ABSTRACT
Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity.
Subject(s)
Arabidopsis Proteins , Arabidopsis , DNA-Binding Proteins , Arabidopsis/metabolism , Arabidopsis Proteins/metabolism , Disease Susceptibility , DNA-Binding Proteins/metabolism , Phylogeny , Plant Diseases/genetics , Plant Immunity/physiologyABSTRACT
Ligand recognition by cell-surface receptors underlies development and immunity in both animals and plants. Modulating receptor signalling is critical for appropriate cellular responses but the mechanisms ensuring this are poorly understood. Here, we show that signalling by plant receptors for pathogen-associated molecular patterns (PAMPs) in immunity and CLAVATA3/EMBRYO SURROUNDING REGION-RELATED peptides (CLEp) in development uses a similar regulatory module. In the absence of ligand, signalling is dampened through association with specific type-2C protein phosphatases. Upon activation, PAMP and CLEp receptors phosphorylate divergent cytosolic kinases, which, in turn, phosphorylate the phosphatases, thereby promoting receptor signalling. Our work reveals a regulatory circuit shared between immune and developmental receptor signalling, which may have broader important implications for plant receptor kinase-mediated signalling in general.
Subject(s)
Pathogen-Associated Molecular Pattern Molecules , Protein Kinases , Animals , Ligands , Pathogen-Associated Molecular Pattern Molecules/metabolism , Phosphoprotein Phosphatases , Plants/metabolism , Protein Kinases/metabolismABSTRACT
A protein domain (Toll and Interleukin-1 receptor [TIR]-like) with homology to animal TIRs mediates immune signaling in prokaryotes and eukaryotes. Here, we present an overview of TIR evolution and the molecular versatility of TIR domains in different protein architectures for host protection against microbial attack. Plant TIR-based signaling emerges as being central to the potentiation and effectiveness of host defenses triggered by intracellular and cell-surface immune receptors. Equally relevant for plant fitness are mechanisms that limit potent TIR signaling in healthy tissues but maintain preparedness for infection. We propose that seed plants evolved a specialized protein module to selectively translate TIR enzymatic activities to defense outputs, overlaying a more general function of TIRs.