Formation of volatiles in response to tea green leafhopper (Empoasca onukii Matsuda) herbivory in tea plants: a multi-omics study.

KEY MESSAGE: Combined transcriptome and metabolome analysis of fresh leaf infestation by tea green leafhoppers (Empoasca (Matsumurasca) onukii Matsuda) suggests roles for alternative pre-mRNA splicing and mRNAs in the regulation of aroma formation in tea plants. Oriental Beauty is a high-grade, oolong tea with a pronounced honey-like aroma and rich ripe fruit flavor that develops primarily as a result of the infestation of the fresh leaves by tea green leafhoppers (Empoasca (Matsumurasca) onukii Matsuda). Here, we used PacBio Iso-Seq and RNA-seq analyses to determine the full-length transcripts and gene expression profiles of fresh tea leaves in response to E. (M.) onukii herbivory. We investigated the relationship between RNA-seq, tea metabolites, and aroma response mechanisms in leaves infested by leafhoppers. We found 3644 differentially expressed genes, of which 2552 were up- and 1092 were down-regulated. A total of 49,913 alternative splicing events were predicted, including 324 differential AS events. Moreover, 3105 differentially expressed transcripts were also identified, of which 2295 were up- and 810 were down-regulated. The characterization of expression patterns of the key gene transcript isoforms involved in the aroma formation pathways identified 130 differentially expressed metabolites, 97 of which were up- and 33 were down-regulated. Two key aroma compounds (phenylacetaldehyde and 4-hydroxybenzaldehyde) were highly correlated with genes of the aroma formation pathways. Our results revealed that pre-mRNA AS plays a crucial role in the metabolic regulation surrounding aroma formation under leafhopper herbivory in tea plants.