Grey mould disease of strawberry in northern Germany: causal agents, fungicide resistance and management strategies

  • Roland W. S. WeberEmail author
  • Matthias Hahn


Grey mould, the most important disease of strawberry worldwide, is caused by Botrytis cinerea and a few additional Botrytis spp. Fungicide resistance is a growing problem and has become a limiting factor in strawberry production. In northern Germany, an annual survey of Botrytis isolates from commercial strawberry fields in 2010 to 2017 has revealed high (> 20%) frequencies of resistance to quinone-outside inhibitors, fenhexamid, boscalid, fludioxonil and cyprodinil, as well as lower (< 10%) shares of resistance to the recently released fluopyram. Iprodione and benzimidazoles have not been used in northern Germany for several years or decades, respectively, yet resistance to them was still detected. These observations are largely representative of the situation in many other strawberry-producing regions worldwide. The spread of strains with multiple resistance to several or even all currently used single-site fungicides is of particular concern and is probably promoted by their excessive use. Contaminated nursery material is a newly detected potential vehicle for the spread of strains with (multiple) fungicide resistance. Several complementary non-chemical measures are available to secure strawberry production in the face of weakening fungicide efficacies, and these are briefly discussed.


Botrytis cinerea Botrytis fragariae Botrytis pseudocinerea Multiple fungicide resistance Nursery stock Sanitation 


Funding information

Many of our results and conclusions reported here were generated in the course of an innovation support programme (FKZ 2814705711) funded by the German Federal Ministry of Food and Agriculture.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by either of the authors.


