J. Anim Sci. 2008. 86:1283-1290. doi:10.2527/jas.2007-0568
© 2008 American Society of Animal Science
Mitochondrial genome polymorphisms associated with longissimus muscle composition in Iberian pigs1
A. I. Fernández*,2,
E. Alves*,
A. Fernández*,
E. de Pedro
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M. A. López-García*,
C. Ovilo*,
M. C. Rodríguez* and
L. Silió*
* Departamento de Mejora Genética Animal, INIA, Ctra. de la Coruña km 7.5, 28040 Madrid, Spain, and
Departamento de Producción Animal, Universidad de Córdoba, Campus de Rabanales, 14071 Córdoba, Spain
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Abstract
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We carried out a study to investigate the associations between mitochondrial DNA polymorphisms and meat quality traits (intramuscular fat and protein content of the longissimus) in an Iberian porcine line named Torbiscal. The studied pigs (n = 319) belong to 9 maternal lineages and were previously assigned to 6 mitochondrial haplotypes (H1 to H6), based on Cytochrome b and Dloop sequences. Statistical analyses, following a bivariate mixed model, show a greater fat content and lower protein content in H3 haplotype carriers than H1, H2, H4, H5, and H6 haplotype carriers. The magnitudes of these differences are close to 1 g of fat and –0.5 g of protein per 100 g of muscle. To identify the causative mutation of these effects on intramuscular fat and protein contents, the complete mitochondrial DNA sequence of 6 individuals was determined, each one carrying a different mitochondrial haplotype. The alignments of these 6 complete mitochondrial sequences allowed identification of 32 substitutions and 2 indels. Two polymorphic positions were exclusively detected in H3 carriers: a synonymous transition 9104C > T in the gene-coding region of Cytochrome c oxidase subunit III and a substitution 715A > G in 12S rRNA. Genotyping results of a larger number of Torbiscal samples showed the exclusive presence of 9104T and 715G alleles in H3 carriers. The detected candidate substitutions are located in essential mitochondrial genes, and although they do not change the amino acid composition, we cannot disregard a potential change in the secondary structure of their corresponding mRNA. The usefulness of these polymorphisms as markers in selection programs requires validation of the consistency of these results in other Iberian pig lines.
Key Words: Cytochrome c oxidase subunit III • Iberian pig • intramuscular fat • protein content • mitochondrial DNA • 12S rRNA
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INTRODUCTION
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Mammalian mitochondria use oxidative phosphorylation to convert dietary calories into energy in the form of ATP and heat. Mitochondrial DNA (mtDNA) is essential for maintaining the mitochondria functions. After a seminal paper on cytoplasmic effects on yield traits in dairy cattle (Kennedy, 1986
), diverse studies have been performed in farm animals trying to identify associations between mtDNA polymorphisms and economically important traits (Schutz et al., 1994; Boettcher et al., 1996; Mannen et al., 1998; Sutarno et al., 2002; Mannen et al., 2003). However, the importance of these mitochondrial effects in the genetic architecture of productive traits still remains doubtful, and caution should be exercised in interpreting the scarce number of significant association results reported.
Carcass characteristics and meat quality traits are the main breeding objectives in Iberian pigs in which production is focused on obtaining high sensorial quality meat (López-Bote, 1998). Quality of Iberian pig meat suitable for the production of dry-cured products mostly depends on its intramuscular fat (IMF) content, but selection to improve ham and loin weights may reduce the IMF content, according to the negative value of their genetic correlations (Fernández et al., 2003). The necessary inclusion of IMF in the selection goal is hampered by its expensive measurement, only possible late in life and not available on the candidate for selection. The use of molecular genetic tests to control the response to selection (Dekkers, 2004; Rothschild, 2004) could be advisable in the future to overcome these difficulties.
The first objective of our study was to estimate the effects of Dloop and Cyt b Iberian pig haplotypes (hyper-variable regions) on IMF content and protein in longissimus dorsi (LD) muscle. The second objective was to identify the possible causative mutations of the detected effects through the analysis of the complete mtDNA sequences, and to assess their usefulness as direct markers.
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MATERIALS AND METHODS
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Animals and Traits
Research protocols followed the guidelines stated in the Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching (FASS, 1999).
