Skip to main content
Log in

Enhanced transcriptome responses in herbivore-infested tea plants by the green leaf volatile (Z)-3-hexenol

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Green leaf volatiles (GLVs) play a vital role in enhancing herbivore-associated defense responses, but the mechanism by which they precisely regulate such responses is not well understood. (Z)-3-Hexenol (z3HOL), an important component of GLVs, effectively activates the defense of tea plants (Camellia sinensis) against a tea geometrid (TG) Ectropis obliqua Prout. To elucidate the molecular mechanisms of defense activation by z3HOL, RNA-Sequencing was employed to investigate the effect of z3HOL on transcriptome responses to TG in tea plants. A total of 318 upregulated genes were identified, and expression of 10 unigenes was validated by quantitative real-time PCR. Among these 318 upregulated genes, 56 were defense-related, including 6 key enzyme genes in jasmonic acid, and ethylene biosynthesis, 24 signal transduction genes, and 12 insect-responsive transcription factors. Most of the defense-related genes are induced by JA, TG, or wounding treatments, suggesting that JA signaling plays a vital role in z3HOL-induced tea defense against TG.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

DEGs:

Differentially expressed genes

DGE:

Digital gene expression

GC–MS:

Gas chromatography-mass spectrometry

GLVs:

Green leaf volatiles

HIPVs:

Herbivore-induced plant volatiles

JA:

Jasmonic acid

MPKs:

Mitogen-activated protein kinases

PIs:

Proteinase inhibitors

PPO:

Polyphenol oxidase

qRT-PCR:

Quantitative real-time PCR

RH:

Relative air humidity

RLKs:

Receptor-like protein kinases

RNA-seq:

RNA sequencing

TFs:

Transcription factors

TG:

Tea geometrid

TPS:

Terpene synthase

XIPs:

Xylanase inhibitor proteins

z3HOL:

(Z)-3-Hexenol

References

  • Aljbory Z, Chen MS (2018) Indirect plant defense against insect herbivores: a review. Insect Sci 2018 25:2–23

    CAS  Google Scholar 

  • Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–1078

    Article  CAS  Google Scholar 

  • Ameye M, Audenaert K, De Zutter N, Steppe K, Van Meulebroek L, Vanhaecke L, De Vleesschauwer D, Haesaert G, Smagghe G (2015) Priming of wheat with the green leaf volatile Z-3-hexenyl acetate enhances defense against Fusarium graminearum but boosts deoxynivalenol production. Plant Physiol 167:1671–1684

    Article  CAS  Google Scholar 

  • Arfaoui A, El Hadrami A, Daayf F (2018) Pre-treatment of soybean plants with calcium stimulates ROS responses and mitigates infection by Sclerotinia sclerotiorum.. Plant Physiol Biochem 122:121–128

    Article  CAS  Google Scholar 

  • Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953

    Article  CAS  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore induced plant volatiles, beyond the cry for help. Trends Plant Sci 15:167–175

    Article  CAS  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS, Olga A, Aleynova OA (2017) The calcium-dependent protein kinase gene VaCPK29 is involved in grapevine responses to heat and osmotic stresses. Plant Growth Regul 82:79–89

    Article  CAS  Google Scholar 

  • Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785

    Article  CAS  Google Scholar 

  • Engelberth J, Contreras CF, Dalvi C, Li T, Engelberth M (2013) Early transcriptome analyses of Z-3-hexenol-treated Zea mays revealed distinct transcriptional networks and anti-herbivore defense potential of green leaf volatiles. PLoS One 810:e77465

    Article  Google Scholar 

  • Farag MA, Fokar M, Zhang HA, Allen RD, Paré PW (2005) Z-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220:900–909

    Article  CAS  Google Scholar 

  • Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. N Phytol 180:722–734

    Article  CAS  Google Scholar 

  • He XR, Chen X, Lin SB, Mo XC, Zhou PY, Zhang ZH, Lu YY, Gu HN, Shang ZC, Lou YG, Wu J (2017) Diversity-oriented synthesis as a tool for identifying new chemical elicitors. ChemistryOpen 6:102–111

    Article  CAS  Google Scholar 

  • Hu LF, Ye M, Zhang TF, Li R, Zhou GX, Wang Q, Lu J, Lou YG (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of map kinase activity. Plant Physiol 169:2907–2921

