To better dissect non-host resistance against haustorium-forming powdery mildew pathogens, a sow thistle powdery mildew isolate designated Golovinomyces cichoracearum UMSG1 that has largely overcome penetration resistance but is invariably stopped by post-invasion non-host resistance of Arabidopsis thaliana was identified. The post-invasion non-host resistance is mainly manifested as the formation of a callosic encasement of the haustorial complex (EHC) and hypersensitive response (HR), which appears to be controlled by both salicylic acid (SA)-dependent and SA-independent defence pathways, as supported by the susceptibility of the pad4/sid2 double mutant to the pathogen. While the broad-spectrum resistance protein RPW8.2 enhances post-penetration resistance against G. cichoracearum UCSC1, a well-adapted powdery mildew pathogen, RPW8.2, is dispensable for post-penetration resistance against G. cichoracearum UMSG1, and its specific targeting to the extrahaustorial membrane is physically blocked by the EHC, resulting in HR cell death. Taken together, the present work suggests an evolutionary scenario for the Arabidopsis-powdery mildew interaction: EHC formation is a conserved subcellular defence evolved in plants against haustorial invasion; well-adapted powdery mildew has evolved the ability to suppress EHC formation for parasitic growth and reproduction; RPW8.2 has evolved to enhance EHC formation, thereby conferring haustorium-targeted, broad-spectrum resistance at the post-invasion stage.
Bibliographical noteFunding Information:
Urban for technical support, Grace Yang for advice on statistical analyses, and Zhanao Deng and the Xiao lab members for critical reading of this manuscript. Funding for this study was provided by a scholarship from the Ministry of Education of the People’s Republic of China and a grant from the National Science Foundation of China (31071772) to YW and JF, and by the National Science Foundation Grant IOS-0842877 to SX and MCB-0918908 to FK.
- encasement of haustorial complex
- extrahaustorial membrane
- jasmonic acid
- non-host resistance
- post-invasion resistance
- powdery mildew
- salicylic acid