Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan; RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Japan
Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan; RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Japan
Plant Immunity Research Group, RIKEN Center for Sustainable Resource Science, Yokohama, Japan; Department of Biological Science, Graduate School of Science, The University of Tokyo, Tokyo, Japan
Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Japan; RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Japan
Plants often generate secondary metabolites as defense mechanisms against parasites. Although some fungi may potentially overcome the barrier presented by antimicrobial compounds, only a limited number of examples and molecular mechanisms of resistance have been reported. Here, we found an Aglaia plant-parasitizing fungus that overcomes the toxicity of rocaglates, which are translation inhibitors synthesized by the plant, through an amino acid substitution in a eukaryotic translation initiation factor (eIF). De novo transcriptome assembly revealed that the fungus belongs to the Ophiocordyceps genus and that its eIF4A, a molecular target of rocaglates, harbors an amino acid substitution critical for rocaglate binding. Ribosome profiling harnessing a cucumber-infecting fungus, Colletotrichum orbiculare, demonstrated that the translational inhibitory effects of rocaglates were largely attenuated by the mutation found in the Aglaia parasite. The engineered C. orbiculare showed a survival advantage on cucumber plants with rocaglates. Our study exemplifies a plant–fungus tug-of-war centered on secondary metabolites produced by host plants.