Septoria spot of citrus and California orange exports to South Korea

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Septoria spot of citrus and California orange exports to South Korea Brief overview of a successful fruit certification and export program J. E. Adaskaveg, Professor Department of Plant Pathology and Microbiology University of California, Riverside

Septoria spot of citrus caused by Septoria citri A disease of leaves, fruit, and twigs of oranges, lemons, and grapefruit. Occurs in many citrus-growing countries Early symptoms: Small, irregular, pitted, shallow lesions Advanced symptoms: Dark lesions that extend into the albedo. Pycnidia producing filiform conidia

Economic importance of Septoria spot Septoria spot has generally been considered to be a minor problem In 2004, Korean National Plant Protection and Quarantine Service (NPQS), detected and rejected orange fruit that was infected with Septoria spot from California. S. citri is a quarantine pest in Korea because it has not been reported on the Unshu orange grown in the Cheju province. Korean market a major export market valued at $112 million was jeopardized for the CA citrus industry.

The Navel and Valencia Exports to Korea program (NAVEK) Established through negotiations between USDA APHIS and Korean NPQS to comply with quarantine laws and help the California orange industry maintain trade with Korea NAVEK is part of a Work Plan to certify fruit as diseasefree Accomplishment: Korean market maintained through compliance with quarantine measures following GAPs and fruit certification of NAVEK - currently voluntary (mandatory for 6 / 8 years of program).

The Navel and Valencia Exports to Korea program (NAVEK) - Goals Compliance with quarantine regulations of Korea through: Development of information on forecasting and managing the disease Designing rapid detection methods Certification of disease-free orange fruit destined for Korea Diverting disease-positive fruit to other markets Develop new management strategies

Major accomplishments of NAVEK Numerical Risk Model for forecasting Septoria Spot Precipitation (mm) Hrs with T< -1 C 31-60 61-90 91-120 121-150 151-180 <10 0 1 2 3 4 10-20 1 2 3 4 4 21-30 2 3 4 4 4 >30 3 4 4 4 4 Provided color guides and sampling strategies based on growers and packers evaluating and submitting fruit to lab. Developed molecular-based detection method for Septoria spot to be used in a fruit certification program. Implemented on-line submission forms and confidential reporting system Developed a disease forecasting system and optimal timing of fungicide treatments Identified and evaluated pre- and postharvest fungicide treatments for management of the disease and for inhibition of sporulation

Detection of Septoria spot Development from a fruit incubation test based on visual inspections alone to a molecular-based method that can detect the pathogen accurately in the absence of characteristic signs. S. citri-specific primers Orange-specific primers

Development of a Risk Assessment Model for Forecasting Septoria Spot of Citrus Numerical Risk Model for forecasting Septoria Spot Precipitation (mm) Hrs with T< -1 C 31-60 61-90 91-120 121-150 151-180 <10 0 1 2 3 4 10-20 1 2 3 4 4 21-30 2 3 4 4 4 >30 3 4 4 4 4 Model based on accumulation of low temperature (rind injury) and precipitation (fungal growth) is being used for recommendations of copper/zinc/lime applications. High accumulation of low temperatures (>69 hr < -1 C) & low precipitation (0.8-1.8 in) = High levels of disease Timing of Second Application (1st application Oct. 15 - Jan. 22) Oct 15 to County Date Hrs <-1 Range Pp (mm) Pp Range RISK Fresno 11-Dec 38.3 34-41 19.2 12.6-23.1 1 Tulare 11-Dec 40.5 15-64 25.6 23-28.1 2 Kern 11-Dec 26.0 25-28 19.0 13.7-26 1 Fresno 8-Jan 95.7 85-102 20.44 12.8-23.5 2 Tulare 8-Jan 115.5 62-169 26.4 23.1-28.3 2 Kern 8-Jan 59.7 54-71 19.8 13.8-28 2 Fresno 22-Jan 120.3 103-136 44.8 19.1-35.5 3 Tulare 22-Jan 140.0 81-198 45.9 27.1-30.8 3 Kern 22-Jan 69.7 66-89 21.2 13.8-28 2 Risk Assessment in the 2011-12 Season

Management of the Disease with Fungicides Fungicide applications are protective treatments. Copper-zinc and lime treatments have been part of management guidelines for the disease in California for the past 65 years. Development of alternative treatments - The first field-application of the fungicide treatment of zinc-copper-lime treatment or registered alternative (Quadris Top) is highly recommended for all oranges (Navels and Valencias) planned for exportation to Korea. The treatment should be applied between October 15 and November 30.