  1. Amiri A, Heath SM, Peres NA (2014) Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry. Plant Dis 98:532–539CrossRefGoogle Scholar
  2. Amiri A, Zuniga AI, Peres NA (2018a) Prevalence of Botrytis cryptic species in strawberry nursery transplants and strawberry and blueberry commercial fields in the eastern United States. Plant Dis 102:398–404CrossRefGoogle Scholar
  3. Amiri A, Zuniga AI, Peres NA (2018b) Potential impact of populations drift on Botrytis occurrence and resistance to multi- and single-site fungicides in Florida southern highbush blueberry fields. Plant Dis 102:2142–2148CrossRefGoogle Scholar
  4. Bardas GA, Veloukas T, Koutita O, Karaoglanidis GS (2010) Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Manag Sci 66:967–973CrossRefGoogle Scholar
  5. Baroffio CA, Siegfried W, Hilber UW (2003) Long-term monitoring for resistance of Botryotinia fuckeliana to anilinopyrimidine, phenylpyrrole, and hydroxyanilide fungicides in Switzerland. Plant Dis 87:662–666CrossRefGoogle Scholar
  6. Braun PG, Sutton JC (1987) Inoculum sources of Botrytis cinerea in fruit rot of strawberries in Ontario. Can J Plant Pathol 9:1–5CrossRefGoogle Scholar
  7. Brent KJ, Hollomon DW (2007) Fungicide resistance: the assessment of risk. Fungicide Resistance Action Committee, Brussels, Belgium. Accessed 1 Nov. 2018
  8. Bulger MA, Ellis MA, Madden LV (1987) Influence of temperature and wetness duration on infection of strawberry flowers by Botrytis cinerea and disease incidence of fruit originating from infected flowers. Phytopathology 77:1225–1230CrossRefGoogle Scholar
  9. Chatzidimopoulos M, Papaevaggelou D, Pappas AC (2013) Detection and characterization of fungicide resistant phenotypes of Botrytis cinerea in lettuce crops in Greece. Eur J Plant Pathol 137:363–376CrossRefGoogle Scholar
  10. Chen SN, Luo CX, Hu MJ, Schnabel G (2016) Fitness and competitive ability of Botrytis cinerea isolates with resistance to multiple chemical classes of fungicides. Phytopathology 106:997–1005CrossRefGoogle Scholar
  11. Daugaard H (1999) Cultural methods for controlling Botrytis cinerea Pers. in strawberry. Biol Agric Hortic 16:351–361CrossRefGoogle Scholar
  12. Dowling ME, Hu M-J, Schnabel G (2018) Fungicide resistance in Botrytis fragariae and species prevalence in the mid-Atlantic United States. Plant Dis 102:964–969CrossRefGoogle Scholar
  13. Elad Y, Pertot I, Prado AMC, Stewart A (2016) Plant hosts of Botrytis spp. In: Fillinger S, Elad Y (eds) Botrytis – the fungus, the pathogen and its management in agricultural systems. Springer, Cham, pp 413–486CrossRefGoogle Scholar
  14. Faretra F, Pollastro S, di Tonno AP (1989) New natural variants of Botryotinia fuckeliana (Botrytis cinerea) coupling benzimidazole-resistance to insensitivity toward the N-phenylcarbamate diethofencarb. Phytopathol Mediterr 28:98–104Google Scholar
  15. Fernández-Ortuño D, Chen F, Schnabel G (2013) Resistance to cyprodinil and lack of fludioxonil resistance in Botrytis cinerea isolates from strawberry in North and South Carolina. Plant Dis 97:81–85CrossRefGoogle Scholar
  16. Fernández-Ortuño D, Grabke A, Li X, Schnabel G (2015) Independent emergence of resistance to seven chemical classes of fungicides in Botrytis cinerea. Phytopathology 105:424–432CrossRefGoogle Scholar
  17. Fillinger S, Ajouz S, Nicot PC, Leroux P, Bardin M (2012) Functional and structural comparison of pyrrolnitrin- and iprodione-induced modifications in the class III histidine kinase Bos1 of Botrytis cinerea. PLoS One 7:e42520CrossRefGoogle Scholar
  18. Giraud T, Fortini D, Levis C, Leroux P, Brygoo Y (1997) RFLP markers show genetic recombination in Botryotinia fuckeliana (Botrytis cinerea) and transposable elements reveal two sympatric species. Mol Biol Evol 14:1177–1185CrossRefGoogle Scholar
  19. Grabke A, Fernández-Ortuño D, Schnabel G (2013) Fenhexamid resistance in Botrytis cinerea from strawberry fields in the Carolinas is associated with four target gene mutations. Plant Dis 97:271–276CrossRefGoogle Scholar
  20. Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91:621–627CrossRefGoogle Scholar
  21. Hahn M (2014) The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Biol 7:133–141CrossRefGoogle Scholar
