Skip to main content
SpringerLink
Log in

GDF9 gene polymorphism and its association with litter size in two Russian sheep breeds

  • Published:
Rendiconti Lincei. Scienze Fisiche e Naturali Aims and scope Submit manuscript

Abstract

The purpose of this work was to study the GDF9 gene polymorphism in two sheep breeds raised in Russia and to identify its association with litter size. A variety of allelic variants of the GDF9 gene (GDF9/G1 and GDF9/G4 sites) in Salsk and Volgograd sheep breeds was studied. Mutations of the GDF9 gene that lead to improvement of reproductive traits in these sheep breeds were revealed. The obtained results of the alleles and genotypes frequencies for the GDF9 gene showed a low level of polymorphism at G1 and G4 sites. The studied populations were found to have high frequencies of G allele and GG genotype at G1 site and of A allele and AA genotype at G4 site of the GDF9 gene. Herewith all the individuals heterozygous at G1 site were also heterozygous at G4 site. Homozygous AA (G1) and GG (G4) genotypes in the study population were not observed. In the Salsk sheep population the individuals with AG genotype at G1 site had the highest fertility. A similar pattern was observed at G4 site. The litter size of Salsk sheep with GG genotype (G1) was 1.13. Among the Volgograd sheep, the individuals with AG genotype were also characterized by the highest fertility; the litter size of the individuals with the GG genotype (G1) was 1.22. A similar pattern was observed at G4 site. The litter size of animals with AG genotype was 1.88 and the AA genotype − 1.22. Thus, the positive and significant relation between the heterozygous AG/GDF9 genotype and litter size of animals has been established.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmadi A, Afraz F, Talebi R, Farahavar A, Vahidi SMF (2016) Investigation of GDF9 and BMP15 polymorphisms in Mehraban sheep to find the missenses as impact on protein. Iran J Appl Anim Sci 6:863–872

    Google Scholar 

  • Bravo S, Larama G, Paz E, Inostroza K, Montaldo HH, Sepulveda N (2016) Polymorphism of the GDF9 gene associated with litter size in Araucana creole sheep. Anim Genet 47:390–391

    Article  CAS  Google Scholar 

  • Davis GH (2005) Major genes affecting ovulation rate in sheep. Genet Sel Evol 37:S11–S23

    Article  CAS  Google Scholar 

  • 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 Genet 9:e1003482

    Article  CAS  Google Scholar 

  • Dong JW, Albertini DF, Nishimori K, Kumar TR, Lu NF, Matzuk MM (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531–535

    Article  CAS  Google Scholar 

  • Ernst LK, Zinovieva NA (2008) Biological problems of livestock production in XXI century. Acad Agric Sci, Moscow

    Google Scholar 

  • Fabre S, Pierre A, Mulsant P, Bodin L, Di Pasquale E, Persani L, Monget P, Monniaux D (2006) Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod Biol Endocrin 4:20

    Article  Google Scholar 

  • Galloway SM, McNatty KP, Cambridge LM, Laitinen MPE, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O (2000) Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 25:279–283

    Article  CAS  Google Scholar 

  • Gorlov IF, Fedunin AA, Randelin DA, Sulimova GE (2014) Polymorphisms of bGH, RORC, and DGAT1 genes in Russian beef cattle breeds. Russ J Genet 50:1302–1307

    Article  CAS  Google Scholar 

  • Gorlov IF, Shirokova NV, Randelin AV, Voronkova VN, Mosolova NI, Zlobina EY, Kolosov YA, Bakoev NF, Leonova MA, Bakoev SY, Kolosov AY, Getmantseva LV (2016) CAST/MspI gene polymorphism and its impact on growth traits of Soviet Merino and Salsk sheep breeds in the South European part of Russia. Turk J Vet Anim Sci 40:399–405

    Article  Google Scholar 

  • Gorlov IF, Kolosov YuA, Shirokova NV, Getmantseva LV, Slozhenkina MI, Mosolova NI, Bakoev NF, Leonova MA, Kolosov AYu, Zlobina EYu (2017) Association of the growth hormone gene polymorphism with growth traits in Salsk sheep breed. Small Rumin Res 150:11–14

    Article  Google Scholar 

  • Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM (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). Biol Reprod 70:900–909

