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Gene-for-gene immunity between plants and host-adapted pathogens is often linked to population-level diversification of immune receptors encoded by disease resistance (R) genes. The complex barley (Hordeum vulgareL.)Rgene locusMildew Locus A(Mla) provides isolate-specific resistance against the powdery mildew fungusBlumeria graminisf. sp.hordei(Bgh) and has been introgressed into modern barley cultivars from diverse germplasms, including the wild relativeH. spontaneum. KnownMladisease resistance specificities toBghappear to encode allelic variants of the R Gene Homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. To gain insights intoMladiversity in wild barley populations, we here sequenced and assembled the transcriptomes of 50 accessions ofH. spontaneumrepresenting nine populations distributed throughout the Fertile Crescent. The assembledMlatranscripts exhibited rich sequence diversity, which is linked neither to geographic origin nor population structure.Mlatranscripts in the testedH. spontaneumaccessions could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil signaling domains that are both capable of eliciting cell death. The presence of positively selected sites, located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both coiled-coil signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the host population. Unexpectedly, known MLA receptor variants that conferBghresistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor.