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Salicylic acid promotes autophagy via NPR3 and NPR4 in Arabidopsis senescence and innate immune response

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Abstract

In Arabidopsis thaliana, the non-expresser pathogenesis-related (NPR) multigene family members NPR1, NPR3, and NPR4 are necessary for salicylic acid (SA) perception. NPR3 and NPR4 are the CUL3 E3-ligase substrate adaptors allowing for the ubiquitination and turnover of NPR1 by the 26s proteasome. Concurrently, roots treated with the SA agonist benzothiadiazole accumulate autophagic bodies via NPR1-dependent signal pathway. However, the mechanisms by which NPR3 and NPR4 regulate autophagy remain unclear. In the present study, using single, double, and triple npr1-, npr3-, and npr4-null mutants and wild-type plants, the following results were obtained: (1) leaf senescence progressed faster in npr3/npr4 mutants than in wild type, suggesting that NPR3 and NPR4 negatively regulated leaf senescence. Moreover, npr3/npr4 promoted the expression of pathogenesis-related 1 (PR1) gene and enhanced resistance in response to avirulent pathogen infections suppressing cell death. Still, all mutants had similar SA levels, suggesting that NPR3 and NPR4 positive regulation of cell death and disease resistance was not associated with SA levels; (2) the number of autophagosomes, ATG7, and ATG8a-phosphatidylethanolamine and the concentration of free green-fluorescence protein were lower in npr3/npr4 mutants than in wild-type plants, indicating that NPR3 and NPR4 affected the two ubiquitination-like conjugation systems during the autophagosome formation and degradation of autophagic bodies.

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Acknowledgments

We thank Professor Xinnian Dong (Duke University) for providing seeds from npr1-1, npr3-1, npr4-3, npr3-1/npr4-3 double mutants, and npr1-1/npr3-1/npr4-3 triple mutants. We also thank Dr. Li Faqiang (Department of Genetics, University of Wisconsin, Madison, WI, USA) for providing the transgenic Arabidopsis expressing GFP-ATG8a. This research was supported by the National Natural Science Foundation of China (Grant Numbers 31570256 and 31170250), and by the Natural Science Foundation of Guangdong Province, China (Grant Number, 2014A030313420).

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Correspondence to Yanyan Gao or Wenli Chen.

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Communicated by P. K. Nagar.

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Wang, X., Gao, Y., Yan, Q. et al. Salicylic acid promotes autophagy via NPR3 and NPR4 in Arabidopsis senescence and innate immune response. Acta Physiol Plant 38, 241 (2016). https://doi.org/10.1007/s11738-016-2257-9

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