Little Cherry Disease: the “little” disease with big consequences

Ken Eastwell, Plant Pathologist Clean Plant Center Northwest Washington State University - Prosser United States (2012) produced 384,646 metric tonnes with $843M farm gate value  Washington produces 62% (13,759 hectares)*  California produces 23% (12, 545 hectares)  Oregon produces 13% (5,058 hectares)  Small acreage in Michigan, Montana, Idaho, Utah, and New York *Washington yield per acre is greater than other states:  Washington 7.8 tons/acre (17.4 metric tonnes/hectare)  California 3.0 tons/acre (6.7 metric tonnes/hectare)  Oregon 4.5 tons/acre (10.0 metric tonnes/hectare) Canada (2005) produced 6,883 metric tonnes  British Columbia produces 76% (971 hectares)  Ontario produces about 24% (304 hectares)  Small acreage in Nova Scotia, Manitoba and Quebec

Yakima County Grant County Chelan County A different pathogen involved in each case! Little cherry virus 1 (LChV1) Little cherry virus 2 (LChV2) Western X disease phytoplasma (WX) Little cherry virus 1:  Family Closteroviridae  Genus unassigned  Includes: Grapevine leafroll associated virus 7 Mint vein banding-associated virus

Little cherry virus 2 :  Family Closteroviridae Thread-like particles  Genus Ampelovirus  Includes: Grapevine leafroll associated virus 3 Pineapple mealybug wilt-associated viruses 1 and 2 Cytopathology:  Little cherry disease degrades phloem tissue and companion cells

(Raine et al, Phytopathology 1976) LChV2 infected fruit is small, late ripening, poor color and insipid (low sugars and low acid)

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0 Yellow Pink Ripe (-22 days) (-10 days) (Harvest) Degree of fruit symptoms determined by scion:

Sensitive Tolerant Lambert Amber Hedelfingen Bradbourne Black

Royal Ann Dawson Florence Shock symptoms Napoleon Bing Roundel Early Rivers Symptomless Merton Bigarreau

‘Lambert’ ‘Sweetheart’ Premature autumn coloration is unreliable in most cherry cultivars in most years

‘Bing’ ‘Canindex 1’ Stunted growth, decreased annual extension: Horticultural variables: Rootstock affects disease development  Fruit symptoms more severe on P. avium ‘Mazzard’ or F12/1 than on P. mahaleb or P. serotina Warmer weather during ripening partially masks fruit symptoms Shaded portions of tree have milder symptoms Mixed virus infections

Known Prunus hosts: Sweet cherry P. avium Sour cherry P. cerasus Wild bitter cherry (some clones) P. emarginata var. mollis Mahaleb P. mahaleb Des Fontaines cherry P. fontanesiana Pin cherry P. pennsylanica Nanking cherry P. tomentosa Flowering cherry: • ‘Fuji’ P. incisa • ‘Siebold’ P. sieboldii • ‘Kwanzan’ & ‘Shirofugen’ P. serrulata • ‘Higan’ type P. subhirtella • ‘Yoshina’ P. yedoensis ‘Kwanzan’

K&S Disease source Known Prunus non-hosts: Almond P. amygdalus Apricot P. armenianca Western chokecherry P. virginiana Peach P. persica Plum P. domestica  First observed in 1933 in Kootenay Valley, B.C.  More than 30,000 trees within 15 years

Little cherry virus 2 epidemiology:

1969 1933 Little cherry virus 2 transmission: Apple mealybug:  Introduced into Maine from Europe in 1910 . Reported in Kootenay Valley in 1927  No natural control . Reported in Washington in 1994 (R. Miller, 1997)

MB Orchard tree from 30s

1936 Allotropa utilis introduced from Nova Scotia in 1938 to 1943 Released at 11 sites Well established 40-80% parasitism

Why are we experiencing a resurgence? Two consecutive cool springs

Chelan County Photo courtesy Landon Michaelson Mealybug control is difficult:  Hard to scout  Overwinter in crevices, under bark  Tree tops  Usually “not an economic pest”  No existing spray programs in WA

Changes in orchard management:  Movement away from OP’s  Resistance to contact sprays  Effects on parasitoids  Proximity to pear orchards

(E. Beers) Little cherry virus 2 transmission:  Grape mealybug:

 Populations increasing from Southwest

 Confirmed vector of LChV2  Other mealybugs / soft bodied scales?

 GLRaV3 transmitted by wide range of mealybugs and soft bodied scales

 Citrophilus mealybug?

Management of LChV2:  Vector control  Crawlers dispersed long distances:  in wind  on debris  on farm equipment

 Protect parasitic wasps  Caution during tree removal (winter?) (E. Beers) Management of Little cherry virus 2: Plant only virus-free trees (pollinators) Prompt removal and replanting Rogue symptomatic trees and replace

. Be wary of root grafting Remove entire orchard and replant Alternate hosts:

. Bitter cherry (Prunus emarginata)

. Ornamental flowering cherries

. Seedlings

. Choke cherry (Prunus virginiana) is NOT a host

Management of Little cherry virus 2 (cont’d): Pruning? Root grafting? Pollen?

