Résumé
SignificanceNOD-like receptors (NLRs) are fundamental components of plant and animal innate immune systems. Some fungal proteins with NLR-like architecture are involved in an allorecognition process that results in cell death, termed heterokaryon incompatibility. A role for fungal NLR-like proteins in pathogen defense has also been proposed. Here, we show that a fungal NLR-like protein, patatin-like phospholipase-1 (PLP-1), monitors the essential SNARE protein SEC-9 in two distantly related fungal species, Neurospora crassa and Podospora anserina. Both plp-1 and sec-9 are highly polymorphic in fungal populations and show evidence of balancing selection. This study provides biochemical evidence that fungal NLRs function similar to NLRs in plants and animals, indicating that these fundamental players of innate immunity evolved independently in all three kingdoms.
In plants and metazoans, intracellular receptors that belong to the NOD-like receptor (NLR) family are major contributors to innate immunity. Filamentous fungal genomes contain large repertoires of genes encoding for proteins with similar architecture to plant and animal NLRs with mostly unknown function. Here, we identify and molecularly characterize patatin-like phospholipase-1 (PLP-1), an NLR-like protein containing an N-terminal patatin-like phospholipase domain, a nucleotide-binding domain (NBD), and a C-terminal tetratricopeptide repeat (TPR) domain. PLP-1 guards the essential SNARE protein SEC-9; genetic differences at plp-1 and sec-9 function to trigger allorecognition and cell death in two distantly related fungal species, Neurospora crassa and Podospora anserina. Analyses of Neurospora population samples revealed that plp-1 and sec-9 alleles are highly polymorphic, segregate into discrete haplotypes, and show transspecies polymorphism. Upon fusion between cells bearing incompatible sec-9 and plp-1 alleles, allorecognition and cell death are induced, which are dependent upon physical interaction between SEC-9 and PLP-1. The central NBD and patatin-like phospholipase activity of PLP-1 are essential for allorecognition and cell death, while the TPR domain and the polymorphic SNARE domain of SEC-9 function in conferring allelic specificity. Our data indicate that fungal NLR-like proteins function similar to NLR immune receptors in plants and animals, showing that NLRs are major contributors to innate immunity in plants and animals and for allorecognition in fungi.