2. Academic Validation
  3. 14-3-3 proteins inhibit autophagy by regulating SINAT-mediated proteolysis of ATG6 in Arabidopsis

14-3-3 proteins inhibit autophagy by regulating SINAT-mediated proteolysis of ATG6 in Arabidopsis

  • BMC Plant Biol. 2024 Nov 29;24(1):1148. doi: 10.1186/s12870-024-05854-3.
Ting Liu # 1 2,  Yuping Zheng # 1,  Shunkang Zhou # 1 2,  Yao Wang 3,  Xue Lei 3,  Lijuan Xie 1,  Qingqi Lin 1,  Changqing Chang 2,  Shi Xiao 4,  Rongliang Qiu 5,  Hua Qi 6
Affiliations

Affiliations

  • 1 Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory of Agricultural & Rural Pollution Abatement and Environmental Safety, College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, China.
  • 2 Guangdong Provincial Key Laboratory of Microbial Signals and Disease Control, Integrate Microbiology Research Center, College of Plant Protection, South China Agricultural University, Guangzhou, 510642, China.
  • 3 State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, China.
  • 4 State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, China. xiaoshi3@mail.sysu.edu.cn.
  • 5 Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory of Agricultural & Rural Pollution Abatement and Environmental Safety, College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, China. qiurl@scau.edu.cn.
  • 6 Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory of Agricultural & Rural Pollution Abatement and Environmental Safety, College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, China. qihua@scau.edu.cn.
  • # Contributed equally.
PMID: 39609744 DOI: 10.1186/s12870-024-05854-3
Abstract

Background: Autophagy is a conserved cellular process crucial for recycling cytoplasmic components and maintaining cellular homeostasis in eukaryotes. During Autophagy, the formation of a protein complex involving AUTOPHAGY-RELATED PROTEIN 6 (ATG6) and phosphatidylinositol 3-kinase is pivotal for recruiting proteins involved in phagophore expansion. However, the intricate molecular mechanism regulating this protein complex in Plants remains elusive.

Results: Here, we aimed to unravel the molecular regulation of Autophagy dynamics in Arabidopsis thaliana by investigating the involvement of the scaffold proteins 14-3-3λ and 14-3-3κ in regulating the proteolysis of ATG6. Phenotypic analyses revealed that 14-3-3λ and 14-3-3κ overexpression lines exhibited increased sensitivity to nutrient starvation, premature leaf senescence, and a decrease in starvation-induced autophagic vesicles, resembling the phenotypes of autophagy-defective mutants, suggesting the potential roles of 14-3-3 proteins in regulating Autophagy in Plants. Furthermore, our investigation unveiled the involvement of 14-3-3λ and 14-3-3κ in the RING finger E3 Ligase SINAT1-mediated ubiquitination and destabilization of ATG6 in vivo. We also observed repressed turnover of ATG6 and translocation of GFP-ATG6 to mCherry-ATG8a-labelled punctate structures in the autophagy-defective mutant, which suggesting that ATG6 is probably a target of Autophagy. Additionally, 14-3-3λ and 14-3-3κ interacted with Tumor necrosis factor Receptor Associated Factor 1a (TRAF1a) to promote the stability of TRAF1a in vivo under nutrient-rich conditions, suggesting a feedback regulation of Autophagy. These findings demonstrate that 14-3-3λ and 14-3-3κ serve as scaffold proteins to regulate Autophagy by facilitating the SINAT1-mediated proteolysis of ATG6, involving both direct and indirect mechanisms, in Plants.

Conclusions: 14-3-3 proteins regulate Autophagy by directly or indirectly binding to ATG6 and SINAT1 to promote ubiquitination and degradation of ATG6. 14-3-3 proteins are involved in modulating Autophagy dynamics by facilitating SINAT1-mediated ubiquitination and degradation of ATG6.

Keywords

Arabidopsis thaliana; 14-3-3 proteins; Autophagy; Autophagy-related protein 6 (ATG6); Ubiquitination.

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