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Advances in Animal and Veterinary Sciences

AAVS_Nexus 669

 

 

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 (TyrHis) (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 (ArgGln). 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

-

El-Shazly et al., 2012

Harry

Meat

-

1.000

-

El-Shazly et al., 2012

Muzzafarnagri

Meat, Carpet wool

0.100

0.900

-

Arora et al., 2010

Zel

Meat

0.140

0.860

-

Yousefi et al, 2013

Jalauni

Meat, Carpet wool

0.160

0.840

-

Arora et al., 2010

Magra

Carpet wool

0.193

0.807

-

Arora et al., 2010

Rampur Bushair

Carpet wool

0.273

0.727

-

Arora et al., 2010

Mandya

Meat

0.273

0.727

-

Arora et al., 2010

Garole

Meat

0.277

0.723

-

Arora et al., 2010

Ganjam

Meat, Carpet wool

0.326

0.674

-

Arora et al., 2010

Afshari

Meat

0.340

0.660

-

Elyasi et al., 2010

Awassi

Dairy

0.348

0.352

-

Anton et al., 1999

Moghani

Meat

0.360

0.640

-

Elyasi et al., 2010

Changthangi

Carpet wool

0.386

0.614

-

Arora et al., 2010

Patanwadi

Carpet wool

0.410

0.590

-

Jyotsana et al., 2014

Jaisalmeri

Carpet wool

0.425

0.575

-

Arora et al., 2010

Kheri

Meat, carpet wool

0.472

0.528

-

Arora et al., 2010

Arkharmerino

Fine wool

0.480

0.520

-

Elyasi et al., 2010

Kendrapada

Meat

0.480

0.520

-

Jyotsana et al., 2014

Sonadi

Meat, carpet wool

0.499

0.501

-

Arora et al., 2010

Dekkani

Meat, coarse wool

0.500

0.500

-

Arora et al., 2010

Madgyal

Meat

0.500

0.500

-

Jyotsana et al., 2014

Kurdi

Meat

0.510

0.490

-

Nassiry et al., 2007

Malpura

Wool

0.510

0.490

-

Jyotsana et al., 2014

Makoei

Meat, Carpet wool

0.530

0.470

-

Elyasi et al., 2010

Chhotanagpuri

Carpet wool

0.531

0.469

-

Arora et al., 2010

Ghezel

Meat, Carpet wool

0.560

0.440

-

Elyasi et al., 2010

Morkaraman

Meat, Carpet wool

0.560

0.440

-

Çelik and Özdemir, 2006

Marwari

Carpet wool

0.562

0.438

-

Arora et al., 2010

Chokla

Carpet wool

0.569

0.431

-

Arora et al., 2010

Awassi

Dairy

0.630

0.370

-

Çelik and Özdemir, 2006

Nali

Carpet wool

0.630

0.370

-

Jyotsana et al., 2014

Karakul

Pelt, wool, meat

0.714

0.286

-

Kevorkian et al., 2008

Gökçeada

Dairy, meat, wool

0.763

0.237

-

Elmaci et al., 2006

Kivircik

Meat, wool, dairy

0.776

0.224

-

Elmaci et al., 2006

Dumba

Carpet wool

0.950

0.050

-

Jyotsana et al., 2014

Sakiz

Dairy, wool, meat

0.976

0.024

-

Elmaci et al., 2006

Noami

Meat

1.000

-

-

El-Shazly et al., 2012

Sawakni

Meat

1.000

-

-

El-Shazly et al., 2012

 

