Resistance of Botrytis to fungicides in California strawberries

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Resistance of Botrytis to fungicides in California strawberries S.D. Cosseboom 1, G. Schnabel 2, K.L. Ivors 1, and G.J. Holmes 1 1 Strawberry Center, California Polytechnic State University; 2 Clemson University, SC

Outline Background of Botrytis resistance to fungicides in strawberry How fungicide resistance develops Current status of resistance in California strawberries Conclusions Disease management options Resistance management strategies

Background Eastern U.S. High levels of resistance to important fungicides for Botrytis gray mold control in strawberries Resistance increasing from year to year Isolates resistant to multiple modes of action California Resistance reported to frequently used fungicides Resistance increasing in a population within a season

Fungicide resistance sensitive individual resistant individual fungicide application regeneration Adapted from: Deisling, H. B., Reimann, S., Pascholati, S. F. 2008. Mechanisms and significance of fungicide resistance. Brazilian Journal of Microbiology. 39:286-295.

U.S. Department of Agriculture, National Agricultural Statistics Service 40 ranches 888 isolates collected 2 sampling times

Production (millions of trays) 20 18 16 14 12 10 8 6 4 2 Northern district Central district Southern district 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Early-season sampling Late-season sampling

Table. Fungicides labeled for Botrytis gray mold of strawberry in California Example trade name Active ingredient(s) FRAC code(s) Topsin Thiophanate-methyl 1 Rovral Iprodione 2 Fontelis Penthiopyrad 7 Kenja 400 Isofetamid 7 Luna Sensation Fluopyram Trifloxystrobin 7 11 Luna Tranquility Fluopyram Pyrimethanil 7 9 Pristine Boscalid Pyraclostrobin 7 11 Merivon Fluxapyroxad Pyraclostrobin 7 11 Scala Pyrimethanil 9 Switch Cyprodinil Fludioxonil 9 12 Elevate Fenhexamid 17 PH-D Polyoxin-D 19 active ingredient was not tested in this study

No fungicide Cyprodinil Iprodione Fludioxonil 1 2 3 4 5 6 Fenhexamid T-methyl Boscalid Fluopyram Penthiopyrad Isofetamid Experimental 1 Experimental 2 Ferna ndez-ortuno, D., Grabke, A., Bryson, P.K., Amiri, A., Peres, N. A., and Schnabel, G. 2014. Fungicide resistance profiles in Botrytis cinerea from strawberry fields of seven southern U.S. states. Plant Dis. 98:825-833.

Boscalid Fludioxonil Fenhexamid Control

100 90 California conventional Early-season (n=340) Late-season (n= 362) Frequency of resistance (%) 80 70 60 50 40 30 20 10 0 T-methyl Iprodione Boscalid Penthiopyrad Isofetamid Fluopyram Cyprodinil Pyraclostrobin* Fludioxonil Fenhexamid 1 2 7 7 7 7 9 11 12 17 Active ingredient FRAC code * Early-season n=73; Late-season n=342

100 90 California conventional Early-season (n=340) Late-season (n=362) 80 Frequency of resistance (%) 70 60 50 40 30 20 10 0 0 1 2 3 4 5 6 *Pyraclostrobin (FRAC 11) not included Chemical class resistances (CCR)

100 90 California organic Early-season (n=92) Late-season (n=94) Frequency of resistance (%) 80 70 60 50 40 30 20 10 0 T-methyl Iprodione Boscalid Penthiopyrad Isofetamid Fluopyram Cyprodinil Pyraclostrobin* Fludioxonil Fenhexamid 1 2 7 7 7 7 9 11 12 17 Active ingredient FRAC code * Early-season n=21; Late-season n=83

Strawberry nursery 100 90 Frequency of resistance (%) 80 70 60 50 40 30 20 10 0 T-methyl Iprodione Boscalid Penthiopyrad Isofetamid Fluopyram Cyprodinil Pyraclostrobin* Fludioxonil Fenhexamid 1 2 7 7 7 7 9 11 12 17 Active ingredient n=10 FRAC code

Summary of results High levels of resistance to thiophanate-methyl, pyraclostrobin and fenhexamid Within-season shift of frequencies of resistance to all fungicides Within-season shift towards isolates resistant to more modes of action Fungicide resistant isolates may be disseminated with strawberry transplant stock

Disease control and resistance management Rotate between modes of action Tank mix single-site with multi-site fungicides Decrease selection pressure Spray less often Weather-based applications Use multisite fungicides or biologicals solo when disease pressure is low Use a recently calibrated sprayer and labeled rates Reduce inoculum Remove senescent foliage and overripe fruit from the field Make the environment less favorable for gray mold Keep the plants dry Fungicides can only prevent gray mold, they do not heal the strawberry

Acknowledgements Funding CDFA Specialty Crop Block Grant Program California Strawberry Commission www.strawberry.calpoly.edu Special Thanks Dr. Guido Schnabel Clemson University ~30 cooperating growers Mark Edsall & Jason Sharrett California Strawberry Commission Sage Finch Pest control advisor Randy Widerburg Pest control advisor Dan Chellemi Driscoll s & Naturipe