Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study

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 pes...

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Main Authors: Xiaoman Zhao, Si Chen, Shanshan Wang, Wenna Shan, Xiaxia Wang, Yuzhen Lin, Feng Su, Zhenbiao Yang, Xiaomin Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01705/full
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record_format Article
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language English
format Article
sources DOAJ
author Xiaoman Zhao
Xiaoman Zhao
Si Chen
Si Chen
Shanshan Wang
Wenna Shan
Wenna Shan
Xiaxia Wang
Yuzhen Lin
Feng Su
Zhenbiao Yang
Zhenbiao Yang
Xiaomin Yu
spellingShingle Xiaoman Zhao
Xiaoman Zhao
Si Chen
Si Chen
Shanshan Wang
Wenna Shan
Wenna Shan
Xiaxia Wang
Yuzhen Lin
Feng Su
Zhenbiao Yang
Zhenbiao Yang
Xiaomin Yu
Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
Frontiers in Plant Science
plant-herbivore interaction
tea green leafhopper
defense response
hormone signaling
metabolomics
RNA-Seq
author_facet Xiaoman Zhao
Xiaoman Zhao
Si Chen
Si Chen
Shanshan Wang
Wenna Shan
Wenna Shan
Xiaxia Wang
Yuzhen Lin
Feng Su
Zhenbiao Yang
Zhenbiao Yang
Xiaomin Yu
author_sort Xiaoman Zhao
title Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
title_short Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
title_full Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
title_fullStr Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
title_full_unstemmed Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics Study
title_sort defensive responses of tea plants (camellia sinensis) against tea green leafhopper attack: a multi-omics study
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-01-01
description 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.
topic plant-herbivore interaction
tea green leafhopper
defense response
hormone signaling
metabolomics
RNA-Seq
url https://www.frontiersin.org/article/10.3389/fpls.2019.01705/full
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spelling doaj-1f1cbc51f2fa42fe88de961290e0a5202020-11-25T02:55:55ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-01-011010.3389/fpls.2019.01705498998Defensive Responses of Tea Plants (Camellia sinensis) Against Tea Green Leafhopper Attack: A Multi-Omics StudyXiaoman Zhao0Xiaoman Zhao1Si Chen2Si Chen3Shanshan Wang4Wenna Shan5Wenna Shan6Xiaxia Wang7Yuzhen Lin8Feng Su9Zhenbiao Yang10Zhenbiao Yang11Xiaomin Yu12College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Farming Technology Extension Center, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaCenter for Plant Cell Biology, Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, United StatesFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, ChinaTea 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.https://www.frontiersin.org/article/10.3389/fpls.2019.01705/fullplant-herbivore interactiontea green leafhopperdefense responsehormone signalingmetabolomicsRNA-Seq