18 diseases of apple - cabi.org

18 Diseases of Apple

Gary G. Grove1, Kenneth C. Eastwell1, Alan L. Jones2 and Turner B. Sutton31Irrigated Agriculture Research and Extension Center, Washington State University,

Prosser, Washington, USA; 2Department of Botany and Plant Pathology, Michigan StateUniversity, East Lansing, Michigan, USA; 3Department of Plant Pathology, North

Carolina State University, Raleigh, North Carolina, USA

18.1 Introduction 46018.2 Diseases Caused by Bacteria 460

18.2.1 Fire blight 46018.3 Diseases Caused by Fungi 468

18.3.1 Apple scab 46818.3.2 Powdery mildew 47018.3.3 Brown-rot diseases 47218.3.4 Summer diseases 47318.3.5 Phytophthora crown and root rot 47618.3.6 European or Nectria canker 477

18.4 Postharvest Diseases 47718.4.1 Blue mould 478

18.5 Diseases Caused by Viruses, Viroids, Phytoplasmas and Other Virus-like Agents 47818.5.1 Chlorotic leaf spot 47918.5.2 Apple decline (on ‘Virginia Crab’) 48018.5.3 Flat apple 48018.5.4 Apple mosaic 48118.5.5 Stem pitting 48118.5.6 Union necrosis 481

18.6 Diseases Caused by Phytoplasmas 48218.6.1 Proliferation 48218.6.2 Chat fruit 482

18.7 Diseases of Apple Caused by Viroids 48218.7.1 Blister bark 48218.7.2 Dapple apple 48318.7.3 Dimple fruit 48318.7.4 Fruit crinkle 483

18.8 ’Virus-like’ or Graft-transmissible Diseases of Apple with No Known Causal Agents 48318.8.1 Green crinkle 48418.8.2 Rubbery wood 48418.8.3 Dead spur 485

18.9 Control Measures 485

© CAB International 2003. Apples: Botany, Production and Uses (eds D.C. Ferree and I.J. Warrington) 459

Apples - Chap 18 21/3/03 3:03 pm Page 459

18.1 Introduction

Apples are host to over 70 infectious dis-eases, the vast majority of which are causedby pathogenic fungi (Table 18.1). Apples arealso susceptible to diseases caused by bac-teria, phytoplasma and virus/virus-likeagents. The authors discuss several but notall economically important pre- and posthar-vest apple diseases in this chapter. Readersshould keep in mind that some of the dis-eases discussed might be major in someareas and minor in others. Others (e.g. fireblight) are of importance or potential impor-tance wherever apples are grown. In mostapple-producing regions, disease control is amajor annual expense for the grower. Forexample, in the eastern USA, the manage-ment of apple scab can require eight to tenprotective fungicide applications annually. Inthose areas, the apple grower must manageearly-season diseases, such as apple scab andcedar apple rust, as well as a group of dis-eases termed ‘summer diseases’. Conversely,in the arid production regions of the PacificNorthwest, these diseases are non-existent orsporadic in nature and powdery mildew ismuch more problematic.

Successful disease management usuallyresults from the integration of several meth-ods of disease control. The use of resistantrootstocks and scions, fungicides, bacteri-cides, biological control agents, environmen-tal modification and site selection are someof the means used to control apple diseases.The precise combination and order of controlmeasures are usually disease-specific.

18.2 Diseases Caused by Bacteria (Table 18.2)

Fire blight, blister spot, blister bark, crowngall and hairy root are diseases of applecaused by bacteria. Fire blight is the mostimportant of these diseases and is describedin more detail below. Blister spot, caused byPseudomonas syringae pv. papulans (Rose)Dhanvantari, occurs in North America andEurope. It causes a fruit spot on‘Mutsu’/‘Crispin’, ‘Fuji’, ‘Redcort’, ‘SunCrisp’, ‘Smoothee’ and a few other cultivars.

Blister bark has been described from SouthAfrica but the pathogen P. s. pv. syringae vanHall is found as a common epiphyte onapple foliage worldwide. Crown gall andhairy root are soil-borne diseases caused bytwo species of Agrobacterium; crown gall isthe most common of the two problems.

In areas where these bacterial pathogenseither are not established or are rare, bacter-ial diseases are often avoided by plantingpathogen-free nursery stock. Where thesediseases are established, they are managedthrough orchard sanitation, wound mini-mization, the use of resistant rootstocks andcultivars, site selection, cultural practicesthat promote air movement and drying ofplant surfaces and, in some cases, the use ofcopper and antibiotic sprays.

18.2.1 Fire blight

Fire blight is of major concern in all countrieswhere apples are grown including countriesthat are currently free of this disease(Vanneste, 2000). When fire blight is epi-demic, it can cause serious tree loss in nurs-eries and orchards (Plate 18.1), even leadingto orchard removal. In high-risk areas, fireblight is limiting the planting of some highlysusceptible apple cultivars and rootstocks.Strict quarantines and restrictions are main-tained in countries where the disease doesnot currently occur; enforcing quarantineregulations and restrictions and, if necessary,eradicating the disease are very costly.

The fire blight pathogen kills fruit-bear-ing spurs, branches and entire trees. Infectedblossoms are initially water-soaked anddarker green; spurs with infected blossomsturn brown to dark brown and collapse after4–5 days. Infected shoots turn brown toblack from the tip and bend near the tip toresemble a shepherd’s crook (Plate 18.2).When shoots are invaded from the base, thebasal leaves and stem turn brown to black.Leaves may exhibit discoloration of themidrib, followed shortly by a darkening ofthe lateral veins and surrounding tissues.Bark on infected branches and scaffoldlimbs is darker than normal. When the outerbark is peeled away, the inner tissues are

460 G.G. Grove et al.


Diseases of Apple 461

Tab

le 1

8.1.

Fun

gal d

isea

ses

of a

pple

s, n

ames

of t

he a

sexu

al a

nd s

exua

l sta

ges

of th

e ca

usal

fung

i and

thei

r re

prod

uctiv

e st

ages

, the

sym

ptom

s an

d da

mag

em

ost l

ikel

y to

be

enco

unte

red

and

gene

ral m

etho

ds o

f con

trol

. (M

alus

�do

mes

tica

Bor

kh.)

A.L

. Jon

es, p

rimar

y co

llato

r (la

st u

pdat

e 3/

12/9

3).

Dis

ease

(di

strib

utio

na )F

unga

l pat

hoge

nR

epro

duct

ive

stag

eC

omm

on s

ympt

omsb

Mai

n co

ntro

l met

hod

Alte

rnar

iabl

otch

(A

, A

ltern

aria

mal

iRob

erts

; =A

ltern

aria

C

onid

ia/c

onid

ioph

ores

Leaf

spo

ts, d

efol

iatio

nF

ungi

cide

s,

AF,

NA

)al

tern

ata

(Fr.:

Fr)

Kes

sl a

pple

pat

hoty

pe

culti

var

sele

ctio

n

Alte

rnar

ia r

ot (

W)

Alte

rnar

ia a

ltern

ata

(Fr.:

Fr.)

Kei

ssl

Con

idia

/con

idio

phor

esD

ecay

of f

ruit

Non

e

Am

eric

an b

row

n ro

t M

onili

nia

fruc

ticol

a (G

. Win

t.) H

oney

Con

idia

in s

poro

doch

ia;

Dec

ay o

f fru

it (P

)A

void

pre

harv

est i

njur

y to

frui

t(A

, AF,

NA

,O)

asco

spor

es in

apo

thec

ia

Ant

hrac

nose

can

ker

Pez

icul

a m

alic

ortic

is(H

. Jac

ks.)

Nan

nfC

onid

ia in

ace

rvul

i;C

anke

rs o

n w

ood,

dec

ay

Fun

gici

des

and

bull’

s-ey

e ro

t (E

, C

rypt

ospo

riops

is c

urvi

spor

a(P

eck)

as

cosp

ores

in a

poth

ecia

of fr

uit (

P)

NA

, O)

Gre

mm

en in

Boe

rem

a &

Gre

mm

en

[ana

mor

ph]

App

le s

cab

(W)

Ven

turia

inae

qual

is(C

ooke

) G

. Win

t. A

scos

pore

s in

pse

udot

heci

a;Le

af s

pots

, sca

bs o

n fr

uit,

San

itatio

n, fu

ngic

ides

, res

ista

nt

Spi

loca

ea p

omiF

r.:F

r. [a

nam

orph

]co

nidi

a/co

nidi

opho

res

defo

liatio

ncu

ltiva

rs

App

le r

ing

rot a

nd

Bot

ryos

phae

ria b

eren

geria

naD

e N

ot. (

syn.

Con

idia

in p

ycni

dia;

Can

kers

on

woo

d, d

ecay

F

ungi

cide

sca

nker

(A

)P

hysa

losp

ora

piric

ola

Nos

e)as

cosp

ores

in p

seud

othe

cia

of fr

uit

Arm

illar

ia(s

hoes

trin

g)

Arm

illar

ia m

elle

a(V

ahl:F

r.) P

. Kum

m.

Bas

idio

spor

es in

bas

idio

carp

s D

ecay

of r

oots

Non

e, a

void

pro

blem

site

sro

ot r

ot (

W)

(mus

hroo

ms)

; rhi

zom

orph

s

Bitt

er r

ot (

W)

Glo

mer

ella

cin

gula

ta(S

tone

man

) S

paul

d.

Con

idia

in a

cerv

uli;

Dec

ay o

f fru

itF

ungi

cide

s, s

anita

tion

& H

. Sch

renk

as

cosp

ores

in p

erith

ecia

Col

leto

tric

hum

glo

eosp

orio

ides

(Pen

z.)

Pen

z. &

Sac

c. in

Pen

z. [a

nam

orph

]C

olle

totr

ichu

m a

cuta

tum

J.H

. Sim

mon

s

Bla

ck p

ox (

NA

)H

elm

inth

ospo

rium

pap

ulos

umB

erg.

C

onid

ia/c

onid

ioph

ores

Spo

ts o

n fr

uit a

nd le

aves

Fun

gici

des

Bla

ck r

oot r

ot (

NA

for

Xyl

aria

mal

iFro

mm

e A

scos

pore

s in

per

ithec

iaD

ecay

of r

oots

Non

eX

. mal

i; W

)X

ylar

ia p

olym

orph

a(P

ers.

:Fr.)

Gre

v.

Bla

ck r

ot, f

rog-

eye

Bot

ryos

phae

ria o

btus

a(S

chw

ein.

) Sho

emak

erC

onid

ia in

pyc

nidi

a,

Spo

ts o

n le

aves

and

frui

t, S

anita

tion,

fung

icid

esle

af s

pot a

nd c

anke

r S

phae

rops

is m

alor

umB

erk.

[ana

mor

ph]

asco

spor

es in

pse

udot

heci

ade

folia

tion,

can

kers

on

(AF,

E, N

A, S

A, O

) w

ood

Blis

ter

cank

er (

nail-

Bis

cogn

iaux

ia m

argi

nata

(Fr.)

Pou

zar

Con

idia

in a

scl

erot

ia-li

ke

Can

kers

on

bran

ches

Rem

oval

of i

nfec

ted

bran

ches

head

can

ker)

(N

A)

= N

umm

ular

ia d

iscr

eta

(Sch

wei

n.)

Tul.

& C

. st

rom

a, a

scos

pore

s in

Tu

l. pe

rithe

cia

Con

tinue

d



Tab

le 1

8.1.

Con

tinue

d.

Dis

ease

(di

strib

utio

na )F

unga

l pat

hoge

nR

epro

duct

ive

stag

eC

omm

on s

ympt

omsb

Mai

n co

ntro

l met

hod

Blo

tch

(NA

) P

hyllo

stic

ta s

olita

riaE

llis

& E

verh

. C

onid

ia in

pyc

nidi

aB

lotc

hes

on fr

uit,

leaf

F

ungi

cide

ssp

ots,

blis

ters

in b

ark

Blu

e m

ould

(W

)P

enic

illiu

msp

p.

Con

idia

/con

idio

phor

esD

ecay

of f

ruit

(P)

Pac

king

-hou

se s

anita

tion,

P.

exp

ansu

mLi

nk

fung

icid

es

Bro

oks

frui

t spo

t (N

A)

Myc

osph

aere

lla p

omi(

Pas

s.)

Lind

au

Con

idia

/con

idio

phor

es;

Spo

ts o

n fr

uit,

ofte

n at

Fun

gici

des

Cyl

indr

ospo

rium

pom

iC. B

rook

s as

cosp

ores

in p

seud

othe

cia

caly

x en

d[a

nam

orph

]

Bro

wn-

rot b

loss

om

Mon

ilini

a la

xa(A

derh

. & R

uhl.)

