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Effect of Rosemary Essential Oil and Trichoderma koningiopsis T-403 VOCs on Pathogenic Fungi Responsible for Ginseng Root Rot Disease

  • Hussein, Khalid Abdallah (Soil Biochemistry Lab, Department of Biological Environment, Kangwon National University) ;
  • Lee, Young-Don (Soil Biochemistry Lab, Department of Biological Environment, Kangwon National University) ;
  • Joo, Jin Ho (Soil Biochemistry Lab, Department of Biological Environment, Kangwon National University)
  • Received : 2020.02.11
  • Accepted : 2020.04.06
  • Published : 2020.07.28

Abstract

Rosemary essential oil was evaluated for antifungal potentiality against six major ginseng pathogens: Sclerotinia sclerotiorum, Sclerotinia nivalis, Cylindrocarpon destructans, Alternaria panax, Botrytis cinerea, and Fusarium oxysporum. The in vitro fungicidal effects of two commonly used fungicides, namely mancozeb and fenhexamid, and the volatile organic compounds (VOCs) of Trichoderma koningiopsis T-403 on the mycelial growth were investigated. The results showed that rosemary essential oil is active against all of the pathogenic strains of ginseng root rot, whereas rosemary oil displayed high ability to inhibit the Sclerotinia spp. growth. The highest sensitivity was S. nivalis, with complete inhibition of growth at 0.1% v/v of rosemary oil, followed by Alternaria panax, which exhibited 100% inhibition at 0.3% v/v of the oil. Minimum inhibitory concentrations (MICs) of rosemary oil ranged from 0.1 % to 0.5 % (v/v). Chemical analysis using GC-MS showed the presence of thirty-two constituents within rosemary oil from R. officinals L. Camphore type is the most frequent sesquiterpene in rosemary oil composition. Mancozeb and fenhexamid showed their highest inhibition effect (45% and 30%, respectively) against A. panax. T. koningiopsis T-403 showed its highest inhibition effect (84%) against C. destructans isolate. This study may expedite the application of antifungal natural substances from rosemary and Trichoderma in the prevention and control of phytopathogenic strains in ginseng root infections.

