Advances in the subject of prolificacy genes or fertility in sheep: a review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i11.19333

Keywords:

Genetics; Heritability; Breeds; Reproduction.

Abstract

Reproductive traits relatively have low or medium heritability and do not exhibit a remarkable response to phenotypic selection. Therefore, the inclusion of genetic information from genes associated with reproductive capacity can efficiently improve the selection response. The main important genes affecting prolificacy and their genetic diversity in different breeds of sheep have been studied on a global scale. Where, different mutations associated with reproductive traits, including ovulation rate and litter size, have been found in various sheep breeds around the world. An overview of studies on major proliferation genes showed that some alleles may express different phenotypic effects in different breeds and therefore, further studies on interaction effects are needed for a greater understanding of the genetic control of reproduction in sheep. Regarding the evaluation methodology for prolificacy traits, the application of new technologies is necessary to find new variants, which is essential for future studies. The methodology adopted was a descriptive study, resulting in a literature review based on worldwide scientific articles.

References

Abdoli, R., Zamani, P., Deljou, A., & Rezvan, H. (2013). Association of BMPR-1B and GDF9 genes polymorphisms and secondary protein structure changes with reproduction traits in Mehraban ewes. Gene, 524(2), 296–303. https://doi.org/10.1016/j.gene.2013.03.133

Abdoli, R., Zamani, P., Mirhoseini, S. Z., Ghavi Hossein-Zadeh, N., & Nadri, S. (2016). A review on prolificacy genes in sheep. Reproduction in Domestic Animals, 51(5), 631–637. https://doi.org/10.1111/rda.12733

Ahmad, H. I., Liu, G., Jiang, X., Edallew, S. G., Wassie, T., Tesema, B., Yun, Y., Pan, L., Liu, C., Chong, Y., Yu, Z. J., & Jilong, H. (2017). Maximum-likelihood approaches reveal signatures of positive selection in BMP15 and GDF9 genes modulating ovarian function in mammalian female fertility. Ecology and Evolution, July, 8895–8902. https://doi.org/10.1002/ece3.3336

Barakat, I. A. H., Salem, L. M., Daoud, N. M., Khalil, W. K. B., & Mahrous, K. F. (2017). Genetic polymorphism of candidate genes for fecundity traits in Egyptian sheep breeds. Biomedical Research (India), 28(2), 851–857

Bastos, E., Ávila, S., Cravador, A., Renaville, R., Guedes-Pinto, H., & Luis Castrillo, J. (2006). Identification and characterization of four splicing variants of ovine POU1F1 gene. Gene, 382, 12–19. https://doi.org/10.1016/j.gene.2006.05.028

Bedhiaf-Romdhani, S., Djemali, M., Zaklouta, M., & Iniguez, L. (2008). Monitoring crossbreeding trends in native Tunisian sheep breeds. Small Ruminant Research, 74(1–3), 274–278. https://doi.org/10.1016/j.smallrumres.2007.07.008

Bodin, L., Di Pasquale, E., Fabre, S., Bontoux, M., Monget, P., Persani, L., & 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(1), 393–400. https://doi.org/10.1210/en.2006-0764

Ceko, M. J., Hummitzsch, K., Hatzirodos, N., Bonner, W. M., Aitken, J. B., Russell, D. L., Lane, M., Rodgers, R. J., & Harris, H. H. (2015). X-Ray fluorescence imaging and other analyses identify selenium and GPX1 as important in female reproductive function. Metallomics, 7(1), 71–82. https://doi.org/10.1039/c4mt00228h

Chu, M. X., Liu, Z. H., Jiao, C. L., He, Y. Q., Fang, L., Ye, S. C., Chen, G. H., & Wang, J. Y. (2007). Mutations in BMPR-IB and BMP-15 genes are associated with litter size in Small Tailed Han sheep (Ovis aries). Journal of Animal Science, 85(3), 598–603. https://doi.org/10.2527/jas.2006-324

