Fungal CFEM effectors negatively regulate a maize wall-associated kinase by interacting with its alternatively spliced variant to dampen resistance

Abstract

The fungus Fusarium graminearum causes a devastating disease Gibberella stalk rot of maize. Our knowledge of molecular interactions between F. graminearum effectors and maize immunity factors is lacking. Here, we show that a group of cysteine-rich common in fungal extracellular membrane (CFEM) domain proteins of F. graminearum are required for full virulence in maize stalk infection and that they interact with two secreted maize proteins, ZmLRR5 and ZmWAK17ET. ZmWAK17ET is an alternative splicing isoform of a wall-associated kinase ZmWAK17. Both ZmLRR5 and ZmWAK17ET interact with the extracellular domain of ZmWAK17. Transgenic maize overexpressing ZmWAK17 shows increased resistance to F. graminearum, while ZmWAK17 mutants exhibit enhanced susceptibility to F. graminearum. Transient expression of ZmWAK17 in Nicotiana benthamiana triggers hypersensitive cell death, whereas co-expression of CFEMs with ZmWAK17ET or ZmLRR5 suppresses the ZmWAK17-triggered cell death. Our results show that ZmWAK17 mediates stalk rot resistance and that F. graminearum delivers apoplastic CFEMs to compromise ZmWAK17-mediated resistance.

Keywords: CFEM proteins; CP: Plants; alternative splicing; apoplastic effector; hypersensitive cell death; maize Gibberella stalk rot; plant immunity; plant-fungal interaction; wall-associated kinase.