Hon

ey

Con

idia

in s

poro

doch

iaB

light

ing

of b

loss

oms,

F

ungi

cide

sbl

ight

(A

, AF,

E, N

A,

spur

die

back

SA

)

Cal

yx-e

nd r

ot (

NA

)S

cler

otin

ia s

cler

otio

rum

(Lib

.) d

e B

ary

Asc

ospo

res

in a

poth

eciu

mD

ecay

of f

ruit

Non

e

Clit

ocyb

ero

ot r

ot (

NA

)A

rmill

aria

tabe

scen

s(S

cop.

) D

enni

s et

al

Bas

idio

spor

es in

bas

idio

carp

sD

ecay

of r

oots

Non

e=

Clit

ocyb

e ta

besc

ens

(Sco

p.)

Bre

s.

Dia

port

heca

nker

(A

)D

iapo

rthe

tana

kae

Kob

ayas

hi &

Sak

uma

Con

idia

(�

and

ß s

pore

s) in

C

anke

rs o

n 1-

and

S

anita

tion

Pho

mop

sis

tana

kae

Kob

ayas

hi &

Sak

uma

pycn

idia

; asc

ospo

res

in

2-ye

ar-o

ld s

hoot

s[a

nam

orph

]pe

rithe

cia

Dip

lodi

aca

nker

(E

, B

otry

osph

aeria

ste

vens

iiS

hoem

aker

P

ycni

dia

and

pseu

doth

ecia

; C

anke

rs o

n br

anch

esP

runi

ng o

ut o

f inf

ecte

d N

A, O

)=

Phy

salo

spor

a m

alor

umS

hear

et a

l.of

ten

in th

e sa

me

stro

ma

bran

ches

Dip

lodi

a m

utila

(F

r.: F

r.) M

ont.

[ana

mor

ph]

Eur

opea

n br

own

rot

Mon

ilini

a fr

uctig

ena

Hon

ey in

Whe

tzel

C

onid

ia in

spo

rodo

chia

;B

loss

oms

and

spur

S

anita

tion,

fung

icid

es

(A, E

, AF

)M

onili

a fr

uctig

ena

Per

s.:F

r. [a

nam

orph

]as

cosp

ores

in a

poth

ecia

blig

ht, d

ecay

of i

njur

ed

Mon

ilini

a la

xa(A

derh

old

& R

uhla

nd)

frui

tH

oney

Fis

h-ey

e ro

t (A

, E,

But

lere

lfia

eust

acei

Wer

esub

& Il

lman

B

asid

iom

ycet

e, m

ay p

rodu

ce

Dec

ay o

f fru

it (P

)N

one

NA

)=

Cor

ticiu

m c

entr

ifugu

m(L

év.)

Bre

s.

basi

dios

pore

s in

cul

ture

Fly

-spe

ck (

W)

Sch

izot

hyriu

m p

omi(

Mon

t.:F

r.) A

rx

Con

idia

in p

ycni

dia

Sm

all,

supe

rfici

al, d

ark

Cul

tura

l pra

ctic

es, f

ungi

cide

sZ

ygop

hial

a ja

mai

cens

isE

. Mas

on

spot

s on

frui

t[a

nam

orph

]

Glo

mer

ella

leaf

spo

t G

lom

erel

la c

ingu

lata

(Sto

nem

an)

Spa

uld.

&

Con

idia

in a

cerv

uli;

Spo

ts o

n le

aves

, F

ungi

cide

s(N

A, S

A)

H. S

chre

nk

asco

spor

es in

per

ithec

iade

folia

tion

Col

leto

tric

hum

glo

eosp

orio

ides

(Pen

z.)

Pen

z. &

Sac

c. in

Pen

z. [a

nam

orph

]

Apples - Chap 18 21/3/03 3:03 pm 62


Gre

y-m

ould

rot

(W

)B

otry

tis c

iner

eaP

ers.

Fr.

Con

idia

and

scl

erot

ia (

rare

in

Dec

ay o

ften

at c

alyx

end

Pac

king

-hou

se s

anita

tion

and

= d

ry-e

ye r

ot,

Bot

ryot

inia

fuck

elia

na(d

e B

ary)

Whe

tzel

natu

re)

of fr

uit;

nest

rot

of f

ruit

infu

ngic

ides

bl

osso

m-e

nd r

ot[te

leom

orph

]st

orag

e (P

) Le

ptos

phae

riaca

nker

D

iapl

eella

con

ioth

yriu

m(F

ucke

l) B

arr

Leav

esan

d fr

uit r

ot (

W)

= L

epto

spha

eria

con

ioth

yriu

m(F

ucke

l) S

acc.

C

onio

thyr

ium

fuck

elii

Sac

c. [a

nam

orph

]

Leuc

osto

ma

cank

er

Leuc

osto

ma

cinc

ta(F

r.:F

r.) H

ohn.

P

erith

ecia

l str

oma

with

a

Can

kers

on

bran

ches

Rem

oval

of a

ffect

ed b

ranc

hes

and

dieb

ack

(E, N

A)

Cyt

ospo

ra c

inct

aS

acc.

[ana

mor

ph]

cent

ral p

ycni

dium

Val

sa a

uers

wal

diiN

itsch

ke

= L

euco

stom

a au

ersw

aldi

i(N

itsch

ke)

Hoh

n.C

ytos

pora

per

sona

taF

r. [a

nam

orph

]

Mar

sson

ina

blot

ch (

A,

Dip

loca

rpon

mal

iHar

ada

& S

awam

ura

Asc

ospo

res

in a

poth

ecia

;Le

af s

pots

, def

olia

tion,

S

anita

tion,

fung

icid

esN

A, E

)M

arss

onin

a co

rona

ria(E

llis

& J

.J. D

avis

) co

nidi

a in

ace

rvul

isp

ots

on s

urfa

ce o

f fru

itJ.

J. D

avis

[ana

mor

ph]

Mou

ldy

core

and

cor

e A

ltern

aria

spp.

; Ste

mph

yliu

msp

p.;

Con

idia

of v

ario

us ty

pes

Dis

colo

ratio

n an

d de

cay

Pac

king

-hou

se s

anita

tion

rot (

W)

Cla

dosp

oriu

msp

p.; U

locl

adiu

msp

p.ar

ound

the

frui

t cor

e E

pico

ccum

spp.

; Con

ioth

yriu

msp

p.

and

Ple

ospo

rahe

rbar

um (

Per

s.)

Rab

enh.

wet

cor

e ro

t, m

ainl

y P

enic

illiu

msp

p.

Mon

ilia

leaf

blig

ht (

A)

Mon

ilini

a m

ali(

Taka

hash

i) W

hetz

el

Asc

ospo

res

in a

poth

ecia

;B

loss

om a

nd s

pur

blig

ht,

San

itatio

n an

d ch

emic

al c

ontr

olM

onili

asp

p. [a

nam

orph

]co

nidi

a w

ith d

isju

ncto

rsde

cay

of y

oung

frui

t

Mon

ocha

etia

twig

S

eirid

ium

uni

corn

e(C

ooke

& E

llis)

Sut

ton

Can

kers

in w

ound

s on

N

one

cank

er (

NA

)=

Mon

ocha

etia

mal

i(E

llis

& E

verh

.) S

acc.

sm

all t

wig

sLe

pteu

typa

cup

ress

i(N

attr

as e

t al.)

H.J

. S

war

t [te

leom

orph

]

Muc

orro

t (A

F, N

A,

Muc

orsp

p.S

pora

ngio

spor

es a

nd

Sof

t, w

ater

y de

cay

of

Pac

king

-hou

se s

anita

tion

O)

M. p

irifo

rmis

E. F

isch

er

zygo

spor

esfr

uit (

P)

Nec

tria

cank

er (

A, A

F,

Nec

tria

gal

ligen

aB

res.

in S

tras

s.

Con

idia

on

phia

lides

;C

anke

rs o

n br

anch

es,

Fun

gici

des

NA

, SA

, O)

Cyl

indr

ocar

pon

hete

rone

mum

(Ber

k. &

as

cosp

ores

in p

erith

ecia

occa

sion

al fr

uit d

ecay

Bro

ome)

Wol

lenw

eb. [

anam

orph

]

Nec

tria

twig

blig

ht

Nec

tria

cin

naba

rina

(Tod

e:F

r.) F

r. C

onid

ia o

n sp

orod

ochi

a;C

anke

rs o

n br

anch

es

Rem

oval

of a

ffect

ed b

ranc

hes

= c

oral

spo

t (E

, O, N

A)

Tube

rcul

aria

vul

garis

Tode

:Fr.

[ana

mor

ph]

asco

spor

es in

per

ithec

iaan

d tr

unk

Con

tinue

d



Tab

le 1

8.1.

Con

tinue

d.

Dis

ease

(di

strib

utio

na )F

unga

l pat

hoge

nR

epro

duct

ive

stag

eC

omm

on s

ympt

omsb

Mai

n co

ntro

l met

hod

Pen

ioph

ora

root

can

ker

Pen

ioph

ora

sacr

ata

G.H

. Cun

n.B

asid

iom

ycet

e w

ith c

rust

-like

In

fect

ed r

oots

with

R

esis

tant

roo

tsto

cks

and

(O)

frui

ting-

bodi

esch

arac

teris

tic c

rack

ssa

nita

tion

Per

enni

al c

anke

r (N

A)

Neo

fabr

ae p

eren

nans

Kie

nhol

z C

onid

ia in

ace

rvul

i;C

anke

rs o

n br

anch

es,

San

itatio

n, fu

ngic

ides

Cry

ptos

porio

psis

per

enna

ns(Z

elle

r &

as

cosp

ores

in a

poth

ecia

deca

y of

frui

tC

hild

s) W

olle

nweb

. [an

amor

ph]

Pho

mop

sis

cank

er, f

ruit

Pho

mop

sis

mal

iRob

erts

Con

idia

(�

and

ß s

pore

s) in

C

anke

rs o

n w

ood,

frui

t N

one

deca

y an

d ro

ugh

bark

D

iapo

rthe

per

nici

osa

Em

. Mar

chal

py

cnid

ia, a

scos

pore

s in

de

cay

(P)

(A, E

, NA

)[te

leom

orph

]pe

rithe

cia

Phy

mat

otric

hum

root

P

hym

atot

richo

psis

om

nivo

ra(D

ugga

r)

Hyp

hae

with

con

idia

on

Dec

ay o

f roo

ts

Non

ero

t H

enne

bert

co

nidi

opho

res

and

scle

rotia

= c

otto

n ro

ot r

ot (

NA

)=

Phy

mat

otric

hum

om

nivo

rum

Dug

gar

Phy

toph

thor

acr

own,

P

hyto

phth

ora

spp.

Z

oosp

ores

pro

duce

d in

Dec

ay o

f cro

wn

and

root

C

ultu

ral p

ract

ices

, hos

t co

llar

and

root

rot

; P.

cac

toru

m(L

eber

t & C

ohn)

J. S

chrö

t. sp

oran

gia

from

hyp

hae

or

tissu

esre

sist

ance

, che

mic

al tr

eatm

ent

(spr

inkl

er r

ot)

(W)

P. c

ambi

vora

(Pet

r.) B

uism

ange

rmin

atin

g oo

spor

es o

r P.

cry

ptog

eaP

ethy

br. &

Laf

fert

y ch

lam

ydos

pore

sP.

meg

aspe

rma

Dre

chs.

P.

syr

inga

e (K

leb.

) K

leb.

Phy

toph

thor

a fr

uit r

ot

Phy

toph

thor

aca

ctor

um(L

eber

t & C

ohn)

S

ee a

bove

Rot

ting

of fr

uit

Late

-sea

son

fung

icid

e sp

rays

(E

, NA

)J.

Sch

röt.;

or p

osth

arve

st tr

eatm

ents

Phy

toph

thor

a sy

ringa

e(K

leb.

) K

leb.

Pin

k m

ould

rot

(W

)Tr

icho

thec

ium

ros

eum

(P

ers.

:Fr.)

Lin

kC

onid

iaD

ecay

of f

ruit

(P)

Pre

vent

ed b

y re

frig

erat

ed c

old

= C

epha

loth

eciu

m r

oseu

mC

orda

st

orag

e

Pow

dery

mild

ew (

W)

Pod

osph

aera

leuc

otric

ha(E

llis

& E

verh

.)

