Finding the missing honey bee genes: Lessons learned from a genome upgrade

Handle URI:
http://hdl.handle.net/10754/325245
Title:
Finding the missing honey bee genes: Lessons learned from a genome upgrade
Authors:
Elsik, Christine G; Worley, Kim C; Bennett, Anna K; Beye, Martin; Camara, Francisco; Childers, Christopher P; de Graaf, Dirk C; Debyser, Griet; Deng, Jixin; Devreese, Bart; Elhaik, Eran; Evans, Jay D; Foster, Leonard J; Graur, Dan; Guigo, Roderic; Hoff, Katharina Jasmin; Holder, Michael E; Hudson, Matthew E; Hunt, Greg J; Jiang, Huaiyang; Joshi, Vandita; Khetani, Radhika S; Kosarev, Peter; Kovar, Christie L; Ma, Jian; Maleszka, Ryszard; Moritz, Robin F A; Munoz-Torres, Monica C; Murphy, Terence D; Muzny, Donna M; Newsham, Irene F; Reese, Justin T; Robertson, Hugh M; Robinson, Gene E; Rueppell, Olav; Solovyev, Victor ( 0000-0001-8885-493X ) ; Stanke, Mario; Stolle, Eckart; Tsuruda, Jennifer M; Vaerenbergh, Matthias Van; Waterhouse, Robert M; Weaver, Daniel B; Whitfield, Charles W; Wu, Yuanqing; Zdobnov, Evgeny M; Zhang, Lan; Zhu, Dianhui; Gibbs, Richard A; Patil, S.; Gubbala, S.; Aqrawi, P.; Arias, F.; Bess, C.; Blankenburg, K. B.; Brocchini, M.; Buhay, C.; Challis, D.; Chang, K.; Chen, D.; Coleman, P.; Drummond, J.; English, A.; Evani, U.; Francisco, L.; Fu, Q.; Goodspeed, R.; Haessly, T. H.; Hale, W.; Han, H.; Hu, Y.; Jackson, L.; Jakkamsetti, A.; Jayaseelan, J. C.; Kakkar, N.; Kalra, D.; Kandadi, H.; Lee, S.; Li, H.; Liu, Y.; Macmil, S.; Mandapat, C. M.; Mata, R.; Mathew, T.; Matskevitch, T.; Munidasa, M.; Nagaswamy, U.; Najjar, R.; Nguyen, N.; Niu, J.; Opheim, D.; Palculict, T.; Paul, S.; Pellon, M.; Perales, L.; Pham, C.; Pham, P.
Abstract:
Background: The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes. Results: Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data. Conclusions: Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination. 2014 Elsik et al.; licensee BioMed Central Ltd.
KAUST Department:
Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division
Citation:
Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, et al. (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 15: 86. doi:10.1186/1471-2164-15-86.
Publisher:
Springer Nature
Journal:
BMC Genomics
Issue Date:
30-Jan-2014
DOI:
10.1186/1471-2164-15-86
PubMed ID:
24479613
PubMed Central ID:
PMC4028053
Type:
Article
ISSN:
14712164
Appears in Collections:
Articles; Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorElsik, Christine Gen
dc.contributor.authorWorley, Kim Cen
dc.contributor.authorBennett, Anna Ken
dc.contributor.authorBeye, Martinen
dc.contributor.authorCamara, Franciscoen
dc.contributor.authorChilders, Christopher Pen
dc.contributor.authorde Graaf, Dirk Cen
dc.contributor.authorDebyser, Grieten
dc.contributor.authorDeng, Jixinen
dc.contributor.authorDevreese, Barten
dc.contributor.authorElhaik, Eranen
dc.contributor.authorEvans, Jay Den
dc.contributor.authorFoster, Leonard Jen
dc.contributor.authorGraur, Danen
dc.contributor.authorGuigo, Rodericen
dc.contributor.authorHoff, Katharina Jasminen
dc.contributor.authorHolder, Michael Een
dc.contributor.authorHudson, Matthew Een
dc.contributor.authorHunt, Greg Jen
dc.contributor.authorJiang, Huaiyangen
dc.contributor.authorJoshi, Vanditaen
dc.contributor.authorKhetani, Radhika Sen
dc.contributor.authorKosarev, Peteren
dc.contributor.authorKovar, Christie Len
dc.contributor.authorMa, Jianen
dc.contributor.authorMaleszka, Ryszarden
dc.contributor.authorMoritz, Robin F Aen
dc.contributor.authorMunoz-Torres, Monica Cen
dc.contributor.authorMurphy, Terence Den
dc.contributor.authorMuzny, Donna Men
dc.contributor.authorNewsham, Irene Fen
dc.contributor.authorReese, Justin Ten
dc.contributor.authorRobertson, Hugh Men
dc.contributor.authorRobinson, Gene Een
dc.contributor.authorRueppell, Olaven
dc.contributor.authorSolovyev, Victoren
dc.contributor.authorStanke, Marioen
dc.contributor.authorStolle, Eckarten
dc.contributor.authorTsuruda, Jennifer Men
dc.contributor.authorVaerenbergh, Matthias Vanen
