Mitochondrial-nuclear crosstalk, haplotype and copy number variation distinct in muscle fiber type, mitochondrial respiratory and metabolic enzyme activities

Xuan Liu,Siriluck Ponsuksili,Klaus Wimmers,Eduard Murani,Nares Trakooljul,Frieder Hadlich

doi:10.1038/s41598-017-14491-w

Xuan Liu, Siriluck Ponsuksili + Show 4 more

Open Access

https://doi.org/10.1038/s41598-017-14491-w

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Abstract

Genes expressed in mitochondria work in concert with those expressed in the nucleus to mediate oxidative phosphorylation (OXPHOS), a process that is relevant for muscle metabolism and meat quality. Mitochondrial genome activity can be efficiently studied and compared in Duroc and Pietrain pigs, which harbor different mitochondrial haplotypes and distinct muscle fiber types, mitochondrial respiratory activities, and fat content. Pietrain pigs homozygous-positive for malignant hyperthermia susceptibility (PiPP) carried only haplotype 8 and showed the lowest absolute mtDNA copy number accompanied by a decrease transcript abundance of mitochondrial-encoded subunits ND1, ND6, and ATP6 and nuclear-encoded subunits NDUFA11 and NDUFB8. In contrast, we found that haplotype 4 of Duroc pigs had significantly higher mitochondrial DNA (mtDNA) copy numbers and an increase transcript abundance of mitochondrial-encoded subunits ND1, ND6, and ATP6. These results suggest that the variation in mitochondrial and nuclear genetic background among these animals has an effect on mitochondrial content and OXPHOS system subunit expression. We observed the co-expression pattern of mitochondrial and nuclear encoded OXPHOS subunits suggesting that the mitochondrial-nuclear crosstalk functionally involves in muscle metabolism. The findings provide valuable information for understanding muscle biology processes and energy metabolism, and may direct use for breeding strategies to improve meat quality and animal health.

Highlights

Mitochondria are involved in many key cellular processes such as apoptosis, calcium homeostasis, reactive oxygen species production, and most importantly, adenosine triphosphate (ATP) generation by oxidative phosphorylation (OXPHOS)
Pietrain homozygous-negative for MHS (PiNN) pigs had the highest activity of phosphofructokinase (PFK), whereas no significant differences in the activities of glycogen phosphorylase (GP) and lactate dehydrogenase (LDH) were detected among breeds
Specific expression pattern of mt transcript including ND1, ND6, and ATP6 and nuclear-encoded subunits NDUFA11 and NDUFB8 was identified and in turn play a role in muscle fibers type and enzyme activities of complex I. All of these changes in the positive for malignant hyperthermia susceptibility (PiPP) haplotype 8 pigs may partially contribute to negative outcomes of meat quality such as pale soft exudative pork

Summary

Introduction

Mitochondria are involved in many key cellular processes such as apoptosis, calcium homeostasis, reactive oxygen species production, and most importantly, adenosine triphosphate (ATP) generation by oxidative phosphorylation (OXPHOS) These organelles contain their own DNA distinct from the nuclear genome. PiPP pigs showed increased drip loss and shear force comparing to other three pig breeds These results directly supported the association between muscle fiber type and meat quality. We investigated mtDNA variation genes involved in mtDNA copy number in conjunction with muscle fiber types and metabolic enzyme activities in postmortem longissimus muscles (LM) from four different pig breeds: Duroc, Pietrain homozygous-negative for MHS (PiNN), Pietrain homozygous-positive for MHS (PiPP), and an F2 crossbred Duroc-Pietrain homozygous-negative for MHS (DuPi)

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