKJBX2NCCtx1rWtr1JQJwsVbA-r4E1mDB-Gn26qC72bYT9h3a6JWRG68n5XfSKS3_zlg9ysHdSChECWIv8OIo4N23LYYoJx06NGk26LZBVrSCmvLmThAa0TDO4G6wggJqKBL4_B_w2m19WlqQLCG85s0e4geoS5sLHte__wZU7r0kf3kpXQh58FKqevbnWG5rjua5bXLUwzhrjzJMypiEg5znGSomQTLB-U8fbtjp</recordid><startdate>20060101</startdate><enddate>20060101</enddate><creator>Wilson, Thomas G</creator><creator>Yerushalmi, Yoram</creator><creator>Donnell, David M</creator><creator>Restifo, Linda L</creator><general>Genetics Soc America</general><general>Genetics Society of America</general><general>Copyright © 2006 by the Genetics Society of America</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060101</creationdate><title>Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex</title><author>Wilson, Thomas G ; 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Application of JH agonist insecticides to Drosophila melanogaster during the ecdysone-driven onset of metamorphosis results in lethality and specific morphogenetic defects, some of which resemble those in mutants of the ecdysone-regulated Broad-Complex (BR-C). The Methoprene-tolerant (Met) bHLH-PAS gene mediates JH action, and Met mutations protect against the lethality and defects. To explore relationships among these two genes and JH, double mutants were constructed between Met alleles and alleles of each of the BR-C complementation groups: broad (br), reduced bristles on palpus (rbp), and 2Bc. Defects in viability and oogenesis were consistently more severe in rbp Met or br Met double mutants than would be expected if these genes act independently. Additionally, complementation between BR-C mutant alleles often failed when MET was absent. Patterns of BRC protein accumulation during metamorphosis revealed essentially no difference between wild-type and Met-null individuals. JH agonist treatment did not block accumulation of BRC proteins. We propose that MET and BRC interact to control transcription of one or more downstream effector genes, which can be disrupted either by mutations in Met or BR-C or by application of JH/JH agonist, which alters MET interaction with BRC.</abstract><cop>United States</cop><pub>Genetics Soc America</pub><pmid>16204218</pmid><doi>10.1534/genetics.105.046631</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
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subjects Alleles
Animals
Animals, Genetically Modified
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - metabolism
Cell Survival - drug effects
Drosophila melanogaster
Drosophila melanogaster - genetics
Drosophila melanogaster - growth & development
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Female
Gene expression
Gene Expression Regulation
Genetic Complementation Test
Insecticide Resistance
Insects
Investigations
Male
Metamorphosis, Biological - genetics
Methoprene - pharmacology
Mutation
Oogenesis
Ovary - drug effects
Ovary - metabolism
Proteins
Signal Transduction
Transcription Factors - genetics
Transcription Factors - metabolism
Transcription, Genetic
Zinc Fingers
title Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex
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