Advances in Animal and Veterinary Sciences
Review Article
β-Lactoglobulin Gene Polymorphisms in Sheep and Effects on Milk Production Traits: A Review
Maria Selvaggi, Vito Laudadio, Cataldo Dario*, Vincenzo Tufarelli
Department DETO – Section of Veterinary Science and Animal Production, University of Bari ‘Aldo Moro’, 70010 Valenzano (BA) Italy.
Abstract | β-lactoglobulin is the main whey protein of milk from different species. To date, β-lactoglobulin gene (BLG) is one of the most investigated in ruminants including sheep. β-lactoglobulin was the first protein, in which polymorphism was found. Polymorphisms of BLG gene have been detected in several sheep breeds, but studies on the effects of BLG genetic variants on milk production traits and cheese making ability have given conflicting results. Therefore, this paper represents a detailed and updated review on β-lactoglobulin gene polymorphisms in many sheep breeds worldwide. Moreover, the associations among BLG polymorphisms and milk yield and composition as well as milk coagulation properties were reported to offer a complete overview on these topics.
Keywords | Sheep, β-lactoglobulin, Gene polymorphisms, Milk production, Milk coagulation
Editor | Kuldeep Dhama, Indian Veterinary Research Institute, Uttar Pradesh, India.
Received | June 14, 2015; Revised | July 15, 2015; Accepted | July 17, 2015; Published | July 29, 2015
*Correspondence | Cataldo Dario, University of Bari ‘Aldo Moro’, Valenzano, Italy; Email: cataldo.dario@uniba.it
Citation | Selvaggi M, Laudadio V, Dario C, Tufarelli V (2015). β-lactoglobulin gene polymorphisms in sheep and effects on milk production traits: A review. Adv. Anim. Vet. Sci. 3(9): 478-484.
DOI | http://dx.doi.org/10.14737/journal.aavs/2015/3.9.478.484
ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331
Copyright © 2015 Selvaggi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction
Milk and dairy products from small ruminant species represent a significant part of the agricultural economy worldwide especially in marginal areas. However, goat and sheep milks have peculiar composition and properties and, as a consequence, specific productive destinations (Selvaggi et al., 2014a). In fact, sheep milk is used mainly for cheese production (Selvaggi and Tufarelli, 2012; Selvaggi et al., 2014b). There is a strong association among milk protein polymorphisms and milk yield, composition and technological aspects. So, it is necessary to make available in-depth information regarding genetic polymorphisms of milk proteins in ovine species also considering the great genetic biodiversity of sheep breeds.
β-lactoglobulin is the main whey protein of cow, sheep, goat and horse milk; it is lacking in milk from human, rodents, rabbits and camels in which, instead, another major whey protein (whey acidic protein) is found (Perez and Calvo, 1995). The whey proteins showed a high nutritive value being a precious source of digestible proteins. Sheep milk whey proteins account for 17–22% of total proteins. Whey obtained from sheep milk is particularly rich in proteins with a high β-lactoglobulin and low α-lactalbumin content (Moatsou et al., 2005). β-lactoglobulin is a globular protein member of the lipocalin family, small proteins with many properties, such as the ability to bind small hydrophobic molecules. Although its biological function is still unclear, β-lactoglobulin provides amino acids to the offspring and a possible role in the transport of retinol and fatty acids has been suggested (Perez and Calvo, 1995). β-lactoglobulin was the first protein in which polymorphism was found; it consists of 162 amino acids and forms stable dimers in milk having a molecular weight of 18 kDa per monomer (Kontopidis et al., 2004).
