Indirect recognition of pathogen effectors by NLRs

Abstract

Abstract To perceive pathogen threats, plants utilize both plasma membrane-localized and intracellular receptors. Nucleotide-binding domain leucine-rich repeat containing (NLR) proteins are key receptors that can recognize pathogen-derived intracellularly delivered effectors and activate downstream defense. Exciting recent findings have propelled our understanding of the various recognition and activation mechanisms of plant NLRs. Some NLRs directly bind to effectors, but others can perceive effector-induced changes on targeted host proteins (guardees), or non-functional host protein mimics (decoys). Such guarding strategies are thought to afford the host more durable resistance to quick-evolving and diverse pathogens. Here, we review classic and recent examples of indirect effector recognition by NLRs and discuss strategies for the discovery and study of new NLR-decoy/guardee systems. We also provide a perspective on how executor NLRs and helper NLRs (hNLRs) provide recognition for a wider range of effectors through sensor NLRs and how this can be considered an expanded form of indirect recognition. Furthermore, we summarize recent structural findings on NLR activation and resistosome formation upon indirect recognition. Finally, we discuss existing and potential applications that harness NLR indirect recognition for plant disease resistance and crop resilience.