The metacaspase-Peps-PEPR immune module confers resistance to Fusarium head blight in wheat.

Abstract

Pathogens constantly attack staple crops, leading to substantial yield losses. Plant-pathogen interactions activate endogenous plant-secreted peptides, which act as immunity inducers and are promising breeding targets for enhancing crop resistance to pathogens. However, the identification and mechanisms of immunogenic peptides in staple crops remain largely unexplored. Here, we demonstrated that plant elicitor peptides (TaPeps) in wheat (Triticum aestivum), processed by a metacaspase, are competent to trigger plant immunity and contribute to resistance against Fusarium head blight (FHB). Using exogenous phytocytokine peptide screens, we identified three potential TaPeps acting as elicitors that significantly improve FHB resistance. Mechanistically, these elicitors activate innate immune signals and calcium dynamics in response to the Fusarium pathogen via wheat PEP RECEPTOR 1 (TaPEPR1). Overexpression of endogenous PRECURSOR OF PEPs (TaPROPEPs) further reduces FHB severity. Moreover, we characterized the natural form of TaPeps in planta, revealing that the wheat type-II metacaspase TaMCA-IIa cleaves TaPROPEPs at a conserved arginine residue, promoting TaPep maturation and immune activation. In Tamca-IIa mutants, the efficiency of TaPep maturation was decreased and calcium dynamics were impaired, resulting in FHB susceptibility. Conversely, overexpressing TaMCA-IIa in wheat enhanced the immune response and FHB resistance without causing pleiotropic growth penalties. Our findings highlight TaPeps as potential immune-inducing biologicals for crop protection and uncover the metacaspase-Peps-receptor module in mediating plant disease resistance.