Major postharvest diseases of. and their management

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1 Major postharvest diseases of citrus in California and their management James E. Adaskaveg Professor Department of Plant Pathology and Microbiology University of California Riverside, CA, USA

2 California citrus production - Over 100, ha: 70% of acreage is oranges, 17% is lemons - Ranking: - Oranges: 80% of US fresh market production - Lemons: 90% of US production - Tangerines, mandarins, clementines: increasing acreage - Major export markets: Canada, Asia, Japan Korea, Mexico

3 California citrus production Crop Acreage Value (x10 6 ) Navel oranges 135,000 A $ million cartons ($7/carton) Valencia oranges 46,000 A $ million cartons ($8/carton) Lemons 44,000 A $ million cartons ($12/carton) Tangerines 14,000 A $ million cartons ($11/carton) Grapefruit 11,500 A $79-12 million cartons ($7/carton) Total Value $1.1 Billion

4 Important pre- and postharvest fungal diseases and disorders of citrus in California Disease Brown rot Septoria spot Anthracnose Cause Phytophthora spp. Septoria citri Colletotrichum gloeosporioides Clear rot, Green/Blue mold Sour rot Penicillium spp. Galactomyces citri-aurantii Stem- /Blossom-end rot Alternaria, Botryosphaeria spp., etc. MRD Environmental conditions All are high-rainfall diseases disease incidence in most years is relatively low.

5 Fruit decays initiated preharvest Brown rot caused by Phytophthora spp. Infection through intact tissue. Alternaria decay caused by Alternaria sp. Tear stain and anthracnose caused by Colletotrichum gloeosporioides Stem end rot caused by Botryodiplodia theobromae

6 Symptoms and signs of Septoria spot on orange fruit Pycnidia are formed within the dark lesions. Conidia are exuded in spore tendrils.

7 Fruit decays initiated at or after harvest Penicillium decays wound pathogens Green mold caused by Penicillium digitatum (most important on citrus) Blue mold caused by Penicillium italicum Penicillium soilage

8 Postharvest decays of citrus: Sour rot caused by Geotrichum citri-aurantii Second most important postharvest disease of citrus Pathogenic on weak, wounded, bruised, and split fruit Infects all citrus species but due to long-term storage is especially prevalent in lemons and grapefruit. Chilling stimulates infection

9 Integrated Postharvest Disease Management Postharvest decay control utilizing ing a variety of complementary disease management strategies. May include but not limited to: Handling procedures Spore exclusion and sanitation Use of sanitizers and fungicides Temperature management Monitoring inoculum levels and fungicide resistance

10 Postharvest fungicide treatments as a component of postharvest handling Example: Lemons in California Fruit arrival Sorting Chlorine wash, soda ash treatment, water rinse Application of pp fungicide and fruit coating

11 Usage of borax, sodium carbonate (soda ash), and sodium bicarbonate in postharvest treatments of lemons Wash with chlorine and ddetergent soda ash tank Direction of fruit movement

12 Usage of borax, sodium carbonate (soda ash), and sodium bicarbonate in postharvest treatments of lemons Treatment with heated soda ash Water rinse after soda ash treatment

13 Storage wax application Pack wax application Bulk packing in bins Boxing, shipping, marketing Storage for up to 3 months

14 Chlorine wash after storage Sorting Boxing and marketing Fungicide and pack wax application

15 Current and future postharvest fungicides for decay control of citrus in the US Phenols Sodium ortho-phenyl phenate (SOPP) Benzimidazoles Thiabendazole (TBZ) DMI-imidazoles Imazalil (Deccocil, Freshgard, Fungaflor) Anilino- pyrimidines Phenylpyrroles ypy QoIs DMI-triazoles Pyrimethanil* (Penbotec) Fludioxonil* (Graduate) Azoxystrobin* (Diploma) Propiconazole ? * Reduced d risk fungicides id is an EPA classification of a pesticide id with: 1) Low environmental impact 3) Compatible with IPM programs 2) Greater human and animal safety 4) Used at lower rates

16 Efficacy of old and new 'reduced-risk' fungicides against postharvest decays of citrus Fungicide Common Name Green Mold* Blue Mold Sporulation Control Sour Rot Imazalil Imazalil +++ S /+ R Thiabendazole TBZ +++ S /+ R SOPP SOPP ++ S /+ R Pyrimethanil Penbotec Fludioxonil Graduate/ Scholar Azoxystrobin Diploma Propiconazole (In development) ? *- No multiple-resistance: Azoxystrobin, fludioxonil, and pyrimethanil are effective against decay caused by TBZ- or imazalil-resistant Penicillium populations.

