Transcriptomic studies in resistant and susceptible tea cultivars have been performed to reveal the different defense molecular mechanisms of tea after E. onukii feeding.
The molecular mechanism by which tea plants respond to small green leafhopper Empoasca onukii (Matsuda) damage is unclear. Using the resistant tea plant cultivar Juyan (JY) and the susceptible tea plant cultivar Enbiao (EB) as materials, this study performed RNA-seq on tea leaf samples collected at three time points (6 h, 12 h, 24 h) during exposure of the plants to leafhopper to reveal the molecular mechanisms that are activated in susceptible and resistant tea plant cultivars in response to leafhopper damage. The numbers of DEGs in the susceptible tea cultivar during early (6 h) and late (24 h) stages of leafhopper induction were higher than those in the resistant cultivar at the same time points. The stress responses to leafhopper were most intense at 12 h in both tea cultivars. Pathway enrichment analysis showed that most up-regulated DEGs and their related metabolic pathways were similar in the two tea cultivars. However, during the early stage of leafhopper induction (6 h), jasmonic acid (JA)-related genes were significantly up-regulated in the resistant cultivar. The terpenoid biosynthetic pathway and the α-linolenic acid metabolic pathway were activated earlier in the resistant cultivar and remained activated until the late stage of leafhopper damage. Our results confirmed that after leafhopper damage, the resistant tea cultivar activated its defense responses earlier than the susceptible cultivar, and these defense responses were mainly related to terpenoid metabolism and JA biosynthetic pathway. The results provide important clues for further studies on resistance strategy of tea plants to pest.
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Differentially expressed gene
Kyoto Encyclopedia of Genes and Genomes
Alibory Z, Chen MS (2018) Indirect plant defense against insect herbivores: a review. Insect Sci 25:2–23. https://doi.org/10.1111/1744-7917.12436
Browse J (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60:183–205. https://doi.org/10.1146/annurev.arplant.043008.092007
Cai XM (2009) The emission of tea plant volatiles induced by three herbivore insect pests. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/article/cdmd-82101-2010171082.htm
Chen CJ, Chen H, He YH, Xia R (2018) TBtools, a Toolkit for biologists integrating various biological data handling tools with a user-friendly interface. bioRxiv. https://doi.org/10.1101/289660(Preprint)
Du H, Li X, Ning L, Qin R, Du Q, Wang Q, Song H, Huang F, Wang H, Yu D (2019) RNA-Seq analysis reveals transcript diversity and active genes after common cutworm (Spodoptera litura Fabricius) attack in resistant and susceptible wild soybean lines. BMC Genomics 20: 237. https://doi.org/10.1186/s12864-019-5599-z
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259
Fu JY (2017) The sesquiterpene metabolism and response to diverse biotic stresses in tea plant. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/Article/CDMD-82101-1017255172.htm
Furstenberg-Hagg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297. https://doi.org/10.3390/ijms140510242
Gan X, Stegle O, Behr J et al (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477:419–423. https://doi.org/10.1038/nature10414
Han GZ (2017) Evolution of jasmonate biosynthesis and signaling mechanisms. J Exp Bot 68:1323–1331. https://doi.org/10.1093/jxb/erw470
Hettenhausen C, Baldwin IT, Wu JQ (2013) Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytol 199:787–799. https://doi.org/10.1111/nph.12312
Hohenstein JD, Studham ME, Klein A, Kovinich N, Barry K, Lee YJ, MacIntosh GC (2019) Transcriptional and chemical changes in soybean leaves in response to long-term aphid colonization. Front Plant Sci 10:310. https://doi.org/10.3389/fpls.2019.00310
Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant cell wall: a complex and dynamic structure as rrevealed by the responses of genes under stress conditions. Front Plant Sci 7:984–993. https://doi.org/10.3389/fpls.2016.00984
Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69:387–415. https://doi.org/10.1146/annurev-arplant-042817-040047
Huang C, Zhang J, Zhang X, Yu Y, Bian W, Zeng Z, Sun X, Li X (2018) Two new polyphenol oxidase Genes of tea plant (Camellia sinensis) respond differentially to the regurgitant of tea geometrid Ectropis obliqua. Int J Mol Sci 19(8):2414. https://doi.org/10.3390/ijms19082414
Jeyaraj A, Liu S, Zhang X, Zhang R, Shangguan M, Wei C (2017) Genome-wide identification of microRNAs responsive to Ectropis oblique feeding in tea plant (Camellia sinensis L.). Sci Rep 7(13634):13634. https://doi.org/10.1038/s41598-017-13692-7
Jin S, Sun XL, Chen ZM, Xiao B (2012a) Resistance of different tea cultivars to Empoasca vitis Göthe. Scientia Agricultura Sinica 45:255–265. https://doi.org/10.3864/j.issn.0578-1752.2012.02.007
Jin S, Sun XL, Chen ZM, Xiao B et al (2012b) Applications of electric penetration graph (EPG)Technique in the research of resistance of tea plant to piercing-sucking insects. J Tea Sci 32: 393–401
Jin S, Chen ZM, Backus EA, Sun XL, Xiao B (2012) Characterization of EPG waveforms for the tea green leafhopper, Empoasca vitis Göthe (Hemiptera: Cicadellidae), on tea plants and their correlation with stylet activities. J Insect Physiol 58(9):1235–1244. https://doi.org/10.1016/j.jinsphys.2012.06.008
Jin S, Sun XL, Zhang XZ, Ye NX, Chen ZM (2016) Chemical analysis of 8 tea cultivars with different levels of resistance to Empoasca vitis Göthe the and a preliminary identification of the chemical basis of this resistance. Chin J Appl Entomol 53: 516–527
Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:1040–1045. https://doi.org/10.1093/nar/gkw982
Jin S, Han LW, Ye NX, Wang W, Huang HS, Liu W (2019) Analysis on volatiles of oolong tea Varieties induced by Empoasca sp. Chin J Trop Crops 40: 576–582
Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27
Kersten B, Ghirardo A, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Fladung M, Schroeder H (2013) Integrated transcriptomics and metabolomics decipher differences in the resistance of pedunculate oak to the herbivore Tortrix viridana L. BMC Genom 14: 737. https://doi.org/10.1186/1471-2164-14-737
Koo AJ, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580. https://doi.org/10.1016/j.phytochem.2009.07.018
Kostyn K, Czemplik M, Kulma A, Bortniczuk M, Skala J, Szopa J (2012) Genes of phenylpropanoid pathway are activated in early response to Fusarium attack in flax plants. Plant Sci 190:103–115. https://doi.org/10.1016/j.plantsci.2012.03.011
Li HL, Lin NQ (2009) The difference of egg number in different positions of tea shoot. Tea Sci Tech 3: 18–19
Li H, Yu Y, Li Z, Arkorful E, Yang Y, Liu X, Li X, Li R (2018) Benzothiadiazole and B-aminobutyric acid induce resistance to Ectropis obliqua in tea plants (Camellia Sinensis (L.) O. Kuntz). Molecules 23:1290. https://doi.org/10.3390/molecules23061290
Liechti R, Farmer EE (2002) The jasmonate pathway. Science 296:1649–1650
Liu QS, Wang XY, Tzin V, Romeis J, Peng YF, Li YH (2016) Combined transcriptome and metabolome analyses to understand the dynamic responses of rice plants to attack by the rice stem borer Chilo suppressalis (Lepidoptera: Crambidae). BMC Plant Biol 16:259. https://doi.org/10.1186/s12870-016-0946-6
Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793. https://doi.org/10.1093/bioinformatics/bti430
Mu D (2011) Studies on efficacy of volatile infochemicals from tea plants regulating behaviours of tea green leafhopper and its egg parasitoid Stethynium empoascae. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/article/cdmd-82101-1011159158.htm
Pei MS, Niu JX, Li CJ, Cao FJ, Quan SW (2016) Identification and expression analysis of genes related to calyx persistence in Korla fragrant pear. BMC Genom 17:132. https://doi.org/10.1186/s12864-016-2470-3
Sanchez-Moran E (2013) Genomics and chromatin packaging. Annual plant reviews. Wiley, New York, pp 123–156
Soni RP, Katoch M, Kuman A, Ladohiya R, Verma P (2015) Tea: production, composition, consumption and its potential an antioxidant and antimicrobial agent. Int J Food Ferment Technol 5:95–106
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. https://doi.org/10.1016/j.tplants.2012.02.010
Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766. https://doi.org/10.1093/jxb/erj135
Tian L, Chang CL, Ma L, Nasir F, Zhang JF, Li WQ, Tran LP, Tian CJ (2019) Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae. Rice 12:35. https://doi.org/10.1186/s12284-019-0287-9
Tronchet M, Balague C, Kroj T, Jouanin L, Roby D (2010) Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol Plant Pathol 11:83–92. https://doi.org/10.1111/j.1364-3703.2009.00578.x
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86. https://doi.org/10.1186/s12870-016-0771-y
Wang GC (2010) Ecological functions of tea plant volatiles induced by three herbivores. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/article/cdmd-82101-2010171082.htm
Wang D (2015) Exploring the molecular mechanisms underlying the resistance of Camellia sinensis to Ectropis oblique provided by transcriptomic comparisons. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/Article/CDMD-82101-1015378842.htm
