J. E. AdaskavegUniversity of California, Riverside

Phytophthora Brown rot of Citrus - A Quarantine Issue for Fruit Exports to China -

- GAPS for Managing Brown Rot -

H. Forster and W. HaoUniversity of California, Riverside

Cooperating

Historically primary species:P. citrophthora - fall, winter, springP. parasitica (P. nicotianae) - summer

Phytophthora diseases of citrus trees

Foot rot & Gummosis

Root rot

Tree decline, dieback, yield reduction

Healthy tree

Citrus Brown Rot

- P. citrophthora- P. syringae- P. parasitica (P. nicotianae) - P. hibernalis

Causal pathogens: species ofPhytophthora

Occur in all growing regions in CA.P. citrophthora is considered most important.The four species also cause Phytophthora root rot, foot rot, and gummosis.Losses are associated with periods of high rainfall.

Citrus Brown Rot – Symptoms and Economic Impact

• Develops mainly on mature fruit in the lower tree canopy

• Olive-brown discoloration of the rind• Distinctive pungent odor• Fruit remain firm and leathery, unless invaded by

secondary decay organisms. • At high humidity, fruit become covered by white

growth of the fungus.• Fruit infected before harvest may not show

symptoms. If infected fruit get mixed with healthy fruit, the disease may spread quickly from fruit to fruit in storage and during transit.

• Citrus brown rot: pre- and postharvest losses

Brown rot caused by Phytophthora spp. infection through intact tissue.

Historical distribution of Phytophthoradiseases of citrus in California

Phytophthora diseases of citrus occur throughout California

Survey area

Disease cycle of Phytophthora species

• 18 h of wetness required for sporangia production and zoospore release.

• 3 h of wetness required for infection.

• Zoospores produced in sporangia on the ground may be splashed up onto low-hanging fruit and the trunk. Brown rot mainly develops on fruit growing near the ground.

• Continuous rainy periods are important in forecasting brown rot epidemics.

• Inoculum levels in orchards determines severity of infections.

9 hr at 10 C 4 hr at 20 C 4 hr at 20 C

Cyst

GermTube

AppressoriumInfection hypha

Infection hypha

Germtube

Cyst

Wetness and temperature effects on infection of Navel oranges by P. citrophthora

• Zoospores encysted within an hour at incubation at 20C. • Germ tubes were observed after 1 h.

Fruit inoculation studies at 20C: 1 h wetness - no disease1.5 h wetness - 10% incidence2 h wetness - 70% incidence

Experiments with P. syringae pending

Phytophthora syringae is an ongoing regulatory issue in the exportation of California orange fruit to China.

Summary Part I- Phytophthora brown rot in CA• P. citrophthora, P. syringae, P. hibernalis, and P. parasitica

are responsible for brown rot of citrus in California. • P. citrophthora and P. syringae are most common.• Copper is the cornerstone for disease management• Phosphonates are effective as pre- and postharvest

treatments for the management of brown rot but cannot be used because there are no MRLs in China.

• New fungicides are in development.• Management practices historically included preharvest

copper applications (postharvest applications with phosphonates are proposed).

• Integrated strategies required to open China market.

Industry’s response• Improved understanding of Phytophthora root rot and

brown rot: – Species: P. syringae, potentially P. hibernalis (quarantine reasons)

• New product registrations for management of brown rot & root rot

• Characterize new treatments - guidelines for usage• GAPs prepared for industry-wide meetings -

– Guidelines to manage Phytophthora brown rot– Information on how to meet Chinese export agreement (2-yr pilot

program)– Management: Efficacy of preharvest cultural practices and pre-

and postharvest chemical treatments is cumulative and warrants a “systems approach” for control of Phytophthora brown rot of citrus.