Chu, M., Xiao, C., Feng, T., Fu, Y., Cao, G., Fang, L., Di, R., Tang, Q., Huang, D., Ma, Y., Li, K., & Li, N. (2012). Polymorphisms of KiSS-1 and GPR54 genes and their relationships with litter size in sheep. Molecular Biology Reports, 39(3), 3291–3297. https://doi.org/10.1007/s11033-011-1097-3

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., Hanrahan, J. P., Bradford, G. E., & 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(6), 1869–1874. https://doi.org/10.1095/biolreprod66.6.1869

Demars, J., Fabre, S., Sarry, J., Rossetti, R., Gilbert, H., Persani, L., Tosser-Klopp, G., Mulsant, P., Nowak, Z., Drobik, W., Martyniuk, E., & Bodin, L. (2013). Genome-Wide Association Studies Identify Two Novel BMP15 Mutations Responsible for an Atypical Hyperprolificacy Phenotype in Sheep. PLoS Genetics, 9(4). https://doi.org/10.1371/journal.pgen.1003482

Dias, F. C. F., Khan, M. I. R., Adams, G. P., Sirard, M. A., & Singh, J. (2014). Granulosa cell function and oocyte competence: Super-follicles, super-moms and super-stimulation in cattle. Animal Reproduction Science, 149(1–2), 80–89. https://doi.org/10.1016/j.anireprosci.2014.07.016

El-Seedy, A. S., Hashem, N. M., El-Azrak, K. M., Nour El-Din, A. N. M., Ramadan, T. A., Taha, T. A., & Salem, M. H. (2017). Genetic screening of FecB, FecXG and FecXI mutations and their linkage with litter size in Barki and Rahmani sheep breeds. Reproduction in Domestic Animals, 52(6), 1133–1137. https://doi.org/10.1111/rda.13002

Escobar-Chaparro, R. A., Guillén, G., Espejo-Galicia, L. U., Meza-Villalvazo, V. M., Peña-Castro, J. M., & Abad-Zavaleta, J. (2017). qPCR and HRM-based diagnosis of SNPs on growth differentiation factor 9 (GDF9), a gene associated with sheep (Ovis aries) prolificacy. 3 Biotech, 7(3). https://doi.org/10.1007/s13205-017-0837-z

Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P. E., Juengel, J. L., Jokiranta, T. S., McLaren, R. J., Luiro, K., Dodds, K. G., Montgomery, G. W., Beattie, A. E., Davis, G. H., & 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(3), 279–283. https://doi.org/10.1038/77033

Gholizadeh, M., Rahimi-Mianji, G., Nejati-Javaremi, A., De Koning, D. J., & Jonas, E. (2014). Genomewide association study to detect QTL for twinning rate in Baluchi sheep. Journal of Genetics, 93(2), 489–493. https://doi.org/10.1007/s12041-014-0372-1

Hanrahan, J. P., Gregan, S. M., Mulsant, P., Mullen, M., Davis, G. H., Powell, R., & 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(4), 900–909. https://doi.org/10.1095/biolreprod.103.023093

Kasiriyan, M. M., Hafezian, S. H., & Hassani, N. (2011). Genetic polymorphism BMP15 and GDF9 genes in Sangsari sheep of Iran. International Journal of Genetics and Molecular Biology, 3(1), 31–34

Khodabakhshzadeh, R., Mohammadabadi, M. R., Esmailizadeh, A. K., Moradi Shahrebabak, H., Bordbar, F., & Ansari Namin, S. (2016). Identification of point mutations in exon 2 of GDF9 gene in Kermani sheep. Polish Journal of Veterinary Sciences, 19(2), 281–289. https://doi.org/10.1515/pjvs-2016-0035

Lassoued, N., Benkhlil, Z., Woloszyn, F., Rejeb, A., Aouina, M., Rekik, M., Fabre, S., & Bedhiaf-Romdhani, S. (2017). FecX Bar a Novel BMP15 mutation responsible for prolificacy and female sterility in Tunisian Barbarine Sheep. BMC Genetics, 18(1), 1–10. https://doi.org/10.1186/s12863-017-0510-x

