Plani Pathology {]<iHf,) 35.

477^90

Components of resistance of apple to powdery mildew

{Podosphaera leucotricha)

M, J. J E G E R * . D, J. BUTT ami A. A, J. SWAIT

East Mailing Re.search Station. Maidstone. Kent MEI9 6BJ. UK

Components of resistance of apple to Podn.sphaera leucotricha were assessed in the glasshouse by

spraying shoot tipsofcultivars with conidia. Disease incidence (proportion of leafsurfaces with mildew )
and colony numbers were higher and incubation periods correspondingly shorter on the older leaves,
unrolled at the time of inoculation. Numbers nf colonies were higher on the lower surface. Spore
production per colony was bigher on the younger !eii\es. In general, a shori ineubation period on a
cultivar was associated with a higb disease incidence, many colonies and high spore produetion. For
some eultivars the associatioti between these components permitted resistance to be classified as very
higb (cv. Discovery), very low (cv. Golden Delicious), or intermediate (evs Bramley's Seedling, Suntan).
The effects of inoculum concentration and post-inoculation environment (glassbouse or outdoors) on
components of resistance were assessed in a further study. No interactions between eultivar and
inocuiutn concentration were detected. There was generally an associated variation in components
between cultivars within an en\ironment, but inconsistencies in cultivar rankings were noted between
the two environments and the two studies. Mean incubation period was shorter and eolony area larger in
the glasshouse than outdoors. Tbere were significant differenees in conidia em- eolony between cultivars
onl\ in theglasshou.se. Components conferring high resistance in cv. Discovery and low resistance in ev.
Golden Delicious were confirmed in both environments and in both studies.

