Analyses of pig genomes provide insight into porcine demography and evolution

Martien A.M. Groenen; Alan L. Archibald; Hirohide Uenishi; Christopher K. Tuggle; Yasuhiro Takeuchi; Max F. Rothschild; Claire Rogel-Gaillard; Chankyu Park; Denis Milan; Hendrik Jan Megens; Shengting Li; Denis M. Larkin; Heebal Kim; Laurent A.F. Frantz; Mario Caccamo; Hyeonju Ahn; Bronwen L. Aken; Anna Anselmo; Christian Anthon; Loretta Auvil; Bouabid Badaoui; Craig W. Beattie; Christian Bendixen; Daniel Berman; Frank Blecha; Jonas Blomberg; Lars Bolund; Mirte Bosse; Sara Botti; Zhan Bujie; Megan Bystrom; Boris Capitanu; Denise Carvalho-Silva; Patrick Chardon; Celine Chen; Ryan Cheng; Sang Haeng Choi; William Chow; Richard C. Clark; Christopher Clee; Richard P.M.A. Crooijmans; Harry D. Dawson; Patrice Dehais; Fioravante De Sapio; Bert Dibbits; Nizar Drou; Zhi Qiang Du; Kellye Eversole; Joao Fadista; Susan Fairley; Thomas Faraut; Geoffrey J. Faulkner; Katie E. Fowler; Merete Fredholm; Eric Fritz; James G.R. Gilbert; Elisabetta Giuffra; Jan Gorodkin; Darren K. Griffin; Jennifer L. Harrow; Alexander Hayward; Kerstin Howe; Zhi Liang Hu; Sean J. Humphray; Toby Hunt; Henrik Hornshoøj; Jin Tae Jeon; Patric Jern; Matthew Jones; Jerzy Jurka; Hiroyuki Kanamori; Ronan Kapetanovic; Jaebum Kim; Jae Hwan Kim; Kyu Won Kim; Tae Hun Kim; Greger Larson; Kyooyeol Lee; Kyung Tai Lee; Richard Leggett; Harris A. Lewin; Yingrui Li; Wansheng Liu; Jane E. Loveland; Yao Lu; Joan K. Lunney; Jian Ma; Ole Madsen; Katherine Mann; Lucy Matthews; Stuart McLaren; Takeya Morozumi; Michael P. Murtaugh; Jitendra Narayan; Dinh Truong Nguyen; Peixiang Ni; Song Jung Oh; Suneel Onteru; Frank Panitz; Eung Woo Park; Hong Seog Park; Geraldine Pascal; Yogesh Paudel; Miguel Perez-Enciso; Ricardo Ramirez-Gonzalez; James M. Reecy; Sandra Rodriguez-Zas; Gary A. Rohrer; Lauretta Rund; Yongming Sang; Kyle Schachtschneider; Joshua G. Schraiber; John Schwartz; Linda Scobie; Carol Scott; Stephen Searle; Bertrand Servin; Bruce R. Southey; Goran Sperber; Peter Stadler; Jonathan V. Sweedler; Hakim Tafer; Bo Thomsen; Rashmi Wali; Jian Wang; Jun Wang; Simon White; Xun Xu; Martine Yerle; Guojie Zhang; Jianguo Zhang; Jie Zhang; Shuhong Zhao; Jane Rogers; Carol Churcher; Lawrence B. Schook

doi:10.1038/nature11622

Analyses of pig genomes provide insight into porcine demography and evolution

Martien A.M. Groenen, Alan L. Archibald, Hirohide Uenishi, Christopher K. Tuggle, Yasuhiro Takeuchi, Max F. Rothschild, Claire Rogel-Gaillard, Chankyu Park, Denis Milan, Hendrik Jan Megens, Shengting Li, Denis M. Larkin, Heebal Kim, Laurent A.F. Frantz, Mario Caccamo, Hyeonju Ahn, Bronwen L. Aken, Anna Anselmo, Christian Anthon, Loretta AuvilBouabid Badaoui, Craig W. Beattie, Christian Bendixen, Daniel Berman, Frank Blecha, Jonas Blomberg, Lars Bolund, Mirte Bosse, Sara Botti, Zhan Bujie, Megan Bystrom, Boris Capitanu, Denise Carvalho-Silva, Patrick Chardon, Celine Chen, Ryan Cheng, Sang Haeng Choi, William Chow, Richard C. Clark, Christopher Clee, Richard P.M.A. Crooijmans, Harry D. Dawson, Patrice Dehais, Fioravante De Sapio, Bert Dibbits, Nizar Drou, Zhi Qiang Du, Kellye Eversole, Joao Fadista, Susan Fairley, Thomas Faraut, Geoffrey J. Faulkner, Katie E. Fowler, Merete Fredholm, Eric Fritz, James G.R. Gilbert, Elisabetta Giuffra, Jan Gorodkin, Darren K. Griffin, Jennifer L. Harrow, Alexander Hayward, Kerstin Howe, Zhi Liang Hu, Sean J. Humphray, Toby Hunt, Henrik Hornshoøj, Jin Tae Jeon, Patric Jern, Matthew Jones, Jerzy Jurka, Hiroyuki Kanamori, Ronan Kapetanovic, Jaebum Kim, Jae Hwan Kim, Kyu Won Kim, Tae Hun Kim, Greger Larson, Kyooyeol Lee, Kyung Tai Lee, Richard Leggett, Harris A. Lewin, Yingrui Li, Wansheng Liu, Jane E. Loveland, Yao Lu, Joan K. Lunney, Jian Ma, Ole Madsen, Katherine Mann, Lucy Matthews, Stuart McLaren, Takeya Morozumi, Michael P. Murtaugh, Jitendra Narayan, Dinh Truong Nguyen, Peixiang Ni, Song Jung Oh, Suneel Onteru, Frank Panitz, Eung Woo Park, Hong Seog Park, Geraldine Pascal, Yogesh Paudel, Miguel Perez-Enciso, Ricardo Ramirez-Gonzalez, James M. Reecy, Sandra Rodriguez-Zas, Gary A. Rohrer, Lauretta Rund, Yongming Sang, Kyle Schachtschneider, Joshua G. Schraiber, John Schwartz, Linda Scobie, Carol Scott, Stephen Searle, Bertrand Servin, Bruce R. Southey, Goran Sperber, Peter Stadler, Jonathan V. Sweedler, Hakim Tafer, Bo Thomsen, Rashmi Wali, Jian Wang, Jun Wang, Simon White, Xun Xu, Martine Yerle, Guojie Zhang, Jianguo Zhang, Jie Zhang, Shuhong Zhao, Jane Rogers, Carol Churcher, Lawrence B. Schook

Veterinary and Biomedical Sciences

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

1030 Scopus citations

Abstract

For 10,000a €‰years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ∼1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.

Original language	English (US)
Pages (from-to)	393-398
Number of pages	6
Journal	Nature
Volume	491
Issue number	7424
DOIs	https://doi.org/10.1038/nature11622
State	Published - Nov 15 2012

