Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival

Dev Cell. 2017 Apr 10;41(1):33-46.e7. doi: 10.1016/j.devcel.2017.03.013.

Abstract

Plants encounter a variety of stresses and must fine-tune their growth and stress-response programs to best suit their environment. BES1 functions as a master regulator in the brassinosteroid (BR) pathway that promotes plant growth. Here, we show that BES1 interacts with the ubiquitin receptor protein DSK2 and is targeted to the autophagy pathway during stress via the interaction of DSK2 with ATG8, a ubiquitin-like protein directing autophagosome formation and cargo recruitment. Additionally, DSK2 is phosphorylated by the GSK3-like kinase BIN2, a negative regulator in the BR pathway. BIN2 phosphorylation of DSK2 flanking its ATG8 interacting motifs (AIMs) promotes DSK2-ATG8 interaction, thereby targeting BES1 for degradation. Accordingly, loss-of-function dsk2 mutants accumulate BES1, have altered global gene expression profiles, and have compromised stress responses. Our results thus reveal that plants coordinate growth and stress responses by integrating BR and autophagy pathways and identify the molecular basis of this crosstalk.

Keywords: brassinosteroid; drought response; growth and stress responses; kinases; selective autophagy; signal transduction; transcription factors; ubiquitin receptor.

MeSH terms

  • Amino Acid Motifs
  • Arabidopsis / growth & development*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / metabolism*
  • Autophagy* / drug effects
  • Autophagy-Related Protein 8 Family / metabolism
  • Brassinosteroids / pharmacology
  • Carbon / deficiency
  • Carbon Cycle / drug effects
  • DNA-Binding Proteins
  • Droughts
  • Nuclear Proteins / metabolism*
  • Phosphorylation / drug effects
  • Plant Development* / drug effects
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding / drug effects
  • Proteolysis / drug effects
  • Receptors, Cell Surface / chemistry
  • Receptors, Cell Surface / metabolism
  • Receptors, Cytoplasmic and Nuclear / chemistry
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Stress, Physiological / drug effects
  • Ubiquitin / metabolism
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • ATG8 protein, Arabidopsis
  • Arabidopsis Proteins
  • Autophagy-Related Protein 8 Family
  • BES1 protein, Arabidopsis
  • Brassinosteroids
  • DNA-Binding Proteins
  • DSK2A protein, Arabidopsis
  • DSK2B protein, Arabidopsis
  • Nuclear Proteins
  • Receptors, Cell Surface
  • Receptors, Cytoplasmic and Nuclear
  • Ubiquitin
  • Carbon
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex