Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep
Some sheep breeds are naturally prolific, and they are very informative for the studies of reproductive genetics and physiology. Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify g...
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| creator | Demars, Julie Fabre, Stéphane Sarry, Julien Rossetti, Raffaella Gilbert, Hélène Persani, Luca Tosser-Klopp, Gwenola Mulsant, Philippe Nowak, Zuzanna Drobik, Wioleta Martyniuk, Elzbieta Bodin, Loys |
| description | Some sheep breeds are naturally prolific, and they are very informative for the studies of reproductive genetics and physiology. Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify genetic variants responsible for the highly prolific phenotype in these two breeds, genome-wide association studies (GWAS) followed by complementary genetic and functional analyses were performed. Highly prolific ewes (cases) and normal prolific ewes (controls) from each breed were genotyped using the Illumina OvineSNP50 Genotyping Beadchip. In both populations, an X chromosome region, close to the BMP15 gene, harbored clusters of markers with suggestive evidence of association at significance levels between 1E(-05) and 1E(-07). The BMP15 candidate gene was then sequenced, and two novel non-conservative mutations called FecX(Gr) and FecX(O) were identified in the Grivette and Olkuska breeds, respectively. The two mutations were associated with the highly prolific phenotype (p FecX (Gr) = 5.98E(-06) and p FecX(O) = 2.55E(-08)). Homozygous ewes for the mutated allele showed a significantly increased prolificacy (FecX(Gr)/FecX(Gr), LS = 2.50 ± 0.65 versus FecX(+)/FecX(Gr), LS = 1.93 ± 0.42, p |
| doi_str_mv | 10.1371/journal.pgen.1003482 |
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Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify genetic variants responsible for the highly prolific phenotype in these two breeds, genome-wide association studies (GWAS) followed by complementary genetic and functional analyses were performed. Highly prolific ewes (cases) and normal prolific ewes (controls) from each breed were genotyped using the Illumina OvineSNP50 Genotyping Beadchip. In both populations, an X chromosome region, close to the BMP15 gene, harbored clusters of markers with suggestive evidence of association at significance levels between 1E(-05) and 1E(-07). The BMP15 candidate gene was then sequenced, and two novel non-conservative mutations called FecX(Gr) and FecX(O) were identified in the Grivette and Olkuska breeds, respectively. The two mutations were associated with the highly prolific phenotype (p FecX (Gr) = 5.98E(-06) and p FecX(O) = 2.55E(-08)). Homozygous ewes for the mutated allele showed a significantly increased prolificacy (FecX(Gr)/FecX(Gr), LS = 2.50 ± 0.65 versus FecX(+)/FecX(Gr), LS = 1.93 ± 0.42, p<1E(-03) and FecX(O)/FecX(O), OR = 3.28 ± 0.85 versus FecX(+)/FecX(O), OR = 2.02 ± 0.47, p<1E(-03)). Both mutations are located in very well conserved motifs of the protein and altered the BMP15 signaling activity in vitro using a BMP-responsive luciferase test in COV434 granulosa cells. Thus, we have identified two novel mutations in the BMP15 gene associated with increased LS and OR. Notably, homozygous FecX(Gr)/FecX(Gr) Grivette and homozygous FecX(O)/FecX(O) Olkuska ewes are hyperprolific in striking contrast with the sterility exhibited by all other known homozygous BMP15 mutations. Our results bring new insights into the key role played by the BMP15 protein in ovarian function and could contribute to a better understanding of the pathogenesis of women's fertility disorders.