Skip to main content
SpringerLink
Log in

Phytotoxicity mechanisms of two coumarin allelochemicals from Stellera chamaejasme in lettuce seedlings

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Stellera chamaejasme, a perennial weed which is an ecological threat, is widely distributed in some grasslands of Central and Eastern Asia. Our previous studies have identified several allelochemicals including two coumarins (umbelliferone and daphnoretin), from S. chamaejasme, and confirmed that allelopathy contributed to the competitive behavior of this weed. In this study, the inhibitory effects of umbelliferone and daphnoretin on lettuce seedlings and the mechanisms of their phytotoxicity were investigated. Results showed that shoot and root elongation and fresh weight of lettuce seedlings were effectively inhibited by umbelliferone in a concentration-dependent manner. Daphnoretin showed a weaker phytotoxicity. Both of the coumarins arrested the mitosis process in lettuce root tips and induced proline overproduction. Additionally, loss of cell viability and overproduction of reactive oxygen species in lettuce root cells were found after treatments with umbelliferone. Moreover, umbelliferone caused lipid peroxidation. These results suggested that umbelliferone displayed stronger phytotoxicity than daphnoretin on lettuce growth, and that the two coumarins had different mechanisms of phytotoxicity. That of daphnoretin was mainly dependent on its inhibitory effects on mitosis. Umbelliferone caused membrane lipid peroxide formation and cell death by inducing ROS overproduction, and impacted cell division, which resulted in growth inhibition of the receptor plant.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

DHE:

Dihydroethidium

FDA:

Fluorescein diacetate

FW:

Fresh weight

MDA:

Malondialdehyde

MI:

Mitosis index

PCD:

Program cell death

PI:

Propidium iodide

ROS:

Reactive oxygen species

References

  • Abenavoli MR, Sorgonà A, Sidari M, Badiani M, Fuggi A (2003) Coumarin inhibits the growth of carrot (Daucus carota L. cv. Saint Valery) cells in suspension culture. J Plant Physiol 160:227–237

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Baker CJ, Mock NM (1994) An improved method for monitoring cell death in a cell suspension and leaf disk assays using Evans blue. Plant Cell Tiss Org Cult 39:7–12

    Article  Google Scholar 

  • Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Chuang JY, Huang YF, Lu HF, Ho HC, Yang JS, Li TM, Chang NW, Chung JG (2007) Coumarin induces cell cycle arrest and apoptosis in human cervical cancer HeLa cells through a mitochondria- and caspase-3 dependent mechanism and NF-κB down-regulation. In vivo 21:1003–1010

    CAS  PubMed  Google Scholar 

  • Cui HY, Jin H, Liu Q, Yan ZQ, Ding L, Qin B (2014) Nematicidal metabolites from roots of Stellera chamaejasme against Bursaphelenchus xylophilus and Bursaphelenchus mucronatus. Pest Manag Sci 70:827–835

    Article  CAS  PubMed  Google Scholar 

  • Cullen JJ, Hinkhouse MM, Grady M, Gaut AW, Liu J, Zhang Y, Weydert CJD, Domann FE, Oberley LW (2003) Dicumarol inhibition of NADPH: quinone oxidoreductase induces growth inhibition of pancreatic cancer via a superoxide-mediated mechanism. Cancer Res 63:5513–5520

    CAS  PubMed  Google Scholar 

  • Frew JE, Jones P, Scholes G (1983) Spectrophotometric determination of hydrogen peroxide and organic hydropheroxides at low concentrations in aqueous solution. Anal Chim Acta 155:139–150

    Article  CAS  Google Scholar 

  • Garnczarska M (2005) Response of the ascorbate-glutathione cycle to re-aeration following hypoxia in lupine roots. Plant Physiol Biochem 43:583–590

    Article  CAS  PubMed  Google Scholar 

  • Goodwin RH, Taves C (1950) The effect of coumarin derivatives on the growth of Avena roots. Am J Bot 37:224–231

