ATG4 Mediated Psm ES4326/AvrRpt2-Induced Autophagy Dependent on Salicylic Acid in Arabidopsis Thaliana

Abstract

Psm ES4326/AvrRpt2 (AvrRpt2) was widely used as the reaction system of hypersensitive response (HR) in Arabidopsis. The study showed that in npr1 (GFP-ATG8a), AvrRpt2 was more effective at inducing the production of autophagosome and autophagy flux than that in GFP-ATG8a. The mRNA expression of ATG1, ATG6 and ATG8a were more in npr1 during the early HR. Based on transcriptome data analysis, enhanced disease susceptibility 1 (EDS1) was up-regulated in wild-type (WT) but was not induced in atg4a4b (ATG4 deletion mutant) during AvrRpt2 infection. Compared with WT, atg4a4b had higher expression of salicylic acid glucosyltransferase 1 (SGT1) and isochorismate synthase 1 (ICS1); but less salicylic acid (SA) in normal condition and the same level of free SA during AvrRpt2 infection. These results suggested that the consumption of free SA should be occurred in atg4a4b. AvrRpt2 may trigger the activation of Toll/Interleukin-1 receptor (TIR)-nucleotide binding site (NB)-leucine rich repeat (LRR)—TIR-NB-LRR—to induce autophagy via EDS1, which was inhibited by nonexpressor of PR genes 1 (NPR1). Moreover, high expression of NPR3 in atg4a4b may accelerate the degradation of NPR1 during AvrRpt2 infection.

Research Progress of ATGs Involved in Plant Immunity and NPR1 Metabolism

“…Yoshimoto et al found that BTH could induce senescence and cell death in atg5 mutants but could not induce senescence and cell death in atg5 npr1 double mutants, indicating that the cell death phenotype in atg5 mutants depended on NPR1 under SA induction [57]. Our previous study also found that ATG4 promoted NPR1 degradation by inhibiting the consumption of free SA [61]. In recent years, the relationship between ATGs and NPR1 has been gradually revealed (Table 2), but there are still many problems to be solved.…”

“…Studies have found that NPR1 regulates ATGs expression. NPR1 inhibited the mRNA expression of ATG1, ATG6, and ATG8a during the early HR induced by Psm ES4326/AvrRpt2 [61]. SA analog benzothiadiazole (BTH) was confirmed to induce autophagy through the NPR1-dependent signaling pathway, and NPR1, NPR3, and NPR4 are jointly involved in the regulation of autophagosomes [91].…”

“…Some of ATGs knockout mutations exhibited enhanced susceptibility to pathogen infection, such as atg2, atg5, atg6, atg7, atg9, atg10, and atg18 [13,[53][54][55][56][57][58][59][60]. While atg2 mutants displayed less HR-PCD and ATG4, ATG5 inhibited the occurrence of HR-PCD, ATG6 antisense plants displayed enhanced HR-PCD during pathogen infection [53][54][55][56][57][58][59]61]. A recent study reported that phosphorylation modification of ATG18a suppressed autophagosome formation during pathogen infection, resulting in compromised plant resistance, which provides evidence for the involvement of autophagy in plant immune regulation [62].…”

Plant Autophagy: An Intricate Process Controlled by Various Signaling Pathways

“…ATG4 inhibits SA consumption resulting in the inhibition of NPR3 (non-expressor of pathogenesis-related genes 3) synthesis and enhanced expression of NPR1, which inhibits autophagy durin g AvrRpt2 affection. These results indicate that ATG4 mediates AvrRpt2 -induced autophagy dependent on SA ( Gong et al, 2020 ). Therefore, the role of autophagy in the immune response depends on what pathogen signals the plant cell receives.…”

“…In Nicotiana benthamiana autophagy-deficient plants, HR-PCD spreads uncontrollably to uninfected cells ( Liu et al, 2005 ). In Arabidopsis , Psm ES4326/ AvrRpt2 can trigger autophagy-dependent HR via the EDS1 (enhanced disease susceptibility 1) pathway, but NPR1 (non-expressor of pathogenesis-related genes 1) suppresses the autophagy flux ( Gong et al, 2020 ). In Arabidopsis atg4a4b double mutant, total SA (salicylic acid) content decreased and free SA unchanged compared with wild type after AvrRpt2 infection, indicating that ATG4 can suppress the consumption of free SA.…”