Articles
In vitro evaluation of grapevine endophytes, epiphytes and sap micro-organisms for potential use to control grapevine trunk disease pathogens
Published 2021-12-30
Keywords
- Biological control,
- endophytes,
- microbial antagonism,
- antifungal
How to Cite
[1]
R. Blundell, M. . Arreguin, and A. Eskalen, “In vitro evaluation of grapevine endophytes, epiphytes and sap micro-organisms for potential use to control grapevine trunk disease pathogens”, Phytopathol. Mediterr., vol. 60, no. 3, pp. 535–548, Dec. 2021.
Abstract
Grapevine trunk diseases (GTDs) threaten the economic sustainability of viticulture, causing reductions of yield and quality of grapes. Biological control is a promising sustainable alternative to cultural and chemical methods to mitigate the effects of pathogens causing GTDs, including Botryosphaeria dieback, Eutypa dieback and Esca. This study aimed to identify naturally occurring potential biological control agents from grapevine sap, cane and pith tissues, and evaluate their in vitro antagonistic activity against selected fungal GTD pathogens. Bacterial and fungal isolates were preliminarily screened in dual culture assays to determine their antifungal activity against Neofusicoccum parvum and Eutypa lata. Among the fungal isolates, Trichoderma spp. inhibited mycelium growth of E. lata by up to 64% and of N. parvum by up to 73%, with overgrowth and growth cessation being the likely antagonistic mechanisms. Among the bacterial isolates, Bacillus spp. inhibited mycelium growth of E. lata by up to 20% and of N. parvum by up to 40%. Selected antagonistic isolates of Trichoderma, Bacillus and Aureobasidium spp. were subjected to further dual culture antifungal analyses against Diplodia seriata and Diaporthe ampelina, with Trichoderma isolates consistently causing the greatest inhibition. Volatile organic compound antifungal analyses showed that these Trichoderma isolates inhibited mycelium growth of N. parvum (20% inhibition), E. lata (61% inhibition) and Dia. ampelina (71% inhibition). Multilocus sequence analyses revealed that the Trichoderma isolates were most closely related to Trichoderma asperellum and Trichoderma hamatum. This study had identified grapevine sap as a novel source of potential biological control agents for control of GTDs. Further testing will be necessary to fully characterize modes of antagonism of these microorganisms, and assess their efficacy for pruning wound protection in planta.
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References
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Cawoy H., Bettiol W., Fickers P., Ongena M., 2011. Bacillus‐based biological control of plant diseases, pesticides in the modern world. In: Pesticides in the Modern World-Pesticides Use and Management (Stoytcheva, M, ed.), Intech: 273-283.
Chambers, S., Scott E., 1995. In vitro antagonism of Phytophthora cinnamomi and P. citricola by Trichoderma species and Gliocladium virens. Journal of Phytopathology 143: 471–477.
Choudray D. K., Johri B. N., 2009. Interactions of Bacillus spp. and plants – With special reference to induced systemic resistance (ISR). Microbiological Research 164: 593–513.
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Halleen, F., Fourie, P. H., Lombard, P. J., 2010. Protection of grapevine pruning wounds against Eutypa lata by biological and chemical methods. South African Journal for Enology and Viticulture 31: 125–132.
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Idris, H. A., Labuschagne, N., Korsten, L., 2007. Screening rhizobacteria for biological control of Fusarium root and crown rot of sorghum in Ethiopia. Biological Control 40: 97–106.
Kotze, C., Van Niekerk, J., Mostert, L., Halleen, F., Fourie, P., 2011. Evaluation of biocontrol agents for grapevine pruning wound protection against trunk pathogen infection. Phytopathologia Mediterranea 50: 247–263.
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John, S., Wicks, T. J., Hunt, J., Lorimer, M., Oakey, H., Scott, E. S., 2005. Protection of grapevine pruning wounds from infection by Eutypa lata using Trichoderma harzianum and Fusarium lateritium. Australasian Plant Pathology 34: 569.
John, S., Wicks, T. J., Hunt, J. S., Scott, E. S., 2008. Colonisation of grapevine wood by Trichoderma harzianum and Eutypa lata. Australian Journal of Grape and Wine Research 14: 18–24.
Kaplan, J., Travadon., R., Cooper, M., Hilis, V., Lubell, M., Baumgartner, K., 2016. Identifying economic hurdles to early adoption of preventative practices: The case of trunk diseases in California winegrape vineyards. Wine Economics and Policy 5: 127–141.
Kexiang, G., Xiaoguang, L., Yonghong, L., Tianbo, Z., Shuliang, W., 2002. Potential of Trichoderma harzianum and T. atroviride to control Botryosphaeria berengeriana f. sp. piricola, the cause of apple ring rot. Journal of Phytopathology 150: 271–276.
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Billones-Baaijens R., Jones E. E., Ridgway H. J., Jaspers M. V., 2013. Virulence Affected by Assay Parameters during Grapevine Pathogenicity Studies with Botryosphaeriaceae Nursery Isolates. Plant Pathology 62: 1214–25.
