The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species

The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world,...

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Veröffentlicht in:Genome Biology 2016-09, Vol.17 (1), p.192-192, Article 192
Hauptverfasser: Papanicolaou, Alexie, Schetelig, Marc F, Arensburger, Peter, Atkinson, Peter W, Benoit, Joshua B, Bourtzis, Kostas, Castañera, Pedro, Cavanaugh, John P, Chao, Hsu, Childers, Christopher, Curril, Ingrid, Dinh, Huyen, Doddapaneni, HarshaVardhan, Dolan, Amanda, Dugan, Shannon, Friedrich, Markus, Gasperi, Giuliano, Geib, Scott, Georgakilas, Georgios, Gibbs, Richard A, Giers, Sarah D, Gomulski, Ludvik M, González-Guzmán, Miguel, Guillem-Amat, Ana, Han, Yi, Hatzigeorgiou, Artemis G, Hernández-Crespo, Pedro, Hughes, Daniel S T, Jones, Jeffery W, Karagkouni, Dimitra, Koskinioti, Panagiota, Lee, Sandra L, Malacrida, Anna R, Manni, Mosè, Mathiopoulos, Kostas, Meccariello, Angela, Munoz-Torres, Monica, Murali, Shwetha C, Murphy, Terence D, Muzny, Donna M, Oberhofer, Georg, Ortego, Félix, Paraskevopoulou, Maria D, Poelchau, Monica, Qu, Jiaxin, Reczko, Martin, Robertson, Hugh M, Rosendale, Andrew J, Rosselot, Andrew E, Saccone, Giuseppe, Salvemini, Marco, Savini, Grazia, Schreiner, Patrick, Scolari, Francesca, Siciliano, Paolo, Sim, Sheina B, Tsiamis, George, Ureña, Enric, Vlachos, Ioannis S, Werren, John H, Wimmer, Ernst A, Worley, Kim C, Zacharopoulou, Antigone, Richards, Stephen, Handler, Alfred M
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creator Papanicolaou, Alexie
Schetelig, Marc F
Arensburger, Peter
Atkinson, Peter W
Benoit, Joshua B
Bourtzis, Kostas
Castañera, Pedro
Cavanaugh, John P
Chao, Hsu
Childers, Christopher
Curril, Ingrid
Dinh, Huyen
Doddapaneni, HarshaVardhan
Dolan, Amanda
Dugan, Shannon
Friedrich, Markus
Gasperi, Giuliano
Geib, Scott
Georgakilas, Georgios
Gibbs, Richard A
Giers, Sarah D
Gomulski, Ludvik M
González-Guzmán, Miguel
Guillem-Amat, Ana
Han, Yi
Hatzigeorgiou, Artemis G
Hernández-Crespo, Pedro
Hughes, Daniel S T
Jones, Jeffery W
Karagkouni, Dimitra
Koskinioti, Panagiota
Lee, Sandra L
Malacrida, Anna R
Manni, Mosè
Mathiopoulos, Kostas
Meccariello, Angela
Munoz-Torres, Monica
Murali, Shwetha C
Murphy, Terence D
Muzny, Donna M
Oberhofer, Georg
Ortego, Félix
Paraskevopoulou, Maria D
Poelchau, Monica
Qu, Jiaxin
Reczko, Martin
Robertson, Hugh M
Rosendale, Andrew J
Rosselot, Andrew E
Saccone, Giuseppe
Salvemini, Marco
Savini, Grazia
Schreiner, Patrick
Scolari, Francesca
Siciliano, Paolo
Sim, Sheina B
Tsiamis, George
Ureña, Enric
Vlachos, Ioannis S
Werren, John H
Wimmer, Ernst A
Worley, Kim C
Zacharopoulou, Antigone
Richards, Stephen
Handler, Alfred M
description The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control. The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT. The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.
