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

Christine G Elsik; Kim C Worley; Anna K Bennett; Martin Beye; Francisco Camara; Christopher P Childers; Dirk C de Graaf; Griet Debyser; Jixin Deng; Bart Devreese; Eran Elhaik; Jay D Evans; Leonard J Foster; Dan Graur; Roderic Guigo; Katharina Jasmin Hoff; Michael E Holder; Matthew E Hudson; Greg J Hunt; Huaiyang Jiang; Vandita Joshi; Radhika S Khetani; Peter Kosarev; Christie L Kovar; Jian Ma; Ryszard Maleszka; Robin F A Moritz; Monica C Munoz-Torres; Terence D Murphy; Donna M Muzny; Irene F Newsham; Justin T Reese; Hugh M Robertson; Gene E Robinson; Olav Rueppell; Victor Solovyev; Mario Stanke; Eckart Stolle; Jennifer M Tsuruda; Matthias Van Vaerenbergh; Robert M Waterhouse; Daniel B Weaver; Charles W Whitfield; Yuanqing Wu; Evgeny M Zdobnov; Lan Zhang; Dianhui Zhu; Richard A Gibbs; S. Patil; S. Gubbala; P. Aqrawi; F. Arias; C. Bess; K. B. Blankenburg; M. Brocchini; C. Buhay; D. Challis; K. Chang; D. Chen; P. Coleman; J. Drummond; A. English; U. Evani; L. Francisco; Q. Fu; R. Goodspeed; T. H. Haessly; W. Hale; H. Han; Y. Hu; L. Jackson; A. Jakkamsetti; J. C. Jayaseelan; N. Kakkar; D. Kalra; H. Kandadi; S. Lee; H. Li; Y. Liu; S. Macmil; C. M. Mandapat; R. Mata; T. Mathew; T. Matskevitch; M. Munidasa; U. Nagaswamy; R. Najjar; N. Nguyen; J. Niu; D. Opheim; T. Palculict; S. Paul; M. Pellon; L. Perales; C. Pham; P. Pham

doi:10.1186/1471-2164-15-86

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

Christine G Elsik, Kim C Worley, Anna K Bennett, Martin Beye, Francisco Camara, Christopher P Childers, Dirk C de Graaf, Griet Debyser, Jixin Deng, Bart Devreese, Eran Elhaik, Jay D Evans, Leonard J Foster, Dan Graur, Roderic Guigo, Katharina Jasmin Hoff, Michael E Holder, Matthew E Hudson, Greg J Hunt, Huaiyang JiangVandita Joshi, Radhika S Khetani, Peter Kosarev, Christie L Kovar, Jian Ma, Ryszard Maleszka, Robin F A Moritz, Monica C Munoz-Torres, Terence D Murphy, Donna M Muzny, Irene F Newsham, Justin T Reese, Hugh M Robertson, Gene E Robinson, Olav Rueppell, Victor Solovyev, Mario Stanke, Eckart Stolle, Jennifer M Tsuruda, Matthias Van Vaerenbergh, Robert M Waterhouse, Daniel B Weaver, Charles W Whitfield, Yuanqing Wu, Evgeny M Zdobnov, Lan Zhang, Dianhui Zhu, Richard A Gibbs, S. Patil, S. Gubbala, P. Aqrawi, F. Arias, C. Bess, K. B. Blankenburg, M. Brocchini, C. Buhay, D. Challis, K. Chang, D. Chen, P. Coleman, J. Drummond, A. English, U. Evani, L. Francisco, Q. Fu, R. Goodspeed, T. H. Haessly, W. Hale, H. Han, Y. Hu, L. Jackson, A. Jakkamsetti, J. C. Jayaseelan, N. Kakkar, D. Kalra, H. Kandadi, S. Lee, H. Li, Y. Liu, S. Macmil, C. M. Mandapat, R. Mata, T. Mathew, T. Matskevitch, M. Munidasa, U. Nagaswamy, R. Najjar, N. Nguyen, J. Niu, D. Opheim, T. Palculict, S. Paul, M. Pellon, L. Perales, C. Pham, P. Pham

Research output: Contribution to journal › Article › peer-review

325 Scopus citations

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.

