Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens

Abstract

SUMMARYIn plants, autophagy has been assigned 'pro-death' and 'pro-survival' roles in controlling programmed cell death associated with microbial effector-triggered immunity. The role of autophagy in basal immunity to virulent pathogens has not been addressed systematically, however. Using several autophagy-deficient (atg) genotypes, we determined the function of autophagy in basal plant immunity. Arabidopsis mutants lacking ATG5, ATG10 and ATG18a develop spreading necrosis upon infection with the necrotrophic fungal pathogen, Alternaria brassicicola, which is accompanied by the production of reactive oxygen intermediates and by enhanced hyphal growth. Likewise, treatment with the fungal toxin fumonisin B1 causes spreading lesion formation in atg mutant genotypes. We suggest that autophagy constitutes a 'pro-survival' mechanism that controls the containment of host tissue-destructive microbial infections. In contrast, atg plants do not show spreading necrosis, but exhibit marked resistance against the virulent biotrophic phytopathogen, Pseudomonas syringae pv. tomato. Inducible defenses associated with basal plant immunity, such as callose production or mitogen-activated protein kinase activation, were unaltered in atg genotypes. However, phytohormone analysis revealed that salicylic acid (SA) levels in non-infected and bacteria-infected atg plants were slightly higher than those in Col-0 plants, and were accompanied by elevated SA-dependent gene expression and camalexin production. This suggests that previously undetected moderate infection-induced rises in SA result in measurably enhanced bacterial resistance, and that autophagy negatively controls SA-dependent defenses and basal immunity to bacterial infection. We infer that the way in which autophagy contributes to plant immunity to different pathogens is mechanistically diverse, and thus resembles the complex role of this process in animal innate immunity.

Aspartyl Protease-Mediated Cleavage of BAG6 Is Necessary for Autophagy and Fungal Resistance in Plants

“…MDC-labeled structures were absent, which was coupled with increased fungal growth ( Figures 7A to 7C). In accordance, previous reports (Lai et al, 2011;Lenz et al, 2011) have also linked autophagy mutants (i.e., atg18) to enhanced susceptibility to B. cinerea. Taken together, these results indicate that B. cinerea challenge triggers the formation of MDC-labeled autophagosomal structures in Arabidopsis plants during the resistant response, and when this response is blocked, susceptibility ensues.…”

“…In accordance, we show that BAG6 processing triggers autophagy and inhibits B. cinerea pathogenic development. When autophagy is inhibited chemically or genetically, a marked increase in susceptibility to B. cinerea is observed (Lai et al, 2011;Lenz et al, 2011). Finally, using transient assays with the cleaved BAG6 followed by TEM, we provide clear evidence for autophagic structures during this immune response.…”

“…A key question is how is complex formation linked to protease cleavage and ultimately to resistance? Previous reports have linked autophagy to basal resistance to necrotrophs (Lai et al, 2011;Lenz et al, 2011;Kabbage et al, 2013). Blocking autophagy inhibits such resistance and results in greatly enhanced susceptibility.…”

“…Co-IP was performed with an anti-HA antibody (IP) and proteins analyzed using immunoblotting with either anti-FLAG or anti-Myc antibody (IB). a role for autophagy in partial resistance to B. cinerea (Lai et al, 2011;Lenz et al, 2011), we examined whether BAG6 processing is linked to autophagy. Autophagy is a major catabolic process in which proteins and damaged organelles are engulfed and sequestered in characteristic double membrane vesicles termed autophagosomes.…”

Role of plant autophagy in stress response

“…Arabidopsis ATG7 knockout mutants and ATG6 RNAi plants reportedly support the increased growth of the virulent hemibiotrophic pathogen Pst DC3000 (Patel and Dinesh-Kumar, 2008;Hofius et al, 2009). However, these observations obviously contradict the recent report that three Arabidopsis mutant lines, Atatg5, atg10, and atg18a, showed an enhanced resistance towards the same virulent pathogen Pst DC3000 (Lenz et al, 2011). Lenz et al reported that these atg plants have a higher level of SA and an increased SA-dependent gene expression, indicating that autophagy negatively regulates SA-dependent immunity resistance to the hemibiotrophic pathogen Pst DC3000 (Lenz et al, 2011).…”