Vol. 62 No. 2 (2023): including 12th Special issue on Grapevine Trunk Diseases
Research papers - 12th Special Issue on Grapevine Trunk Diseases

Phenolic compounds inhibit viability and infectivity of the grapevine pathogens Diplodia seriata, Eutypa lata, Fomitiporia mediterranea, and Neofusicoccum parvum

Kateřina ŠTŮSKOVÁ
1Mendeleum – Institute of Genetics, Mendel University in Brno, Valtická 334, 691 44, Lednice, Czech Republic
Vincenzo MONDELLO
Unité Résistance Induite et Bioprotection des Plantes USC INRAE 1488, Université de Reims Champagne–Ardenne, Moulin de la Housse, Bâtiment 18, Reims, France
Eliška HAKALOVÁ
Mendeleum – Institute of Genetics, Mendel University in Brno, Valtická 334, 691 44, Lednice, Czech Republic
Dorota TEKIELSKA
Mendeleum – Institute of Genetics, Mendel University in Brno, Valtická 334, 691 44, Lednice, Czech Republic
Florence FONTAINE
Unité Résistance Induite et Bioprotection des Plantes USC INRAE 1488, Université de Reims Champagne–Ardenne, Moulin de la Housse, Bâtiment 18, Reims
Aleš EICHMEIER
Mendeleum – Institute of Genetics, Mendel University in Brno, Valtická 334, 691 44, Lednice, Czech Republic
Categories

Published 2023-09-15

Keywords

  • Grapevine trunk diseases,
  • thymol,
  • eugenol,
  • epigallocatechin-3-O-gallate,
  • mycelium growth,
  • spore germination,
  • wound protection
  • ...More
    Less

How to Cite

[1]
ŠTŮSKOVÁ K., V. MONDELLO, HAKALOVÁ E., D. TEKIELSKA, F. FONTAINE, and A. EICHMEIER, “Phenolic compounds inhibit viability and infectivity of the grapevine pathogens Diplodia seriata, Eutypa lata, Fomitiporia mediterranea, and Neofusicoccum parvum”, Phytopathol. Mediterr., vol. 62, no. 2, pp. 307–319, Sep. 2023.

Abstract

Many fungal pathogens are associated with grapevine trunk diseases (GTDs), which cause important yield and economic losses in grape production. There are no effective control methods against GTDs once plants are infected, so research is aimed at preventive measures to avoid infections in nurseries and vineyards. Inhibitory activities of the phenolic compounds eugenol, epigallocatechin–3–O–gallate (EGCG) and thymol against the GTD fungi Diplodia seriata, Eutypa lata, Fomitiporia mediterranea and Neofusicoccum parvum were assessed in vitro, and in planta as grapevine pruning wound treatments. Greatest inhibition of pathogen mycelium growth was observed with eugenol (fungistatic at 1,500 µg mL–1, fungicidal at 2,500 µg mL–1). No inhibitory activity against GTD fungi was observed with EGCG. Minimum concentrations with in vitro inhibitory effects on D. seriata and N. parvum spore germination were 360 µg mL–1 for thymol and 750 µg mL–1 for eugenol. In the grapevine wound protection tests, thymol was effective against N. parvum at 360 µg mL–1, but eugenol was not.

