Skip to main content
Log in

(Z)-3-Hexen-1-ol accumulation enhances hyperosmotic stress tolerance in Camellia sinensis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Volatile components in fresh leaves are involved in the regulation of many stress responses, such as insect damage, fungal infection and high temperature. However, the potential function of volatile components in hyperosmotic response is largely unknown. Here, we found that 7-day hyperosmotic treatment specifically led to the accumulation of (Z)-3-hexen-1-ol, (E)-2-hexenal and methyl salicylate. Transcriptome and qRT-PCR analyses suggested the activation of linolenic acid degradation and methyl salicylate processes. Importantly, exogenous (Z)-3-hexen-1-ol pretreatment dramatically enhanced the hyperosmotic stress tolerance of tea plants and decreased stomatal conductance, whereas (E)-2-hexenal and methyl salicylate pretreatments did not exhibit such a function. qRT-PCR analysis revealed that exogenous ABA induced the expressions of related enzyme genes, and (Z)-3-hexen-1-ol could up-regulate the expressions of many DREB and RD genes. Moreover, exogenous (Z)-3-hexen-1-ol tremendously induced the expressions of specific LOX and ADH genes within 24 h. Taken together, hyperosmotic stress induced (Z)-3-hexen-1-ol accumulation in tea plant via the activation of most LOX, HPL and ADH genes, while (Z)-3-hexen-1-ol could dramatically enhance the hyperosmotic stress tolerance via the decrease of stomatal conductance and MDA, accumulation of ABA and proline, activation of DREB and RD gene expressions, and probably positive feedback regulation of LOXs and ADHs.

Key message

Hyperosmotic stress induced (Z)-3-hexen-1-ol accumulation in Camellia sinensis via the up-regulation of most LOX, HPL and ADH genes, while (Z)-3-hexen-1-ol could dramatically enhance the hyperosmotic stress tolerance via the decrease of stomatal conductance, accumulation of proline, activation of DREB and RD gene expressions, and probably positive feedback regulation of LOXs and ADHs.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ADH:

Alcohol dehydrogenase

bp:

Base pair

DEG:

Differentially expressed gene

DREB:

Dehydration responsive element binding protein

DW:

Dry weight

GC–MS:

Gas chromatography-mass spectrometer

GLV:

Green leaf volatile

GO:

Gene ontology

HI:

Hexenal isomerase

HPL:

Hydroperoxide lyase

KEGG:

Kyoto encyclopedia of genes and genomes

LOX:

Lipoxygenase

qRT-PCR:

Quantitative real-time polymerase chain reaction

References

  • Bate NJ, Riley JCM, Thompson JE, Rothstein SJ (2010) Quantitative and qualitative differences in C6-volatile production from the lipoxygenase pathway in an alcohol dehydrogenase mutant of Arabidopsis thaliana. Physiol Plant 104(1):97–104

    Google Scholar 

  • Cao H, Wang L, Yue C, Hao X, Wang X, Yang Y (2015) Isolation and expression analysis of 18 CsbZIP genes implicated in abiotic stress responses in the tea plant (Camellia sinensis). Plant Physiol Biochem 97:432–442

    CAS  PubMed  Google Scholar 

  • Chen G, Hackett R, Walker D, Taylor A, Lin Z, Grierson D (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant Physiol 136(1):2641–2651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Copolovici L, Kännaste A, Pazouki L, Niinemets U (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169(7):664–672

    CAS  PubMed  Google Scholar 

  • Dong F, Yang Z, Baldermann S, Sato Y, Asai T, Watanabe N (2011) Herbivore-induced volatiles from tea (Camellia sinensis) plants and their involvement in intraplant communication and changes in endogenous nonvolatile metabolites. J Agric Food Chem 59(24):13131–13135

    CAS  PubMed  Google Scholar 

  • Expositoalonso M, Vasseur F, Ding W, Wang G, Burbano HA, Weigel D (2018) Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana. Nat Ecol Evol 2:352–358

    Google Scholar 

  • Fang W, Zhang Y, Zhou L, Wang W, Li X (2013) Isolation and characterization of Histone1 gene and its promoter from tea plant (Camellia sinensis). Mol Biol Rep 40(5):3641–3648

    CAS  PubMed  Google Scholar 

  • Galvez DA, Landhäusser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31(3):250–257

    PubMed  Google Scholar 

  • Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69(9):1838–1849

    CAS  PubMed  Google Scholar 

  • Halitschke R, Ziegler J, Keinänen M, Baldwin IT (2010) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. Plant J 40(1):35–46