Con

idia

/con

idio

phor

e;P

owde

ry s

pots

on

leav

es,

Cul

tivar

sel

ectio

n, fu

ngic

ides

E.S

. Sal

mon

as

cosp

ores

in c

leis

toth

ecia

frui

t rus

setin

g

Ros

ellin

iaro

ot r

ot (

W)

Ros

ellin

iane

catr

ixP

rill.

Asc

ospo

res

in p

erith

ecia

;D

ecay

of r

oots

Cul

tura

l pra

ctic

es, s

olar

izat

ion

= D

emat

opho

raro

ot ro

t D

emat

opho

ra n

ecat

rixR

. Har

tig

pycn

idia

on

synn

emat

a[a

nam

orph

]

Rus

t, A

mer

ican

G

ymno

spor

angi

um g

lobo

sum

(Far

l.) F

arl.

Pyc

nia

and

aeci

dia

on a

pple

;Le

aves

Rem

oval

of a

ltern

ativ

e ho

st,

haw

thor

ne (

NA

)te

lent

ospo

res

in te

lial h

orns

fu

ngic

ides

on c

edar

Rus

t, ce

dar a

pple

(NA

)G

ymno

spor

angi

um ju

nipe

ri-vi

rgin

iana

e P

ycni

a an

d ae

cidi

a on

app

le;

Spo

ts o

n le

aves

, R

emov

al o

f alte

rnat

ive

host

, S

chw

ein

tele

ntos

pore

s in

telia

l hor

ns

defo

liatio

n an

d di

stor

tion

fung

icid

eson

ced

arof

frui

t



Rus

t, Ja

pane

se a

pple

G

ymno

spor

angi

um y

amad

aeM

iyab

e ex

P

ycni

a an

d ae

cidi

a on

app

le;

Leav

esR

emov

al o

f alte

rnat

e ho

st,

(A)

Yam

ada

tele

ntos

pore

s in

telia

on

fung

icid

esJu

nipe

rus

chin

ensi

s

Rus

t, P

acifi

c C

oast

G

ymno

spor

angi

um li

boce

dri(

C.H

enn.

) F.

A

ecid

ia o

n ap

ple;

pear

(N

A)

Ker

n te

lent

ospo

res

in te

lia o

n Li

boce

drus

dec

urre

ns

Rus

t, qu

ince

(N

A)

Gym

nosp

oran

gium

cla

vipe

s(C

ooke

& P

eck)

P

ycni

a an

d ae

cidi

a on

app

le;

Dis

tort

ion

of fr

uit

Rem

oval

of a

ltern

ativ

e ho

st,

Coo

ke &

Pec

k in

Pec

k te

lent

ospo

res

in te

lia o

n ce

dar

fung

icid

es

Sid

e ro

t (E

, NA

)P

hial

opho

ra m

alor

um(M

.N. K

idd

& A

. C

onid

ia a

t the

ape

x of

D

ecay

of f

ruit

(P)

Cul

tura

l pra

ctic

es, p

osth

arve

st

Bea

umon

t) M

cCol

loch

ph

ialid

estr

eatm

ents

Silv

er le

af (

W)

Cho

ndro

ster

eum

pur

pure

um(P

ers.

:Fr.)

Pou

zar

Bas

idio

spor

esW

ood

deca

yC

ultu

ral p

ract

ices

Soo

ty-b

lotc

h co

mpl

ex

Pel

tast

er fr

uctic

ola

(Joh

nson

, Sut

ton,

C

onid

ia in

pyc

nidi

aB

lotc

hes

of v

ario

us s

ize

Cul

tura

l pra

ctic

es a

nd

(W)

Hod

ges)

; Gea

stru

mia

pol

ystig

mat

ison

the

surf

ace

of fr

uit

fung

icid

esB

atis

ta &

M.L

. Far

r; L

epto

dont

ium

el

atiu

s(G

. Man

geno

t) (

De

Hoo

g); a

nd

Glo

eode

s p

omig

ena

(Sch

wei

n.)

Col

by)

Sou

ther

n bl

ight

(A

F,

Scl

erot

ium

rol

fsii

Sac

c.

Scl

erot

iaD

ecay

at b

ase

of tr

unk

Cul

tura

l pra

ctic

esN

A, S

A)

Ath

elia

rol

fsii

(Cur

zi)

Tu &

Kim

brou

gh

[tele

omor

ph]

Thr

ead

blig

ht

Cor

ticiu

m s

teve

nsii

Bur

t R

hizo

mor

phs

and

scle

rotia

; B

light

ing

of b

ranc

hes

Fun

gici

des

= H

ypoc

hnus

leaf

blig

ht =

Pel

licul

aria

kol

erog

aC

ooke

ba

sidi

a w

ith b

asid

iosp

ores

(N

A)

= H

ypoc

hnus

och

role

ucus

Noa

ck

Val

saca

nker

(A)

Val

sa c

erat

ospe

rma

(Tod

e:F

r.) M

aire

P

ycni

dia

and

perit

heci

a in

a

Can

kers

on

bran

ches

San

itatio

nC

ytos

pora

sac

culu

s(S

chw

ein.

) G

vriti

schv

ili

stro

ma

[ana

mor

ph]

Vio

let r

oot r

ot (

O)

Hel

icob

asid

ium

mom

paTa

naka

B

asid

iosp

ores

in b

asid

ioca

rps

Roo

t dec

ayS

oil s

teril

izat

ion

Whi

te r

oot r

ot (

NA

)S

cytin

ostr

oma

gala

ctin

um(F

r.) D

onk

Bas

idia

on

a re

supi

nate

D

ecay

of r

oots

Non

e=

Cor

ticiu

m g

alac

tinum

(Fr.)

Bur

t hy

men

ium

Whi

te r

ot (

AF,

NA

, B

otry

osph

aeria

dot

hide

a(M

oug.

) C

es. &

De

Con

idia

in p

ycni

dia;

Dec

ay o

f fru

it, c

anke

rs

Fun

gici

des

and

sani

tatio

nS

A, O

)N

ot.

asco

spor

es in

pse

udot

heci

aon

lim

bs a

nd tw

igs

Fus

icoc

cum

aes

culi

Cor

da [a

nam

orph

]

Zon

ate

leaf

spo

t (A

) C

ristu

larie

lla m

oric

ola

(Hin

o) R

edhe

ad

Asc

ospo

res

in a

poth

ecia

;Le

af s

pot,

defo

liatio

nS

anita

tion

Gro

vesi

nia

pyra

mid

alis

M. C

line

et a

l.co

nidi

a [te

leom

orph

]

a App

roxi

mat

e ge

ogra

phic

al d

istr

ibut

ion

of th

e di

seas

e: A

, Asi

a; A

F, A

fric

a; E

, Eur

ope;

NA

, Nor

th A

mer

ica;

O, O

cean

ia; S

A, S

outh

Am

eric

a; W

, wor

ldw

ide.

b P, p

osth

arve

st d

isea

se p

robl

em.


water-soaked with reddish streaks whenfirst invaded; later the tissues are brown. Aslesion expansion slows, the bark sometimescracks, delineating a canker. Infected fruitdevelop a brown-to-black decay. Duringwet, humid weather, droplets of whitish toreddish-brown, sticky liquid (known asooze) seeps from the surface of infected tis-sues (Plate 18.3). Infected rootstocks mayshow bleeding or ooze from rootstock tissueearly in summer and internal necrosis of thebark and the leaves of the scion turn reddishearly in the autumn.

Fire blight is caused by Erwinia amylovora(Burrill) Winslow et al., a Gram-negative,rod-shaped, non-fluorescent bacterium withperitrichous flagella. More than 130 speciesin 39 genera of the Rosaceae are hosts.Important hosts include apple, pear, orna-mental Pyrus and Malus species, quince(Cydonia oblonga), loquat (Eriobotrya japon-ica), hawthorn (Crataegus spp.), Cotoneasterspp., Sorbus spp., Pyracantha spp. and Rubusspp. Most strains of E. amylovora from Rubusdo not infect apple and are therefore consid-ered to be pathologically distinct. Primaryisolation of the bacteria is by culturing onLuria–Bertani (LB) agar or some semi-selec-tive medium. They are distinguished fromother plant pathogenic bacteria based oncolony colour and morphology on MM2Cu

and LB media (see Bereswill et al., 1998, forthe composition of these media), patho-genicity tests performed on immature fruit,seedlings or vigorous plants, and molecularassays (Bereswill et al., 1995; McManus andJones, 1995).

The pathogen overwinters in cankerslocated on branches and tree trunks (Fig.18.1). Ooze can begin to appear on the sur-face of these cankers at or just before theonset of bloom. Bacteria are disseminated toflowers by splashing rain and, occasionally,flies and other insects that visit both bacterialooze and blossoms. Eventually, honey beesvisit infected blossoms and pick up pollen ornectar contaminated with bacteria. Spread ofbacteria from flower to flower by bees israpid. Bacteria colonize the stigmatic surfaceof the pistils of healthy apple and pear flow-ers, resulting in epiphytic populations ofbacteria (Thomson, 1986). Climatic condi-tions govern the rate of spread and severityof blossom blight and even the infectionprocess itself. Temperatures between 18.3and 30°C (accompanied by rain or highhumidity during the day) favour infection.Although bacteria invade the flowers pri-marily through natural openings, stormscontaining wind-driven rain or hail areimportant in spreading bacteria during thesummer months, which under some condi-


Table 18.2. Bacterial diseases of apple, scientific name of the pathogen, symptoms and main control method.

Disease Common (distributiona) Pathogen symptoms Main control method

Fire blight (E, NA, Erwinia amylovora Blight, cankers, Resistant cultivars and New Zealand) dead trees rootstocks, sanitation,

antibiotics

Blister spot (E, NA) Pseudomonas syringae pv. Spots on fruit Avoiding susceptible papulans (Rose) Dhanvantari cultivars, antibiotics

Blister bark (AF) Pseudomonas syringae pv. Terminal dieback, Nonesyringae van Hall blossom blight,

Crown gall (W) Agrobacterium tumefaciens Galls on roots Sanitation, biocontrol but (E.F. Smith & Townsend) Conn often less effective than

on Prunus species

Hairy root (W) Agrobacterium rhizogenes Excessive production Sanitation(Riker et al.) Conn of fibrous roots

aApproximate geographical distribution of the pathogen: A, Africa; E, Europe; NA, North America, W,worldwide.


tions lead to sudden and severe outbreaks ofdisease. Inoculum for secondary infectionoriginates from droplets of ooze producedon infected flowers, fruits and shoots.

Temperature, as measured by the accumu-lation of degree-days (DD), governs the rateof symptom development. Symptoms areexpressed when 55 DD (base 12.5°C) areaccumulated following the infection date.The susceptible rootstocks M.9 and M.26 areinfected by systemic movement of bacteriathrough symptomless scion tissue or throughinfected rootstock shoots (Momol et al., 1998).Although the rootstock Bud.9 is blight-sus-ceptible, rootstock blight has not developedon many Bud.9/scion combinations. Lossesfrom rootstock blight can be avoided byusing resistant rootstocks, such as G.16, G.30,G.65 and other blight-resistant rootstocksfrom the US Department of Agriculture–Agricultural Research Service (USDA-ARS)/Cornell apple-rootstock programme.

Many practices help to prevent or reducethe severity of fire blight. In countries whereE. amylovora is not established, only trees pro-duced in fire-blight-free regions should beused when establishing new orchards. Thesecountries may already have strict quarantines

to prevent the importation of plant materialthat may harbour the pathogen.

In countries where fire blight is a prob-lem, sanitation – the removal of infected por-tions of the tree – is critical to the success ofother control measures and is effective pro-vided it is done during the early stages of anepidemic. New orchards should be plantedon blight-resistant rootstocks if available. Arealistic plan for controlling fire blight isneeded before making large plantings ofblight-susceptible cultivars. Antibiotics havebeen highly effective for preventing the blos-som-blight stage of fire blight, but in someregions or orchards control with antibiotics isno longer possible, due to the developmentof streptomycin-resistant strains of E.amylovora. Predictive models, particularlyMaryblyt and Cougarblight in the USA andBillings’ integrated system and Firescreens inEurope, help growers identify potentialinfection periods (Billings, 2000). Such infor-mation is helpful in timing antibiotic treat-ment and for avoiding unnecessarytreatment. Bacterial antagonists that sup-press fire blight may be integrated withantibiotics to control flower infections(Stockwell et al., 1996).