Original language	English (US)
Pages (from-to)	86
Journal	BMC Genomics
Volume	15
Issue number	1
DOIs	https://doi.org/10.1186/1471-2164-15-86
State	Published - Jan 30 2014

ASJC Scopus subject areas

Genetics
Biotechnology

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10.1186/1471-2164-15-86

https://repository.kaust.edu.sa/bitstream/10754/325245/1/Article-BMC_Genomi-Finding_th-2014.pdf

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Elsik, C. G., Worley, K. C., Bennett, A. K., Beye, M., Camara, F., Childers, C. P., de Graaf, D. C., Debyser, G., Deng, J., Devreese, B., Elhaik, E., Evans, J. D., Foster, L. J., Graur, D., Guigo, R., Hoff, K. J., Holder, M. E., Hudson, M. E., Hunt, G. J., ... Pham, P. (2014). Finding the missing honey bee genes: Lessons learned from a genome upgrade. BMC Genomics, 15(1), 86. https://doi.org/10.1186/1471-2164-15-86

@article{494d53b6b0dd4263a4db7558df7ecb74,

title = "Finding the missing honey bee genes: Lessons learned from a genome upgrade",

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.",

author = "Elsik, {Christine G} and Worley, {Kim C} and Bennett, {Anna K} and Martin Beye and Francisco Camara and Childers, {Christopher P} and {de Graaf}, {Dirk C} and Griet Debyser and Jixin Deng and Bart Devreese and Eran Elhaik and Evans, {Jay D} and Foster, {Leonard J} and Dan Graur and Roderic Guigo and Hoff, {Katharina Jasmin} and Holder, {Michael E} and Hudson, {Matthew E} and Hunt, {Greg J} and Huaiyang Jiang and Vandita Joshi and Khetani, {Radhika S} and Peter Kosarev and Kovar, {Christie L} and Jian Ma and Ryszard Maleszka and Moritz, {Robin F A} and Munoz-Torres, {Monica C} and Murphy, {Terence D} and Muzny, {Donna M} and Newsham, {Irene F} and Reese, {Justin T} and Robertson, {Hugh M} and Robinson, {Gene E} and Olav Rueppell and Victor Solovyev and Mario Stanke and Eckart Stolle and Tsuruda, {Jennifer M} and Vaerenbergh, {Matthias Van} and Waterhouse, {Robert M} and Weaver, {Daniel B} and Whitfield, {Charles W} and Yuanqing Wu and Zdobnov, {Evgeny M} and Lan Zhang and Dianhui Zhu and Gibbs, {Richard A} and S. Patil and S. Gubbala and P. Aqrawi and F. Arias and C. Bess and Blankenburg, {K. B.} and M. Brocchini and C. Buhay and D. Challis and K. Chang and D. Chen and P. Coleman and J. Drummond and A. English and U. Evani and L. Francisco and Q. Fu and R. Goodspeed and Haessly, {T. H.} and W. Hale and H. Han and Y. Hu and L. Jackson and A. Jakkamsetti and Jayaseelan, {J. C.} and N. Kakkar and D. Kalra and H. Kandadi and S. Lee and H. Li and Y. Liu and S. Macmil and Mandapat, {C. M.} and R. Mata and T. Mathew and T. Matskevitch and M. Munidasa and U. Nagaswamy and R. Najjar and N. Nguyen and J. Niu and D. Opheim and T. Palculict and S. Paul and M. Pellon and L. Perales and C. Pham and P. Pham",

note = "KAUST Repository Item: Exported on 2020-10-01",

year = "2014",

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doi = "10.1186/1471-2164-15-86",

language = "English (US)",

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Elsik, CG, Worley, KC, Bennett, AK, Beye, M, Camara, F, Childers, CP, de Graaf, DC, Debyser, G, Deng, J, Devreese, B, Elhaik, E, Evans, JD, Foster, LJ, Graur, D, Guigo, R, Hoff, KJ, Holder, ME, Hudson, ME, Hunt, GJ, Jiang, H, Joshi, V, Khetani, RS, Kosarev, P, Kovar, CL, Ma, J, Maleszka, R, Moritz, RFA, Munoz-Torres, MC, Murphy, TD, Muzny, DM, Newsham, IF, Reese, JT, Robertson, HM, Robinson, GE, Rueppell, O, Solovyev, V, Stanke, M, Stolle, E, Tsuruda, JM, Vaerenbergh, MV, Waterhouse, RM, Weaver, DB, Whitfield, CW, Wu, Y, Zdobnov, EM, Zhang, L, Zhu, D, Gibbs, RA, Patil, S, Gubbala, S, Aqrawi, P, Arias, F, Bess, C, Blankenburg, KB, 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, TH, Hale, W, Han, H, Hu, Y, Jackson, L, Jakkamsetti, A, Jayaseelan, JC, Kakkar, N, Kalra, D, Kandadi, H, Lee, S, Li, H, Liu, Y, Macmil, S, Mandapat, CM, 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 2014, 'Finding the missing honey bee genes: Lessons learned from a genome upgrade', BMC Genomics, vol. 15, no. 1, pp. 86. https://doi.org/10.1186/1471-2164-15-86

