NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses

PLoS Genet. 2013;9(1):e1003196. doi: 10.1371/journal.pgen.1003196. Epub 2013 Jan 17.


Plant autophagy plays an important role in delaying senescence, nutrient recycling, and stress responses. Functional analysis of plant autophagy has almost exclusively focused on the proteins required for the core process of autophagosome assembly, but little is known about the proteins involved in other important processes of autophagy, including autophagy cargo recognition and sequestration. In this study, we report functional genetic analysis of Arabidopsis NBR1, a homolog of mammalian autophagy cargo adaptors P62 and NBR1. We isolated two nbr1 knockout mutants and discovered that they displayed some but not all of the phenotypes of autophagy-deficient atg5 and atg7 mutants. Like ATG5 and ATG7, NBR1 is important for plant tolerance to heat, oxidative, salt, and drought stresses. The role of NBR1 in plant tolerance to these abiotic stresses is dependent on its interaction with ATG8. Unlike ATG5 and ATG7, however, NBR1 is dispensable in age- and darkness-induced senescence and in resistance to a necrotrophic pathogen. A selective role of NBR1 in plant responses to specific abiotic stresses suggest that plant autophagy in diverse biological processes operates through multiple cargo recognition and delivery systems. The compromised heat tolerance of atg5, atg7, and nbr1 mutants was associated with increased accumulation of insoluble, detergent-resistant proteins that were highly ubiquitinated under heat stress. NBR1, which contains an ubiquitin-binding domain, also accumulated to high levels with an increasing enrichment in the insoluble protein fraction in the autophagy-deficient mutants under heat stress. These results suggest that NBR1-mediated autophagy targets ubiquitinated protein aggregates most likely derived from denatured or otherwise damaged nonnative proteins generated under stress conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / physiology
  • Autophagy / genetics*
  • Autophagy-Related Protein 5
  • Carrier Proteins* / genetics
  • Carrier Proteins* / metabolism
  • Mutation
  • Phenotype
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Solubility
  • Stress, Physiological / genetics*
  • Ubiquitin / metabolism
  • Ubiquitinated Proteins / metabolism


  • Arabidopsis Proteins
  • Autophagy-Related Protein 5
  • Carrier Proteins
  • NBR1 protein, Arabidopsis
  • Ubiquitin
  • Ubiquitinated Proteins
  • Atg5 protein, Arabidopsis
  • Phosphoric Monoester Hydrolases

Grants and funding

This work was supported by the Natural Science Foundation of China (grant 2013C150203 to ZC), the National Basic Research Program of China (grant 2009CB119000 to J-QY), and the U.S. National Science Foundation (grant IOS–0958066 to ZC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.