Development and validation of a set of standard area diagrams to assess severity of gray mold in strawberry fruit

Abstract

Gray mold (Botrytis cinerea) is one of the main diseases that affect strawberries. Severity assessments of the disease in fruits have been mainly performed without any aid. Although there has been a rating scale already published, there are no standard area diagrams (SADs) that could be used. Therefore, our objective was to develop and validate a set of SADs to assess severity of gray mold in strawberry fruit. The set of SADs has seven levels of disease severity (0, 8, 28, 46, 77, 82 and 100%) and they were validated by five experienced raters and five inexperienced raters in plant disease assessment. Photos of 50 strawberry fruits were provided to raters for gray mold severity assessment, which was performed in three stages: i) without any aid; ii) with a rating scale previously published; and iii) with the SADs. Lin’s concordance correlation coefficient (LCCC) of estimated and actual severity was improved with the use of SADs (0.94) compared to the rating scale (0.74) and assessment without aid (−0.07). Peer comparison of all raters showed that 87% of the coefficient of determination from the regression models between actual and estimated severity were greater than 0.81 with the SADs, while only 37% and 9% of the values were higher than 0.81 with the rating scale and without any aid, respectively. Hence, there was greater consistency of disease assessment among raters. The set of SADs proposed in this study can improve accuracy and precision to estimate severity of gray mold in strawberry fruit.

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Data Availability

The datasets generated during the current study are available from the corresponding author upon reasonable request.

References

  1. Antunes, L. E. C., & Reisser Junior, C. (2007). Caracterização da produção de morangos no Brasil. Bologna - Rivista di Frutticoltura e Ortofloricoltura, 69, 60–65.

    Google Scholar 

  2. Araújo, E. R., Resende, R. S., Krezanoski, C. E., & Duarte, H. S. S. (2018). A standard area diagram set for severity assessment of Botrytis leaf blight of onion. European Journal of Plant Pathology, 153, 273–277.

    Article  Google Scholar 

  3. Bock, C. H., Poole, G., Parker, P. E., & Gottwald, T. R. (2010). Plant disease severity estimated visually, by digital photography and image analysis, and by hyperspectral imaging. Critical Reviews in Plant Science, 29, 59–107.

    Article  Google Scholar 

  4. Braido, R., Gonçalves-Zuliani, A. M. O., Janeiro, V., Carvalho, S. A., Belasque, J. J., Bock, C. H., & Nunes, W. M. C. (2014). Development and validation of standard area diagrams as assessment aids for estimating the severity of citrus canker on unripe oranges. Plant Disease, 98, 1543–1550.

    Article  Google Scholar 

  5. Capucho, A. S., Zambolim, L., Duarte, H. S. S., & Vaz, G. R. O. (2011). Development and validation of a standard area diagram set to estimate severity of leaf rust in Coffea arabica and C. canephora. Plant Pathology, 60, 1144–1150.

    Article  Google Scholar 

  6. Chaves, V. C., Calvete, E., & Reginatto, F. H. (2017). Quality properties and antioxidant activity of seven strawberry (Fragaria X ananassa Duch) cultivars. Scientia Horticulturae, 225, 293–298.

    CAS  Article  Google Scholar 

  7. Chiang, K. S., Liu, H. I., Chen, Y. L., Jarroudi, M. E., & Bock, C. H. (2020). Quantitative ordinal scale estimates of plant disease severity: Comparing treatments using a proportional odds model. Phytopathology, 110, 734–743.

    CAS  Article  Google Scholar 

  8. Chiomento, J. L. T., Costa, R. C., Nardi, F. S., Trentin, N. S., Nienow, A. A., & Calvete, E. O. (2019). Arbuscular mycorrhizal fungi communities improve the phytochemical quality of strawberry. The Journal of Horticultural Science and Biotechnology, 94, 653–663.

    Article  Google Scholar 

  9. Costa, A. P., Pires de Carvalho, M., Peixoto, J. R., Blum, L. E. B., & Faleiro, F. G. (2018). Standard area diagram set for bacterial spot assessment in fruits of yellow passion fruit. Revista Brasileira de Fruticultura, 40, 1–15.

    CAS  Article  Google Scholar 

  10. Del Ponte, E., Pethybridge, S. J., Bock, C. H., Michereff, S. J., Machado, F. J., & Spolti, P. (2017). Standard area diagrams for aiding severity estimation: Scientometrics, pathosystems, and methodological trends in the last 25 years. Phytopathology, 107, 1161–1174.

    Article  Google Scholar 

  11. Domiciano, G. P., Duarte, H. S. S., Moreira, E. N., & Rodrigues, F. A. (2014). Development and validation of a set of standard area diagrams to aid in estimation of spot blotch severity on wheat leaves. Plant Pathology, 63, 922–928.

    Article  Google Scholar 

  12. Duan, J., Zhao, B., Wang, Y., & Yang, W. (2015). Development and validation of a standard area diagram set to aid estimation of bacterial spot severity on tomato leaves. European Journal of Plant Pathology, 142, 665–675.

    Article  Google Scholar 

  13. Duarte, L. J., Chaves, V. C., Nascimento, M. V. P. S., Calvete, E., Li, M., Ciraolo, E., et al. (2018). Molecular mechanism of action of Pelargonidin-3-O-glucoside, the main anthocyanin responsible for the anti-inflammatory effect of strawberry fruits. Food Chemistry, 247, 56–65.

