Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis

Plant Cell. 2012 Jun;24(6):2578-95. doi: 10.1105/tpc.112.098640. Epub 2012 Jun 15.

Abstract

The phytohormone ethylene regulates multiple aspects of plant growth and development and responses to environmental stress. However, the exact role of ethylene in freezing stress remains unclear. Here, we report that ethylene negatively regulates plant responses to freezing stress in Arabidopsis thaliana. Freezing tolerance was decreased in ethylene overproducer1 and by the application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid but increased by the addition of the ethylene biosynthesis inhibitor aminoethoxyvinyl glycine or the perception antagonist Ag+. Furthermore, ethylene-insensitive mutants, including etr1-1, ein4-1, ein2-5, ein3-1, and ein3 eil1, displayed enhanced freezing tolerance. By contrast, the constitutive ethylene response mutant ctr1-1 and EIN3-overexpressing plants exhibited reduced freezing tolerance. Genetic and biochemical analyses revealed that EIN3 negatively regulates the expression of CBFs and type-A Arabidopsis response regulator5 (ARR5), ARR7, and ARR15 by binding to specific elements in their promoters. Overexpression of these ARR genes enhanced the freezing tolerance of plants. Thus, our study demonstrates that ethylene negatively regulates cold signaling at least partially through the direct transcriptional control of cold-regulated CBFs and type-A ARR genes by EIN3. Our study also provides evidence that type-A ARRs function as key nodes to integrate ethylene and cytokinin signaling in regulation of plant responses to environmental stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids, Cyclic / metabolism
  • Amino Acids, Cyclic / pharmacology
  • Arabidopsis / drug effects
  • Arabidopsis / genetics*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism*
  • Cytokinins / metabolism
  • Cytokinins / pharmacology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Ethylenes / metabolism*
  • Freezing
  • Gene Expression Regulation, Plant*
  • Glycine / analogs & derivatives
  • Glycine / pharmacology
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism
  • Signal Transduction
  • Stress, Physiological
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • ARR15 protein, Arabidopsis
  • ARR5 protein, Arabidopsis
  • ARR7 protein, Arabidopsis
  • Amino Acids, Cyclic
  • Arabidopsis Proteins
  • CBF1 protein, Arabidopsis
  • Cytokinins
  • DNA-Binding Proteins
  • DREB1A protein, Arabidopsis
  • EIL1 protein, Arabidopsis
  • EIN2 protein, Arabidopsis
  • EIN3 protein, Arabidopsis
  • EIN4 protein, Arabidopsis
  • ETR1 protein, Arabidopsis
  • Ethylenes
  • Nuclear Proteins
  • Receptors, Cell Surface
  • Trans-Activators
  • Transcription Factors
  • 1-aminocyclopropane-1-carboxylic acid
  • ethylene
  • aminoethoxyvinylglycine
  • Glycine