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

-

Pietrolà et al., 2000

Churra

Dairy

0.310

0.690

-

Gutiérrez-Gil et al., 2001

Rhön

Meat

0.324

0.676

-

Erhardt, 1989

Carranzana

Dairy

0.350

0.640

0.010

Calavia, 1997

Valle del Belice

Dairy

0.350

0.650

-

Giaccone et al., 2000

Valachian

Dairy, wool, meat

0.353

0.647

-

Miluchová et al., 2011

Black Merino

Fine wool

0.392

0.607

0.001

Ramos et al., 2009

Romanian Rusty Tsigai

Dairy, wool, meat

0.420

0.580

-

Kusza et al., 2015

Romanov

Meat, wool

0.430

0.570

-

Mácha and Novackova, 1974

Gyimesi Racka

Dairy, wool, meat

0.460

0.540

-

Kusza et al., 2015

White Merino

Fine wool

0.464

0.535

0.001

Ramos et al., 2009

Lacha

Dairy

0.470

0.530

-

Recio et al., 1997

Bosnian Pramenka

Dairy

0.470

0.530

-

Kusza et al., 2015

Lacaune

Dairy

0.473

0.527

-

Anton et al., 1999

Polish Merino

Fine wool

0.480

0.520

-

Kaweka and Radko, 2011

Polish Merino

Fine wool

0.498

0.502

-

Mroczkowski et al., 2004

Polish Mountain

Carpet wool, dairy

0.500

0.500

-

Kaweka and Radko, 2011

Lacha

Dairy

0.500

0.490

0.010

Calavia, 1997

Comisana

Dairy

0.500

0.500

-

Chiofalo et al., 1986

Hungarian Tsigai

Dairy

0.510

0.490

-

Kusza et al., 2015

Lithuanian Blackface

Meat, wool

0.520

0.480

-

Kučinskiene et al., 2005

Massese

Dairy

0.520

0.480

-

Mele et al., 2007

Pleven

Dairy

0.528

0.472

-

Erhardt, 1989

Slovakian Tsigai

Dairy, wool, meat

0.540

0.460

-

Kusza et al., 2015

Bergschaf

Meat, coarse wool

0.550

0.450

-

Kaweka and Radko, 2011

Serbian Cokanski Tsigai

Dairy, wool, meat

0.550

0.450

-

Kusza et al., 2015

Merinoland

Fine wool

0.579

0.246

0.175

Erhardt, 1989

Spanish Merino

Fine wool

0.580

0.410

0.010

Recio et al., 1997

Croatian Tsigai

Dairy, wool, meat

0.580

0.420

-

Kusza et al., 2015

Manchega

Dairy

0.610

0.390

-

Martínez et al., 1993

Gentile di Puglia

Wool, meat

0.613

0.387

-

Chessa et al., 2003

Serra da Estrela

Dairy

0.620

0.378

0.002

Ramos et al., 2009

Altamurana

Dairy

0.625

0.375

-

Dario et al., 2005

Lacaune

Dairy

0.630

0.370

-

Barillet et al., 1993

Leccese

Dairy

0.630

0.370

-

Dario et al., 2008

Racka

Dairy, wool, meat

0.640

0.360

-

Kusza et al., 2015

Friesian

Dairy

0.660

0.340

-

Kaweka and Radko, 2011

Bulgarian Tsigai

Dairy, wool, meat

0.680

0.320

-

Kusza et al., 2015

Merino

Fine wool

0.684

0.316

-

Corral et al., 2010

Lithuanian Native Coarsewooled

Meat, wool

0.690

0.310

-

Kučinskiene et al., 2005

East Friesian

Dairy

0.690

0.310

-

Staiger et al., 2010

 

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

-

Othman et al., 2012

Ossimi

Carpet wool, meat

0.828

0.172

-

Othman et al., 2012

Rahmani

Carpet wool, meat

0.950

0.050

-

Othman et al., 2012

America

West African

Meat

0.900

0.100

-

Aranguren-Méndez et al., 2012

Oceania

Border Leicester×Merino

Meat, wool

0.750

0.250

-

Thomas et al., 1989

Hyfer

Meat, wool

0.840

0.160

-

Thomas et al., 1989

 

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.

 

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    Advances in Animal and Veterinary Sciences

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