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References

  1. Abbaszadeh S., Sharifzadeh A., Shokri H., Khosravi A.R., Abbaszadeh A., 2014. Antifungal efficacy of thymol, carvacrol, eugenol and menthol as alternative agents to control the growth of food–relevant fungi. Journal de Mycologie Médicale 24(2): 51–56. DOI: 10.1016/j.mycmed.2014.01.063 DOI: https://doi.org/10.1016/j.mycmed.2014.01.063
  2. Abd–Elsalam K.A., Khokhlov A.R., 2015. Eugenol oil nanoemulsion: antifungal activity against Fusarium oxysporum f. sp. vasinfectum and phytotoxicity on cottonseeds. Applied Nanoscience 5(2): 255–265. DOI:10.1007/s13204–014–0398–y DOI: https://doi.org/10.1007/s13204-014-0398-y
  3. Amiri A., Dugas R., Pichot A., Bompeix G., 2008. In vitro and in vitro activity of eugenol oil (Eugenia caryophylata) against four important postharvest apple pathogens. International Journal of Food Microbiology 126(1-2): 13–19. DOI: 10.1016/j.ijfoodmicro.2008.04.022 DOI: https://doi.org/10.1016/j.ijfoodmicro.2008.04.022
  4. Baránek M., Pečenka J., Eichmeier A., 2017. Incidence symptomů a popis houbových patogenů spojených s onemocněním kmenů révy vinné v podmínkách České republiky. Vinařský obzor 110(10): 486–489. ISSN: 1212–7884
  5. Bartosikova L., Necas J., 2018. Epigallocatechin gallate: a review. Veterinární Medicína 63(10): 443–467. DOI: 10.17221/31/2018–VETMED DOI: https://doi.org/10.17221/31/2018-VETMED
  6. Bertsch C., Larignon P., Farine S., Clément C., Fontaine F., 2009. The Spread of Grapevine Trunk Disease. Science 324(5928): 721–721. DOI: 10.1126/science.324_721a DOI: https://doi.org/10.1126/science.324_721a
  7. Bruez E., Lecomte P., Grosman J., Doublet B., Bertsch …, Rey P., 2013. Overview of grapevine trunk diseases in France in the 2000s. Phytopathologia Mediterranea 52(2): 262–275. DOI: 10.14601/Phytopathol_Mediterr–11578
  8. Calland N., Albecka A., Belouzard S., Wychowski C., Duverlie …, Séron K., 2012. (−)–Epigallocatechin–3–gallate is a new inhibitor of hepatitis C virus entry. Hepatology 55(3): 720–729. DOI: 10.1002/hep.24803 DOI: https://doi.org/10.1002/hep.24803
  9. Chauhan K.R., Le T.C., Chintakunta P.K., Lakshman D.K., 2017. Phyto–Fungicides: Structure Activity Relationships of the Thymol Derivatives against Rhizoctonia solani. Journal of Agricultural Chemistry and Environment 06(04): 175–185. DOI: 10.4236/jacen.2017.64012 DOI: https://doi.org/10.4236/jacen.2017.64012
  10. Chen M., Zhai L., Arendrup M.C., 2015. In vitro activity of 23 tea extractions and epigallocatechin gallate against Candida species. Medical Mycology 53(2): 194–198. DOI: 10.1093/mmy/myu073 DOI: https://doi.org/10.1093/mmy/myu073
  11. Cobos R., Mateos R.M., Álvarez–Pérez J.M., Olego M.A., Sevillano S., …, Coque, J.J., 2015. Effectiveness of Natural Antifungal Compounds in Controlling Infection by Grapevine Trunk Disease Pathogens through Pruning Wounds. Applied and environmental microbiology 81(18): 6474–6483. DOI: 10.1128/AEM.01818–15 DOI: https://doi.org/10.1128/AEM.01818-15
  12. Compant S., Mathieu F., 2016. Biocontrol of major grapevine diseases: leading research. CABI, Boston, MA, USA. ISBN 978–1780647128. 240 pp. DOI: https://doi.org/10.1079/9781780647128.0000
  13. de la Rosa L.A., Moreno–Escamilla J.O., Rodrigo–García J., Alvarez–Parrilla, 2019. Phenolic Compounds. In: Postharvest Physiology and Biochemistry of Fruits and Vegetables. Woodhead Publishing, Sawston, United Kingdom, 253–271. ISBN 9780128132784. DOI: 10.1016/B978–0–12–813278–4.00012–9 DOI: https://doi.org/10.1016/B978-0-12-813278-4.00012-9
