The Highly Conserved Barley Powdery Mildew Effector BEC1019 Confers Susceptibility to Biotrophic and Necrotrophic Pathogens in Wheat

Effector proteins secreted by plant pathogens play important roles in promoting colonization.Blumeriaeffector candidate (BEC) 1019, a highly conserved metalloprotease ofBlumeria graminisf. sp.hordei(Bgh), is essential for fungal haustorium formation, and silencingBEC1019significantly reducesBghvirulence. In this study, we found thatBEC1019homologs inB. graminisf. sp.tritici(Bgt) andGaeumannomyces graminisvar.tritici(Ggt) have complete sequence identity with those inBgh, prompting us to investigate their functions. Transcript levels ofBEC1019were abundantly induced concomitant with haustorium formation inBgtand necrosis development inGgt-infected plants.BEC1019overexpression considerably increased wheat susceptibility toBgtandGgt, whereas silencing this gene using host-induced gene silencing significantly enhanced wheat resistance toBgtandGgt, which was associated with hydrogen peroxide accumulation, cell death, and pathogenesis-related gene expression. Additionally, we found that the full and partial sequences ofBEC1019can trigger cell death inNicotiana benthamianaleaves. These results indicate thatBgtandGgtcan utilizeBEC1019as a virulence effector to promote plant colonization, and thus these genes represent promising new targets in breeding wheat cultivars with broad-spectrum resistance.Keywords:effector protein;Blumeria graminisf. sp.tritici;Gaeumannomyces graminisvar.tritici;haustorium formation;necrosis development;cell death