The PPR domain of mitochondrial RNA polymerase is an exoribonuclease required for mtDNA replication in Drosophila melanogaster

Nat Cell Biol. 2022 May;24(5):757-765. doi: 10.1038/s41556-022-00887-y. Epub 2022 Apr 21.

Abstract

Mitochondrial DNA (mtDNA) replication and transcription are of paramount importance to cellular energy metabolism. Mitochondrial RNA polymerase is thought to be the primase for mtDNA replication. However, it is unclear how this enzyme, which normally transcribes long polycistronic RNAs, can produce short RNA oligonucleotides to initiate mtDNA replication. We show that the PPR domain of Drosophila mitochondrial RNA polymerase (PolrMT) has 3'-to-5' exoribonuclease activity, which is indispensable for PolrMT to synthesize short RNA oligonucleotides and prime DNA replication in vitro. An exoribonuclease-deficient mutant, PolrMTE423P, partially restores mitochondrial transcription but fails to support mtDNA replication when expressed in PolrMT-mutant flies, indicating that the exoribonuclease activity is necessary for mtDNA replication. In addition, overexpression of PolrMTE423P in adult flies leads to severe neuromuscular defects and a marked increase in mtDNA transcript errors, suggesting that exoribonuclease activity may contribute to the proofreading of mtDNA transcription.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • DNA Replication / genetics
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / metabolism
  • Exoribonucleases* / genetics
  • Mitochondrial Proteins / metabolism
  • Oligonucleotides
  • RNA / genetics
  • RNA, Mitochondrial / genetics

Substances

  • DNA, Mitochondrial
  • Mitochondrial Proteins
  • Oligonucleotides
  • RNA, Mitochondrial
  • RNA
  • Exoribonucleases