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.

The genus Paedocypris is a newly described taxon of minifish species that are characterized by extensive chromosome evolution and one of the smallest known vertebrate nuclear genomes. Paedocypris features a tiny adult size, a short generation time, low fecundity and fragmented tropical habitats, which are factors that favor rapid speciation. Most recently, we have revealed that P. progenetica (Pp), the type species of the genus Paedocypris, has an unusual mtDNA bearing - within its D-loop - a tandem array of a 34-bp repeat sequence called the minifish repeat, which shows compromised replication efficiency in vitro. Here we report that Pp exhibits high genetic variation in mtDNA size. The efficiency of D-loop amplification was found to depend upon primers. Interestingly, Pp individuals of one and the same population differed drastically in mtDNA size resulting from varying copy numbers of the minifish repeat. We conclude that minifish has a high mutation rate and perhaps represents a rapidly evolving taxon of vertebrates.

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