ERFVIIs as transducers of oxygen-sensing in the evolution of land plant response to hypoxia

The transcriptional response to low oxygen (hypoxia) in flowering plants is mediated by group VII Ethylene Response Factor (ERFVII) transcription factors, whose proteolysis is oxygen-dependent via the PLANT CYSTEINE OXIDASE (PCO) N-degron pathway. However, when and how this hypoxia response evolved in land plants remains unknown. In this study, we investigated the conservation and divergence of transcriptional responses to hypoxia across major land plant clades. We found that the induction of gene functions associated with glycolysis and fermentation is part of a conserved response across all land plant divisions.Evolutinary analyses suggest that ERFVIIs emerged in the last common ancestor of vascular plants with true roots, coinciding with the evolution of oxygen-dependent destabilization mechanisms that regulate hypoxia-adaptive genes. Proteins from other ERF groups have been independently recruited multiple times in different clades as substrates of the PCO N-degron pathway. Taken together, our results demonstrate that the response of land plants to hypoxia has been refined in derived clades through the evolution of ERFVIIs as transcriptional transducers, which occurred concurrently with the emergence of vascular systems and roots as foraging structures in hypoxic soils.