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1003482</identifier><identifier>PMID: 23637641</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology ; Bone Morphogenetic Protein 15 - genetics ; Bone morphogenetic proteins ; Fertility ; Gene mutations ; Genetic aspects ; Genetics ; Genome-Wide Association Study ; Genomes ; Genomics ; Genotype ; Grants ; Health aspects ; Humans ; Life Sciences ; Litter Size - genetics ; Medicine ; Molecular weight ; Mutation ; Ovulation - genetics ; Pathogenesis ; Phenotype ; Physiological aspects ; Sheep ; Women</subject><ispartof>PLoS genetics, 2013-04, Vol.9 (4), p.e1003482</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2013 Demars et al 2013 Demars et al</rights><rights>2013 Demars et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Demars J, Fabre S, Sarry J, Rossetti R, Gilbert H, et al. (2013) Genome-Wide Association Studies Identify Two Novel BMP15 Mutations Responsible for an Atypical Hyperprolificacy Phenotype in Sheep. PLoS Genet 9(4): e1003482. doi:10.1371/journal.pgen.1003482</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c657t-88a04cc73d11e21cdb0a286fa04af9b96c43b1623772ab0af45abbf8b2a00abe3</citedby><cites>FETCH-LOGICAL-c657t-88a04cc73d11e21cdb0a286fa04af9b96c43b1623772ab0af45abbf8b2a00abe3</cites><orcidid>0000-0002-4385-3228 ; 0000-0001-7350-9500 ; 0000-0003-0550-4673 ; 0000-0003-2068-9581</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636084/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636084/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23637641$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02650114$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Demars, Julie</creatorcontrib><creatorcontrib>Fabre, Stéphane</creatorcontrib><creatorcontrib>Sarry, Julien</creatorcontrib><creatorcontrib>Rossetti, Raffaella</creatorcontrib><creatorcontrib>Gilbert, Hélène</creatorcontrib><creatorcontrib>Persani, Luca</creatorcontrib><creatorcontrib>Tosser-Klopp, Gwenola</creatorcontrib><creatorcontrib>Mulsant, Philippe</creatorcontrib><creatorcontrib>Nowak, Zuzanna</creatorcontrib><creatorcontrib>Drobik, Wioleta</creatorcontrib><creatorcontrib>Martyniuk, Elzbieta</creatorcontrib><creatorcontrib>Bodin, Loys</creatorcontrib><title>Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Some sheep breeds are naturally prolific, and they are very informative for the studies of reproductive genetics and physiology. Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify genetic variants responsible for the highly prolific phenotype in these two breeds, genome-wide association studies (GWAS) followed by complementary genetic and functional analyses were performed. Highly prolific ewes (cases) and normal prolific ewes (controls) from each breed were genotyped using the Illumina OvineSNP50 Genotyping Beadchip. In both populations, an X chromosome region, close to the BMP15 gene, harbored clusters of markers with suggestive evidence of association at significance levels between 1E(-05) and 1E(-07). The BMP15 candidate gene was then sequenced, and two novel non-conservative mutations called FecX(Gr) and FecX(O) were identified in the Grivette and Olkuska breeds, respectively. The two mutations were associated with the highly prolific phenotype (p FecX (Gr) = 5.98E(-06) and p FecX(O) = 2.55E(-08)). Homozygous ewes for the mutated allele showed a significantly increased prolificacy (FecX(Gr)/FecX(Gr), LS = 2.50 ± 0.65 versus FecX(+)/FecX(Gr), LS = 1.93 ± 0.42, p<1E(-03) and FecX(O)/FecX(O), OR = 3.28 ± 0.85 versus FecX(+)/FecX(O), OR = 2.02 ± 0.47, p<1E(-03)). Both mutations are located in very well conserved motifs of the protein and altered the BMP15 signaling activity in vitro using a BMP-responsive luciferase test in COV434 granulosa cells. Thus, we have identified two novel mutations in the BMP15 gene associated with increased LS and OR. Notably, homozygous FecX(Gr)/FecX(Gr) Grivette and homozygous FecX(O)/FecX(O) Olkuska ewes are hyperprolific in striking contrast with the sterility exhibited by all other known homozygous BMP15 mutations. Our results bring new insights into the key role played by the BMP15 protein in ovarian function and could contribute to a better understanding of the pathogenesis of women's fertility disorders.