New insights into polymorphisms in candidate genes associated with incidence to repeat breeder in Italian buffaloes (Bubalus bubalis)


Published: Jul 5, 2025
Keywords:
Italian buffaloes candidate gene repeat breeder
A Ateya
FA Safhi
AR Alhimaidi
AA Ammari
RA Amran
B Marghani
SI Rakha
S Sakr
H El-Emam
Abstract

This study looked at the reproductive genes that could interact with repeat breeder incidence in Italian buffaloes. Two hundred and forty female Italian buffaloes (120 repeat breeder and 120 apparently normal) were used. Blood samples were collected from each buffalo into tubes encompassing EDTA anticoagulant to isolate DNA. PCR-DNA sequencing elicited nucleotide sequence differences between normal and repeat breeder buffaloes for the reproductive (MFSD14A, PALMD, VPS13B, BMP, MTNR1A, TSHR, CSGALNACT1, CADM2, ZNF503, KRR1, MTPN, IGFBP7, LEP, and ABCC4) genes. The likelihood of dissemination of all notable nucleotide variations varied noticeably between buffalo groups with and without repeat breeders, depending on Fisher's exact test (p˂ 0.01). All of the reproductive markers under research had the exonic region mutations in repeat breeder buffaloes versus normal ones. The results may confirm the importance of these markers' nucleotide variations as candidates for repeat breeder occurrence and offer a practical buffalo management strategy.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Abbas, H. S., El-Magd, M. A., El-Bayomi, K. M. & Sosa, G. A. (2014).
Detection of SNPs in exon7 locus of Cyp19 gene and their association
with anestrus in Egyptian buffaloes (Bubalus bubalis). Benha
Veterinary Medical Journal, 26, 151–160.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D. J.
(1990). Basic local alignment search tool. Journal of Molecular
Biology, 215, 403–410.
Ashwell, M.S., Rexroad Jr, C. E., Miller, R. H., Van Raden, P.M. & Da,
Y. (1997). Detection of loci affecting milk production and health
traits in an elite US Holstein population using microsatellite markers.
Animal Genetics, 28, 216-222.
Baloza, S. H., Abo-Salem, M. E. S. & Hemeda, S. A. (2017). Effect
of genetic variations in BMP 4 gene (exon 2 plus part of intron 2)
on infertility in Egyptian Buffalo cows.Benha Journal of Applied
Sciences, 2, 37–41.
Barrett, P., Ebling, F. J. P., Schuhler, S., Wilson, D., Ross, A.W., Warner,
A, Jethwa, P., Boelen, A., Visser, T. J., Ozanne, D. M. (2007). Hypothalamic
thyroid hormone catabolism acts as a gatekeeper for the
seasonal control of body weight and reproduction. Endocrinology,
, 3608–17.
Berry, D.P. & Evans, R. (2014). Genetics of reproductive performance
in seasonal calving beef cows and its association with performance
traits. Journal of Animal Science, 92, 1412–1422.
Bishop, M. D., Hawkins, G.A. & Keeler, C.L. (1995). Use of DNA
markers in animal selection. Theriogenology, 43, 61-70.
Boesenberg-Smith, K. A., Pessarakli, M. M. & Wolk, D. M. (2012).
Assessment of DNA Yield and Purity: An Overlooked Detail of
PCR Troubleshooting. Clinical Microbiology Newsletter, 34, 1–6.
Boichard, D. (1990). Estimation of the economic value of conception
rate in dairy cattle.Livestock Production Science Journal, 24,
–204.
Boom, R., Sol, C. J., Salimans, M. M. & Jansen, C. L. (1990). Wertheim-
van Dillen PM, Noordaa JVD. Rapid and simple method for
purification of nucleic acids. Journal of Clinical Microbiology,
, 495–503.
Buch, L.H., Kargo, M., Berg, P., Lassen, J. & Sørensen A. C. (2012).
The value of cows in reference populations for genomic selection
of new functional traits. Animals, 6, 880–886.
Cammack, K., Thomas, M. & Enns, R. (2009). Reproductive traits and
their heritabilities in beef cattle. The Professional Animal Scientist
Journal, 25, 517–528.
Capitan, A., Michot, P., Baur, A., Saintilan, R., Hoze, C., Valour, D.,
Guillaume, F., Boichon, D., Barbat, A. &Boichard, D. (2014). Genetic
tools to improve reproduction traits in dairy cattle. Reproduction
Fertility Development, 27, 14–21.
