Abstract

Mitochondrial homoplasmy signifies the existence of identical copies of mitochondrial DNA (mtDNA) and is essential for normal development, as heteroplasmy causes abnormal development and diseases in human. Homoplasmy in many organisms is ensured by maternal mtDNA inheritance through either absence of paternal mtDNA delivery or early elimination of paternal mtDNA. However, whether paternal mtDNA is transcribed has remained unknown. Here we report that paternal mtDNA shows late elimination and transcriptional quiescence in cyprinid fishes. Paternal mtDNA was present in zygotes but absent in larvae and adult organs of goldfish and blunt-snout bream, demonstrating paternal mtDNA delivery and elimination for maternal mtDNA inheritance. Surprisingly, paternal mtDNA remained detectable up to the heartbeat stage, suggesting its late elimination leading to embryonic heteroplasmy up to advanced embryogenesis. Most importantly, we never detected the cytb RNA of paternal mtDNA at all stages when paternal mtDNA was easily detectable, which reveals that paternal mtDNA is transcriptionally quiescent and thus excludes its effect on the development of heteroplasmic embryos. Therefore, paternal mtDNA in cyprinids shows late elimination and transcriptional quiescence. Clearly, transcriptional quiescence of paternal mtDNA represents a new mechanism for maternal mtDNA inheritance and provides implications for treating mitochondrion-associated diseases by mitochondrial transfer or replacement.

Highlights

  • The mitochondrion (MT) is a membraned organelle present in all eukaryotic organisms

  • We have performed a hybrid analysis of the germline transmission and behavior of fertilization-delivered paternal mitochondrial DNA (mtDNA) in goldfish and blunt-snout bream as a model of cyprinid fishes

  • We show that Maternally uniparental inheritance (MUI) operates in both cyprinid fishes as in the majority of organisms examined so far[1,3,16,32,36]

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Summary

Introduction

The mitochondrion (MT) is a membraned organelle present in all eukaryotic organisms. MT converts the energy of food molecules into ATP to support cellular and organismal metabolism, and is involved in regulating diverse processes such as apoptosis and innate immunity[1,2]. The human mtDNA is a double-stranded circular molecule and 16,569 bp in length, has a D-loop as the control region for replication and transcription, and 37 genes for 13 proteins, 22 transfer RNAs and 2 ribosomal RNAs3 These mtDNA features are highly conserved in diverse animal phyla including fish[4,5]. Exceptions are certain bivalve mollusks, which show doubly uniparental inheritance (DUI)[17] These mollusks have two distinct mtDNAs, namely female type (F-type) mtDNA and male type (M-type) mtDNA. Female mollusks possess only F-type mtDNA and are hemoplasmic, and males are heteroplasmic because they have F-type in their somatic organs and M-type mtDNAs in their gonads. We demonstrate that paternal mtDNA can persist to fairly advanced stages of embryogenesis and remains transcriptionally quiescent, excluding its phenotypic contribution to the developing embryos

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