dc.contributor.authorWaterhouse, Robert Men
dc.contributor.authorWeaver, Daniel Ben
dc.contributor.authorWhitfield, Charles Wen
dc.contributor.authorWu, Yuanqingen
dc.contributor.authorZdobnov, Evgeny Men
dc.contributor.authorZhang, Lanen
dc.contributor.authorZhu, Dianhuien
dc.contributor.authorGibbs, Richard Aen
dc.contributor.authorPatil, S.en
dc.contributor.authorGubbala, S.en
dc.contributor.authorAqrawi, P.en
dc.contributor.authorArias, F.en
dc.contributor.authorBess, C.en
dc.contributor.authorBlankenburg, K. B.en
dc.contributor.authorBrocchini, M.en
dc.contributor.authorBuhay, C.en
dc.contributor.authorChallis, D.en
dc.contributor.authorChang, K.en
dc.contributor.authorChen, D.en
dc.contributor.authorColeman, P.en
dc.contributor.authorDrummond, J.en
dc.contributor.authorEnglish, A.en
dc.contributor.authorEvani, U.en
dc.contributor.authorFrancisco, L.en
dc.contributor.authorFu, Q.en
dc.contributor.authorGoodspeed, R.en
dc.contributor.authorHaessly, T. H.en
dc.contributor.authorHale, W.en
dc.contributor.authorHan, H.en
dc.contributor.authorHu, Y.en
dc.contributor.authorJackson, L.en
dc.contributor.authorJakkamsetti, A.en
dc.contributor.authorJayaseelan, J. C.en
dc.contributor.authorKakkar, N.en
dc.contributor.authorKalra, D.en
dc.contributor.authorKandadi, H.en
dc.contributor.authorLee, S.en
dc.contributor.authorLi, H.en
dc.contributor.authorLiu, Y.en
dc.contributor.authorMacmil, S.en
dc.contributor.authorMandapat, C. M.en
dc.contributor.authorMata, R.en
dc.contributor.authorMathew, T.en
dc.contributor.authorMatskevitch, T.en
dc.contributor.authorMunidasa, M.en
dc.contributor.authorNagaswamy, U.en
dc.contributor.authorNajjar, R.en
dc.contributor.authorNguyen, N.en
dc.contributor.authorNiu, J.en
dc.contributor.authorOpheim, D.en
dc.contributor.authorPalculict, T.en
dc.contributor.authorPaul, S.en
dc.contributor.authorPellon, M.en
dc.contributor.authorPerales, L.en
dc.contributor.authorPham, C.en
dc.contributor.authorPham, P.en
dc.date.accessioned2014-08-27T09:42:08Z-
dc.date.available2014-08-27T09:42:08Z-
dc.date.issued2014-01-30en
dc.identifier.citationElsik CG, Worley KC, Bennett AK, Beye M, Camara F, et al. (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 15: 86. doi:10.1186/1471-2164-15-86.en
dc.identifier.issn14712164en
dc.identifier.pmid24479613en
dc.identifier.doi10.1186/1471-2164-15-86en
dc.identifier.urihttp://hdl.handle.net/10754/325245en
dc.description.abstractBackground: The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes. Results: Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data. Conclusions: Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination. 2014 Elsik et al.; licensee BioMed Central Ltd.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.rightsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.en
dc.rights.urihttp://creativecommons.org/licenses/by/2.0en
dc.subjectApis melliferaen
dc.subjectGC contenten
dc.subjectGene annotationen
dc.subjectGene predictionen
dc.subjectGenome assemblyen
dc.subjectGenome improvementen
dc.subjectGenome sequencingen
dc.subjectRepetitive DNAen
dc.subjectTranscriptomeen
dc.subjectcomplementary DNAen
dc.subjectcytosineen
dc.subjectguanineen
dc.subjectRNAen
dc.subjectanimal cellen
dc.subjectanimal tissueen
dc.subjectDNA contenten
dc.subjectembryoen
dc.subjectgenetic codeen
dc.subjectgenetic resourceen
dc.subjecthoneybeeen
dc.subjectinsect geneticsen
dc.subjectinsect genomeen
dc.subjectnucleotide sequenceen
dc.subjectRNA sequenceen
dc.subjectsequence alignmenten
dc.subjectsequence analysisen
dc.subjectunindexed sequenceen
dc.subjectHexapodaen
dc.subjectMetazoaen
dc.titleFinding the missing honey bee genes: Lessons learned from a genome upgradeen
dc.typeArticleen
dc.contributor.departmentComputer, Electrical and Mathematical Sciences and Engineering (CEMSE) Divisionen
dc.identifier.journalBMC Genomicsen
dc.identifier.pmcidPMC4028053en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDivision of Animal Sciences, Division of Plant Sciences and MU Informatics Institute, University of Missouri, Columbia, MO 65211, United Statesen
