Natural variations of maize ZmLecRK1 determine its interaction with ZmBAK1 and resistance patterns to multiple pathogens.

ABSTRACT

Maize (Zea mays L.) is one of the most important crops in the world, but its yield and quality are seriously affected by diverse diseases. Identifying broad-spectrum resistance genes is crucial for developing effective strategies to control the disease in maize. In a genome-wide study in maize, we identified a G-type lectin receptor kinase ZmLecRK1 as a new resistance protein against Pythium aphanidermatum, one of the causal pathogens of stalk rot in maize. Genetic analysis showed that the specific ZmLecRK1 allele can confer resistance to multiple pathogens in maize. The resistant variant of ZmLecRK1-mediated cell death and disease resistance require the co-receptor leucine-rich repeat kinase ZmBAK1. A naturally occurring A404S variant in the extracellular domain of ZmLecRK1 determines the ZmLecRK1-ZmBAK1 interaction and the formation of ZmLecRK1-related protein complexes. The amino acid S404, as found in the ZmLecRK1 susceptibility variant, constitutes the ancestral version and is conserved among the majority of grass species, while the resistance variant with A404 is only present in a few maize inbred lines. Substitution of S by A at position 404 in ZmLecRK1-like proteins of sorghum and rice greatly enhances their ability to induce cell death. We propose that selection for the ZmLecRK1 resistance variant enhances its binding affinity to the co-receptor ZmBAK1, thereby enhancing the formation of active complexes for defense. Finally, transcriptomic analysis suggests that ZmLecRK1 likely regulates gene expression related to pathways in cell wall organization or biogenesis in response to pathogen infection. Our work highlights the biotechnological potential for generating disease-resistant crops by precisely modulating the activity of ZmLecRK1 and its homologs through targeted base editing.