Autophagy Negatively Regulates Cell Death by Controlling NPR1-Dependent Salicylic Acid Signaling during Senescence and the Innate Immune Response inArabidopsis

Kohki Yoshimoto,Yuji Kamiya,Chiara Consonni,Yoshinori Ohsumi,Yusuke Jikumaru,Ralph Panstruga,Ken Shirasu,Miyako Kusano

doi:10.1105/tpc.109.068635

Abstract

Autophagy is an evolutionarily conserved intracellular process for vacuolar degradation of cytoplasmic components. In higher plants, autophagy defects result in early senescence and excessive immunity-related programmed cell death (PCD) irrespective of nutrient conditions; however, the mechanisms by which cells die in the absence of autophagy have been unclear. Here, we demonstrate a conserved requirement for salicylic acid (SA) signaling for these phenomena in autophagy-defective mutants (atg mutants). The atg mutant phenotypes of accelerated PCD in senescence and immunity are SA signaling dependent but do not require intact jasmonic acid or ethylene signaling pathways. Application of an SA agonist induces the senescence/cell death phenotype in SA-deficient atg mutants but not in atg npr1 plants, suggesting that the cell death phenotypes in the atg mutants are dependent on the SA signal transducer NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1. We also show that autophagy is induced by the SA agonist. These findings imply that plant autophagy operates a novel negative feedback loop modulating SA signaling to negatively regulate senescence and immunity-related PCD.

Highlights

Autophagy is an intracellular degradation process that delivers cytoplasmic constituents to the vacuole/lysosome (Klionsky and Ohsumi, 1999; Klionsky, 2005, 2007)
We found that atg2 and atg5 mutant plants, which completely lack autophagy, showed an early senescence phenotype even under favorable growth conditions (Figure 1A)
In addition to the senescence phenotype, the atg2 and atg5 mutants showed growth retardation (Figures 1A and 3B). These results suggest that autophagy has an additional function apart from the role in recycling of proteins to serve as a source of amino acids in plants

Summary

Introduction

Autophagy is an intracellular degradation process that delivers cytoplasmic constituents to the vacuole/lysosome (Klionsky and Ohsumi, 1999; Klionsky, 2005, 2007). Bulk cytoplasmic constituents and organelles are engulfed into a double membrane vesicle called an autophagosome. The autophagy-mediated degradation process has been well elucidated at the molecular level in yeast (Saccharomyces cerevisiae). Genetic analyses in yeast identified 18 autophagy-related (ATG) genes that are essential for autophagosome formation (Tsukada and Ohsumi, 1993; Thumm et al, 1994; Barth et al, 2001). Most of the ATG genes are well conserved across plant and animal kingdoms, suggesting that the molecular basis of the core autophagy machinery is essentially the same in higher eukaryotes, four out of 18 ATG

Methods

Results

Conclusion