Casey, O. M., Fitzpatrick, R., Mcinerney, J. O., Morris, D. G., Powell,
R., &Sreenan, J. M. (2004). Analysis of gene expression in
the bovine corpus luteum through generation and characterisation
of 960 ESTs.Biochimica et Biophysica Acta - Gene Structure and
Expression, 1679, 10–7
Chang, H., Brown, C.B. &Matzuk, M.M. (2002). Genetic analysis of the
Mammalian transforming growth factor superfamily. Endocrinology
Reviews, 23,787–823.
Chang, S. L., Liu, Y. C., Chen, S. Y., Huang, T. H., Liu, P. T. & Liu, F.
C. (2013). Identification of two evolutionarily conserved 5′ cis-elements
involved in regulating spatiotemporal expression of Nolz-1
during mouse embryogenesis. PLOS One, 8, e54485.
Chen, Y., Arthur, P. F., Barchia, I. M., Quinn, K., Parnell, P. F., Herd, R.
M. (2012). Using gene expression information obtained by quantitative
real-time PCR to evaluate Angus bulls divergently selected
for feed efficiency. Animal Production Science, 52, 1058–67.
Chu, D. & Wei, L. (2019). Nonsynonymous, synonymous and nonsense
mutations in human cancer-related genes undergo stronger purifying
selections than expectation. BMC Cancer, 19, 359.
Dakal, T.C., Kala, D., Dhiman, G., Yadav, V., Krokhotin, A. &Dokholyan,
N.V. (2017). Predicting the functional consequences of
non-synonymous single nucleotide polymorphisms in IL8 gene.
Scientific Reports, 7, 6525.
Das, G.K. & Khan, F.A. (2010). Summer anestrus in buffalo-A review.
Reproduction in Domestic Animals,45:e483-e494.
Day, F. R., Hinds, D. A., Tung, J. Y., Stolk, L., Styrkarsdottir, U., Saxena,
R., Bjonnes, A., Broer, L., Dunger, D. B. & Halldorsson, B. V. et
al. (2015). Causal mechanisms and balancing selection inferred
from genetic associations with polycystic ovary syndrome. Nature
Communication, 6, 8464.
De Camargo, G. M., Aspilcueta-Borquis, R. R., Fortes, M. R., Porto-
Neto, R., Cardoso, D. F., Santos, D. J., Lehnert, S. A., Reverter,
A., Moore, S. S. &Tonhati, H. (2015). Prospecting major genes in
dairy buffaloes. BMC Genomics, 16, 872.
Dekkers, J. (1991). Estimation of economic values for dairy cattle breeding
goals: bias due to sub-optimal management policies. Livestock
Production Science Journal, 29, 131–149.
Devkota, B., Shah, S. & Gautam, G. (2022). Reproduction and Fertility
of Buffaloes in Nepal. Animals. 13, 70.
Doran, J., Walters, C., Kyle, V., Wooding, P., Hammett-Burke, R.
&Colledge, W.H. (2016). Mfsd14a (Hiat1) gene disruption causes
globozoospermia and infertility in male mice. Reproduction, 152,
– 99.
Dubocovich, M. L., Cardinali, D. P., Delagrange, P. R. M., Krause,
D. N., Strosberg,D. &. Sugden, D. (2000). Melatonin Receptors.
In Girdlestone, D. (ed.) The IUPHAR Compendium of Receptor
Characterization and Classifcation, 2nd ed. London, UK. 270-277.
El-Bayomi, K. M., Saleh, A. A., Awad, A., El-Tarabany, M. S., El-Qaliouby,
H. S., Afifi, M., El-Komy, S., Essawi, W. M., Almadaly,
E.A. & El-Magd, M. A. (2018). Association of CYP19A1 gene
polymorphisms with anoestrus in water buffaloes. Reproduction
and Fertility Development, 30, 487-497.
El-Debaky, H., Mahmoud, K. M., Abd El-Razik, K. A., Sosa, A. S. A.,
Kandiel, M. M. M. & Ahmed, Y. F. (2020). PCR-SSCP and Sequencing
Analysis for Studying Leptin Gene Polymorphism and Its
Association with Reproductive Status of Egyptian Buffalo. Egyptian
Journal of Veterinary Science, 51, 11-21.