Li, Y. X., Zhang, J., Qian, Y., Meng, C. H., Wang, H. L., Tao, X. J., Zhong, S., Cao, S. X., & Li, Q. F. (2015). Molecular characterization, expression, polymorphism of NR5A2 and its relationship with litter size in Hu sheep. Genetics and Molecular Research, 14(4), 12765–12775. https://doi.org/10.4238/2015.October.19.20

Mahdavi, M., Nanekarani, S., & Hosseini, S. D. (2014). Mutation in BMPR-IB gene is associated with litter size in Iranian Kalehkoohi sheep. Animal Reproduction Science, 147(3–4), 93–98. https://doi.org/10.1016/j.anireprosci.2014.04.003

Martinez-Royo, A., Jurado, J. J., Smulders, J. P., Martí, J. I., Alabart, J. L., Roche, A., Fantova, E., Bodin, L., Mulsant, P., Serrano, M., Folch, J., & Calvo, J. H. (2008). A deletion in the bone morphogenetic protein 15 gene causes sterility and increased prolificacy in Rasa Aragonesa sheep. Animal Genetics, 39(3), 294–297. https://doi.org/10.1111/j.1365-2052.2008.01707.x

McNatty, K. P., Galloway, S. M., Wilson, T., Smith, P., Hudson, N. L., O’Connell, A., Bibby, A. H., Heath, D. A., Davis, G. H., Hanrahan, J. P., & Juengel, J. L. (2005). Physiological effects of major genes affecting ovulation rate in sheep. Genetics Selection Evolution, 37(SUPPL. 1), 25–38. https://doi.org/10.1051/gse:2004029

Meistertzheim, A.-L., Meistertzheim, A.-L., Calves, I., Artigaud, S., Friedman, C. S., Paillard, C., Laroche, J., & Ferec, C. (2012). High Resolution Melting Analysis for fast and cheap polymorphism screening of marine populations. Protocol Exchange. https://doi.org/10.1038/protex.2012.015

Miao, X., & Qin, Q. L. X. (2015). Genome-wide transcriptome analysis of mRNAs and microRNAs in Dorset and Small Tail Han sheep to explore the regulation of fecundity. Molecular and Cellular Endocrinology, 402, 32–42. https://doi.org/10.1016/j.mce.2014.12.023

Moghadaszadeh, M., Mohammadabadi, M., & Koshkoieh, A. E. (2015). Association of exon 2 of BMP15 gene with the litter size in the Raini Cashmere goat. Genetics in the Third Millennium, 13(3), 4062–4067

Monteagudo, L. V., Ponz, R., Tejedor, M. T., Laviña, A., & 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(1–2), 139–146. https://doi.org/10.1016/j.anireprosci.2008.01.005

Mulsant, P., Lecerf, F., Fabre, S., Schibler, L., Monget, P., Lanneluc, I., Pisselet, C., Riquet, J., Monniaux, D., Callebaut, I., Cribiu, E., Thimonier, J., Teyssier, J., Bodin, L., Cognié, Y., Chitour, N., & Elsen, J. M. (2001). Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Mérino ewes. Proceedings of the National Academy of Sciences of the United States of America, 98(9), 5104–5109. https://doi.org/10.1073/pnas.091577598

Nicol, L., Bishop, S. C., Pong-Wong, R., Bendixen, C., Holm, L. E., Rhind, S. M., & McNeilly, A. S. (2009). Homozygosity for a single base-pair mutation in the oocyte-specific GDF9 gene results in sterility in Thoka sheep. Reproduction, 138(6), 921–933. https://doi.org/10.1530/REP-09-0193

Ozmen, O., Seker, I., Ertugrul, O., Ozkan, E., & Tekin, N. (2011). Prolactin receptor (PRLR) gene polymorphism in Chios, White Karaman and Awassi sheep breeds. Archives Animal Breeding, 54(4), 381–390. https://doi.org/10.5194/aab-54-381-2011

