Vacuolar Processing Enzyme Is Essential for Mycotoxin-induced Cell Death in Arabidopsis thaliana

• Published in: The Journal of biological chemistry Vol. 280; no. 38; pp. 32914 - 32920
• Main Authors: Kuroyanagi, Miwa, Yamada, Kenji, Hatsugai, Noriyuki, Kondo, Maki, Nishimura, Mikio, Hara-Nishimura, Ikuko
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.09.2005; American Society for Biochemistry and Molecular Biology
• Subjects: Animals; Apoptosis; Arabidopsis - drug effects; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis thaliana; Caspase Inhibitors; Catalysis; Cell Death; Cysteine Endopeptidases - metabolism; Cysteine Endopeptidases - physiology; Enzyme Inhibitors - pharmacology; Fumonisins - pharmacology; Gene Expression Regulation, Plant; Genes, Plant; Genome, Plant; Hydrogen-Ion Concentration; Immunoblotting; Insecta; Ions; Kinetics; Microscopy, Electron; Mutation; Mycotoxins - toxicity; Plant Physiological Phenomena; Protein Binding; Reverse Transcriptase Polymerase Chain Reaction; Time Factors
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1074/jbc.M504476200

Some compatible pathogens secrete toxins to induce host cell death and promote their growth. The toxin-induced cell death is a pathogen strategy for infection. To clarify the executioner of the toxin-induced cell death, we examined a fungal toxin (fumonisin B1 (FB1))-induced cell death of Arabidopsis plants. FB1-induced cell death was accompanied with disruption of vacuolar membrane followed by lesion formation. The features of FB1-induced cell death were completely abolished in the Arabidopsis vacuolar processing enzyme (VPE)-null mutant, which lacks all four VPE genes of the genome. Interestingly, an inhibitor of caspase-1 abolished FB1-induced lesion formation, as did a VPE inhibitor. The VPE-null mutant had no detectable activities of caspase-1 or VPE in the FB1-treated leaves, although wild-type leaves had the caspase-1 and VPE activities, both of which were inhibited by a caspase-1 inhibitor. γVPE is the most essential among the four VPE homologues for FB1-induced cell death in Arabidopsis leaves. Recombinant γVPE recognized a VPE substrate with Km = 30.3 μm and a caspase-1 substrate with Km = 44.2 μm, which is comparable with the values for mammalian caspase-1. The γVPE precursor was self-catalytically converted into the mature form exhibiting caspase-1 activity. These in vivo and in vitro analyses demonstrate that γVPE is the proteinase that exhibits a caspase-1 activity. We show that VPE exhibiting a caspase-1 activity is a key molecule in toxin-induced cell death. Our findings suggest that a susceptible response of toxin-induced cell death is caused by the VPE-mediated vacuolar mechanism similar to a resistance response of hypersensitive cell death (Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2004) Science 305, 855–858).