Elucidation of the RNA Recognition Code for Pentatricopeptide Repeat Proteins Involved in Organelle RNA Editing in Plants

Yusuke Yagi,Keiko Kobayashi,Takashi Hirayama,Shimpei Hayashi,Takahiro Nakamura,Carol J Wilusz

doi:10.1371/journal.pone.0057286

Yusuke Yagi, Keiko Kobayashi + Show 4 more

Open Access

https://doi.org/10.1371/journal.pone.0057286

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Abstract

Pentatricopeptide repeat (PPR) proteins are eukaryotic RNA-binding proteins that are commonly found in plants. Organelle transcript processing and stability are mediated by PPR proteins in a gene-specific manner through recognition by tandem arrays of degenerate 35-amino-acid repeating units, the PPR motifs. However, the sequence-specific RNA recognition mechanism of the PPR protein remains largely unknown. Here, we show the principle underlying RNA recognition for PPR proteins involved in RNA editing. The distance between the PPR-RNA alignment and the editable C was shown to be conserved. Amino acid variation at 3 particular positions within the motif determined recognition of a specific RNA in a programmable manner, with a 1-motif to 1-nucleotide correspondence, with no gap sequence. Data from the decoded nucleotide frequencies for these 3 amino acids were used to assign accurate interacting sites to several PPR proteins for RNA editing and to predict the target site for an uncharacterized PPR protein.

Highlights

Plant mitochondria and chloroplasts, believed to have been acquired during ancient endosymbiotic events, participate in cellular biogenesis as factories for energy production, photosynthesis, and metabolite synthesis [1,2]
We showed that 3 amino acids (1, 4, and ‘‘ii’’[-2]) comprised the nucleotide-specifying residue (NSR) of pentatricopeptide repeat (PPR) motifs, determining the sequencespecific recognition of target RNA sequences
We showed that the decoded nucleotide frequency for the 3 NSRs could facilitate in silico prediction of RNA targets for editing PPR proteins

Summary

Introduction

Plant mitochondria and chloroplasts, believed to have been acquired during ancient endosymbiotic events, participate in cellular biogenesis as factories for energy production, photosynthesis, and metabolite synthesis [1,2]. These organelles contain limited genetic information; as such, numerous nuclear-encoded factors are imported into them to perform various cellular functions. Roughly 30 individual PPR proteins have been assigned to 1 or several targets each by connecting dysfunctional genes with the loss of RNA editing at specific sites both in chloroplasts and mitochondria [7,8]

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