Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Nature volume 479, pages 419–422 (2011)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

Accession codes

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).

References

  1. Webb, J. D., Coleman, M. L. & Pugh, C. W. Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell. Mol. Life Sci. 66, 3539–3554 (2009)

    Article  CAS  Google Scholar 

  2. Kelly, D. P. Hypoxic reprogramming. Nature Genet. 40, 132–134 (2008)

    Article  CAS  Google Scholar 

  3. Mustroph, A. et al. Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol. 152, 1484–1500 (2010)

    Article  CAS  Google Scholar 

  4. Bailey-Serres, J. & Voesenek, L. A. C. J. Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313–339 (2008)

    Article  CAS  Google Scholar 

  5. Green, J., Crack, J. C., Thomson, A. J. & LeBrun, N. E. Bacterial sensors of oxygen. Curr. Opin. Microbiol. 12, 145–151 (2009)

    Article  CAS  Google Scholar 

  6. Hou, S. et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544 (2000)

    Article  CAS  ADS  Google Scholar 

  7. Osborne, T. F. & Espenshade, P. J. Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it’s been. Genes Dev. 23, 2578–2591 (2009)

    Article  CAS  Google Scholar 

  8. Semenza, G. L. HIF-1, O2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107, 1–3 (2001)

    Article  CAS  Google Scholar 

  9. van der Wel, H. et al. Requirements for Skp1 processing by cytosolic Prolyl 4(trans)-hydroxylase and α-N-acetylglucosaminyltransferase enzymes involved in O2 signaling in Dictyostelium . Biochemistry 50, 1700–1713 (2011)

    Article  CAS  Google Scholar 

  10. Lee, M. J. et al. RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl Acad. Sci. USA 102, 15030–15035 (2005)

    Article  CAS  ADS  Google Scholar 

  11. Graciet, E., Mesiti, F. & Wellmer, F. Structure and evolutionary conservation of the plant N-end rule pathway. Plant J. 61, 741–751 (2010)

    Article  CAS  Google Scholar 

  12. Hinz, M. et al. Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol. 153, 757–772 (2010)

    Article  CAS  Google Scholar 

  13. Licausi, F. et al. HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana . Plant J. 62, 302–315 (2010)

    Article  CAS  Google Scholar 

  14. Xu, K. et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708 (2006)

    Article  CAS  ADS  Google Scholar 

  15. Hattori, Y. et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026–1030 (2009)

    Article  CAS  ADS  Google Scholar 

  16. Papdi, C. et al. Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol. 147, 528–542 (2008)

    Article  CAS  Google Scholar 

  17. Licausi, F. et al. Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol. 190, 442–456 (2011)

    Article  CAS  Google Scholar 

  18. Li, H. Y. & Chye, M. L. Membrane localization of Arabidopsis acyl-CoA binding protein ACBP2. Plant Mol. Biol. 51, 483–492 (2003)

    Article  CAS  Google Scholar 

  19. Li, H. Y. & Chye, M. L. Arabidopsis Acyl-CoA-binding protein ACBP2 interacts with an ethylene-responsive element-binding protein, AtEBP, via its ankyrin repeats. Plant Mol. Biol. 54, 233–243 (2004)

    Article  CAS  Google Scholar 

  20. Okamuro, J. K., Caster, B., Villarroel, R., Van Montagu, M. & Jofuku, K. D. The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis . Proc. Natl Acad. Sci. USA 94, 7076–7081 (1997)

    Article  CAS  ADS  Google Scholar 

  21. Kwon, Y. T. et al. An essential role of N-terminal arginylation in cardiovascular development. Science 297, 96–99 (2002)

    Article  CAS  ADS  Google Scholar 

  22. Graciet, E. & Wellmer, F. The plant N-end rule pathway: structure and functions. Trends Plant Sci. 15, 447–453 (2010)

    Article  CAS  Google Scholar 

  23. Bradshaw, R. A., Brickey, W. W. & Walker, K. W. N-terminal processing: the methionine aminopeptidase and Nα-acetyl transferase families. Trends Biochem. Sci. 23, 263–267 (1998)

    Article  CAS  Google Scholar 

  24. Garzón, M. et al. PRT6/At5g02310 encodes an Arabidopsis ubiquitin ligase of the N-end rule pathway with arginine specificity and is not the CER3 locus. FEBS Lett. 581, 3189–3196 (2007)

    Article  Google Scholar 

  25. Voges, D., Zwickl, P. & Baumeister, W. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015–1068 (2000)

    Article  Google Scholar 

  26. Vallon, U. & Kull, U. Localization of proteasomes in plant cells. Protoplasma 182, 15–18 (1994)

    Article  Google Scholar 

  27. Pierik, R., de Wit, M. & Voesenek, L. A. C. J. Growth-mediated stress escape: convergence of signal transduction pathways activated upon exposure to two different environmental stresses. New Phytol. 189, 122–134 (2011)

    Article  CAS  Google Scholar 

  28. Zhang, X., Henriques, R., Lin, S. S., Niu, Q. W. & Chua, N. H. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1, 641–646 (2006)

    Article  CAS  Google Scholar 

  29. Lee, M. W. & Yang, Y. Transient expression assay by agroinfiltration of leaves. Methods Mol. Biol. 323, 225–229 (2006)

    PubMed  Google Scholar 

  30. Lohse, M. et al. Robin: An intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 153, 642–651 (2010)

    Article  CAS  Google Scholar 

  31. Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3. (2004)

  32. Reiner, A., Yekutieli, D. & Benjamini, Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19, 368–375 (2003)

    Article  CAS  Google Scholar 

  33. Wu, Z., Irizarry, R. A., Gentleman, R., Martinez-Murillo, F. & Spencer, F. A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99, 909–917 (2004)

    Article  MathSciNet  Google Scholar 

  34. Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565–1572 (2007)

    Article  CAS  Google Scholar 

  35. Gehl, C., Waadt, R., Kudla, J., Mendel, R.-R. & Hänsch, R. New GATEWAY vectors for high throughput analyses of protein–protein interactions by bimolecular fluorescence complementation. Mol. Plant 2, 1051–1058 (2009)

    Article  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Max Planck Institute of Molecular Plant Physiology, Am Muehlenberg 1, 14476, Potsdam-Golm, Germany

    Francesco Licausi, Monika Kosmacz, Daan A. Weits, Federico M. Giorgi & Joost T. van Dongen

  2. PlantLab, Institute of Life Sciences, Scuola Superiore Sant’Anna, Piazza Martiri della Libertà 33, 56127 Pisa, Italy

    Francesco Licausi, Beatrice Giuntoli & Pierdomenico Perata

  3. Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands

    Laurentius A. C. J. Voesenek

  4. Centre for Biosystems Genomics, 6708 PB Wageningen, the Netherlands

    Laurentius A. C. J. Voesenek

Authors
  1. Francesco Licausi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Kosmacz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daan A. Weits
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Beatrice Giuntoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Federico M. Giorgi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laurentius A. C. J. Voesenek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pierdomenico Perata
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Joost T. van Dongen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature10536

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing