Infection mechanisms of Rhizoctonia cerealis in wheat.

Rhizoctonia cerealis (Rc) as a major pathogen causing sharp eyespot (SE) seriously affects wheat production worldwide. We collected 1683 wheat plants exhibiting SE symptoms from 30 locations in China over 7 years. We next constructed high-quality genome maps by de novo sequencing of five representative Rc isolates and established an atlas of genomic variation by resequencing 207 isolates. We identified a key effector, RcPL3, conferring Rc pathogenicity. RcPL3 increased the protein accumulation of histone deacetylase TaHDA9 in wheat cytoplasm to promote Rc infection. TaHDA9 inhibited the E3 ubiquitin ligase TaRHC1A through deacetylation. RcPL3 indirectly inhibited the accumulation of TaRHC1A by mediating TaHDA9. TaRHC1A promoted the degradation of TaRBOH3 synthesizing reactive oxygen species (ROS) to cause wheat SE resistance. We further discovered an antagonist HY-19741 to prevent Rc infection. The high-quality genome maps of Rc and a SE RcPL3-TaHDA9-TaRHC1A-TaRBOH3 regulatory cascade will be valuable for SE prevention in wheat.