nMAT4, a maturase factor required for nad1 pre-mRNA processing and maturation, is essential for holocomplex I biogenesis in Arabidopsis mitochondria

Plant J. 2014 Apr;78(2):253-68. doi: 10.1111/tpj.12466. Epub 2014 Mar 26.

Abstract

Group II introns are large catalytic RNAs that are found in bacteria and organellar genomes of lower eukaryotes, but are particularly prevalent within mitochondria in plants, where they are present in many critical genes. The excision of plant mitochondrial introns is essential for respiratory functions, and is facilitated in vivo by various protein cofactors. Typical group II introns are classified as mobile genetic elements, consisting of the self-splicing ribozyme and its own intron-encoded maturase protein. A hallmark of maturases is that they are intron-specific, acting as cofactors that bind their intron-containing pre-RNAs to facilitate splicing. However, the degeneracy of the mitochondrial introns in plants and the absence of cognate intron-encoded maturase open reading frames suggest that their splicing in vivo is assisted by 'trans'-acting protein factors. Interestingly, angiosperms harbor several nuclear-encoded maturase-related (nMat) genes that contain N-terminal mitochondrial localization signals. Recently, we established the roles of two of these paralogs in Arabidopsis, nMAT1 and nMAT2, in the splicing of mitochondrial introns. Here we show that nMAT4 (At1g74350) is required for RNA processing and maturation of nad1 introns 1, 3 and 4 in Arabidopsis mitochondria. Seed germination, seedling establishment and development are strongly affected in homozygous nmat4 mutants, which also show modified respiration phenotypes that are tightly associated with complex I defects.

Keywords: Arabidopsis; group II intron; maturase; mitochondria; respiration; splicing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Arabidopsis Proteins / physiology*
  • Germination / genetics
  • Introns
  • Mitochondria / metabolism*
  • Mitochondria / ultrastructure
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Mitochondrial Proteins / physiology*
  • NADH Dehydrogenase / genetics
  • NADH Dehydrogenase / metabolism*
  • Phenotype
  • RNA Precursors / metabolism
  • RNA Processing, Post-Transcriptional
  • RNA Splicing
  • RNA, Messenger / metabolism
  • Seedlings / genetics
  • Seedlings / growth & development
  • Seedlings / metabolism

Substances

  • Arabidopsis Proteins
  • Mitochondrial Proteins
  • RNA Precursors
  • RNA, Messenger
  • nMAT4 protein, Arabidopsis
  • NADH Dehydrogenase
  • Nad1 protein, Arabidopsis