Good Agricultural practices (GAPs) for the Management of

Phytophthora Brown Rot

http://calcitrusquality.org/wp-content/uploads/JEA-Brown-Rot-GAPs-Citrus20141.pdf

http://calcitrusquality.org/export-issues/

Management of Phytophthora Diseases•Cultural practices

• Resistant rootstocks• Planting on berms for

adequate drainage• Avoid over-irrigation

• Alternate side irrigation• Drainage tiles

• Skirting of trees – 24 in• Fumigation

•Surfactants•Fungicides

• Preharvest• Postharvest

P. citrophthora releasing zoospores

Management of Phytophthora Diseases - Rootstocks

Type Rootstock Root rot GummosisLemon Macrophylla Tolerant Tolerant

Rough lemon Susceptible SusceptibleVolkameriana Susceptible Susceptible

Yuma ponderosa Tolerant TolerantOrange Taiwanica Susceptible Tolerant

Sour orange Intermediate TolerantSweet orange Susceptible Susceptible

Trifoliate Tolerant TolerantHybrids C-35 citrange Tolerant Tolerant

C-32 citrange Tolerant TolerantCarrizo citrange Intermediate TolerantTroyer citrange Intermediate Tolerant

Swingle Tolerant Tolerant

Source: UC ANR Publication 21477

A

B

Single-line microsprinklersystem

Dual-line microsprinklersystem

Alternate Side Irrigation to Control of Phytophthora Root Rot

AlternatingIrrigation

Management of Phytophthora Brown Rot- Preharvest Fungicide Sprays -

Current guidelines:- First spray of copper fungicide between October and

December before or just after the first rain.

- Apply at 200-600 gal/A (lower 4 ft of tree > whole tree).

- If frequent and high rainfall occurs after the first application, repeat applications in January or February.

- Spray the skirts to about 4 feet above ground; whole tree applications may be necessary for some varieties or in orchards with a history of the disease or for management of P. hibernalis.

- Spraying the ground underneath the trees may also reduce brown rot infections.

Objective: Persistence of new preharvest treatments for control of brown rot caused by Phytophthora spp.

Field applications

• Revus (Mandipropamid), Prophyt (phosphorous acid), and Badge-Lime (copper oxychloride- copper hydroxide) were very effective when fruit were harvested 2 wk after application.

• After 3 wk, Presidio was no longer effective, efficacy of Prophyt was reduced after 4 wk.

• Copper effective for ca. 6 wk; whereas Revus was still very effective for 8 wk.

2 w

k

3 w

k

4 w

k

5 w

k

6 w

k

7 w

k

8 w

k0

20

40

60

80

100ControlPresidio 4 fl ozProphyt 64 fl ozBadge SC 128 fl oz + Lime 16 lMandipropamid 8 fl oz

Note: Presidio was not evaluated after 4 wks.

Management of Phytophthora Brown Rot- Preharvest fungicide sprays -

Most effective orchard sprays:•Bordeaux mixture (copper sulfate + lime) with 1.6 to 2.4 lb of metallic copper/A. (0.6-0.8 MCE/100 gal)•Neutral (fixed) coppers (copper hydroxide, copper oxide, …) see label (0.6-2.4 MCE/A)

•Phenylamides (e.g., mefenoxam) – Ridomil Gold 0.5-3 qt/A applied to soil

•Phosphonates (e.g., fosetyl-al - Aliette 5 lb/A, potassium phosphite - Prophyt 4 pints/A, etc.)

Not approved in China.

TABLE 1 First Application 2014-15 Season Zinc-Copper-Lime Applications

Fixed coppers (e.g., copper hydroxide and copper oxide) Application

Volume Metallic

Zinc/100 gal Metallic

Copper/100 gal Hydrated

Lime/100 gal 200 gal/A 1.25-2 lb 0.83-1.5 lb 1.0-2 lb 400 gal/A 0.63-1 lb 0.41-0.75 lb 0.5-1.0 lb 600 gal/A 0.42-0.67 lb 0.28-0.5 lb 0.33-0.67 lb

Total* lb/A 2.5-4 1.65-3 2-4

* - If brown rot was observed in a grower lot last season, use a higher rate of each spray component within the range provided. ** - Note that other fungicides can be used in rotation with copper.