The animals studied were 319 castrated male Iberian pigs born in 127 litters of the Torbiscal line at the experimental farm Dehesón del Encinar (Oropesa, Toledo, Spain). The pigs were fed in 5 batches with restricted feeding with concentrates up to a BW of approximately 100 kg. Afterwards, they were fattened in a free-range system (Montanera) based on the ad libitum intake of acorns and pasture (López-Bote, 1998). The slaughter took place at approximately 159 kg of BW, with an average age of 353 d.
After slaughter, individual carcass weight was recorded, and a sample of LD was taken from each animal at the level of the fourth rib and used for determination of IMF and protein content. These analyses were carried out using near infrared reflectance spectroscopy in reflectance mode. Spectra of the muscle samples were obtained using Foss NIRSystems, 6500 SY-I, scanning monochromator equipped with a spinning cup (Foss NIRSystems, Silver Spring, MD; Solís et al., 2001). The WINISI II 1.04 (Infrasoft International, Port Matilda, MD) software was used for the spectra collection and the chemometric analysis of near infrared reflectance spectroscopy data. The raw phenotypic means and SD of the analyzed traits were 7.47 (2.38) g of fat/100 g of muscle, 20.83 (0.76) g of protein/100 g of muscle, and 127.0 (12.3) kg of carcass weight.
The complete genealogy of the studied pigs is available back to 1945, with 1,828 entries (animal-sire-dam) and 21 generations (Fabuel et al., 2004). In a previous study (Alves et al., 2003), we identified 9 surviving maternal lineages of the founder sows, and the Dloop (707 bp) and Cyt b (1,140 bp) regions of mtDNA samples, representing all of these lineages, were sequenced. According to these sequences, the 9 maternal lineages were grouped into 6 mtDNA haplotypes (H1 to H6). Therefore, knowledge of the founder maternal lineages allowed a haplotype to be assigned to each individual of the pedigree.
Six samples representative of all the haplotypes were used to determine their complete mtDNA sequences. Finally, to confirm the adequate assignation of pig genotypes based on their maternal lineages, 260 available DNA samples of the 319 pigs studied were typed for the detected candidate polymorphisms.
Statistical Methods
The following bivariate mixed linear model was used for a joint analysis of the 2 traits:
where the column vectors y1 and y2 represent the measures of IMF and protein content of the LD; β1 and β2 are vectors of the systematic effects on both traits, including the slaughter batch (5 levels), the D-loop and Cyt b haplotype of each slaughtered pig (6 levels), and the carcass weight as a covariate; u1 and u2 are vectors of the additive genetic effects for each trait (1,228); c1 and c2 are vectors of litter common environmental effects (127); and e1 and e2 are vectors of random residuals (319). The incidence matrices Xi, Zi, and Wi associate elements of βi, ui, and ci with the records in yi (i = 1, 2). The expectation of yi is Xiβi and the variance-covariance structure of the random effects of this bivariate animal model is as follows:
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where A is the numerator relationship matrix; 
2u1, 2c1, and 2e1 are variances of direct additive genetic, common environmental, and residual effects for trait i, respectively; u12 and c12 are the genetic and litter common environmental covariances between both traits; and e12 is their residual covariance.
A Bayesian procedure using a Gibbs sampling algorithm (Wang et al., 1994; Rodríguez et al., 1996) was performed to obtain the marginal posterior distributions of the parameters of interest: heritabilities (h12 and h22); common litter environmental coefficients (c21 and c22); genetic, common environmental, and phenotypic correlations between the 2 traits (rG, rC, and 
P); and the effects of the different mitochondrial haplotypes on the IMF and protein contents of the LD. A single Gibbs chain of 480,000 samples was obtained. The first 80,000 iterations were discarded, and 10,000 samples of each parameter were saved. Convergence was assessed by the double chain method (García Cortés et al., 1998). Flat priors were used for all of the parameters. The usual statistics of location (posterior mean, mode, and median) and dispersion (posterior SD and 90% highest posterior density interval) were calculated from the saved samples.
Mitochondrial DNA Amplification and Sequencing
Total DNA was extracted using a conventional phenol-cloroform precipitation protocol from frozen blood samples of the pigs. To amplify the complete mtDNA, 34 primer pairs (Table 1) were designed using the porcine mtDNA sequence AJ002189 as the template. The PCR were performed in a 25-µL final volume containing standard PCR buffer (75 mM Tris-HCl, pH 9.0, 50 mM KCl, 20 mM (NH4)2SO4, 2.0 mM MgCl2, 200 µM of each dNTP, 0.5 U of Tth polymerase (Biotools, Madrid, Spain), 90 ng of DNA, and 0.5 µM of each specific primer (Table 1). Amplification conditions were 94°C for 5 min, followed by 35 cycles of 94°C (30 s), the specific annealing temperature (Table 1; 30 s) and 72°C (45 s), with a final extension step of 10 min at 72°C. The PCR reactions were performed on a PTC-100 thermocycler (MJ Research, Watertown, MA). The PCR products were sequenced in both directions with the Dye-Terminator Cycle Sequencing 3.0 kit in an ABI 377 automatic sequencer (Applied Biosystems, Warrington, UK). The sequences obtained were edited and aligned with Mega3.1 software (http://www.megasoftware.net; Kumar et al., 2004).
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Table 1. Primer pairs used for PCR amplification and sequencing of the complete mitochondrial DNA in the Torbiscal Iberian pig line
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SNP Genotyping
Two pyrosequencing protocols were implemented using PSQ Assay Design 1.0.6 (Biotage AB, Uppsala, Sweden) to genotype 2 mtDNA SNP: 715A > G and 9104C > T. Fragments of 100 and 64 bp were amplified using the primer pairs 12S, forward: 5'-CAGCCTATATACC-GCCATCTTCA-3'and 12S, reverse: biotin-5'-AACCCA-TAAGCTACACCTTGACCT-3'; and COIII, forward: 5'-AGGGGACCGA AAACACATAA-3' and COIII, reverse: biotin-5'-GGTGAAGTATACGCCTAGTGCAA-3', respectively. The pyrosequencing primers were 12Sseq: 5'-GCAAACCCTAAAAAGGA-3' and COIIIseq: 5'-GGACCGAAAACACATAAT-3'. The PCR were performed as above but containing 75 ng of genomic DNA. Thermocycling was performed as described previously with an annealing temperature of 52°C. The pyro-sequencing reactions and genotype determination were carried out using a PSQ-HS96 device (Pyrosequencing AB, Uppsala, Sweden), following standard procedures.
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RESULTS
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The posterior means and SD, between brackets, of the analyzed LD composition traits (IMF and protein content) phenotypic variances are 5.206 (0.501) and 0.554 (0.005), respectively. The main statistics for the marginal posterior distributions of their variance ratios: mean, mode, median, SD, and 90% greatest density intervals of the heritabilities and correlations are summarized in the Table 2. Heritability estimates for these meat quality traits agree with those reviewed from diverse studies in cosmopolitan pig breeds by Sellier (1998), but the heritability estimate for IMF content (0.67) largely exceeds the values (hIMF 2 = 0.25 and 0.38) previously estimated in other Iberian pig populations (Fernández et al., 2003, 2007). As expected, the proportion of phenotypic variance due to common litter environmental effects is very small in both traits, but such effects should be taken into account to avoid confusion with the possible mitochondrial effects. The posterior means of the genetic and phenotypic correlations between fat and protein content are high and negative.
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Table 2. Estimated statistics of marginal posterior distributions of variance ratios: heritability (h2 =  /2P) and common litter environmental coefficient (c2 =  /2P) of the contents of intramuscular fat (IMF) and of protein in M. longissimus dorsi of Torbiscal Iberian pigs, and genetic, common environmental, and phenotypic correlations (G, C, and P) between the 2 traits
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Haplotype H2 is the predominant mitochondrial type in the set of analyzed pigs (132 out of 319 pigs with records = 41.4%). The remaining haplotype frequencies are 5.3% (H1), 10.7% (H3), 7.2% (H4), 10.0% (H5), and 25.4% (H6), and their effects on the LD composition are expressed as differences with respect to the most frequent haplotype (H2) in Table 3. The results of the H3 – H2 contrast show a higher content of intramuscular fat in H3 pigs: 1.17 g/100 g of muscle, with a positive value probability of 0.972 calculated from the marginal posterior density. In agreement with the negative correlation between both traits, the H3 pigs present lower protein content: –0.49 g/100 g of muscle, with a negative value probability of 0.996. In spite of the low frequency of some haplotypes, similar results (not summarized in the table) were obtained for H3 haplotype with H1, H4, H5, and H6 haplotype contrasts. The posterior means of the corresponding contrasts are 1.33, 0.81, 1.09, and 1.25 g/100 g muscle for IMF, with positive value probabilities of 0.941, 0.807, 0.915, and 0.974, respectively. The equivalent results for protein content are –0.58, –0.65, –0.41, and –0.54 g/100 g of muscle, with negative value probabilities of 0.987, 0.991, 0.959, and 0.996, respectively. No differences were found between the other mtDNA haplotypes.
