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Fungicide Resistance in Botrytis in Danish Strawberry Production

Fungizidresistenzen bei Botrytis im dänischen Erdbeeranbau

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Abstract

A fungicide resistance survey of Botrytis populations in Danish strawberry fields was conducted in 2015 to 2019. Among 594 isolates from 46 fields under integrated pest management, 40% were resistant to fenhexamid, 76% to QoI fungicides, 57% to boscalid and 59% to anilinopyrimidines. These resistance levels were higher than in Northern Germany during the same period, reflecting the more frequent use of the corresponding commercial fungicides in Denmark. In contrast, resistance to fludioxonil (21%) was lower in Denmark than in Northern Germany. Fungicide resistance generally increased with the age of strawberry fields. Isolates with multiple resistance to the registered fungicides were more likely than sensitive isolates to possess resistance also to iprodione and thiophanate-methyl, two fungicides which were no longer used in Denmark during the sampling period. This coupling of resistance to current and old fungicides is interpreted as evidence of a differentiation of Botrytis populations into strains with enhanced and reduced competence to develop fungicide resistance. In order to retard resistance development, adjustments to Danish fungicide registration for strawberries are recommended. Further, non-chemical control methods such as removing infected fruit at harvest should be implemented.

Zusammenfassung

Ein Monitoring von Fungizidresistenzen bei Botrytis in dänischen Erdbeerfeldern wurde im Zeitraum von 2015 bis 2019 durchgeführt. Von 594 Isolaten aus 46 Feldern unter Integriertem Pflanzenschutz zeigten 40 % Resistenz gegen Fenhexamid, 76 % gegen QoI-Fungizide, 57 % gegen Boscalid und 59 % gegen Anilinopyrimidine. Diese im Vergleich zum norddeutschen Erdbeeranbau erhöhten Werte spiegelten die intensivere Anwendung der relevanten Fungizide in Dänemark wider. Im Gegensatz dazu lag die Resistenz gegen Fludioxonil mit 21 % niedriger als in Norddeutschland. Der Anteil der Fungizidresistenzen stieg mit längerer Kultivierungsdauer der Felder generell an. Isolate mit multipler Resistenz gegen die zugelassenen Wirkstoffe besaßen häufiger als sensitive Isolate eine gleichzeitige Resistenz gegen Iprodion und MBC-Fungizide, welche in Dänemark während des Untersuchungszeitraums nicht mehr eingesetzt worden waren. Diese Kombination von Resistenzen gegen aktuelle und alte Fungizide lässt auf eine Differenzierung der Botrytis-Populationen in Stämme mit geringerer und höherer Kompetenz zur Resistenzbildung schließen. Um die weitere Ausbreitung von Resistenzen zu verlangsamen, werden Anpassungen in der Fungizidzulassung an Erdbeeren in Dänemark vorgeschlagen. Des Weiteren sollten verstärkt nichtchemische Maßnahmen wie das Entfernen befallener Früchte während der Ernte in die Strategie zur Grauschimmelbekämpfung einbezogen werden.

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References

  • Entrop A‑P, Weber RWS (2007) Botrytis an Erdbeeren im Jahr 2007 – eine Nachlese. Mitt Obstbauversuchsr Alt Land 62:328–329

    Google Scholar 

  • Fernández-Ortuño D, Pérez-García A, Chamorro M, de la Peña E, de Vicente A, Torés JA (2017) Resistance to the SDHI fungicides boscalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from commercial strawberry fields in Spain. Plant Dis 101:1306–1313

    Article  Google Scholar 

  • Hauschildt M, Steinkellner S, Weber RWS (2020) Grey mould populations in Northern German sweet cherry and plum orchards: selection of fungicide-resistant Botrytis cinerea strains over sensitive B. pseudocinerea by fungicide treatments. Eur J Plant Pathol 157:615–623

    Article  CAS  Google Scholar 

  • Hu M‑J, Cox KD, Schnabel G (2016a) Resistance to increasing chemical classes of fungicides by virtue of “selection by association” in Botrytis cinerea. Phytopathology 106:1513–1520

    Article  CAS  Google Scholar 

  • Hu M‑J, Fernández-Ortuño D, Schnabel G (2016b) Monitoring resistance to SDHI fungicides in Botrytis cinerea from strawberry fields. Plant Dis 100:959–965

    Article  CAS  Google Scholar 

  • Kretschmer M, Leroch M, Mosbach A, Walker A‑S, Fillinger S, Mernke D, Schoonbeek H‑J, Pradier J‑M, Leroux P, de Waard MA, Hahn M (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5:e1000696

    Article  Google Scholar 

  • Leroch M, Plesken C, Weber RWS, Kauff F, Scalliet G, Hahn M (2013) Grey mold populations in German strawberry fields are resistant to multiple fungicides and dominated by a novel clade closely related to Botrytis cinerea. Appl Environ Microbiol 79:159–167