TABLE 2 First Application 2014-15 Season

Zinc-Copper Bordeaux Applications (Zinc monohydrate + Copper pentasulfate)

Application Volume

Metallic Zinc/100 gal

Metallic Copper/100 gal

Hydrated Lime/100 gal

200 gal/A 1.65 lb 0.83-1.23 lb 10-34 lb 400 gal/A 0.83 lb 0.41-0.62 lb 5-17 lb 600 gal/A 0.55 lb 0.28-0.41 lb 3.3-11 lb

Total* lb/A 3.3 1.65-2.45 20-67

* - If brown rot was observed in a grower lot last season, use a higher rate of each spray component within the range provided. ** - Note that other fungicides can be used in rotation with copper.

Recommendations for copper sprays

Always check labels for rates.

Models for industry-wide forecasting of brown rot and timing of fungicide applications

1. Prediction of infection periods

Numerical risk model for forecasting brown rot caused by Phytophthora syringae based on cardinal temperatures, temperature range for growth, and wetness periods.

Numerical risk model for forecasting brown rot caused by P. syringae

Wetness period (h)

Temperature range (°F)

Temperature range (°C) <10 10-18 18-25 >25

<41 <5 0 0 0 0

>41-50 5-10 1 2 2 3

>50-68 >10-20 1 2 3 3

>68-77 >20-25 1 2 2 3

>77 >25 0 0 0 0

Models for industry-wide forecasting of brown rot and timing of fungicide applications2. Persistence of copper applications

Agroclimate - Citrus Copper Application Scheduler (A) and overview (B). Weather station or uploaded weather data (C) can be used for different citrus crops with their bloom date (D). Application attributes are entered for dates of application, amount of copper, volume of application (E).

Models for industry-wide forecasting of brown rot and timing of fungicide applications

3. Risk assessment of orchards

Field monitoring - monthly or within 14 days after every major rainfall, and one week before each harvest.

Rating Category China Export1 Low risk: <10 fruit with brown rot per acre  Shipped 2 Moderate risk: 10‐20 fruit with brown rot per acre Caution if shipping 3 High risk: >20 fruit with brown rot per acre  Ship to other markets

Risk categories for monitoring orchards for Phytophthora brown rot based on field surveys of 50 orchards

Summary Part II - Implementation of Agreement• Two approaches to solving Phytophthora brown rot for

orange export to China –• Preharvest management practices –

– Tree skirting (UC Guidelines - 24 in) (61 cm); – Fruit harvested above 20 in (50 cm) are sent to China (lower

fruit sent to other markets)– Foliar and fruit applications with copper (1st application mand.)– Development of new fungicides for season-long control– Managing soil populations of pathogens and root rot control

with fungicides – (e.g., mefenoxam), tolerant rootstocks– Monitoring orchards and forecasting environmental conditions

conducive for disease and removal of copper• Postharvest treatment – Future registration in China

– Potassium phosphite (Not available for this season)• New guidelines currently being discussed by APHIS

(USA) and AQSIQ (China)

A. Potassium phosphite (Not available)• Potassium phosphite is registered for postharvest use on domestic

fruit and for countries that have MRLs for postharvest usage. • China is currently registering potassium phosphite for postharvest

use. At this time, fruit should NOT be treated postharvest with potassium phosphite or other phosphonate fungicide.

B. Fruit may be treated with registered postharvest fungicides for management of green and blue mold (Penicillium decays). • Aqueous treatments of imazalil (e.g., Fungaflor, Deccocil,

Freshgard, etc.), pyrimethanil (Penbotec), sodium bicarbonate, TBZ (Alumni), or other registered fungicide should be applied prior to a fruit coating or wax.

• Fungicides including imazalil, pyrimethanil, and/or TBZ may also be applied in a fruit coating. Currently, MRLs for azoxystrobin and fludioxonil have not been established in China.