Polley, S., De, S., Brahma, B., Mukherjee, A., P.V., V., Batabyal, S., Arora, J. S., Pan, S., Samanta, A. K., Datta, T. K., & Goswami, S. L. (2010). Polymorphism of BMPR1B, BMP15 and GDF9 fecundity genes in prolific Garole sheep. Tropical Animal Health and Production, 42(5), 985–993. https://doi.org/10.1007/s11250-009-9518-1

Reed, G. H., Kent, J. O., & Wittwer, C. T. (2007). High-resolution DNA melting analysis for simple and efficient molecular diagnostics. Pharmacogenomics, 8(6), 597–608. https://doi.org/10.2217/14622416.8.6.597

Roy, J., Polley, S., De, S., Mukherjee, A., Batabyal, S., Pan, S., Brahma, B., Datta, T. K., & Goswami, S. L. (2011). Polymorphism of fecundity genes (fecb, fecx, and fecg) in the indian bonpala sheep. Animal Biotechnology, 22(3), 151–162. https://doi.org/10.1080/10495398.2011.589239

Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108. https://doi.org/10.1038/nprot.2008.73

Silva, B. D. M., Castro, E. A., Souza, C. J. H., Paiva, S. R., Sartori, R., Franco, M. M., Azevedo, H. C., Silva, T. A. S. N., Vieira, A. M. C., Neves, J. P., & Melo, E. O. (2011). A new polymorphism in the Growth and Differentiation Factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep. Animal Genetics, 42(1), 89–92. https://doi.org/10.1111/j.1365-2052.2010.02078.x

Souza, C. J. H., MacDougall, C., Campbell, B. K., McNeilly, A. S., & 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(2), 3–8. https://doi.org/10.1677/joe.0.169R001

Souza, C. J. H., McNeilly, A. S., Benavides, M. V., Melo, E. O., & Moraes, J. C. F. (2014). Mutation in the protease cleavage site of GDF9 increases ovulation rate and litter size in heterozygous ewes and causes infertility in homozygous ewes. Animal Genetics, 45(5), 732–739. https://doi.org/10.1111/age.12190

Sudhakar, A., Rajendran, R., & Rahumathulla, P. S. (2013). Detection of Booroola (FecB) mutation in Indian sheep--Nilagiri. Small Ruminant Research, 113(1), 55–57. https://doi.org/10.1016/j.smallrumres.2013.02.012

Våge, D. I., Husdal, M., Kent, M. P., Klemetsdal, G., & Boman, I. A. (2013). A missense mutation in growth differentiation factor 9 (GDF9) is strongly associated with litter size in sheep. BMC Genetics, 14, 1–8. https://doi.org/10.1186/1471-2156-14-1

Wilson, T., Wu, X. Y., Juengel, J. L., Ross, I. K., Lumsden, J. M., Lord, E. A., Dodds, K. G., Walling, G. A., McEwan, J. C., O’Connell, A. R., McNatty, K. P., & Montgomery, G. W. (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biology of Reproduction, 64(4), 1225–1235. https://doi.org/10.1095/biolreprod64.4.1225

Zuo, B., Qian, H., Wang, Z., Wang, X., Nisa, N., Bayier, A., Ying, S., Hu, X., Gong, C., Guo, Z., & Wang, F. (2013). A study on BMPR-IB genes of Bayanbulak sheep. Asian-Australasian Journal of Animal Sciences, 26(1), 36–42. https://doi.org/10.5713/ajas.2012.12238

Published

22/08/2021

How to Cite

MACIEL, M. dos S. .; RIBEIRO, A. G. .; CALVACANTE, P. O. S. .; CARVALHO, C. B. de M. .; MARINHO, J. B. M. .; MACAMBIRA, G. M. .; OLIVEIRA, H. S. de H. .; SILVA, D. A. da .; SANTOS, A. C. F. dos .; PESSOA, D. V. .; SILVA, G. D. .; CARVALHO, Y. C. V. de . Advances in the subject of prolificacy genes or fertility in sheep: a review. Research, Society and Development, [S. l.], v. 10, n. 11, p. e67101119333, 2021. DOI: 10.33448/rsd-v10i11.19333. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/19333. Acesso em: 5 nov. 2024.

Issue

Section

Agrarian and Biological Sciences