Wang YN, Tang L, Hou Y, Wang P, Yang H, Wei CL (2016) Differential transcriptome analysis of leaves of tea plant (Camellia sinensis) provides comprehensive insights into the defense responses to Ectropis oblique attack using RNA-Seq. Funct Integr Genom 16:383–398. https://doi.org/10.1007/s10142-016-0491-2
Wang WW, Zheng C, Hao WJ, Ma CL, Ma JQ, Ni DJ, Chen L (2018) Transcriptome and metabolome analysis reveal candidate genes and biochemicals involved in tea geometrid defense in Camellia sinensis. PLoS ONE 13:e0201670. https://doi.org/10.1371/journal.pone.0201670
Wang ZP, Li YJ, Li CN, Song XP, Lei JC, Gao YJ, Liang Q (2019) Comparative transcriptome profiling of resistant and susceptible sugarcane genotypes in response to the airborne pathogen Fusarium verticillioides. Mol Biol Rep 46:3777–3789. https://doi.org/10.1007/s11033-019-04820-9
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058. https://doi.org/10.1093/aob/mct067
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
Wu DY, Jing J, Wang G, Guan CF, Jin C (2014) LchERF, a novel ethylene-responsive transcription factor from Lycium chinense, confers salt tolerance in transgenic tobacco. Plant Cell Report 33(12):2033–2045. https://doi.org/10.1007/s00299-014-1678-4
Xin ZJ, Chen SL, Ge LG, Li X, Sun XL (2019) The involvement of a herbivore-induced acyl-CoA oxidase gene, CsACX1, in the synthesis of jasmonic acid and its expression in flower opening in tea plant (Camellia sinensis). Plant Physiol Biochem 135:132–140. https://doi.org/10.1016/j.plaphy.2018.11.035
Xu XX (2015) Attraction of tea plant volatiles to Empoasca vitis and influencing factors. PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing. https://cdmd.cnki.com.cn/Article/CDMD-82101-1016174614.htm
Yang JF, Li MR (2019) Blue book of tea industry: annual development and research reports on China’s tea industry 2018. Chinese Social Sciences Academic Press, Beijing, China
Yang H, Xie S, Wang L, Jing S, Zhu X, Li X, Zeng W, Yuan H (2011) Identification of up-regulated genes in tea leaves under mild infestation of green leafhopper. Sci Hortic 130:476–481. https://doi.org/10.1016/j.scienta.2011.07.023
Yang H, Wang Y, Li L, Li F, He Y, Wu J, Wei C (2019) Transcriptomic and phytochemical analysis reveal root-mediated resource-based defense response to leaf-herbivory by Ectropis oblique in tea plant (Camellia sinensis). J Agric Food Chem 67:5465–5476. https://doi.org/10.1021/acs.jafc.9b00195
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36(12):2085–2103. https://doi.org/10.1111/pce.12122
Zeng L, Wang SP, Xu M (2001) Study on the resistance of tea plant to leafhopper (Empoasca vitis Gӧthe). J Tea Sci 2:11–14 (in Chinese)
Zhai CJ, Xu P, Zhang X, Guo Q, Zhang XG, Xu ZZ, Shen XL (2015) Development of Gossypium anomalum-derived microsatellite markers and their use for genome-wide identification of recombination between the G. anomalum and G. hirsutum genomes. Theor App Genet 128(8):1531–1540. https://doi.org/10.1007/s00122-015-2528-7
Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA, Gols R, Dicke M (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197(4):1291–1299. https://doi.org/10.1111/nph.12106
Zheng YT, Wang MX, Cui L, Han SJ, Yu PF, Han BY (2017) Resistance of tea cultivars to the tea green leafhopper analyzed by EPG technique and their resistance-related substances. Acta Ecol Sin 37(23):8015–8028. https://doi.org/10.5846/stxb201704270770
Zhou Q, Luo D, Chai XT, Wu YG, Nan ZB, Yang QC, Liu WX, Liu ZP (2018) Multiple regulatory networks are activated during cold stress in medicago sativa L. Int J Mol Sci. 19(10):3169. https://doi.org/10.3390/ijms19103169
We thank the technical staff and students at Chinese Academy of Agricultural Sciences including Ms. Zhaona Meng, Mr. Bo Chu and Mr. Long Jiao for their useful discussions.
Funding was provided by the State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops 2019 Open Fund (SKL20190010); Fu Jian Province “2011 Collaborative Innovation Center”; Chinese Oolong Tea Industry Innovation Center (Cultivation) special project (J2015-75); Industry-University Cooperation Project of Fujian Province (2016N5010); National Natural Science Foundation of China (31702052); Key Research and Development Program of Zhejiang province, China (2019C02033).
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Jin, S., Ren, Q., Lian, L. et al. Comparative transcriptomic analysis of resistant and susceptible tea cultivars in response to Empoasca onukii (Matsuda) damage. Planta 252, 10 (2020). https://doi.org/10.1007/s00425-020-03407-0
- Host plant resistance
- Molecular mechanism
- Tea small green leafhopper