dc.contributor.institutionDepartment of Biology, Georgetown University, Washington, DC 20057, United Statesen
dc.contributor.institutionHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX 77030, United Statesen
dc.contributor.institutionInstitute of Evolutionary Genetics, Heinrich Heine University Duesseldorf, Universitaetsstrasse 1, 40225 Duesseldorf, Germanyen
dc.contributor.institutionCenter for Genomic Regulation, Universitat Pompeu Fabra, C/Dr. Aiguader 88, E-08003 Barcelona, Catalonia, Spainen
dc.contributor.institutionDivision of Animal Sciences, University of Missouri, Columbia, MO 65211, United Statesen
dc.contributor.institutionLaboratory of Zoophysiology, Ghent University, Krijgslaan 281 S2, B-9000 Ghent, Belgiumen
dc.contributor.institutionLaboratory of Protein Biochemistry and Biomolecular Engineering, Ghent University, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgiumen
dc.contributor.institutionDepartment of Mental Health, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205-2103, United Statesen
dc.contributor.institutionBee Research Laboratory, BARC-E, USDA-Agricultural Research Service, Beltsville, MD 20705, United Statesen
dc.contributor.institutionDepartment of Biochemistry and Molecular Biology, Centre for High-Throughput Biology, University of British Columbia, 2125 East Mall, Vancouver, BC, Canadaen
dc.contributor.institutionDepartment of Biology and Biochemistry, University of Houston, Houston, TX 77204-5001, United Statesen
dc.contributor.institutionErnst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, Walther-Rathenau-Str. 47, 17487 Greifswald, Germanyen
dc.contributor.institutionDepartment of Crop Sciences and Institute of Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionDepartment of Entomology, Purdue University, 901 West State Street, West Lafayette, IN 47907-2089, United Statesen
dc.contributor.institutionDepartment of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh, MAGEE 0000, Pittsburgh, PA 15260, United Statesen
dc.contributor.institutionHigh-Performance Biological Computing (HPCBio), Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionSoftberry Inc., 116 Radio Circle, Suite 400, Mount Kisco, NY 10549, United Statesen
dc.contributor.institutionInstitute for Genomic Biology and Department of Bioengineering, University of Illinois at Urbana-Champaign, 1270 DCL, MC-278, 1304 W Springfield Ave, Urbana, IL 61801, United Statesen
dc.contributor.institutionResearch School of Biology, The Australian National University, Canberra ACT 0200, Australiaen
dc.contributor.institutionInstitut fr Zoologie, Molekulare kologie, Martin-Luther-Universitt Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germanyen
dc.contributor.institutionGenomics Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, United Statesen
dc.contributor.institutionNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Building 45, 8600 Rockville Pike, Bethesda, MD 20894, United Statesen
dc.contributor.institutionDepartment of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.institutionInstitute for Genomic Biology, Department of Entomology, Neuroscience Program, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, United Statesen
dc.contributor.institutionDepartment of Biology, University of North Carolina at Greensboro, 321 McIver Street, Greensboro, NC 27412, United Statesen
dc.contributor.institutionExtension Field Operations, Clemson University, 120 McGinty Ct, Clemson, SC 29634, United Statesen
dc.contributor.institutionUniversity of Geneva and Swiss Institute of Bioinformatics, CMU, Michel-Servet 1, Geneva CH-1211, Switzerlanden
dc.contributor.institutionGenformatic, 6301 Highland Hills Drive, Austin, TX 78731, United Statesen
dc.contributor.institutionDepartment of Entomology, Neuroscience Program, Program in Ecology and Evolutionary Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorSolovyev, Victoren

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