Feitosa, F. L. B., Pereira, A. S. C., Venturini, G. C., Tonussi, R. L., Espigolan,
R., & Gordo, D. M. et al. (2014). Genome wide association
study between copy number variation regions with marbling score
in Nelore cattle. In: Proceedings, 10th World Congress of Genetics
Applied to Livestock Production. Vancouver.
Fouda, M., Hemeda, S., El-Bayomi, K., El-Araby, I., Hendam, B. &
Ateya, A. (2021). Genetic polymorphisms in FSHR/ALUI and ESRα
/BG1I loci and their association with repeat breeder incidence in
buffalo. Journal of the Hellenic Veterinary Medical Society, 72,
-2878.
Fu, Y.F., Li, L., Li, B., Fang, X. & Ren, S. (2016). Long form leptin
receptor and SNP effect on reproductive traits during embryo attachment
in Suzhong sows. Animal Reproduction Science, 168, 57–65.
Heidari, M., Kafi, M., Mirzaei, A., Asaadi, A. & Mokhtari, A. (2019).
Effects of follicular fluid of preovulatory follicles of repeat breeder
dairy cows with subclinical endometritis on oocyte developmental
competence. Animal Reproduction Science, 205, 62–69.
Ibrahim, A. H. M. (2019). Association of growth performance and body
conformational traits with BMP4 gene variation in Barki lambs.
Growth Factors, 37, 153–163.
Işık, E., Beck, P. P., Campi, I., Özon, A., Alikaşifoğlu, A., Gönç, N. &
Kandemir N. (2013). Thyroid hormone resistance: a novel mutation
in thyroid hormone receptor beta (THRB) gene - case report. Turkish
Journal of Pediatrics. 55, 322–7
Jorgez, C. J., Klysik, M., Jamin, S. P., Behringer, R. R., &Matzuk, M.
M. (2004). Granulosa cell specific inactivation of follistatin causes
female fertility defects. Molecular Endocrinology, 18, 953–67.
Karsch, F. J., Bittman, E. L., Foster, D. L., Goodman, R. L., Legan,
S. J. & Robinson, J. E. (2013). Neuroendocrine basis of seasonal
reproduction. Recent Progress in Hormone Research, Academic
Press, New York, USA.
Kato, M. V. (2000). A secreted tumor-suppressor, mac25, with activin-
binding activity. Molecular Medicine, 6, 126–35
Kavita, K., Phogat, J. B., Pandey, A. K., Balhara, A. K., Ghuman, S. S.
& Gunwant, P. (2018). Effects of melatonin supplementation prior
to Ovsynch protocol on ovarian activity and conception rates in
anestrous Murrah bufalo heifers during out of breeding season.
Reproductive Biology, 18, 161-168.
Kishigami, S. & Mishina, Y. (2005). BMP signaling and early embryonic
patterning. Cytokine Growth Factor Reviews, 16, 265– 278.
Kukurba, K. R. & Montgomery, S. B. (2015). RNA Sequencing and
Analysis. Cold Spring Harbor Protocols, 13, 951-69.
Kumar, R., Ghosh, M., Kumar, N., Balhara, A. K., Gupta, M., Sharma,
R. K. & Singh, I. (2017). Polymorphism in 5’ untranslated region
of heat-shock protein 70 gene as marker of post-partum anoestrus
in Murrah buffaloes. Reproduction Domestic Animal, 52, 505-512.
Lappalainen, T., Sammeth, M., Friedlander, M. R., Hoen, P. A, Monlong,
J., Rivas, M. A., Gonzalez-Porta, M., Kurbatova, N., Griebel, T. &
Ferreira, P. G. et al. (2013). Transcriptome and genome sequencing
uncovers functional variation in humans. Nature, 501, 506–11.
Lappalainen, T., Sammeth, M., Friedlander, M. R., Hoen, P. A., Monlong,
J., Rivas, M. A., Gonzalez-Porta, M., Kurbatova, N., Griebel,
T. & Ferreira, P. G. et al. (2013). Transcriptome and genome
sequencing uncovers functional variation in humans. Nature, 501,
–11.
Lari, A. M., Mohebbi-Fani, M. & Rowshan-Ghasrodashti, A. (2012).
Causes of culling in dairy cows and its relation to age at culling and
interval from calving in Shiraz, Southern Iran. Veterinary Research
Forum, 3, 233–237.
