<p>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 (<i>Arabidopsis thaliana</i>) 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 <i>RAP2.4h</i> knockout mutant showed increased tolerance of hypoxia and reduced vegetative growth; transgenic lines overexpressing <i>RAP2.4h</i> (<i>RAP2.4h</i>-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 <i>RAP2.4h</i> transcription. Under normoxic conditions, RAP2.4h directly targeted the promoters of the aquaporin genes <i>PIP2;1</i> and <i>PIP2;2</i>, stimulating their expression. Loss of PIP2;1 and PIP2;2 function rescued the hypoxia hypersensitivity and excessive vegetative growth of <i>RAP2.4h</i>-OE lines. Analyzing the hypoxia sensitivity and growth phenotypes of <i>OsRAP2.4h-</i>knockout mutants in rice (<i>Oryza sativa</i>) 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.</p>

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

  • Ke Liao,
  • Lin-Na Wang,
  • Xin-Yu Lu,
  • Hui-Min Zhang,
  • Zhong-Rong Yan,
  • Tian-Yi Zhang,
  • Yi Li,
  • Ling-Jing Xu,
  • Qiao-Ling Zhong,
  • Qin-Fang Chen,
  • Ying Zhou,
  • Ruo-Han Xie,
  • Shi Xiao

摘要

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.