Light-induced stabilization of ACS contributes to hypocotyl elongation during the dark-to-light transition in Arabidopsis seedlings

Plant J. 2019 Jun;98(5):898-911. doi: 10.1111/tpj.14289. Epub 2019 Mar 27.

Abstract

Hypocotyl growth during seedling emergence is a crucial developmental transition influenced by light and phytohormones such as ethylene. Ethylene and light antagonistically control hypocotyl growth in either continuous light or darkness. However, how ethylene and light regulate hypocotyl growth, including seedling emergence, during the dark-to-light transition remains elusive. Here, we show that ethylene and light cooperatively stimulate a transient increase in hypocotyl growth during the dark-to-light transition via the light-mediated stabilization of 1-aminocyclopropane-1-carboxylic acid (ACC) synthases (ACSs), the rate-limiting enzymes in ethylene biosynthesis. We found that, in contrast to the known inhibitory role of light in hypocotyl growth, light treatment transiently increases hypocotyl growth in wild-type etiolated seedlings. Moreover, ACC, the direct precursor of ethylene, accentuates the effects of light on hypocotyl elongation during the dark-to-light transition. We determined that light leads to the transient elongation of hypocotyls by stabilizing the ACS5 protein during the dark-to-light transition. Furthermore, biochemical analysis of an ACS5 mutant protein bearing an alteration in the C-terminus indicated that light stabilizes ACS5 by inhibiting the degradation mechanism that acts through the C-terminus of ACS5. Our study reveals that plants regulate hypocotyl elongation during seedling establishment by coordinating light-induced ethylene biosynthesis at the post-translational level. Moreover, the stimulatory role of light on hypocotyl growth during the dark-to-light transition provides additional insights into the known inhibitory role of light in hypocotyl development.

Keywords: dark-to-light transition; ethylene; hypocotyls; light.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / growth & development*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Darkness
  • Enzyme Stability / drug effects
  • Enzyme Stability / radiation effects
  • Ethylenes / pharmacology*
  • Gene Expression Regulation, Developmental / drug effects
  • Gene Expression Regulation, Developmental / radiation effects
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Enzymologic / radiation effects
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / radiation effects
  • Hypocotyl / drug effects
  • Hypocotyl / growth & development*
  • Hypocotyl / radiation effects
  • Light
  • Lyases / genetics
  • Lyases / metabolism*
  • Mutation
  • Plant Growth Regulators / pharmacology
  • Seedlings / drug effects
  • Seedlings / growth & development*
  • Seedlings / radiation effects

Substances

  • Arabidopsis Proteins
  • Ethylenes
  • Plant Growth Regulators
  • ethylene
  • Lyases
  • 1-aminocyclopropanecarboxylate synthase

Associated data

  • GENBANK/CS16581