Bibliographical note

Funding Information:
Acknowledgements The authors recognize the contributions of the following individuals towards the establishment of the Swine Genome Sequencing Consortium and their leadership in realizing this effort: J. Jen, P. J. Burfening, D. Hamernik, R. A. Easter, N. Merchen, R. D. Green, J. Cassady, B. Harlizius, M. Boggess and M. Stratton. Also the authors acknowledge A. Hernandez, C. Wright at the University of Illinois Keck Center for Comparative and Functional Genomics; N. Bruneau and Prof. Ning Li for their contribution to PERV studies; D. Goodband and D. Berman for their efforts in genome annotation; D. Grafham of the Welcome Trust Sanger Institute for his efforts in the genome assembly and J. Hedegaard, M. Nielsen and R. O. Nielsen for their contribution on the miRNA analysis. We also recognize contributions from the National Institute of Agrobiological Sciences and the Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, Tsukuba, Japan, H. Shinkai, T. Eguchi-Ogawa, K. Suzuki, D. Toki, T. Matsumoto, N. Fujishima-Kanaya, A. Mikawa, N. Okumura, M. Tanaka-Matsuda, K. Kurita, H. Sasaki, K. Kamiya, A. Kikuta, T. Bito and N. Fujitsuka. We acknowledge support from the USDA CSREES/NIFA Swine Genome Coordination Program, College of Agricultural,Consumer andEnvironmental Sciences, University of Illinois; College of Agriculture and Life Sciences, Iowa State University; North Carolina Agricultural Research Service; USA National Pork Board; Iowa Pork Producers Association; North Carolina Pork Council; Danish government; TOPIGS Research Center IPG The Netherlands; INRA Genescope, France; Wellcome Trust Sanger Institute and BGI. We are grateful to the genome team at NCBI for their assistance in checking the Sscrofa10.2 assembly and for their independent annotation of the sequence. This project was also partially supported by grants: BBSRC grants (Ensembl): BB/E010520/1, BB/E010520/2, BB/I025328/1; EC FP6 ‘Cutting edge genomics for sustainable animal breeding (SABRE)’; EC FP7 ‘Quantomics’; C. J. Martin Overseas Based Biomedical Fellowship from the Australian NHMRC (575585); BBSRC (BB/H005935/1); Next-Generation BioGreen 21 Program (PJ009019, PJ0081162012), RDA, Republic of Korea; Consolider programme from Ministry of Research (Spain); NIH R13 RR020283A; NIH R13 RR032267A; ILLU 535-314; ILLU 538-379; ILLU-538-312; ILLU-538-34; CSREES, NIFA for funding genome coordination activities; NIH grant 5 P41LM006252; MAFF grants (IRPPIAUGT-AG 1101/1201); USDA-NRI-2009-35205-05192; USDA-NRSP8 Bioinformatics Coordination and Pig Genome Coordination funds; US-UK Fulbright Commission; Next-Generation BioGreen 21 (no. PJ0080892011) Program, RDA, Republic of Korea; USDA-ARS Project Plan 1235-51000-055-00D; USDA-ARS Project Plan 1265-32000-098-00D; USDA-NRI-2006-35204-17337 USDA AFRI NIFA/DHS 2010-39559-21860; NIH P20-RR017686; USDA ARS; USDA-NRSP8 Bioinformatics; USDA ARS Beltsville Area Summer Undergraduate Fellowships; BBSRC grant BB/ G004013/1; NSFC Outstanding Youth grant (31025026); The Swedish Research Council FORMAS; The Swedish Wenner-Gren Foundations; European Commission FP6 funded project LSHB-CT-2006-037377; BioGreen21, RDA grant PJ00622901; BioGreen21, RDA grant PJ00622902; BioGreen21, RDA grant PJ00622903; BioGreen21, RDA grant PJ00622903. The research leading to these results has received funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 249894 (SelSweep); NIH P20-RR017686; NIH NIDA P30 DA018310; NIH NIDA R21 DA027548; NIAS, RDA grant PJ001758; BioGreen21, RDA grant PJ006229; NIAS, RDA grant 20040301034467; ANR grant ANR07-GANI-001 DeliSus; Danish funding agencies: FTP/DFF (09-066598); DSF/Strategic Growth Technologies (09-067036); the Lundbeck foundation (374/06); DCSC (Scientific Computing); The Funds for International Cooperation from the Ministry of Science and Technology of China 2002AA229061; PL-Grid project: POIG.02.03.00-00-007/08-00 ‘Genome Assembly’; USDA-NIFA-CREES AG 2006-35216-16668; AG 2002-34480-11828; AG 2003-34480-13172; AG 2004-34480-14417; AG 2005-34480-15939; AG 2006-34480-17150; AG 2008-34480-19328; AG 2009-34480-19875; AG 2002-35205-12712;somaticcellgenomics:Integrating QTL Discovery and Validation; AG 2008-35205-18769; AG 2009-65205-05642; AG 2004-3881-02193; AG 2011-67015-30229; AG 58-5438-2-313; AG 58-5438-7-317; and AG 58-0208-7-149; NIH grant 5 P41 LM006252.

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Groenen, M. A. M., Archibald, A. L., Uenishi, H., Tuggle, C. K., Takeuchi, Y., Rothschild, M. F., Rogel-Gaillard, C., Park, C., Milan, D., Megens, H. J., Li, S., Larkin, D. M., Kim, H., Frantz, L. A. F., Caccamo, M., Ahn, H., Aken, B. L., Anselmo, A., Anthon, C., ... Schook, L. B. (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491(7424), 393-398. https://doi.org/10.1038/nature11622