doi_str_mv 10.1186/s13059-016-1049-2
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It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control. The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT. The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.</description><identifier>ISSN: 1474-760X</identifier><identifier>ISSN: 1474-7596</identifier><identifier>EISSN: 1474-760X</identifier><identifier>DOI: 10.1186/s13059-016-1049-2</identifier><identifier>PMID: 27659211</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Adaptation (Biology) ; Animals ; Animals, Genetically Modified - genetics ; Aquaporins ; Biological Evolution ; Ceratitis capitata ; Ceratitis capitata - genetics ; Chemoreception ; Drosophila ; Evolution &amp; development ; evolutionary adaptation ; fruits ; Gene families ; genes ; Genetic analysis ; Genetic aspects ; Genome, Insect ; Genomes ; High-Throughput Nucleotide Sequencing - methods ; Host range ; human health ; Humans ; imagos ; Inbreeding ; insect pests ; insecticides ; integrated pest management ; Introduced Species ; Invasiveness ; Mediterranean fruit-fly ; metabolism ; Methods ; Molecular Sequence Annotation ; Niches ; Nucleotide sequence ; opsin ; Opsins ; Pest control ; Pest Control, Biological ; Pests ; Physiological aspects ; sterile insect technique ; Sterilized organisms ; Structure-function relationships ; subtropics ; vegetables</subject><ispartof>Genome Biology, 2016-09, Vol.17 (1), p.192-192, Article 192</ispartof><rights>COPYRIGHT 2016 BioMed Central Ltd.</rights><rights>2016. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control. The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT. The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.</description><subject>Adaptation (Biology)</subject><subject>Animals</subject><subject>Animals, Genetically Modified - genetics</subject><subject>Aquaporins</subject><subject>Biological Evolution</subject><subject>Ceratitis capitata</subject><subject>Ceratitis capitata - genetics</subject><subject>Chemoreception</subject><subject>Drosophila</subject><subject>Evolution &amp; development</subject><subject>evolutionary adaptation</subject><subject>fruits</subject><subject>Gene families</subject><subject>genes</subject><subject>Genetic analysis</subject><subject>Genetic aspects</subject><subject>Genome, Insect</subject><subject>Genomes</subject><subject>High-Throughput Nucleotide Sequencing - methods</subject><subject>Host range</subject><subject>human health</subject><subject>Humans</subject><subject>imagos</subject><subject>Inbreeding</subject><subject>insect pests</subject><subject>insecticides</subject><subject>integrated pest management</subject><subject>Introduced Species</subject><subject>Invasiveness</subject><subject>Mediterranean fruit-fly</subject><subject>metabolism</subject><subject>Methods</subject><subject>Molecular Sequence Annotation</subject><subject>Niches</subject><subject>Nucleotide sequence</subject><subject>opsin</subject><subject>Opsins</subject><subject>Pest control</subject><subject>Pest Control, Biological</subject><subject>Pests</subject><subject>Physiological aspects</subject><subject>sterile insect technique</subject><subject>Sterilized organisms</subject><subject>Structure-function 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capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species</title><author>Papanicolaou, Alexie ; Schetelig, Marc F ; Arensburger, Peter ; Atkinson, Peter W ; Benoit, Joshua B ; Bourtzis, Kostas ; Castañera, Pedro ; Cavanaugh, John P ; Chao, Hsu ; Childers, Christopher ; Curril, Ingrid ; Dinh, Huyen ; Doddapaneni, HarshaVardhan ; Dolan, Amanda ; Dugan, Shannon ; Friedrich, Markus ; Gasperi, Giuliano ; Geib, Scott ; Georgakilas, Georgios ; Gibbs, Richard