    Google Scholar 

  • Hatanaka A, Kajiwara T, Sekiya J (2017) Biosynthetic pathway for C 6-aldehydes formation from linolenic acid in green leaves. Chem Phys Lipid 44:341–361

    Google Scholar 

  • Howe GA, Lee GI, Li L, Derocher AE (2000) Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol 123(2):711–724

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iyer S, Caplan A (1998) Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol 116(1):203–211

    CAS  PubMed Central  Google Scholar 

  • Jing T, Zhang N, Gao T, Zhao M, Jin J, Chen Y et al (2018) Glucosylation of (Z)-3-hexenol informs intraspecies interactions in plants: a case study in Camellia sinensis. Plant Cell Environ 42(4):1352–1367

    PubMed  Google Scholar 

  • Joshi R, Gulati A (2011) Biochemical attributes of tea flowers ( Camellia sinensis ) at different developmental stages in the Kangra region of India. Sci Hortic 130(1):266–274

    CAS  Google Scholar 

  • Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T et al (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52(12):2136–2146

    CAS  PubMed  Google Scholar 

  • Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K et al (2012) Arabidopsis GROWTH-REGULATING FACTOR7 functions as a transcriptional repressor of abscisic acid–and osmotic stress–responsive genes, including DREB2A. Plant Cell 24(8):3393–3405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46(7):1093–1102

    CAS  PubMed  Google Scholar 

  • Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2006) Components of C6-aldehyde-induced resistance in Arabidopsis thaliana against a necrotrophic fungal pathogen, Botrytis cinerea. Plant Sci 170(4):715–723

    CAS  Google Scholar 

  • Kunishima M, Yamauchi Y, Mizutani M, Kuse M, Takikawa H, Sugimoto Y (2016) Identification of (Z)-3:(E)-2-hexenal isomerases essential to the production of the leaf aldehyde in plants. J Biol Chem 291(27):14023

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li XW, Feng ZG, Yang HM, Zhu XP (2010) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt- and dehydration-tolerance in tobacco. Biochem Biophys Res Commun 394(2):354–359

    CAS  PubMed  Google Scholar 

  • Li Y, Huang J, Song X, Zhang Z, Jiang Y, Zhu Y et al (2017) An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant. Planta 246(1):91–103

    CAS  PubMed  Google Scholar 

  • Liu SC, Yao MZ, Ma CL, Jin JQ, Ma JQ, Li CF et al (2015) Physiological changes and differential gene expression of tea plant under dehydration and rehydration conditions. Sci Hortic 184:129–141

    CAS  Google Scholar 

  • Liu SC, Xu YX, Ma JQ, Wang WW, Chen W, Huang DJ et al (2016) Small RNA and degradome profiling reveals important roles for MicroRNAs and their targets in tea plant response to drought stress. Physiol Plant 158(4):435–451

    CAS  PubMed  Google Scholar 

  • Loreto F, Barta C, Brilli F, Nogues I (2010) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29(9):1820–1828

    Google Scholar 

  • Mano J, Torii Y, Hayashi S, Takimoto K, Matsui K, Nakamura K et al (2002) The NADPH: quinone oxidoreductase P1-ζ-crystallin in Arabidopsis catalyzes the α, β-hydrogenation of 2-alkenals: detoxication of the lipid peroxide-derived reactive aldehydes. Plant Cell Physiol 43(12):1445–1455

    CAS  PubMed  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5(3):237–243

    CAS  PubMed  Google Scholar 

  • Piesik D, Pańka D, Delaney KJ, Skoczek A, Lamparski R, Weaver DK (2011) Cereal crop volatile organic compound induction after mechanical injury, beetle herbivory (Oulema spp.), or fungal infection (Fusarium spp.). J Plant Physiol 168(9):878–886

    CAS  PubMed  Google Scholar 

  • Qin F, Sakuma Y, Tran L-SP, Maruyama K, Kidokoro S, Fujita Y et al (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress–responsive gene expression. Plant Cell 20(6):1693–1707

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanderson GW, Grahamm HN (1973) Formation of black tea aroma. J Agric Food Chem 21(4):576–585

    CAS  Google Scholar 

  • Sharma P, Kumar S (2005) Differential display-mediated identification of three drought-responsive expressed sequence tags in tea [Camellia sinensis (L.) O. Kuntze]. J Biosci 30(2):231–235

    CAS  PubMed  Google Scholar 

  • Shyp V, Tankov S, Ermakov A, Kudrin P, English BP, Ehrenberg M et al (2012) Positive allosteric feedback regulation of the stringent response enzyme RelA by its product. EMBO Rep 13(9):835–839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyaya H, Panda SK (2004) Responses of Camellia sinensis to drought and rehydration. Biol Plant 48(4):597–600

