Non-parent of Origin Expression of Numerous Effector Genes Indicates a Role of Gene Regulation in Host Adaption of the Hybrid Triticale Powdery Mildew Pathogen

Coraline R. Praz, Fabrizio Menardo, Mark D. Robinson, Marion C. Müller, Thomas Wicker, Salim Bourras, Beat Keller

Powdery mildew is an important disease of cereals. It is caused by one species,Blumeria graminis, which is divided intoformae specialeseach of which is highly specialized to one host. Recently, a new form capable of growing on triticale (B.g. triticale) has emerged through hybridization between wheat and rye mildews (B.g. triticiandB.g. secalis, respectively). In this work, we used RNA sequencing to study the molecular basis of host adaptation inB.g. triticale. We analyzed gene expression in threeB.g. triticiisolates, twoB.g. secalisisolates and twoB.g. triticaleisolates and identified a core set of putative effector genes that are highly expressed in allformae speciales. We also found that the genes differentially expressed between isolates of the same form as well as between differentformae specialeswere enriched in putative effectors. Their coding genes belong to several families including some which contain known members of mildew avirulence (Avr) and suppressor (Svr) genes. Based on these findings we propose that effectors play an important role in host adaptation that is mechanistically based onAvr-Resistance gene-Svrinteractions. We also found that gene expression in theB.g. triticalehybrid is mostly conserved with the parent-of-origin, but some genes inherited fromB.g. triticishowed aB.g. secalis-like expression. Finally, we identified 11 unambiguous cases of putative effector genes with hybrid-specific, non-parent of origin gene expression, and we propose that they are possible determinants of host specialization in triticale mildew. These data suggest that altered expression of multiple effector genes, in particularAvrandSvrrelated factors, might play a role in mildew host adaptation based on hybridization.