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Table 3. Estimated statistics of marginal posterior distributions of the effects of mtDNA haplotypes of the Torbiscal Iberian pig line on the contents of intramuscular fat (IMF) and of protein in M. longissimus dorsi expressed as differences with respect to the H2 type
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To identify the possible causative mutation of these effects, we have sequenced the complete mtDNA of 6 Torbiscal pigs representative of the 6 determined mtDNA haplotypes. The alignment of these 6 sequences allowed identification of 32 SNP and 2 indels (Table 4). Nine of them were located in the D-loop regulatory region, 1 in a tRNA, 3 in rRNA, and 21 in protein-coding genes. Seven of the substitutions detected in these genes produce amino acid replacements: 2 in NADH-ubiquinone oxidoreductase chain-2 (NADH2) consisting of 4104A (Thr) > T (Ser) and 4516T (Ile) > C (Thr), 3 in ATPase 6 consisting of 8091 T (Trp) > A (Leu), 8351C(Pro) > T(Leu) and 8347G (Ala) > A (Thr), and 2 in Cytochrome b (Cyt b) consisting of 14742C (Ala) > T (Val) and 15266A (Ile) > G (Val). The remaining 14 SNP in protein-coding genes were synonymous.
Two out of the 34 polymorphic positions were exclusively detected in the sequence corresponding to haplotype H3. These were the synonymous substitution 9104C > T in the gene-coding region of Cytochrome c oxidase subunit III (COIII) and 715A > G substitution in 12S rRNA. The exclusive presence of these substitutions in the haplotype H3 was verified by genotyping a greater number of Torbiscal DNA samples, including samples for each different maternal lineage and mtDNA haplotype (Table 5). The results corroborated that the 715G and 9104T substitutions are exclusively present in pigs of the founder sow number 1 (haplotype H3) maternal lineage and absent in the remaining maternal lineages and mtDNA types.
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Table 5. Estimated frequencies of the 2 identified candidate substitutions by founder maternal lineages and mtDNA haplotypes of the Torbiscal Iberian pig line
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DISCUSSION
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Association studies of mtDNA polymorphisms pose some sampling problems in populations of livestock (Boettcher et al., 1996) and human beings (Raule et al., 2007). Mitochondrial variation may diminish in closed populations by the transmission of mtDNA through a limited number of maternal lineages. To avoid this risk, the steers examined in the study of Mannen et al. (1998) were collected from all over Japan. The problem increases in polytocous species such as pigs or rabbits, in which particular maternal lineages may be quickly diffused. This fact is exemplified by the low number (9) of founder maternal lineages surviving in the Torbiscal pig line, genetically isolated since 1963. However, this line is a valuable genetic material for tracing back the mtDNA variation in Iberian pigs, due to its composite origin from 4 ancient Spanish and Portuguese strains (representative of the most important varieties of this breed) and the availability of a complete and reliable genealogical record back to its origin (Fernández et al., 2002; Fabuel et al., 2004). Founder genetic origin diversity explains the high number (34) of mtDNA polymorphisms detected in this closed line. As a reference, only 27 nucleotide substitutions were found in the mitochondrial sequences quoted in a survey of Japanese Black cattle (Mannen et al., 2003).
Boettcher et al. (1996) outlined another problem of mtDNA polymorphism association studies. If variability within maternal lineages exists across the entire mtDNA genome, then assigning genotypes to maternal lineages on the basis of 1 or 2 sequenced animals may be inappropriate. In the present study, a deeper genotypic analysis of the 2 candidate nucleotide substitutions validated the initial assignation of these genotypes to founder maternal lineages based on the sequencing of only 1 pig per mtDNA haplotype.
