Corrigendum: Powdery Mildews Are Characterized by Contracted Carbohydrate Metabolism and Diverse Effectors to Adapt to Obligate Biotrophic Lifestyle

Powdery mildew is a widespread plant disease caused by obligate biotrophic fungal pathogens involving species-specific interactions between host and parasite. To gain genomic insights into the underlying obligate biotrophic mechanisms, we analyzed 15 microbial genomes covering powdery and downy mildews and rusts. We observed a genome-wide, massive contraction of multiple gene families in powdery mildews, such as enzymes in the carbohydrate metabolism pathway, when compared with ascomycete phytopathogens, while the fatty acid metabolism pathway maintained its integrity. We also observed significant differences in candidate secreted effector protein (CSEP) families between monocot and dicot powdery mildews, perhaps due to different selection forces. While CSEPs in monocot mildews are likely subject to positive selection causing rapid expansion, CSEP families in dicot mildews are shrinking under strong purifying selection. Our results not only illustrate obligate biotrophic mechanisms of powdery mildews driven by gene family evolution in nutrient metabolism, but also demonstrate how the divergence of CSEPs between monocot and dicot lineages might contribute to species-specific adaption.

Powdery mildew infects a wide range of crops and economic plants, causing substantial losses. Rubber trees (Hevea brasiliensis) are the primary source of natural rubber, and powdery mildew infection causes significant losses to natural rubber yields. How the causal agent, Erysiphe quercicola, establishes successful infection in rubber trees is largely unknown. Previously, 133 candidate secreted effector proteins (CSEPs) were identified in powdery mildew fungus. In this study, we characterize a CSEP named EqCSEP01276 for its function in suppressing host plant defense responses. We show that EqCSEP01276 is a secreted protein and is able to disturb the localization of 9-cis-epoxycarotenoid dioxygenase 5 (HbNCED5), a key enzyme in abscisic acid (ABA) biosynthesis in plant cell chloroplasts of H. brasiliensis. We also show that this effector inhibits ABA biosynthesis, and that in H. brasiliensis ABA is a positive regulator of the plant immune response against powdery mildew. Our study reveals a strategy by which powdery mildew fungus manipulates plant ABA-mediated defense for a successful infection.