Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1

• Published in: The EMBO journal Vol. 35; no. 1; pp. 46 - 61
• Main Authors: Yamada, Kohji, Yamashita-Yamada, Misuzu, Hirase, Taishi, Fujiwara, Tadashi, Tsuda, Kenichi, Hiruma, Kei, Saijo, Yusuke
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 04.01.2016; John Wiley and Sons Inc
• Subjects: Arabidopsis; Arabidopsis - immunology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; BAK1; Colletotrichum - immunology; DAMP; Depletion; Gene Expression Regulation, Plant; Gene Knockout Techniques; Pathogens; PEPR; Peptides; plant immunity; Plant pathology; Plant resistance; Protein Serine-Threonine Kinases - genetics; Protein Serine-Threonine Kinases - metabolism; Receptors, Cell Surface - metabolism; Signal Transduction; Trans-Activators - metabolism; PEPR; BAK1; Arabidopsis; plant immunity; DAMP
• ISSN: 0261-4189; 1460-2075
• DOI: 10.15252/embj.201591807

Pathogens infect a host by suppressing defense responses induced upon recognition of microbe‐associated molecular patterns (MAMPs). Despite this suppression, MAMP receptors mediate basal resistance to limit host susceptibility, via a process that is poorly understood. The Arabidopsis leucine‐rich repeat (LRR) receptor kinase BAK1 associates and functions with different cell surface LRR receptors for a wide range of ligands, including MAMPs. We report that BAK1 depletion is linked to defense activation through the endogenous PROPEP peptides (Pep epitopes) and their LRR receptor kinases PEPR1/PEPR2, despite critical defects in MAMP signaling. In bak1‐knockout plants, PEPR elicitation results in extensive cell death and the prioritization of salicylate‐based defenses over jasmonate‐based defenses, in addition to elevated proligand and receptor accumulation. BAK1 disruption stimulates the release of PROPEP3, produced in response to Pep application and during pathogen challenge, and renders PEPRs necessary for basal resistance. These findings are biologically relevant, since specific BAK1 depletion coincides with PEPR‐dependent resistance to the fungal pathogen Colletotrichum higginsianum. Thus, the PEPR pathway ensures basal resistance when MAMP‐triggered defenses are compromised by BAK1 depletion. Synopsis LRR signaling co‐receptor BAK1 is a central mediator of plant immunity, but when absent—as seen upon certain fungal invasions—its function is compensated by signaling through danger peptide receptors PEPRs. Loss of BAK1 leads to the sensitization of PEPR pro‐death signaling. PEPRs are required for basal resistance against pathogens in absence of BAK1. PEPR‐mediated signaling is rewired to reinforce salicylate‐based defenses instead of jasmonate‐based defenses in absence of BAK1. Pathogen effectors and BAK1 depletion additively enhance the generation and release of the PEPR pro‐ligand PROPEP3. Fungal pathogen C. higginsianum invasion leads to depletion of BAK1. LRR signaling co‐receptor BAK1 is a central mediator of plant immunity, but when absent—as seen upon certain fungal invasions—its function is compensated by signaling through danger peptide receptors PEPRs.