The effects of leptin receptor (LEPR) and melanocortin-4 receptor (MC4R) polymorphisms on fat content, fat distribution and fat composition in a Duroc × Landrace/Large White cross

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Abstract

The effects of mutations LEPR c.1987C>T and MC4R c.1426G>A on leptin receptor and melanocortin receptor genes, which are involved in regulating appetite, have been studied in a Duroc × Landrace/Large White cross. To the best of our knowledge, this is the first report of the presence of LEPR c.1987C>T effects outside the Iberian breed or crosses of Iberian with other breeds. Both mutations modify several traits related to adipose tissue content. LEPR TT pigs have a lower percentage of joints rich in muscle tissue and a higher percentage of joints rich in adipose tissue in the carcass (5.8% lighter loins, 6.0% heavier lard) than LEPR CC pigs. LEPR TT pigs also have a greater adipose tissue content in their hams (8.0%) and shoulders (24%) than LEPR CC homozygous pigs. They also have larger backfat thickness values (between 1.5 and 7.5 mm depending on anatomical location). LEPR TT pigs show a clear increase in saturated fatty acid content at the expense of monounsaturated and polyunsaturated content when compared to LEPR CC pigs. MC4R GG pigs have a higher percentage of joints rich in muscle tissue and a lower percentage of joins rich in adipose tissue in the carcass (6.3% heavier loins and 4.7% lighter lard), lower fat cover and higher muscle fraction in hams (9.3% and 3.4%, respectively), and a larger fat content in B. femoris (12.2%) and in whole ham muscle mass (8.6%) than MC4R AA pigs. Whereas most effects of both mutations can be explained by an increase in feed intake, the strong effects of LEPR c.1987C>T on saturated fatty acid content in several anatomical locations are probably due to the local effect of a compromised leptin signaling system. The consequences of selecting these mutations for cured meat production are discussed.

Introduction

Fat content and its distribution have a significant influence on the quality of meat and its products. There is no absolute optimal fat content for meat products given the huge variety of such products and their varying requirements in terms of fat content. Whereas for fresh meat intended for direct consumption lean meat is usually preferred, the elaboration of cured meat products of high quality demands higher levels of fat infiltration (Ventanas and Andrés, 2000). Fat content is strongly influenced by feeding intake, which makes this phenotypic trait an important one from an economic and a technological point of view. Several studies have confirmed an important genetic determinism of the trait (Huisman and Van Arendonk, 2004, Labroue et al., 1997) and also some genomic regions have been associated with its genetic variation (Gilbert et al., 2010).

Pig selection in recent decades has been directed mainly toward obtaining lean carcasses with higher meat content. Due to a correlated response, this strategy has indirectly led to the selection of pigs with reduced feed intake (Webb, 1998). Instead, some breeds not selected for muscularity, such as the Iberian, are characterized by a high voluntary feed intake developed to adapt to seasonal variations of food abundance (Daza et al., 2007). This is called the thrifty genotype: under a constant and abundant food supply, individuals belonging to the thrifty genotype tend to develop obesity. Several genes are known to underlie, at least partially, these different feeding behaviors. Many of them participate in the leptin signaling pathway. Leptin is a protein hormone synthesized in the adipose tissue (Friedman, 2002). One of its target cells belongs to the neuronal circuits that regulate appetite. Correct leptin binding to its receptor and the events thereafter trigger a signal that reduces appetite (Friedman, 2002). Several mutations have been described in members of the signaling cascade triggered by leptin. Among others, a mutation in the leptin receptor (LEPR c.1987C>T) gene has been described by Ovilo et al. (2005) in Iberian pigs and crosses of Iberian with other breeds. This mutation affects carcass composition and meat content probably due to a lower hypothalamic leptin receptor expression of the T allele that reduces leptin signaling and enhances feed intake and, consequently, increases the general fat content of the carcass (Ovilo et al., 2010). LEPR c.1987T, the adipogenic allele, has been described only in individuals of Iberian genetic background, whether pure Iberians or crosses thereof. It is even fixed in the Iberian breed (Muñoz et al., 2009, Rodríguez et al., 2010). Another widely studied mutation, that causes lack of function of the protein, (Kim et al., 2000) is located in the melanocortin receptor-4 (MC4R c.1426A>G). MC4R encodes a G protein coupled receptor involved also in the leptin cascade. Conflicting effects on feeding behavior, and/or meat composition, and carcass conformation have been described for MC4R c.1426A>G: whereas Houston et al. (2004), Kim et al. (2000), and Ovilo et al. (2006) found higher feed intake and/or larger fat content in carriers of MC4R c.1426G>A, Park et al. (2002) failed to find any effect of the mutation. The MC4R c.1426G>A mutation, unlike LEPR c.1987C>T, has been found in several pig breeds (Burgos et al., 2006).

We decided to investigate the effect of LEPR c.1987C>T and MC4R c.1426G>A polymorphisms in a commercial population of Duroc × Landrace/Large White cross raised for cured meat production under the protected brand (“Denominación de Origen”, DO) “Jamón de Teruel”, one of the most important cured ham producers in Spain. We did so because a high degree of fat infiltration (both intramuscular and intermuscular) together with a sufficient adipose tissue cover is crucial to assure the quality of any cured ham. Considering that both genes have several effects on carcass fat content and distribution in other breeds (Kim et al., 2000, Rodríguez et al., 2010), the aims of our study were, first, to study if these mutations segregate in pigs raised for the “DO Jamón de Teruel” and, second, to investigate what effects these two mutations could have on carcass conformation, fat infiltration and on fat composition in these pigs with a view to introducing these genetic markers in selection schemes for “DO Jamón de Teruel” products.

Section snippets

Animals

202 pigs of both sexes (the males were castrated) from 9 sires to 32 dams of a Duroc × Landrace/Large White cross were raised in an experimental farm, fed ad libitum a standard diet and slaughtered at 114.5 +/− 10.98 kg, following the specifications of the “DO, Jamón de Teruel” (BOE, 2011).

Carcass processing

The pigs were stunned with CO2, slaughtered early in the morning and chilled for 6–8 h. Backfat thickness was measured at three levels (thoracic vertebrae 4 –T4–, thoracic vertebrae 14 –T14–, lumborum vertebrae 5,

Effects of LEPR c.1987C>T and MC4R c.1426G>A on conformational traits and on intramuscular fat content

Table 2 shows the influence of LEPR c.1987C>T and MC4R c.1426G>A on the relative contribution of ten carcass joints to the total carcass weight. LEPR c.1987C>T has above threshold effects on three of the ten carcass pieces and MC4R c.1426G>A on five out of ten. All the negative effects of both mutations affect muscle rich meat cuts (i.e., loin and tenderloin) whereas all the positive effects are observed in fat rich cuts, especially in the lard. Backfat thickness values measured at two

Conflict of interest statement

We have no conflict of interest in manuscript LIVSCI-D-11-545.

Acknowledgments

This work was supported by a grant for project AGL2008-01487ALI awarded to Pascual López Buesa. Almudena Galve thanks the Diputación General de Aragón for a predoctoral fellowship. We acknowledge the technical assistance of M. Ángeles López.

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