</description><subject>Animals</subject><subject>Biology</subject><subject>Bone Morphogenetic Protein 15 - genetics</subject><subject>Bone morphogenetic proteins</subject><subject>Fertility</subject><subject>Gene mutations</subject><subject>Genetic aspects</subject><subject>Genetics</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype</subject><subject>Grants</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Litter Size - genetics</subject><subject>Medicine</subject><subject>Molecular weight</subject><subject>Mutation</subject><subject>Ovulation - genetics</subject><subject>Pathogenesis</subject><subject>Phenotype</subject><subject>Physiological aspects</subject><subject>Sheep</subject><subject>Women</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNpdkk2P0zAQhiMEYpeFf4DAEhKCQ4s_E-eCVFawu1IRHOBsTRynceXGwU666pVfjtN2Vy2SJTszz7xvPJ4se03wnLCCfFr7MXTg5v3KdHOCMeOSPskuiRBsVnDMn56cL7IXMa4TI2RZPM8uKMtZkXNymf29MZ3fmNm9rQ2CGL22MFjfoTiMtTURpXg32GaHhnuPOr81Dn35_pMItBmHPRlRMLFPu62cQY0PCDoEw663Ghxqd70JffDONulb71DfJsOUNcgmk9aY_mX2rAEXzavjfpX9_vb11_XtbPnj5u56sZzpXBTDTErAXOuC1YQYSnRdYaAyb1IUmrIqc81ZRXLKioJCyjVcQFU1sqKAMVSGXWVvD7q981Ed2xcVYYKUOC2ZiLsDUXtYqz7YDYSd8mDVPuDDSkEYrHZGGWYIJSWTknEOUMtCE1yXFaMVr0E0Sevz0W2sNqbWqYsB3JnoeaazrVr5rUpPk2PJk8DHg0D7X9ntYqmmGKa5wITwLUnsh6NZ8H9GEwe1sVEb56AzfpzuyKXAmGKW0HcHdAXpGrZrfHLXE64WjGEqiMgnwfcnVGvADW30btw_-DnID6AOPsZgmsdfJVhNc_rQaDXNqTrOaSp7c9qdx6KHwWT_AOjo53k</recordid><startdate>20130401</startdate><enddate>20130401</enddate><creator>Demars, Julie</creator><creator>Fabre, Stéphane</creator><creator>Sarry, Julien</creator><creator>Rossetti, Raffaella</creator><creator>Gilbert, Hélène</creator><creator>Persani, Luca</creator><creator>Tosser-Klopp, Gwenola</creator><creator>Mulsant, Philippe</creator><creator>Nowak, Zuzanna</creator><creator>Drobik, Wioleta</creator><creator>Martyniuk, Elzbieta</creator><creator>Bodin, Loys</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4385-3228</orcidid><orcidid>https://orcid.org/0000-0001-7350-9500</orcidid><orcidid>https://orcid.org/0000-0003-0550-4673</orcidid><orcidid>https://orcid.org/0000-0003-2068-9581</orcidid></search><sort><creationdate>20130401</creationdate><title>Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep</title><author>Demars, Julie ; Fabre, Stéphane ; Sarry, Julien ; Rossetti, Raffaella ; Gilbert, Hélène ; Persani, Luca ; Tosser-Klopp, Gwenola ; Mulsant, Philippe ; Nowak, Zuzanna ; Drobik, Wioleta ; Martyniuk, Elzbieta ; Bodin, Loys</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c657t-88a04cc73d11e21cdb0a286fa04af9b96c43b1623772ab0af45abbf8b2a00abe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Biology</topic><topic>Bone Morphogenetic Protein 15 - genetics</topic><topic>Bone morphogenetic proteins</topic><topic>Fertility</topic><topic>Gene mutations</topic><topic>Genetic aspects</topic><topic>Genetics</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genotype</topic><topic>Grants</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Litter Size - genetics</topic><topic>Medicine</topic><topic>Molecular weight</topic><topic>Mutation</topic><topic>Ovulation - genetics</topic><topic>Pathogenesis</topic><topic>Phenotype</topic><topic>Physiological