Septoria Spot of Citrus Evaluate copper and non-copper alternatives Multi-site fungicides: Micro-encapsulated coppers (e.g., Kocide 3000, Badge, etc.) EBDCs (e.g., maneb, mancozeb) Registration? DMDCs (e.g., ferbam, ziram) Un-registerable Chlorinated hydrocarbons (e.g., chlorothalonil) In IR-4 registration ongoing Single-site fungicides Azoxystrobin Other new active ingredients such as difenoconazole alone or in combination (e.g., QoI and DMI fungicides - Quadris Top). Quadris Top registered in the US and Korea 2011-12. Implement new use strategy for CA growers 2012-13.

Septoria Spot of Citrus Management Pre- and postharvest fungicide treatments Field trials on the evaluation of preharvest treatments Rate Late Fall Winter Spring Trt Form. (400 gal/a) 11-18-10 2-3-11 Inc. (%) LSD Check --- --- --- --- 28.1 A Bravo Weather Stick 720SC 6 pints @ @ 0 B Inspire EC 7 fl oz @ @ Bravo Weather Stick 720SC 3.2 pints @ @ 1 B Quadris 2F 16 fl oz @ @ Kocide 3000 30% MCE 1.65 lb MCE @ @ 1 B Zinc Oxide 35% MZE 2.5 lb @ @ Lime 99% 4 lb @ @ Bravo Weather Stick 720SC 6 pints @ @ 1 B Zinc Oxide 35% MZE 2.5 lb @ @ Lime 99% 4 lb @ @ Quadris Top SC 14 fl oz @ @ 1 B Highly effective treatments for managing Septoria spot: New copper formulations New fungicides (e.g., Quadris Top) with anti-sporulation properties. Mixtures, rotations

Research Objective: Efficacy of fungicides in field studies Single application in early Feb. Rate Winter Spring Trt Form. (400 gal/a) 2-4-11 Inc. (%) LSD Check --- --- --- 8.3 A Bravo Weather Stick 720SC 6 pints @ 2.1 B Inspire EC 7 fl oz @ Bravo Weather Stick 720SC 3.2 pints @ 1 B Quadris 2F 16 fl oz @ Bravo Weather Stick 720SC 6 pints @ 1 B Zinc Oxide 35% MZE 2.5 lb @ Lime 99% 4 lb @ Quadris Top SC 14 fl oz @ 0 B Thiram 75WDG 3 lb @ 2.1 B Zinc Oxide 35% MZE 2.5 lb @ Quadris 2F 16 fl oz 2.1 B Carbamate (Ferbam) 76DF 15 lb @ 1 B Treatments were applied using a dilute application with a handgun sprayer set at 400 gal/a. Single applications of Quadris Top in midwinter (Jan./early Feb.) or in fall (Nov.) were also very effective in 2009/10 and 2011/12, respectively. Plans: Industry guidelines for the management of Septoria spot (CCQC website) have been revised to include alternative fungicides. Fungicide labels have been amended and Korean MRLs are in place.

Anti-sporulation properties of registered or pending pre- and postharvest fungicides Change in quarantine detection criteria for Septoria spot to signs of the fungus Preharvest Postharvest Pre/ post Fruit assays Control Enable 8 fl oz Bravo Weatherstik 192 fl oz Quadris Top 20 fl oz Imazalil 1000 ppm Penbotec 1000 ppm Graduate A+ 16 fl oz Mentor 8 oz f Experiment 1 Experiment 2 cde cde def bcd abc ab a abc Abound 12.8 fl oz ef bc 0 1 2 3 4 0 1 2 3 4 Sporulation rating (0-4) c abc abc abc ab abc a Laboratory agar and fruit studies identified highly effective antisporulation treatments: Pyrimethanil poor Contact multi-site fungicides intermediate New single-site mode of action fungicides propiconazole, QoIs (Abound, Quadris Top) - highest activity

