High Ambient Temperature Accelerates Leaf Senescence via PHYTOCHROME-INTERACTING FACTOR 4 and 5 in Arabidopsis

Mol Cells. 2020 Jul 31;43(7):645-661. doi: 10.14348/molcells.2020.0117.

Abstract

Leaf senescence is a developmental process by which a plant actively remobilizes nutrients from aged and photosynthetically inefficient leaves to young growing ones by disassembling organelles and degrading macromolecules. Senescence is accelerated by age and environmental stresses such as prolonged darkness. Phytochrome B (phyB) inhibits leaf senescence by inhibiting phytochrome-interacting factor 4 (PIF4) and PIF5 in prolonged darkness. However, it remains unknown whether phyB mediates the temperature signal that regulates leaf senescence. We found the light-activated form of phyB (Pfr) remains active at least four days after a transfer to darkness at 20°C but is inactivated more rapidly at 28°C. This faster inactivation of Pfr further increases PIF4 protein levels at the higher ambient temperature. In addition, PIF4 mRNA levels rise faster after the transfer to darkness at high ambient temperature via a mechanism that depends on ELF3 but not phyB. Increased PIF4 protein then binds to the ORE1 promoter and activates its expression together with ABA and ethylene signaling, accelerating leaf senescence at high ambient temperature. Our results support a role for the phy-PIF signaling module in integrating not only light signaling but also temperature signaling in the regulation of leaf senescence.

Keywords: Arabidopsis; PIF4; phytochrome; senescence; temperature.

MeSH terms

  • Abscisic Acid / metabolism
  • Aging / genetics
  • Aging / metabolism*
  • Aging / radiation effects
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Chromatin Immunoprecipitation
  • Darkness
  • Ethylenes / metabolism
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Gene Expression Regulation, Plant / radiation effects
  • Light
  • Phytochrome B / metabolism*
  • Plant Growth Regulators / pharmacology
  • Plant Leaves / genetics
  • Plant Leaves / metabolism*
  • Plant Leaves / physiology
  • Plant Leaves / radiation effects
  • Plants, Genetically Modified / genetics
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Signal Transduction / radiation effects
  • Temperature
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • ELF3 protein, Arabidopsis
  • Ethylenes
  • ORE1 protein, Arabidopsis
  • PIF4 protein, Arabidopsis
  • PIF5 protein, Arabidopsis
  • Plant Growth Regulators
  • Transcription Factors
  • Phytochrome B
  • Abscisic Acid
  • ethylene