Advertisement

Essential oil of Chrysanthemum indicum L.: potential biocontrol agent against plant pathogen Phytophthora nicotianae

  • Xiao-Bin Han
  • Jian Zhao
  • Jian-Min CaoEmail author
  • Cheng-Sheng ZhangEmail author
Research Article
  • 71 Downloads

Abstract

Phytophthora nicotianae is currently considered one of the most devastating oomycete plant pathogens, and its control frequently relies solely on the use of systemic fungicides. There is an urgent need to find environment-friendly control techniques. This study examined the chemical composition, inhibitory activity, and possible modes of action of the essential oil of Chrysanthemum indicum L. (EOC) flower heads against P. nicotianae. The EOC was obtained using hydrodistillation at a 0.15% yielded. It inhibited mycelial growth and spore germination of P. nicotianae at a minimum inhibitory concentration (MIC) of 200 μL/L, and exhibited fumigation effects (92.68% inhibition at 157.48 μL/L). Marked deformation of P. nicotianae mycelia included deformed tip enlargement, shrinkage, and rupture. Further, 55 and 47 compounds were identified using gas chromatography-mass spectrometry (GC-MS) and headspace solid-phase microextraction (HS-SPME) GC-MS analyses, representing 88.2% and 98.91% of the total EOC, respectively. Monoterpenes (25.77%) and sesquiterpenes (54.14%) were the major components identified using GC-MS, whereas monoterpenes were the main constituents in the HS-SPME GC-MS analysis. The higher proportions of sesquiterpenes and monoterpenes could be responsible for the inhibitory activity of EOC, which increased mycelia membrane permeability and the content of mycelial malondialdehyde (MDA) in a dose-dependent manner. Cell death also occurred. Thus, destruction of the cell wall and membrane might be two modes of action of EOC. Our results would be useful for the development of a new plant source of fungicide for P. nicotianae-induced disease.

Keywords

Botanical fungicide Inhibitory activity Action mode Oomycete pathogen Chemical composition 

Notes

Funding information

This work was supported by the Agricultural Science and Technology Innovation Program of China (ASTIP-TRIC07) and Zunyi Agricultural Science and Technology Project (201610).

Supplementary material

11356_2019_4152_MOESM1_ESM.docx (683 kb)
ESM 1 (DOCX 683 kb)