    Article  CAS  Google Scholar 

  • Johnson RA, Bhattacharyya GK (2010) Statistics principles and methods, 6th edn. Wiley, USA

    Google Scholar 

  • Karagodina N, Kolosov Y, Usatov A, Bakoev S, Kolosov A, Leonova M, Shirokova N, Svyatogorova A, Getmantseva L (2014) Influence of various bio-stimulants on the biochemical and hematological parameters in porcine blood plasma. World Appl Sci J 30:723–726

    Google Scholar 

  • Kolosov Yu, Getmantseva L, Shirokova N (2013) Sheep breeding resources in Rostov region. World Appl Sci J 23:1322–1324

    Google Scholar 

  • Malyuchenko OP, YaI Alekseev, Monakhova YuA, Marzanova SN, Marzanov NS (2011) The study of molecular variability of the BMP15 and GDF9 fertility genes of the Romanov sheep breed. Proc RSAU 6:167–169

    Google Scholar 

  • Marchitelli C, Nardone A (2015) Mutations and sequence variants in GDF9, BMP15, and BMPR1B genes in Maremmana cattle breed with single and twin births. Rend Fis Acc Lincei 26:S553–S560

    Article  Google Scholar 

  • Martin P, Raoul J, Bodin L (2014) Effects of the FecL major gene in the Lacaune meat sheep population. Genet Sel Evol 46:48

    Article  Google Scholar 

  • Marzanov NS, Komkova EA, Maluchenko OP, YaI Alekseev, Ozerov MYu, Kantanen J, Lobkov VY, Marzanova LK, Astafyeva EE, Petrov SN, Kolpakov IN, Andryukhin AP, Adamian KK, Marzanova SN (2015) Characteristics of allele pool of Romanov breed sheep by different types of genetic markers. Problemy Biologii Produktivnyh Zhivotnyh 2:23–40

    Google Scholar 

  • McNatty KP, Smith P, Hudson NL, Heath DA, Tisdall DJ, WS O, Braw-Tal R (1995) Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. J Reprod Fertil Suppl 49:123–135

    CAS  Google Scholar 

  • Montgomery GW, Lord EA, Penty JM, Dodds KG, Broad TE, Cambridge L, Sunden SLF, Stone RT, Crawford AM (1994) The Booroola fecundity (FECB) gene maps to sheep chromosome-6. Genomics 22:148–153

    Article  CAS  Google Scholar 

  • Moradband F, Rahimi G, Gholizadeh M (2011) Association of polymorphisms in fecundity genes of GDF9, BMP15 and BMP15-1B with litter size in Iranian baluchi sheep. Asian-Australas J Anim Sci 24:1179–1183

    Article  CAS  Google Scholar 

  • Muhammad H, Iqbal Z, Bashir Q (2017) Genetic polymorphism among five species of Indus River carps on the basis of random amplified polymorphic DNA (RAPD) analysis. Rend Fis Acc Lincei 28:73–80

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Mol Phylogenet Evol 1:1–333

    Google Scholar 

  • Notter DR (2008) Genetic aspects of reproduction in sheep. Reprod Domest Anim 43:122–128

    Article  Google Scholar 

  • Paz E, Quinones J, Bravo S, Montaldo HH, Sepulveda N (2015) Genotyping of BMPR1B, BMP15 and GDF9 genes in Chilean sheep breeds and association with prolificacy. Anim Genet 46:98–99

    Article  CAS  Google Scholar 

  • Piper LR, Bindon BM (1983) The Booroola merino and the performance of medium non-peppin crosses at armidale. Wool Tech Sheep Bree 31:14

    Google Scholar 

  • Polley S, De S, Brahma B, Mukherjee A, Vinesh PV, Batabyal S, Arora JS, Pan S, Samanta AK, Datta TK, Goswami SL (2010) Polymorphism of BMPR1B, BMP15 and GDF9 fecundity genes in prolific Garole sheep. Trop Anim Health Pro 42:985–993

    Article  Google Scholar 

  • Ricordeau G, Thimonier J, Poivey JP, Driancourt MA, Hochereaudereviers MT, Tchamitchian L (1990) INRA research on the Romanov sheep breed in France: a review. Livest Prod Sci 24:305–332