Septoria Spot of Citrus Alternative Treatments for Management Preharvest registrations of multi- and single-site materials Standard - Copper-zinc-lime Registered alternative Quadris Top (noting that other export markets have not established MRLs for a.i. s in Quadris Top. Korean MRLs for Abound (azoxystrobin) and Quadris Top (a mixture with difenoconazole). Full registration for chlorothalonil (Bravo) for all citrus (oranges, lemons, etc.) ongoing IR-4 residue project since 2009 and MRLs exist for chlorothalonil in Korea and Japan Postharvest registrations of single-site materials CODEX MRLs have been obtained in 2009 for azoxystrobin, fludioxonil, and pyrimethanil. Food Additive Tolerance (FAT) for fludioxonil approved in Japan, whereas pyrimethanil and azoxystrobin are pending.

MRL Guidelines Current United States, Codex, and current Korean tolerances of fungicides on orange: Crop Fungicide US Code x Orange Azoxystrobin 10 15 Fludioxonil 10 7 Imazalil 10 5 Difenoconazole 0.6 --- Thiabendazole 10 7 Korea 5 5 5 1 10 China has a 0.2 whereas Hong Kong is ND for difenoconazole.

Develop and modify GAPs and provide information to growers and packinghouse managers on the most effective management strategies for Septoria spot Good Agricultural Practices or GAPs have been developed from the previous Guidelines for the industry in managing Septoria spot in cooperation with industry, UC, and regulatory officials. Same practices followed but changes made from mandatory to voluntary GAPs for Septoria spot management and Color Symptom Guides for disease identification are posted on the CCQC website (www.calcitrusquality.org). GAPs will be modified to incorporate ongoing research on the biology and management of Septoria spot of oranges.

NAVEK Certification Program for Septoria Spot of Citrus Summary for 2011-2012 Navels total Tulare Co. Kern Co. Fresno Co. Madera Co. Valencia 21/300 = 7% 26/241 = 10.8% 0/18 = 0% 25/112 = 22.3% 241/2150 = 11.2% 194/1591 = 12.2% Total samples evaluated: 2262 Zero Detections in Korea in the last two seasons! 0 500 1000 1500 2000 2500 3000 3500 4000 No. samples In the 2009/10 season, only two detections were found in Korea with 1.3% (56) detections out of 4312 samples evaluated.

Summary NAVEK represents an independent certification program separate from the industry & follows Korean Agreement NAVEK is centrally located and has been in operation for 8 years Industry is familiar with program No detections in Korea last year - Certification program could be concluded in two more seasons of zero detections (USDA-APHIS) Justified by sufficient awareness of GAPs & ability to effectively manage disease Research has identified, developed, and registered new fungicides for disease control and to suppress sporulation NAVEK funded through orange industry sample charges

Current Trade Requirements - Key Points of Plant Quarantine Agreement as of July 2010 Work Plan Septoria spot remains a quarantine pest in Korea Korean Inspectors will evaluate fruit for fungal sporulation on import fruit in Korea using standard 2% sampling procedure No incubation of fruit by NPQS No molecular (PCR) testing by NPQS Growers should prevent prevent disease with the application of preharvest fungicides. Risk assessments based on environmental conditions and Disease Forecasts will be made available to the industry. Growers should continued to submit samples for molecular detection that will allow fruit certification from the NAVEK lab Guidelines for Good Agricultural Practices minimize the occurrence of Septoria spot These advances have resulted in a highly efficient & successful program with minimal burden, while maintaining agreements with Korea

Looking Ahead Plans are in place for APHIS to specifically re-visit the NAVEK certification program with Korean NPQS at the end of the 2012-13 season. The goal is to eliminate the certification of fruit lots based on: 1. No detections of Septoria Spot in Korea for several seasons (currently 2 and hopefully 3 seasons). 2. New preharvest treatments developed Quadris Top and Abound High efficacy in reducing the disease incidence Anti-sporulation properties to prevent dissemination 3. New postharvest treatments Graduate A+ High efficacy in reducing the disease incidence Anti-sporulation properties to prevent dissemination 4. Demonstrable industry-wide disease management and GAPS permanently in place.