Persistence and Transcription of Paternal mtDNA Dependent on the Delivery Strategy Rather than Mitochondria Source in Fish Embryos

Cell Physiol Biochem. 2018;47(5):1898-1908. doi: 10.1159/000491070. Epub 2018 Jun 29.

Abstract

Background/aims: Mitochondria (MT) and mitochondrial DNA (mtDNA) show maternal inheritance in most eukaryotic organisms; the sperm mtDNA is usually delivered to the egg during fertilization and then rapidly eliminated to avoid heteroplasmy, which can affect embryogenesis. In our previous study, fertilization-delivered sperm mtDNA exhibited late elimination and transcriptional quiescence in cyprinid fish embryos. However, the mechanisms underlying elimination and transcriptional quiescence of paternal mtDNA are unclear.

Methods: Goldfish and zebrafish were used to investigate the fate of mtDNAs with different parental origins delivered by fertilization or microinjection in embryos. Goldfish MT from heart, liver and spermatozoa were microinjected into zebrafish zygotes, respectively. Specific PCR primers were designed so that the amplicons have different sizes to characterize goldfish and zebrafish cytb genes or their cDNAs.

Results: The MT injection-delivered paternal mtDNA from sperm, as well as those from the heart and liver, was capable of persistence and transcription until birth, in contrast to the disappearance and transcriptional quiescence at the heartbeat stage of fertilization-delivered sperm mtDNA. In addition, the exogenous MT-injected zebrafish embryos have normal morphology during embryonic development.

Conclusions: The fate of paternal mtDNA in fishes is dependent on the delivery strategy rather than the MT source, suggesting that the presence of sperm factor(s) is responsible for elimination and transcriptional quiescence of fertilization-delivered sperm mtDNA. These findings provide insights into the mechanisms underlying paternal mtDNA fate and heteroplasmy in cyprinid fishes.

Keywords: Heteroplasmy; Maternal inheritance; Mitochondria microinjection; MtDNA; Transcriptional quiescence.

MeSH terms

  • Animals
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism*
  • Embryo, Nonmammalian / embryology*
  • Goldfish / embryology*
  • Goldfish / genetics
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Zebrafish / embryology*
  • Zebrafish / genetics

Substances

  • DNA, Mitochondrial