Tropical Animal Health and Production

, Volume 42, Issue 5, pp 985–993 | Cite as

Polymorphism of BMPR1B, BMP15 and GDF9 fecundity genes in prolific Garole sheep

  • Shamik Polley
  • Sachinandan De
  • Biswajit Brahma
  • Ayan Mukherjee
  • Vinesh P.V.
  • Subhasis Batabyal
  • Jaspreet Singh Arora
  • Subhransu Pan
  • Ashis Kumar Samanta
  • Tirtha Kumar Datta
  • Surender Lal Goswami
Article

Abstract

Mutation studies in different prolific sheep breeds have shown that the transforming growth factor beta super family ligands viz. the growth differentiation factor 9 (GDF9/FecG), bone morphogenetic protein 15 (BMP15/FecX) and associated type I receptors, bone morphogenetic protein receptor (BMPR1B/FecB), are major determinant of ovulation rate and consequent increase in litter size. The Garole sheep is a highly prolific sheep breed of India. Characterization of fecundity genes in these animals could substantially improvise the breeding programme in these animals as well as other sheep breeds of the region. The present study was therefore designed with the objective of polymorphism study of fecundity genes in these prolific microsheep. A total of 11 point mutations were detected by polymerase chain reaction (PCR)-based method. A competitive technique called tetra-primer amplification refractory mutation system-PCR was adapted to type a total of ten points of two ovine fecundity genes (GDF9 and BMP15). The FecB locus of the BMPR1B gene and G1 locus of GDF9 gene were found to be polymorphic. In FecB locus, two genotypes, wild type (FecB+) and mutant (FecBB), were detected with allele frequencies of 0.39 and 0.61, respectively. At G1 locus, two genotypes, mutant (A) and wild types (G) were detected with allele frequencies of 0.18 and 0.82, respectively. This study reports Garole sheep as the fourth sheep breed after Belclare/Cambridge, Lacaune and Small-tailed Han sheep, where coexisting polymorphism has been found in two different fecundity genes (BMPRIB and GDF9 genes).