Keywords

References

  1. Randall JA, Cook J. 2013. American Ginseng in Iowa: Producing IOWA STATE UNIVERSITY F-401 Forestry Extension Ames, Iowa Series on Ginseng. F -400, F401, F402, & F403.
  2. Davis JW, Persons S. 2014. Growing and marketing ginseng, goldenseal and other woodland medicinals. Printed in Canada. First printing June 2014.
  3. Tawaha, K, Alali FQ, Gharaibeh M, Mohammad M, El-Elimat T. 2007. Antioxidant activity and total phenolic content of selected Jordanian plant species. Food Chem. 104: 1372- 1378. https://doi.org/10.1016/j.foodchem.2007.01.064
  4. Moreira MR, Ponce AG, dell Valle CE, Roura SI. 2005. Inhibitory parameters of essential oils to reduce a foodborne pathogen. LWT 38: 565-570. https://doi.org/10.1016/j.lwt.2004.07.012
  5. Peng Y, Yuan J, Liu F, Ye J. 2005. Determination of active components in rosemary by capillary electrophoresis with electrochemical detection. J. Pharm. Biomed. Anal. 39: 431-437. https://doi.org/10.1016/j.jpba.2005.03.033
  6. Hyldgaard M, Mygind T, Meyer RL. 2012. Essential oils in food preservation: mode of action, synergies and interactions with food matrix components. Front. Microbiol. 3: 12. https://doi.org/10.3389/fmicb.2012.00012
  7. Cardile V, Russo A, Formisano C, Rigano D, Senatore F. 2009. Essential oils of Salvia bracteata and Salvia rubifolia from Lebanon: Chemical composition, antimicrobial activity and inhibitory effect on human melanoma cells. J. Ethnopharmacol. 126: 265-272. https://doi.org/10.1016/j.jep.2009.08.034
  8. Oussalah M, Caillet S, Saucier L, Lacroix M. 2007. Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 18: 414-420. https://doi.org/10.1016/j.foodcont.2005.11.009
  9. Silva F, Ferreira S. Duarte A, Mendonca, 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: 42-47. https://doi.org/10.1016/j.phymed.2011.06.033
  10. Schnitzler P, Astani A, Reichling J. 2011. Screening for antiviral activities of isolated compounds from essential oils. 253643 J. Evid. Based Complement. Alternat. Med. 25: 36-43.
  11. Bertoli A, Cirak C, Teixeira da Silva JA. 2010. Hypericum species as sources of valuable essential oils. Med. Arom. Plant Sci. Biotechnol. 5: 29-47.
  12. Tian J, Ban X, Zeng H, He J, Chen Y. 2012. The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS One 7: e30147. https://doi.org/10.1371/journal.pone.0030147
  13. Habtemariam S. 2016. The therapeutic potential of rosemary (Rosmarinus officinalis) diterpenes for Alzheimer's disease. J. Evid. Based Complement. Alternat. Med. Article 2016: 2680409.
  14. Estevez M, Ramirez R, Ventanas S Cava R. 2007. Sage and rosemary essential oils versus BHT for the inhibition of lipid oxidative reactions in liver pate. LWT Food Sci. Technol. 40: 58-65. https://doi.org/10.1016/j.lwt.2005.07.010
  15. Valgimigli L. 2012. Essential Oils as Natural Food Additives: Composition, Applications, Antioxidant and Antimicrobial Properties, Nova Science Publishers, New York, NY, USA,
  16. Issabeagloo E, Kermanizadeh P, Taghizadieh M, Forughi R. 2012. Antimicrobial effects of rosemary (Rosmarinus officinalis L.) essential oils against Staphylococcus spp. Afr. J. Microbiol. Res. 6: 5039-5042.
  17. Ojeda-Sana AM, van Baren CM, Elechosa M, Ju'arez AMA, Moreno S. 2013. New insights into antibacterial and antioxidant activities of rosemary essential oils and their main components. Food Control 31: 189-195. https://doi.org/10.1016/j.foodcont.2012.09.022
  18. Zaouali Y, Bouzaine T, Boussaid M. 2010. Essential oils composition in two Rosmarinus officinalis L. varieties and incidence for antimicrobial and antioxidant activities. Food Chem. Toxicol. 48: 3144-3152. https://doi.org/10.1016/j.fct.2010.08.010
  19. Piechulla B, Degenhardt J. 2014. The emerging importance of microbial volatile organic compounds. Plant Cell Environ. 37: 811-812. https://doi.org/10.1111/pce.12254
  20. Campos VP, Pinho RSC, de Freire ES. 2010. Volatiles produced by interacting microorganisms potentially useful for the control of plant pathogens. Cienciae Agrotec Lavras 34: 525-535. https://doi.org/10.1590/S1413-70542010000300001
  21. Cortes-Barco AM, Goodwin PH, Hsiang T. 2010. Comparison of induced resistance activated by benzothiadiazole, (2R, 3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol. 59: 643-653. https://doi.org/10.1111/j.1365-3059.2010.02283.x
  22. Lee S, Hung R, Yap M, Bennett JW. 2015. Age matters: the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth. Arch. Microbiol. 197: 723-727. https://doi.org/10.1007/s00203-015-1104-5
  23. Domsch KH, Gams W, Anderson T. 1980. Compendium of soil fungi. Academic Press. London 1-2: 405-859.
  24. Moubasher AH. 1993. Soil fungi in Qatar and other Arab countries. The Centre of Scientific and Applied Research University of Qater, Doha, Qater.
  25. Jiang L. 2011. Comparison of disk diffusion, agar dilution, and broth microdilution for antimicrobial susceptibility testing of five chitosans. PhD diss. 2011; Louisiana State University.
  26. Ben Kaab S, Rebey IB, Hanafi M, Berhal C, Fauconnier ML, De Clerck C, et al. 2019. Rosmarinus officinalis essential oil as an effective antifungal and herbicidal agent. Spanish J. Agr. Res. 17: e1006. https://doi.org/10.5424/sjar/2019172-14043
  27. Messgo-Moumene S, LiY, Bachir K, Houmani Z, Bouznad Z, Chemat F. 2015. Antifungal power of citrus essential oils against potato late blight causative agent. J. Essen. Oil Res. 27: 169-176. https://doi.org/10.1080/10412905.2014.982877