    Google Scholar 

  • Upadhyaya H, Panda SK, Dutta BK (2008) Variation of physiological and antioxidative responses in tea cultivars subjected to elevated water stress followed by rehydration recovery. Acta Physiol Plant 30(4):457–468

    CAS  Google Scholar 

  • Wang L, Lin Z, Hai-Peng L, Tan JF, Guo L (2010) Research progress in affecting factors of tea aroma. Food Sci 31(15):293–298

    Google Scholar 

  • Wang W, Wang Y, Du Y, Zhao Z, Zhu X, Jiang X et al (2014) Overexpression of Camellia sinensis H1 histone gene confers abiotic stress tolerance in transgenic tobacco. Plant Cell Rep 33(11):1829–1841

    CAS  PubMed  Google Scholar 

  • Wang P, Zhao L, Hou H, Zhang H, Huang Y, Wang Y et al (2015) Epigenetic changes are associated with programmed cell death induced by heat stress in seedling leaves of Zea mays. Plant Cell Physiol 56(5):965–976

    CAS  PubMed  Google Scholar 

  • Wang YX, Liu ZW, Wu ZJ, Li H, Zhuang J (2016a) Transcriptome-wide identification and expression analysis of the NAC gene family in tea plant [Camellia sinensis (L.) O. Kuntze]. PLoS ONE 11(11):e0166727

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Shu Z, Wang W, Jiang X, Li D, Pan J et al (2016b) CsWRKY2, a novel WRKY gene from Camellia sinensis, is involved in cold and drought stress responses. Biol Plant 60(3):1–9

    Google Scholar 

  • Wenda-Piesik A (2011) Volatile organic compound emissions by winter wheat plants (Triticum aestivum L.) under Fusarium spp. infestation and various abiotic conditions. Pol J Environ Stud 20:1335–1342

    CAS  Google Scholar 

  • Xu YX, Mao J, Chen W, Qian TT, Liu SC, Hao WJ et al (2016) Identification and expression profiling of the auxin response factors (ARFs) in the tea plant (Camellia sinensis (L.) O. Kuntze) under various abiotic stresses. Plant Physiol Biochem 98:46–56

    CAS  PubMed  Google Scholar 

  • Yamauchi Y, Kunishima M, Mizutani M, Sugimoto Y (2015) Reactive short-chain leaf volatiles act as powerful inducers of abiotic stress-related gene expression. Sci Rep 5:8030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Kobayashi E, Katsuno T, Asanuma T, Fujimori T, Ishikawa T et al (2012) Characterisation of volatile and non-volatile metabolites in etiolated leaves of tea (Camellia sinensis) plants in the dark. Food Chem 135(4):2268–2276

    CAS  PubMed  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    CAS  PubMed  Google Scholar 

  • Zhang S, Yue Y, Sheng L, Wu Y, Fan G, Li A et al (2013) PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress. BMC Plant Biol 13(1):33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Cai M, Yu X, Wang L, Guo C, Ming R et al (2017) Transcriptome dynamics of Camellia sinensis in response to continuous salinity and drought stress. Tree Genet Genomes 13(4):78

    Google Scholar 

  • Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S et al (2014) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS ONE 9:e106070

    PubMed  PubMed Central  Google Scholar 

  • Zhou L, Xu H, Mischke S, Meinhardt LW, Zhang D, Zhu X et al (2014) Exogenous abscisic acid significantly affects proteome in tea plant (Camellia sinensis) exposed to drought stress. Hortic Res 1:14029

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Key R&D Program of China (2018YFD1000601) and Fundamental Research Funds for the Central Universities (2662016QD024).

Author information

Authors and Affiliations

Authors

Contributions

SH and PW designed the experiments. SH and QC performed the experiments. SH and PW wrote the manuscript. FG, MW, HZ, YW and DN revised the manuscript.

Corresponding author

Correspondence to Pu Wang.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Publisher's Note

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

Accession numbers

The data sets of raw sequencing reads have been deposited in the National Center for Biotechnology Information (NCBI) database and can be retrieved under the BioProject Accession Number PRJNA513275.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 688 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, S., Chen, Q., Guo, F. et al. (Z)-3-Hexen-1-ol accumulation enhances hyperosmotic stress tolerance in Camellia sinensis. Plant Mol Biol 103, 287–302 (2020). https://doi.org/10.1007/s11103-020-00992-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-00992-2

Keywords

Navigation