The SnRK1-RAP2.4h-PIP2 module contributes to the trade-off between growth and hypoxia tolerance in plants

Balancing growth and stress tolerance helps plants survive unfavorable environments such as hypoxia caused by submergence. However, the underlying mechanisms by which plant cells fine-tune growth and responses to hypoxia remain unclear. Here, we identified an Arabidopsis (Arabidopsis thaliana) RELATED TO APETALA2 (RAP2) transcription factor, RAP2.4h, that functions in controlling the energy-signaling-mediated trade-off between growth and tolerance of hypoxia. The Arabidopsis RAP2.4h knockout mutant showed increased tolerance of hypoxia and reduced vegetative growth; transgenic lines overexpressing RAP2.4h (RAP2.4h-OE) showed decreased tolerance of hypoxia with increased vegetative growth. During hypoxia, the α-catalytic KIN10 subunit of the energy sensor SnRK1 interacted with and phosphorylated RAP2.4h, thereby suppressing RAP2.4h transcription. Under normoxic conditions, RAP2.4h directly targeted the promoters of the aquaporin genes PIP2;1 and PIP2;2, stimulating their expression. Loss of PIP2;1 and PIP2;2 function rescued the hypoxia hypersensitivity and excessive vegetative growth of RAP2.4h-OE lines. Analyzing the hypoxia sensitivity and growth phenotypes of OsRAP2.4h-knockout mutants in rice (Oryza sativa) revealed functional conservation of the RAP2.4h-PIP2 module in rice and Arabidopsis. Thus, this work uncovers a genetic link connecting energy signaling with the hypoxia response and demonstrates that the SnRK1-RAP2.4h-PIP2 module functions to balance growth and hypoxia tolerance in plants.