Latifah, L. & Saa N.R. (2021). Single nucleotide Polymorphism gen
BMP4 pada kambingberdasarkan data GenBank. Journal of Tropical
Animal Research, 2,1, 24–29
Li, J., Liu, J., Campanile, G., Plastow, G., Zhang, C., Wang, Z., Cassandro,
M., Gasparrini, B., Salzano, A., Hua, G., Liang, A. & Yang, L.
(2018). Novel insights into the genetic basis of buffalo reproductive
performance. BMC Genomics, 9, 814.
Li, J., Liu, X., Yang, J., Wang, H., Jiang, J., Liu, L., He, S., Ding,
X., Liu, J. & Zhang, Q. (2014). Targeted resequencing of GWAS
loci reveals novel genetic variants for milk production traits. BMC
Genomics, 15, 1–9.
Liu, J. J., Liang, A. X., Campanile, G., Plastow, G., Zhang, C., Wang, Z.,
Salzano, A., Gasparrini, B., Cassandro., M. & Yang, L. G. (2018).
Genome-wide association studies to identify quantitative trait loci
affecting milk production traits in water buffalo. Journal of Dairy
Science, 101, 433-444.
Mahrous, K. F., El-Kader, H. A. M., Abdelhafez, M. A., Aboelenin, M.
M., Balabel, E. A., Mabrouk, D. M., El Malky, O. M. &Hassanan,
M. S. (2022). Genetic structure of some candidate genes of repeat
breeder syndrome in Egyptian buffaloes. Journal of genetic engineering
and biotechnology, 20, 110.
Makina, S. O., Muchadeyi, F. C., Van Marle-Koster, E., Taylor, J. F.,
Makgahlela, M. L., &Maiwashe, A. (2015). Genome-wide scan for
selection signatures in six cattle breeds in South Africa. Genetics
Selection Evolution, 47, 92.
Malpaux, B., Migaud, M., Tricoire, H. &Chemineau, P. (2001). Biology
of mammalian photoperiodism and the critical role of the pineal
gland and melatonin. Journal of Biological Rhythms. 16, 336-347.
Martínez-Montes, A. M., Fernandez, A., Pérez-Montarelo, D., Alves,
D., Benitez, R., Nunez, Y., Ovilo, C., Ibañez-Escriche, N., Folch,
J. & Fernandez, A. (2017). Using RNA-Seq SNP data to reveal
potential causal mutations related to pig production traits and RNA
editing. Animal Genetics, 48, 151–165.
Moioli, B., Scatà, M. C., Steri, R., Napolitano, F. & Catillo, G. (2013).
Signatures of selection identify loci associated with milk yield in
sheep. BMC Genetics, 14, 76.
Moioli, B., Scatà, M., Catillo, G., Napolitano, F. & Pilla, F. (2013).
Whole-genome genotyping for detecting mutations in the genes
that are directly responsible for the trait variation. Page P0621 in
Proc. Plant and Animal Genome XXI, San Diego, CA.
Morfeld, K. A. & Brown, J. L. (2014). Ovarian acyclicity in zoo African
elephants (Loxodonta africana) is associated with high body condition
scores and elevated serum insulin and leptin. Reproduction,
Fertility and Development, 28, 640–7.
Musunuru, K., Strong, A., Frank-Kamenetsky, M., Lee, N. E., Ahfeldt,
T., Sachs, K.V., Li, X., Li, H., Kuperwasser, N,& Ruda, V. M.
(2010). From noncoding variant to phenotype via SORT1 at the
p13 cholesterol locus. Nature, 466, 714–9.
Muttukrishna, S., Tannetta, D., Groome, N., & Sargent I. (2004). Activin
and follistatin in female reproduction. Molecular and Cellular
Endocrinology, 225, 45–56.
Ortiz, W. H., Quirino, C. R., Silva, A., Oliveira, C. S., Serapiao, R. V.,
Pacheco, A. &Bartholazzi, A. (2015). Association between BMP4
gene polymorphism and in vitro embryo production traits in Gyr
cows.Revista Colombiana de CienciasPecuarias, 28, 156–164.
Otsuka, F., Yamamoto, S., Erickson, G. F. & Shimasaki, S. (2001).