Fig. 18.1. The fire blight disease cycle. The pathogen overwinters in cankers. At the onset of bloom, bacteriabegin to ooze on to the surface of cankers; splashing rain, along with flies and other insects, moves thebacteria to open flowers. Then, honey bees spread the bacteria from flower to flower on contaminatedpollen and nectar. The bacteria multiply on the stigmatic surface of the pistils to produce high epiphyticpopulations. Favourable combinations of moisture and temperature govern infection of the flowers. Summerstorms with wind-driven rain spread the bacteria, leading to sudden and severe outbreaks of diseases.Inoculum for secondary infection originates from droplets of ooze produced on infected flowers, fruit andshoots. (Figure courtesy A.L. Jones.)


18.3 Diseases Caused by Fungi

Within this diverse group of plant pathogensare the causes of most apple diseases (Table18.1). Fungi pathogenic to apple can causeroot rots, leaf spots, leaf blights, blossomblights, fruit decay, fruit spots, defoliationand trunk, branch and twig cankers. Thefungal diseases discussed in this chapter arecaused by fungi belonging to the general tax-onomic groups represented by the mush-rooms (Basidiomycetes) and morels(Ascomycetes). The phylum Oomycota alsocontains the water moulds, an importantgroup of plant pathogens formerly classifiedas fungi. Fungi in the ascomycete grouphave scientific names for the anamorph andteleomorph. The anamorph is the asexualform (also called the imperfect stage) of thefungus and produces asexual spores (such asconidia) or no asexual spores. The teleo-morph is the sexual form (also called the per-fect or sexual state) and produces sexualspores (ascospores) in various fruiting bodies(pseudothecia, perithecia, apothecia, etc.).These fungi generally reproduce by sporesthat are dispersed by air currents or splash-ing water. Fungal diseases are prevented ormanaged by using resistant cultivars androotstocks, site selection, sanitation, culturalpractices and fungicide practices. Specificmanagement measures vary according todisease and geographical location.

18.3.1 Apple scab

Scab occurs in virtually all apple-producingregions worldwide (MacHardy, 1996). Thedisease is an annual threat in cool, humidregions with frequent rainfall in spring andearly summer. In semiarid regions, scab is athreat in years with above-normal rainfall orin orchards where artificial wetting periodsare created from the improper use of over-head irrigation.

Scab attacks the leaves and fruit through-out most of the growing season; blossoms andbud scales are attacked for short periods inspring and late summer, respectively.Symptoms first appear on the undersides ofleaves, the side exposed as buds open. Later,

symptoms are found on both sides of leaves.Conidia are produced abundantly in newlesions; therefore, lesions appear as velvetybrown to olive spots that turn black with age(Plate 18.4). Severe infection can cause leavesto abscise, resulting in defoliated trees. Returnbloom on trees defoliated in midsummer isoften reduced due to a lack of flower-bud for-mation the previous summer. Fruit infectionsresemble leaf infections when young but turnbrown and corky with age (Plate 18.5). Early-season infections are often associated with theblossom end of the fruit; later they can occuranywhere on the surface. Scab infectionsresult in uneven growth of fruit and evencracking of the skin and flesh. Rough, blackcircular lesions develop in cold storage onfruit infected close to harvest. The latter phaseis known as pinpoint scab. Infection of blos-soms and bud scales may be observed inhigh-inoculum orchards when infection peri-ods occur at critical times. Lesions on blos-soms and bud scales resemble those on leavesbut are seldom observed because these tissuesnormally drop to the ground before the symp-toms are well developed.

Venturia inaequalis (Cooke) G. Wint.,anamorph Spilocea pome Fr., causes applescab. It has one sexual cycle and a series ofasexual cycles per year. Flask-shaped, ascus-bearing fruiting bodies (pseudothecia)develop in overwintering infected leaves.Pseudothecia form as a result of the interac-tion of two strains of opposite mating types(heterothallic fungus). Asci in pseudotheciaare eight-spored. Mature ascospores are two-celled, with the upper cell shorter and widerthan the lower cell, yellowish green to tanand with smooth walls. Conidia are one-celled, yellowish-olive and pointed.

From late autumn to spring, microscopic,black, pimple-like pseudothecia develop inleaves on the orchard floor (Fig. 18.2).Normally, pseudothecia contain matureascospores when the blossom buds start toopen in spring. Maturation and discharge ofascospores lasts about 5–9 weeks. Whenleaves on the orchard floor become wet fromrain, spores are ejected into the air. Air cur-rents carry them to the emerging tissues,where infection occurs. Young leaves and fruitare highly susceptible to infection, but their



susceptibility declines with maturity. Sporegermination begins soon after ascosporesland on wet leaves or fruit. Prevailing temper-atures govern the infection rate, provided acontinuous film of moisture is present for ger-mination of the spores. Depending on theaverage temperature after penetration, 9–17days are required before the appearance ofthe olive-green, velvety scab lesions. In someapple-producing regions and on some culti-vars, the fungus also overwinters in lesionson twigs and bud scales (Becker et al., 1992);conidia produced in these lesions are a secondform of primary inoculum. However, thenumber of conidia available from overwinter-ing lesions at bud break is low compared withthe number of ascospores potentially avail-able from leaf litter.

Secondary infections are initiated by coni-dia produced in primary and secondarylesions. Conidia can be produced in newlesions beginning as soon as 7–9 days afterinfection and these lesions can produce coni-dia in continuous crops for several weeks.Conidial germination and infection occurunder about the same conditions as germina-tion and infection by ascospores. Secondaryinfection on fruit can occur in the autumn

but fails to develop until after the fruit hasbeen held in cold storage for several months.Infections can also build up in leaves afterharvest and prior to normal leaf abscission.The fungus overwinters in these leaves andthey are often the source of very high levelsof inoculum the following spring.

Basic studies on the biology and epidemi-ology of apple scab from the 1920s to the1940s established a rational basis for scabcontrol and these concepts continue to berefined. The initial ascosporic inoculum isusually present in large amounts; therefore,estimating the risk of the initial ascosporicinoculum and forecasts of its efficiency arevery important for determining when to ini-tiate scab-control programmes and theapplication frequency. Inoculum risk isdetermined by monitoring pseudotheciafrom early spring to midsummer to deter-mine whether ascospores are mature andavailable for discharge and by detectingascospore release in orchards during wettingperiods. Statistical models have been devel-oped to predict ascospore maturity based on DD accumulations and these models are replacing ascospore-monitoring pro-grammes. Inoculum risk forecasts assume


Fig. 18.2. The apple scab disease cycle. The fungus Venturia inaequalis overwinters in leaves on the orchardfloor and sometimes in apple buds. Pseudothecia with ascospore-bearing asci in dead leaves discharge theirascospores when the leaves become wet from rain. Ascospores produce the first, or primary, infections onthe young fruit and leaves. Conidia produced on the inner surface of apple-bud scales can also causeprimary infections. Depending on temperature, 9–17 days are required before new scab lesions appear onthe infected tissues. Conidia, formed in continual crops of new lesions, produce secondary infections.Secondary cycles are repeated many times until leaf fall in autumn. (Figure courtesy A.L. Jones.)


high inoculum levels, an assumption that isusually incorrect for orchards where scabwas well controlled the previous season.Therefore, methods for assessing differencesin inoculum among orchards based on apotential ascospore density (PAD) systemwere developed (Gadoury and MacHardy,1986). It was found that in low-inoculumorchards spray programmes in spring couldbe delayed until about the tight-cluster stageof bud development, rather than green tip inthe normal spray schedule for high-inocu-lum orchards. Integrating inoculum riskwith environmental risk is accomplished bythe identification of ‘infection periods’.Rainfall is necessary for the discharge ofascospores – free water for the germinationof ascospores and penetration of tissues. Therate of this infection process is temperature-dependent, and the duration of wetnessrequired for successful infection across awide range of temperatures is well known(Jones, 1998). Therefore, temperature andwetness measurement can be used to fore-cast the success or failure of each ascospore-discharge event. These events can bemonitored with environmental sensorslinked to small computers placed in theorchard or with automated weather stationsconnected directly to computers. Fungicideswith post-infection efficacy are applied afterpredicted but unprotected infection periods.

Apple-breeding programmes aiming forhigh-quality, disease-resistant cultivars are inprogress in New Zealand and someEuropean and North American countries.Over 50 scab-resistant cultivars have beenreleased and are gaining in commercialacceptance as fruit quality and other horti-cultural characteristics are improved.Guarding against races of the scab pathogenthat can overcome the resistance sourcesused by apple breeders is a high priority inthese breeding programmes (Bénaouf andParisi, 2000).

Prevention of pseudothecia formation inoverwintering leaves would probably elimi-nate scab. Unfortunately, complete elimina-tion of pseudothecia is not possible underorchard conditions using current methods.Spring ascospore production can be reducedby making autumn applications of urea or

fungal antagonists to the foliage just prior toleaf fall (Carisse et al., 2000), but this strategyalone is not adequate for season-long scabcontrol. This approach may be more feasiblein areas with lower amounts of overwinter-ing inoculum and mild winters.

Scab is controlled primarily with fungi-cides applied in predetermined schedules,beginning at green tip. The fungicides areapplied on a 7–14-day interval with eight toten applications per season. Several classesof fungicides are available for apple-scabcontrol. They are often rotated during theseason or applied as mixtures because of thehigh potential of the scab fungus to developfungicide-resistant strains.

18.3.2 Powdery mildew

Powdery mildew is circumglobal and apotentially serious disease wherever applesare grown. The disease is particularly prob-lematic in the western and mid-Atlanticregions of the USA. Severe infections reducetree photosynthesis and transpiration (Elliset al., 1981) and may result in partial defoli-ation (Ogawa and English, 1991). Chronicinfections can result in reduced tree vigour,poor return bloom and yield reduction.Fruit infection can result in the rejection offruit for fresh-market sale. Apple cultivarsvary in their susceptibility to powderymildew. ‘Gala’, ‘Braeburn’, ‘Ginger Gold’,‘Mutsu’ (Crispin), ‘Cortland’, ‘Baldwin’,‘Monroe’, ‘Idared’, ‘Honeycrisp’, ‘Jonathan’,‘Granny Smith’, ‘Ginger Gold’, ‘RomeBeauty’, ‘Jonagold’ and ‘Pink Lady®’ areparticularly susceptible. ‘Delicious’ and‘Golden Delicious’ are less susceptible.

Leaves, flowers and fruit are susceptibleto infection by the powdery mildew fungus.The foliage of new terminal growth isextremely susceptible to infection. The ini-tial signs of powdery mildew consist ofwhite to grey felt-like patches on the lowerleaf surface. These patches are comprised ofmasses of fungal mycelia and spores (coni-dia). As disease progresses, mildew signsmay also appear on the upper leaf surfaceand eventually cover the entire leaf. Infectedfoliage may curl, blister and eventually



become brittle and necrotic (Plate 18.6).Internodal shortening may occur onseverely infected shoots. Infected flowerpetals are distorted, stunted and light yel-low to light green. Fruit infection typicallyresults in stunting accompanied by the pres-ence of a fine network of rough lines (russet-ing) (Plate 18.7).

Powdery mildew is caused by Podosphaeraleucotricha (Ell. & Ev.) E.S. Salmon. The fun-gus is superficial on the host surface butwithdraws water and nutrients from host tis-sue, using a structure called a haustorium.The fungus produces barrel-shaped conidiain chains, which are dispersed by air cur-rents and initiate subsequent infections offoliage and fruit (Fig. 18.3). P. leucotrichasurvives through winter as mycelium ininfected buds. This mode of perennationresults in the production of ‘flag shoots’(shoots covered with powdery mildew)when shoots emerge in the spring. Wintertemperatures are the most important factoraffecting the amount of carry-over inoculum.Temperatures colder than �12ºC kill the fun-gal mycelium in buds; temperatures lowerthan �24ºC may kill the infected buds(Spotts et al., 1981). Conidia produced on flagshoots initiate the first spring infections and

are therefore primary inocula, which initiateadditional new infections. This cycle ofsporulation and foliar infection can continueas long as susceptible foliage is being pro-duced. This secondary phase of powderymildew can cycle many times during thegrowing season. Temperature is the mostimportant factor affecting disease develop-ment. Conidia germinate at temperaturebetween 10 and 25ºC; the optimum tempera-tures for germination are 20–22ºC. The sex-ual stage (ascocarps) of P. leucotrichaoccasionally forms on infected twigs.Ascocarps are minute, brown to black, spher-ical fruiting bodies that contain eight unicel-lular ascospores. Various researchers havesuggested that this stage is insignificant inthe epidemiology of the disease. Fruits areespecially susceptible to infection during thebloom period (Daines et al., 1984).