Groenen, MAM, Archibald, AL, Uenishi, H, Tuggle, CK, Takeuchi, Y, Rothschild, MF, Rogel-Gaillard, C, Park, C, Milan, D, Megens, HJ, Li, S, Larkin, DM, Kim, H, Frantz, LAF, Caccamo, M, Ahn, H, Aken, BL, Anselmo, A, Anthon, C, Auvil, L, Badaoui, B, Beattie, CW, Bendixen, C, Berman, D, Blecha, F, Blomberg, J, Bolund, L, Bosse, M, Botti, S, Bujie, Z, Bystrom, M, Capitanu, B, Carvalho-Silva, D, Chardon, P, Chen, C, Cheng, R, Choi, SH, Chow, W, Clark, RC, Clee, C, Crooijmans, RPMA, Dawson, HD, Dehais, P, De Sapio, F, Dibbits, B, Drou, N, Du, ZQ, Eversole, K, Fadista, J, Fairley, S, Faraut, T, Faulkner, GJ, Fowler, KE, Fredholm, M, Fritz, E, Gilbert, JGR, Giuffra, E, Gorodkin, J, Griffin, DK, Harrow, JL, Hayward, A, Howe, K, Hu, ZL, Humphray, SJ, Hunt, T, Hornshoøj, H, Jeon, JT, Jern, P, Jones, M, Jurka, J, Kanamori, H, Kapetanovic, R, Kim, J, Kim, JH, Kim, KW, Kim, TH, Larson, G, Lee, K, Lee, KT, Leggett, R, Lewin, HA, Li, Y, Liu, W, Loveland, JE, Lu, Y, Lunney, JK, Ma, J, Madsen, O, Mann, K, Matthews, L, McLaren, S, Morozumi, T, Murtaugh, MP, Narayan, J, Nguyen, DT, Ni, P, Oh, SJ, Onteru, S, Panitz, F, Park, EW, Park, HS, Pascal, G, Paudel, Y, Perez-Enciso, M, Ramirez-Gonzalez, R, Reecy, JM, Rodriguez-Zas, S, Rohrer, GA, Rund, L, Sang, Y, Schachtschneider, K, Schraiber, JG, Schwartz, J, Scobie, L, Scott, C, Searle, S, Servin, B, Southey, BR, Sperber, G, Stadler, P, Sweedler, JV, Tafer, H, Thomsen, B, Wali, R, Wang, J, Wang, J, White, S, Xu, X, Yerle, M, Zhang, G, Zhang, J, Zhang, J, Zhao, S, Rogers, J, Churcher, C & Schook, LB 2012, 'Analyses of pig genomes provide insight into porcine demography and evolution', Nature, vol. 491, no. 7424, pp. 393-398. https://doi.org/10.1038/nature11622

@article{8188b38bafdb42e88f202034113da109,

title = "Analyses of pig genomes provide insight into porcine demography and evolution",

abstract = "For 10,000a €‰years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ∼1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.",

author = "Groenen, {Martien A.M.} and Archibald, {Alan L.} and Hirohide Uenishi and Tuggle, {Christopher K.} and Yasuhiro Takeuchi and Rothschild, {Max F.} and Claire Rogel-Gaillard and Chankyu Park and Denis Milan and Megens, {Hendrik Jan} and Shengting Li and Larkin, {Denis M.} and Heebal Kim and Frantz, {Laurent A.F.} and Mario Caccamo and Hyeonju Ahn and Aken, {Bronwen L.} and Anna Anselmo and Christian Anthon and Loretta Auvil and Bouabid Badaoui and Beattie, {Craig W.} and Christian Bendixen and Daniel Berman and Frank Blecha and Jonas Blomberg and Lars Bolund and Mirte Bosse and Sara Botti and Zhan Bujie and Megan Bystrom and Boris Capitanu and Denise Carvalho-Silva and Patrick Chardon and Celine Chen and Ryan Cheng and Choi, {Sang Haeng} and William Chow and Clark, {Richard C.} and Christopher Clee and Crooijmans, {Richard P.M.A.} and Dawson, {Harry D.} and Patrice Dehais and {De Sapio}, Fioravante and Bert Dibbits and Nizar Drou and Du, {Zhi Qiang} and Kellye Eversole and Joao Fadista and Susan Fairley and Thomas Faraut and Faulkner, {Geoffrey J.} and Fowler, {Katie E.} and Merete Fredholm and Eric Fritz and Gilbert, {James G.R.} and Elisabetta Giuffra and Jan Gorodkin and Griffin, {Darren K.} and Harrow, {Jennifer L.} and Alexander Hayward and Kerstin Howe and Hu, {Zhi Liang} and Humphray, {Sean J.} and Toby Hunt and Henrik Hornsho{\o}j and Jeon, {Jin Tae} and Patric Jern and Matthew Jones and Jerzy Jurka and Hiroyuki Kanamori and Ronan Kapetanovic and Jaebum Kim and Kim, {Jae Hwan} and Kim, {Kyu Won} and Kim, {Tae Hun} and Greger Larson and Kyooyeol Lee and Lee, {Kyung Tai} and Richard Leggett and Lewin, {Harris A.} and Yingrui Li and Wansheng Liu and Loveland, {Jane E.} and Yao Lu and Lunney, {Joan K.} and Jian Ma and Ole Madsen and Katherine Mann and Lucy Matthews and Stuart McLaren and Takeya Morozumi and Murtaugh, {Michael P.} and Jitendra Narayan and Nguyen, {Dinh Truong} and Peixiang Ni and Oh, {Song Jung} and Suneel Onteru and Frank Panitz and Park, {Eung Woo} and Park, {Hong Seog} and Geraldine Pascal and Yogesh Paudel and Miguel Perez-Enciso and Ricardo Ramirez-Gonzalez and Reecy, {James M.} and Sandra Rodriguez-Zas and Rohrer, {Gary A.} and Lauretta Rund and Yongming Sang and Kyle Schachtschneider and Schraiber, {Joshua G.} and John Schwartz and Linda Scobie and Carol Scott and Stephen Searle and Bertrand Servin and Southey, {Bruce R.} and Goran Sperber and Peter Stadler and Sweedler, {Jonathan V.} and Hakim Tafer and Bo Thomsen and Rashmi Wali and Jian Wang and Jun Wang and Simon White and Xun Xu and Martine Yerle and Guojie Zhang and Jianguo Zhang and Jie Zhang and Shuhong Zhao and Jane Rogers and Carol Churcher and Schook, {Lawrence B.}",