Polymorphisms of BLG gene
β-lactoglobulin is encoded by the BLG gene that has been mapped on chromosome 3 in sheep (Hayes and Petit, 1993). This gene is expressed in the mammary gland in a tissue-specific manner during pregnancy and lactation (Clark, 1998). β-lactoglobulin gene is highly polymorphic in ruminants: in cattle, 12 polymorphic variants of this protein are known, with variants A and B being the most frequent and commonly related to differences in milk protein yield and quality (Lunden et al., 1997; Yang et al., 2012). In sheep, β-lactoglobulin polymorphism was widely investigated in many breeds worldwide. Three co-dominant alleles (A, B and C) have been reported in this species differing by one or more amino acid changes. The genetic variant A differs from variant B in the amino acid sequence at position 20 (Tyr→His) (Bell and McKenzie, 1967; Kolde and Braunitzer, 1983; Ali et al., 1990). Later, Erhardt (1989) found a new and rare variant indicated as C that is a subtype of variant A with a single amino acid exchange at position 148 (Arg→Gln). Variants A and B are the most common and have been detected in many breeds (see Table 1, 2 and 3). The rare variant C was detected only in few breeds such as: Merinoland, Lacha, Carranzana, Spanish Merino, Serra da Estrela, White Merino, and Black Merino (Erhardt, 1989; Calavia, 1997; Recio et al., 1997; Ramos et al., 2009). Erhardt (1989) suggested that the allele C perhaps originated from the Spanish Merinos considering that both Merinoland and Hungarian Merino, in which the allele C was detected, contain blood from Spanish Merinos. This hypothesis may be strengthened by the allele C detection in Black Merino and White Merino (Ramos et al., 2009). As reported in Table 1, four sheep breeds from Saudi Arabia were found monomorphic: in particular, in Noami and Sawakni breeds only the allele A was found; whereas Nagdi and Harry breeds were genotyped as BB (El-Shazly et al., 2012). Moreover, most of sheep breeds from India showed a prevalence of B allele; as a consequence, Arora et al. (2010) suggested that the B allele could possibly be considered the ancestral variant of BLG in Indian sheep. In fact, in many breeds from India, the frequency of allele B was higher than that reported in breeds from Southwest Asia, Eastern and Central Europe and Mediterranean countries (Table 1 and 2). In addition, only few investigations on BLG polymorphisms were carried out in countries other than Europe and Asia; sheep breeds from Africa, America and Oceania showed a frequency of A allele ranging from 0.704-0.950, and no evidence of C allele was found (Table 3).
Table 1: Summary of published allelic frequencies of β-lactoglobulin gene in different sheep breeds with different purpose from Asia
Breed |
Purpose |
A |
B |
C |
References |
Nagdi |
Meat |
- |
1.000 |
- |
|
Harry |
Meat |
