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

Abstract

The Bcl-2-associated athanogene (BAG) family is an evolutionarily conserved group of cochaperones that modulate numerous cellular processes. Previously we found that Arabidopsis thaliana BAG6 is required for basal immunity against the fungal phytopathogen Botrytis cinerea. However, the mechanisms by which BAG6 controls immunity are obscure. Here, we address this important question by determining the molecular mechanisms responsible for BAG6-mediated basal resistance. We show that Arabidopsis BAG6 is cleaved in vivo in a caspase-1-like-dependent manner and via a combination of pulldowns, mass spectrometry, yeast two-hybrid assays, and chemical genomics, we demonstrate that BAG6 interacts with a C2 GRAM domain protein (BAGP1) and an aspartyl protease (APCB1), both of which are required for BAG6 processing. Furthermore, fluorescence and transmission electron microscopy established that BAG6 cleavage triggers autophagy in the host that coincides with disease resistance. Targeted inactivation of BAGP1 or APCB1 results in the blocking of BAG6 processing and loss of resistance. Mutation of the cleavage site blocks cleavage and inhibits autophagy in plants; disease resistance is also compromised. Taken together, these results identify a mechanism that couples an aspartyl protease with a molecular cochaperone to trigger autophagy and plant defense, providing a key link between fungal recognition and the induction of cell death and resistance.

Autophagy functions as an antiviral mechanism against geminiviruses in plants

“…Plant cells also employ autophagy to defend themselves against several pathogens (Han et al, 2011; Li et al, 2016). Autophagy positively regulates plant resistance against necrotrophic pathogens (Lai et al, 2011; Lenz et al, 2011; Kabbage et al, 2013) but negatively affects plant resistance against the biotrophic pathogen powdery mildew (Wang et al, 2011).…”

Limited and digestive proteolysis: crosstalk between evolutionary conserved pathways

“…A recent study in Arabidopsis thaliana provides an example of the opposite role of limited proteolysis: activation of autophagy and switching of cellular stress response from death to survival (Li et al, 2016). The authors have shown that cleavage of the plant Bcl2-associated athanogene 6 (BAG6) by aspartyl protease APCB1 induces formation of autophagosomes in plants ( Fig.…”

Two Membrane-Anchored Aspartic Proteases Contribute to Pollen and Ovule Development

“…However, most reported plant aspartic proteases induce PCD, such as NtCDN41, nucellin, OsS5, AtCDR1, OsAP25/37, and APCB1 (Chen and Foolad, 1997;Xia et al, 2004;Kato et al, 2005;Chen et al, 2008;Niu et al, 2013;Li et al, 2016). These findings suggest that plant aspartic proteases have different, even contrary, functions in PCD, which may be due to the specific substrates of these aspartic proteases in different tissues or cell types.…”