note = "Funding Information: Acknowledgements The authors recognize the contributions of the following individuals towards the establishment of the Swine Genome Sequencing Consortium and their leadership in realizing this effort: J. Jen, P. J. Burfening, D. Hamernik, R. A. Easter, N. Merchen, R. D. Green, J. Cassady, B. Harlizius, M. Boggess and M. Stratton. Also the authors acknowledge A. Hernandez, C. Wright at the University of Illinois Keck Center for Comparative and Functional Genomics; N. Bruneau and Prof. Ning Li for their contribution to PERV studies; D. Goodband and D. Berman for their efforts in genome annotation; D. Grafham of the Welcome Trust Sanger Institute for his efforts in the genome assembly and J. Hedegaard, M. Nielsen and R. O. Nielsen for their contribution on the miRNA analysis. We also recognize contributions from the National Institute of Agrobiological Sciences and the Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, Tsukuba, Japan, H. Shinkai, T. Eguchi-Ogawa, K. Suzuki, D. Toki, T. Matsumoto, N. Fujishima-Kanaya, A. Mikawa, N. Okumura, M. Tanaka-Matsuda, K. Kurita, H. Sasaki, K. Kamiya, A. Kikuta, T. Bito and N. Fujitsuka. We acknowledge support from the USDA CSREES/NIFA Swine Genome Coordination Program, College of Agricultural,Consumer andEnvironmental Sciences, University of Illinois; College of Agriculture and Life Sciences, Iowa State University; North Carolina Agricultural Research Service; USA National Pork Board; Iowa Pork Producers Association; North Carolina Pork Council; Danish government; TOPIGS Research Center IPG The Netherlands; INRA Genescope, France; Wellcome Trust Sanger Institute and BGI. We are grateful to the genome team at NCBI for their assistance in checking the Sscrofa10.2 assembly and for their independent annotation of the sequence. This project was also partially supported by grants: BBSRC grants (Ensembl): BB/E010520/1, BB/E010520/2, BB/I025328/1; EC FP6 {\textquoteleft}Cutting edge genomics for sustainable animal breeding (SABRE){\textquoteright}; EC FP7 {\textquoteleft}Quantomics{\textquoteright}; C. J. Martin Overseas Based Biomedical Fellowship from the Australian NHMRC (575585); BBSRC (BB/H005935/1); Next-Generation BioGreen 21 Program (PJ009019, PJ0081162012), RDA, Republic of Korea; Consolider programme from Ministry of Research (Spain); NIH R13 RR020283A; NIH R13 RR032267A; ILLU 535-314; ILLU 538-379; ILLU-538-312; ILLU-538-34; CSREES, NIFA for funding genome coordination activities; NIH grant 5 P41LM006252; MAFF grants (IRPPIAUGT-AG 1101/1201); USDA-NRI-2009-35205-05192; USDA-NRSP8 Bioinformatics Coordination and Pig Genome Coordination funds; US-UK Fulbright Commission; Next-Generation BioGreen 21 (no. PJ0080892011) Program, RDA, Republic of Korea; USDA-ARS Project Plan 1235-51000-055-00D; USDA-ARS Project Plan 1265-32000-098-00D; USDA-NRI-2006-35204-17337 USDA AFRI NIFA/DHS 2010-39559-21860; NIH P20-RR017686; USDA ARS; USDA-NRSP8 Bioinformatics; USDA ARS Beltsville Area Summer Undergraduate Fellowships; BBSRC grant BB/ G004013/1; NSFC Outstanding Youth grant (31025026); The Swedish Research Council FORMAS; The Swedish Wenner-Gren Foundations; European Commission FP6 funded project LSHB-CT-2006-037377; BioGreen21, RDA grant PJ00622901; BioGreen21, RDA grant PJ00622902; BioGreen21, RDA grant PJ00622903; BioGreen21, RDA grant PJ00622903. The research leading to these results has received funding from the European Research Council under the European Community{\textquoteright}s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 249894 (SelSweep); NIH P20-RR017686; NIH NIDA P30 DA018310; NIH NIDA R21 DA027548; NIAS, RDA grant PJ001758; BioGreen21, RDA grant PJ006229; NIAS, RDA grant 20040301034467; ANR grant ANR07-GANI-001 DeliSus; Danish funding agencies: FTP/DFF (09-066598); DSF/Strategic Growth Technologies (09-067036); the Lundbeck foundation (374/06); DCSC (Scientific Computing); The Funds for International Cooperation from the Ministry of Science and Technology of China 2002AA229061; PL-Grid project: POIG.02.03.00-00-007/08-00 {\textquoteleft}Genome Assembly{\textquoteright}; USDA-NIFA-CREES AG 2006-35216-16668; AG 2002-34480-11828; AG 2003-34480-13172; AG 2004-34480-14417; AG 2005-34480-15939; AG 2006-34480-17150; AG 2008-34480-19328; AG 2009-34480-19875; AG 2002-35205-12712;somaticcellgenomics:Integrating QTL Discovery and Validation; AG 2008-35205-18769; AG 2009-65205-05642; AG 2004-3881-02193; AG 2011-67015-30229; AG 58-5438-2-313; AG 58-5438-7-317; and AG 58-0208-7-149; NIH grant 5 P41 LM006252.",