Mandatory control Kootenay Valley Little Cherry Control Program

Year Inspected Infected Removed 1982 4,356 1,910 1,919 1983 3,358 515 575 1984 3,003 386 393 1985 3,748 99 296 1986 3,374 101 11 1987 3,285 101 33 1988 1,692 129 193 1989 2,596 84 100 1990 3,407 148 139 1991 3,654 88 101 1992 3,800 36 94 1993 4,366 113 0 1994 5,201 29 NA 1995 6,050 NA NA Damage to vascular tissue contributes to small fruit: Physiological / Horticultural Winter damage to vascular system Mineral imbalance (Zn+2 deficiency) Pathogens Root or crown rots Virus-like agents (64 diseases)

Diagnostics :  Woody indexing eclipsed by RT-PCR  Developed a Reverse transcription - Recombinase Polymerase Amplification Assay (RT-RPA)  No RNA purification needed

 User -friendly kits available for LChV2 May 2014 (Agdia Inc.) . Mekuria, Zhang, Eastwell. Journal of Virological Methods 205 (2014) 24–30  101= crude extract with GEB3 (Agdia)  102 = 1:10 dilution  103 = 1:100 dilution  104 = 1:1,000 dilution  105 = 1:10,000 dilution  106 = 1:100,000 dilution  107 = 1:1,000000 dilution  108 = 1:10,000,000 dilution Little cherry virus 1

Little cherry virus 1: Contributed to outbreak of little cherry disease in N. Germany during 1980s

Primarily spread by grafting in Europe

Occurs in Washington State and British Columbia

. Relatively low incidence throughout WA State Vector(s) unknown for Little cherry virus 1

Spreads slowly if at all Little cherry virus 1 Symptoms:

Milder than those of Little cherry virus 2

Together, symptoms are very severe Control:

Plant only virus-tested trees

Rogue based on economics (no vector?) Western X disease Western X phytoplasma Specialized bacteria with no cell wall

 Symptoms spread slowly through tree  Reduced extension

 Fruit severely impacted  Bitter taste

“Albino” Western X

Quick decline on Mahaleb rootstock Western X disease  X-disease of peaches subject of 1942 survey

 8,286 symptomatic trees (1.80%) observed

 Incidence varied greatly across counties

Most prevalent “in close proximity to virgin, sagebrush land.” (Coe 1942) First diagnosed in cherry in Washington in 1946 Surveyed in 1947: 170,949 trees inspected; 1,491 symptomatic Highest incidence in desert counties Aggressive tree removal affects disease progression

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Trees infected (%) 0 1947 1948 1949 Year 95% removal 21% removal (Blodgett et al., 1949) Western X phytoplasma transmission: Mountain leafhopper (Colladonus montanus)  Overwinters on winter annual weeds near water  Adults migrate to orchard weeds in late spring  Most abundant in sweet cherry (only) but not preferred host and does not colonize Western X phytoplasma transmission:  Sharp-nosed leafhopper (Scaphytopius acutus)  Cherry leafhopper (Fieberiella florii) Feed on wide range of woody plants Most important species for tree-to-tree spread  Neither species identified in 2004 survey of lower Columbia basin (Munyaneza et al., 2008)

Sharp-nosed leafhopper

Cherry leafhopper Photo by Tom Murray

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Leafhopp P Alfalfa Medicago sativa ------+++ California burclover Medicago polymorpha +++ --- +++ Clovers Trifolium spp. +++ --- +++ Curly dock Rumex crispus ------+++ Dandelion Taraxacum officinale +++ ------Sweet clovers Melilotus spp. +++ --- +++ Cahaba white vetch Vicia sativa x V. cordata ------Other vetches Vicia spp. N/D --- +

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Leafhopp P Almond Prunus dulcis + + --- Bitter cherry Prunus emarginata +++ + --- Boxwood Buxus m. japonica --- +++ --- Chokecherry Prunus virginiana +++ + --- Lilac Syringia spp. --- +++ --- Myrtle Myrtus communis --- +++ --- Peach Prunus persica + + --- Japanese plum Prunus saliciana + + --- Sweet cherry Prunus avium +++ +++ + Western X management:  Remove diseased trees  Most important source  Treat with insecticide before removal  Manage nearby ornamental hosts  Includes chokecherry and bitter cherry  Remove or treat with insecticide  Control weeds that harbor leafhoppers and phytoplasma  Treat orchard for leaf hopper vectors(?) Field diagnosis: Poor colour and size fruit development Poor flavour development Insipid? Bitter? Poor annual shoot extension Absence of winter/trunk injury Multiple limbs involved How quickly do symptoms spread through tree? Area of orchard affected – is it spreading?

Sampling: Best in late season Leaves on 1-year old wood or budwood Close to leader Collect from symptomatic limbs If no symptoms, create composite from each scaffold Removal: Broad spectrum insecticide 5 days in advance Or remove in winter Remove wood from orchard – chipping, burning Monitor (or test) adjacent trees (2 years) http://healthyplants.wsu.edu OR [email protected]