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Exploring the microbial communities associated with Botrytis cinerea during berry development in table grape with emphasis on potential biocontrol yeasts

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Abstract

Table grapes harbour a wide diversity of microbes, some of which are potential biocontrol agents that may be responsible for the control of fungal pathogens in the phyllosphere. This study evaluated the diversity of microbial communities associated with naturally present Botrytis cinerea inoculum, with special emphasis on populations of potential biocontrol yeasts during berry development in table grapes. Samples were collected from two agro-ecological habitats in South Africa (Northern Province), characterised by low rainfall (site A) and high rainfall (site B). The phenological development samples included those at full bloom, pea size and mature berry stages. Within the group of yeasts known to be natural antagonists, Aureobasidium, Cryptococcus, Rhodotorula and Sporobolomyces could be cultured, while pathogenic fungal genera from asymptomatic samples included Cladosporium, Alternaria, and Aspergillus. Botrytis cinerea could only be cultured at the harvest stage from symptomatic and asymptomatic berries. Overall, the study showed the highest prevalence of Alternaria (35.6%), Cladosporium (27.2%) and Rhodoturula (21.2%). In conclusion, the study reveals a diverse pathogenic and beneficial naturally-known yeast genera in the presence of B. cinerea. Such information and knowledge can be further explored to manipulate potential antagonistic populations to prevent establishment of pathogenic populations and secure dominance of antagonistic populations at the harvest stage.

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References

  • Abdelfattah, A., Nicosia, M.G.L.D., Cacciola, S.O., Droby, S., & Schena, L. (2015). Metabarcoding analysis of fungal diversity in the phyllosphere and carposphere of olive (Olea europaea). PLoS One, 10, e0131069.

  • Abdelfattah, A., Wisniewski, M., Droby, S., & Schena, L. (2016a). Spatial and compositional variation in the fungal communities of organic and conventionally grown apple fruit at the consumer point-of-purchase. Horticulture Research, 3, 16047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdelfattah, A., Wisniewski, M., Li Destri Nicosia, M. G., Cacciola, S. O., & Schena, L. (2016b). Metagenomic analysis of fungal diversity on strawberry plants and the effect of management practices on the fungal community structure of aerial organs. PLoS One, 11(8), e0160470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aleklett, K., Hart, M., & Shade, A. (2014). The microbial ecology of flowers: An emerging frontier in phyllosphere research. Botany, 92(4), 253–266.

    Article  Google Scholar 

  • Andrews, J. H., & Harris, R. F. (2000). The ecology and biogeography of microorganisms on plant surfaces. Annual Review of Phytopathology, 38(1), 145–180.

    Article  PubMed  Google Scholar 

  • Briceño, E. X., & Latorre, B. A. (2008). Characterization of Cladosporium rot in grapevines, a problem of growing importance in Chile. Plant Disease, 92(12), 1635–1642.

    Article  PubMed  Google Scholar 

  • Brum, M. C. P. D., Araujo, W. L. D., Maki, C. S., & Azevedo, J. L. D. (2012). Endophytic fungi from Vitis labrusca L. ('Niagara Rosada') and its potential for the biological control of Fusarium oxysporum. Genetics and Molecular Research, 11(4), 4187–4197.

    Article  CAS  PubMed  Google Scholar 

  • Bukulich, N. A., Thorngate, J. H., Richardson, P. M., & Mills, D. A. (2014). Microbial biogeography of wine grapes is conditioned by cultivar, vintage and climate. Proceedings of the National Academy of Sciences of the United States of America, 111(1), E139–E148.

    Article  CAS  Google Scholar 

  • Carmichael, P. C., Siyoum, N., Chidamba, L., & Korsten, L. (2017). Characterization of fungal communities of developmental stages in table grape grown in the northern region of South Africa. Journal of Applied Microbiology, 123(5), 1251–1262.

    Article  CAS  PubMed  Google Scholar 

  • Carmichael, P. C., Siyoum, N., Jongman, M., & Korsten, L. (2018). Prevalence of Botrytis cinerea at different phenological stages of table grapes grown in the northern region of South Africa. Scientia Horticulturae, 239, 57–63.

