Phase separation drives the self-assembly of mitochondrial nucleoids for transcriptional modulation

Nat Struct Mol Biol. 2021 Nov;28(11):900-908. doi: 10.1038/s41594-021-00671-w. Epub 2021 Oct 28.

Abstract

Mitochondria, the only semiautonomous organelles in mammalian cells, possess a circular, double-stranded genome termed mitochondrial DNA (mtDNA). While nuclear genomic DNA compaction, chromatin compartmentalization and transcription are known to be regulated by phase separation, how the mitochondrial nucleoid, a highly compacted spherical suborganelle, is assembled and functions is unknown. Here we assembled mitochondrial nucleoids in vitro and show that mitochondrial transcription factor A (TFAM) undergoes phase separation with mtDNA to drive nucleoid self-assembly. Moreover, nucleoid droplet formation promotes recruitment of the transcription machinery via a special, co-phase separation that concentrates transcription initiation, elongation and termination factors, and retains substrates to facilitate mtDNA transcription. We propose a model of mitochondrial nucleoid self-assembly driven by phase separation, and a pattern of co-phase separation involved in mitochondrial transcriptional regulation, which orchestrates the roles of TFAM in both mitochondrial nucleoid organization and transcription.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomolecular Condensates / physiology
  • Cell Line
  • DNA, Mitochondrial / genetics*
  • DNA-Binding Proteins / metabolism*
  • Gene Expression Regulation / genetics*
  • Genome, Mitochondrial / genetics
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Mice
  • Mitochondria / genetics*
  • Mitochondria / metabolism
  • Mitochondrial Proteins / metabolism*
  • Transcription Factors / metabolism*
  • Transcription, Genetic / genetics*

Substances

  • DNA, Mitochondrial
  • DNA-Binding Proteins
  • Mitochondrial Proteins
  • Transcription Factors
  • mitochondrial transcription factor A