The RCC1 family protein RUG3 is required for splicing of nad2 and complex I biogenesis in mitochondria of Arabidopsis thaliana

Plant J. 2011 Sep;67(6):1067-80. doi: 10.1111/j.1365-313X.2011.04658.x. Epub 2011 Jul 6.

Abstract

We have identified a mitochondrial protein (RUG3) that is required for accumulation of mitochondrial respiratory chain complex I. RUG3 is related to human REGULATOR OF CHROMOSOME CONDENSATION 1 (RCC1) and Arabidopsis UV-B RESISTANCE 8 (UVR8). Although the family of RCC1-like proteins in Arabidopsis has over 20 members, UVR8 is the sole plant representative of this family to have been functionally characterized. Mitochondria from Arabidopsis plants lacking a functional RUG3 gene showed greatly reduced complex I abundance and activity. In contrast, accumulation of complexes III, IV and V of the oxidative phosphorylation system and the capacity for succinate-dependent respiration were unaffected. A comprehensive study of processes contributing to complex I biogenesis in rug3 mutants revealed that RUG3 is required for efficient splicing of the nad2 mRNA, which encodes a complex I subunit. A comparison of the formation of complex I assembly intermediates between rug3 and wild type mitochondria indicated that NAD2 enters the assembly pathway at an early stage. Remarkably, rug3 mutants displayed increased capacities for import of nucleus-encoded mitochondrial proteins into the organelle and showed moderately increased mitochondrial transcript levels. This observation is consistent with global transcript changes indicating enhanced mitochondrial biogenesis in the rug3 mutant in response to the complex I defect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / metabolism
  • Electron Transport Complex I / genetics*
  • Electron Transport Complex I / metabolism*
  • Electron Transport Complex III / metabolism
  • Electron Transport Complex IV / metabolism
  • Gene Expression Regulation, Plant
  • Mitochondria / genetics*
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism*
  • Mitochondrial Proton-Translocating ATPases / metabolism
  • Mutation
  • Phosphorylation
  • RNA Splicing
  • RNA, Messenger

Substances

  • Arabidopsis Proteins
  • Chromosomal Proteins, Non-Histone
  • Mitochondrial Proteins
  • RNA, Messenger
  • RUG3 protein, Arabidopsis
  • Uvr8 protein, Arabidopsis
  • complex V (mitochondrial oxidative phosphorylation system)
  • Electron Transport Complex IV
  • Mitochondrial Proton-Translocating ATPases
  • Electron Transport Complex I
  • Electron Transport Complex III