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. 2020 Oct 19;21(1):720.
doi: 10.1186/s12864-020-07018-7.

Expression of mitochondrial protein genes encoded by nuclear and mitochondrial genomes correlate with energy metabolism in dairy cattle

Jigme Dorji  1   2 , Christy J Vander Jagt  3 , Josie B Garner  4 , Leah C Marett  4 , Brett A Mason  3 , Coralie M Reich  3 , Ruidong Xiang  3   5 , Emily L Clark  6 , Benjamin G Cocks  7   3 , Amanda J Chamberlain  3 , Iona M MacLeod  3 , Hans D Daetwyler  7   3
Affiliations

Expression of mitochondrial protein genes encoded by nuclear and mitochondrial genomes correlate with energy metabolism in dairy cattle

Jigme Dorji et al. BMC Genomics. .

Erratum in

Abstract

Background: Mutations in the mitochondrial genome have been implicated in mitochondrial disease, often characterized by impaired cellular energy metabolism. Cellular energy metabolism in mitochondria involves mitochondrial proteins (MP) from both the nuclear (NuMP) and mitochondrial (MtMP) genomes. The expression of MP genes in tissues may be tissue specific to meet varying specific energy demands across the tissues. Currently, the characteristics of MP gene expression in tissues of dairy cattle are not well understood. In this study, we profile the expression of MP genes in 29 adult and six foetal tissues in dairy cattle using RNA sequencing and gene expression analyses: particularly differential gene expression and co-expression network analyses.

Results: MP genes were differentially expressed (DE; over-expressed or under-expressed) across tissues in cattle. All 29 tissues showed DE NuMP genes in varying proportions of over-expression and under-expression. On the other hand, DE of MtMP genes was observed in < 50% of tissues and notably MtMP genes within a tissue was either all over-expressed or all under-expressed. A high proportion of NuMP (up to 60%) and MtMP (up to 100%) genes were over-expressed in tissues with expected high metabolic demand; heart, skeletal muscles and tongue, and under-expressed (up to 45% of NuMP, 77% of MtMP genes) in tissues with expected low metabolic rates; leukocytes, thymus, and lymph nodes. These tissues also invariably had the expression of all MtMP genes in the direction of dominant NuMP genes expression. The NuMP and MtMP genes were highly co-expressed across tissues and co-expression of genes in a cluster were non-random and functionally enriched for energy generation pathway. The differential gene expression and co-expression patterns were validated in independent cow and sheep datasets.

Conclusions: The results of this study support the concept that there are biological interaction of MP genes from the mitochondrial and nuclear genomes given their over-expression in tissues with high energy demand and co-expression in tissues. This highlights the importance of considering MP genes from both genomes in future studies related to mitochondrial functions and traits related to energy metabolism.

Keywords: Cattle; Differential gene expression; Energy metabolism; Gene co-expression; Mitochondria.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Percentage of differentially expressed genes by gene categories for 29 tissues in the Main Cows dataset. m. = muscle, LN = lymph node; Gene category: All = All protein coding genes from nuclear and mitochondrial genomes, Nu = Mitochondrial protein coding genes from the nuclear genome (NuMP), Mt = Mitochondrial protein coding genes from the mitochondrial genome (MtMP)
Fig. 2
Fig. 2
Heatmap of nuclear genome encoded mitochondrial protein (NuMP) gene expression the Main Cows dataset. 6819 and 2181 are Cow No. 6819 and Cow No. 2181 respectively
Fig. 3
Fig. 3
Heatmap of mitochondrial genome encoded mitochondrial protein (MtMP) gene expression in the Main Cows dataset. Based on the log2 counts per million of MtMP genes across 29 tissues from cows 6819 and 2181
Fig. 4
Fig. 4
Gene co-expression network clusters across tissues in the Main Cows based on similarity matrix computed using Pearson correlations > |0.95|
Fig. 5
Fig. 5
Scatterplot of log2 fold change values of differentially expressed mitochondrial protein genes from nuclear genome in the Main Cows against the Validation Cow
Fig. 6
Fig. 6
Venn diagram showing the number of genes in common among the NuMP-MtMP co-expression clusters. a. Mitochondrial protein genes encoded by the nuclear genome (NuMP genes), b. Mitochondrial protein genes encoded by the mitochondrial genome (MtMP genes) and c. non-mitochondrial protein genes from nuclear genomes in common between the Main Cows and Validation Cow
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