Biophysical analysis of Arabidopsis protein-only RNase P alone and in complex with tRNA provides a refined model of tRNA binding

J Biol Chem. 2017 Aug 25;292(34):13904-13913. doi: 10.1074/jbc.M117.782078. Epub 2017 Jul 10.

Abstract

RNase P is a universal enzyme that removes 5' leader sequences from tRNA precursors. The enzyme is therefore essential for maturation of functional tRNAs and mRNA translation. RNase P represents a unique example of an enzyme that can occur either as ribonucleoprotein or as protein alone. The latter form of the enzyme, called protein-only RNase P (PRORP), is widespread in eukaryotes in which it can provide organellar or nuclear RNase P activities. Here, we have focused on Arabidopsis nuclear PRORP2 and its interaction with tRNA substrates. Affinity measurements helped assess the respective importance of individual pentatricopeptide repeat motifs in PRORP2 for RNA binding. We characterized the PRORP2 structure by X-ray crystallography and by small-angle X-ray scattering in solution as well as that of its complex with a tRNA precursor by small-angle X-ray scattering. Of note, our study reports the first structural data of a PRORP-tRNA complex. Combined with complementary biochemical and biophysical analyses, our structural data suggest that PRORP2 undergoes conformational changes to accommodate its substrate. In particular, the catalytic domain and the RNA-binding domain can move around a central hinge. Altogether, this work provides a refined model of the PRORP-tRNA complex that illustrates how protein-only RNase P enzymes specifically bind tRNA and highlights the contribution of protein dynamics to achieve this specific interaction.

Keywords: PRORP; RNA processing; X-ray crystallography; pentatricopeptide repeat (PPR); precursor tRNA (pre-tRNA); ribonuclease P (RNase P); small-angle X-ray scattering (SAXS); tRNA maturation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Substitution
  • Arabidopsis / enzymology
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Biophysical Phenomena
  • Catalytic Domain
  • Enzyme Stability
  • Models, Molecular*
  • Mutation
  • Nucleic Acid Conformation
  • Nucleotide Motifs
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • RNA / chemistry
  • RNA / metabolism
  • RNA Precursors / chemistry
  • RNA Precursors / metabolism*
  • RNA Processing, Post-Transcriptional*
  • RNA, Plant / chemistry
  • RNA, Plant / metabolism*
  • RNA, Transfer, Cys / chemistry
  • RNA, Transfer, Cys / metabolism*
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Ribonuclease P / chemistry
  • Ribonuclease P / genetics
  • Ribonuclease P / metabolism*
  • Solubility

Substances

  • Arabidopsis Proteins
  • Peptide Fragments
  • RNA Precursors
  • RNA, Plant
  • RNA, Transfer, Cys
  • RNA, recombinant
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • RNA
  • PRORP2 protein, Arabidopsis
  • Ribonuclease P

Associated data

  • PDB/1U0B
  • PDB/4G23
  • PDB/5FT9