  14. Dable-Tupas G., Egbuna C., 2022. Role of Nutrigenomics in Modern-day Healthcare and Drug Discovery. 1st ed. Elsevier, Amsterdam, Netherlands, 596 pp.
  15. Ding J., Liu C., Huang P., Zhang Y., Hu X., ..., Qin, W., (2023). Effects of thymol concentration on postharvest diseases and quality of blueberry fruit. Food Chemistry 402: 134227. DOI: 10.1016/j.foodchem.2022.134227 DOI: https://doi.org/10.1016/j.foodchem.2022.134227
  16. European Union, European Parliament and the Council of the European Union (2009). Directive 2009/128/EC of the European Parliament and the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides (Text with EEA relevance). http://data.europa.eu/eli/dir/2009/128/oj
  17. Fischer J., Beckers S.J., Yiamsawas D., Thines E., Landfester K., Wurm F.R., 2019. Targeted Drug Delivery in Plants: Enzyme‐Responsive Lignin Nanocarriers for the Curative Treatment of the Worldwide Grapevine Trunk Disease Esca. Advanced Science 6(15). DOI:10.1002/advs.201802315 DOI: https://doi.org/10.1002/advs.201802315
  18. Fontaine F., Gramaje D., Armengol J., Smart R., Nagy Z.A., …, Corio–Costet M.F., 2016. Grapevine trunk diseases. A review. OIV Publications, 24 p., 979–10–91799–60–7. ⟨hal–01604038⟩
  19. Fussler L., Kobes N., Bertrand F., Maumy M., Grosman J., Savary S., 2008. A Characterization of Grapevine Trunk Diseases in France from Data Generated by the National Grapevine Wood Diseases Survey. Phytopathology 98(5): 571–579. DOI: 10.1094/PHYTO–98–5–0571 DOI: https://doi.org/10.1094/PHYTO-98-5-0571
  20. Gao T., Zhou H., Zhou W., Hu L., Chen J., Shi Z., 2016. The Fungicidal Activity of Thymol against Fusarium graminearum via Inducing Lipid Peroxidation and Disrupting Ergosterol Biosynthesis. Molecules 21(6). DOI: 10.3390/molecules21060770 DOI: https://doi.org/10.3390/molecules21060770
  21. Gramaje D., Úrbez–Torres J.R., Sosnowski M.R., 2018. Managing Grapevine Trunk Diseases with Respect to Etiology and Epidemiology: Current Strategies and Future Prospects. Plant Disease 102(1): 12–39. DOI: 10.1094/PDIS–04–17–0512–FE DOI: https://doi.org/10.1094/PDIS-04-17-0512-FE
  22. Hakalová E., Čechová J., Tekielska D.A., Eichmeier A., Pothier J.F., 2022. Combined effect of thyme and clove phenolic compounds on Xanthomonas campestris pv. campestris and biocontrol of black rot disease on cabbage seeds. Frontiers in Microbiology 13:1007988. DOI: 10.3389/fmicb.2022.1007988 DOI: https://doi.org/10.3389/fmicb.2022.1007988
  23. Hastoy X., Franc C., Riquier L., Ségur M.-C., de Revel G., Fermaud M., 2023. Fungitoxic role of endogenous eugenol in the hybrid grapevine cultivar Baco blanc resistant to Botrytis cinerea. OENO One 57(2): 159–175 DOI: 10.20870/oeno-one.2023.57.2.7454 DOI: https://doi.org/10.20870/oeno-one.2023.57.2.7454
  24. Hirasawa M., Takada K., 2004. Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans. Journal of Antimicrobial Chemotherapy 53(2): 225–229. DOI: 10.1093/jac/dkh046 DOI: https://doi.org/10.1093/jac/dkh046
  25. Hofstetter V., Buyck B., Croll D., Viret O., Couloux A., Gindro K., 2012. What if esca disease of grapevine were not a fungal disease? Fungal Diversity 54(1): 51–67. DOI: 10.1007/s13225–012–0171–z DOI: https://doi.org/10.1007/s13225-012-0171-z
  26. Jankura E., 2012 Soak treatment of grapevine propagation material against Petri disease. Agriculture (Poľnohospodárstvo)58 (1): 34–38. ISSN 1338–4376.
  27. Kaihatsu K., Yamabe M., Ebara Y., 2018. Antiviral Mechanism of Action of Epigallocatechin–3–O–gallate and Its Fatty Acid Esters. Molecules 23(10): DOI: 10.3390/molecules23102475 DOI: https://doi.org/10.3390/molecules23102475