Powdery-mildew epidemics are favouredby high humidity; therefore problems withmildew can often be avoided or reducedwith cultural practices that promote airmovement and light penetration. On suscep-tible cultivars, effective disease managementusually depends on a fungicide-spray pro-gramme. Benzimidazole, sulphur, horticul-tural mineral, oils, demethylation-inhibiting


Fig. 18.3. The apple powdery mildew disease cycle. The fungus overwinters as mycelium in infected buds.Mildew conidia, produced on leaves arising from the infected buds, become wind-borne and cause primaryinfections on healthy leaves and fruit. Secondary infections are produced from conidia produced in bothprimary and other secondary infections and are repeated until shoot growth stops in late summer. (Figurecourtesy A.L. Jones.)


(DMI) and strobilurin fungicides are effec-tive against powdery mildew. Spray pro-grammes should commence at tight clusterand continue until the production of newfoliage ceases. Because powdery mildewscan develop resistance to benzimidazole,DMI and strobilurin fungicides, rationalresistance-management strategies usuallyrequire the inclusion of two or more fungi-cide classes in a season-long programme.DMI fungicides applied in apple-scab-man-agement programmes generally provide theadded benefit of mildew control.

A predictive system has been developedfor aid in managing infections caused by P.leucotricha. Podem© (Xu, 1999) is a systemdeveloped in the UK that simulates epi-demics of secondary mildew on vegetativeshoots. The effects of weather on conidialproduction, dispersal and germination areused to calculate a favourability index. Themodel itself is driven by hourly ambienttemperature, relative humidity, shade tem-perature and the total daily duration of rain-fall. The model has been incorporated intoan integrated apple disease warning system(ADEM) and successfully used to timefungicide applications and in some cases hasresulted in improved disease control, with a40% reduction in fungicide usage (Berrieand Xu, 1999).

18.3.3 Brown-rot diseases

Several brown-rot fungi attack apple in dif-ferent parts of the world. The species andtheir distribution are: Monilinia fructicola(Wint.) Honey in most regions exceptEurope, where it is a European Union-listedquarantine pest (Smith et al., 1992); Monilinialaxa (Aderh. & Ruhl.) Honey in Asia, Europe,North and South America and South Africa;and Monilinia fructigena (Aderh. & Ruhl.)Honey in Europe and Asia (Byrde andWilletts, 1977). A related species, Moniliniamali (Takahashi) Whetzel, causes Monilia leafblight of apple in Asia.

The brown-rot fungi cause blossom wilt,spur dieback, cankering and fruit rot (Plate18.8); the incidence and severity of thesesymptoms depend on the species of

pathogen present. M. laxa causes blossomblight, spur dieback and cankering ofbranches; M. fructigena causes fruit rot andsometimes cankers when the fungusspreads into branches from the fruit; andM. fructicola causes a fruit rot. Monilia leafblight infects young apple leaves;mycelium invading from leaves kills flowerclusters, young fruits and fruiting spurs.

The species of Monilinia can be differenti-ated by microscopic observation of conidiaformed in chains in culture or on infected tis-sue. M. mali can be differentiated by disjunc-tors present within the conidial chains. M.fructicola, M. fructigena and M. laxa can bedifferentiated based on cultural characteris-tics, isozyme variation, vegetative interac-tions and PCR assays.

The life cycles of these pathogens differonly in the role that the perfect stage(apothecia) plays in the overwintering of thefungi. M. mali and occasionally M. fructicolaproduce apothecia on mummified fruit onthe ground. All species overwinter ininfected parts of the tree. Secondary spreadis by conidia produced on infected host tis-sue within the tree and on trees of neigh-bouring hosts, particularly Prunus species.

Losses due to fruit decay caused by M.fructigena and M. fructicola increase gradu-ally up to harvest time and are usually asso-ciated with injuries to the fruit. Cultivarsprone to fruit cracking, such as ‘Cox’sOrange Pippin’ and ‘James Grieve’, areespecially susceptible to infection. Infectionalso occurs through wounds caused bybirds pecking at fruit, insects infesting fruitand hail. Fruit decay is prevented by avoid-ing cultivars prone to fruit cracking, by lim-iting the damage caused by birds and otherwounding agents and by orchard sanitationmethods aimed at reducing the build-up ofinoculum.

Blossom infections from M. laxa, M. fructi-gena and Monilia leaf blight are controlled byorchard sanitation, combined with the appli-cation of fungicides. Blighted spurs andcankers are removed and destroyed duringthe dormant period and in the growing sea-son. Fungicides applied as the flowers beginto open and one or two times 5–7 days latershould prevent blossom blight.



18.3.4 Summer diseases

Summer diseases refer to a collection of ninediseases that tend to be most severe from 2–3weeks after petal fall until harvest. They aremost prevalent in warm and moist growingregions of the world, where they can causeextensive losses if not controlled. They arerelatively minor problems in arid and coolergrowing regions.

Of all the summer diseases, rot diseasesare most destructive and can cause losses of50% or more if not controlled. These diseasestend to be most severe in the south-easternUSA but cause problems in other areas aswell. The life cycles of the pathogens thatcause these diseases are similar, as is theoverall strategy for managing them.

18.3.4.1 Bitter rot

Bitter rot is the most destructive of the threerot diseases and is the most difficult of thethree to control once an epidemic has begun.It is caused by Colletotrichum gloeosporioides(Penz.) & Sacc. in Penz. and Colletotrichumacutatum J.H. Simmons. These pathogenscoexist in many orchards, whereas in othersone or the other species predominates.Glomerella cingulata (Stoneman) Spauld & H.Shrenk is often listed as the sexual stage of C.gloeosporioides but may be a distinct taxon(Shane and Sutton, 1981a; TeBeest et al., 1997).

The Colletotrichum spp. that cause bitterrot survive from one growing season toanother in mummified apples, twig cankersand other dead wood in the tree. In the latespring when temperatures begin to warm,conidia are released, initiating infections onfruit. Fruit is susceptible throughout the sea-son (Shane and Sutton, 1981b; Noe andStarkey, 1982). Lesions begin as small, circu-lar, light tan to brown spots, sometimes sur-rounded by a red halo. As the lesions enlarge,they become brown and sunken (Plate 18.9)and extend into the flesh of the apple in a V-shaped pattern, which is a good diagnostictechnique. Fruiting structures on the surfaceof the lesion, called aecidia, produce copiousamounts of salmon-coloured conidia, whichcan be splash-dispersed to other fruit, initiat-ing new infections. Consequently, the disease

has enormous potential for secondary spreadand is very difficult to control when theweather is warm and wet.

G. cingulata also survives from year toyear on dead wood and mummified apples.There appear to be several strains, whichproduce somewhat different symptoms. Aserious leaf-spot disease, Glomerella leaf spot,occurs on ‘Gala’ in Brazil, which is associ-ated with G. cingulata (Sutton and Sanhueza,1998). It causes small irregular lesions3–12 mm in diameter on leaves and canresult in significant defoliation when severe.It also causes small corky lesions on fruit.This strain overwinters in leaves on theorchard floor, much like apple scab, andinfection is initiated in the late spring by air-borne ascospores, which are discharged dur-ing periods of rain. Perennation also occursin twig cankers and mummified apples.Glomerella leaf spot has been observed in thesouth-eastern USA (Gonzalez and Sutton,1999). Another strain of G. cingulata producesa large, firm, brown lesion on the fruit,which is not sunken, and few spores are pro-duced on the surface of the lesion (Shaneand Sutton, 1981b). It is not known whetherthis strain causes a leaf-spot symptom.

Management of bitter rot is based on sani-tation and a preventive spray programme. Inwarm, rainy, growing regions, the diseasecannot be successfully managed withoutpruning to remove inoculum sources andfacilitate drying in the tree canopy. Current-season fire blight strikes need to be removedbecause they can be colonized by the bitter-rot fungi and serve as an inoculum sourcelate in the season. The ethylenebisdithiocar-bamate (EBDC) fungicides are most effective,but restrictions on their application afterpetal fall in the USA have limited their use-fulness. Captan, ziram and thiram (appliedon a 10–14-day schedule from petal fall toharvest) are the most effective fungicidescurrently registered in the USA. The benzim-idazole fungicides are ineffective.

18.3.4.2. Black rot and bot (white) rot

Black rot and bot rot are caused byBotryosphaeria obtusa (Schwein.) Shoemakerand Botryosphaeria dothidea (Moug.) Ces. &



DeNot., respectively. Although caused by thesame fungal genus, the diseases caused bythe two species are different in many ways.Both overwinter in dead wood, mummifiedapples and cankers in the tree canopy andproduce ascospores and conidia throughmost of the growing season. Both cause afruit rot and cankers, but only B. obtusacauses a leaf spot. Infections by B. obtusa canbegin as early as silver tip and occurthroughout the season, whereas infections byB. dothidea occur mainly during the warmsummer months. B. obtusa infections developinto firm brown lesions on the fruit andB. dothidea infections develop into lightbrown, soft, watery rots.

B. obtusa infections can occur on the sepalsas soon as the buds begin to open. Theseinfections spread into the fruit as they beginto mature, resulting in a firm brown rot onthe calyx end (Plate 18.10). Other fruit infec-tions can occur from soon after petal fall untilharvest during favourable weather (Arauzand Sutton, 1989). Infections that occur soonafter petal fall first appear as small, dark pim-ples. As lesions enlarge, they become darkand irregular in shape and are often sur-rounded by a red halo. Eventually the entirefruit may become rotten and shrivel, remain-ing attached to the tree. Leaf spots (known asfrog-eye leaf spot) begin as small purple tobrown necrotic lesions, which enlarge to4–5 mm in diameter and are often sur-rounded by a purple halo. When infectionsare numerous, leaves may turn yellow andabscise.

B. dothidea infections can occur from soonafter petal fall until harvest (Parker andSutton, 1993). Infections that occur early inthe season often remain quiescent and donot begin developing until the solublesolids in the fruit begin increasing. Thisoften leads growers to think that their late-season spray programme is ineffective,when in actuality the disease increase thatthey are observing is more closely related totheir spray programme earlier in the season.As lesions begin to develop on the fruit,they extend in a cylindrical manner towardsthe core. Once the core is invaded, the entireapple becomes infected. Rotten fruit areoften light tan in colour and are very soft

and mushy (Plate 18.11). Under cooler tem-peratures, the rot tends to be darker incolour and firmer, making it more difficultto separate from black rot. Infected fruitmay fall or may remain attached to the treeand mummify.

Control of the black rot and bot rot isbased on sanitation and preventive fungicidesprays. Colonized dead wood and mummi-fied apples can both serve as inoculumsources. Wood infected by the fire blightpathogen can become colonized by thesefungi and produce spores during the currentgrowing season. This wood should beremoved during the early summer. Pruningsshould be chopped by a flail mower orpushed out of the orchard and burned.Fungicides should be applied every 10–14days from petal fall to harvest. Captan andthe benzimidazole fungicides are most effec-tive; the dithiocarbamate fungicides are notespecially efficacious.

18.3.4.3 Sooty blotch and fly-speck

Sooty blotch and fly-speck are two of themost common diseases in humid growingareas. While they do not reduce yield,affected fruit are usually downgraded fromfresh-market to processing or juice grades.Sooty blotch is a disease complex caused byseveral fungi and is characterized by dustyto dark colonies of fungi growing epiphyti-cally on the surface of the fruit (Williamsonand Sutton, 2000; Plate 18.12). They rangefrom small discreet colonies to large, amor-phous ones. Each colony has a characteristicappearance, depending on the fungusinvolved. Fly-speck colonies are character-ized by numerous thyrothecia, which arescattered throughout the thallus, giving it anappearance of ‘fly-specks’ (Plate 18.13).Colonies range from several to many mil-limetres in diameter.

Sooty blotch is a disease complex causedby Peltaster fructicola Johnson, Sutton &Hodges, Leptodontium elatius (G. Mangenot)De Hoog, Geastrumia polystigmatis Batista &M.L. Farr and probably other fungi. Thesefungi grow superficially on the cuticle ofaffected fruit. All have numerous reservoirhosts in the wooded areas in close proximity



to orchards and most inoculum comes fromoutside the orchard. Conidia of P. fructicolaand G. polystigmatis are primarily water-borne and are spread by wind-blown rain;conidia of L. elatius are airborne. Infectioncan occur as early as several weeks afterpetal fall. Symptom expression is closelyassociated with the hours of wetting thatoccur in the spring. Brown and Sutton (1995)found that the first symptoms of sooty blotch(and fly-speck) appeared after an average of273 h of leaf wetting of 4 h duration orgreater accumulated following the first rainwhich occurs 10 days after petal fall. P.fructicola, G. polystigmatis and L. elatius allproduce conidia on fruit, which serve assecondary inoculum. All apple cultivars areequally susceptible, but the colonies aremore visible on light-skinned cultivars.Washing and brushing in the packing linecan often remove small colonies with lightlypigmented thalli.

