Consequences of selection for higher growth rate on muscle fibre development in cattle

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Abstract

The aim of this study was to analyse the consequences of selection on the development of muscle fibres in the semitendinosus muscle of two groups of Charolais bulls with a high or low muscle growth index. Muscle fibre kinetics were analysed during foetal life (110, 180, 210, 260 days of gestation) and after birth (3 weeks, 9, 15, 19 months). The weight, length and area of muscle were measured. The total number of fibres and muscle fibre area were calculated for each stage. The contractile properties of fibres were revealed by immunohistochemistry. Oxidative capacity of individual fibres was determined on serial sections stained for Succinate Dehydrogenase. Finally, whole muscle metabolic properties were measured on homogenates of muscle with analysis of the activity of Lactate Dehydrogenase (glycolytic) and Isocitrate Dehydrogenase (oxidative). The main results showed muscle hypertrophy in bulls with a high growth potential due to a higher total number of fibres (indicating hyperplasia). From the last trimester of gestation onwards, this is associated with particular contractile and metabolic properties, with mainly a higher proportion of IIX fibres (fast glycolytic). However, the delayed physiological maturity of these bulls induced a delay in the plasticity of muscle fibres after birth. Consequently, the effects of selection on growth rate on muscle properties are not evident at each stage.

Introduction

In farm animals, it has been shown that muscle fibre properties play a key role in meat quality. So understanding the growth and development of skeletal muscle is one of the most important goals in meat production science. The major components of muscles are muscle fibres. Muscle mass is largely determined by the number and size of muscle fibres. These fibre characteristics are determined by hyperplasia before birth and by hypertrophy after. Different studies conducted on bovine foetuses showed that the total number of fibres is fixed by the end of the second trimester of pregnancy (for review, Picard et al., 2002). The fibre size increases mainly during post-natal life (Jurie et al., 1999, Brandstetter et al., 1998). The properties of bovine muscle fibres are acquired in a three-generation process (for a review, Picard et al., 2002). Primary generation is observed from 30 days of foetal life onwards and is completely differentiated by the end of the second trimester (around 180 days).

These primary fibres mature to slow twitch type I fibres in most muscles except in exclusively fast adult muscles in which it is converted into fast fibres (Picard et al., 1994). A secondary generation is observed from the end of the first trimester, and mostly matures to secondary fast IIX fibres. A third generation is observed from 40% of the gestation period onwards as in sheep (Wilson et al., 1992) and human (Draeger et al., 1987). In cattle, this generation gives rise to fast IIA fibres, slow I fibres and IIC fibres. These last 3 types of fibres are undifferentiated at birth, they contain both fast and slow myosin heavy chain (MHC) isoforms and are converted after birth into fast or slow fibres depending on the muscle (Picard et al., 2002). The analysis of different differentiation markers showed that contractile and metabolic differentiation occurred during the last trimester (Picard et al., 2002). Among the different bovine breeds, cattle with enlarged muscles show particular fibre properties. For example, double-muscled cattle (DM) display muscle hypertrophy (20% higher muscle mass on average than other cattle breeds). The responsible gene myostatin, or GDF8, is mutated or deleted in DM cattle resulting in an inactive protein (Grobet et al., 1997). The muscles of these cattle contain twice the number of fibres as other breeds with normal musculature (Ashmore et al., 1974, Wegner et al., 2000). The results of Picard et al. (1998a) and Deveaux et al. (2001) have shown that this higher total number of fibres originates from greater proliferation of the secondary cell generation. This greater proliferation is accompanied by a delay in the differentiation phase (Gagnière et al., 2000). So, adult DM muscles exhibit a higher proportion of fast glycolytic fibres simultaneously with a higher total number of fibres than other cattle breeds. This gives a paler meat with a higher tenderness (Wegner et al., 2000).

An increase in muscle mass can also be obtained by selection (for example see Renand et al., 1994). Charolais cattle selected on their muscle growth capacity, high (H) comparatively to low (L), had muscles with a higher proportion of fast glycolytic fibres (Cassar-Malek et al., 2003) as observed for DM cattle at slaughter. In vitro studies have also shown a higher proliferation of H muscle myoblasts (Duris and Picard, 1999) as observed for DM myoblasts.

The aim of the present study was to demonstrate difference in muscle development, which may account for the superior growth characteristics of the H line in comparison to the L line.

Section snippets

Animals

The study was carried out as part of a research program approved by the Ethical Committee of “Institut National de la Recherche Agronomique” (INRA, France). The cows were bred and slaughtered, and foetuses were collected, according to ethical guidelines concerning animal care. The Charolais breed foetuses were produced by artificial insemination in Charolais culled cows. Four foetuses of each strain H and L were collected at 110, 180, 210 and 260 days post conception (dpc). The four H foetuses

Characteristics of animals

During foetal life, length and weight of foetuses were not different between the two strains. From birth onwards weight was higher in H strains (Fig. 1).

Characteristics of semitendinosus muscle

The weight of ST became higher, but not significantly, in H strain from 260 days onwards. The length was not different at any stage. The muscle area was higher in H strain from 260 days onwards, the differences being significant only at 9 (P < 0.05) and 15 (P < 0.1) months (Fig. 2).

Characteristics of semitendinosus muscle fibres

The muscle fibre mean cross section areas were different only at 15

Discussion

All these data indicate that the differences in fibre properties between H and L cattle appear early during foetal life. From 210 days, H semitendinosus muscle contained on average 34% of additional fibres. From 260 days onwards the proportion of IIX fibres was higher and that of IIA and I lower in H muscle. These differences due to genetic type were very marked during foetal life and in the young animal but they were reduced at slaughter because of a different evolution of fibre properties

Acknowledgements

The authors thank D. Krauss of the Experimental facilities of INRA Bourges for the production of foetuses, R. Jailler and his staff for the slaughter of cattle, Christiane Barboiron for the dissection of foetus, Sevda Koc and all the members of Growth and Metabolism group of Unit of Research on Herbivores for their technical assistance.

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