Natural Variation in Small Molecule–Induced TIR-NB-LRR Signaling Induces Root Growth Arrest via EDS1- and PAD4-Complexed R Protein VICTR inArabidopsis   

Abstract

In a chemical genetics screen we identified the small-molecule [5-(3,4-dichlorophenyl)furan-2-yl]-piperidine-1-ylmethanethione (DFPM) that triggers rapid inhibition of early abscisic acid signal transduction via PHYTOALEXIN DEFICIENT4 (PAD4)-and ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1)-dependent immune signaling mechanisms. However, mechanisms upstream of EDS1 and PAD4 in DFPM-mediated signaling remain unknown. Here, we report that DFPM generates an Arabidopsis thaliana accession-specific root growth arrest in Columbia-0 (Col-0) plants. The genetic locus responsible for this natural variant, VICTR (VARIATION IN COMPOUND TRIGGERED ROOT growth response), encodes a TIR-NB-LRR (for Toll-Interleukin1 Receptornucleotide binding-Leucine-rich repeat) protein. Analyses of T-DNA insertion victr alleles showed that VICTR is necessary for DFPM-induced root growth arrest and inhibition of abscisic acid-induced stomatal closing. Transgenic expression of the Col-0 VICTR allele in DFPM-insensitive Arabidopsis accessions recapitulated the DFPM-induced root growth arrest. EDS1 and PAD4, both central regulators of basal resistance and effector-triggered immunity, as well as HSP90 chaperones and their cochaperones RAR1 and SGT1B, are required for the DFPM-induced root growth arrest. Salicylic acid and jasmonic acid signaling pathway components are dispensable. We further demonstrate that VICTR associates with EDS1 and PAD4 in a nuclear protein complex. These findings show a previously unexplored association between a TIR-NB-LRR protein and PAD4 and identify functions of plant immune signaling components in the regulation of root meristematic zone-targeted growth arrest.

Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways

“…For example, many Toll-interleukin-1 receptor-like domain (TIR)-NBSleucine rich repeat (LRR) or coiled coil (CC)-NBS-LRR-type resistance proteins are upregulated upon SAR activation ( Figure 4E; Supplemental Figure 15). These include VICTR, which encodes a TIR-NBS-LRR protein that associates with EDS1 and PAD4 in protein complexes and is required for small molecule-mediated crosstalk between abscisic acid and immune signaling (Kim et al, 2012). Furthermore, genes coding for receptor-like proteins and members of specific receptor-like kinase families prominently occur in the SAR + gene group ( Figure 4E).…”

Identification of Open Stomata1-Interacting Proteins Reveals Interactions with Sucrose Non-fermenting1-Related Protein Kinases2 and with Type 2A Protein Phosphatases That Function in Abscisic Acid Responses

“…In-gel kinase assays were performed as previously described (Ichimura et al, 2000;Kim et al, 2012) with slight modifications. Proteins of 1-week-old Arabidopsis seedlings, grown on vertical one-half-strength MS agar plates, were transferred to liquid one-half-strength MS for 1 h followed by 1 h of treatment with or without 10 mM ABA.…”

Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance ,

“…Arabidopsis EDS1 signals with two sequence-related proteins, PHYTOALEXIN DEFICIENT4 (PAD4) and SENESCENCE-ASSOCIATED GENE101 (SAG101), by forming separate nucleocytoplasmic and nuclear complexes, respectively, with each partner (Feys et al, 2001Rietz et al, 2011;Wagner et al, 2013). Also, Arabidopsis EDS1 was found to reside in nuclear complexes with the TIR-NLR receptors RESISTANT TO PSEUDOMONAS SYRINGAE4 (RSP4), RPS6, and VARIATION IN COMPOUND TRIGGERED ROOT growth response, the RPS4-and RPS6-recognized effectors AvrRps4 and HopA1, as well as the CC-NLR HYPERSENSITIVE RESPONSE TO Turnip crinkle virus (HRT), recognizing turnip crinkle virus coat protein (Bhattacharjee et al, 2011;Heidrich et al, 2011;Zhu et al, 2011;Kim et al, 2012). EDS1 shuttles between the cytoplasm and nucleus through the nuclear pore machinery, and the accumulation of EDS1 inside nuclei is necessary for both TIR-NLR-mediated ETI and basal resistance and their associated transcriptional reprogramming of defense pathways (García et al, 2010;Heidrich et al, 2011).…”