Low-oxygen response is triggered by an ATP-dependent shift in oleoyl-CoA in Arabidopsis

Proc Natl Acad Sci U S A. 2018 Dec 18;115(51):E12101-E12110. doi: 10.1073/pnas.1809429115. Epub 2018 Dec 3.

Abstract

Plant response to environmental stimuli involves integration of multiple signals. Upon low-oxygen stress, plants initiate a set of adaptive responses to circumvent an energy crisis. Here, we reveal how these stress responses are induced by combining (i) energy-dependent changes in the composition of the acyl-CoA pool and (ii) the cellular oxygen concentration. A hypoxia-induced decline of cellular ATP levels reduces LONG-CHAIN ACYL-COA SYNTHETASE activity, which leads to a shift in the composition of the acyl-CoA pool. Subsequently, we show that different acyl-CoAs induce unique molecular responses. Altogether, our data disclose a role for acyl-CoAs acting in a cellular signaling pathway in plants. Upon hypoxia, high oleoyl-CoA levels provide the initial trigger to release the transcription factor RAP2.12 from its interaction partner ACYL-COA BINDING PROTEIN at the plasma membrane. Subsequently, according to the N-end rule for proteasomal degradation, oxygen concentration-dependent stabilization of the subgroup VII ETHYLENE-RESPONSE FACTOR transcription factor RAP2.12 determines the level of hypoxia-specific gene expression. This research unveils a specific mechanism activating low-oxygen stress responses only when a decrease in the oxygen concentration coincides with a drop in energy.

Keywords: ACBP; ERFVII; acyl-CoA; integrative signaling; low-oxygen stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyl Coenzyme A / metabolism*
  • Adenosine Triphosphate / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / metabolism*
  • Arabidopsis Proteins / physiology
  • Cell Hypoxia
  • Diazepam Binding Inhibitor / metabolism
  • Gene Expression Regulation, Plant
  • Models, Biological
  • Oxygen / metabolism
  • Signal Transduction
  • Stress, Physiological*

Substances

  • Acyl Coenzyme A
  • Arabidopsis Proteins
  • Diazepam Binding Inhibitor
  • oleoyl-coenzyme A
  • Adenosine Triphosphate
  • Oxygen