- |
1.000 |
- |
|
Muzzafarnagri |
Meat, Carpet wool |
0.100 |
0.900 |
- |
|
Zel |
Meat |
0.140 |
0.860 |
- |
|
Jalauni |
Meat, Carpet wool |
0.160 |
0.840 |
- |
|
Magra |
Carpet wool |
0.193 |
0.807 |
- |
|
Rampur Bushair |
Carpet wool |
0.273 |
0.727 |
- |
|
Mandya |
Meat |
0.273 |
0.727 |
- |
|
Garole |
Meat |
0.277 |
0.723 |
- |
|
Ganjam |
Meat, Carpet wool |
0.326 |
0.674 |
- |
|
Afshari |
Meat |
0.340 |
0.660 |
- |
|
Awassi |
Dairy |
0.348 |
0.352 |
- |
|
Moghani |
Meat |
0.360 |
0.640 |
- |
|
Changthangi |
Carpet wool |
0.386 |
0.614 |
- |
|
Patanwadi |
Carpet wool |
0.410 |
0.590 |
- |
|
Jaisalmeri |
Carpet wool |
0.425 |
0.575 |
- |
|
Kheri |
Meat, carpet wool |
0.472 |
0.528 |
- |
|
Arkharmerino |
Fine wool |
0.480 |
0.520 |
- |
|
Kendrapada |
Meat |
0.480 |
0.520 |
- |
|
Sonadi |
Meat, carpet wool |
0.499 |
0.501 |
- |
|
Dekkani |
Meat, coarse wool |
0.500 |
0.500 |
- |
|
Madgyal |
Meat |
0.500 |
0.500 |
- |
|
Kurdi |
Meat |
0.510 |
0.490 |
- |
|
Malpura |
Wool |
0.510 |
0.490 |
- |
|
Makoei |
Meat, Carpet wool |
0.530 |
0.470 |
- |
|
Chhotanagpuri |
Carpet wool |
0.531 |
0.469 |
- |
|
Ghezel |
Meat, Carpet wool |
0.560 |
0.440 |
- |
|
Morkaraman |
Meat, Carpet wool |
0.560 |
0.440 |
- |
|
Marwari |
Carpet wool |
0.562 |
0.438 |
- |
|
Chokla |
Carpet wool |
0.569 |
0.431 |
- |
|
Awassi |
Dairy |
0.630 |
0.370 |
- |
|
Nali |
Carpet wool |
0.630 |
0.370 |
- |
|
Karakul |
Pelt, wool, meat |
0.714 |
0.286 |
- |
|
Gökçeada |
Dairy, meat, wool |
0.763 |
0.237 |
- |
|
Kivircik |
Meat, wool, dairy |
0.776 |
0.224 |
- |
|
Dumba |
Carpet wool |
0.950 |
0.050 |
- |
|
Sakiz |
Dairy, wool, meat |
0.976 |
0.024 |
- |
|
Noami |
Meat |
1.000 |
- |
- |
|
Sawakni |
Meat |
1.000 |
- |
- |
Sheep breeds in which the associations among polymorphism and milk traits where investigated are highlighted in bold
Table 2: Summary of published allelic frequencies of β-lactoglobulin gene in different sheep breeds with different purpose from Europe
Breed |
Purpose |
A |
B |
C |
References |
Sarda |
Dairy |
0.274 |
0.726 |
- |
|
Churra |
Dairy |
0.310 |
0.690 |
- |
|
Rhön |
Meat |
0.324 |
0.676 |
- |
|
Carranzana |
Dairy |
0.350 |
0.640 |
0.010 |
|
Valle del Belice |
Dairy |
0.350 |
0.650 |
- |
|
Valachian |
Dairy, wool, meat |
0.353 |
0.647 |
- |
|
Black Merino |
Fine wool |
0.392 |
0.607 |
0.001 |
|
Romanian Rusty Tsigai |
Dairy, wool, meat |
0.420 |
0.580 |
- |
|
Romanov |
Meat, wool |
0.430 |
0.570 |
- |
|
Gyimesi Racka |
Dairy, wool, meat |
0.460 |
0.540 |
- |
|
White Merino |
Fine wool |
0.464 |
0.535 |
0.001 |
|
Lacha |
Dairy |
0.470 |
0.530 |
- |
|
Bosnian Pramenka |
Dairy |
0.470 |
0.530 |
- |
|
Lacaune |
Dairy |
0.473 |
0.527 |
- |
|
Polish Merino |
Fine wool |
0.480 |
0.520 |
- |
|
Polish Merino |
Fine wool |
0.498 |
0.502 |
- |
|
Polish Mountain |
Carpet wool, dairy |
0.500 |
0.500 |
- |
|
Lacha |
Dairy |
0.500 |
0.490 |
