A cell type-specific view on the translation of mRNAs from ROS-responsive genes upon paraquat treatment of Arabidopsis thaliana leaves

Plant Cell Environ. 2015 Feb;38(2):349-63. doi: 10.1111/pce.12355. Epub 2014 Jun 2.

Abstract

Oxidative stress causes dramatic changes in the expression levels of many genes. The formation of a functional protein through successful mRNA translation is central to a coordinated cellular response. To what extent the response towards reactive oxygen species (ROS) is regulated at the translational level is poorly understood. Here we analysed leaf- and tissue-specific translatomes using a set of transgenic Arabidopsis thaliana lines expressing a FLAG-tagged ribosomal protein to immunopurify polysome-bound mRNAs before and after oxidative stress. We determined transcript levels of 171 ROS-responsive genes upon paraquat treatment, which causes formation of superoxide radicals, at the whole-organ level. Furthermore, the translation of mRNAs was determined for five cell types: mesophyll, bundle sheath, phloem companion, epidermal and guard cells. Mesophyll and bundle sheath cells showed the strongest response to paraquat treatment. Interestingly, several ROS-responsive transcription factors displayed cell type-specific translation patterns, while others were translated in all cell types. In part, cell type-specific translation could be explained by the length of the 5'-untranslated region (5'-UTR) and the presence of upstream open reading frames (uORFs). Our analysis reveals insights into the translational regulation of ROS-responsive genes, which is important to understanding cell-specific responses and functions during oxidative stress.

Keywords: Arabidopsis; gene regulation; oxidative stress; tissue-specific; translation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions / genetics
  • Arabidopsis / cytology*
  • Arabidopsis / drug effects
  • Arabidopsis / genetics*
  • Base Sequence
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / drug effects
  • Genes, Plant*
  • Molecular Sequence Data
  • Nucleotides / metabolism
  • Oxidative Stress / drug effects
  • Paraquat / toxicity*
  • Plant Leaves / cytology*
  • Plant Leaves / drug effects
  • Plant Leaves / genetics
  • Plant Leaves / physiology
  • Polyribosomes / drug effects
  • Polyribosomes / metabolism
  • Protein Biosynthesis / drug effects*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism*
  • Transcription Factors / metabolism

Substances

  • 5' Untranslated Regions
  • Nucleotides
  • RNA, Messenger
  • Reactive Oxygen Species
  • Transcription Factors
  • Paraquat