    Article  Google Scholar 

  • de Vega, C., & Herrera, C. M. (2012). Relationships among nectar-dwelling yeasts, flowers and ants: Patterns and incidence on nectar traits. Oikos, 121(11), 1878–1888.

    Article  Google Scholar 

  • de Vega, C., & Herrera, C. M. (2013). Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinated plant. American Journal of Botany, 100(4), 792–800.

    Article  CAS  PubMed  Google Scholar 

  • Dean, R., Van Kan, J., A, L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., et al. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13(4), 414–430.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dennis, C., & Cohen, E. (1976). The effect of temperature on strains of soft fruit spoilage fungi. Annals of Applied Biology, 82(1), 51–56.

    Article  Google Scholar 

  • Dufour, M. C., Fontaine, S., Montarry, J., & Corio-Costet, M. F. (2011). Assessment of fungicide resistance and pathogen diversity in Erysiphe necator using quantitative real-time PCR assays. Pest Management Science, 67(1), 60–69.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, J. H. S., Van Wyk, P. S., & Venter, E. (2017). Slow dieback of grapevine: Association of Phialophora parasitica with slow dieback of grapevines. South African Journal of Enology and Viticulture, 15(1), 9–11.

    Article  Google Scholar 

  • Fu, D., Zeng, L., Zheng, X., & Yu, T. (2015). Effect of β-glucan on stress tolerances and biocontrol efficacy of Cryptococcus laurentii against Penicillium expansum in pear fruit. BioControl, 60(5), 669–679.

    Article  CAS  Google Scholar 

  • Glenn, D. M., Bassett, C., & Dowd, S. (2015). Effect of pest management system on ‘Empire’apple leaf phyllosphere populations. Scientia Horticulturae, 183, 58–65.

    Article  Google Scholar 

  • Holz, G., Gütschow, M., Coertze, S., & Calitz, F. J. (2003). Occurrence of Botrytis cinerea and subsequent disease expression at different positions on leaves and bunches of grape. Plant Disease, 87(4), 351–358.

    Article  PubMed  Google Scholar 

  • Huang, M., Sanchez-Moreiras, A. M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J., & Tholl, D. (2012). The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytopathology, 193(4), 997–1008.

    Article  CAS  Google Scholar 

  • Ianiri, G., Pinedo, C., Fratianni, A., Panfili, G., & Castoria, R. (2017). Patulin degradation by the biocontrol yeast Sporobolomyces sp. is an inducible process. Toxins, 9(2), 61.

    Article  CAS  PubMed Central  Google Scholar 

  • Jara, C., Laurie, V. F., Mas, A., & Romero, J. (2016). Microbial terroir in Chilean valleys: Diversity of non-conventional yeast. Frontiers in Microbiology, 7.

  • Johnson, G. I., Mead, A. J., Cooke, A. W., & Dean, J. R. (1992). Mango stem end rot pathogens-fruit infection by endophytic colonisation of the inflorescence and pedicel. Annals of Applied Biology, 120(2), 225–234.

    Article  Google Scholar 

  • Junker, R. R., Loewel, C., Gross, R., Dötterl, S., Keller, A., & Blüthgen, N. (2011). Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biology, 13(6), 918–924.

    Article  CAS  PubMed  Google Scholar 

  • Kernaghan, G., Mayerhofer, M., & Griffin, A. (2017). Fungal endophytes of wild and hybrid Vitis leaves and their potential for vineyard biocontrol. Canadian Journal of Microbiology, 63(7), 583–595.

    Article  CAS  PubMed  Google Scholar 

  • Lai, T., Bai, X., Wang, Y., Zhou, J., Shi, N., & Zhou, T. (2015). Inhibitory effect of exogenous sodium bicarbonate on development and pathogenicity of postharvest disease Penicillium expansum. Scientia Horticulturae, 187, 108–114.

    Article  CAS  Google Scholar 

  • Latorre, B. A., & Guerrero, M. J. (2001). First report of shoot blight of grapevine caused by Sclerotinia sclerotiorum in Chile. Plant Disease, 85(10), 1122–1122.