0.010 |
|
Comisana |
Dairy |
0.500 |
0.500 |
- |
|
Hungarian Tsigai |
Dairy |
0.510 |
0.490 |
- |
|
Lithuanian Blackface |
Meat, wool |
0.520 |
0.480 |
- |
|
Massese |
Dairy |
0.520 |
0.480 |
- |
|
Pleven |
Dairy |
0.528 |
0.472 |
- |
|
Slovakian Tsigai |
Dairy, wool, meat |
0.540 |
0.460 |
- |
|
Bergschaf |
Meat, coarse wool |
0.550 |
0.450 |
- |
|
Serbian Cokanski Tsigai |
Dairy, wool, meat |
0.550 |
0.450 |
- |
|
Merinoland |
Fine wool |
0.579 |
0.246 |
0.175 |
|
Spanish Merino |
Fine wool |
0.580 |
0.410 |
0.010 |
|
Croatian Tsigai |
Dairy, wool, meat |
0.580 |
0.420 |
- |
|
Manchega |
Dairy |
0.610 |
0.390 |
- |
|
Gentile di Puglia |
Wool, meat |
0.613 |
0.387 |
- |
|
Serra da Estrela |
Dairy |
0.620 |
0.378 |
0.002 |
|
Altamurana |
Dairy |
0.625 |
0.375 |
- |
|
Lacaune |
Dairy |
0.630 |
0.370 |
- |
|
Leccese |
Dairy |
0.630 |
0.370 |
- |
|
Racka |
Dairy, wool, meat |
0.640 |
0.360 |
- |
|
Friesian |
Dairy |
0.660 |
0.340 |
- |
|
Bulgarian Tsigai |
Dairy, wool, meat |
0.680 |
0.320 |
- |
|
Merino |
Fine wool |
0.684 |
0.316 |
- |
|
Lithuanian Native Coarsewooled |
Meat, wool |
0.690 |
0.310 |
- |
|
East Friesian |
Dairy |
0.690 |
0.310 |
- |
Sheep breeds in which the associations among polymorphism and milk traits where investigated are highlighted in bold
Relationship between genetic variants of BLG gene and milk production traits
Polymorphisms of BLG gene may be helpful as informative molecular markers for milk yield and composition as well as for rheological properties of milk. However, the influence of BLG polymorphism on milk yield and composition and cheese-making properties is controversial, indicating superiority of either the A or B allele or no relationship with quantitative traits.
In Valle del Belice ewes, the AA genotype was associated with greater milk production (Giaccone et al., 2000). A similar result was found in Sarda breed; in this case, animals carrying AA and AB genotypes had higher milk yield than BB ewes (Nudda et al., 2000, 2003). In East Friesian sheep, it was observed a higher milk yield during the first lactation in individuals carrying AA genotype; whereas BB genotype ewes had the highest milk yield in the following lactations (Schmoll et al., 1999). In Portuguese dairy sheep studied by Ramos et al. (2009), homozygous AA ewes presented lower values of milk yield and no differences between AB and BB genotypes were found. No differences in terms of milk production among genotypes were found in Sarda (Pietrolà et al., 2000), East Friesian (Staiger et al., 2010), Polish Mountain, Polish Merino, East Friesian, and Bergschaf (Kaweka and Radko, 2011) and in West African sheep (Aranguren-Méndez et al., 2012). Some investigations assessed the superiority of the B allele (Rampilli et al., 1997; Bolla et al., 1989). Later, this result was confirmed by Corral et al. (2010) in Merino sheep breed.