Bonemorphogenetic protein-15 inhibits follicle stimulating hormone
(FSH) action by suppressing FSH receptor expression. Journal of
Biological Chemistry, 276, 11387-11392
Pal, A. & Chakravarty, A. K. (2020). Disease resistance for different
livestock species. Genetics and Breeding for Disease Resistance
of Livestock, 19, 271–96.
Parmeggiani, A., Di Palo, R., Zicarelli, L., Campanille, G., Esposito,
L., Seren, E., Accorsi, P. A &Sofai, S. M. (1994). Melatonin and
reproductive seasonality in the bufalo cow. Agricoltura Ricerca,
, 41-48
Ramadan, S. I., Abo-Gamil, Z. H. & El-Qaliouby, H. S. (2018). Polymorphism
of IGF-1 and Its Receptor (IGF-1R) Genes and Their
Association with Fertility Problems of Egyptian Buffaloes. Alexandria
Journal of Veterinary Sciences, 59, 119-124.
Rangashamaiah, M. M., Ghuman, S. S. & Cheema, R. (2022). Association
of melatonin receptor 1a (MTNR1A) gene polymorphism
with seasonal suppression of fertility in buffaloes. Buffalo Bulletin,
, 749-763.
Refsdal, A.O. (2000). To treat or not to treat: a proper use of hormones
and antibiotics. Animal Reproduction Science, 60, 109–19.
Regmi, G.& Dhakal, I.P. (2020). Systemic levels of iron, phosphorus,
and total protein in normocyclic versus repeat breeder Holstein
Friesian crossbred cows of Kesharbag, Chitwan. Nepalese Veterinary
Journal, 13, 2353-2357.
Reshma, R., Mishra, S. R., Thakur, N., Parmar, M. S., Somal, A., Bharti,
M. K., Pandey, S., Chandr, V., Chouhan, V. S., Verma, M. R., Singh,
G., Sharm, G. T., Maurya, V. P.&Sarkara,M. (2016). Modulatory role
of leptin on ovarian functions in water bufalo (Bubalus bubalis).
Theriogenology, 86, 1720–1739.
Roberts, A.B. & Sporn, M. B. (1990). The transforming growth factors.
In: Sporn, M.B., Roberts, A.B. (Eds.), Peptide Growth Factors and
Their Receptors, Part I. Springer-Verlag Berlin, 419–472.
Roxström, A. & Strandberg, E. (2002). Genetic analysis of functional,
fertility-, mastitis-, and production-determined length of productive
life in Swedish dairy cattle.Livestock Production Science Journal,
–135.
Sammad, A., Khan, M. Z., Abbas, Z., Hu, L., Ullah, Q., Wang, Y., Zhu,
H. & Wang, Y. (2022). Major Nutritional Metabolic Alterations
Influencing the Reproductive System of Postpartum Dairy Cows.
Metabolites, 12, 60.
Sanger, F., Nicklen, S. & Coulson, A. R. (1997). DNA sequencing
with chain-terminating inhibitors. The Proceedings of the National
Academy of Sciences, USA, 74, 5463–5467.
Schaeffer, L. R. (2006). Strategy for applying genome-wide selection
in dairy cattle. Journal of Animal Breeding and Genetics, 123,
–223.
Seo, H., Choi, Y., Shim, J., Yoo, I., & Ka, H. (2014). Prostaglandin
Transporters ABCC4 and SLCO2A1 in the Uterine Endometrium
and Conceptus During Pregnancy in Pigs. Biology of Reproduction,
, 5.
Seo, M., Lee, H. J., Kim, K., Caetano-Anolles, K., Jeong, J.Y., Park, S.,
Oh, Y. K., Cho, S. & Kim, H. (2016). Characterizing milk production
related genes in Holstein using RNA-seq. Asian-australas. Journal
of Animal Science, 29, 343.
Shahi, P., Slorach E.M., Wang, C.Y., Chou, J., Lu, A., Ruderisch, A.
& Werb, Z. (2015). The transcriptional repressor ZNF503/Zeppo2
promotes mammary epithelial cell proliferation and enhances cell
invasion. Journal Biological Chemistry, 290, 3803–13.
Shao, B., Sun, H., Ahmad, M. J., Ghanem, N., Abdel-Shafy, H., Du, C.,
Deng, T., Mansoor, S., Zhou, Y., Yang, Y., Zhang, S., Yang, L. &
Hua, G. (2021). Genetic features of reproductive traits in bovine
and Buffalo: lessons from bovine to Buffalo. Frontiers in Genetics,
, 617128.
