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

First author: Francesco Licausi; Affiliations: Max Planck Institute of Molecular Plant Physiology (马克斯·普朗克分子植物生理研究所)Potsdam-Golm, Germany

Corresponding author: Joost T. van Dongen 

The majority of eukaryotic organisms rely on molecular oxygen for respiratory energy production. When the supply of oxygen is compromised, a variety of acclimation responses are activated to reduce the detrimental effects of energy depletion. Various oxygen-sensing mechanisms have been described that are thought to trigger these responses, 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 plants, 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.


通讯:Joost T. van Dongen (https://www.mpimp-golm.mpg.de/11030/Joost_van_Dongen)



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

Journal: Nature

Published date: November 17, 2011

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

First author: Daniel J. Gibbs; Affiliations: University of Nottingham (诺丁汉大学)Loughborough, UK

Corresponding author: Michael J. Holdsworth

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 (无氧代谢) 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.


通讯:Michael J. Holdsworth (https://www.nottingham.ac.uk/biosciences/people/michael.holdsworthv)



doi: https://doi.org/10.1038/nature10534

Journal: Nature

Published date: November 17, 2011

P.S. 感兴趣的还有一篇综述可以参考参考,链接:https://doi.org/10.1146/annurev-arplant-043014-114813(下图来自该文)


Figure 4. Cross-kingdom comparison of low-oxygen-sensing mechanisms. Oxygen-dependent relocalization of a transcription factor that acts as a master regulator of the anaerobic response (shown in red ) from membrane systems into the nucleus is common to fungi and plants. In Schizosaccharomyces pombe, the transcription factor Sre1 is cleaved in an indirect oxygen-dependent manner, thereby releasing an active N-terminal fragment into the nucleus. In Arabidopsis thaliana, RAP2.12 is localized at the plasma membrane, where it interacts with acyl–coenzyme A (CoA)–binding proteins (ACBPs). Hypoxic conditions trigger its release by an unknown mechanism. Oxygen-dependent destabilization of the hypoxic master regulator is also shared among eukaryotes, although through different mechanisms: In yeast, Sre1 is degraded by the protease Ofd1, whose activity is directly stimulated by oxygen binding. In plants, plant cysteine oxidases (PCOs) prepare RAP2.12 for protein degradation by oxidizing the N-terminal cysteine. In animals, the HIF-1α transcription factor is hydroxylated at a proline residue in the presence of oxygen by prolyl dehydrogenases (PHDs), a modification that initiates HIF degradation by the proteasome. A second hydroxylation at an asparagine residue by FIH also inactivates the transcription factor.



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