The 2 detected candidate substitutions are located in essential mitochondrial genes, 12S rRNA and Cytochrome c oxidase subunit 3; however the functional effects of these mutations are not easily explainable. Cytochrome c oxidase is the terminal enzyme complex of the respiratory chain found in the mitochondrial inner membrane (Capaldi, 1990). In mammals, there are interacting subunits encoded by mitochondrial and nuclear DNA. In the present study, we have found a substitution, 9104C > T, in the mitochondrial subunit 3, which does not change the amino acid composition, although this nucleotide position is very well conserved between mammals, based on the alignment of mtDNA sequences available in GenBank. Recently, it has been shown that synonymous mutations can modify protein abundance, probably mediated by alteration in mRNA stability, and protein structure and activity, by induction of translational pausing. It has also been suggested that they can disrupt splicing and interfere with miRNA binding (Parmley and Hurst, 2007). We have tried to investigate changes in secondary structure due to C/T transition, using the GeneBee RNA secondary structure prediction tool based on phylogenetic considerations for energy optimization (Brodsky et al., 1995). The predicted results did not show notable changes between the 2 structures, and it only estimates a change in free energy of 0.2 kcal/mol.
Ribosomal RNA has a primary functional role in almost of all the processes of protein synthesis: binding aminoacyl-tRNA and mRNA, binding initiation, elongation, and termination factors, and in peptide bond formation (Dahlberg, 1989). More recently, another function for the mitochondrial ribosomal RNA has been proposed regarding protein folding in mitochondria, as in nuclear chaperones (Sulijoadikusumo et al., 2001). Secondary structures of ribosomal RNA, stems and loops, have a crucial relevance for their functional activities. In this way, changes in rRNA sequences could alter their secondary structure, the function of the ribosome and hence the protein synthesis rate, which may affect phenotypic traits. The substitution 715A > G detected in the present study occurs in a very well conserved nucleotide position in mammals, which may indicate the importance of this nucleotide for ribosomal function. Besides, we have tried to investigate changes in secondary structure due to A/G transition in the RNA molecule, using the GeneBee RNA secondary structure prediction tool. The results showed a notable change between the predicted structures of the 2 variants in the substitution region, implicating an estimated free energy change of 1 kcal/mol.
Some previous studies support the causal relationship between the substitution in 12S rRNA and the detected effects in the present analysis for muscle composition. Expression studies in subcutaneous and visceral fat tissues in cattle, pig, and mouse detected differential 12S rRNA expression patterns related to species, tissues, and diets (Hishikawa et al., 2005). Another study performed by Mannen et al. (2003) identified a substitution in a ribosomal RNA (16S) as a strong candidate for the mitochondrial effect detected on meat quality in a population of Japanese Black steers. Finally, Boettcher et al. (1996), in a similar study performed in Holstein cows, found significant effects of ribosomal RNA polymorphisms on yield traits, although it should be noted that analyses carried out in that study were exclusively based on ribosomal RNA genes.
The associated effect of the candidate substitutions on loin IMF content is important and could justify the use of the 715A > G polymorphism as a marker for maintaining an adequate IMF level when selecting to improve the weight of premium cuts in Iberian pigs. However, several complementary studies should be performed to validate the association of haplotype H3 polymorphisms with meat quality traits, as well as to evaluate possible undesirable changes in other economically important traits. Moreover, the diffusion through maternal lineages of mitochondria carrying the 715G nucleotide is a slow process. In a preliminary survey, we have genotyped an additional 75 Iberian pigs, belonging to different populations and unknown maternal lineage, for both candidate substitutions, and only 1 individual carried the 715G nucleotide (jointly with the 9104T). This low frequency could be a handicap to confirm the reported results, and much additional research would be required.
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Footnotes
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1 The authors acknowledge the staff of the CIA Dehesón del Encinar for animal care, Rita Benítez for technical assistance, L. Varona for original software for Gibbs sampling, and Miguel Toro and Jesús Fernández for useful comments. This research was funded by INIA RZ03-010 grant. 
2 Corresponding author: avila{at}inia.es
Received for publication September 7, 2007.
Accepted for publication February 29, 2008.
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Abstract
INTRODUCTION