17 Current Challenges in Managing Postharvest Decays of Citrus in California Penicillium decays Imazalil and TBZ: wide-spread resistance Imazalil Old EC formulations must be phased out, new formulations must be phased into usage New fungicides Codex MRLs and Japanese food usage tolerances pending for azoxystrobin, fludioxonil, & pyrimethanil Propiconazole is being developed Best usage strategies are being developed Understanding resistance potential Resistance management strategies need to be implemented

18 Current Challenges in Managing Postharvest Decays of Citrus Sour rot (Geotrichum citri-aurantii) Improved understanding di of the biology Biological and molecular species identification Population dynamics Understanding resistance potential Propiconazole development Efficacy and usage strategies Septoria spot Preharvest treatments for postharvest control Postharvest treatments Brown rot (Phytophthora spp.) New materials

19 Efficacy of new fungicides against Penicillium decays Understanding Performance: Contact vs. Systemic

20 Timing of post-inoculation treatments with Scholar Control 9 h after inoculation 12 h after inoculation 15 h after inoculation Treatments with aqueous solutions of 1,000 ppm Scholar

21 Time effect in controlling citrus green mold - Treatments selected times after inoculation - S R Flu Flu Inoculated fruit studies - P. digitatum sensitive (top) or resistant (bottom) to imazalil and TBZ Spray treatments selected times after inoculation Fungicides: each at 1,000 ppm Treatment time after inoculation (h) Incidence of decay in the controls was >90% Fungicides with systemic activity (azoxystrobin, imazalil, TBZ, pyrimethanil) have a longer post-infection activity than Scholar.

22 Sporulation Control and Optimizing treatment efficacy Compatibility with fruit coatings Fungicide application methods

23 Effect of fruit coatings on the efficacy of postharvest fungicides for sporulation control Inoculated fruit studies - P. digitatum resistant to imazalil and TBZ 30 sec dip treatment Fungicides: each at 500 ppm Storage coating: 1:15 dilution Efficacy of Scholar and Diploma for sporulation control is increased when applied in storage fruit coating. Pyrimethanil does not control sporulation. Control Azoxystrobin Fludioxonil Pyrimethanil Imazalil Control Azoxystrobin Fludioxonil Pyrimethanil Imazalil c Control c d Aqueous application a c b a Storage fruit coating a Sporulation Rating b Fludioxonil in storage coating a

24 Addition of sodium bicarbonate improves fungicide efficacy and extends post-infection activity Control Fludioxonil SBC Fludioxonil + SBC d c b 14 h a Inoculated fruit studies - Dip-treatments 14 or 24 h after inoculation Fludioxonil at 500 ppm, SBC at 3% (w/v) Control a Fludioxonil b SBC b 24 h Fludioxonil + SBC c Decay incidence (%) Efficacy of Scholar is increased when applied in mixture with sodium bicarbonateb Control Fludioxonil + SBC

25 Application methods for postharvest fungicide treatments Flooder CDA

26 Comparative efficacy of postharvest application methods Azoxystrobin Fludioxonil Pyrimethanil a b Drench CDA/Brushes b CDA/Rollers In-line drench (flooder) applications provide the highest efficacy. a b b a b b Standardized improved efficacy (%) Efficacies for each fungicide were compared to the least efficient application method. Statistical comparisons of application methods were done for each fungicide.

27 Summary 1. Fungicide properties: contact vs. systemic determines treatment timing 2. Anti-sporulation activity: important characteristic for stored fruit. 3. Mixtures of fungicides, or of fungicides with sanitizers or other treatments (e.g., SBC) 4. Application methods: Treatments are best done as staged postharvest applications - Aqueous application followed by an application in fruit coating.