Song, L. J., Wu, J. F., Yang, Z. B., Guo, L., Zhang S. J. & Wu, J.J.
(2013). Investigation of transferability of BovineSNP50 BeadChip
from cattle to water buffalo for genome wide association study.
Molecular Biology Reports, 40, 743–50.
Sosa, A. S. A, Mahmoud, K. M., Kandiel, M. M. M., Eldebaky, H.
A. A., Nawito, M. F. & Abou El Roos, M. E. A. (2016). Genetic
Polymorphism of Luteinizing Hormone Receptor Gene in Relation
to Fertility of Egyptian Buffalo.Biotechnology Journal, 12, 1-11.
Spencer, T. E., Forde, N., Dorniak, P., Hansen, T. R., Romero, J. J. &
Lonergan, P. (2013). Conceptus-derived prostaglandins regulate
gene expression in the endometrium prior to pregnancy recognition
in ruminants. Reproduction, 146, 377–87.
Sreedharan, S., Stephansson, O., Schiöth, H. B. & Fredriksson, R.
(2011). Long evolutionary conservation and considerable tissue
specificity of several atypical solute carrier transporters. Gene,
, 11–18.
Sun, R. Z., Lei, L., Cheng, L., Jin, Z. F., Zu, S. J. & Shan, Z. Y. (2010).
Expression of GDF-9, BMP-15 and their receptors in mammalian
ovary follicles. Journal of Molecular Histology, 41, 325–32.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: Molecular
Evolutionary Genetics Analysis (MEGA) Software Version 4.0.
Molecular Biology Evolution, 24, 1596–1599.
Tanwar, P.S. & McFarlane, J.R. (2011). Dynamic expression of bone
morphogenetic protein 4 in reproductive organs of female mice.
Reproduction, 142, 573–9.
Van den Berg, I., Fritz, S., Rodriguez, S., Rocha, D., Boussaha, M.,
Lund, M. S. &Boichard, D. (2014). Concordance analysis for QTL
detection in dairy cattle: A case study of leg morphology. Genetics
Selection Evolution, 46, 31.
Wandji, S. A., Gadsby, J. E, Barber, J. A, & Hammond, J. M. (2000).
Messenger ribonucleic acids for IGFBP-7 and connective tissue
growth factor (CTGF) are inversely regulated during folliculogenesis
and early luteogenesis. Journal of Endocrinology, 141, 2648–57.
Wang, L. & Wang, Y. (2012). Molecular characterization, expression
patterns and subcellular localization of Myotrophin (MTPN) gene
in porcine skeletal muscle. Molecular Biology Reproduction, 39,
–8.
Warriach, H. M., Mcgill, D.M., Bush, R.D., Wynn, P.C. & Chohan,
K.R. (2015). A review of recent developments in buffalo reproduction
- a review. Asian-Australasian Journal of Animal Sciences,
, 451–455.
Watanabe, Y., Takeuchi, K., Onaga, S. H., Sato, M., Tsujita, M., Abe,
M., Natsume, R., Li, M., Furuichi, T. & Saeki, M. (2010). Chondroitin
sulfate N-acetylgalactosaminyltransferase-1 is required for
normal cartilage development. Biochemistry Journal, 432, 47–55.
Whitworth, K. M., Zhao, J., Spate, L. D., Li, R. & Prather, R. S.
(2011). Scriptaid corrects gene expression of a few aberrantly reprogrammed
transcripts in nuclear transfer pig blastocyst stage
embryos. Cellular Reprogramming, 13, 191–204.
Wiles, J.R., Katchko, R.A., Benavides, E.A., O’Gorman, C.W., Escudero,
J.M., Keisler, D.H., Stanko, R.L., & Garcia, M.R. (2014).
The effect of leptin on luteal angio‑ genic factors during the luteal
phase of the estrous cycle in goats. Animal Reproduction Science,
, 121–129.
Yusuf, M., Toshihiko, N., Ranasinghe, B., Gautam, G., Long, S., Yoshida,
C., Koike, K. & Hayashi, A. (2010). Reproductive performance
of repeat breeders in dairy herds. Theriogenology, 73, 1220-1229.
Most read articles by the same author(s)