Keywords

Garole sheep Prolificacy BMPR1B GDF9 BMP15 

References

  1. Bindon, B. M., Piper, L. R. and Hillarda, M. A., 1996. Prolific Sheep. Fahmy, M. H. Ed. (CAB International, UK).Google Scholar
  2. Bodin, L., SanCristobal, M., Lecerf, F., Mulsant, P., Bibe, B., Lajous, D., Belloc, J.P., Eychenne, F., Amigues, Y. and Elsen, J.M., 2002. Segregation of a major gene influencing ovulation in progeny of Lacaune meat sheep. Genetics Selection Evolution, 34, 447-464.CrossRefGoogle Scholar
  3. Bodin, L., Di Pasquale, E., Fabre, S., Bontoux, M., Monget, P., Ersani, L. and Mulsant, P., 2007. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep, Endocrinology, 148, 393-400.CrossRefPubMedGoogle Scholar
  4. Chu, M. X., Cheng, R., Chen, G. H., Fang, L. and Ye, S. C., 2005a. Study on bone morphogenetic protein 15 as a candidate gene for prolificacy of Small Tailed Han sheep and Hu sheep. Journal of Anhui Agriculture University, 32, 278-282.Google Scholar
  5. Chu, M. X., Sang, L. H., Wang, J. Y., Fang, L. and Ye, S. C., 2005b. Study on BMP15 and GDF9 as candidate genes for prolificacy of Small Tailed Han sheep. Acta Genetica Sinica, 32, 38-45.PubMedGoogle Scholar
  6. Chu, M. X., Jiao, C. L., He, Y. Q.,Wang, J. Y., Liu, Z. H. and Chen, G. H., 2007. Association between PCR-SSCP of bone morphogenetic protein 15 gene and prolificacy in Jining grey goats. Animal Biotechnology, 18, 263–274.CrossRefPubMedGoogle Scholar
  7. Dai, R., 2004. Analyzed relationship between CLPG, BMP15 gene polymorphic and production performance of seven sheep populations in north of Xinjiang. (Master's Thesis Nanjing Agriculture University. [in Chinese])Google Scholar
  8. Davis, G. H., Montgomery, G. W., Allison, A. J., Kelly, R. W. and Bray, A. R., 1982. Segregation of a major gene influencing fecundity in progeny of Booroola sheep. New Zealand Journal of Agricultural Research, 25, 525–529.Google Scholar
  9. Davis, G. H., Galloway, S. M., Ross, I. K., Gregan, S. M., Ward, J., Nimbkar, B. V., Ghalsasi, P. M., Nimbkar, C., Gray, G. D., Subandriyo, Inounu, I., Tiesnamurti, B., Martyniuk, E., Eythorsdottir, E., Mulsant, P., Lecerf, F., James, P., Hanrahan, Bradford, G. E. and Wilson, T., 2002. DNA Tests in Prolific Sheep from Eight Countries Provide New Evidence on Origin of the Booroola (FecB) Mutation. Biology of Reproduction, 66, 1869-1874.CrossRefPubMedGoogle Scholar
  10. Davis, G. H., Balkrishnan, L., Ross, I. K., Wilson, T., Galloway, S. M., Lumsden, B. M., Hanrahan, J. P., Mullen, M., Mao, X. Z., Wang, G. L., Zhao, Z. S., Zeng, Y. Q., Robinson, J. J., Mavrogenis, A. P., Papachristoforou, C., Peter, C., Baumung, R., Cardyn, Baujenane, I., Cockett, N. E., Eythorsdottir, E., Arranz, J. J. and Notter, D. R., 2006. Investigation of the Booroola (Fec B) and Inverdale (Fec X I) muatation in 21 prolific breeds and strains of sheep samples in 13 countries. Animal Reproduction Science, 92, 87-96.CrossRefPubMedGoogle Scholar
  11. Dube, J. L., Wang, P., Elvin, J., Lyons, K. M., Celeste, A. J. and Matzuk, M. M., 1998. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Molecular Endocrinology, 12, 1809–1817.CrossRefPubMedGoogle Scholar
  12. Fabre, S., Pierre, A., Mulsant, P., Bodin, L., DiPasquale, E., Persani, L., Monget, P. and Monniaux, D., 2006. Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reproductive Biology and Endocrinology, 4, 20.CrossRefPubMedGoogle Scholar
  13. Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P., Jennifer, J. L., Jokiranta, S., McLaren, R. J., Luiro, K., Dodds, K. G., Montgomery, G. W., Beattie, A. E., Davis, G. H. and Ritvos, O., 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nature Genetics, 25, 279–283.CrossRefPubMedGoogle Scholar
  14. Guan, F., Shou-ren, L., Shi, G. Q. and Yang, L. G., 2007. Polymorphism of FecB gene in nine sheep breeds or strains and its effects on litter size, lamb growth and development. Animal Reproduction Science, 99, 44–52CrossRefPubMedGoogle Scholar
  15. Hanrahan, P. J., Gregan, S. M., Mulsant, P., Mullen, M., Davis, G. H., Powell, R. and Galloway, S. M., 2004. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biology of Reproduction, 70, 900–909.CrossRefPubMedGoogle Scholar
