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. 2016 Dec 9;11(12):e0167858.
doi: 10.1371/journal.pone.0167858. eCollection 2016.

Developmental Stage, Muscle and Genetic Type Modify Muscle Transcriptome in Pigs: Effects on Gene Expression and Regulatory Factors Involved in Growth and Metabolism

Miriam Ayuso  1 , Almudena Fernández  2 , Yolanda Núñez  2 , Rita Benítez  2 , Beatriz Isabel  1 , Ana I Fernández  2 , Ana I Rey  1 , Antonio González-Bulnes  3 , Juan F Medrano  4 , Ángela Cánovas  4 , Clemente J López-Bote  1 , Cristina Óvilo  2
Affiliations

Developmental Stage, Muscle and Genetic Type Modify Muscle Transcriptome in Pigs: Effects on Gene Expression and Regulatory Factors Involved in Growth and Metabolism

Miriam Ayuso et al. PLoS One. .

Abstract

Iberian pig production includes purebred (IB) and Duroc-crossbred (IBxDU) pigs, which show important differences in growth, fattening and tissue composition. This experiment was conducted to investigate the effects of genetic type and muscle (Longissimus dorsi (LD) vs Biceps femoris (BF)) on gene expression and transcriptional regulation at two developmental stages. Nine IB and 10 IBxDU piglets were slaughtered at birth, and seven IB and 10 IBxDU at four months of age (growing period). Carcass traits and LD intramuscular fat (IMF) content were measured. Muscle transcriptome was analyzed on LD samples with RNA-Seq technology. Carcasses were smaller in IB than in IBxDU neonates (p < 0.001), while growing IB pigs showed greater IMF content (p < 0.05). Gene expression was affected (p < 0.01 and Fold change > 1.5) by the developmental stage (5,812 genes), muscle type (135 genes), and genetic type (261 genes at birth and 113 at growth). Newborns transcriptome reflected a highly proliferative developmental stage, while older pigs showed upregulation of catabolic and muscle functioning processes. Regarding the genetic type effect, IBxDU newborns showed enrichment of gene pathways involved in muscle growth, in agreement with the higher prenatal growth observed in these pigs. However, IB growing pigs showed enrichment of pathways involved in protein deposition and cellular growth, supporting the compensatory gain experienced by IB pigs during this period. Moreover, newborn and growing IB pigs showed more active glucose and lipid metabolism than IBxDU pigs. Moreover, LD muscle seems to have more active muscular and cell growth, while BF points towards lipid metabolism and fat deposition. Several regulators controlling transcriptome changes in both genotypes were identified across muscles and ages (SIM1, PVALB, MEFs, TCF7L2 or FOXO1), being strong candidate genes to drive expression and thus, phenotypic differences between IB and IBxDU pigs. Many of the identified regulators were known to be involved in muscle and adipose tissues development, but others not previously associated with pig muscle growth were also identified, as PVALB, KLF1 or IRF2. The present study discloses potential molecular mechanisms underlying phenotypic differences observed between IB and IBxDU pigs and highlights candidate genes implicated in these molecular mechanisms.

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Conflict of interest statement

The authors have declared that no competing interests exist, excepting that the coauthors Antonio Gonzalez-Bulnes and Cristina Óvilo are PLOS ONE Editorial Board members. However, this does not alter the authors’ adherence to all the PLOS ONE policies.

Figures

Fig 1
Fig 1. Venn diagram showing common differentially expressed genes across studied conditions.
Developmental stage, the biggest studied effect, shows several common differentially expressed genes with other effects, while expression of any gene was affected by the three studied effects.
Fig 2
Fig 2. Enriched biological functions related to body growth in growing Iberian (IB) pigs.
The network generated by IPA software shows enriched biological functions in IB pigs (blue color) and genes predicted to be involved in enrichment of these functions. The activation of cell proliferation and body size in growing IB pigs might be related to a compensatory growth occurring in those pigs when compared to crossbred (IBxDU) pigs during the early growing period.
Fig 3
Fig 3. Enriched biological functions related to growth and development in newborn Iberian (IB) piglets.
The activation of muscle atrophy and the upregulation of genes involved in protein metabolism and degradation in IB pigs suggests a more active protein turnover in these pigs when compared to crossbred (IBxDU) pigs. Functions associated with animal growth were also enriched in IB newborn pigs.
Fig 4
Fig 4. Enriched biological functions related to lipid metabolism in growing Iberian (IB) pigs.
The network generated by IPA software shows metabolism-related enriched biological functions in IB pigs. Concentration of lipid seems to be a more active process in IB pigs, in agreement with phenotypic differences observed in loin intramuscular fat content.
Fig 5
Fig 5. Adipogenesis pathway.
Several transcription factor identified in the regulators study and one gene upregulated in Iberian pigs are involved in the adipogenesis pathway, most of them regulate PPARg expression or activation.
Fig 6
Fig 6. Enriched biological functions in Biceps femoris (BF) muscle.
The network generated by IPA software shows enriched biological functions in BF muscle, suggesting that lipid metabolism is more active in BF when compared to Longissimus dorsi muscle.
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Grants and funding

The experimental work was supported by funds from the Spanish Ministry of Science and Innovation (project AGL2010-21991-C03) and the Ministry of Economy and Competitiveness (project AGL2013-48121-C3), co-funded by FEDER. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Miriam Ayuso was granted by the Ministry of Science and Innovation (BES-2011-045136).