Tea is one of the most popular healthy and non-alcoholic beverages worldwide. Tea anthracnose is a disease in tea mature leaves and ultimately affects yield and quality. Colletotrichum camelliae is a dominant fungal pathogen in the tea field that infects tea plants in China. The pathogenic factors of fungus and the susceptible factors in the tea plant are not known. In this work, we performed molecular and genetic studies to observe a cerato-platanin protein CcCp1 from C. camelliae, which played a key role in fungal pathogenicity. △CcCp1 mutants lost fungal virulence and reduced the ability to produce conidia. Transcriptome and metabolome were then performed and analysed in tea-susceptible and tea-resistant cultivars, Longjing 43 and Zhongcha 108, upon C. camelliae wild-type CCA and △CcCp1 infection, respectively. The differentially expressed genes and the differentially accumulated metabolites in tea plants were clearly overrepresented such as linolenic acid and linoleic acid metabolism, glycerophospholipid metabolism, phenylalanine biosynthesis and metabolism, biosynthesis of flavonoid, flavone and flavonol etc. In particular, the accumulation of jasmonic acid was significantly increased in the susceptible cultivar Longjing 43 upon CCA infection, in the fungal CcCp1 protein dependent manner, suggesting the compound involved in regulating fungal infection. In addition, other metabolites in the glycerophospholipid and phenylalanine pathway were observed in the resistant cultivar Zhongcha 108 upon fungal treatment, suggesting their potential role in defense response. Taken together, this work indicated C. camelliae CcCp1 affected the tea plant lipid metabolism pathway to promote disease while the lost function of CcCp1 mutants altered the fungal virulence and plant response.

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