Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants

Daniel J. Gibbs, Seung Cho Lee, Nurulhikma Md Isa, Silvia Gramuglia, Takeshi Fukao, George W. Bassel, Cristina Sousa Correia, Françoise Corbineau, Frederica L. Theodoulou, Julia Bailey-Serres, Michael J. Holdsworth

Research output: Contribution to journalArticle

294 Citations (Scopus)

Abstract

Plants and animals are obligate aerobes, requiring oxygen for mitochondrial respiration and energy production. In plants, an unanticipated decline in oxygen availability (hypoxia), as caused by roots becoming waterlogged or foliage submergence, triggers changes in gene transcription and messenger RNA translation that promote anaerobic metabolism and thus sustain substrate-level ATP production. In contrast to animals, oxygen sensing has not been ascribed to a mechanism of gene regulation in response to oxygen deprivation in plants. Here we show that the N-end rule pathway of targeted proteolysis acts as a homeostatic sensor of severe low oxygen levels in Arabidopsis, through its regulation of key hypoxia-response transcription factors. We found that plants lacking components of the N-end rule pathway constitutively express core hypoxia-response genes and are more tolerant of hypoxic stress. We identify the hypoxia-associated ethylene response factor group VII transcription factors of Arabidopsis as substrates of this pathway. Regulation of these proteins by the N-end rule pathway occurs through a characteristic conserved motif at the amino terminus initiating with Met-Cys. Enhanced stability of one of these proteins, HRE2, under low oxygen conditions improves hypoxia survival and reveals a molecular mechanism for oxygen sensing in plants via the evolutionarily conserved N-end rule pathway. SUB1A-1, a major determinant of submergence tolerance in rice, was shown not to be a substrate for the N-end rule pathway despite containing the N-terminal motif, indicating that it is uncoupled from N-end rule pathway regulation, and that enhanced stability may relate to the superior tolerance of Sub1 rice varieties to multiple abiotic stresses.

Original languageEnglish
Pages (from-to)415-418
Number of pages4
JournalNature
Volume479
Issue number7373
DOIs
Publication statusPublished - 17 Nov 2011
Externally publishedYes

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Oxygen
Arabidopsis
Transcription Factors
Anaerobiosis
Genes
Plant Structures
Factor VII
Protein Stability
Hypoxia
Proteolysis
Respiration
Adenosine Triphosphate
Messenger RNA
Proteins
Oryza

ASJC Scopus subject areas

  • General

Cite this

Gibbs, D. J., Lee, S. C., Md Isa, N., Gramuglia, S., Fukao, T., Bassel, G. W., ... Holdsworth, M. J. (2011). Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479(7373), 415-418. https://doi.org/10.1038/nature10534

Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. / Gibbs, Daniel J.; Lee, Seung Cho; Md Isa, Nurulhikma; Gramuglia, Silvia; Fukao, Takeshi; Bassel, George W.; Correia, Cristina Sousa; Corbineau, Françoise; Theodoulou, Frederica L.; Bailey-Serres, Julia; Holdsworth, Michael J.

In: Nature, Vol. 479, No. 7373, 17.11.2011, p. 415-418.

Research output: Contribution to journalArticle

Gibbs, DJ, Lee, SC, Md Isa, N, Gramuglia, S, Fukao, T, Bassel, GW, Correia, CS, Corbineau, F, Theodoulou, FL, Bailey-Serres, J & Holdsworth, MJ 2011, 'Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants', Nature, vol. 479, no. 7373, pp. 415-418. https://doi.org/10.1038/nature10534
Gibbs DJ, Lee SC, Md Isa N, Gramuglia S, Fukao T, Bassel GW et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature. 2011 Nov 17;479(7373):415-418. https://doi.org/10.1038/nature10534
Gibbs, Daniel J. ; Lee, Seung Cho ; Md Isa, Nurulhikma ; Gramuglia, Silvia ; Fukao, Takeshi ; Bassel, George W. ; Correia, Cristina Sousa ; Corbineau, Françoise ; Theodoulou, Frederica L. ; Bailey-Serres, Julia ; Holdsworth, Michael J. / Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. In: Nature. 2011 ; Vol. 479, No. 7373. pp. 415-418.
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