Tenuazonic acid-induced change in volatile emission from rose plants and its chemometrical analysis

  • Fa-zhong Yang
  • Yun-xian Li
  • Min Tang
  • Guo-lei Zhu
  • Shi-ping Zhou
  • Bin YangEmail author
Original Article


This study investigated changes in volatile organic chemicals (VOCs) of rose plants (Rosa chinensis Jacq.) after treatment with tenuazonic acid (TeA). TeA is a toxin produced by Alternaria alternata (Fr.) Keissler and is a key virulence factor for infection of the plants by the fungus. VOCs were collected in situ separately from intact live twigs of healthy and TeA-treated rose plants by dynamic headspace adsorption (DHSA) or from cut twigs of healthy and treated roses by headspace solid-phase microextraction (HS-SPME) and identified by gas chromatography–mass spectrum (GC–MS). VOC emissions changed significantly after the plants were treated with TeA based on the results obtained with both methods. GC–MS and chemometrical analysis show that the content of monoterpenes significantly increased the most, followed by ketones and alcohols, whereas sesquiterpenes decreased significantly, resulting from the induction by TeA. Twelve VOCs were emitted at significantly higher or lower levels from TeA-treated roses compared with healthy roses. After TeA treatment, the content of 4-hydroxy-4-methyl-2-pentanone increased by 80.1% (DHSA) and 67.8% (HS-SPME) while β-elemene decreased by 84.93% (DHSA) and 71.21% (HS-SPME). Butyl acetate, allo-ocimene, decanol and tetradecanol with their relatively large contents were detected only from TeA-treated roses as early as 2–4 days after treatment with TeA. This means that theses VOCs could be used as the markers for the detection of the fungus infection in rose plants before disease symptoms become visible. The obvious temporal effects of the changes in contents of these four VOCs were also recorded. The results will help to understand the chemical mechanisms of indirect plant-mediated interactions between phytopathogens and herbivorous insects in the ternary systems.


Volatile organic compound Rosa chinensis Tenuazonic acid GC–MS Terpenes Semiochemicals Biomarker Principal component analysis (PCA) Alternaria alternata Dynamic headspace adsorption (DHSA) Headspace solid-phase microextraction (HS-SPME) 



