Volume 43 Issue 1
Jan.  2022
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Ran Xu, Mariangela Iannello, Justin C. Havird, Liliana Milani, Fabrizio Ghiselli. Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes. Zoological Research, 2022, 43(1): 111-128. doi: 10.24272/j.issn.2095-8137.2021.348
Citation: Ran Xu, Mariangela Iannello, Justin C. Havird, Liliana Milani, Fabrizio Ghiselli. Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes. Zoological Research, 2022, 43(1): 111-128. doi: 10.24272/j.issn.2095-8137.2021.348

Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes

doi: 10.24272/j.issn.2095-8137.2021.348
Funds:  This work was supported by the China Scholarship Council, Italian Ministry of Education University and Research (MIUR) FIR2013 Programme (RBFR13T97A to F.G.), MIUR SIR Programme (RBSI14G0P5 to L.M.), Canziani Bequest to F.G., and “Ricerca Fondamentale Orientata” (RFO) from the University of Bologna to F.G. and L.M.
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  • In most eukaryotes, oxidative phosphorylation (OXPHOS) is the main energy production process and it involves both mitochondrial and nuclear genomes. The close interaction between the two genomes is critical for the coordinated function of the OXPHOS process. Some bivalves show doubly uniparental inheritance (DUI) of mitochondria, where two highly divergent mitochondrial genomes, one inherited through eggs (F-type) and the other through sperm (M-type), coexist in the same individual. However, it remains a puzzle how nuclear OXPHOS genes coordinate with two divergent mitochondrial genomes in DUI species. In this study, we compared transcription, polymorphism, and synonymous codon usage in the mitochondrial and nuclear OXPHOS genes of the DUI species Ruditapes philippinarum using sex- and tissue-specific transcriptomes. Mitochondrial and nuclear OXPHOS genes showed different transcription profiles. Strong co-transcription signal was observed within mitochondrial (separate for F- and M-type) and within nuclear OXPHOS genes but the signal was weak or absent between mitochondrial and nuclear OXPHOS genes, suggesting that the coordination between mitochondrial and nuclear OXPHOS subunits is not achieved transcriptionally. McDonald-Kreitman and frequency-spectrum based tests indicated that M-type OXPHOS genes deviated significantly from neutrality, and that F-type and M-type OXPHOS genes undergo different selection patterns. Codon usage analysis revealed that mutation bias and translational selection were the major factors affecting the codon usage bias in different OXPHOS genes, nevertheless, translational selection in mitochondrial OXPHOS genes appears to be less efficient than nuclear OXPHOS genes. Therefore, we speculate that the coordination between OXPHOS genes may involve post-transcriptional/translational regulation.
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