Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Laura Lorenzo-Orts
  • Janika Witthoeft
  • Jules Deforges
  • Jacobo Martinez
  • Sylvain Loubéry
  • Aleksandra Placzek
  • Yves Poirier
  • Ludwig A. Hothorn
  • Yvon Jaillais
  • Michael Hothorn

Research Organisations

External Research Organisations

  • University of Geneva
  • Friedrich Miescher Laboratory of the Max Planck Society
  • University of Lausanne (UNIL)
  • École normale supérieure de Lyon (ENS de Lyon)
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Details

Original languageEnglish
Pages (from-to)184-193
Number of pages10
JournalNature plants
Volume5
Issue number2
Early online date8 Feb 2019
Publication statusPublished - Feb 2019

Abstract

Eukaryotic mRNAs frequently contain upstream open reading frames (uORFs), encoding small peptides that may control translation of the main ORF (mORF). Here, we report the characterization of a distinct bicistronic transcript in Arabidopsis. We analysed loss-of-function phenotypes of the inorganic polyphosphatase TRIPHOSPHATE TUNNEL METALLOENZYME 3 (AtTTM3), and found that catalytically inactive versions of the enzyme could fully complement embryo and growth-related phenotypes. We could rationalize these puzzling findings by characterizing a uORF in the AtTTM3 locus encoding CELL DIVISION CYCLE PROTEIN 26 (CDC26), an orthologue of the cell cycle regulator. We demonstrate that AtCDC26 is part of the plant anaphase promoting complex/cyclosome (APC/C), regulates accumulation of APC/C target proteins and controls cell division, growth and embryo development. AtCDC26 and AtTTM3 are translated from a single transcript conserved across the plant lineage. While there is no apparent biochemical connection between the two gene products, AtTTM3 coordinates AtCDC26 translation by recruiting the transcript into polysomes. Our work highlights that uORFs may encode functional proteins in plant genomes.

ASJC Scopus subject areas

Cite this

Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants. / Lorenzo-Orts, Laura; Witthoeft, Janika; Deforges, Jules et al.
In: Nature plants, Vol. 5, No. 2, 02.2019, p. 184-193.

Research output: Contribution to journalArticleResearchpeer review

Lorenzo-Orts, L, Witthoeft, J, Deforges, J, Martinez, J, Loubéry, S, Placzek, A, Poirier, Y, Hothorn, LA, Jaillais, Y & Hothorn, M 2019, 'Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants', Nature plants, vol. 5, no. 2, pp. 184-193. https://doi.org/10.1038/s41477-019-0358-3
Lorenzo-Orts, L., Witthoeft, J., Deforges, J., Martinez, J., Loubéry, S., Placzek, A., Poirier, Y., Hothorn, L. A., Jaillais, Y., & Hothorn, M. (2019). Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants. Nature plants, 5(2), 184-193. https://doi.org/10.1038/s41477-019-0358-3
Lorenzo-Orts L, Witthoeft J, Deforges J, Martinez J, Loubéry S, Placzek A et al. Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants. Nature plants. 2019 Feb;5(2):184-193. Epub 2019 Feb 8. doi: 10.1038/s41477-019-0358-3
Lorenzo-Orts, Laura ; Witthoeft, Janika ; Deforges, Jules et al. / Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants. In: Nature plants. 2019 ; Vol. 5, No. 2. pp. 184-193.
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abstract = "Eukaryotic mRNAs frequently contain upstream open reading frames (uORFs), encoding small peptides that may control translation of the main ORF (mORF). Here, we report the characterization of a distinct bicistronic transcript in Arabidopsis. We analysed loss-of-function phenotypes of the inorganic polyphosphatase TRIPHOSPHATE TUNNEL METALLOENZYME 3 (AtTTM3), and found that catalytically inactive versions of the enzyme could fully complement embryo and growth-related phenotypes. We could rationalize these puzzling findings by characterizing a uORF in the AtTTM3 locus encoding CELL DIVISION CYCLE PROTEIN 26 (CDC26), an orthologue of the cell cycle regulator. We demonstrate that AtCDC26 is part of the plant anaphase promoting complex/cyclosome (APC/C), regulates accumulation of APC/C target proteins and controls cell division, growth and embryo development. AtCDC26 and AtTTM3 are translated from a single transcript conserved across the plant lineage. While there is no apparent biochemical connection between the two gene products, AtTTM3 coordinates AtCDC26 translation by recruiting the transcript into polysomes. Our work highlights that uORFs may encode functional proteins in plant genomes.",
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AU - Lorenzo-Orts, Laura

AU - Witthoeft, Janika

AU - Deforges, Jules

AU - Martinez, Jacobo

AU - Loubéry, Sylvain

AU - Placzek, Aleksandra

AU - Poirier, Yves

AU - Hothorn, Ludwig A.

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AU - Hothorn, Michael

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