Accumulation of endogenous peptides triggers a pathogen stress response in Arabidopsis thaliana

• Published in: The Plant journal : for cell and molecular biology Vol. 96; no. 4; pp. 705 - 715
• Main Authors: Kmiec, Beata, Branca, Rui M.M., Berkowitz, Oliver, Li, Lu, Wang, Yan, Murcha, Monika W., Whelan, James, Lehtiö, Janne, Glaser, Elzbieta, Teixeira, Pedro F.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.11.2018
• Subjects: Accumulation; Activation; Amino acids; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - immunology; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Chloroplasts; Chloroplasts - metabolism; Coverage; defense response; Degradation; Degradation products; Fitness; Gene Knockout Techniques; Gene sequencing; Medicin och hälsovetenskap; Metalloendopeptidases - genetics; Metalloendopeptidases - metabolism; Mitochondria; Oligopeptidase; Pathogens; peptide degradation; Peptide Hydrolases - genetics; Peptide Hydrolases - metabolism; Peptides; Peptides - metabolism; Plant Diseases - immunology; Plant mitochondria; Proteins; Proteomics; Reproductive fitness; Seedlings; Signal Transduction; Stress; Stress response; Stress, Physiological - immunology; Stresses; Transcriptome; oligopeptidase; peptide degradation; chloroplasts; peptides; defense response
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.14100

Summary The stepwise degradation of peptides to amino acids in plant mitochondria and chloroplasts is catalyzed by a network of oligopeptidases (presequence protease PreP, organellar oligopeptidase OOP) and aminopeptidases. In the present report, we show that the lack of oligopeptidase activity in Arabidopsis thaliana results in the accumulation of endogenous free peptides, mostly of chloroplastic origin (targeting peptides and degradation products). Using mRNA sequencing and deep coverage proteomics, allowing for the identification of 17 000 transcripts and 11 000 proteins, respectively, we uncover a peptide‐stress response occurring in plants lacking PreP and OOP oligopeptidase activity. The peptide‐stress response results in the activation of the classical plant defense pathways in the absence of pathogenic challenge. The constitutive activation of the pathogen‐defense pathways imposes a strong growth penalty and a reduction of the plants reproductive fitness. Our results indicate that the absence of organellar oligopeptidases PreP1/2 and OOP results in the accumulation of peptides that are perceived as pathogenic effectors and activate the signaling pathways of plant‐defense response. Significance Statement Arabidopsis thaliana mutants lacking oligopeptidase (presequence protease 1/2 and organellar oligopeptidase) activity in mitochondria and chloroplasts accumulate uncleaved peptide fragments. These peptides, mostly of chloroplastic origin, are perceived as foreign elements triggering a stress response that activates the pathogen‐defense pathways. This study shows that organellar oligopeptidases have an important role beyond the recycling of protein building blocks: avoiding peptide accumulation and the deleterious activation of a peptide stress response.