Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen

New Phytol. 2018 May;218(3):999-1014. doi: 10.1111/nph.15078. Epub 2018 Mar 12.

Abstract

The phytohormone ethylene impacts secondary stem growth in plants by stimulating cambial activity, xylem development and fiber over vessel formation. We report the effect of ethylene on secondary cell wall formation and the molecular connection between ethylene signaling and wood formation. We applied exogenous ethylene or its precursor 1-aminocyclopropane-1-carboxylic acid (ACC) to wild-type and ethylene-insensitive hybrid aspen trees (Populus tremula × tremuloides) and studied secondary cell wall anatomy, chemistry and ultrastructure. We furthermore analyzed the transcriptome (RNA Seq) after ACC application to wild-type and ethylene-insensitive trees. We demonstrate that ACC and ethylene induce gelatinous layers (G-layers) and alter the fiber cell wall cellulose microfibril angle. G-layers are tertiary wall layers rich in cellulose, typically found in tension wood of aspen trees. A vast majority of transcripts affected by ACC are downstream of ethylene perception and include a large number of transcription factors (TFs). Motif-analyses reveal potential connections between ethylene TFs (Ethylene Response Factors (ERFs), ETHYLENE INSENSITIVE 3/ETHYLENE INSENSITIVE3-LIKE1 (EIN3/EIL1)) and wood formation. G-layer formation upon ethylene application suggests that the increase in ethylene biosynthesis observed during tension wood formation is important for its formation. Ethylene-regulated TFs of the ERF and EIN3/EIL1 type could transmit the ethylene signal.

Keywords: cell wall; ethylene signaling; gelatinous layer (G-layer); hybrid aspen; tension wood; transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids, Cyclic / pharmacology
  • Cell Wall / drug effects
  • Cell Wall / metabolism
  • Cell Wall / ultrastructure
  • Cellulose / metabolism
  • Computer Simulation
  • Ethylenes / metabolism*
  • Genes, Plant
  • Hybridization, Genetic*
  • Populus / genetics
  • Populus / metabolism*
  • Populus / ultrastructure
  • Principal Component Analysis
  • Promoter Regions, Genetic / genetics
  • Signal Transduction*
  • Spectroscopy, Fourier Transform Infrared
  • Water / pharmacology
  • Wood / drug effects
  • Wood / growth & development
  • Wood / metabolism*
  • Wood / ultrastructure
  • Xylem / drug effects
  • Xylem / metabolism
  • Xylem / ultrastructure

Substances

  • Amino Acids, Cyclic
  • Ethylenes
  • Water
  • 1-aminocyclopropane-1-carboxylic acid
  • Cellulose
  • ethylene