Abstract
Tea green leafhopper [Empoasca (Matsumurasca) onukii Matsuda] is one of the most devastating pests of tea plants (Camellia sinensis), greatly impacting tea yield and quality. A thorough understanding of the interactions between the tea green leafhopper and the tea plant would facilitate a better pest management. To gain more insights into the molecular and biochemical mechanisms behind their interactions, a combined analysis of the global transcriptome and metabolome reconfiguration of the tea plant challenged with tea green leafhoppers was performed for the first time, complemented with phytohormone analysis. Non-targeted metabolomics analysis by ultra-performance liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-QTOF MS), together with quantifications by ultra-performance liquid chromatography triple quadrupole mass spectrometry (UPLC-QqQ MS), revealed a marked accumulation of various flavonoid compounds and glycosidically bound volatiles but a great reduction in the level of amino acids and glutathione upon leaf herbivory. RNA-Seq data analysis showed a clear modulation of processes related to plant defense. Genes pertaining to the biosynthesis of phenylpropanoids and flavonoids, plant-pathogen interactions, and the biosynthesis of cuticle wax were significantly up-regulated. In particular, the transcript level for a CER1 homolog involved in cuticular wax alkane formation was most drastically elevated and an increase in C29 alkane levels in tea leaf waxes was observed. The tea green leafhopper attack triggered a significant increase in salicylic acid (SA) and a minor increase in jasmonic acid (JA) in infested tea leaves. Moreover, transcription factors (TFs) constitute a large portion of differentially expressed genes, with several TFs families likely involved in SA and JA signaling being significantly induced by tea green leafhopper feeding. This study presents a valuable resource for uncovering insect-induced genes and metabolites, which can potentially be used to enhance insect resistance in tea plants.
Highlights
Plants as sessile organisms are constantly attacked by a wide range of herbivorous insects
We investigated the effects of tea green leafhopper feeding on the metabolic response of “Jinxuan”, a widely grown tea cultivar in South China
To gain an overview of the metabolome changes induced by different treatments, non-targeted metabolomics analysis of tea samples was performed via UPLC-QTOF MS in both ESI+ and ESI- modes, which detected 2, 381 and 906 mass/ retention time features, respectively (Supplemental Table S2)
Summary
Plants as sessile organisms are constantly attacked by a wide range of herbivorous insects. To cope with herbivore challenges, plants have developed a battery of sophisticated mechanisms to fence against herbivore attacks, while maintaining functional flexibility and minimizing impacts on plant fitness (Baldwin and Preston, 1999; Yang et al, 2015). Plants confront herbivores by launching direct or indirect defenses. Indirect defenses do not directly impact insect herbivores but can attract their natural enemies by emitting a blend of VOCs called herbivore-induced plant volatiles (HIPVs) so as to prevent further damage to plant tissues (Aljbory and Chen, 2018). Plant defenses can be classified as being constitutive or inducible and the latter allows energy allocation to growth and reproduction in the absence of insect attack, reducing the metabolic costs in plants (Zhou et al, 2015)
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