Postharvest Fungicides

Crop Imazalil Pyrimethanil TBZOrange 5 7 10Lemon 5 7 10

China MRLs

Postharvest Heated-Water Treatments

Temperature (°C/F)

48 50 52 54 56 58 60 62

Red

uctio

n in

dec

ay in

cide

nce

(%)

-40

-20

0

20

40

60

80

100

120y = -409 + 8.4xr2 = 0.996 P <0.038

118 122 125 129 132 136 140 143

• Fawcett (1936) - 2-min dips at 49C (30 h after inoculation)

• Klotz and DeWolfe(1961) - 4-min dips at 48C after 48 h at 25C or 60 h at 12C after inoculation.

• Adaskaveg et al. (2015) linear response for reduction in decay from 50 to 60C (24 h after inoculation at 20C). Fig. to right

Note: Dip temperatures are for fungicide reservoir solutions. Dip times were 15 sec.

Treatment time after inoculation (h)20 25 30 35 40 45 50

Red

uctio

n in

bro

wn

rot i

ncid

. (%

)

0

20

40

60

80

100

120

K-phosphite - ambientImazalil+K-phosphite - heatedy = 159 - 2.4x, r2 = 0.95, P < 0.01y = 153 - 2.2x, r2 = 0.94, P < 0.01

Postharvest Heated-Phosphite Solutions Adaskaveg et al. (2015) linear response for reduction in decay using heated or ambient solutions of phosphite from 24 to 48 h after inoculation at 20C). Fig. to right

Grading - All fruit destined for China should be graded. 1. Fruit with symptoms of brown rot should be identified and

reported to packinghouse managers.2. If fruit lots are confirmed to have brown rot, the lots should not

be further considered for export to China. Phytosanitary inspection prior to export –

1. APHIS will apply a 0% tolerance for any type of decay during inspection. Any grower lot displaying decay of any kind (brown rot, green mold, sour rot, etc.) will be rejected and not certified.

2. All fruit lots that pass inspection shall be provided with a Phytosanitary Certificate and state the additional declaration:

“This shipment complies with ‘The Protocol of Phytosanitary Requirements of California Citrus exported to China’ and ‘Supplementary Inspection and Quarantine Requirements for California Citrus to be Exported to China’.”

Regulatory Aspects

Good Agricultural practices (GAPs) for the Management of

Phytophthora Brown Rot

http://calcitrusquality.org/wp-content/uploads/JEA-Brown-Rot-GAPs-Citrus20141.pdf

http://calcitrusquality.org/export-issues/

Fungicide treatments ………for brown rot control:1) Fungicide treatments can protect fruit from infection by

Phytophthora spp. Multiple treatments may have to be applied during the harvest season.

2) The first protective application is mandatory and must be a registered copper compound and must be done after the first rain to all citrus planned for exportation to China. …October 15 and November 30.

3) Second and third applications may be needed 4) Registered fungicides include fixed coppers, Bordeaux

mixtures, and mefenoxam (this latter fungicide is used as a soil treatment) can be used. Phosphites not allowed at this time.

5) Foliar applications of copper sprays - effective for ca. 6 weeks. 6) Pesticide Use Reports should be available.

GAPs - Fungicides

Timing of additional fungicide applications:1) Based on rainfall and when copper residues are significantly

depleted.2) Based on empirical forecasting model - numerical risk based

on cardinal temperatures (i.e., minimum, optimum, and maximum temperatures) and wetness periods for growth and sporulation of P. syringae.

Monitoring guidelines:1) All grower lots must be field scouted for brown rotted fruit.2) Risk assessment:a)Low risk: <10 diseased fruit/A – OK to ship to Chinab)Moderate risk: 10-20 diseased fruit/A - Caution in shippingc)High risk: >20 diseased fruit/A – Do not ship to China3) Frequency – Monthly or within 14 days after rainfall or 7 days

before harvest.

GAPs – Timing of Fungicides and Monitoring

Potential Changes for Next Season • Whole-tree fungicide applications -

• Phytophthora hibernalis detected - second quarantined pathogen detected along with P. syringae.

• Stricter requirements –• Documentation (checklists & records: orchard,

spray, harvest, etc.) • Tree Skirting• Harvesting and segregation of fruit (low fruit)• Monitoring, sampling, and certification

• Diseased fruit vs. soil?• Postharvest heated water treatments?

Questions?