year = "2012",

month = nov,

day = "15",

doi = "10.1038/nature11622",

language = "English (US)",

volume = "491",

pages = "393--398",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7424",

}

TY - JOUR

T1 - Analyses of pig genomes provide insight into porcine demography and evolution

AU - Groenen, Martien A.M.

AU - Archibald, Alan L.

AU - Uenishi, Hirohide

AU - Tuggle, Christopher K.

AU - Takeuchi, Yasuhiro

AU - Rothschild, Max F.

AU - Rogel-Gaillard, Claire

AU - Park, Chankyu

AU - Milan, Denis

AU - Megens, Hendrik Jan

AU - Li, Shengting

AU - Larkin, Denis M.

AU - Kim, Heebal

AU - Frantz, Laurent A.F.

AU - Caccamo, Mario

AU - Ahn, Hyeonju

AU - Aken, Bronwen L.

AU - Anselmo, Anna

AU - Anthon, Christian

AU - Auvil, Loretta

AU - Badaoui, Bouabid

AU - Beattie, Craig W.

AU - Bendixen, Christian

AU - Berman, Daniel

AU - Blecha, Frank

AU - Blomberg, Jonas

AU - Bolund, Lars

AU - Bosse, Mirte

AU - Botti, Sara

AU - Bujie, Zhan

AU - Bystrom, Megan

AU - Capitanu, Boris

AU - Carvalho-Silva, Denise

AU - Chardon, Patrick

AU - Chen, Celine

AU - Cheng, Ryan

AU - Choi, Sang Haeng

AU - Chow, William

AU - Clark, Richard C.

AU - Clee, Christopher

AU - Crooijmans, Richard P.M.A.

AU - Dawson, Harry D.

