Target of rapamycin signaling couples energy to oxygen sensing to modulate hypoxic gene expression in Arabidopsis

• Published in: Proceedings of the National Academy of Sciences - PNAS 2023-01, Vol.120 (3), p.e2212474120-e2212474120
• Main Authors: Kunkowska, Alicja B, Fontana, Fabrizia, Betti, Federico, Soeur, Raphael, Beckers, Gerold J M, Meyer, Christian, De Jaeger, Geert, Weits, Daan A, Loreti, Elena, Perata, Pierdomenico
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - metabolism; Aerobic conditions; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; ATP; Biological Sciences; C-Terminus; Carbohydrate metabolism; Carbohydrates; Cysteine Dioxygenase - metabolism; Deprivation; Energy; Gene Expression; Gene Expression Regulation, Plant; Genes; Hypoxia; Life Sciences; Oxidation; Oxygen; Oxygen - metabolism; Phosphatidylinositol 3-Kinases - genetics; Phosphatidylinositol 3-Kinases - metabolism; Rapamycin; Residues; Submergence; Sugars - metabolism; Survival; TOR protein; Transcription activation; Transcription factors
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2212474120

Plants respond to oxygen deprivation by activating the expression of a set of hypoxia-responsive genes (HRGs). The master regulator of this process is a small group of transcription factors belonging to group VII of the ethylene response factors (ERF-VIIs). ERF-VIIs are highly unstable under aerobic conditions due to the continuous oxidation of their characteristic Cys residue at the N terminus by plant cysteine oxidases (PCOs). Under hypoxia, PCOs are inactive and the ERF-VIIs activate transcription of the HRGs required for surviving hypoxia. However, if the plant exposed to hypoxia has limited sugar reserves, the activity of ERF-VIIs is severely dampened. This suggests that oxygen sensing by PCO/ERF-VII is fine-tuned by another sensing pathway, related to sugar or energy availability. Here, we show that oxygen sensing by PCO/ERF-VII is controlled by the energy sensor target of rapamycin (TOR). Inhibition of TOR by genetic or pharmacological approaches leads to a much lower induction of HRGs. We show that two serine residues at the C terminus of RAP2.12, a major ERF-VII, are phosphorylated by TOR and are needed for TOR-dependent activation of transcriptional activity of RAP2.12. Our results demonstrate that oxygen and energy sensing converge in plants to ensure an appropriate transcription of genes, which is essential for surviving hypoxia. When carbohydrate metabolism is inefficient in producing ATP because of hypoxia, the lower ATP content reduces TOR activity, thus attenuating the efficiency of induction of HRGs by the ERF-VIIs. This homeostatic control of the hypoxia-response is required for the plant to survive submergence.