This study was financially supported by grants from the National Natural Science Foundation of China (Grant Nos. 31560517 and 31160354), the Yunnan Provincial Scientific and Technological Program (Grant No. 2017HB031) and the open funding from Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China (Southwest Forestry University, Grant No. KLESWFU-201806).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Baek S-J, Park A, Ahn Y-J, Choo J (2015) Baseline correction using asymmetrically reweighted penalized least squares smoothing. Analyst 140:250–257. CrossRefPubMedGoogle Scholar
  2. Beck JJ, Alborn HT, Block AK et al (2018) Interactions among plants, insects, and microbes: elucidation of inter-organismal chemical communications in agricultural ecology. J Agric Food Chem 66:6663–6674. CrossRefPubMedGoogle Scholar
  3. Becker EM, Herrfurth C, Irmisch S et al (2014) Infection of corn ears by Fusarium spp. induces the emission of volatile sesquiterpenes. J Agric Food Chem 62:5226–5236. CrossRefPubMedGoogle Scholar
  4. Franco FP, Moura DS, Vivanco JM et al (2017) Plant–insect–pathogen interactions: a naturally complex ménage à trois. Curr Opin Microbiol 37:54–60. CrossRefPubMedGoogle Scholar
  5. Giusto BD, Bessière JM, Guéroult M et al (2010) Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. J Ecol 98:845–856. CrossRefGoogle Scholar
  6. Gupta G, Agarwal U, Kaur H et al (2017) Aphicidal effects of terpenoids present in Citrus limon on Macrosiphum roseiformis and two generalist insect predators. J Asia Pac Entomol 20(4):1087–1095. CrossRefGoogle Scholar
  7. Hatcher PE (1995) Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol Rev 70:639–694. CrossRefGoogle Scholar
  8. Heikkenen HJ, Hrutfiord BF (1965) Dendroctonus pseudotsugae: a hypothesis regarding its primary attractant. Science 150(3702):1457–1459. CrossRefPubMedGoogle Scholar
  9. Indahl UG, Sahni NS, Kirkus B et al (1999) Multivariate strategies for classification based on NIR-spectra with application to mayonnaise. Chemometr Intell Lab 49:19–31. CrossRefGoogle Scholar
  10. Jackels SC, Marshall EE, Omaiye AG et al (2014) GCMS investigation of volatile compounds in green coffee affected by potato taste defect and the Antestia bug. J Agric Food Chem 62:10222–10229. CrossRefPubMedGoogle Scholar
  11. Kang Y, Feng H, Zhang J et al (2017) TeA is a key virulence factor for Alternaria alternata (Fr.) Keissler infection of its host. Plant Physiol Bioch 115:73–82. CrossRefGoogle Scholar
  12. Karban R, Adamchak R, Schnathorst WC (1987) Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 235(4789):678–680. CrossRefPubMedGoogle Scholar
  13. Nielsen N-PV, Carstensen JM, Smedsgaard J (1998) Aligning of single and multiple wavelength chromatographic profiles for chemometric data analysis using correlation optimized warping. J Chromatogr A 805:17–35. CrossRefGoogle Scholar
  14. Ostry V (2008) Alternaria mycotoxins: an overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs. World Mycotoxin J 1(2):175–188. CrossRefGoogle Scholar
  15. Pajaro-Castro N, Caballero-Gallardo K, Olivero-Verbel J (2017) Neurotoxic effects of linalool and β-pinene on Tribolium castaneum Herbst. Molecules 22(12):2052. CrossRefPubMedCentralGoogle Scholar
  16. Rizvi SZM, Raman A (2016) Volatiles from Botrytis cinerea-infected and healthy berries of Vitis vinifera influence the oviposition behaviour of Epiphyas postvittana. Entomol Exp Appl 160:47–56. CrossRefGoogle Scholar
  17. Rizvi SZM, Raman A (2017) Botrytis cinerea (Helotiales Sclerotiniaceae)-induced changes in Vitis vinifera (Vitales Vitaceae) leaves influence the oviposition behaviour and life history of Epiphyas postvittana (Lepidoptera Tortricidae). Ethol Ecol Evol 29:574–588. CrossRefGoogle Scholar
  18. Rizvi SZM, Raman A, Wheatley WM et al (2016) Oviposition preference and larval performance of Epiphyas postvittana (Lepidoptera: Tortricidae) on Botrytis cinerea (Helotiales: Sclerotiniaceae) infected berries of Vitis vinifera (Vitales: Vitaceae). Insect Sci 23:313–325. CrossRefPubMedGoogle Scholar
  19. Rostás M, Simon M, Hilker M (2003) Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl Ecol 4:43–62. CrossRefGoogle Scholar
  20. Sharifi R, Lee S-M, Ryu C-M (2017) Microbe-induced plant volatiles. New Phytol 220(3):1–8. CrossRefGoogle Scholar
  21. Simon M, Hilker M (2005) Does rust infection of willow affect feeding and oviposition behavior of willow leaf beetles? J Insect Behav 18:115–129. CrossRefGoogle Scholar
  22. Tan Y, Li D, Hua J et al (2017) Localization of a defensive volatile 4-hydroxy-4-methylpentan-2-one in the capitate glandular trichomes of Oenothera glazioviana. Plant Divers 39(3):154–159. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Tomasi G, van den Berg F, Andersson C (2004) Correlation optimized warping and dynamic time warping as preprocessing methods for chromatographic data. J Chemometr 18:231–241. CrossRefGoogle Scholar
  24. Yang FZ, Li L, Yang B (2012) Alternaria toxin-induced resistance against rose aphids and olfactory response of aphids to toxin-induced volatiles of rose plants. J Zhejiang Univ Sci B Biomed Biotechnol 13(2):126–135. CrossRefGoogle Scholar
  25. Yang FZ, Li Y, Yang B (2013) The inhibitory effects of rose powdery mildew infection on the oviposition behaviour and performance of beet armyworms. Entomol Exp Appl 148:39–47. CrossRefGoogle Scholar
  26. Yang FZ, Yang B, Li BB, Xiao C (2015) Alternaria toxin-induced resistance in rose plants against rose aphid (Macrosiphum rosivorum): effect of tenuazonic acid. J Zhejiang Univ Sci B Biomed Biotechnol 16(4):264–274. CrossRefGoogle Scholar
  27. Yekeler H, Bitmis K, Özcelik N et al (2001) Analysis of toxic effects of Alternaria toxins on esophagus of mice by light and electron microscopy. Toxicol Pathol 29(4):492–497. CrossRefPubMedGoogle Scholar

Copyright information

© Deutsche Phytomedizinische Gesellschaft 2019

Authors and Affiliations

  1. 1.Key Laboratory of Forest Disaster Warning and Control of Yunnan ProvinceSouthwest Forestry UniversityKunmingPeople’s Republic of China
  2. 2.College of Chemical EngineeringSouthwest Forestry UniversityKunmingPeople’s Republic of China

Personalised recommendations