AU - Dehais, Patrice

AU - De Sapio, Fioravante

AU - Dibbits, Bert

AU - Drou, Nizar

AU - Du, Zhi Qiang

AU - Eversole, Kellye

AU - Fadista, Joao

AU - Fairley, Susan

AU - Faraut, Thomas

AU - Faulkner, Geoffrey J.

AU - Fowler, Katie E.

AU - Fredholm, Merete

AU - Fritz, Eric

AU - Gilbert, James G.R.

AU - Giuffra, Elisabetta

AU - Gorodkin, Jan

AU - Griffin, Darren K.

AU - Harrow, Jennifer L.

AU - Hayward, Alexander

AU - Howe, Kerstin

AU - Hu, Zhi Liang

AU - Humphray, Sean J.

AU - Hunt, Toby

AU - Hornshoøj, Henrik

AU - Jeon, Jin Tae

AU - Jern, Patric

AU - Jones, Matthew

AU - Jurka, Jerzy

AU - Kanamori, Hiroyuki

AU - Kapetanovic, Ronan

AU - Kim, Jaebum

AU - Kim, Jae Hwan

AU - Kim, Kyu Won

AU - Kim, Tae Hun

AU - Larson, Greger

AU - Lee, Kyooyeol

AU - Lee, Kyung Tai

AU - Leggett, Richard

AU - Lewin, Harris A.

AU - Li, Yingrui

AU - Liu, Wansheng

AU - Loveland, Jane E.

AU - Lu, Yao

AU - Lunney, Joan K.

AU - Ma, Jian

AU - Madsen, Ole

AU - Mann, Katherine

AU - Matthews, Lucy

AU - McLaren, Stuart

AU - Morozumi, Takeya

AU - Murtaugh, Michael P.

AU - Narayan, Jitendra

AU - Nguyen, Dinh Truong

AU - Ni, Peixiang

AU - Oh, Song Jung

AU - Onteru, Suneel

AU - Panitz, Frank

AU - Park, Eung Woo

AU - Park, Hong Seog

AU - Pascal, Geraldine

AU - Paudel, Yogesh

AU - Perez-Enciso, Miguel

AU - Ramirez-Gonzalez, Ricardo

AU - Reecy, James M.

AU - Rodriguez-Zas, Sandra

AU - Rohrer, Gary A.

AU - Rund, Lauretta

AU - Sang, Yongming

AU - Schachtschneider, Kyle

AU - Schraiber, Joshua G.

AU - Schwartz, John

AU - Scobie, Linda

AU - Scott, Carol

AU - Searle, Stephen

AU - Servin, Bertrand

AU - Southey, Bruce R.

AU - Sperber, Goran

AU - Stadler, Peter

AU - Sweedler, Jonathan V.

AU - Tafer, Hakim

AU - Thomsen, Bo

AU - Wali, Rashmi

AU - Wang, Jian

AU - Wang, Jun

AU - White, Simon

AU - Xu, Xun

AU - Yerle, Martine

AU - Zhang, Guojie

AU - Zhang, Jianguo

AU - Zhang, Jie

AU - Zhao, Shuhong

AU - Rogers, Jane

AU - Churcher, Carol

AU - Schook, Lawrence B.