  22. Hortynski JA (1991) The problem of grey mold in strawberry breeding. In: Dale A, Luby JJ (eds) The Strawberry into the 21st Century. Timber Press, Portland, pp 54–56Google Scholar
  23. 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 106:1513–1520CrossRefGoogle Scholar
  24. Hu M-J, Fernández-Ortuño D, Schnabel G (2016b) Monitoring resistance to SDHI fungicides in Botrytis cinerea from strawberry fields. Plant Dis 100:959–965CrossRefGoogle Scholar
  25. Hyde KD, Nilsson RH, Alias SA, Ariyawansa HA, Blair JE, Cai L, de Cock AWAM, Dissanayake AJ, Glockling SL, Goonasekara ID, Gorczak M, Hahn M, Jayawardena RS, van Kan JAL, Laurence MH, Lévesque CA, Li X, Liu J-K, Maharachchikumbura SSN, Manamgoda DS, Martin FN, McKenzie EHC, McTaggart AR, Mortimer PE, Nair PVR, Pawłowska J, Rintoul TL, Shivas RG, Spies CFJ, Summerell BA, Taylor PWJ, Terhem RB, Udayanga D, Vaghefi N, Walther G, Wilk M, Wrzosek M, Xu J-C, Yan J, Zhou N (2014) One stop shop: backbones trees for important phytopathogenic genera: I (2014). Fungal Divers 67:21–125CrossRefGoogle Scholar
  26. Jarvis WR (1962) The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Ann Appl Biol 50:569–575CrossRefGoogle Scholar
  27. Johnston PR, Hoksbergen K, Park D, Beever RE (2014) Genetic diversity of Botrytis in New Zealand vineyards and the significance of its seasonal and regional variation. Plant Pathol 63:888–898CrossRefGoogle Scholar
  28. Katan T (1982) Persistence of dicarboximide-fungicide resistance in populations of Botrytis cinerea in a warm, dry temperate agroclimate. Phytoparasitica 10:209–211CrossRefGoogle Scholar
  29. Kovach J, Petzold R, Harman GE (2000) Use of honey bees and bumble bees to disseminate Trichoderma harzianum 1295-22 to strawberries for Botrytis control. Biol Control 18:235–242CrossRefGoogle Scholar
  30. 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:e1000696CrossRefGoogle Scholar
  31. Legard DE, Xiao CL, Mertely JC, Chandler CK (2000) Effects of plant spacing and cultivar on incidence of Botrytis fruit rot in annual strawberry. Plant Dis 84:531–538CrossRefGoogle Scholar
  32. Leroch M, Plesken C, Weber RWS, Kauff F, Scalliet G, Hahn M (2013) Gray 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 79:159–167CrossRefGoogle Scholar
  33. Leroux P (2007) Chemical control of Botrytis and its resistance to chemical fungicides. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Springer, Dordrecht, pp 195–222CrossRefGoogle Scholar
  34. Leroux P, Gredt M, Leroch M, Walker A-S (2010) Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Appl Environ Microbiol 76:6615–6630CrossRefGoogle Scholar
  35. Li X, Fernández-Ortuño D, Chai W, Wang F, Schnabel G (2012) Identification and prevalence of Botrytis spp. from blackberry and strawberry fields of the Carolinas. Plant Dis 96:1634–1637CrossRefGoogle Scholar
  36. 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 98:1066–1074CrossRefGoogle Scholar
  37. Ma ZH, Yan LY, Luo Y, Michailides TJ (2007) Sequence variation in the two-component histidine kinase gene of Botrytis cinerea associated with resistance to dicarboximide fungicides. Pestic Biochem Physiol 88:300–306CrossRefGoogle Scholar
  38. Mernke D, Dahm S, Walker A-S, Lalève A, Fillinger S, Leroch M, Hahn M (2011) Two promoter rearrangements in a drug efflux transporter gene are responsible for the appearance and spread of multi-drug resistance phenotype MDR2 in Botrytis cinerea isolates in French and German vineyards. Phytopathology 101:1176–1183CrossRefGoogle Scholar
  39. Mertely JC, MacKenzie SJ, Legard DE (2002) Timing of fungicide applications for Botrytis cinerea based on developmental stage of strawberry flowers and fruit. Plant Dis 86:1019–1024CrossRefGoogle Scholar
  40. Mosbach A, Edel D, Farmer AD, Widdison S, Barchietto T, Dietrich RA, Corran A, Scalliet G (2017) Anilinopyrimidine resistance in Botrytis cinerea is linked to mitochondrial function. Front Microbiol 8:2361CrossRefGoogle Scholar
  41. Nunes MCN, Morais AMMB, Brecht JK, Sargent SA, Bartz JA, Allen RA, Lee JH, Pires DM, Pittet-Moore J (2012) Occurrence of gray mold in stored strawberries as affected by ripeness, temperature and atmosphere. Proc Florida State Hortic Soc 125:287–294Google Scholar