Bruisson, S., Zufferey, M., L'haridon, F., Trutmann, E., Anand, A., Dutartre, A., De Vrieze, Am., Weisskopf, L., 2019. Endophytes and Epiphytes From the Grapevine Leaf Microbiome as Potential Biocontrol Agents Against Phytopathogens. Frontiers in Microbiology 10: 1-17.
Carbone I., Kohn L. M., 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556.
Cawoy H., Bettiol W., Fickers P., Ongena M., 2011. Bacillus‐based biological control of plant diseases, pesticides in the modern world. In: Pesticides in the Modern World-Pesticides Use and Management (Stoytcheva, M, ed.), Intech: 273-283.
Chambers, S., Scott E., 1995. In vitro antagonism of Phytophthora cinnamomi and P. citricola by Trichoderma species and Gliocladium virens. Journal of Phytopathology 143: 471–477.
Choudray D. K., Johri B. N., 2009. Interactions of Bacillus spp. and plants – With special reference to induced systemic resistance (ISR). Microbiological Research 164: 593–513.
Claydon, N., Allan, M.; Hanson, J. R. , Avent, A. G., 1987. Antifungal alkyl pyrones of Trichoderma harzianum. Transactions of the British Mycological Society 88: 503–513.
Deyett, E., Rolshausen, P. E., Temporal Dynamics of the Sap Microbiome of Grapevine Under High Pierce’s Disease Pressure. 2019. Frontiers in Plant Science 10: 1-15.
Di Marco, S., Osti, F. , Roberti, R., Calzarano, F., Cesari, A., 2002. Attivita` di specie di Trichoderma nei confronti di Phaeomoniella chlamydospora, patogeno associato al mal delll’esca della vite. Atti Giornate Fitopatologiche 419–424.
Di Marco, S., Osti, F., Cesari, A., 2004. Experiments on the control of esca by Trichoderma. Phytopathologia Mediterranea. 43: 108–115.
Dos Reis Almeida, F. B., Cerqueria, F. M., do Nascimento Silva, R., Ulhoa, C. J., Lima, A. L., 2007. Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani: evaluation of coiling and hydrolytic enzyme production. Biotechnology Letters 29: 1189–1193.
Ferreira, J. H. S., Matthee, F. N., Thomas, A. C., 1991. Biological Control of Eutypa lata on Grapevine by an Antagonistic Strain of Bacillus subtilis. Ecology and Epidemiology 81: 283–287.
Gilbert, J. A., Van der Lelie, D., Zarraonaindia, I., 2014. Microbial terroir for wine grapes. PNAS 111: 5–6.
Glass, N. L., Donaldson, G. C., 1995. Development of Primer Sets Designed for Use with the PCR To Amplify Conserved Genes from Filamentous Ascomycetes. Applied and Environmental Microbiology 61: 1323–1330.
Gotor-Vila, A., Teixado, N., Di Francesco, A., Usall, J., Ugolini, L., Torres, R., Mari, M., 2017. Antifungal effect of volatile organic compounds produced by Bacillus amyloliquefaciens CPA-8 against fruit pathogen decays of cherry. Food Microbiology 64: 219–225.
Gramaje, D., Armengol, J., 2011. Fungal Trunk Pathogens in the Grapevine Propagation Process: Potential Inoculum Sources, Detection, Identification, and Management Strategies. Plant Disease 95: 1040–1055.
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: 12–39.
Grube, M., Schmid, F., Berg, G., 2011 Black fungi and associated bacterial communities in the phyllosphere of grapevine. Fungal Biology 115: 978–986.
Gubler, W. D., Rolshausen, P. E., Trouillas, F. P., Urbez Torres, J. R., Voegel, T., 2005. Grapevine trunk diseases in California. Practical Winery and Vineyard. 2005.
Haidar, R., Deschamps, A., Roudet, J., Calvo-Garrido, C., Bruez, E., Rey, P., Fermaud, M., 2016. Multi-organ screening of efficient bacterial control agents against two major pathogens of grapevine. Biological Control 92: 55–65.
Halleen, F.; Crous, P.; Petrini, O. 2003. Fungi associated with healthy grapevine cuttings in nurseries, with special reference to pathogens involved in the decline of young vines. Australasian Plant Pathology 32: 47–52.
Halleen, F., Fourie, P. H., Lombard, P. J., 2010. Protection of grapevine pruning wounds against Eutypa lata by biological and chemical methods. South African Journal for Enology and Viticulture 31: 125–132.
Hardoim, P. R., Can Overbeek, L. S., Berg, G., Pirttila, A. M., Compant, S., Campisano, A., Doring, M., Sessitsch, A., 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular. Biology Reviews 79: 293–320.
Harman, G. E., 2006. Overview of Mechanisms and Uses of Trichoderma spp. Phytopathology 96: 190–194.
Heimpel, G. E., Mills, N., 2017. Biological Control - Ecology and Applications. Cambridge University Press, Cambridge, UK, 1 pp.