    Article  CAS  Google Scholar 

  • Guo HR, Cui HY, Jin H, Yan ZQ, Ding L, Qin B (2015) Potential allelochemicals in root zone soils of Stellera chamaejasme L. and variations at different geographical growing sites. Plant Growth Regul 77:335–342

    Article  CAS  Google Scholar 

  • Hao W, Zhang X, Zhao W, Chen X (2014) Psoralidin induces autophagy through ROS generation which inhibits the proliferation of human lung cancer A549 cells. PeerJ 2:e555

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Jankay P, Muller WH (1976) The relationships among umbelliferone, growth, and peroxidase levels in cucumber roots. Am J Bot 63:126–132

    Article  Google Scholar 

  • Katsuhara M, Otsuka T, Ezaki B (2005) Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci 169:369–373

    Article  CAS  Google Scholar 

  • Ko CH, Shen SC, Chen YC (2004) Hydroxylation at C4′ or C6 is essential for apoptosis-inducing activity of flavanone through activation of the caspase-3 cascade and production of reactive oxygen species. Free Radic Biol Med 36:897–910

    Article  CAS  PubMed  Google Scholar 

  • Koodkaew I, Sunohara Y, Matsuyama S, Matsumoto H (2012) Phytotoxic action mechanism of hapalocyclamide in lettuce seedlings. Plant Physiol Biochem 58:23–28

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Zhou Y, Xie C, Chen D, Li J (2012) Novel microtubule-targeted agent 6-chloro-4-(methoxyphenyl) coumarin induces G2-M arrest and apoptosis in HeLa cells. Acta Pharmacol Sin 33:407–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makepeace W, Dobson AT (1985) Interference phenomena due to mouse-ear and king devil hawkweed. N Z J Bot 23:79–90

    Article  Google Scholar 

  • Morikawa CIO, Miyaura R, Kamo T, Hiradate S, Perez JAC, Fujii Y (2011) Isolation of umbelliferone as a principal allelochemical from the Peruvian medicinal plant Diplostephium foliosissimum (Asteraceae). Rev Soc Quím Perú 77:285–291

    CAS  Google Scholar 

  • Nebo L, Varela RM, Molinillo JMG, Sampaio OM, Severino VGP, Cazal CM, Fernandes MFG, Fernandes JB, Macías FA (2014) Phytotoxicity of alkaloids, coumarins and flavonoids isolated from 11 species belonging to the Rutaceae and Meliaceae families. Phytochem Lett 8:226–232

    Article  CAS  Google Scholar 

  • Pan J, Zhu M, Chen H (2001) Aluminum-induced cell death in root-tip cells of barley. Environ Exp Bot 46:71–79

    Article  CAS  PubMed  Google Scholar 

  • Pan L, Li XZ, Yan ZQ, Guo HR, Qin B (2015) Phytotoxicity of umbelliferone and its analogs: structure-activity relationships and action mechanisms. Plant Physiol Biochem 97:272–277

    Article  CAS  PubMed  Google Scholar 

  • Pollock BM, Goodwin RH, Greene S (1954) Studies on roots. II. Effects of coumarin, scopoletin and other substances on growth. Am J Bot 41:521–529

    Article  CAS  Google Scholar 

  • Razavi SM (2011) Plant coumarins as allelopathic agents. Int J Biol Chem 5:86–90

    Article  CAS  Google Scholar 

  • Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444

    Article  CAS  PubMed  Google Scholar 

  • Sharma OP, Sharma S, Pattabhi V, Mahato SB, Sharma PD (2007) A review of the hepatotoxic plant Lantana camara. Crit Rev Toxicol 37:313–352

    Article  CAS  PubMed  Google Scholar 

  • Shettel NL, Balke NE (1983) Plant growth response to several allelopathic chemicals. Weed Sci 31:293–298

