Two complementary NLRs from wild emmer wheat confer powdery mildew resistance

Powdery mildew is a devastating disease that affects wheat yield and quality globally. Here, we identify a powdery mildew resistance locus MlIW39 from wild emmer wheat through map-based cloning, mutagenesis, and stable genetic transformation. Unlike many other cloned Pm genes, the MlIW39-mediated resistance is conferred by the combined effect of two complementary nucleotide-binding and leucine-rich repeat (NLR) genes, encoding a canonical coiled-coil (CC) type NLR protein (MlIW39-R1) and an atypical NLR protein (MlIW39-R2) with an unknown domain (CC-like), respectively. Overexpression of the NLR pair induces cell death in Nicotiana benthamiana, whereas MlIW39-R1 or MlIW39-R2 alone does not. The MlIW39-R1 and MlIW39-R2 proteins physically interact with each other. MlIW39-R1 and MlIW39-R2 likely originate independently and become neighborly located during evolution. Our findings shed light on the significance of NLR pairs in plant immunity and can facilitate wheat disease-resistance breeding using the developed MlIW39 introgression lines and functional marker.