    Article  CAS  Google Scholar 

  • Li X, Fernández-Ortuño D, Chen S, Grabke A, Luo C‑X, Bridges WC, Schnabel G (2014) Location-specific fungicide resistance profiles and evidence for stepwise accumulation of resistance in Botrytis cinerea. Plant Dis 98:1066–1074

    Article  Google Scholar 

  • Plesken C, Weber RWS, Rupp S, Leroch M, Hahn M (2015) Botrytis pseudocinerea is a significant pathogen of several crop plants but susceptible to displacement by fungicide-resistant B. cinerea strains. Appl Environ Microbiol 81:7048–7056

    Article  CAS  Google Scholar 

  • Rupp S, Plesken S, Rumsey S, Dowling M, Schnabel G, Weber RWS, Hahn M (2017a) Botrytis fragariae, a new species causing gray mold on strawberries, shows high frequencies of specific and efflux-based fungicide resistance. Appl Environ Microbiol 83:e00269-17

    Article  CAS  Google Scholar 

  • Rupp S, Weber RWS, Rieger D, Detzel P, Hahn M (2017b) Spread of Botrytis cinerea strains with multiple fungicide resistance in German horticulture. Front Microbiol 7:2075

    Article  Google Scholar 

  • Sutton JC (1998) Botrytis fruit rot (gray mold) and blossom blight. In: Maas JL (ed) Compendium of strawberry diseases, 2nd edn. APS Press, St Paul, pp 28–31

    Google Scholar 

  • Veloukas T, Kalogeropoulou P, Markoglou AN, Karaoglanidis GS (2014) Fitness and competitive ability of Botrytis cinerea field isolates with dual resistance to SDHI and QoI fungicides, associated with several sdhB and the cytb G143A mutations. Phytopathology 104:347–356

    Article  CAS  Google Scholar 

  • Veloukas T, Markoglou AN, Karaoglanidis GS (2013) Differential effect of SdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea. Plant Dis 97:118–122

    Article  CAS  Google Scholar 

  • Weber RWS (2011) Resistance of Botrytis cinerea to multiple fungicides in Northern German small-fruit production. Plant Dis 95:1263–1269

    Article  CAS  Google Scholar 

  • Weber RWS (2016) Resistent gråskimmel i danske jordbær. Gartner Tid 132(5):20–21

    Google Scholar 

  • Weber RWS (2020) Zehn Jahre Fungizidresistenztests bei Botrytis im norddeutschen Erdbeeranbau. Erwerbs-Obstbau 62:155–161

    Article  Google Scholar 

  • Weber RWS, Entrop A‑P (2011) Auftreten, Bedeutung und Vermeidung von Fungizid-Resistenzen bei Botrytis an Erdbeeren und Himbeeren. Mitt Obstbauversuchsr Alt Land 66:136–144

    Google Scholar 

  • Weber RWS, Entrop A‑P (2017) Recovery of fungicide-resistant Botrytis isolates from strawberry nursery plants. Eur J Plant Pathol 149:739–742

    Article  CAS  Google Scholar 

  • Weber RWS, Hahn M (2011) A rapid and simple method for determining fungicide resistance in Botrytis. J Plant Dis Protect 118:17–25

    Article  CAS  Google Scholar 

  • Weber RWS, Hahn M (2019) Grey mould disease of strawberry in northern Germany: causal agents, fungicide resistance and management strategies. Appl Microbiol Biotechnol 103:1589–1597

    Article  CAS  Google Scholar 

  • Weber RWS, Entrop A‑P, Goertz A, Mehl A (2015) Status of sensitivity of Northern German Botrytis populations to the new SDHI fungicide fluopyram prior to its release as a commercial fungicide. J Plant Dis Protect 122:81–90

    Article  Google Scholar 

  • Weber RWS, Raddatz C, Kutz S (2018) Relative abundance and fungicide resistance patterns of Botrytis cinerea and B. pseudocinerea on apple in Northern Germany. J Plant Dis Protect 125:501–504

    Article  Google Scholar 

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Acknowledgements

This work was supported by research grant HORTPROTECT from Grønt Udviklings- og Demonstrationsprogram, GUDP, Denmark (Project number 34009-16-1097). We thank Hanne Birgitte Christensen, Anne-Pia Larsen and Stefanie Kutz for assistance in performing laboratory assays, and Dan Christensen for help with the sampling of strawberry fields.

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Correspondence to Roland W. S. Weber.

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B.J. Nielsen, N.L. Jensen, P. Hartvig, L. Hjelmroth and R.W.S. Weber declare that they have no competing interests.

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Nielsen, B.J., Jensen, N.L., Hartvig, P. et al. Fungicide Resistance in Botrytis in Danish Strawberry Production. Erwerbs-Obstbau 63, 1–6 (2021). https://doi.org/10.1007/s10341-021-00541-1

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  • DOI: https://doi.org/10.1007/s10341-021-00541-1

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