  28. Kanagaratnam R., Sheikh R., Alharbi F., Kwon D.H.:2017. An efflux pump (MexAB–OprM) of Pseudomonas aeruginosa is associated with antibacterial activity of Epigallocatechin–3–gallate (EGCG). Phytomedicine 36: 194–200. DOI: 10.1016/j.phymed.2017.10.010 DOI: https://doi.org/10.1016/j.phymed.2017.10.010
  29. Kordali S., Cakir A., Ozer H., Cakmakci R., Kesdek M., Mete E., 2008. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p–cymene. Bioresource Technology 99(18): 8788–8795. DOI: 10.1016/j.biortech.2008.04.048 DOI: https://doi.org/10.1016/j.biortech.2008.04.048
  30. Larignon P., Fulchic R., Cere L., Dubos B.,2001. Observation on black dead arm in French vineyards. Phytopathologia Mediterranea 40: 336–342. DOI: 10.14601/Phytopathol_Mediterr–1629
  31. Lasorella V., Antonino N., Grande O., Guario A., 2018. Attivita estintiva nei confronti dei cleistoteci di Erysiphe necator con trattamenti autunnali a base di olio essenziale di arancio dolce. ATTI Giornate Fitopatologiche 2 : 389–394.
  32. Laveau C., Letouze A., Louvet G., Bastien S., Guérin–Dubrana L.,2009. Differential aggressiveness of fungi implicated in esca and associated diseases of grapevine in France. Phytopathologia Mediterranea 48: 32–46. DOI: 10.14601/Phytopathol_Mediterr–2873
  33. Lecomte P., Dewasme C., 2004. Lutte préventive contre les maladies du bois: premiers résultats de protection des plaies de taille par pulvérisation vis-à-vis de l’eutypiose. Progrès Agricole et Viticole 121: N°4.
  34. Lee S., Al Razqan G.S., Kwon D.H., 2017. Antibacterial activity of epigallocatechin–3–gallate (EGCG) and its synergism with β–lactam antibiotics sensitizing carbapenem–associated multidrug resistant clinical isolates of Acinetobacter baumannii. Phytomedicine 24: 49–55. DOI: 10.1016/j.phymed.2016.11.007 DOI: https://doi.org/10.1016/j.phymed.2016.11.007
  35. Li J., Fu S., Fan G., Li D., Yang S., …, Pan S., 2021. Active compound identification by screening 33 essential oil monomers against Botryosphaeria dothidea from postharvest kiwifruit and its potential action mode. Pesticide Biochemistry and Physiology 179: 104957. DOI: 10.1016/j.pestbp.2021.104957 DOI: https://doi.org/10.1016/j.pestbp.2021.104957
  36. Li X.C., Elsohly H., Nimrod A., Clark A., 1999. Antifungal Activity of (–)–Epigallocatechin Gallate from Coccoloba dugandiana. Planta Medica 65(08): 780–780. DOI: 10.1055/s–2006–960871 DOI: https://doi.org/10.1055/s-2006-960871
  37. Liu Y., Liu S., Luo X., Wu X., Ren J., ..., Dong P., 2022. Antifungal activity and mechanism of thymol against Fusarium oxysporum, a pathogen of potato dry rot, and its potential application. Postharvest Biology and Technology 192. DOI: 10.1016/j.postharvbio.2022.112025 DOI: https://doi.org/10.1016/j.postharvbio.2022.112025
  38. Matsumoto Y., Kaihatsu K., Nishino K., Ogawa M., Kato N., Yamaguchi A., 2012. Antibacterial and antifungal activities of new acylated derivatives of epigallocatechin gallate. Frontiers in Microbiology 16(3): 53. DOI: 10.3389/fmicb.2012.00053 DOI: https://doi.org/10.3389/fmicb.2012.00053
  39. Marchese A., Orhan I.E., Daglia M., Barbieri R., Di Lorenzo A., ..., Nabavi S.M., 2016. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chemistry 210: 402–414. DOI: 10.1016/j.foodchem.2016.04.111 DOI: https://doi.org/10.1016/j.foodchem.2016.04.111