28 FUNGICIDE RESISTANCE MANAGEMENT IN CITRUS A Coordinated Effort for the Prevention of Fungicide Resistance with the Widespread Use of New Pre- and Postharvest Fungicides in Citrus All new fungicides, including Scholar, should be considered high risk for developing resistance. Avoid what happened with TBZ and imazalil

29 Fungicide resistance management for postharvest decays of citrus fruit A high risk for resistance development in postharvest pathogens of citrus fruit: Treated fruit are sometimes stored for long periods and the pathogen is exposed to the fungicides. Sometimes repeated treatments of the same fruit lot The pathogens produce abundant spores. All postharvest fungicides are single-site mode of action materials. Many parallels to postharvest aspects of pome fruit.

30 Resistance development in pathogen populations Recipe for resistance development: Large amount of pathogen propagules Low fungicide concentration Repeated exposure to the fungicide Resistance development is optimal + development + = Populations of Penicillium spp. in packinghouse can be high. Sporulation often not inhibited by posth. fungicides. Sub-optimal application method. Equipment not calibrated. Cost-saving. Long-term exposure in storage. Fruit re-packing and second fungicide application. Resistance management strategies target these factors by using optimal application methods, fungicide mixtures, and sanitation procedures that minimize the pathogen population that is being exposed and the number of survivors after treatment.

31 Method for detecting rare resistant variants within a population Selection plates amended with a fungicide concentration gradient used for air-sampling EC 95 for mycelial growth Pd s Pdi P. digitatumit t Air sampling radially streaked plate with P. on a plate with a digitatum (EC 95 fungicide conc. concentration gradient indicated) (e.g. imazalil)

32 Method for detecting rare resistant variants within a population Exposure of selection plates in a packinghouse

33 EC 95 Summary: Resistance potential and characterization of resistant isolates of P. digitatum Azoxystrobin* Fludioxonil Pyrimethanil Lab selection No Yes Yes Field selection No Yes Yes Pathogenicity it - ++/ Resistance factor - HR 1,577 ppm MR = 3 26 ppm > 255 Res. frequency Codes: - : not applicable; +++: Highly pathogenic; ++: Moderately pathogenic. * Isolates of P. italicum resistant to azoxystrobin were commonly found

34 Trends in postharvest fungicide registrations in the US: Pre-mixtures Imidazole Imazalil + Anilinopyrimidine = pyrimethanil Philabuster citrus - registered Phenylpyrrole Fludioxonil QoI + Azoxystrobin = Graduate A+ citrus - registered Fludioxonil Azoxystrobin SBI + Propiconazole + = Citrus in development

35 Use of fungicide mixtures: The resistance potential of fungicide mixtures is lower than for single active ingredients Single applications Resistance frequency of Mixture applications (i.e., Graduate A+) pyrimethanil (Rf pyr ): 10-4 Rf = mix Resistance frequency of fludioxonil o (Rf fld): Each application is still a selection event, but the probability for changes to occur concurrently at independent loci is lower than for a single locus.

36 Septoria spot of citrus caused by Septoria citri Adi disease of fleaves, fruit, and dtwigs 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.

37 Economic importance of Septoria spot Negotiations between USDA- APHIS/UC researchers and Korean officials in the fall of Further detection of diseased fruit in Korea could result in closure of this important export market. Disease levels in export fruit have to kept tto an absolute minimum. i Citrus industry representatives thought the Septoria quarantine was in retaliation against the US quarantine against Korean citrus because of citrus canker

38 NAVEK Program - Integrated approach to minimize the occurrence of Septoria spot on oranges for export Guidelines Field applications with copper/zinc/lime 1 st application calendar-based 2 nd and 3 rd appl. based on environmental conditions (using the Septoria Risk Assessment Model) Color Guides Guidelines Survey of orchards for symptomatic fruit by field personnel Sampling Frequency, Sample Size, and Harvest Detection procedures Guidelines Fruit sample evaluation for disease detection - Pre-screening, Incubation and Molecular assays - Communication of results to CCQC, packinghouses, APHIS Postharvest fungicide applications Shipment requirements