  16. Juengel, J. L., Hudson, N. L., Whiting, L. and McNatty, K. P., 2004. Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization, and pregnancy in ewes. Biology of Reproduction, 70, 557–561.CrossRefPubMedGoogle Scholar
  17. Liu, S. F., Jiang, Y. L. and Du, L. X., 2003. Studies of BMPR-IB and BMP15 as candidate genes for fecundity in little tailed han sheep. Yi Chuan Xue Bao [Acta Genetica Sinica], 30, 755-760Google Scholar
  18. McNatty, K. P., Lun, S., Heath, D. A., Ball, K., Smith, P., Hudson, N. L., McDiarmid, J., Gibb, M. and Henderson, K. M., 1986. Differences in ovarian activity between Booroola Merino ewes which were homozygous, heterozygous and non-carriers of a major gene influencing their ovulation rate. Journal of Reproduction and Fertility, 77, 193-205.PubMedCrossRefGoogle Scholar
  19. McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., Lawrence, S. B., Western, A., Meerasahib, M. F., Mottershead, D. G., Groome, N. P., Ritvos, O. and Laitinen, M. P., 2005. Bone morphogenetic protein 15 and growth differentiation factor 9 cooperate to regulate granulosa cell function. Reproduction, 129, 473–480.CrossRefPubMedGoogle Scholar
  20. Monteagudo, L. V., Ponz, R., Tejedor, M. T., Lavina, A. and Sierra, I., 2009. A 17 bp deletion in the Bone Morphogenetic Protein 15 (BMP15) gene is associated to increased prolificacy in the Rasa Aragonesa sheep breed. Animal Reproduction Science, 110, 139-146.CrossRefPubMedGoogle Scholar
  21. Newton, C. R., Graham, A., Heptinstall, L. E., Powell, S. J., Summers, C., Kalsheker, N., Smith, J. G. and Markham, A.F., 1989. Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Research, 17, 2503-2516.CrossRefPubMedGoogle Scholar
  22. Nimbkar, C., Ghalsasi, P. M., Ghatge, R. R. and Gray, G. D., 1998. Establishment of prolific Garole sheep from West Bengal in the semi-arid Deccan plateau of Maharashtra. In Proceedings of 6th World Congress on Genetics Applied to Livestock Production, Armidale, Australia, 1998, vol. 25, pp. 257–260.Google Scholar
  23. Piper, L. R. and Bindon, B. M., 1982. The Booroola Merino and the performance of medium non-peppin crosses at Armidale. In: Piper, L. R., Bindon, B. M., and Nethery, R. D. (Eds.), The Booroola Merino. Proceedings of a Workshop, Armidale, 24-25 August 1980, CSIRO, pp. 9–19.Google Scholar
  24. Polley, S., De, S., Batabyal, S., Kaushik, R., Yadav, P., Arora, J. S., Chattopadhyay, S., Pan, S., Brahma, B., Datta, T. K. and Goswami, S. L., 2009. Polymorphism of fecundity genes (BMPR1B, BMP15 and GDF9) in the Indian prolific Black Bengal goat. Small Ruminant Research, 85, 122–129.CrossRefGoogle Scholar
  25. Sambrook, J., and Russell, D., 2001. Molecular cloning. A laboratory manual 3rd ed. (Cold Spring Harbor Press, Cold Spring Harbor N.Y.)Google Scholar
  26. Souza, C. J., MacDougall, C., Campbell, B. K., McNeilly, A. S. and Baird, D. T., 2001. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. Journal of Endocrinology, 169, R1-R6.CrossRefPubMedGoogle Scholar
  27. Wang, G. L., Mao, X. Z., Davis, G. H., Zhao, Z. S., Zhang, L. J. and Zeng, Y. Q., 2003. DNA tests in Hu sheep and Han sheep (small tail) showed the existence of Booroola (FecB) mutation. Journal of Nanjing Agricultural University, 26, 104-106.Google Scholar
  28. Ye, S., Dhillon, S., Ke, X., Collins, A. R. and Day, I. N., 2001. An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Research, 29, e88–8.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Shamik Polley
    • 1
  • Sachinandan De
    • 1
  • Biswajit Brahma
    • 2
  • Ayan Mukherjee
    • 1
  • Vinesh P.V.
    • 1
  • Subhasis Batabyal
    • 3
  • Jaspreet Singh Arora
    • 1
  • Subhransu Pan
    • 3
  • Ashis Kumar Samanta
    • 3
  • Tirtha Kumar Datta
    • 1
  • Surender Lal Goswami
    • 1
  1. 1.Animal Biotechnology CentreNational Dairy Research InstituteKarnalIndia
  2. 2.Krishi Vigyan Kendra, SKUAST-JammuBhaderwahIndia
  3. 3.West Bengal University of Animal and Fishery SciencesKolkataIndia

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