Fly-speck is caused by Schizothyrium pomi(Mont.: Fr.) Arx (anamorph Zygophialajamaicensis E. Mason). Ascospores of S. pomi,which are produced in thyrothecia on reser-voir hosts, provide the primary inoculum forinfections. While some infections occur onfruit, the most important infections occur onreservoir hosts, which serve as a source ofinoculum (conidia) throughout the growingseason. Moisture and temperature require-ments for colony development are similar tothose of the fungi causing sooty blotch. Whilethe fungi that cause sooty blotch grow super-ficially on the cuticle, Z. jamaicensis metabo-lizes the cuticle and the incipient thyrotheciabecome firmly attached to it, making thecolonies difficult to remove during washingand brushing in the packing line. There areno differences in susceptibility among culti-vars to either fly-speck or sooty blotch.

Control of sooty blotch and fly-speck isbased on sanitation to remove reservoirhosts, pruning to open the canopy and facili-tate drying, thinning fruit clusters toimprove drying, and fungicide sprays. Thebenzimidazole and dithiocarbamate fungi-cides are most effective; captan is not veryeffective. The benzimidazole fungicides havesome eradicant activity against the diseases.Brown and Sutton (1995) developed a model

for timing sprays of benzimidazole fungi-cides to manage sooty blotch and fly-speck.They found that sprays of benzimidazolescould be omitted in the cover-spray pro-gramme until 225 h of wetting had accumu-lated. In dry years, using the model couldsave three to five spray applications.Rosenberger (Agnello et al., 1999) andHartman and Smigell (Hartman, 1995;Smigell and Hartman, 1998) have modifiedthis model for their growing regions.

18.3.4.4 Brooks fruit spot

Brooks fruit spot caused by Mycosphaerellapomi (Pass.) Lindau affects apples primarilyin the south-eastern and mid-Atlantic apple-growing regions of the USA (Sutton et al.,1987). Symptoms on fruit appear as small,slightly sunken, superficial lesions on thefruit (Plate 18.14). Lesions resemble corkspot, but there is no corky tissue beneaththem. Leaf spots appear as small purpleflecks on leaves (Plate 18.15). Affected fruitare often downgraded from fresh-market toprocessing or juice grades.

M. pomi overwinters in apple leaves andascospores are discharged from pseudothe-cia during rainfall. The ascospores are pro-duced during a distinct period, about 6weeks in duration, beginning about 2 weeksafter petal fall (Sutton et al., 1987). Symptomsdo not appear on fruit and leaves until 6–8weeks after infection. There is no secondaryspread. There are some differences amongcultivars; ‘Golden Delicious’, ‘Rome Beauty’,‘Stayman’ and ‘Idared’ are quite susceptible;‘Delicious’ is relatively resistant. A preven-tive fungicide program that includes adithiocarbamate or benzimidazole fungicidecontrols the disease.

18.3.4.5 Alternaria blotch

Alternaria blotch, caused by Alternaria maliRoberts (= Alternaria alternata apple patho-type), was first reported in the USA in thelate 1980s (Filajdic and Sutton, 1991). Thedisease affects ‘Delicious’ and cultivars with‘Delicious’ as a parent (e.g. ‘Empire’) and ischaracterized by circular, necrotic spots onthe leaves (Plate 18.16), which, when abun-



dant, can cause extensive defoliation.Defoliation by the fungus is exacerbated bymite injury. A. mali and the European redmite act synergistically to increase defolia-tion (Filajdic et al., 1995). When defoliation isextensive, fruit size and soluble solids arereduced. Fruit symptoms are usually limitedto small, corky, dark lesions, often associatedwith the lenticels.

The fungus overwinters in leaves on theorchard floor and to a lesser extent in leafbuds. Infection by airborne conidia occurswithin a month of petal fall if temperatureand moisture conditions are favourable. Thenumerous secondary cycles that can occurthroughout the growing season may result inextensive defoliation.

Control of the disease is based primarilyon preventive control of mites to minimizedefoliation. Most fungicides currently regis-tered for apples in the USA, with the excep-tion of the strobilurins, have little effect onAlternaria blotch.

18.3.4.6 Black pox

Black pox, caused by Helminthosporium papu-losum Berg., is a problem, especially on‘Golden Delicious’ in the south-eastern USA.It is characterized by small, black, slightlysunken lesions, 3–9 mm in diameter on thefruit (Plate 18.17). Leaf spots begin as redhaloes with light green centres, enlarge to1.5–11.0 mm and turn tan to brown with pur-ple borders (Taylor, 1963). H. papulosum over-winters in twig lesions. Conidia produced inthese lesions initiate infections during thesummer. Black pox is one of the least-studiedsummer diseases, and conditions favouringinfection are not known. Preventive fungicidesprays of dithiocarbamate or benzimidazolefungicides provide effective control.

18.3.4.7 Necrotic leaf blotch of ‘GoldenDelicious’

Necrotic leaf blotch is a physiological disor-der that affects primarily ‘Golden Delicious’and its progeny (Sutton and Sanhueza, 1998)and is a particular problem on the new culti-var ‘Pacific Rose’. It is characterized by thesudden appearance of large, irregular

lesions, often bounded by veins. Mid-shootleaves are most severely affected. Lesions areinitially pale green, over a few hours turnchocolate brown and, as they age, oftenappear tan (Plate 18.18). Severely affectedleaves turn yellow in a few days and abscise.The disorder appears following periods ofcloudy, cool weather during the summer andcan result in 50% or more defoliation. It hasbeen associated with an increase in the pro-duction of gibberellins, which is triggered byenvironmental factors. Necrotic leaf blotchcan be controlled by applications of heavymetal-containing fungicides, such as ziram,thiram, mancozeb and Bordeaux, or foliarnutrient sprays (e.g. zinc oxide).

18.3.5 Phytophthora crown and root rot

Phytophthora crown and root rot is a poten-tially serious soil-borne disease whereverapples are grown. The disease is prevalentwhen susceptible rootstocks are planted inheavy soils or in areas of poor soil drainage.Infected trees exhibit a variety of symptoms.During summer, foliage on infected treesmay appear light green. As the season pro-gresses, leaves on infected trees turn a red-dish-bronze. Branches on infected treestypically have stunted leaves and poor ter-minal growth. Fruit on infected trees issmaller than normal and colours prema-turely. Accurate diagnosis of Phytophthoracrown and root rot frequently requires dig-ging in order to expose the upper portionsof the root system. Infected tissue is reddishbrown and delineated from healthy tissueby a definite margin (Plate 18.19). Diseasedtrees are often randomly distributedthroughout a planting. The disease is some-times confused with the rootstock phase offire blight.

The Phytophthora species present, soilmoisture and temperature, relative resistanceof the rootstock and contamination of nurserystock all affect the incidence and severity ofthe disease (Welsh, 1942; Sewell and Wilson,1959; Browne, 1984; Jeffers and Aldwinckle,1986; Ogawa and English, 1991). The diseasecan result from infection by any of severalspecies in the genus Phytophthora: P. cactorum,



P. cryptogea, P. cambivora, P. megasperma, P.syringae, P. citricola and P. drechsleri. Thesefungi can persist in soil for extended periodsof time as thick-walled sexual spores, calledoospores. When soil becomes saturated andtemperatures are conducive for sporulation,oospores germinate to produce sporangia.Within sporangia are numerous unicellularmotile spores that are liberated into the soilwater. The spores, known as zoospores, swimshort distances in the soil pore spaces or canbe transported longer distances by runoff orirrigation water. When zoospores contactroots of susceptible hosts, they germinate andestablish new infections. Zoospores are liber-ated only when soil is saturated. Prolongedflooding favours the production of sporangiaand dissemination of zoospores and may alsopredispose the host to infection. The majorityof new infections are initiated between thepink stage of blossom development and thebeginning of shoot elongation. The optimumtemperature for disease developmentdepends upon the Phytophthora species pre-sent, but in general soil temperatures between20 and 30°C favour the disease.

Phytophthora crown and root rot is man-aged through the integration of chemical andcultural practices. Two of the most importantdecisions of the producer are to plantpathogen-free nursery stock and to avoid theuse of susceptible rootstocks. Rootstocksvary in their susceptibility to the variousspecies of Phytophthora. The vast majority ofrootstock-susceptibility evaluations havebeen conducted using P. cactorum. TheMM.104 and MM.106 rootstocks are particu-larly susceptible to the disease, while M.9 isrelatively resistant. During planting, orchardmanagers should ensure that the graft unionis not in contact with soil. Heavy or poorlydrained soils should be avoided. In irrigatedareas, water should be managed to avoidprolonged flooding and the presence ofstanding water around the base of trees.Plantings are sometimes established onraised beds in order to facilitate drainagearound the base of trees. Acylalanine andethyl phosphonate fungicides available forcontrol of this disease are applied as soildrenches or foliar sprays, respectively(Jeffers and Wilcox, 1990).

18.3.6 European or Nectria canker

Nectria or European canker is circumglobalin distribution and particularly problematicin northern Europe and parts of SouthAmerica (Grove, 1990). The disease is consid-ered minor in most of North America, butcan be a serious problem in the productionareas of coastal California. The disease ischaracterized by zonate cankers located onthe main trunk or scaffold limbs (Plate18.20). Young infected tissue is darker thansurrounding healthy tissue. Limb or treedeath can occur from girdling, which resultsfrom canker enlargement. A layer of callustissue is formed annually around eachcanker. The fungus invades callus tissue andspreads to healthy tissue outside the calluslayer. Over a period of years this results incankers with characteristic zonate appear-ances. In some areas nurseries are importantsources of infected trees.

The disease is caused by Nectria galligenaBres. The fungus produces ascospores andconidia in orange-red fruiting-bodies pro-duced in twig, branch or trunk cankers. Sporesare produced in a gelatinous matrix and dis-persed by the impaction of water droplets.The disease can be aggravated by over-the-canopy irrigation. Infection occurs throughleaf scars and pruning wounds. Nectria cankeris favoured by cool, moist weather.

An integrated approach is required forsuccessful disease management. Diseasedwood should be removed from the orchardand destroyed. Young infected trees should beseverely pruned or removed. In some areasdiseased bark is removed to prevent sporeproduction. Copper fungicides (e.g. Bordeauxmixture) are sometimes applied prior toautumn rains in order to protect leaf scars.

18.4 Postharvest Diseases

Apples are also host to a multitude ofpostharvest diseases and disorders. The for-mer are caused exclusively by pathogenicfungi. Two of the more serious postharvestdiseases are blue mould and grey mould,which are the first and second most impor-tant postharvest diseases of apple, respec-



tively. Most postharvest pathogens invadefruit wounded during harvest, shipping orhandling. Therefore, the management ofpostharvest diseases begins with very carefulfruit harvest, bin sanitation and transport.Fruit bins used for transport should be freeof soil, leaves and rotten fruit debris. Fruitshould be picked individually and placedvery gently into bins. Orchard access roadsshould be smooth and free of ruts and majorbumps. Bins should be transported at speedsthat will not result in shifting or bouncing.Additional means of postharvest diseasemanagement include packing-house sanita-tion, rapid immediate postharvest cooling,fungicide drenches and the provision of ade-quate tree nutrition.

18.4.1 Blue mould

Blue mould, which is caused by fungi in thegenus Penicillium, is the most commonpostharvest disease of apple (Rosenberger,1990; Plate 18.21). Decayed flesh is soft andwatery and separates readily from healthytissue. Infected epidermal tissue is light todark brown. Infected fruit are malodorous.The causal organism produces blue or blue-green conidia on the surface of infected fruit.Penicillium spp. are present in orchard soilsand on decayed fruit in the orchard andpacking-house and in postharvest drenchsolutions and flume water. Fruit infectiontypically occurs through wounds. Woundingshould be prevented during harvest, ship-ping and processing. Infested fruit bins andwarehouses should be disinfested beforeprocessing fruit.

18.5 Diseases Caused by Viruses,Viroids, Phytoplasmas and Other Virus-

like Agents

Viruses or virus-like agents incite over 50described diseases of apple. These agentsinclude viruses, viroids and phytoplasmasand several graft-transmissible agents thathave yet to be identified. Some of these dis-eases have great economic consequences inthat they are associated with fruit deformi-

ties or severe tree decline and even death.The degree of affliction depends greatly onthe rootstock and scion selection, pathogenisolate and climate. Viruses or virus-likeagents that incite severe symptoms on someapple selections will cause no obvious symp-toms on others. However, even in the lattercase, significant yield reductions have beendocumented in the few studies undertakento study such effects (van Oosten, 1983).Thus, infections by viruses and virus-likeagents are important to the commercial pro-duction of apples.

