Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Genetic variability detected at the lactoferrin locus (LTF) in the Italian Mediterranean river buffalo

Alfredo Pauciullo A B , Luigi Ramunno C F , Nicolò P. P. Macciotta D , Giustino Gaspa D , Angelo Coletta E , Elisa Apicella C , Daniela Gallo C and Gianfranco Cosenza C
+ Author Affiliations
- Author Affiliations

A ISPAAM, Laboratory of Animal Cytogenetics and Gene Mapping, National Research Council, via Argine 1085, Napoli 80147, Italy.

B Department of Agricultural, Forest and Food Sciences, University of Torino, Largo Braccini 2, Grugliasco, Torino 10095, Italy.

C Department of Agriculture, University of Naples Federico II, via Università 100, Portici, Napoli 80055, Italy.

D Department of Agriculture, University of Sassari, via De Nicola 9, Sassari 07100, Italy.

E Italian National Association of Buffalo Breeders (ANASB), Via F. Petrarca 42-44 Località Centurano, Caserta 81100, Italy.

F Corresponding author. Email: ramunno@unina.it

Animal Production Science 56(1) 102-107 https://doi.org/10.1071/AN14612
Submitted: 30 May 2014  Accepted: 10 September 2014   Published: 18 February 2015

Abstract

Lactoferrin (LTF) is a multi-functional protein belonging to the whey protein fractions of milk. The gene LTF encoding for such protein is considered a potential candidate for body measurement, milk composition and yield. This study reports on the genetic variability at the LTF locus in the Italian Mediterranean river buffalo and its possible association with milk yield. Eleven polymorphic sites were found in the DNA fragment spanning exons 15–16. In particular, intron 15 was extremely polymorphic with nine single nucleotide polymorphisms (SNPs) detected, whereas the remaining two SNPs were exonic mutations (g.88G > A at exon 15 and g.1351G > A at exon 16) and both synonymous. The genotyping of the informative samples evidenced three haplotypes, whose frequencies were 0.6, 0.3 and 0.1, respectively, whereas the analysis of the exonic SNPs showed a perfect condition of linkage disequilibrium (g.88A/g.1351G and g.88G/g.1351A). The association study carried out by using the SNP g.88G > A showed that buffalo LTF gene has no statistically significant influence on daily milk yield. This study adds knowledge to the genetic variability of a species less investigated than the other ruminant species. These findings may serve as a useful tool for large-scale screening of buffalo populations.

Additional keywords: Bubalus bubalis, haplotype, lactoferrin, marker-assisted selection, milk yield, polymorphism.


References

Arnould VM, Soyeurt H, Gengler N, Colinet FG, Georges MV, Bertozzi C, Portetelle D, Renaville R (2009) Genetic analysis of lactoferrin content in bovine milk. Journal of Dairy Science 92, 2151–2158.
Genetic analysis of lactoferrin content in bovine milk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFyms7o%3D&md5=a226bb20dff5f6b308f77397b1703233CAS | 19389973PubMed |

Ashwell MS, Heyen DW, Sonstegard TS, Van Tassel CP, Da Y, Van Raden PM, Ron M, Weller JI, Lewin HA (2004) Detection of quantitative trait loci affecting milk production, health, and reproduction traits in Holstein cattle. Journal of Dairy Science 87, 468–475.
Detection of quantitative trait loci affecting milk production, health, and reproduction traits in Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Whsrk%3D&md5=924766c32405df547b2f913a303c4835CAS | 14762090PubMed |

Bonfatti V, Giantin M, Gervaso M, Rostellato R, Coletta A, Dacasto M, Carnier P (2012) CSN1S1–CSN3 (αs1-k-casein) composite genotypes affect detailed milk protein composition of Mediterranean water buffalo. Journal of Dairy Science 95, 6801–6805.
CSN1S1–CSN3 (αs1-k-casein) composite genotypes affect detailed milk protein composition of Mediterranean water buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFClt7nP&md5=975ae7551dcca7023030d40261cfe8daCAS | 22959943PubMed |

Borghese A (2005) Buffalo production and research. (Ed. A Borghese) p. 67. FAO Regional Office for Europe, REU Technical Series, Rome, Italy.

