Upstream open reading frame-mediated upregulation of ANAC082 expression in response to nucleolar stress in Arabidopsis

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  • Sasaki Shun
    Graduate School of Agriculture, Hokkaido University
  • Murakami Toru
    Faculty of Agriculture, Hokkaido University
  • Yasumuro Miharu
    Faculty of Agriculture, Hokkaido University
  • Makita Ayaka
    Graduate School of Agriculture, Hokkaido University
  • Oi Yutaro
    Graduate School of Agriculture, Hokkaido University
  • Hiragori Yuta
    Graduate School of Agriculture, Hokkaido University
  • Watanabe Shun
    Graduate School of Agriculture, Hokkaido University
  • Kudo Rin
    Graduate School of Agriculture, Hokkaido University
  • Hayashi Noriya
    Graduate School of Agriculture, Hokkaido University
  • Ohbayashi Iwai
    Department of Life Sciences, National Cheng Kung University Institute of Tropical Plant Sciences and Microbiology, National Cheng Kung University
  • Sugiyama Munetaka
    Department of Biological Sciences, Graduate School of Science, The University of Tokyo
  • Yamashita Yui
    Graduate School of Agriculture, Hokkaido University Research Faculty of Agriculture, Hokkaido University
  • Naito Satoshi
    Research Faculty of Agriculture, Hokkaido University Graduate School of Life Science, Hokkaido University
  • Onouchi Hitoshi
    Graduate School of Agriculture, Hokkaido University Research Faculty of Agriculture, Hokkaido University

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<p>Perturbations in ribosome biogenesis cause a type of cellular stress called nucleolar or ribosomal stress, which triggers adaptive responses in both animal and plant cells. The Arabidopsis ANAC082 transcription factor has been identified as a key mediator of the plant nucleolar stress response. The 5′-untranslated region (5′-UTR) of ANAC082 mRNA contains an upstream ORF (uORF) encoding an evolutionarily conserved amino acid sequence. Here, we report that this uORF mediates the upregulation of ANAC082 expression in response to nucleolar stress. When transgenic Arabidopsis plants containing a luciferase reporter gene under the control of the ANAC082 promoter and 5′-UTR were treated with reagents that induced nucleolar stress, expression of the reporter gene was enhanced in a uORF sequence-dependent manner. Additionally, we examined the effect of an endoplasmic reticulum (ER) stress-inducing reagent on reporter gene expression because the closest homolog of ANAC082 in Arabidopsis, ANAC103, is involved in the ER stress response. However, the ANAC082 uORF did not respond to ER stress. Interestingly, although ANAC103 has a uORF with an amino acid sequence similar to that of the ANAC082 uORF, the C-terminal sequence critical for regulation is not well conserved among ANAC103 homologs in Brassicaceae. Transient expression assays revealed that unlike the ANAC082 uORF, the ANAC103 uORF does not exert a sequence-dependent repressive effect. Altogether, our findings suggest that the ANAC082 uORF is important for the nucleolar stress response but not for the ER stress response, and that for this reason, the uORF sequence-dependent regulation was lost in ANAC103 during evolution.</p>

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