    Article  Google Scholar 

  • Sadighi M, Bodensteiner KJ, Beattie AE, Galloway SM (2002) Genetic mapping of ovine growth differentiation factor 9 (GDF9) to sheep chromosome 5. Anim Genet 33:244–245

    Article  CAS  Google Scholar 

  • Shafieiyan Z, Mohammadi G, Jolodarzadeh A, Amiri S (2013) No mutations of FecB and FecG(H) in Iranian Lory sheep. Vet Res Forum 4:265–268

    Google Scholar 

  • Silva BDM, Castro EA, Souza CJH, Paiva SR, Sartori R, Franco MM, Azevedo HC, Silva TASN, Vieira AMC, Neves JP, Melo EO (2011) A new polymorphism in the growth and differentiation factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep. Anim Genet 42:89–92

    Article  CAS  Google Scholar 

  • Souza CJH, MacDougall C, Campbell BK, McNeilly AS, Baird DT (2001) The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J Endocrinol 169:R1–R6

    Article  CAS  Google Scholar 

  • Sulimova GE, Voronkova VN, Perchun AV, Gorlov IF, Randelin AV, Slozhenkina MI, Zlobina EY (2016) Characterization of the Russian beef cattle breed gene pools using inter simple sequence repeat DNA analysis (ISSR analysis). Russ J Genet 52:963–968

    Article  CAS  Google Scholar 

  • Wilson T, Wu XY, Juengel JL, Ross IK, Lumsden JM, Lord EA, Dodds KG, Walling GA, McEwan JC, O’Connell AR, McNatty KP, Montgomery GW (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. Biol Reprod 64:1225–1235

    Article  CAS  Google Scholar 

  • Xiao-Dan B, Ming-Xing C, Hai-Guo J, Li F, Su-Cheng Y (2005) Estrogen receptor as a candidate gene for prolificacy of small tail han sheep. Acta Genet Sin 32:1060–1065

    Google Scholar 

  • Mullen MP, Hanrahan JP, Howard DJ, Powell R (2013) Investigation of prolific sheep from UK and Ireland for evidence on origin of the mutations in BMP15 (FecX(G), FecX(B)) and GDF9 (FecG(H)) in Belclare and Cambridge sheep. PLoS One 8:e53172

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Russian Science Foundation for the financial support in the implementation of this research according to the scientific project # 15-16-10000, NIIMMP.

Author information

Authors and Affiliations

  1. Volga Region Research Institute of Manufacture and Processing of Meat-and-Milk Production, Rokossovskogo Street, 6, Volgograd, 400131, Russian Federation

    Ivan F. Gorlov, Nadezhda V. Shirokova, Marina I. Slozhenkina, Natali I. Mosolova & Elena Yu. Zlobina

  2. Volgograd State Technical University, Volgograd, 400005, Russian Federation

    Ivan F. Gorlov, Marina I. Slozhenkina & Natali I. Mosolova

  3. Laboratory of Molecular Diagnostics and Biotechnology of Farm Animals, Don State Agrarian University, Persianovsky, Rostov, 346493, Russian Federation

    Yuri A. Kolosov, Nadezhda V. Shirokova, Lyubov V. Getmantseva, Nekruz F. Bakoev, Maria A. Leonova & Anatoli Yu. Kolosov

  4. Volgograd State University, 100, University av., Volgograd, 400062, Russian Federation

    Elena Yu. Zlobina

Authors
  1. Ivan F. Gorlov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuri A. Kolosov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadezhda V. Shirokova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lyubov V. Getmantseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marina I. Slozhenkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natali I. Mosolova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nekruz F. Bakoev
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria A. Leonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anatoli Yu. Kolosov
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elena Yu. Zlobina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivan F. Gorlov.

Ethics declarations

Funding

This study was funded by the Russian Science Foundation (Grant number 15-16-10000 NIIMMP).

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gorlov, I.F., Kolosov, Y.A., Shirokova, N.V. et al. GDF9 gene polymorphism and its association with litter size in two Russian sheep breeds. Rend. Fis. Acc. Lincei 29, 61–66 (2018). https://doi.org/10.1007/s12210-017-0659-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12210-017-0659-2

Keywords

Search

Navigation