  42. Park SY, Jung OJ, Chung YR, Lee CW (1997) Isolation and characterization of a benomyl-resistant form of beta-tubulin-encoding gene from the phytopathogenic fungus Botryotinia fuckeliana. Mol Cells 28:104–109Google Scholar
  43. Peng G, Sutton JC (1991) Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. Can J Plant Pathol 13:247–257CrossRefGoogle Scholar
  44. 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 81:7048–7056CrossRefGoogle Scholar
  45. Reddy MVB, Belkacemi K, Corcuff R, Castaigne F, Arul J (2000) Effect of pre-harvest chitosan sprays on post-harvest infection by Botrytis cinerea and quality of strawberry fruit. Postharvest Biol Technol 20:39–51CrossRefGoogle Scholar
  46. Ren W, Shao W, Han X, Zhou M, Chen C (2016) Molecular and biochemical characterization of laboratory and field mutants of Botrytis cinerea resistant to fludioxonil. Plant Dis 100:1414–1423CrossRefGoogle Scholar
  47. Romanazzi G, Smilanick JL, Feliziani E, Droby S (2016) Integrated management of postharvest gray mold on fruit crops. Postharvest Biol Technol 113:69–76CrossRefGoogle Scholar
  48. Rosslenbroich H-J (1999) Efficacy of fenhexamid (KBR 2738) against Botrytis cinerea and related fungal pathogens. Pflanzensch-Nachr Bayer 52:127–144Google Scholar
  49. Rupp S, Weber RWS, Rieger D, Detzel P, Hahn M (2017a) Spread of Botrytis cinerea strains with multiple fungicide resistance in German horticulture. Front Microbiol 7:2075CrossRefGoogle Scholar
  50. Rupp S, Plesken S, Rumsey S, Dowling M, Schnabel G, Weber RWS, Hahn M (2017b) 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–e00217CrossRefGoogle Scholar
  51. Staats M, van Baarlen P, van Kan JAL (2005) Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Mol Biol Evol 22:333–346CrossRefGoogle Scholar
  52. 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 28–31Google Scholar
  53. 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 104:347–356CrossRefGoogle Scholar
  54. Walker A-S, Gautier A, Confais J, Martinho D, Viaud M, Le Pêcheur P, Dupont J, Fournier E (2011) Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101:1433–1445CrossRefGoogle Scholar
  55. Weber RWS (2010) Schnelle und einfache Methode zum Nachweis der Fenhexamid-Resistenz bei Botrytis. Erwerbs-Obstbau 52:27–32CrossRefGoogle Scholar
  56. Weber RWS (2011) Resistance of Botrytis cinerea to multiple fungicides in northern German small-fruit production. Plant Dis 95:1263–1269CrossRefGoogle Scholar
  57. Weber RWS (2016) Resistent gråskimmel i danske jordbær. Gartner Tidende 2016(5):20–21Google Scholar
  58. Weber RWS, Entrop A-P (2011) Multiple fungicide resistance in Botrytis: a growing problem in German soft-fruit production. In: Thajuddin N (ed) Fungicides – beneficial and harmful aspects. InTech Publishing, Rijeka, pp 45–60Google Scholar
  59. Weber RWS, Entrop A-P (2017a) Infection of raspberry nursery plants with fungicide-resistant strains of the grey mould fungus Botrytis. Eur J Plant Pathol 147:933–936CrossRefGoogle Scholar
  60. Weber RWS, Entrop A-P (2017b) Recovery of fungicide-resistant Botrytis isolates from strawberry nursery plants. Eur J Plant Pathol 149:739–742CrossRefGoogle Scholar
  61. Weber RWS, Fried A (2011) Fungizid-Resistenzen bei Botrytis im Beerenobst. Obstb 36:144,167–171Google Scholar
  62. Weber RWS, Hahn M (2011) A rapid and simple method for determining fungicide resistance in Botrytis. J Plant Dis Protect 118:17–25CrossRefGoogle Scholar
  63. 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 122:81–90CrossRefGoogle Scholar
  64. 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 125:501–504CrossRefGoogle Scholar
  65. Wilcox WF, Seem RC (1994) Relationship between strawberry gray mold incidence, environmental variables, and fungicide applications during different periods of the fruiting season. Phytopathology 84:264–270CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Esteburg Fruit Research and Advisory CentreJorkGermany
  2. 2.Department of Food ScienceAarhus UniversityÅrslevDenmark
  3. 3.Department of BiologyUniversity of KaiserslauternKaiserslauternGermany

Personalised recommendations