Cassandro M, Comin A, Ojala M, Dal Zotto R, De Marchi R, Gallo L, Carnier P, Bittante G (2008) Genetic parameters of milk coagulation properties and their relationships with milk yield and quality traits in Italian Holstein cows. Journal of Dairy Science 91, 371–376.
Genetic parameters of milk coagulation properties and their relationships with milk yield and quality traits in Italian Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGiug%3D%3D&md5=a99da07b450554c161b54d69b97cc97bCAS | 18096961PubMed |

Cosenza G, Pauciullo A, Mancusi A, Nicodemo D, Di Palo R, Zicarelli L, Di Berardino D, Ramunno L (2007) Mediterranean river buffalo oxytocin-neurophysin I (OXT) gene: structure, promoter analysis and allele detection. Italian Journal of Animal Science 6, 303–306.
Mediterranean river buffalo oxytocin-neurophysin I (OXT) gene: structure, promoter analysis and allele detection.Crossref | GoogleScholarGoogle Scholar |

Cosenza G, Feligini M, Mancusi A, D’Avino A, Coletta A, Di Berardino D, Ramunno L (2009a) Italian Mediterranean river buffalo CSN2 gene structure and promoter analysis Italian. Journal of Animal Science 8, 57–59.
Italian Mediterranean river buffalo CSN2 gene structure and promoter analysis Italian.Crossref | GoogleScholarGoogle Scholar |

Cosenza G, Pauciullo A, Feligini M, Coletta A, Colimoro L, Di Berardino D, Ramunno L (2009b) A point mutation in the splice donor site of intron 7 in the αs2-casein encoding gene of the Mediterranean River buffalo results in an allele-specific exon skipping. Animal Genetics 40, 791
A point mutation in the splice donor site of intron 7 in the αs2-casein encoding gene of the Mediterranean River buffalo results in an allele-specific exon skipping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Kit7jN&md5=4a3415572572caecd27657884a3e73a2CAS | 19422363PubMed |

Cosenza G, Pauciullo A, Macciotta NPP, Apicella E, Steri R, La Battaglia A, Jemma L, Coletta A, Di Berardino D, Ramunno L (2014) Mediterranean River Buffalo CSN1S1 gene: search for polymorphisms and association studies. Animal Production Science
Mediterranean River Buffalo CSN1S1 gene: search for polymorphisms and association studies.Crossref | GoogleScholarGoogle Scholar |

Daly M, Ross P, Giblin L, Buckley F (2006) Polymorphisms within the lactoferrin gene promoter in various cattle breeds. Animal Biotechnology 17, 33–42.
Polymorphisms within the lactoferrin gene promoter in various cattle breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsFamsrY%3D&md5=74cbfc347a40323b2d0a95dbde70a90aCAS | 16621758PubMed |

Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296, 2225–2229.
The structure of haplotype blocks in the human genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGhtrc%3D&md5=7ccc3722ad58ea7c48e9df74cc4df26bCAS | 12029063PubMed |

Giacinti G, Basiricò L, Ronchi B, Bernabucci U (2013) Lactoferrin concentration in buffalo milk. Italian Journal of Animal Science 12, e23–139–143.
Lactoferrin concentration in buffalo milk.Crossref | GoogleScholarGoogle Scholar |

Goossens M, Kan YW (1981) DNA analysis in the diagnosis of hemoglobin disorders. Methods in Enzymology 76, 805–817.
DNA analysis in the diagnosis of hemoglobin disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xhtl2hsrw%3D&md5=3c026bba34159bdd67fc90970de3940dCAS | 6276651PubMed |

Guo BL, Jiao Y, He C, Wei LX, Chang ZH, Yue XP, Lan XY, Chen H, Lei CZ (2010) A novel polymorphism of the lactoferrin gene and its association with milk composition and body traits in dairy goats. Genetics and Molecular Research 9, 2199–2206.
A novel polymorphism of the lactoferrin gene and its association with milk composition and body traits in dairy goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVyjsr7L&md5=4024ef94a9ec76438e541ebc548d04faCAS | 21064027PubMed |

Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, Podkolodny NL, Kolchanov NA (1998) Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Research 26, 362–367.
Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXovVCktQ%3D%3D&md5=5ffdf6b98bbfe6931e542896eff1b0fdCAS | 9399875PubMed |

Heyen DW, Weller JI, Ron M, Band M, Beever JE, Feldmesser E, Da Y, Wiggans GR, VanRaden PM, Lewin HA (1999) A genome scan for QTL influencing milk production and health traits in dairy cattle. Physiological Genomics 1, 165–175. http://physiolgenomics.physiology.org/content/1/3/165

Huang J, Wang H, Wang C, Li J, Li Q, Hou M, Zhong J (2010) Single nucleotide polymorphisms, haplotypes and combined genotypes of lactoferrin gene and their associations with mastitis in Chinese Holstein cattle. Molecular Biology Reports 37, 477–483.
Single nucleotide polymorphisms, haplotypes and combined genotypes of lactoferrin gene and their associations with mastitis in Chinese Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisFSgsQ%3D%3D&md5=5d38be2a5858e7a1fad22fa75b0d1afdCAS | 19672694PubMed |