Although most of these agents do notspread naturally, many are common in com-mercial orchards. The universal presence ofmany of these agents is due to collectinggrafting material from infected but appar-ently symptomless trees while preparing forvegetative propagation of new trees. Thepropagation of trees from infected sourcesultimately affects yield and, under certainenvironmental circumstances or clone com-binations, results in orchards that are noteconomically productive due to fruit-qualityissues or tree decline. The only reasonablemethod for controlling these diseases is theinitial use of virus-tested propagation materials.

Quick and reliable diagnostic assays areavailable for a few of the viruses and virus-like agents that infect apple. However, forthe most part, detection of such infections isa cumbersome and laborious proposition.Furthermore, only a few of the agents thatincite these diseases have been identified.The use of modern laboratory diagnosis isprecluded until such identifications aremade. Most assays for these agents are con-ducted by inoculative assays on sensitivewoody indicator selections; these testsrequire 2 months to 3 years to complete.

Aetiological studies of viruses that infectwoody plants are greatly enhanced if thevirus is first transmitted to a herbaceoushost. Unfortunately, many of the virus-likeagents that elicit disease in apple trees havenot been successfully transmitted to herba-ceous plants and therefore are called ‘non-sap-transmissible’. This may simply meanthat the correct combinations of host plantsand transfer conditions have not yet been



found. The significance of this limitation isthat progress towards characterization ofthese pathogens has been dramaticallyslowed. Nevertheless, the non-sap-transmis-sible viruses of fruit trees present a veryinteresting and challenging group of viruses,since relatively little is known about them.Contemporary methods in molecular biol-ogy have accelerated investigation of thesepathogens.

Pathogens are frequently referred to asviruses based on the ability to transmit thepathogen by grafting and/or budding andthe absence of any other obvious pathogens.This simplistic distinction is often incorrect.Many disease-causing agents are more cor-rectly referred to as ‘virus-like’ agents sinceno direct association between a pathogenand disease has been established – that is,Koch’s postulates have not been fulfilled.

The disease names commonly used in theliterature are descriptive of the disease andhost but provide little information about thepathogen. Consequently, a pathogen or vari-ant thereof may be associated with differentdisease names, depending on the symptomproduced, the latter frequently affected bycultivar and environment. With advances inour ability to isolate and characterize fruit-tree pathogens at the molecular level, thiscomplicated structure of nomenclature isevolving to reflect more accurately thenature of the pathogen, rather than thesymptoms that they elicit. This is of practicalas well as academic importance. By relatinga pathogen to other members of a group that

share many important qualities, we may beable to predict the behaviour of thatpathogen based on the epidemiology of afew well-studied pathogens in the samegroup.

The list of apple diseases caused by‘virus-like’ agents is alarming in its length.However, many of these disease names wereapplied locally to a particular symptom andthus many of the names are duplicative.Also, many of these diseases have very lim-ited distribution. Only diseases that remainof a more general importance will be dis-cussed in detail. For an expanded list ofreported diseases of apple that are inducedby virus-like agents, see Németh (1986).

18.5.1 Chlorotic leaf spot

Relatively few well-characterized virusesare routinely found in the Malus of com-merce (Table 18.3). Each of these virusesincites disease with major characteristics onselected host cultivars that help identify thedisease agent.

The causal agent apple chlorotic leaf-spot trichovirus (ACLSV) is one of the mostwidely distributed viruses of fruit trees.Although first described as a virus inapples, it was subsequently found to bevery widespread in stone fruits, where itcan cause severe losses in production.Although the interaction of ACLSV withmany commercial apple cultivars is latent, itwas first discovered associated with the


Table 18.3. Diseases of apple with known virus aetiology and their vectors.

Known means of Disease Causal agent transmission

Apple chlorotic leaf spot Apple chlorotic leaf-spot trichovirus GraftingApple decline Apple stem-grooving capillovirus Grafting(on Virginia crab)

Apple mosaic Apple mosaic ilarvirus GraftingApple mosaic (Tulare) Tulare apple-mosaic ilarvirus GraftingApple stem grooving Apple stem-grooving capillovirus GraftingApple stem pitting Apple stem-pitting foveavirus GraftingApple union necrosis Tomato ringspot nepovirus Nematodes and graftingFlat apple Cherry rasp-leaf nepovirus Nematodes and graftingSpy decline Apple stem pitting foveavirus Grafting


decline and death of new Malus breedinglines in an apple-scab-resistance breedingprogramme. Over the past few decades,there have been several examples where theinteraction of the virus with specific root-stocks is not latent. The top-working dis-ease of Japan is believed to be ahypersensitive reaction of rootstocks (Malusprunifolia var. ringo) to isolates of ACLSVfound in contaminated apple scions fromNorth America. This resulted in significantfailure of mature trees (reviewed in Mink,1989). The death of cells at the graft unionresults in weakened trees with reducedvigour and productivity and which are verysusceptible to wind damage.

ACLSV is diagnosed by serological test-ing, indexing on herbaceous hosts(Chenopodium quinoa) or budding to Malusindicator species, usually Malus sylvestris cv.R12740-7A (also known as ‘Russian’). In thelatter case, chlorotic leaf symptoms appearsoon after new leaves develop unless theambient temperature rises above 20°C. Lowvirus titre and inhibitors in Malus often limitthe use of serology or indexing on herba-ceous plants. Molecular techniques of diag-nosis, such as RT-PCR, are becoming morecommon methods of diagnosis (Kummert etal., 1995; Kinard et al., 1996). The extremestrain variation of ACLSV has limited thewidespread acceptance of serological andmolecular methods.

18.5.2 Apple decline (on ‘Virginia Crab’)

Infection of most apple trees with applestem-grooving capillovirus (ASGV) is latent– that is, there are no acute symptoms visi-ble. However, when infected scion materialis grafted on to sensitive rootstocks, such asM. sylvestris cv. ‘Virginia Crab’, growth anddevelopment of the ‘Virginia Crab’ woodcylinder is impaired and deep groovesappear under the bark. The vascular tissueof the ‘Virginia Crab’ often becomesnecrotic, resulting in weakness and a visiblebrown line at the graft union. The treesoften break at this necrotic union (Németh,1986). Stem grooving caused by ASGV isnot seen on current commercial apple

cultivars, but appears on rootstocks withcrab apple in their heritage.

ASGV can be diagnosed by herbaceousindexing on C. quinoa, although this methodis not very reliable. Woody indexing onMalus micromalus GMAL273.a or M. sylvestriscv. ‘Virginia Crab’ (Howell et al., 1995) ordetection by RT-PCR is the preferred methodof testing (Kummert et al., 1995; Kinard et al.,1996).

18.5.3 Flat apple

This disease is caused by cherry rasp-leafnepovirus (CRLV) (Parish, 1977), a virusthat is believed to be native to westernNorth America, ranging from Utah tosouthern British Columbia. CRLV isbelieved to have originated in one or twospecies of native vegetation and subse-quently been transmitted into horticultur-ally important crop plants, such as appleand cherry. The symptoms in apple aremost striking on the fruit of ‘Red Delicious’and related cultivars. The length of the fruitis significantly reduced to produce a fruitthat is squat, and the stem cavity is almostabsent (Plate 18.22). At first, only a few fruitwill be affected, but eventually the entiretree will be involved.

CRLV is transmitted by the nematodeXiphinema americanum (sensu lato) (Wagnon etal., 1968). Therefore, secondary spread of thedisease is relatively slow. Apple treesplanted on sites previously planted to rasp-leaf-diseased cherry trees can becomeinfected. In addition to fruit trees, manyorchard weeds, such as dandelions and plan-tains, are hosts, although they exhibit nosymptoms of the disease. This makes elimi-nation of the virus from an infected orchardvery difficult. The alternative hosts and/orthe nematode vectors would have to be elim-inated to protect replanted trees.

Since CRLV achieves high concentrationin young shoots, it can be readily detectedby serology and by mechanical inoculationof C. quinoa with extracts from young leavesin early spring. Leaf symptoms and tipnecrosis on C. quinoa usually develop 3 daysafter inoculation.



18.5.4 Apple mosaic

Apple mosaic ilarvirus (ApMV) induces dra-matic white bands or patterns on leaves ofmany apple cultivars (Plate 18.23). Affectedleaves may have irregular distributionthrough the tree or even on individual limbs.The severity of the symptoms can vary dra-matically from year to year, with symptomsbeing almost undetectable in seasons withhigh temperatures during the growing sea-son. This disease can result in significantproduction losses (ranging up to 40%)depending on the cultivar, virus isolate andenvironment (Posnette and Cropley, 1956).

ApMV is detected by serological assaysbut results (when apple tissue is tested) arevariable. Therefore, serological testing is bestlimited to confirming the identity of thepathogen in herbaceous indexing. ApMV canalso be detected by inoculating field-growntrees of ‘Golden Delicious’ apple. Herbaceousindexing on C. quinoa is possible but quiteunreliable. Molecular methods of detection,such as RT-PCR (Rowhani et al., 1995), arebecoming more widely accepted, as themethods are evaluated with more and variedisolates of the virus.

18.5.5 Stem pitting

The viral nature of apple stem pitting wasdiscovered soon after the Second World Warin mid-western North America (Guengerichand Millikan, 1956). Production of crabapples had become uneconomic and old crabapple rootstocks were budded over to stan-dard cultivars, such as ‘Delicious’. Two orthree years after budding, the crab applerootstocks became pitted and severely weak-ened. This is an example where the ‘latent’virus in the ‘Delicious’ scion resulted in sig-nificant economic damage when the varietywas budded on to rootstocks with crab applein their heritage. Apple stem-pitting fovea-virus (ASPV), the causal agent of apple stem-pitting disease, is thought to have beendistributed worldwide in contaminatedapple and pear propagation material.

Woody indexing on any one of a variety ofMalus species is the method most frequently

used to detect ASPV. Epinasty and declinemay be observed after 1 year when ‘Spy227’ isthe recipient. ‘Radiant’ crab apple is a morereliable detection host. It is sensitive to a widerange of ASPV isolates and displays severeepinasty and decline within 6 weeks undercontrolled greenhouse conditions. The devel-opment of stem-pitting symptoms on‘Virginia Crab’ is also reliable, but at least twogrowing seasons are required for trustworthyresults. Fruit with ridges and flutes are pro-duced if the ‘Virginia Crab’ is allowed to bear.Molecular methods are also available for thedetection of ASPV. RT-PCR (Nemchinov et al.,1998) is sensitive and offers faster diagnosisrelative to woody indexing.

18.5.6 Union necrosis

Union necrosis is caused by tomato ringspotnepovirus (TmRSV) (Stouffer and Uyemoto,1976). Symptoms of infection generally donot appear until the tree reaches bearing age,at which time the tree assumes an unthriftygrowth habit. The leaves and bark are red-dish in colour, and bloom and fruit set areabnormally high. Depending on the root-stock/scion combination, the results of infec-tion may range from very mild to a rapiddecline in tree health, resulting in death. Insevere reactions (‘Red Delicious’ on MM.106),the union of rootstock and scion will reveal adark necrotic line spanning the union, withsoft, spongy, orange bark flanking the union.This disease is common in several localesalong the east coast of North America, andhas been reported sporadically in the PacificNorthwest of the USA. TmRSV is transmittedby dagger nematodes, X. americanum (sensulato), which are abundant in eastern fruit-growing areas of North America (Stoufferand Powell, 1989). Other species belonging tothis nematode group, Xiphinema revesi andXiphinema californicum, are also known to bevectors of TmRSV in orchards.

TmRSV is easily transmitted from youngleaves to C. quinoa by mechanical inoculationwith crude extracts. Prunus tomentosa is a diag-nostic woody host for this virus. Alternatively,serological and RT-PCR (Griesbach, 1995)assays can be used to detect it.



18.6 Diseases Caused by Phytoplasmas(Table 18.4)

18.6.1 Proliferation

Apple proliferation occurs throughout muchof Europe, but has not been reported in thewestern hemisphere. The disease is causedby an apple proliferation phytoplasma. Thepattern of occurrence in European orchardssuggests that the pathogen is harboured inthe native weed population, from which itmoves into the orchards. The vector of thispathogen is at least one species of leafhop-per, Fieberiella florii. This disease reduces fruitsize by up to 30–70% and fruit have longerthan normal peduncles. However, the moststriking symptom, for which the disease isnamed, is the proliferation of vegetativeshoots, otherwise known as witches’-broom.In addition, apple leaves exhibit greatlyenlarged stipules. Because the disease isdebilitating and insect-vectored, apple prolif-eration disease has important quarantine sig-nificance in the western hemisphere.