N1 - Funding Information: Acknowledgements The authors recognize the contributions of the following individuals towards the establishment of the Swine Genome Sequencing Consortium and their leadership in realizing this effort: J. Jen, P. J. Burfening, D. Hamernik, R. A. Easter, N. Merchen, R. D. Green, J. Cassady, B. Harlizius, M. Boggess and M. Stratton. Also the authors acknowledge A. Hernandez, C. Wright at the University of Illinois Keck Center for Comparative and Functional Genomics; N. Bruneau and Prof. Ning Li for their contribution to PERV studies; D. Goodband and D. Berman for their efforts in genome annotation; D. Grafham of the Welcome Trust Sanger Institute for his efforts in the genome assembly and J. Hedegaard, M. Nielsen and R. O. Nielsen for their contribution on the miRNA analysis. We also recognize contributions from the National Institute of Agrobiological Sciences and the Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, Tsukuba, Japan, H. Shinkai, T. Eguchi-Ogawa, K. Suzuki, D. Toki, T. Matsumoto, N. Fujishima-Kanaya, A. Mikawa, N. Okumura, M. Tanaka-Matsuda, K. Kurita, H. Sasaki, K. Kamiya, A. Kikuta, T. Bito and N. Fujitsuka. We acknowledge support from the USDA CSREES/NIFA Swine Genome Coordination Program, College of Agricultural,Consumer andEnvironmental Sciences, University of Illinois; College of Agriculture and Life Sciences, Iowa State University; North Carolina Agricultural Research Service; USA National Pork Board; Iowa Pork Producers Association; North Carolina Pork Council; Danish government; TOPIGS Research Center IPG The Netherlands; INRA Genescope, France; Wellcome Trust Sanger Institute and BGI. We are grateful to the genome team at NCBI for their assistance in checking the Sscrofa10.2 assembly and for their independent annotation of the sequence. This project was also partially supported by grants: BBSRC grants (Ensembl): BB/E010520/1, BB/E010520/2, BB/I025328/1; EC FP6 ‘Cutting edge genomics for sustainable animal breeding (SABRE)’; EC FP7 ‘Quantomics’; C. J. Martin Overseas Based Biomedical Fellowship from the Australian NHMRC (575585); BBSRC (BB/H005935/1); Next-Generation BioGreen 21 Program (PJ009019, PJ0081162012), RDA, Republic of Korea; Consolider programme from Ministry of Research (Spain); NIH R13 RR020283A; NIH R13 RR032267A; ILLU 535-314; ILLU 538-379; ILLU-538-312; ILLU-538-34; CSREES, NIFA for funding genome coordination activities; NIH grant 5 P41LM006252; MAFF grants (IRPPIAUGT-AG 1101/1201); USDA-NRI-2009-35205-05192; USDA-NRSP8 Bioinformatics Coordination and Pig Genome Coordination funds; US-UK Fulbright Commission; Next-Generation BioGreen 21 (no. PJ0080892011) Program, RDA, Republic of Korea; USDA-ARS Project Plan 1235-51000-055-00D; USDA-ARS Project Plan 1265-32000-098-00D; USDA-NRI-2006-35204-17337 USDA AFRI NIFA/DHS 2010-39559-21860; NIH P20-RR017686; USDA ARS; USDA-NRSP8 Bioinformatics; USDA ARS Beltsville Area Summer Undergraduate Fellowships; BBSRC grant BB/ G004013/1; NSFC Outstanding Youth grant (31025026); The Swedish Research Council FORMAS; The Swedish Wenner-Gren Foundations; European Commission FP6 funded project LSHB-CT-2006-037377; BioGreen21, RDA grant PJ00622901; BioGreen21, RDA grant PJ00622902; BioGreen21, RDA grant PJ00622903; BioGreen21, RDA grant PJ00622903. The research leading to these results has received funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 249894 (SelSweep); NIH P20-RR017686; NIH NIDA P30 DA018310; NIH NIDA R21 DA027548; NIAS, RDA grant PJ001758; BioGreen21, RDA grant PJ006229; NIAS, RDA grant 20040301034467; ANR grant ANR07-GANI-001 DeliSus; Danish funding agencies: FTP/DFF (09-066598); DSF/Strategic Growth Technologies (09-067036); the Lundbeck foundation (374/06); DCSC (Scientific Computing); The Funds for International Cooperation from the Ministry of Science and Technology of China 2002AA229061; PL-Grid project: POIG.02.03.00-00-007/08-00 ‘Genome Assembly’; USDA-NIFA-CREES AG 2006-35216-16668; AG 2002-34480-11828; AG 2003-34480-13172; AG 2004-34480-14417; AG 2005-34480-15939; AG 2006-34480-17150; AG 2008-34480-19328; AG 2009-34480-19875; AG 2002-35205-12712;somaticcellgenomics:Integrating QTL Discovery and Validation; AG 2008-35205-18769; AG 2009-65205-05642; AG 2004-3881-02193; AG 2011-67015-30229; AG 58-5438-2-313; AG 58-5438-7-317; and AG 58-0208-7-149; NIH grant 5 P41 LM006252.

PY - 2012/11/15

Y1 - 2012/11/15

N2 - For 10,000a €‰years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ∼1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.

AB - For 10,000a €‰years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ∼1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.

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U2 - 10.1038/nature11622

DO - 10.1038/nature11622

M3 - Article

C2 - 23151582

AN - SCOPUS:84869003221

SN - 0028-0836

VL - 491

SP - 393

EP - 398

JO - Nature

JF - Nature

IS - 7424

ER -

Analyses of pig genomes provide insight into porcine demography and evolution

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