Ikonen T, Morri A, Tyriseva AM, Ruottinen O, Ojala M (2004) Genetic and phenotypic correlations between milk coagulation properties, milk production traits, somatic cell count, casein content and pH of milk. Journal of Dairy Science 87, 458–467.
Genetic and phenotypic correlations between milk coagulation properties, milk production traits, somatic cell count, casein content and pH of milk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Whsrg%3D&md5=78640f835fd13ffabbe223706a827107CAS | 14762089PubMed |

Kaminski S, Olenski K, Brym P, Malewski T, Sazanov AA (2006) Single Nucleotide Polymorphism in the promoter region of the lactoferrin gene and its associations with milk performance traits in Polish holstein–friesian cows. Russian Journal of Genetics 42, 924–927.
Single Nucleotide Polymorphism in the promoter region of the lactoferrin gene and its associations with milk performance traits in Polish holstein–friesian cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosFWrurs%3D&md5=95b5264c0f17a2eaafe06353e7e0a553CAS |

Kang JF, Li XL, Zhou RY, Li LH, Feng FJ, Guo XL (2008) Bioinformatics analysis of lactoferrin gene for several species. Biochemical Genetics 46, 312–322.
Bioinformatics analysis of lactoferrin gene for several species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1SitL0%3D&md5=0a3f91967a345c722d7302f1b3d18890CAS | 18228129PubMed |

Kathiravan P, Kataria RS, Mishra BP (2009) Single nucleotide polymorphism (SNP) identification and sequence analysis of 5ʹ flanking region of lactoferrin gene in Indian buffaloes (Bubalus bubalis). Livestock Science 121, 38–44.
Single nucleotide polymorphism (SNP) identification and sequence analysis of 5ʹ flanking region of lactoferrin gene in Indian buffaloes (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar |

Kathiravan P, Kataria RS, Mishra BP, Dubey PK, Selvakumar M, Tyagi N (2010) Seven novel single nucleotide polymorphisms identified within river buffalo (Bubalus bubalis) lactoferrin gene. Tropical Animal Health and Production 42, 1021–1026.
Seven novel single nucleotide polymorphisms identified within river buffalo (Bubalus bubalis) lactoferrin gene.Crossref | GoogleScholarGoogle Scholar | 20012192PubMed |

Khatibi M, Roshanfekr H, Fayazi J, Mirzade K (2013) Polymorphism of 5ʹ flanking region of lactoferrin gene in Khuzestan buffaloes. International Journal of Advanced Biological and Biomedical Research 1, 777–782.

Lee TH, Shimazaki K, Yu SL, Nam MS, Kim SJ, Lee KK, Yu DY (1997) Polymorphic sequence of Korean native goat lactoferrin exhibiting greater antibacterial activity. Animal Genetics 28, 367–369.
Polymorphic sequence of Korean native goat lactoferrin exhibiting greater antibacterial activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntV2gurw%3D&md5=3c28387124aab146b7abcfee1f6ec1e7CAS | 9363601PubMed |

Li GH, Zhang Y, Sun DX, Li N (2004) Study on the polymorphism of bovine lactoferrin gene and its relationship with mastitis. Animal Biotechnology 15, 67–76.
Study on the polymorphism of bovine lactoferrin gene and its relationship with mastitis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVSms7w%3D&md5=8fb0ce4e91bafcb9e4058e0cad548a23CAS | 15248601PubMed |

Masina P, Rando A, Di Gregorio P, Cosenza G, Mancusi A (2007) Water buffalo kappa-casein gene sequence. Italian Journal of Animal Science 6, 353–355.
Water buffalo kappa-casein gene sequence.Crossref | GoogleScholarGoogle Scholar |

Mc Parland S, Giblin L, Veerkamp RF, Berry DP (2010) The impact of selection on milk production on the lactoferrin content of milk in Irish Holstein-Friesians. Advances in Animal Biosciences 1, 305
The impact of selection on milk production on the lactoferrin content of milk in Irish Holstein-Friesians.Crossref | GoogleScholarGoogle Scholar |

O’Halloran F, Bahar B, Buckley F, O’Sullivan O, Sweeney T, Giblin L (2009) Characterisation of single nucleotide polymorphisms identified in the bovine lactoferrin gene sequences across a range of dairy cow breeds. Biochimie 91, 68–75.
Characterisation of single nucleotide polymorphisms identified in the bovine lactoferrin gene sequences across a range of dairy cow breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktF2gtA%3D%3D&md5=38aa2b58fc61a13afd2e694a9e376620CAS | 18554515PubMed |

O’Halloran F, Berry DP, Bahar B, Howard DJ, Sweeney T, Giblin L (2010) Polymorphisms in the bovine lactoferrin promoter are associated with reproductive performance and somatic cell count. Journal of Dairy Science 93, 1253–1259.
Polymorphisms in the bovine lactoferrin promoter are associated with reproductive performance and somatic cell count.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlOis7w%3D&md5=00cfa9b0775946cae21ff73e6fe89a9fCAS | 20172245PubMed |

