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Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization

Abstract

The majority of eukaryotic organisms rely on molecular oxygen for respiratory energy production1. When the supply of oxygen is compromised, a variety of acclimation responses are activated to reduce the detrimental effects of energy depletion2,3,4. Various oxygen-sensing mechanisms have been described that are thought to trigger these responses5,6,7,8,9, but they each seem to be kingdom specific and no sensing mechanism has been identified in plants until now. Here we show that one branch of the ubiquitin-dependent N-end rule pathway for protein degradation, which is active in both mammals and plants10,11, functions as an oxygen-sensing mechanism in Arabidopsis thaliana. We identified a conserved amino-terminal amino acid sequence of the ethylene response factor (ERF)-transcription factor RAP2.12 to be dedicated to an oxygen-dependent sequence of post-translational modifications, which ultimately lead to degradation of RAP2.12 under aerobic conditions. When the oxygen concentration is low—as during flooding—RAP2.12 is released from the plasma membrane and accumulates in the nucleus to activate gene expression for hypoxia acclimation. Our discovery of an oxygen-sensing mechanism opens up new possibilities for improving flooding tolerance in crops.

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Figure 1: The transcription factor RAP2.12 regulates hypoxia tolerance of plants.
Figure 2: RAP2.12 is membrane localized and re-localizes in the nucleus upon hypoxia.
Figure 3: Oxygen-dependent destabilization of RAP2.12.
Figure 4: Model describing the oxygen sensor mechanism in plants.

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Primary accessions

Gene Expression Omnibus

Data deposits

The raw data files of the microarray experiments have been deposited in the Gene Expression Omnibus database (http://www.ncbi.nlm.nih.gov/geo; accession number: GSE29187). The gene sequences for the Rumex spp. used in this work have been deposited at NCBI (RaERF1: JF968115; RaERF2: JF968116; RpERF1: JF968117; RpERF2: JF968118; and RpERF3: JF968119).

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Acknowledgements

We would like to thank H. van Veen and R. Sasidharan (for providing Rumex data), E. Maximova, F. Kragler (microscopy), W. Schulze and R. Bock (support and discussion), A. Fernie and R. Pierik (commenting on the manuscript) and S. Parlanti, L. Bartezko and K. Seehaus (plant cultivation). This work was financially supported by the Max Planck Institute of Molecular Plant Physiology, Scuola Superiore Sant’Anna, and the Deutsche Forschungsgemeinschaft (DFG) (DO 1298/2-1).

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F.L., M.K., D.A.W. and B.G. performed the experiments. F.M.G. carried out the bioinformatical analysis. F.L., L.A.C.J.V., P.P. and J.T.v.D. designed the experiments. F.L., P.P. and J.T.v.D. wrote the manuscript. All the authors discussed and commented on the content of the paper.

Corresponding authors

Correspondence to Francesco Licausi or Joost T. van Dongen.

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The authors declare no competing financial interests.

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The file contains Supplementary Figures 1-16 with legends, Supplementary Tables 1-8 and additional references. (PDF 3312 kb)

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Licausi, F., Kosmacz, M., Weits, D. et al. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419–422 (2011). https://doi.org/10.1038/nature10536

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