Idris, H. A., Labuschagne, N., Korsten, L., 2007. Screening rhizobacteria for biological control of Fusarium root and crown rot of sorghum in Ethiopia. Biological Control 40: 97–106.
Kotze, C., Van Niekerk, J., Mostert, L., Halleen, F., Fourie, P., 2011. Evaluation of biocontrol agents for grapevine pruning wound protection against trunk pathogen infection. Phytopathologia Mediterranea 50: 247–263.
John, S., Scott, E., Wicks, T. J., Hunt, J., 2004 Interactions between Eutypa lata and Trichoderma harzianum. Phytopathologia Mediterranea 43: 95–104.
John, S., Wicks, T. J., Hunt, J., Lorimer, M., Oakey, H., Scott, E. S., 2005. Protection of grapevine pruning wounds from infection by Eutypa lata using Trichoderma harzianum and Fusarium lateritium. Australasian Plant Pathology 34: 569.
John, S., Wicks, T. J., Hunt, J. S., Scott, E. S., 2008. Colonisation of grapevine wood by Trichoderma harzianum and Eutypa lata. Australian Journal of Grape and Wine Research 14: 18–24.
Kaplan, J., Travadon., R., Cooper, M., Hilis, V., Lubell, M., Baumgartner, K., 2016. Identifying economic hurdles to early adoption of preventative practices: The case of trunk diseases in California winegrape vineyards. Wine Economics and Policy 5: 127–141.
Kexiang, G., Xiaoguang, L., Yonghong, L., Tianbo, Z., Shuliang, W., 2002. Potential of Trichoderma harzianum and T. atroviride to control Botryosphaeria berengeriana f. sp. piricola, the cause of apple ring rot. Journal of Phytopathology 150: 271–276.
Kotze, C., 2019. Biological control of the grapevine trunk disease pathogens: pruning wound protection. MSc. thesis, Stellenbosch University, Stellenbosch, South Africa, 2008, SUNScholar Research Repositary, https://scholar.sun.ac.za/handle/10019.1/2117, (accessed on 13th October 2019).
Kucuk, C., Kivanc, M., 2004. In Vitro Antifungal Activity of Strains of Trichoderma harzianum. Turkish Journal of Biology 28: 111–115.
Lu, J. J., Perng, C. L., Lee, S. Y., Wan, C. C., 2000. Use of PCR with Universal Primers and Restriction Endonuclease Digestions for Detection and Identification of Common Bacterial Pathogens in Cerebrospinal Fluid. Journal of Clinical Microbiology 38: 2076–2080.
Luque, J., Elena, G., Garcia-Figueres, F., Reyes, J., Barrios, G., Legorburu, F.J., 2014. Natural infections of pruning wounds by fungal trunk pathogens in mature grapevines in Catalonia (Northeast Spain). Australian Journal of Grape and Wine Research 20: 134–143.
Martinez-Diz, M. D. P., Diaz-Losada, E., Andres-Sodupe, M., Bujanda, R., Maldonadao-Gonzalez, M. M., Ojeda, S., Yacoub, A., Rey, P., Gramaje, D., 2020. Field evaluation of biocontrol agents against black-foot and Petri diseases of grapevine. Pest Management. Science.
Martini, M., Musetti, R., Grisan, R., Polizzotto, R., Borselli, S., Pavan, F., Osler, R., 2009. DNA-dependent detection of the grapevine fungal endophytes Aureobasidium pullulans and Epicoccum nigrum. Plant Disease 93: 993–998.
Mondello, V., Songy, A., Battison, E., Pinto, C., Coppin, C., Trotel-Aziz, P., Clement, C., Mugnai, L., Fontaine, F., 2018. Grapevine Trunk Diseseases: A Review of Fifteen Years of Trials for Their Control with Chemicals and Biocontrol Agents. Plant Disease 102: 1189–1217.
Mukherjee, P. K., Horwitz, B. A., Herrera-Estrella, A., Schmoll, M., Kenerley, C. M., 2013. Trichoderma Research in the Genome Era. Annual. Review of Phytopathology 51: 105–129.
Mugnai, L., Graniti, A., Surico, G., 1999. Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease 83: 404–418.
Munkvold, G., Duthie, J., Marois, J., 1994. Reductions in yield and vegetative growth of grapevines due to Euytpa dieback. Phytopathology 84: 186–192.
Mutawila, C., Halleen, F., Mostert, L., 2015. Development of benzimidazole resistant Trichoderma strains for the integration of chemical and biocontrol methods of grapevine pruning wound protection. BioControl 60: 387–399.
Otoguro, M., Suzuki, S., 2018. Status and future of disease protection and grape berry quality alteration by micro-organisms in viticulture. Letters in Applied Microbiology 67: 106–112.
Pascoe, I., Cottral, E., 2000. Developments in grapevine trunk diseases research in Australia. Phytopathologia Mediterranea 39: 68–75.
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