    Article  CAS  Google Scholar 

  • Kachroo A, Robin GP (2013) Systemic signaling during plant defense. Curr Opin Plant Biol 16:527–533

    Article  CAS  Google Scholar 

  • Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292

    Article  Google Scholar 

  • Kiep V, Vadassery J, Lattke J, Maass JP, Boland W, Peiter E, Mithofer A (2015) Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis. N Phytol 207:996–1004

    Article  CAS  Google Scholar 

  • Liu S, Han B (2010) Differential expression pattern of an acidic 9/13-lipoxygenase in flower opening and senescence and in leaf response to phloem feeders in the tea plant. BMC Plant Biol 10:228

    Article  Google Scholar 

  • Lu J, Ju HP, Zhou GX, Zhu CS, Erb M, Wang XP, Wang P, Lou YG (2011) An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. Plant J 68:583–596

    Article  CAS  Google Scholar 

  • Lu J, Li JC, Ju HP, Liu XL, Erb M, Wang X, Lou YG (2014) Contrasting effects of ethylene biosynthesis on induced plant resistance against a chewing and a piercing-sucking herbivore in rice. Mol Plant 7:1670–1682

    Article  CAS  Google Scholar 

  • Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512

    Article  CAS  Google Scholar 

  • Mazars C, Thuleau P, Lamotte O, Bourque S (2010) Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 3:706–718

    Article  CAS  Google Scholar 

  • Mithofer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on Lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168

    Article  Google Scholar 

  • Parry D, Spence JR, Volney WJA (1998) Budbreak phenology and natural enemies mediate survival of first-instar forest tent caterpillar (Lepidoptera: Lasiocampidae). Environ Entomol 27:1368–1374

    Article  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  Google Scholar 

  • Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: A plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811

    Article  CAS  Google Scholar 

  • Szczegielniak J, Borkiewicz L, Szurmak B, Lewandowska-Gnatowska E, Statkiewicz M, Klimecka M, Cieśla J, Muszyńska G (2012) Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Plant Physiol 146:1–14

    Article  CAS  Google Scholar 

  • Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, Midega CAO, Ogol CKPO, Mayon P, Birkett MA, Pickett JA, Khan ZR (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14:1075–1083

    Article  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  Google Scholar 

  • Xin Z, Wang Q, Yu Z, Hu L, Li J, Xiang C, Wang B, Lou Y (2014) Overexpression of a xylanase inhibitor gene, OsHI-XIP, enhances resistance in rice to herbivores. Plant Mol Biol Rep 32:465–475

    Article  CAS  Google Scholar 

  • Xin Z, Li X, Li J, Chen Z, Sun X (2016) Application of chemical elicitor (Z)-3-hexenol enhances direct and indirect plant defenses against tea geometrid Ectropis obliqua. Biocontrol 61:1–12

    Article  CAS  Google Scholar 

  • Yang ZW, Duan XN, Jin S, Li XW, Chen ZM, Ren BZ, Sun XL (2013) Regurgitant derived from the tea geometrid Ectropis obliqua suppresses wound-induced polyphenol oxidases activity in tea plants. J Chem Ecol 39:744–751

    Article  CAS  Google Scholar 

  • Ye GY, Xiao Q, Chen M, Chen XX, Yuan ZJ, Stanley DW, Hu C (2014) Tea: biological control of insect and mite pests in China. Biol Control 68:73–91

    Article  Google Scholar 

  • Zhao QY, Wang Y, Kong YM, Luo D, Li X, Hao P (2011) Optimizing de novo transcriptome assembly from short-read RNA-Seq data: a comparative study. BMC Bioinform 12:s2

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The study was jointly sponsored by the Special Fund for Agro-scientific Research in the Public Interest (201403030), the Central Public-interest Scientific Institution Basal Research Fund (no. 1610212016019), the National Natural Science Foundation of China (31401758), and the Science and Technology Program of Zhejiang Province (2016C32026).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoling Sun.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 219 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xin, Z., Ge, L., Chen, S. et al. Enhanced transcriptome responses in herbivore-infested tea plants by the green leaf volatile (Z)-3-hexenol. J Plant Res 132, 285–293 (2019). https://doi.org/10.1007/s10265-019-01094-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-019-01094-x

Keywords

Navigation