aspects</topic><topic>Sheep</topic><topic>Women</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Demars, Julie</creatorcontrib><creatorcontrib>Fabre, Stéphane</creatorcontrib><creatorcontrib>Sarry, Julien</creatorcontrib><creatorcontrib>Rossetti, Raffaella</creatorcontrib><creatorcontrib>Gilbert, Hélène</creatorcontrib><creatorcontrib>Persani, Luca</creatorcontrib><creatorcontrib>Tosser-Klopp, Gwenola</creatorcontrib><creatorcontrib>Mulsant, Philippe</creatorcontrib><creatorcontrib>Nowak, Zuzanna</creatorcontrib><creatorcontrib>Drobik, Wioleta</creatorcontrib><creatorcontrib>Martyniuk, Elzbieta</creatorcontrib><creatorcontrib>Bodin, Loys</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Demars, Julie</au><au>Fabre, Stéphane</au><au>Sarry, Julien</au><au>Rossetti, Raffaella</au><au>Gilbert, Hélène</au><au>Persani, Luca</au><au>Tosser-Klopp, Gwenola</au><au>Mulsant, Philippe</au><au>Nowak, Zuzanna</au><au>Drobik, Wioleta</au><au>Martyniuk, Elzbieta</au><au>Bodin, Loys</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2013-04-01</date><risdate>2013</risdate><volume>9</volume><issue>4</issue><spage>e1003482</spage><pages>e1003482-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Some sheep breeds are naturally prolific, and they are very informative for the studies of reproductive genetics and physiology. Major genes increasing litter size (LS) and ovulation rate (OR) were suspected in the French Grivette and the Polish Olkuska sheep populations, respectively. To identify genetic variants responsible for the highly prolific phenotype in these two breeds, genome-wide association studies (GWAS) followed by complementary genetic and functional analyses were performed. Highly prolific ewes (cases) and normal prolific ewes (controls) from each breed were genotyped using the Illumina OvineSNP50 Genotyping Beadchip. In both populations, an X chromosome region, close to the BMP15 gene, harbored clusters of markers with suggestive evidence of association at significance levels between 1E(-05) and 1E(-07). The BMP15 candidate gene was then sequenced, and two novel non-conservative mutations called FecX(Gr) and FecX(O) were identified in the Grivette and Olkuska breeds, respectively. The two mutations were associated with the highly prolific phenotype (p FecX (Gr) = 5.98E(-06) and p FecX(O) = 2.55E(-08)). Homozygous ewes for the mutated allele showed a significantly increased prolificacy (FecX(Gr)/FecX(Gr), LS = 2.50 ± 0.65 versus FecX(+)/FecX(Gr), LS = 1.93 ± 0.42, p<1E(-03) and FecX(O)/FecX(O), OR = 3.28 ± 0.85 versus FecX(+)/FecX(O), OR = 2.02 ± 0.47, p<1E(-03)). Both mutations are located in very well conserved motifs of the protein and altered the BMP15 signaling activity in vitro using a BMP-responsive luciferase test in COV434 granulosa cells. Thus, we have identified two novel mutations in the BMP15 gene associated with increased LS and OR. Notably, homozygous FecX(Gr)/FecX(Gr) Grivette and homozygous FecX(O)/FecX(O) Olkuska ewes are hyperprolific in striking contrast with the sterility exhibited by all other known homozygous BMP15 mutations. Our results bring new insights into the key role played by the BMP15 protein in ovarian function and could contribute to a better understanding of the pathogenesis of women's fertility disorders.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23637641</pmid><doi>10.1371/journal.pgen.1003482</doi><orcidid>https://orcid.org/0000-0002-4385-3228</orcidid><orcidid>https://orcid.org/0000-0001-7350-9500</orcidid><orcidid>https://orcid.org/0000-0003-0550-4673</orcidid><orcidid>https://orcid.org/0000-0003-2068-9581</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biology Bone Morphogenetic Protein 15 - genetics Bone morphogenetic proteins Fertility Gene mutations Genetic aspects Genetics Genome-Wide Association Study Genomes Genomics Genotype Grants Health aspects Humans Life Sciences Litter Size - genetics Medicine Molecular weight Mutation Ovulation - genetics Pathogenesis Phenotype Physiological aspects Sheep Women |
| title | Genome-wide association studies identify two novel BMP15 mutations responsible for an atypical hyperprolificacy phenotype in sheep |
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