  40. Mondello V., Larignon P., Armengol J., Kortekamp A., Vaczy K., …, Fontaine F., 2018a. Management of grapevine trunk diseases: Knowledge transfer, current strategies and innovative strategies adopted in Europe. Phytopathologia Mediterranea 57: 369–383. DOI: 10.14601/Phytopathol_Mediterr–23942
  41. Mondello V., Songy A., Battiston E., Pinto C., Coppin C., …, Fontaine F., 2018b. Grapevine Trunk Diseases: A Review of Fifteen Years of Trials for Their Control with Chemicals and Biocontrol Agents. Plant Disease 102(7): 1189–1217. DOI: 10.1094/PDIS–08–17–1181–FE DOI: https://doi.org/10.1094/PDIS-08-17-1181-FE
  42. Moretti S., Pacetti A., Pierron R., Kassemeyer H., Ficher M., …, Farine S., 2021. Fomitiporia mediterranea M. Fisch., the historical Esca agent: a comprehensive review on the main grapevine wood rot agent in Europe. Phytopathologia Mediterranea 60 (2): 351–379. DOI: 10.36253/phyto-13021 DOI: https://doi.org/10.36253/phyto-13021
  43. Müeller–Riebau F., Berger B., Yegen O., 1995. Chemical Composition and Fungitoxic Properties to Phytopathogenic Fungi of Essential Oils of Selected Aromatic Plants Growing Wild in Turkey. Journal of Agricultural and Food Chemistry 43(8): 2262–2266. DOI: 10.1021/jf00056a055 DOI: https://doi.org/10.1021/jf00056a055
  44. Nagle D.G., Ferreira D., Zhou Y.D., 2006. Epigallocatechin–3–gallate (EGCG): Chemical and biomedical perspectives. Phytochemistry 67(17): 1849–1855. DOI: 10.1016/j.phytochem.2006.06.020 DOI: https://doi.org/10.1016/j.phytochem.2006.06.020
  45. Navarro–Martinez M.D., García–Cánovas F., Rodríguez–López J.N., 2006. Tea polyphenol epigallocatechin–3–gallate inhibits ergosterol synthesis by disturbing folic acid metabolism in Candida albicans. Journal of Antimicrobial Chemotherapy 57(6): 1083–1092. DOI: 10.1093/jac/dkl124 DOI: https://doi.org/10.1093/jac/dkl124
  46. Numpaque M.A., Oviedo L.A., Gil J.H., García C.M., Durango D.L., 2011. Thymol and carvacrol: biotransformation and antifungal activity against the plant pathogenic fungi Colletotrichum acutatum and Botryodiplodia theobromae. Tropical Plant Pathology 36(1): 3–13. DOI: 10.1590/S1982–56762011000100001 DOI: https://doi.org/10.1590/S1982-56762011000100001
  47. Oh J.Y., Sajidah S., Volynchikova E., Kim Y.J., Han G.D., …, Kim K.D., 2022. Antifungal Activity of Thymol against Aspergillus awamori and Botrytis aclada Isolated from Stored Onion Bulbs. Mycobiology 50(6): 475–486. DOI: 10.1080/12298093.2022.2158557 DOI: https://doi.org/10.1080/12298093.2022.2158557
  48. Oxenham S.K., Svoboda K.P., Walters D.R., 2005. Eugenol reduces growth and increases activity of S–adenosylmethionine decarboxylase in the phytopathogenic fungus Botrytis fabae. Phytoparasitica 33(3): 247–252. DOI: 10.1007/BF02979862 DOI: https://doi.org/10.1007/BF02979862
  49. Park B.J., Park J.C., Taguchi H., Fukushima K., Hyon S.H., Takatori K., 2006. Antifungal susceptibility of epigallocatechin 3–O–gallate (EGCG) on clinical isolates of pathogenic yeasts. Biochemical and Biophysical Research Communications 347(2): 401–405. DOI: 10.1016/j.bbrc.2006.06.037 DOI: https://doi.org/10.1016/j.bbrc.2006.06.037
  50. Péros J.P., Berger, G., 1994. A rapid method to assess the aggressiveness of Eutypa lata isolates and the susceptibility of grapevine cultivars to Eutypa dieback. Agronomie 14(8): 515–523. DOI: 10.1051/agro:19940804 DOI: https://doi.org/10.1051/agro:19940804
  51. Pramod K., Ansari S.H., Ali, J., 2010. Eugenol: A Natural Compound with Versatile Pharmacological Actions. Natural Product Communications 5(12). DOI: 10.1177/1934578X1000501236 DOI: https://doi.org/10.1177/1934578X1000501236
  52. Raveau R., Fontaine J., Lounès-Hadj Sahraoui A., 2020. Essential Oils as Potential Alternative Biocontrol Products against Plant Pathogens and Weeds: A Review. Foods 9(3). DOI: 10.3390/foods9030365 DOI: https://doi.org/10.3390/foods9030365
  53. Rego C., Nascimento T., Cabral A., Silva M.J., Oliveira H., 2009. Control of grapevine wood fungi in commercial nurseries. Phytopathologia Mediterranea 48. DOI: 10.14601/Phytopathol_Mediterr–2881
  54. Reis P., Magnin–Robert M., Nascimento T., Spagnolo A., Abou–Mansour E., … Fontaine F., 2016. Reproducing Botryosphaeria Dieback Foliar Symptoms in a Simple Model System. Plant Disease 100(6): 1071–1079. DOI: 10.1094/PDIS–10–15–1194–RE DOI: https://doi.org/10.1094/PDIS-10-15-1194-RE
  55. Robert–Siegwald G., Vallet J., Abou–Mansour E., Xu J., Rey P., …, Lebrun, M.H., 2017. Draft Genome Sequence of Diplodia seriata F98.1, a Fungal Species Involved in Grapevine Trunk Diseases. Genome Announcements 5(14): e00061–17. DOI: 10.1128/genomeA.00061–17 DOI: https://doi.org/10.1128/genomeA.00061-17
  56. Scoralik M.G., Daemon E., De Oliveira Monteiro C.M., Maturano R., 2012. Enhancing the acaricide effect of thymol on larvae of the cattle tick Rhipicephalus microplus (Acari: Ixodidae) by solubilization in ethanol. Parasitology Research 110(2): 645–648. DOI: 10.1007/s00436–011–2539–5 DOI: https://doi.org/10.1007/s00436-011-2539-5
  57. Songy A., Fernandez O., Clément C., Larignon P., Fontaine F., 2019. Grapevine trunk diseases under thermal and water stresses. Planta 249: 1655–1679. DOI:10.1007/s00425-019-03111-8 DOI: https://doi.org/10.1007/s00425-019-03111-8
  58. Steinmann J., Buer J., Pietschmann T., Steinmann E., 2013. Anti–infective properties of epigallocatechin–3–gallate (EGCG), a component of green tea. British Journal of Pharmacology 168(5): 1059–1073. DOI: 10.1111/bph.12009 DOI: https://doi.org/10.1111/bph.12009
  59. Torre A.L., Mandalà C., Pezza L., Caradonia F., Battaglia V., 2014. Evaluation of essential plant oils for the control of Plasmopara viticola. Journal of Essential Oil Research 26(4): 282–291. DOI: 10.1080/10412905.2014.889049 DOI: https://doi.org/10.1080/10412905.2014.889049
  60. Úrbez–Torres J.R., Gubler W.D., 2009. Pathogenicity of Botryosphaeriaceae species isolated from grapevine cankers in California. Plant Disease 93(6): 584–592. DOI: 10.1094/PDIS-93-6-0584 DOI: https://doi.org/10.1094/PDIS-93-6-0584
  61. Úrbez–Torres J.R., 2011. The status of Botryosphaeriaceae species infecting grapevines. Phytopathologia Mediterranea 50: 5–45. DOI: 10.14601/Phytopathol_Mediterr–9316
  62. Wang C., Zhang J., Chen H., Fan Y., Shi Z., 2010. Antifungal activity of eugenol against Botrytis cinerea. Tropical Plant Pathology 35(3). DOI: 10.1590/S1982–56762010000300001 DOI: https://doi.org/10.1590/S1982-56762010000300001
  63. Zhang J., Ma S., Du S., Chen S., Sun H., 2019. Antifungal activity of thymol and carvacrol against postharvest pathogens Botrytis cinerea. Journal of Food Science and Technology 56(5): 2611–2620. DOI: 10.1007/s13197–019–03747–0 DOI: https://doi.org/10.1007/s13197-019-03747-0
  64. Zhao Y., Wang Q., Wu X., Jiang M., Jin H., Tao K., Hou T.: 2021. Unravelling the polypharmacology of a natural antifungal product, eugenol, against Rhizoctonia solani. Pest Management Science 77(7): 3469–3483. DOI: 10.1002/ps.6400 DOI: https://doi.org/10.1002/ps.6400
  65. Živković, S., Vasić T., Trkulja V., Krnjaja V., and Marković J., 2012. Pathogenicity on grapevine and sporulation of E. lata isolates originating from Serbia. Romanian Biotechnological Letters, Vol. 17 (3), 7379- 7388.