  28. Dennis C, Webster J. 1971. Antagonistic properties of species-groups of Trichoderma: iii. hyphal interaction. Trans. Br. Mycol. Soc. 57: 363-369. https://doi.org/10.1016/S0007-1536(71)80050-5
  29. SAS Institute. 2011. The SAS 10.2 software. Statistical Analysis System for Windows [Softaware]. Cary, N.C.: SAS.
  30. Punja ZK, Wan A, Goswami RS. 2008. Growth, pathogenicity and infection behaviour, and genetic diversity of Rhexocercosporidium panicis isolates from ginseng roots in British Columbia. Canadian J. Plant Pathol. 35: 503-513. https://doi.org/10.1080/07060661.2013.843315
  31. Shin J, Fu T, Park K H, Kim KS. 2017. The effect of fungicides on mycelial growth and conidial germination of the ginseng root rot fungus, Cylindrocarpon destructans. Mycobiology 45: 220-225. https://doi.org/10.5941/MYCO.2017.45.3.220
  32. Billard A, Fillinger S, Leroux P, Bach J, Lanen C, Lachaise H, Beffa R, Debieu D. 2011. Fenhexamid resistance in the Botrytis species complex, responsible for grey mould disease N. Thajuddin (Ed.), pp. 61-78. Fungicides-Beneficial and Harmful Aspects, InTech Publisher, Rijeka, Croatia.
  33. Gullino ML, Tinivella F, Garibaldi A, Kemmitt GM, Bacci L, Sheppard B. 2010. Mancozeb: past, present, and future. Plant Dis. 94: 1076-1087. https://doi.org/10.1094/PDIS-94-9-1076
  34. Jose LHS, Oliver SV, Paula AC. 2011. Sensitivity of Venturia inaequalis chilean isolates to difenoconazole, fenarimol, mancozeb, and pyrimethanil. Chil. J. Agr. Res. 71: 39-44. https://doi.org/10.4067/S0718-58392011000100005
  35. Hwang E, Cash J, Zabik M. 2001 Postharvest treatments for the reduction of mancozeb in fresh apples. J. Agr. Food Chem. 49: 3127-3132. https://doi.org/10.1021/jf010234h
  36. Buck JW. 2004. Combinations of fungicides with phylloplane yeasts for improved control of Botrytis cinerea on geranium seedlings. Phytopathology 94: 196-202. https://doi.org/10.1094/PHYTO.2004.94.2.196
  37. Walker AS, Gautier A, Confais C, Martinho D, Viaud M, Le Pêcheur P, et al. 2011. Botrytis pseudocinerea, a new cryptic species causing grey mould in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101:1433-1445. https://doi.org/10.1094/PHYTO-04-11-0104
  38. Szabo M, Csepregi K, Galber M, Fekete C. 2012. Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: the role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biol. Control 63: 121-128. https://doi.org/10.1016/j.biocontrol.2012.06.013
  39. Howell CR. 1998. The role of antibiosis in biocontrol. In: Harman GE, Kubicek CP, editors. Trichoderma and Gliocladium London: Taylor and Francis 2: 173-184.
  40. Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, et al. 2012. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 3: 108. https://doi.org/10.3389/fpls.2012.00108
  41. Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez- Bucio J. 2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 149: 1579-1592. https://doi.org/10.1104/pp.108.130369
  42. Lee S, Yap M, Behringer G, Hung R, Bennett JW. 2016. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol. Biotechnol. 3: 7. https://doi.org/10.1186/s40694-016-0025-7
  43. Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L. 2009. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J. Med. Microbiol. 58: 1454-1462. https://doi.org/10.1099/jmm.0.010538-0
  44. Sirocchi V, Caprioli G, Cecchini C, Coman MM. Cresci A, Maggi F, et al. 2013. Biogenic amines as freshness index of meat wrapped in a new active packaging system formulated with essential oils of Rosmarinus officinalis. Inter. J. Food Nutr. Sci. 64: 921-928. https://doi.org/10.3109/09637486.2013.809706
  45. Sanchez-Gonzalez L, Chafer M, Hernandez MA, Chiralt C, Gonzalez-Martinez. 2011. Antimicrobial activity of polysaccharide films containing essential oils. Food Control 22: 1302-1310. https://doi.org/10.1016/j.foodcont.2011.02.004
  46. Atti-Santos AC, Rossato M, Pauletti GF, Rota LD, Rech JC, Marcia Regina F, Atti L, Moyna P. 2005. Physico-chemical Evaluation of Rosmarinus officinalis L. Essential Oils 48: 1035-1039, ISSN 1516-8913 Printed in Brazil.
  47. Baser KHC, Buchbauer G. 2010. Handbook of Essential Oils: Science, Technology and Applications. CRC Press, Boca Raton, London, New York, ISBN: 978-1-4200-6315-8.
  48. Bai J, Baldwin EA, Imahori Y, Kostenyuk I, Burns J, Brecht JK. 2011. Chilling and heating may regulate C6 volatile aroma production by different mechanisms in tomato (Solanum lycopersicum) fruit. Postharvest Biol. Technol. 60: 111-120. https://doi.org/10.1016/j.postharvbio.2010.12.002
  49. Elaissi A, Rouis Z, Mabrouk S, Harzallah-Skhiri F. 2012. Correlation between chemical composition and antibacterial activity of essential oils from fifteen Eucalyptus species growing in the Korbous and Jbel Abderrahman Arboreta (North East Tunisia). Molecules 17: 3044-3057. https://doi.org/10.3390/molecules17033044
  50. Fu Y, Zu Y, Chen L, Shi X, Wang Z, Sun S, Efferth T. 2007. Antimicrobial activity of clove and rosemary essential oils alone and in combination. Phytother. Res. 21: 989-994. https://doi.org/10.1002/ptr.2179
  51. Sienkiewicz M, Lysakowska M, Pastuszka M, Bienias W, Kowalczyk E. 2013. The potential of use basil and rosemary essential oils as effective antibacterial agents. Molecules 18: 9334-9351. https://doi.org/10.3390/molecules18089334

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