Integrative transcriptome and metabolome analysis uncovers the Toxoptera aurantii (Hemiptera: Aphididae) response of two Camellia sinensis (Ericales: Theaceae) cultivars

The tea aphid Toxoptera aurantii Boyer (Hemiptera: Aphididae) is a destructive pest that infests tea plants. The resistance mechanisms of the tea plant against T. aurantii infestation are largely unexplored. This study investigates the defensive response of tea plants to T. aurantii feeding using an aphid-resistant Camellia sinensis cultivar 'Qiancha1' (QC1) and an aphid-susceptible C. sinensis cultivar 'Huangjinya' (HJY). Transcriptomics and metabolomics analyses were conducted on 4 samples: QCCK (T. aurantii non-infested QC1), HJYCK (T. aurantii non-infested HJY), QC24 (T. aurantii-infested QC1 for 24 h), and HJY24 (T. aurantii-infested HJY for 24 h). The results showed that the differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) in the 2 comparison groups (QCCK vs. QC24 and HJYCK vs. HJY24) were primarily enriched in metabolic pathways, including hormone signal transduction, phenylpropanoid biosynthesis and flavonoid biosynthesis. Following aphid infestation, the resistant cultivar QC1 exhibited more DEGs and DAMs than the susceptible cultivar HJY, indicating a stronger response to T. aurantii feeding stress. Additionally, the expression of phenylpropanoid- and flavonoid-related genes (CYP, 4CL, FLS, F3H, and LAR) was significantly upregulated in the resistant cultivar QC1 compared with that in the susceptible cultivar HJY. Metabolites involved in phenylpropanoid/flavonoid pathways, such as p-coumaroyl-CoA, caffeoylquinic acid, and feruloyl-CoA, were exclusively induced in QC1. These findings suggest that phenylpropanoid/flavonoid pathways play pivotal roles in tea plant resistance to T. aurantii infestation, providing valuable insights for the breeding and utilization of resistant germplasms.