The most widely accepted detectionmethod for apple proliferation phyto-plasma has been woody indexing in thefield. Bark patches from roots of the testplant are budded on to ‘Golden Delicious’and the tree is observed for 2 years for theappearance of witches’-broom and theenlarged stipules. However, the long obser-vation period and concern about reliabletransmission of the pathogen encouragedthe development of alternative detectionmethods. Detection by PCR (Lorenz et al.,1995) is becoming widely accepted and thetechniques are becoming increasinglyrefined to improve the reliability of molecu-lar methods (Carraro et al., 1998;Skrzeczkowski et al., 2001). PCR is now thepreferred test method.

18.6.2 Chat fruit

Apple chat fruit is believed to be caused byphytoplasma infection. Sensitive cultivarsdevelop undersized fruit, many of whichdrop in June. The remaining fruit do notdevelop colour properly and may exhibitdark water-soaked spots. Many of the cur-rent commercial cultivars do not express anysymptoms of apple chat fruit. The pathogenis detected by budding on to ‘LordLambourne’. An incubation period of up to 3years is required for reliable detection. Untila firm association of a biological agent withapple chat-fruit disease can be established,the use of biological indicators remains theonly means of detection.

18.7 Diseases of Apple Caused by Viroids(Table 18.5)

Viroids are sub-virus particles that are diffi-cult to detect. Since proteins are not part oftheir structure, serological methods are notuseful. Woody indexing and moleculardetection methods are commonly used todiagnose these pathogens.

18.7.1 Blister bark

Apple blister bark is characterized by areasof the bark taking on the appearance oforange tissue-paper. The disease can beinduced by apple fruit-crinkle viroid(AFCVd) (Ito et al., 1993). As the underlyingtissue becomes desiccated, the bark cracksand peels. Scarring of the underlying tissueoccurs. Several mineral deficiencies canmimic infection by AFCVd, so proper diag-nosis is important.


Table 18.4. Diseases of apple suspected to be caused by phytoplasma.

Known means ofDisease Causal agent transmission

Apple chat fruit Phytoplasma GraftingApple proliferation Apple-proliferation phytoplasma Leafhoppers and grafting


18.7.2 Dapple apple

Dapple apple aptly describes one of the dis-eases caused by apple scar-skin viroid (ASSVd).Affected fruit, especially near the calyx end,bear small circular spots, which enlarge andincreasingly contrast with the backgroundcolour as the fruit matures (Plate 18.24). Largerspots may coalesce to produce dappling or abroad zone of discoloration. There are no pro-nounced leaf or bark symptoms. Since manycommercial cultivars do not express symptoms,this disease has been particularly problematicwhen old orchards are top-worked to changecultivars. The original cultivar may not expresssymptoms, whereas the new cultivar does. Pearalso appears to be a symptomless carrier ofASSVd; the role of pear as a symptomless car-rier of this pathogen in apple-disease aetiologyis unknown. ‘Stark’s Earliest’ (‘ScarletPimpernel’) or ‘Delicious’ can be used forwoody indexing, and three crops must beobserved for accurate assessment of viroid sta-tus. ‘Scarlet Pimpernel’ grown at 18ºC underconstant light for 2 months will yield diagnosticsymptoms on its foliage (Skrzeczkowski et al.,1993). Molecular techniques are preferred fortheir speed and reliability. Both RT-PCR(Hadidi and Yang, 1990) and hybridization(Hadidi et al., 1991) assays are used for ASSVd.

Apple scar-skin disease is a more severedisease caused by ASSVd, as compared withthe milder one referred to as dapple apple.Symptoms usually begin at the distal portionof the fruit and the severity increases as thefruit matures. Small discoloured circles mergeto form large green-brown to brown patches(Plate 18.25). Eventually, the brown patchesbecome necrotic and fissures appear on thefruit. Diseased fruit are significantly smaller

than fruit from uninfected trees. Diagnosis isperformed as described for dapple-apple dis-ease. The dapple and scar-skin diseasesevoked by ASSVd appear to be dependentupon climatic and cultivar differences. Theoriginal isolates of each produce similar dis-eases on fruiting trees of ‘Scarlet Pimpernel’ (W.E. Howell, Washington State University,unpublished data).

18.7.3 Dimple fruit

Apple dimple fruit caused by apple dimple-fruit viroid (ADFVd) has been observed inseveral commercial cultivars of southernItaly (DiSerio et al., 1996). The diseaseinduces depressions on the fruit surface as itmatures. Under the depression will be anarea of necrotic tissue.

18.7.4 Fruit crinkle

Apple fruit-crinkle disease is caused by iso-lates of AFCVd (Ito et al., 1993). The viroidwas described in Japan, where fruit symp-toms are most severe on the cultivar ‘Ohrin’.This pathogen can be detected by woodyindexing on the apple cultivars ‘Delicious’or, preferably, ‘NY5822’, where it inducessymptoms of blister bark (Ito et al., 1993).

18.8 ’Virus-like’ or Graft-transmissibleDiseases of Apple with No Known Causal

Agents (Table 18.6)

There are many diseases of apple for whichno pathogen has been identified. The disease


Table 18.5. Diseases of apple known to be caused by viroids.

Known means of Disease Causal agent transmission

Apple blister bark Apple fruit-crinkle viroid (AFCVd) GraftingApple dimple fruit Apple dimple-fruit viroid (ADFVd) GraftingApple fruit crinkle Apple fruit-crinkle viroid (AFCVd) GraftingApple scar skin Apple scar-skin viroid (ASSVd) GraftingDapple apple Apple scar-skin viroid (ASSVd) Grafting


names are generally descriptive of the symp-toms. Some may be caused by pathogensdescribed above but, until more informationis obtained about their aetiology, the causalagents remain an enigma. Since the agents forthese diseases have not been identified, con-firmation of the pathogen depends on symp-tom expression on susceptible cultivars. Allare graft-transmissible. Furthermore, as mostof these diseases are spread primarilythrough the use of infected propagationmaterial, the creation of virus-certificationprogrammes over the past 40 years has essen-tially eliminated many of these diseases fromcommercial apple production. Still a few con-tinue to cause concern.

18.8.1 Green crinkle

Apple green-crinkle disease, a severelydebilitating disease of some apple cultivars,is always associated with trees infected withASGV, ASPV and ACLSV. The individualviruses have not been separated to deter-mine if this disease symptom is induced by amixture of viruses, by a particular isolate ofone of the viruses or by another as yetuncharacterized pathogen. Apple green-crin-kle disease is diagnosed by woody indexingon the apple indicator ‘Golden Delicious’.The trees are observed for the developmentof fruit symptoms during the following threecrops. Symptoms begin to appear after thefruit reaches 1–2 cm in diameter. Fruitsdevelop deep depressions and distortions,which become more severe as the fruitsmature. Cracks may develop in pits andcrevices (Plate 18.26). Depressions are linkedthrough the flesh to the vascular system bydiscoloured tissue. Severe fruit symptoms

may appear on only one or two limbs of aninfected tree, and there are no acute foliarsymptoms associated with the disease(Thomsen, 1989). Budding and grafting ofcontaminated propagation material is themajor mechanism by which apple green-crinkle disease is spread. If field spreadoccurs, it is very slow and possibly by rootgrafting only.

18.8.2 Rubbery wood

Apple rubbery wood affects 2-year-old woodof apple and pear trees. On sensitive culti-vars, branches develop that are very pliableand droop under their own weights(Waterworth and Fridlund, 1989). Affectedlimbs are also very sensitive to cold and frostdamage. The disease originated in Europeand was later introduced to North Americawith infected rootstock. Many older root-stocks introduced from Europe were uni-formly infected with rubbery wood. Incountries with active certification pro-grammes, this disease has become increas-ingly rare. The degree of symptomdevelopment is dependent on climate. Thepliable limbs and poor growth are moreextreme in moderate climates, relative towarmer environments. No obvious symp-toms are associated with many commercialcultivars. Nevertheless, fruit yield and qual-ity can be adversely affected (van Oosten,1983). The pathogen has been assumed to bea phytoplasma, based on electron-microscopic examination of affected tissues,but attempts to confirm this association bymolecular techniques have been contradic-tory (Poggi Pollini et al., 1995; Bertaccini etal., 1998). The disease is detected by indexing


Table 18.6. Graft-transmissible diseases of apple for which there are no known causal agents.a

Apple blister bark Apple green crinkle Apple ringspotApple dead spur Apple horseshoe wound Apple rosetteApple decline Apple internal bark necrosis Apple rough skinApple false sting Apple leaf pucker Apple rubbery woodApple flat limb Apple ring russet Apple pustule cankerApple freckle scurf Apple ring-line pattern

aThere are many more described but rare graft-transmissible diseases of apple (Németh, 1986).


on ‘Lord Lambourne’, followed by 3 years ofobservation for the development of limbslacking normal lignification.

Apple flat limb is believed to be causedby the same agent that causes apple rubberywood (see above). Apple flat limb is onlyobserved in those areas where sensitive culti-vars, such as ‘Gravenstein’, are grown. Thedisease results in flattening of the shoots andbranches on limbs that are 2–3 years old andeventually leads to deep furrows thatbecome more severe as the branches becomeolder (Fridlund and Waterworth, 1989). Inaddition to reduced vigour and production,the weak limbs are susceptible to easy break-ing. Severely affected limbs are also moresusceptible to winter or frost damage. Thedisease is detected by woody indexing on‘Gravenstein’ or ‘Lord Lambourne’, followedby 3 years of observation.

18.8.3 Dead spur

Apple dead spur was originally observed inthe western USA, but has since beenreported throughout North America and inEurope and Asia (Parish, 1989). The charac-teristic symptom is death of fruiting spurs,with the resulting development of long seg-ments of blind wood. This is most pro-nounced on the interior of the tree, so thecanopy in the centre of the tree is sparse,with fruiting spurs at the shoot tips. The dis-ease is spread through the use of infectedpropagation material. No natural spread hasbeen observed. The only means by which thediagnosis based on symptoms can be con-firmed is bud-inoculating spur-type‘Delicious’ trees. Symptoms will develop inthe third or fourth year after inoculation.Since this disease is difficult to diagnose, itmay be overlooked in virus-testing pro-grammes. Like green-crinkle disease, deadspur has not been observed in the absence ofACLSV, ASPV or ASGV. Therefore, althoughthe dead-spur agent poses a concern for thesafe propagation of healthy apple trees, elimi-nation from propagation programmes of treeswith these three ‘sentinel’ viruses may wellindicate freedom from this and other graft-transmitted diseases of unknown aetiology.

18.9 Control Measures

Very few viruses or virus-like agents of appledisease spread naturally in the orchard. Thismeans that the most efficient and cost-effec-tive control measure for apple virus diseasesis the use of propagation material and plantsthat are certified to be free from viruses. Oncethe trees are planted in the orchard, theyshould, for the most part, remain virus-free.Still, some spread of these pathogens occursin orchards via tree-to-tree root grafts. Suchroot grafts provide effective means by whichpathogens can move from an infected tree tothe next. However, this process is relativelyslow and involves spread only to adjacenttrees. Thus, if a diseased tree is detected in anestablished orchard, it may be prudent toremove adjacent trees to eliminate the virus.

In those cases where some form of naturalfield transmission exists, diseases can bemuch more difficult to control. Again, initialplanting of certified virus-free material is thefirst step in maintaining a healthy orchard.In European countries, where apple prolifer-ation phytoplasma is prevalent, regularinsecticide applications to control theleafhopper vector can significantly reducethe incidence of this disease (Kunze, 1976).

The two diseases of apple whose causalagents are known to be transmitted by nema-todes, flat apple and union necrosis, can bevery difficult to control. Exclusion of the virusinitially is crucial since, once the virus is pre-sent, it is very difficult to eliminate it from anorchard. Dagger nematodes, Xiphinema spp.,are nearly universal and difficult to eradicate.Fumigation and soil pretreatment before plant-ing will reduce but not eliminate these nema-todes from soil. Leaving the ground planted inplants that are not virus hosts for 1–2 yearsbefore replanting will help prevent transmis-sion of these viruses to the young trees. Thenematodes lose the ability to transmit theseviruses with each moult. Since many weedplants common in the orchard floor, such asdandelion and plantain, act as reservoirs ofthese two nepoviruses, intense weed control isrequired during this period of fallow. If theseviruses and their nematode vectors are presentin an area, it is best to select rootstock/scioncombinations that offer protection against thenematode and/or virus disease.



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