    CAS  Google Scholar 

  • Shimomura H, Sashida Y, Nakata H, Kawasaki J, lto Y (1982) Plant growth regulators from Heracleunr lanatunr. Photochemistry 2(l):2213–2215

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Veselin P, Jacques H, Bernd MR, Savov GT (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:e69

    Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan ZQ, Guo HR, Yang JY, Liu Q, Jin H, Xu R, Cui HY, Qin B (2014) Phytotoxic flavonoids from roots of Stellera chamaejasme L. (Thymelaeaceae). Phytochemistry 106:61–68

    Article  CAS  PubMed  Google Scholar 

  • Yan ZQ, Wang DD, Ding L, Cui HY, Jin H, Yang XY, Yang JS, Qin B (2015) Mechanism of artemisinin phytotoxicity action: induction of reactive oxygen species and cell death in lettuce seedlings. Plant Physiol Biochem 88:53–59

    Article  CAS  PubMed  Google Scholar 

  • Yang JY, Yan ZQ, Xu R, Liu Q, Jin H, Cui HY, Qin B (2011) Isolation of plant growth inhibitory components from the root of Stellera chamaejasme and function mechanism. Acta Bot Boreal Occident Sin 31:0291–0297

    CAS  Google Scholar 

  • Yaoya S, Kanho HY, Itani T, Umehara K, Kuroyanagi M (2004) Umbelliferone released from hairy root cultures of Pharbitis nil treated with copper sulfate and its subsequent glucosylation. Biosci Biotechnol Biochem 68:1837–1841

    Article  CAS  PubMed  Google Scholar 

  • Yu S, Hu D, Zhang J (2015) Umbelliferone exhibits anticancer activity via the induction of apoptosis and cell cycle arrest in HepG2 hepatocellular carcinoma cells. Mol Med Rep 12:3869–3873

    CAS  PubMed  Google Scholar 

  • Zhang ZQ, Zhang YH, Sun H (2011) The reproductive biology of Stellera chamaejasme (Thymelaeaceae): a self-incompatible weed with specialized flowers. Flora 206:567–574

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31300290, 21302195 and 31570354), CAS "Light of West China" Program, Agricultural Biotechnology Research and Development Program of Gansu Province (GNSW-2015-25), Cooperation Program to Gansu Province of Lanzhou Branch of the Chinese Academy of Sciences, and the Open Project of Key Laboratory for Tobacco Gene Resources, Institute of Tobacco Research, Chinese Academy of Agricultural Sciences.

Author information

Authors and Affiliations

  1. CAS Key Laboratory of Chemistry of Northwestern Plant Resources, Key Laboratory for Natural Medicine of Gansu Province, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, Lanzhou, 730000, People’s Republic of China

    Zhiqiang Yan, Dandan Wang, Hui Jin, Xiuzhuang Li, Xiaoyan Yang, Hongru Guo, Xiaofeng He, Le Pan, Xia Ren, Kai Guo & Bo Qin

  2. School of Forensic Medicine, Shanxi Medical University, Taiyuan, 030001, People’s Republic of China

    Haiyan Cui

  3. Enshi Academy of Agricultural Sciences, Enshi, 445000, People’s Republic of China

    Denghong Zhang

  4. Key Laboratory for Tobacco Gene Resources, Institute of Tobacco Research, Chinese Academy of Agricultural Sciences, Qingdao, 266101, People’s Republic of China

    Yuhe Sun

Authors
  1. Zhiqiang Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dandan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiyan Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denghong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuhe Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hui Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiuzhuang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaoyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hongru Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiaofeng He
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Le Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Xia Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kai Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Bo Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bo Qin.

Additional information

Communicated by A. Gniazdowska-Piekarska.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, Z., Wang, D., Cui, H. et al. Phytotoxicity mechanisms of two coumarin allelochemicals from Stellera chamaejasme in lettuce seedlings. Acta Physiol Plant 38, 248 (2016). https://doi.org/10.1007/s11738-016-2270-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2270-z

Keywords

Search

Navigation