A critical role of autophagy in plant resistance to necrotrophic fungal pathogens

Abstract

SUMMARYAutophagy is a pathway for degradation of cytoplasmic components. In plants, autophagy plays an important role in nutrient recycling during nitrogen or carbon starvation, and in responses to abiotic stress. Autophagy also regulates age-and immunity-related programmed cell death, which is important in plant defense against biotrophic pathogens. Here we show that autophagy plays a critical role in plant resistance to necrotrophic pathogens. ATG18a, a critical autophagy protein in Arabidopsis, interacts with WRKY33, a transcription factor that is required for resistance to necrotrophic pathogens. Expression of autophagy genes and formation of autophagosomes are induced in Arabidopsis by the necrotrophic fungal pathogen Botrytis cinerea. Induction of ATG18a and autophagy by B. cinerea was compromised in the wrky33 mutant, which is highly susceptible to necrotrophic pathogens. Arabidopsis mutants defective in autophagy exhibit enhanced susceptibility to the necrotrophic fungal pathogens B. cinerea and Alternaria brassicicola based on increased pathogen growth in the mutants. The hypersusceptibility of the autophagy mutants was associated with reduced expression of the jasmonate-regulated PFD1.2 gene, accelerated development of senescence-like chlorotic symptoms, and increased protein degradation in infected plant tissues. These results strongly suggest that autophagy cooperates with jasmonate-and WRKY33-mediated signaling pathways in the regulation of plant defense responses to necrotrophic pathogens.

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.…”

“…Blocking autophagy inhibits such resistance and results in greatly enhanced susceptibility. Importantly, B. cinerea can induce autophagy in plants (Lai et al, 2011). In accordance, we show that BAG6 processing triggers autophagy and inhibits B. cinerea pathogenic development.…”

“…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.…”