Arabidopsis thimet oligopeptidases are redox-sensitive enzymes active in the local and systemic plant immune response.

J Biol Chem

Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University, Mississippi State, Mississippi, USA. Electronic address:

Published: August 2021

AI Article Synopsis

  • Plants initiate localized immune responses (effector-triggered immunity, ETI) and systemic responses (systemic acquired response, SAR) upon pathogen infection, alongside changes in their redox environment that activate response mechanisms involving specific protein modifications.
  • The study investigates the roles of Arabidopsis thaliana thimet oligopeptidases TOP1 and TOP2 in plant immunity and oxidative stress, revealing their redox sensitivity and regulatory mechanisms, including oxidative dimerization and activation.
  • Findings show that TOPs are crucial for defense against pathogens, with wild-type plants showing increased activity during immune responses, while mutants lacking certain components exhibit misregulation of immune-related genes and compromised SAR.

Article Abstract

Upon pathogen infection, receptors in plants will activate a localized immune response, the effector-triggered immunity (ETI), and a systemic immune response, the systemic acquired response (SAR). Infection also induces oscillations in the redox environment of plant cells, triggering response mechanisms involving sensitive cysteine residues that subsequently alter protein function. Arabidopsis thaliana thimet oligopeptidases TOP1 and TOP2 are required for plant defense against pathogens and the oxidative stress response. Herein, we evaluated the biochemical attributes of TOP isoforms to determine their redox sensitivity using ex vivo Escherichia coli cultures and recombinant proteins. Moreover, we explored the link between their redox regulation and plant immunity in wild-type and mutant Arabidopsis lines. These analyses revealed that redox regulation of TOPs occurs through two mechanisms: (1) oxidative dimerization of full-length TOP1 via intermolecular disulfides engaging cysteines in the N-terminal signal peptide, and (2) oxidative activation of all TOPs via cysteines that are unique and conserved. Further, we detected increased TOP activity in wild-type plants undergoing ETI or SAR following inoculation with Pseudomonas syringae strains. Mutants unable to express the chloroplast NADPH-dependent thioredoxin reductase C (NTRC) showed elevated TOP activity under unstressed conditions and were SAR-incompetent. A top1top2 knockout mutant challenged with P. syringae exhibited misregulation of ROS-induced gene expression in pathogen-inoculated and distal tissues. Furthermore, TOP1 and TOP2 could cleave a peptide derived from the immune component ROC1 with distinct efficiencies at common and specific sites. We propose that Arabidopsis TOPs are thiol-regulated peptidases active in redox-mediated signaling of local and systemic immunity.

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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8215294PMC
http://dx.doi.org/10.1016/j.jbc.2021.100695DOI Listing

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