Autophagy contributes to positive feedback regulation of SnRK1 signaling in plants

Autophagy. 2023 Dec;19(12):3248-3250. doi: 10.1080/15548627.2023.2247741. Epub 2023 Aug 20.

Abstract

SnRK1 (SNF1-related protein kinase 1) is a plant ortholog of yeast Snf1 and mammalian adenosine monophosphate-activated protein kinase (AMPK) that acts as a positive regulator of macroautophagy/autophagy. However, whether and how the autophagy pathway modulates SnRK1 activity remains elusive. Recently, we identified a clade of plant-specific FLZ (FCS-like zinc finger) proteins as novel ATG8 (autophagy-related 8)-interacting partners in Arabidopsis thaliana. These AtFLZs, which mainly localize on the surface of mitochondria, can inhibit SnRK1 signaling by repressing the T-loop phosphorylation of its catalytic α subunits, thereby negatively regulating carbon starvation-induced autophagy and plant tolerance to energy deprivation. Upon energy starvation, autophagy is activated to mediate the degradation of these AtFLZs, thus relieving their repression of SnRK1. More importantly, the ATG8-FLZ-SnRK1 regulatory axis appears to be functionally conserved during seed plant evolution. These findings highlight the positive role of autophagy in SnRK1 signaling activation under energy-limiting conditions in plants.Abbreviations: ADS, AIMs docking site; AIM, ATG8-interacting motif; AMPK, adenosine monophosphate-activated protein kinase; ATG, autophagy-related; ESCRT, endosomal sorting complexes required for transport; FLZ, FCS-like zinc finger protein; FREE1, FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1; RAPTOR, REGULATORY-ASSOCIATED PROTEIN OF TOR; Snf1, SUCROSE NON-FERMENTING 1; SnRK1, SNF1-related kinase 1; TOR, TARGET OF RAPAMYCIN.

Keywords: ATG8; FLZ; SnRK1; autophagy; carbon starvation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Adenosine Monophosphate
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Autophagy
  • Feedback
  • Gene Expression Regulation, Plant
  • Plants / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Transcription Factors / metabolism
  • Vesicular Transport Proteins / metabolism

Substances

  • Arabidopsis Proteins
  • AMP-Activated Protein Kinases
  • Transcription Factors
  • Adenosine Monophosphate
  • SnRK1 protein, Arabidopsis
  • Protein Serine-Threonine Kinases
  • FREE1 protein, Arabidopsis
  • Vesicular Transport Proteins

Grants and funding

This work was supported by grants from the Youth Innovation Promotion Association, Chinese Academy of Sciences (2023364) and the National Natural Science Foundation of China (32270291, 32061160467, and 31870171).