References

  1. Ahmed Y, Onghia AMD, Ippolito A, Shimy HEL, Cirvilleri G, Yaseen T (2012) Phytophthora nicotianae is the predominant Phytophthora species in citrus nurseries in Egypt. Phytopathol Mediterr 51:519–527Google Scholar
  2. Bajpai VK, Rahman A, Kang SC (2007) Chemical composition and anti-fungal properties of the essential oil and crude extracts of Metasequoia glyptostroboides Miki ex Hu. Ind Crop Prod 26:28–35Google Scholar
  3. Benelli G, Pavela R (2018) Repellence of essential oils and selected compounds against ticks—a systematic review. Acta Trop 179:47–54CrossRefGoogle Scholar
  4. Benelli G, Rajeswary M, Vijayan P, Senthilmurugan S, Alharbi NS, Kadaikunnan S, Khaled JM, Govindarajan M (2017) Boswellia ovalifoliolata (Burseraceae) essential oil as an eco-friendly larvicide? Toxicity against six mosquito vectors of public health importance, non-target mosquito fishes, backswimmers, and water bugs. Environ Sci Pollut Res (2018) 25:10264–10271CrossRefGoogle Scholar
  5. Benomari FZ, Andreu V, Kotarba J, Amine Dib ME, Bertrand C, Muselli A, Costa J, Djabou N (2018) Essential oils from Algerian species of Mentha as new bio-control agents against phytopathogen strains. Environ Sci Pollut Res 25:10264–10271CrossRefGoogle Scholar
  6. Bowers JH, Locke JC (2004) Effect of formulated plant extracts and oils on population density of Phytophthora nicotianae in soil and control of Phytophthora blight in the greenhouse. Plant Dis 88:11–16CrossRefGoogle Scholar
  7. Chen J, Xu X, Fang Y, Li S, Zhang Y (2013) Chemical composition and antibacterial activity of the essential oil from the aerial parts of Torilis japonica. J Essent Oil Bear Pl 16:499–505CrossRefGoogle Scholar
  8. Cheng SS, Lin HY, Chang ST (2005) Chemical composition and antifungal activity of essential oils from different tissues of Japanese cedar (Cryptomeria japonica). J Agr Food Chem 53:614–619CrossRefGoogle Scholar
  9. Dewitte K, Landschoot S, Carrette J, Audenaert K, Haesaert G (2018) Exploration of essential oils as alternatives to conventional fungicides in lupin cultivation. Org Agr.  https://doi.org/10.1007/s13165-018-0212-3
  10. Ertaş A, Boğa M, Yılmaz MAY, Yeşil Y, Haşimi N, Kaya MS, Temel H, Kolak U (2014) Chemical compositions by using LC-MS/MS and GC-MS and biological activities of Sedum sediforme (Jacq.). Pau. J Agric Food Chem 62:4601–4609CrossRefGoogle Scholar
  11. Fan S, Chang J, Zong Y, Hu G, Jia J (2018) GC-MS analysis of the composition of the essential oil from Dendranthema indicum var. Aromaticum using three extraction methods and two columns. Molecules 23(3):E576.  https://doi.org/10.3390/molecules23030576
  12. Fujita K, Fujita T, Kubo I (2007) Anethole, a potential antimicrobial synergist, converts a fungistatic dodecanol to a fungicidal agent. Phytother Res 21:47–51CrossRefGoogle Scholar
  13. Gandomi H, Misaghi A, Basti AA, Hamedi H, Shirvani ZR (2011) Effect of Zataria multiflora Boiss. essential oil on colony morphology and ultrastructure of Aspergillus flavus. Mycoses 54:429–437CrossRefGoogle Scholar
  14. Grote D, Claussen W (2011) Severity of root rot on tomato plants caused by Phytophthora nicotianae under nutrient- and light-stress conditions. Plant Pathol 50:702–707CrossRefGoogle Scholar
  15. Guntiya N, Bussaban B, Faiyue B, Uthaibutra J, Saengnil K (2016) Application of gaseous chlorine dioxide for control of fungal fruit rot disease of harvested ‘Daw’ longan. Sci Hortic 213:164–172CrossRefGoogle Scholar
  16. Han T, You C, Zhang L, Feng C, Zhang C, Wang J, Kong F (2015) Biocontrol potential of antagonist Bacillus subtilis Tpb55 against tobacco black shank. BioControl 61:195–205CrossRefGoogle Scholar
  17. Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19:140–145CrossRefGoogle Scholar
  18. Jing C, Gou J, Han X, Wu Q, Zhang C (2017) In vitro and in vivo activities of eugenol against tobacco black shank caused by Phytophthora nicotianae. Pestic Biochem Phys 142:148–154CrossRefGoogle Scholar
  19. Lee Y, Kim J, Lee S, Oh E, Shin S, Park I (2009) Effects of plant essential oils and components from Oriental sweetgum (Liquidambar orientalis) on growth and morphogenesis of three phytopathogenic fungi. Pestic Biochem Phys 93:138–143CrossRefGoogle Scholar
  20. Lin Z, Hua Y (1998) A study on the chemical constituents of the essential oil from Dendranthema indicum (L.) Des Moul. J Integ Plant Biol 30:220–222Google Scholar
  21. Liu X, Ouyang C, Wang Q, Li Y, Yan D, Yang D, Fang W, Cao A, Guo M (2017) Effects of oil extracts of Eupatorium adenophorumon on Phytophthora capsici and other plant pathogenic fungi in vitro. Pestic Biochem Phys 140:90–96CrossRefGoogle Scholar
  22. Lu M, Han Z, Li Z, Zhang Y, Peng Y, Xu Y, Yao L (2012) Antimicrobial activities of lemongrass essential oil against Phytophthora parasitica var. nicotianae. J Shanghai Jiaotong Univ (Agric Sci) 30:67–71Google Scholar
