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

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Abstract

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.

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References

  • Amiri A, Heath SM, Peres NA (2014) Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry. Plant Dis 98:532–539

    Article  CAS  PubMed  Google Scholar 

  • 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 102:398–404

    Article  PubMed  Google Scholar 

  • 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 102:2142–2148

    Article  CAS  PubMed  Google Scholar 

  • 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 66:967–973

    Article  CAS  PubMed  Google Scholar 

  • 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 87:662–666

    Article  CAS  PubMed  Google Scholar 

  • Braun PG, Sutton JC (1987) Inoculum sources of Botrytis cinerea in fruit rot of strawberries in Ontario. Can J Plant Pathol 9:1–5

    Article  Google Scholar 

  • Brent KJ, Hollomon DW (2007) Fungicide resistance: the assessment of risk. Fungicide Resistance Action Committee, Brussels, Belgium. http://www.frac.info/docs/default-source/publications/monographs/monograph-2.pdf?sfvrsn=749d419a_8. Accessed 1 Nov. 2018

  • 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 77:1225–1230

    Article  Google Scholar 

  • 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 137:363–376

    Article  CAS  Google Scholar 

  • 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 106:997–1005

    Article  CAS  PubMed  Google Scholar 

  • Daugaard H (1999) Cultural methods for controlling Botrytis cinerea Pers. in strawberry. Biol Agric Hortic 16:351–361

    Article  Google Scholar 

  • Dowling ME, Hu M-J, Schnabel G (2018) Fungicide resistance in Botrytis fragariae and species prevalence in the mid-Atlantic United States. Plant Dis 102:964–969

    Article  CAS  PubMed  Google Scholar 

  • 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 413–486

    Chapter  Google Scholar 

  • 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 28:98–104

    CAS  Google Scholar 

  • 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 97:81–85

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Ortuño D, Grabke A, Li X, Schnabel G (2015) Independent emergence of resistance to seven chemical classes of fungicides in Botrytis cinerea. Phytopathology 105:424–432

    Article  CAS  PubMed  Google Scholar 

  • 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:e42520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 14:1177–1185

    Article  CAS  PubMed  Google Scholar 

  • 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 97:271–276

    Article  CAS  PubMed  Google Scholar 

  • Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91:621–627

    Article  CAS  PubMed  Google Scholar 

  • Hahn M (2014) The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Biol 7:133–141

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 54–56

    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  PubMed  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  PubMed  Google Scholar 

  • 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 67:21–125

    Article  Google Scholar 

  • Jarvis WR (1962) The infection of strawberry and raspberry fruits by Botrytis cinerea Fr. Ann Appl Biol 50:569–575

    Article  Google Scholar 

  • 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 63:888–898

    Article  Google Scholar 

  • Katan T (1982) Persistence of dicarboximide-fungicide resistance in populations of Botrytis cinerea in a warm, dry temperate agroclimate. Phytoparasitica 10:209–211

    Article  Google Scholar 

  • 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 18:235–242

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 84:531–538

    Article  CAS  PubMed  Google Scholar 

  • 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 79:159–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 195–222

    Chapter  Google Scholar 

  • 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 76:6615–6630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 96:1634–1637

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • 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 88:300–306

    Article  CAS  Google Scholar 

  • 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 101:1176–1183

    Article  CAS  PubMed  Google Scholar 

  • 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 86:1019–1024

    Article  CAS  PubMed  Google Scholar 

  • 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 8:2361

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 125:287–294

    Google Scholar 

  • 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 28:104–109

    Google Scholar 

  • Peng G, Sutton JC (1991) Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. Can J Plant Pathol 13:247–257

    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  PubMed  PubMed Central  Google Scholar 

  • 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 20:39–51

    Article  Google Scholar 

  • 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 100:1414–1423

    Article  CAS  PubMed  Google Scholar 

  • Romanazzi G, Smilanick JL, Feliziani E, Droby S (2016) Integrated management of postharvest gray mold on fruit crops. Postharvest Biol Technol 113:69–76

    Article  CAS  Google Scholar 

  • Rosslenbroich H-J (1999) Efficacy of fenhexamid (KBR 2738) against Botrytis cinerea and related fungal pathogens. Pflanzensch-Nachr Bayer 52:127–144

    Google Scholar 

  • 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 7:2075

    Article  PubMed  PubMed Central  Google Scholar 

  • 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–e00217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 22:333–346

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • 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 101:1433–1445

    Article  PubMed  Google Scholar 

  • Weber RWS (2010) Schnelle und einfache Methode zum Nachweis der Fenhexamid-Resistenz bei Botrytis. Erwerbs-Obstbau 52:27–32

    Article  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  PubMed  Google Scholar 

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

  • 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 45–60

    Google Scholar 

  • 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 147:933–936

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Weber RWS, Fried A (2011) Fungizid-Resistenzen bei Botrytis im Beerenobst. Obstb 36:144,167–171

    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, 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 

  • Wilcox WF, Seem RC (1994) Relationship between strawberry gray mold incidence, environmental variables, and fungicide applications during different periods of the fruiting season. Phytopathology 84:264–270

    Article  Google Scholar 

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Funding

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.

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Correspondence to Roland W. S. Weber.

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Weber, R.W.S., Hahn, M. Grey mould disease of strawberry in northern Germany: causal agents, fungicide resistance and management strategies. Appl Microbiol Biotechnol 103, 1589–1597 (2019). https://doi.org/10.1007/s00253-018-09590-1

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