39 Table 1. Summary of Septoria spot positive fruit lots detected in the CCIP or NAVEK programs and by the Korean National Plant Quarantine Service during the 2004/2005 to 2009/2010 seasons CCIP/NAVEK program Korea Incidence of Incidence of Total samples samples positive for samples positive for Season Variety processed Septoria spot (%) Septoria spot (%) Navel Valencia Navel Valencia Navel Valencia Navel Valencia Navel /0.95* Valencia Navel Valencia * The higher value includes 17 fruit lots declared positive by NPQS but that were disputed by NAVEK.

40 In vitro toxicity of fungicides against S. citri Spiral gradient dilution assay Fungicide EC 50 mycelial growth Mycelial strip Conidial streak TBZ Azoxystrobin Azoxystrobin 0.01 ppm Difenoconazole 0.02 ppm Mancozeb 0.06 ppm Imazalil 0.10 ppm Chlorothalonil 0.16 ppm TBZ ppm Fludioxonil 0.45 ppm Pyrimethanil >10 ppm Among the fungicides evaluated, azoxystrobin, was the most effective material. (Azoxystrobin will be soon be registered for postharvest use on citrus in CA).

41 Evaluation of copper alternatives for management of Septoria spot of oranges Control a Kocide lb ab Bravo pints b Bravo pints b Ziram 76W 8 lb b Dithane M45 8 lb b Disease incidence (%) Orange fruit were wounded, ddtreated, td inoculated, and incubated for 7 weeks at 20C. Possible copper alternatives were identified. Residue trials for chlorothalonil (Bravo Echo) were approved Residue trials for chlorothalonil (Bravo, Echo) were approved for a possible registration on citrus.

42 The collision between regulatory agencies and the California citrus industry USDA-APHIS Allow export of US commodities UCR NPQS Korea Prevent importation of a quarantine disease Citrus growers and associations, CCQC (California Citrus Quality Council) Market citrus fruit

43 The collision between US and international regulatory agencies and US citrus industries USDA-EPA New fungicide registrations (IR-4, New requirements for tolerances) FDC (Florida Dept. of Citrus) Prevent importation of a quarantine disease NPQS Korea Prevent importation of a quarantine disease USDA-APHIS Allow export of US commodities UCR Korean Dept. Food &Ag Ag. Revision of standards & specs for food (MRLs) CDFA (CA Dept. Food & Ag.) Allow export of CA commodities Citrus growers and associations, CCQC (California Citrus Quality Council) Market citrus fruit

44 Tradi- tional New National and international tolerances of postharvest fungicides on citrus Fungicide Active Tolerance/MRL (ppm) Lemon, Orange, Grapefruit Hong Trade Name Ingredient Codex US Japan Korea Kong Taiwan TBZ Thiabendazole 7,7,7 10,10,10 10,10,10 10,10,10 Codex 10,10,10 Deccocil, Fungaflor, Freshgard SOPP SBC Imazalil 5,5,5 10,10,10 5,5,5 5,5,5 Codex 2,2,2 Sodium o- phenylphenol Sodium bicarbonate 10,10,10 10,10,10 10,10,10 10,10,10 Codex 10,10,10 Diploma Azoxystrobin 15,15,15 10,10,10 No FA 0.5,0.5,0.5 Codex 1,1,1 Graduate Fludioxonil 10,10,10 10,1,101 No FA 0.5,0.5, Codex 1,1,11 1 Graduate A+ Azoxystrobin/ Fludioxonil 15,15,15/ 10,10,10 see above No FA 0.5,0.5,0.5 / 0.5,0.5,0.5 Codex 1,1,1 / 1,1,1 Penbotec Pyrimethanil il 777 7,7,7 11,10, No FA ,0.5,0.5 Codex -,-,- Philabuster Pyrimethanil/ Imazalil 7,7,7/ 5,5,5 11,10,10/ 10,10,10 No FA 0.5,0.5,0.5 / 5,5,5 Codex -,-,- / 2,2,2

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