Wall-associated kinases (WAKs) have recently been identified as major components of fungal and bacterial disease resistance in several cereal crop species. However, the molecular mechanisms of WAK-mediated resistance remain largely unknown. Here, we investigated the function of the maize gene ZmWAK-RLK1 (Htn1) that confers quantitative resistance to northern corn leaf blight (NCLB) caused by the hemibiotrophic fungal pathogen Exserohilum turcicum. ZmWAK-RLK1 was found to localize to the plasma membrane and its presence resulted in a modification of the infection process by reducing pathogen penetration into host tissues. A large-scale transcriptome analysis of near-isogenic lines (NILs) differing for ZmWAK-RLK1 revealed that several differentially expressed genes are involved in the biosynthesis of the secondary metabolites benzoxazinoids (BXs). The contents of several BXs including DIM BOA-Glc were significantly lower when ZmWAK-RLK1 is present. DIM BOA-Glc concentration was significantly elevated in ZmWAK-RLK1 mutants with compromised NCLB resistance. Maize mutants that were affected in overall BXs biosynthesis or content of DIM BOA-Glc showed increased NCLB resistance. We conclude that Htn1-mediated NCLB resistance is associated with a reduction of BX secondary metabolites. These findings suggest a link between WAK-mediated quantitative disease resistance and changes in biochemical fluxes starting with indole-3-glycerol phosphate.

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Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.

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