A ; Giers, Sarah D ; Gomulski, Ludvik M ; González-Guzmán, Miguel ; Guillem-Amat, Ana ; Han, Yi ; Hatzigeorgiou, Artemis G ; Hernández-Crespo, Pedro ; Hughes, Daniel S T ; Jones, Jeffery W ; Karagkouni, Dimitra ; Koskinioti, Panagiota ; Lee, Sandra L ; Malacrida, Anna R ; Manni, Mosè ; Mathiopoulos, Kostas ; Meccariello, Angela ; Munoz-Torres, Monica ; Murali, Shwetha C ; Murphy, Terence D ; Muzny, Donna M ; Oberhofer, Georg ; Ortego, Félix ; Paraskevopoulou, Maria D ; Poelchau, Monica ; Qu, Jiaxin ; Reczko, Martin ; Robertson, Hugh M ; Rosendale, Andrew J ; Rosselot, Andrew E ; Saccone, Giuseppe ; Salvemini, Marco ; Savini, Grazia ; Schreiner, Patrick ; Scolari, Francesca ; Siciliano, Paolo ; Sim, Sheina B ; Tsiamis, George ; Ureña, Enric ; Vlachos, Ioannis S ; Werren, John H ; Wimmer, Ernst A ; Worley, Kim C ; Zacharopoulou, Antigone ; Richards, Stephen ; Handler, Alfred M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c595t-e0ff8b989aa94af2932b7c4fe2c1c5f72a059eed366739517e0796bb4ec8a86f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adaptation (Biology)</topic><topic>Animals</topic><topic>Animals, Genetically Modified - genetics</topic><topic>Aquaporins</topic><topic>Biological Evolution</topic><topic>Ceratitis capitata</topic><topic>Ceratitis capitata - genetics</topic><topic>Chemoreception</topic><topic>Drosophila</topic><topic>Evolution &amp; development</topic><topic>evolutionary adaptation</topic><topic>fruits</topic><topic>Gene families</topic><topic>genes</topic><topic>Genetic analysis</topic><topic>Genetic aspects</topic><topic>Genome, Insect</topic><topic>Genomes</topic><topic>High-Throughput Nucleotide Sequencing - methods</topic><topic>Host range</topic><topic>human health</topic><topic>Humans</topic><topic>imagos</topic><topic>Inbreeding</topic><topic>insect pests</topic><topic>insecticides</topic><topic>integrated pest management</topic><topic>Introduced Species</topic><topic>Invasiveness</topic><topic>Mediterranean fruit-fly</topic><topic>metabolism</topic><topic>Methods</topic><topic>Molecular Sequence Annotation</topic><topic>Niches</topic><topic>Nucleotide sequence</topic><topic>opsin</topic><topic>Opsins</topic><topic>Pest control</topic><topic>Pest Control, Biological</topic><topic>Pests</topic><topic>Physiological aspects</topic><topic>sterile insect technique</topic><topic>Sterilized organisms</topic><topic>Structure-function relationships</topic><topic>subtropics</topic><topic>vegetables</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Papanicolaou, Alexie</creatorcontrib><creatorcontrib>Schetelig, Marc F</creatorcontrib><creatorcontrib>Arensburger, Peter</creatorcontrib><creatorcontrib>Atkinson, Peter W</creatorcontrib><creatorcontrib>Benoit, Joshua B</creatorcontrib><creatorcontrib>Bourtzis, Kostas</creatorcontrib><creatorcontrib>Castañera, Pedro</creatorcontrib><creatorcontrib>Cavanaugh, John P</creatorcontrib><creatorcontrib>Chao, Hsu</creatorcontrib><creatorcontrib>Childers, Christopher</creatorcontrib><creatorcontrib>Curril, Ingrid</creatorcontrib><creatorcontrib>Dinh, Huyen</creatorcontrib><creatorcontrib>Doddapaneni, HarshaVardhan</creatorcontrib><creatorcontrib>Dolan, Amanda</creatorcontrib><creatorcontrib>Dugan, Shannon</creatorcontrib><creatorcontrib>Friedrich, Markus</creatorcontrib><creatorcontrib>Gasperi, Giuliano</creatorcontrib><creatorcontrib>Geib, Scott</creatorcontrib><creatorcontrib>Georgakilas, Georgios</creatorcontrib><creatorcontrib>Gibbs, Richard A</creatorcontrib><creatorcontrib>Giers, Sarah D</creatorcontrib><creatorcontrib>Gomulski, Ludvik M</creatorcontrib><creatorcontrib>González-Guzmán, Miguel</creatorcontrib><creatorcontrib>Guillem-Amat, Ana</creatorcontrib><creatorcontrib>Han, Yi</creatorcontrib><creatorcontrib>Hatzigeorgiou, Artemis G</creatorcontrib><creatorcontrib>Hernández-Crespo, Pedro</creatorcontrib><creatorcontrib>Hughes, Daniel S T</creatorcontrib><creatorcontrib>Jones, Jeffery W</creatorcontrib><creatorcontrib>Karagkouni, Dimitra</creatorcontrib><creatorcontrib>Koskinioti, Panagiota</creatorcontrib><creatorcontrib>Lee, Sandra L</creatorcontrib><creatorcontrib>Malacrida, Anna R</creatorcontrib><creatorcontrib>Manni, 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Papanicolaou, Alexie</au><au>Schetelig, Marc F</au><au>Arensburger, Peter</au><au>Atkinson, Peter W</au><au>Benoit, Joshua B</au><au>Bourtzis, Kostas</au><au>Castañera, Pedro</au><au>Cavanaugh, John P</au><au>Chao, Hsu</au><au>Childers, Christopher</au><au>Curril, Ingrid</au><au>Dinh, Huyen</au><au>Doddapaneni, HarshaVardhan</au><au>Dolan, Amanda</au><au>Dugan, Shannon</au><au>Friedrich, Markus</au><au>Gasperi, Giuliano</au><au>Geib, Scott</au><au>Georgakilas, Georgios</au><au>Gibbs, Richard A</au><au>Giers, Sarah D</au><au>Gomulski, Ludvik M</au><au>González-Guzmán, Miguel</au><au>Guillem-Amat, Ana</au><au>Han, Yi</au><au>Hatzigeorgiou, Artemis G</au><au>Hernández-Crespo, Pedro</au><au>Hughes, Daniel S T</au><au>Jones, Jeffery W</au><au>Karagkouni, Dimitra</au><au>Koskinioti, Panagiota</au><au>Lee, Sandra L</au><au>Malacrida, Anna R</au><au>Manni, Mosè</au><au>Mathiopoulos, Kostas</au><au>Meccariello, Angela</au><au>Munoz-Torres, Monica</au><au>Murali, Shwetha C</au><au>Murphy, Terence D</au><au>Muzny, Donna M</au><au>Oberhofer, Georg</au><au>Ortego, Félix</au><au>Paraskevopoulou, Maria D</au><au>Poelchau, Monica</au><au>Qu, Jiaxin</au><au>Reczko, Martin</au><au>Robertson, Hugh M</au><au>Rosendale, Andrew J</au><au>Rosselot, Andrew E</au><au>Saccone, Giuseppe</au><au>Salvemini, Marco</au><au>Savini, Grazia</au><au>Schreiner, Patrick</au><au>Scolari, Francesca</au><au>Siciliano, Paolo</au><au>Sim, Sheina B</au><au>Tsiamis, George</au><au>Ureña, Enric</au><au>Vlachos, Ioannis S</au><au>Werren, John H</au><au>Wimmer, Ernst A</au><au>Worley, Kim C</au><au>Zacharopoulou, Antigone</au><au>Richards, Stephen</au><au>Handler, Alfred M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species</atitle><jtitle>Genome Biology</jtitle><addtitle>Genome Biol</addtitle><date>2016-09-22</date><risdate>2016</risdate><volume>17</volume><issue>1</issue><spage>192</spage><epage>192</epage><pages>192-192</pages><artnum>192</artnum><issn>1474-760X</issn><issn>1474-7596</issn><eissn>1474-760X</eissn><abstract>The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control. The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A high-quality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT. The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>27659211</pmid><doi>10.1186/s13059-016-1049-2</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
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subjects Adaptation (Biology)
Animals
Animals, Genetically Modified - genetics
Aquaporins
Biological Evolution
Ceratitis capitata
Ceratitis capitata - genetics
Chemoreception
Drosophila
Evolution & development
evolutionary adaptation
fruits
Gene families
genes
Genetic analysis
Genetic aspects
Genome, Insect
Genomes
High-Throughput Nucleotide Sequencing - methods
Host range
human health
Humans
imagos
Inbreeding
insect pests
insecticides
integrated pest management
Introduced Species
Invasiveness
Mediterranean fruit-fly
metabolism
Methods
Molecular Sequence Annotation
Niches
Nucleotide sequence
opsin
Opsins
Pest control
Pest Control, Biological
Pests
Physiological aspects
sterile insect technique
Sterilized organisms
Structure-function relationships
subtropics
vegetables
title The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species
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