    Article  CAS  PubMed  Google Scholar 

  • Lievens, B., Hallsworth, J. E., Pozo, M. I., Belgacem, Z. B., Stevenson, A., Willems, K. A., & Jacquemyn, H. (2015). Microbiology of sugar-rich environments: Diversity, ecology and system constraints. Environmental Microbiology, 17(2), 278–298.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Lan, X., Yin, L., Dry, I. B., Xiang, J., & Lu, J. (2018). In planta functional analysis and subcellular localization of the oomycete pathogen Plasmopara viticola candidate RXLR effector repertoire. Frontiers in Plant Science, 9, 286.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martini, M., Musetti, R., Grisan, S., 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(10), 993–998.

    Article  CAS  PubMed  Google Scholar 

  • Ondov, B., Bergman, N., & Phillippy, A. (2011). Interactive metagenomic visualization in a Web browser. BMC Bioinformatics, 12, 385.

  • Ottesen, A. R., Peña, A. G., White, J. R., Pettengill, J. B., Li, C., Allard, S., et al. (2013). Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiology, 13(1), 114.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pancher, M., Ceol, M., Corneo, P. E., Longa, C. M. O., Yousaf, S., Pertot, I., et al. (2012). Fungal endophytic communities in grapevines (Vitis vinifera L.) respond to crop management. Applied and Environmental Microbiology, AEM-07655.

  • Perrone, G., Mulè, G., Susca, A., Battilani, P., Pietri, A., & Logrieco, A. (2006). Ochratoxin A production and amplified fragment length polymorphism analysis of Aspergillus carbonarius, Aspergillus tubingensis, and Aspergillus niger strains isolated from grapes in Italy. Applied and Environmental Microbiology, 72(1), 680–685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinto, C., Pinho, D., Sousa, S., Pinheiro, M., Egas, C., & Gomes, A. C. (2014). Unravelling the diversity of grapevine microbiome. PLoS One, 9(1), e85622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poolsawat, O., Tharapreuksapong, A., Wongkaew, S., Reisch, B., & Tantasawat, P. (2010). Genetic diversity and pathogenicity analysis of Sphaceloma ampelinum causing grape anthracnose in Thailand. Journal of Phytopathology, 158(11–12), 837–840.

    Article  Google Scholar 

  • Rathnayake, R. M. S. P., Savocchia, S., Schmidtke, L. M., & Steel, C. C. (2018). Characterisation of Aureobasidium pullulans isolates from Vitis vinifera and potential biocontrol activity for the management of bitter rot of grapes. European Journal of Plant Pathology, 151(3), 593–611.

    Article  Google Scholar 

  • Rivera, S. A., Zoffolli, J. P., & Latorre, B. A. (2013). Infection risk and critical period for the postharvest control of gray mold (Botrytis cinerea) on blueberry in Chile. Plant Disease, 97(8), 1069–1074.

    Article  CAS  PubMed  Google Scholar 

  • Romanazzi, G., Smilanick, J. L., Feliziani, E., & Droby, S. (2016). Integrated management of postharvest gray mold on fruit crops. Postharvest Biology and Technology, 113, 69–76.

    Article  CAS  Google Scholar 

  • Schloss, P. D., & Handelsman, J. (2006). Toward a census of bacteria in soil. PLoS Computational Biology, 2(7), e92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Setati, M. E., Jacobson, D., & Bauer, F. F. (2015). Sequence-based analysis of the Vitis vinifera L. cv cabernet sauvignon grape must mycobiome in three south African vineyards employing distinct agronomic systems. Frontiers in Microbiology, 6.

  • Shen, Y., Nie, J., Dong, Y., Kuang, L., Li, Y., & Zhang, J. (2018). Compositional shifts in the surface fungal communities of apple fruits during cold storage. Postharvest Biology and Technology, 144, 55–62.

    Article  CAS  Google Scholar 

  • Singh, S., Gupta, R., Kumari, M., & Sharma, S. (2015). Nontarget effects of chemical pesticides and biological pesticide on rhizospheric microbial community structure and function in Vigna radiata. Environmental Science and Pollution Research, 22(15), 11290-11300.