TY - JOUR

T1 - Finding the missing honey bee genes: Lessons learned from a genome upgrade

AU - Elsik, Christine G

AU - Worley, Kim C

AU - Bennett, Anna K

AU - Beye, Martin

AU - Camara, Francisco

AU - Childers, Christopher P

AU - de Graaf, Dirk C

AU - Debyser, Griet

AU - Deng, Jixin

AU - Devreese, Bart

AU - Elhaik, Eran

AU - Evans, Jay D

AU - Foster, Leonard J

AU - Graur, Dan

AU - Guigo, Roderic

AU - Hoff, Katharina Jasmin

AU - Holder, Michael E

AU - Hudson, Matthew E

AU - Hunt, Greg J

AU - Jiang, Huaiyang

AU - Joshi, Vandita

AU - Khetani, Radhika S

AU - Kosarev, Peter

AU - Kovar, Christie L

AU - Ma, Jian

AU - Maleszka, Ryszard

AU - Moritz, Robin F A

AU - Munoz-Torres, Monica C

AU - Murphy, Terence D

AU - Muzny, Donna M

AU - Newsham, Irene F

AU - Reese, Justin T

AU - Robertson, Hugh M

AU - Robinson, Gene E

AU - Rueppell, Olav

AU - Solovyev, Victor

AU - Stanke, Mario

AU - Stolle, Eckart

AU - Tsuruda, Jennifer M

AU - Vaerenbergh, Matthias Van

AU - Waterhouse, Robert M

AU - Weaver, Daniel B

AU - Whitfield, Charles W

AU - Wu, Yuanqing

AU - Zdobnov, Evgeny M

AU - Zhang, Lan

AU - Zhu, Dianhui

AU - Gibbs, Richard A

AU - Patil, S.

AU - Gubbala, S.

AU - Aqrawi, P.

AU - Arias, F.

AU - Bess, C.

AU - Blankenburg, K. B.

AU - Brocchini, M.

AU - Buhay, C.

AU - Challis, D.

AU - Chang, K.

AU - Chen, D.

AU - Coleman, P.

AU - Drummond, J.

AU - English, A.

AU - Evani, U.

AU - Francisco, L.

AU - Fu, Q.

AU - Goodspeed, R.

AU - Haessly, T. H.

AU - Hale, W.

AU - Han, H.

AU - Hu, Y.

AU - Jackson, L.

AU - Jakkamsetti, A.

AU - Jayaseelan, J. C.

AU - Kakkar, N.

AU - Kalra, D.

AU - Kandadi, H.

AU - Lee, S.

AU - Li, H.

AU - Liu, Y.

AU - Macmil, S.

AU - Mandapat, C. M.

AU - Mata, R.

AU - Mathew, T.

AU - Matskevitch, T.

AU - Munidasa, M.

AU - Nagaswamy, U.

AU - Najjar, R.

AU - Nguyen, N.

AU - Niu, J.

AU - Opheim, D.

AU - Palculict, T.

AU - Paul, S.

AU - Pellon, M.

AU - Perales, L.

AU - Pham, C.

AU - Pham, P.

N1 - KAUST Repository Item: Exported on 2020-10-01

PY - 2014/1/30

Y1 - 2014/1/30

N2 - 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.

AB - 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.

UR - http://hdl.handle.net/10754/325245

UR - http://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-15-86

UR - http://www.scopus.com/inward/record.url?scp=84896690037&partnerID=8YFLogxK

U2 - 10.1186/1471-2164-15-86

DO - 10.1186/1471-2164-15-86

M3 - Article

C2 - 24479613

SN - 1471-2164

VL - 15

SP - 86

JO - BMC Genomics

JF - BMC Genomics

IS - 1

ER -

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

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