Translational Landscape of Protein-Coding and Non-Protein-Coding RNAs upon Light Exposure in Arabidopsis

Plant Cell Physiol. 2020 Mar 1;61(3):536-545. doi: 10.1093/pcp/pcz219.

Abstract

Light is one of the most essential environmental clues for plant growth and morphogenesis. Exposure to blue monochromatic light from darkness is a turning point for plant biological activity, and as a result dramatic changes in gene expression occur. To understand the translational impacts of blue light, we have performed ribosome profiling analysis and called translated open reading frames (ORFs) de novo within not only mRNAs but also non-coding RNAs (ncRNAs). Translation efficiency of 3,823 protein-coding ORFs, such as nuclear chloroplast-related genes, was up-regulated by blue light exposure. Moreover, the translational activation of the microRNA biogenesis-related genes, DCL1 and HYL1, was induced by blue light. Considering the 3-nucleotide codon periodicity of ribosome footprints, a few hundred short ORFs lying on ncRNAs and upstream ORFs (uORFs) on mRNAs were found that had differential translation status between blue light and dark. uORFs are known to have a negative effect on the expression of the main ORFs (mORFs) on the same mRNAs. Our analysis suggests that the translation of uORFs is likely to be more stimulated than that of the corresponding mORFs, and uORF-mediated translational repression of the mORFs in five genes was alleviated by blue light exposure. With data-based annotation of the ORFs, our analysis provides insights into the translatome in response to environmental changes, such as those involving light.

Keywords: Light exposure; Ribosome profiling; Translatome; ncRNA; sORF; uORF.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Gene Expression Regulation, Plant / radiation effects
  • Light*
  • MicroRNAs / biosynthesis
  • Open Reading Frames / genetics
  • Protein Biosynthesis
  • Protein Processing, Post-Translational / physiology*
  • Protein Processing, Post-Translational / radiation effects*
  • RNA, Messenger / metabolism
  • RNA, Untranslated / metabolism*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Ribonuclease III / genetics
  • Ribonuclease III / metabolism
  • Ribosomes / metabolism

Substances

  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • HYL1 protein, Arabidopsis
  • MicroRNAs
  • RNA, Messenger
  • RNA, Untranslated
  • RNA-Binding Proteins
  • DCL1 protein, Arabidopsis
  • Ribonuclease III