    CAS  Article  Google Scholar 

  14. Forges, M., Vàsquez, H., Charles, F., Sari, D. C., Urban, L., Lizzi, Y., Bardin, M., & Aarrouf, J. (2018). Impact of UV-C radiation on the sensitivity of three strawberry plantcultivars (Fragaria X ananassa) against Botrytis cinerea. Scientia Horticulturae, 240, 603–613.

    Article  Google Scholar 

  15. González-Domínguez, E., Martins, R, B., Ponte, E, M., Michereff, S, J., García-Jiménez, J., Armengol, J. (2014). Development and validation of a standard area diagram set to aid assessment of severity of loquat scab on fruit. European Journal of Plant Pathology, 419–428.

  16. Jeon, C. W., Kim, D., Park, J. J., Kang, N. J., & Swak, Y. (2017). Exported strawberry gray mold decay related spore density and disease incidence in cultivation field. The Korean Journal of Pesticide Science, 21, 224–231.

    Article  Google Scholar 

  17. Jin, P., Wang, H., Zhang, Y., Huang, Y., Wang, L., & Zheng, Y. (2017). UV-C enhances resistance against gray mold decay caused by Botrytis cinerea in strawberry fruit. Scientia Horticulturae, 225, 106–1111.

    CAS  Article  Google Scholar 

  18. Kim, J., Shin, J.-H., Gumilang, A., Chung, K., Choi, K. Y., & Kim, K. S. (2016). Effectiveness of different classes of fungicides on Botrytis cinerea causing gray mold on fruit and vegetables. The Plant Pathology Journal, 32, 570–574.

    CAS  Article  Google Scholar 

  19. Lopes, U. P., Zambolim, L., Capobriango, N. P., Gracia, N. A. O., & Freitas-Lopes, R. L. (2017). Resistance of Botrytis cinerea to fungicides controlling gray mold on strawberry in Brazil. Bragantia, 76, 266–272.

    Article  Google Scholar 

  20. Monzani, R. M., Silva, G. A., Nutter Junior, F., Duarte, H. S. S., & De Mio, L. L. M. (2018). Development and validation of a standard area set diagrams to evaluate bacterial blight on yellow passion fruit leaves. Summa Phytopathologica, 44, 332–337.

    Article  Google Scholar 

  21. Nita, M., Ellis, M. A., & Madden, L. V. (2003). Reliability and accuracy of visual estimation of Phomopsis leaf blight of strawberry. Phytopathology, 93, 995–1005.

    CAS  Article  Google Scholar 

  22. Nunes, M, C, N., Morais, A, M, M, B., Brecht, J, K., Sargent, S, A., Bartz, J, A., Allen, R, A. et al. (2012). Occurrence of gray mold in stored strawberries as affected by ripeness, temperature, and atmosphere. Proceedings of The Florida State Horticultural Society, 3–5 , Delray Beach, FL, USA. pp. 287-294.

  23. Pedroso, C., Lage, D. A. C., Henz, G. P., & Café-Filho, A. C. (2011). Development and validation of a diagrammatic scale for estimation of anthracnose on sweet pepper fruits for epidemiological studies. Journal of Plant Pathology, 93, 219–225.

    Google Scholar 

  24. Petrasch, S., Knapp, S. J., Kan, J. A. L. V., & Blanco-Ulate, B. (2019). Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea. Molecular Plant Pathology, 20, 877–892.

    Article  Google Scholar 

  25. R Core Team. (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 10 February 2020.

  26. 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.

    CAS  Article  Google Scholar 

  27. Spolti, P., Schneider, L., Sanhueza, R. M. V., et al. (2011). Improving sooty blotch and flyspeck severity estimation on apple fruit with the aid of standard area diagrams. Eur J Plant Pathol, 129, 21–29. https://doi.org/10.1007/s10658-010-9636-7.

  28. Töfoli, J. G., Ferrari, J. T., Domingues, R. J., & Nogueira, E. M. C. (2011). Botrytis sp. em espécies hortícolas: hospedeiros, sintomas e manejo. Biológico, 73, 11–20.

    Google Scholar 

  29. Yadav, N. V. S., de Vos, S. M., Bock, C. H., & Wood, B. W. (2012). Development and validation of standard area diagrams to aid assessment of pecan scab symptoms on fruit. Plant Pathology, 62, 325–335.

    Article  Google Scholar 

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Acknowledgments

We are thankful for the Ph.D. scholarship provided to Débora Filippi by the Graduate Support Program for Community Private Education Institutions (PROSUC) from the Coordination for the Improvement of Higher Education Personnel (CAPES) from Brazil. We also thank the raters for their availability to assess disease severity during this study.

Funding

Ph.D. scholarship of the first author, Débora Filippi, was provided by the Graduate Support Program for Community Private Education Institutions (PROSUC) from the Coordination for the Improvement of Higher Education Personnel (CAPES).

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Conceptualization and experimental design: DF and JHN; Data collection: DF, TST, AGD and JLTC; Data analysis: JHN; Writing - original draft preparation: DF, JLTC and JHN; Writing – review and editing: AAN and EOC. Supervision: AAN and EOC. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Débora Filippi.

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Filippi, D., Nienow, A.A., Chiomento, J.L.T. et al. Development and validation of a set of standard area diagrams to assess severity of gray mold in strawberry fruit. Eur J Plant Pathol (2021). https://doi.org/10.1007/s10658-021-02238-3

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Keywords

  • Botrytis cinerea
  • Disease assessment
  • Disease severity
  • Fragaria X ananassa Duch.
  • Phytopathometry