  23. Lu M, Han Z, Yao L (2013) In vitro and in vivo antimicrobial efficacy of essential oils and individual compounds against Phytophthora parasitica var. nicotianae. J Appl Microbiol 115:187–198CrossRefGoogle Scholar
  24. Ma L, Qiao Y, Du L, Li Y, Huang S, Liu F, Xiao D (2017) Evaluation and optimization of a superior extraction method for the characterization of the volatile profile of black tea by HS-SPME/GC-MS. Food Anal Methods 10:2481–2489CrossRefGoogle Scholar
  25. Marei GIK, Abdel Rasoul MA, Abdelgaleil SAM (2012) Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi. Pestic Biochem Physiol 103:56–56CrossRefGoogle Scholar
  26. Morcia C, Malnati M, Terzi V (2012) In vitro antifungal activity of terpinen-4-ol, eugenol, carvone, 1,8-cineole (eucalyptol) and thymol against mycotoxigenic plant pathogens. Food Addit Contam Part A 29:415–422Google Scholar
  27. Obaid AJ, Al-Janabi JKA, Taj-Aldin W (2017) Chemical composition and bioactivity characteristics of Pimpinella anisum essential oil against Trichophyton rubrum. J Global Pharma Tech 8(9):44–56Google Scholar
  28. Omran SM, Moodi MA, Amiri SMBNA, Mosavi SJ, Saeed SAMGM, Shiade SMJS, Kheradi E, Salehi M (2011) The effects of limonene and orange peel extracts on some spoilage fungi. Int J Molec Clin Microbiol 1:82–86Google Scholar
  29. Panabières F, Ali GS, Allagui MB, Dalio RJD, Gudmestad NC, Kuhn M, Roy SG, Schena L, Zampounis A (2016) Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathol Mediterr 55:20–40Google Scholar
  30. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007CrossRefGoogle Scholar
  31. Pinto E, Goncalves MJ, Olivera P, Coelha J, Cavaleiro C, Salgueiro L (2014) Activity of Thymus caespititius essential oil and α-terpineol against yeasts and filamentous fungi. Ind Crop Prod 62:107–112CrossRefGoogle Scholar
  32. Pitarokili D, Tzakou O, Loukis A (2008) Composition of the essential oil of spontaneous Rosmarinus officinalis from Greece and antifungal activity against phytopathogenic fungi. J Essent Oil Res 20:457–459CrossRefGoogle Scholar
  33. Saddiq AA, Khayyat SA (2010) Chemical and antimicrobial studies of monoterpene: Citral. Pestic Biochem Physiol 98:89–93CrossRefGoogle Scholar
  34. Samaneh ET, Tayebeh R, Hassan E, Vahid N (2010) Composition of essential oils in subterranean organs of three species of Valeriana L. Nat Prod Res 24:1834–1842CrossRefGoogle Scholar
  35. Sameza ML, Boat MAB, Nguemezi ST, Mabou LCN, Dongmo PMJ, Boyom FF, Menut C (2014) Potential use of Eucalyptus globulus essential oil against Phytophthora colocasiae the causal agent of taro leaf blight. Eur J Plant Pathol 140:243–250CrossRefGoogle Scholar
  36. Santana AI, Vila R, Cañigueral S, Gupta MP (2016) Chemical composition and biological activity of essential oils from different species of piper from Panama. Planta Med 82:986–991CrossRefGoogle Scholar
  37. Silva F, Ferreira S, Duarte A, Mendonc DI, Domingues FC (2011) Antifungal activity of Coriandrum sativum essential oil, its mode of action against Candida species and potential synergism with amphotericin B. Phytomedicine 19:42–47CrossRefGoogle Scholar
  38. Tchameni SN, Mbiakeu SN, Sameza ML, Jazet PMD, Tchoumbougnang F (2017) Using Citrus aurantifolia essential oil for the potential biocontrol of Colocasia esculenta (taro) leaf blight caused by Phytophthora colocasiae. Environ Sci Pollut Res 12:1–7Google Scholar
  39. Tian J, Ban XQ, Zeng HZ, He JS, Chen YX, Wang YW (2012) The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS One 7:e30147CrossRefGoogle Scholar
  40. Villa-Ruano N, Pacheco-Hernández Y, Cruz-Durán R, Lozoya-Gloria E (2015) Volatiles and seasonal variation of the essential oil composition from the leaves of Clinopodium macrostemum var. laevigatum and its biological activities. Ind Crop Prod 77:741–747.  https://doi.org/10.1016/j.indcrop.2015.09.050 CrossRefGoogle Scholar
  41. Wu H, Huang Y, Chen K, Yan Y, Xu L, Liu Y (2012) Chemical composition and antimicrobial mechanism of essential oil from Dendranthema indicum var. aromaticum. Food Sci 33:35–39Google Scholar
  42. Wu Y, OuYang Q, Tao N (2016) Plasma membrane damage contributes to antifungal activity of citronellal against Penicillium Digitatum. J Food Sci Technol 53:3853–3858CrossRefGoogle Scholar
  43. You C, Zhang CS, Feng C, Wang J, Kong FY (2015) Myroides odoratimimus, a biocontrol agent from the rhizosphere of tobacco with potential to control Alternaria alternate. Biocontrol 60:555–564CrossRefGoogle Scholar
  44. Zhang CS, Xin H, Zou P (2017) Plants at beach in Shandong. Agricultural science and Technology Press, BeijingGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Pest Integrated Management Key Laboratory of China TobaccoTobacco Research Institute of Chinese Academy of Agricultural SciencesQingdaoChina
  2. 2.Microbial Organic Fertilizer Engineering Center of China Tobacco, Zunyi Branch of Guizhou Tobacco CompanyZunyiChina

Personalised recommendations