Pauciullo A, Cosenza G, D’Avino A, Colimoro L, Nicodemo D, Coletta A, Feligini M, Marchitelli C, Di Berardino D, Ramunno L (2010a) Sequence analysis and genetic variability of stearoyl CoA desaturase (SCD) gene in the Italian Mediterranean river buffalo. Molecular and Cellular Probes 24, 407–410.
Sequence analysis and genetic variability of stearoyl CoA desaturase (SCD) gene in the Italian Mediterranean river buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKrs7fN&md5=b20e1e66a0627bbe4cb69ac3a9f5ff8bCAS | 20691778PubMed |

Pauciullo A, Cosenza G, Nicodemo D, Gallo D, Mancusi A, Crepaldi P, Di Berardino D, Ramunno L (2010b) Molecular cloning, promoter analysis and SNP identification of Italian Nicastrese and Saanen lactoferrin gene. Veterinary Immunology and Immunopathology 134, 279–283.
Molecular cloning, promoter analysis and SNP identification of Italian Nicastrese and Saanen lactoferrin gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivFGrsL0%3D&md5=860f9882570afef3cf9489dbd45fa163CAS | 19853309PubMed |

Pauciullo A, Cosenza G, Steri R, Coletta A, La Battaglia A, Di Berardino D, Macciotta NPP, Ramunno L (2012a) A single nucleotide polymorphism (SNP) in the promoter region of River buffalo Stearoyl CoA Desaturase gene (SCD) is associated with milk yield. The Journal of Dairy Research 79, 429–435.
A single nucleotide polymorphism (SNP) in the promoter region of River buffalo Stearoyl CoA Desaturase gene (SCD) is associated with milk yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ars7bI&md5=9089d28b5f6d6d7416852753cb2bca41CAS | 22994977PubMed |

Pauciullo A, Cosenza G, Steri R, Coletta A, Jemma L, Feligini M, Di Berardino D, Macciotta NPP, Ramunno L (2012b) An association between Single Nucleotide Polymorphisms at the Oxytocin locus and milk yield in Italian Mediterranean river buffalo. The Journal of Dairy Research 79, 150–156.
An association between Single Nucleotide Polymorphisms at the Oxytocin locus and milk yield in Italian Mediterranean river buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVGmsLg%3D&md5=c9e71575e0fdc07262134f57ffecf118CAS | 22280971PubMed |

Risch NJ (2000) Searching for genetic determinants in the new millennium. Nature 405, 847–856.
Searching for genetic determinants in the new millennium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksV2gtLs%3D&md5=eef8d4a8f1a61768d70affcf5ee7e39dCAS | 10866211PubMed |

Schutz MM (1994) Genetic evaluation of Somatic Cell Scores for United States dairy cattle. Journal of Dairy Science 77, 2113–2129.
Genetic evaluation of Somatic Cell Scores for United States dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FhsFWktQ%3D%3D&md5=692587ade477f70662dc659a253f3618CAS | 7929969PubMed |

Seyfert HM, Tuckoricz A, Interthal H, Koczan D, Hobom G (1994) Structure of the bovine lactoferrin encoding gene and its promoter. Gene 143, 265–269.
Structure of the bovine lactoferrin encoding gene and its promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFSiurs%3D&md5=afe16b751ea078acb8de8e3a811cc5e6CAS | 8206385PubMed |

Vogel HJ, Schibli D, Jing W, Lohmeier-Vogel EM, Epand RF, Epand RM (2002) Towards a structure function analysis of bovine lactoferricin and related tryptophan and arginine containing peptides. Biochemistry and Cell Biology 80, 49–63.
Towards a structure function analysis of bovine lactoferricin and related tryptophan and arginine containing peptides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCnsb8%3D&md5=3d259ac8dfaf13a65dbddeeeae07ea6eCAS | 11908643PubMed |

Wang M, Moisá S, Khan MJ, Wang J, Bu D, Loor JJ (2012) MicroRNA expression patterns in the bovine mammary gland are affected by stage of lactation. Journal of Dairy Science 95, 6529–6535.
MicroRNA expression patterns in the bovine mammary gland are affected by stage of lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFClurvE&md5=7d2afeb716020ac72c14d50cd37267afCAS | 22959945PubMed |

Zabolewicz T, Brym P, Olenski K, Suchocki K, Malewski T, Szyda J, Kaminski S (2012) Polymorphism within TATA-box of bovine lactoferrin gene and its association with performance traits in Holstein cattle. Livestock Science 149, 267–274.
Polymorphism within TATA-box of bovine lactoferrin gene and its association with performance traits in Holstein cattle.Crossref | GoogleScholarGoogle Scholar |