As for milk quality, recently Corral et al. (2010) demonstrated that Merino ewes genotyped as AA were those that produced the highest fat and protein percentages. Moreover, heterozygous Serra da Estrela animals presented higher milk fat content than those carrying genotype BB. Besides, AA Merino ewes had higher milk protein content than animals with genotype AB (Ramos et al., 2009). A positive association was found between AB genotype and fat and lactose percentages in milk from Iranian indigenous Zel sheep breed (Yousefi et al., 2013). Previous findings by Dario et al. (2005, 2008) in Altamurana and Leccese breeds reported a superiority of AA and AB genotypes for fat and whey protein percentages in milk. Martínez et al. (1993) pointed out a highly significant and positive effect of AA and AB genotypes on milk protein and casein contents in Manchega sheep. On the other hand, Giaccone et al. (2000) reported a positive effect of BB genotype on milk protein and fat contents, and Mroczkowski et al. (2004) found a positive relationship between BB genotype and milk protein content in comparison with both AA and AB genotypes in Polish Merino. No association among milk composition traits and BLG genotypes was found in Polish Mountain, Polish Merino, East Friesian, Bergschaf (Kaweka and Radko, 2011), Massese (Mele et al., 2007), Sarda (Nudda et al., 2000, 2003), Merino (Recio et al., 1997), and Churra (Gutiérrez-Gil et al., 2001). As reported by Rampilli et al. (1997) in Massese breed, the BB variant of BLG could be related to a higher milk production with
Table 3: Summary of published allelic frequencies of β-lactoglobulin gene in different sheep breeds with different purpose from other countries
Breed |
Purpose |
A |
B |
C |
References |
|
Africa |
Barki |
Carpet wool, meat |
0.704 |
0.296 |
- |
|
Ossimi |
Carpet wool, meat |
0.828 |
0.172 |
- |
||
Rahmani |
Carpet wool, meat |
0.950 |
0.050 |
- |
||
America |
West African |
Meat |
0.900 |
0.100 |
- |
|
Oceania |
Border Leicester×Merino |
Meat, wool |
0.750 |
0.250 |
- |
|
Hyfer |
Meat, wool |
0.840 |
0.160 |
- |
Sheep breeds in which the associations among polymorphism and milk traits where investigated are highlighted in bold
lower casein content and greater overall amount of whey proteins. At the same time, the AA and AB genotypes showed higher β-lactoglobulin and total casein contents and were related to a better quality of milk also in terms of rennetability. To date, only one investigation reported the relationship between BLG genotypes and milk fatty acid composition in sheep; in particular, milk from AB individuals had the lowest concentration of medium-chain fatty acids and the highest level of trans fatty acids, monounsaturated fatty acids and long-chain fatty acids, with no significant differences regarding the polyunsaturated fatty acids level (Mele et al., 2007).
Many investigations have shown a superiority of milk from AA ewes for cheese processing thanks to its shorter clotting time, a better rate of curd firming and a favourable cheese yield (Lopez Galvez et al., 1993; 1994; 1998; Rampilli et al., 1997; Gutierrèz-Gil et al., 2001). In addition, Garzón et al. (1993) reported a superiority of AA and AB genotypes, in comparison to BB homozygotes, in terms of curdling time, medium and maximum firmness, rate of firming, and curd yield in Manchega breed. These results conflict with data reported by Pilla et al. (1995) who found that the B allele positively affected the rennet coagulation properties of milk. No association between BLG polymorphism and milk renneting properties (clotting time, curd firming time and curd firmness) was found by Recio et al. (1997) in Merino ewes and by Nudda et al. (2000) in Sarda breed. More recently, Çelik and Özdemir (2006) investigated the association between BLG genetic variants and rennet clotting time in milk belonging to Awassi and Morkaraman breeds without statistical significant differences.
Conclusions
It is noteworthy that the available literature provides no conclusive remarks about the effects of different β-lactoglobulin genotypes on milk production traits and coagulation properties in ovine species. Sometimes, results from different investigations are not comparable with each other for many reasons: population size, breed, frequency of the considered genotypes, statistical models used for data analysis. Moreover, the conflicting reports on the association of genetic variants of BLG with milk production traits may be due to the lack of knowledge of the relatedness of the studied animals. Despite these controversial results, to include molecular genetic markers in selection to improve livestock productive performance is also a target in sheep breeding to enhance the economy of dairy sheep production worldwide. To improve the local farms productivity in developing countries and in marginal areas of developed countries is a strategy to limit the off-farm migration and safeguard the current wide animal biodiversity. However, the fact remains that to sustain the economy of rural and marginal areas is also a crucial target in developed countries.
Conflict of Interest
The authors declare no competing interests.
Authors contribution
All authors contributed equally to the manuscript.
References