Timely perception of adverse environmental changes is critical to maximize chances of survival. Perturbations in the levels of several gases are important cues for plants to sense environmental changes, such as submergence. In Arabidopsis thaliana, oxygen and nitric oxide (NO) sensing is mediated by the N-degron pathway of proteolysis, which controls the protein stability of ERFVII transcription factors. Enhanced ERFVII stability was shown to regulate the transcriptional acclimation response to flooding-induced low oxygen stress (hypoxia). However, how plants detect and transduce initial submergence signals remained elusive.
We discovered that plants can rapidly detect submergence through passive entrapment of the gaseous plant hormone ethylene and use this signal to pre-adapt to impending hypoxia. We demonstrate that ethylene can enhance ERFVII stability prior to hypoxia by increasing the potent NO-scavenger PHYTOGLOBIN1 (PGB1). This ethylene-mediated NO depletion and consequent ERFVII accumulation acclimates plants to survive subsequent hypoxia stress. Moreover, we discovered that this mechanism is conserved across multiple plant organs and species. Our model suggests that the coupling of ethylene signaling to the hypoxia response is a crucial trait to confer flooding tolerance in plants. We conclude that PGB1 is a key intermediate, linking ethylene signalling, via regulated NO removal, to O2 sensing and hypoxia tolerance. Finally, we propose that the discovered mechanism of ethylene-mediated hypoxia tolerance identifies key regulatory targets for early stress perception that could be pivotal for the development flood-tolerant crops.
Coauthors: Daniel Gibbs – University of Birmingham;Frederica Theodoulou – Rothamsted Research;Julia Bailey-Serres – University of California;Michael Holdsworth – University of Nottingham;Rashmi Sasidharan – Utrecht University;Laurentius Voesenek – Utrecht University