  • Sternad Lemut, M., Sivilotti, P., Butinar, L., Laganis, J., & Vrhovsek, U. (2015). Pre-flowering leaf removal alters grape microbial population and offers good potential for a more sustainable and cost-effective management of a pinot noir vineyard. Australian Journal of Grape and Wine Research, 21(3), 439–450.

    Article  Google Scholar 

  • Swart, A. E., Lennox, C. L., & Holz, G. (2017). Infection of table grape bunches by Alternaria alternata. South African Journal of Enology and Viticulture, 16(1), 3–6.

    Article  Google Scholar 

  • Tadych, M., Bergen, M. S., Johnson-Cicalese, J., Polashock, J. J., Vorsa, N., & White, J. F. (2012). Endophytic and pathogenic fungi of developing cranberry ovaries from flower to mature fruit: Diversity and succession. Fungal Diversity, 54(1), 101–116.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, M. W., Tsai, P., Anfang, N., Ross, H. A., & Goddard, M. R. (2014). Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environmental Microbiology, 16(9), 2848–2858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • United States Department of Agriculture (USDA). (2017). Production, supply, distribution online database. Accessed online 24/08/ 2017 https://apps.fas.usda.gov/psdonline/app/index.html#/app/home.

  • Van Boxstael, S., Habib, I., Jacxsens, L., De Vocht, M., Baert, L., Van de Perre, E., et al. (2013). Food safety issues in fresh produce: Bacterial pathogens, viruses and pesticide residues indicated as major concerns by stakeholders in the fresh produce chain. Food Control, 32(1), 190–197.

    Article  Google Scholar 

  • Wijayawardene, N. N., Crous, P. W., Kirk, P. M., Hawksworth, D. L., Boonmee, S., Braun, U., Dai, D. Q., D’souza, M. J., Diederich, P., Dissanayake, A., Doilom, M., Hongsanan, S., Jones, E. B. G., Groenewald, J. Z., Jayawardena, R., Lawrey, J. D., Liu, J. K., Lücking, R., Madrid, H., Manamgoda, D. S., Muggia, L., Nelsen, M. P., Phookamsak, R., Suetrong, S., Tanaka, K., Thambugala, K. M., Wanasinghe, D. N., Wikee, S., Zhang, Y., Aptroot, A., Ariyawansa, H. A., Bahkali, A. H., Bhat, D. J., Gueidan, C., Chomnunti, P., de Hoog, G. S., Knudsen, K., Li, W. J., McKenzie, E. H. C., Miller, A. N., Phillips, A. J. L., Piątek, M., Raja, H. A., Shivas, R. S., Slippers, B., Taylor, J. E., Tian, Q., Wang, Y., Woudenberg, J. H. C., Cai, L., Jaklitsch, W. M., & Hyde, K. D. (2014). Naming and outline of Dothideomycetes–2014 including proposals for the protection or suppression of generic names. Fungal Diversity, 69(1), 1–55.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zapata, Y., Díaz, A., Grijalba, E., Rodríguez, F., Elad, Y., Cotes, A.M. 2015. Phyllosphere yeasts with potential for biological control of Botrytis cinerea in rose. In III International symposium on postharvest pathology: Using science to increase food availability. 1144, 77–84.

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Acknowledgements

This research was financially supported in part by the Department of Science and Technology in partnership with the Fresh Produce Exporters’ Forum, Post-harvest Innovation Programme. Authors express their appreciation to the table grape growers for granting permission to conduct trials in their vineyards. The authors acknowledge Ms. Zama Zulu for her laboratory assistance.

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  1. Department of Plant and Soil Sciences, University of Pretoria, Private Bag X20, Hatfield, 0028, South Africa

    P. C. Carmichael, N. Siyoum, L. Chidamba & Lise Korsten

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  1. P. C. Carmichael
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  2. N. Siyoum
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  3. L. Chidamba
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  4. Lise Korsten
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Correspondence to Lise Korsten.

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Carmichael, P.C., Siyoum, N., Chidamba, L. et al. Exploring the microbial communities associated with Botrytis cinerea during berry development in table grape with emphasis on potential biocontrol yeasts. Eur J Plant Pathol 154, 919–930 (2019). https://doi.org/10.1007/s10658-019-01710-5

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