INTRODUCTION the rusts (Parlevliet. 1979). and powdery mildews

In the UK the climate favours powdery mildew of
apple, cau.sed by Podnsphaera leueoiricha (Ell. &
Everh.) Salm.. and intensive fungicide pro-
grammes are necessary for many commercial
cultivars (Butt & Jeger. 1982). Sources ol"major-
gene resistance have been identified and utilized
in breeding programmes (Alston. 1983). but have
made little conitnercial impact as yet in the UK.
Apple cultivars differ widely with respect to
orchard epidemics o{ powdery mildew (e.g.
Sprague, 1955; Alston. l%y; Aldwinkle. 1974;
Blazek et al.. 1979; Jeger & Butt. 1986). Differ-
ences in the rate of disease development or partial
resistance. .%ensu Parlevliet (1979), may be attri-
buted to cultivar differences in components of
resistance, such as infection frequency, latent
period, colony growth rate and j:pore produetion.
There has been much work on assessing compo-
nents of resistanee in annual crops, notably for
" Present address: Tropical Development and
Research Institute, 56 62 Gray's Inn Road. London
WC1X8LU. UK.
of cereals (Roberts & Caldweli. 1970; Shaner.
1973; Pauvert. 1976; Rouse et ai.. 1980).
This paper reports on components of partial
resistance (hereafter called resistance) to powdery
mildew in apple cultivars. including several culti-
vars of commercial importance in the UK. and on
the consistency of assessments over years, en-
vironment, and a range oi inoculum concentra-
tions. Eaeh of these three factors has been shown
to affect components of resistance to P. ieuco-
tricha {Roosjc et ai.. 1965; Kaspers, 1967; Butt c;
ai.. 1981). There is no evidence for physiological
specialization in apple mildew (Woodward. 1927;
Butt & Souter, 1973).
MATERIALS A N D M E T H O D S
Plant material and environment
1980 experiment
Thirty potted maiden apple trees of each of cvs
Bramley's Seedling, Cox's Orange Pippin. Cris-
478 M. J. Jeger et at.
p i n . Discovery,Golcien Delicious.Gratiny Smith.
I d a Red. Laxton"s Superb. Spartan. Suntan and
Tydeman"s Early Worcester, all on MM 106 root-
s i o c k . were fully randomized in an unbeated
glasshouse with ihermosial-controlled cooling
f a n and no artificial lighting at tbe end of March
1 9J4O, Each planl was cut buck lo ;i heigbi of
a b o u t 1 m to allow a single vigorous vegetative
s h o o t to grow from a lateral bud. Plants were
s p r a y e d with aphicide and acaricidc w hen necess-
a r y , but not with fungicide. The youngest
unroJIed JearfJej/O) on each shool was labelled
o n 1 2 May and its length and breadth measured.
Before inoculalion and during a brief period of
h o i weather, plants in the glas.sbouse were
e x p o s e d to a maximum of 32 C (screened bulbt
a n d a minimum of 36"i. RH. During inoculalion.
incubation, and the early period ofmildcv. assess-
m e n t , temperature and humidity were 6-28 C
a n d 55-92"'" RH. respectively. Later, and prior to
t h e harvesting of mildewed leaves, corresponding
r a n g e s were 12-25 C and 72-94% RH,
198/ experiment
T h i r t y potted maiden apple trees of each of cvs
B r a m l e y s Seedfing. Cox s Orange Pippin. Dis-
c o v e r y . Golden Delieious. Greensleeves, Jester.
S p a r t a n . Suntan. Tydeman's Early and Worces-
t e r Pearmain. on MM 106 rootstock. were divided
k n l o Iwo groups at the end ol" Mareh 1981. One
g r o u p (17 plants of each cuftivar) was stood in a
glasshouse programmed for 19 C (but with
recorded mean, minimum, and maximum tcm-
peratureii during the eKperitncnt of 19 7. 16 5 and
2 3 - 0 C. respectively), under natural illumination.
T h e other group (13 plants of each eultivar) was
s t o o d outdoors (corresponding temperatures
\K'crc I2'8. 9-.1 und J6 3 C). In each envjronmen)
t h e plants were arranged as a splii-plot design.
w i l h four main plots (inoculum concentrations)
w i l h i n blocks, and 10 sub-plots (cultivars) within
m a i n plots. There were four blocks in the glass-
h o u s e and ihres outdoors. In both environmerifs.
o n e plant of each cultivar was randomly posit-
i o n e d and used as an uninoculated control. Each
p l a n t was cut back to a hcigbt of about I m to
a l l o w a single vigorous vegetative shoot to grow
f r o m a laterat bud; all lower shool growths were
r e m o v e d in May, Tbe youngest unrolled leaf (leaf
O) o n eaeh shoot was labelled on I June in the
glasshouse and on the following day outdoors.
T h e plants were free of visible mildew colonies on
t h e s e dates.
lnDeulation
I9H0 experiment
Fresh conidia wen; harvested from potted mil-
dewed MM 106 rootstocks kept under glass and
were applied over a 6-h period on 13 May 1980,
using a wet inoeulation technique (Hunter &
Blake. 1978), Spore suspensions of 5 ml at 0'22
(±0-09)>cI0^ conidia/ml were prepared every
15 20 min by using a fine brush to detaeh conidia
from colonies into a non-ionic wetting ageni
(Agral. OJ m)/I. ImperiaJ Chemical Industries).
The shooi tips of 26 Irees (one shool per tree) of
each cultivar were sprayed with 0-25 ml of spore
suspension using a DeVilbiss .-Aerograph "Sprite"
Airbrusb. The spray was applied from all direc-
tion,'; al (he six Jeaves in posiliom —3 !O + 4 .
where Icui' 0 was the youngest unrolled leaf
labelled the previous day and leaf — I was the
adjacent and older unrolled leaf. Four plants of
each cultivar were covered by inverted brown
paper bags and not inocuJated.
1981 e.xperimeni
All plants, except the controls, were sprayed in a
separate glasshouse compartment with conidia of
P. leucotricha on 2 June (glasshouse plants) and
on 3 June (outdoor plants), using the same
method as in 1980. and were returned immedia-
tely to their respective environments. Only the
leaves at the shoot tip were inoculated, with the
lower (abaxial) surface of tbe inwardU rolled leaf
a I po.sition + 2 exposed to the spray, Suspen.sions
of conidia were adjusted to contcnlrationsof 0 2.
!•(), 5 0. or 250 >: 10'^ conidia ml. In each block,
the inoculations were done in order of increasing
concentration and the airbrusb was thoroughly
ivjshed with disiilled water between blocks.
Mildew anseasments
fJfiO experiment
The numbers of mildew colonies on each surfaee
of leaves at positions - I to -|-4 at the time of
inoculation were counted on 22. 23. 25. 27, 30
May. 3 and 7 June, Assessments ceased when ihe
first mildew colony was observed on an uninocu-
lateS plant. Irrespective of cultivar. signifying the
occurrence of secondary spread. Mildewed leaves
were harvested on 9 June, washed by mechat^icaUy
rolling each one for 10 min in 20 ml of 01 ml,!
Agrai and the number of eonidia in suspension
 Resistance ofappte to powdery mildew
was estimated with a haemocytometer. Washed
leaves were dried and their areas measured photo-
metrically.
1981 experiment
Mildew was monitored on the lower surface of the
leaf wbich had been at position + 2 . two nodes
above the youngest unrolled leaf (leaf Ol at the
time ol'inoeulation. Visible colonies were mapped
on record cards on 10, 12. 15. 18 and 22 June (on
wbich date mildew was first observed on an
uninoculated plant) Tor greenhouse plants and on
the following days for outdoor plants. Mapping
the position of mildew colonies facilitated moni-
toring and allowance was easily made for doubt-
ful and for merging colonies. On each date the
area of each colony was estimated by means of a
colony radius key and the position, relative to tbe
current leaf 0. of eaeh inoeulated leaf was
recorded. Monitored leaves were harvested on 24
June (glassbouse) and 25 June (outdoors),
washed, and spore production was assessed as
described for 19fiO, Spore production was
expressed as conidia, colony and conidia;cni-^ col-
ony.
Host shoot characteristics
1980 e.xperimeni
The number of leaves produced between inocula-
tion and harvesting of leaves was counted on each
shoot and production rates were calculated. After
leaf harvest, the shoot tip of each plant was
examined under low magnification and tbe
number of rolled leaves counted, Tbe current leaf
0 (i.e. not tbe inoculated leaf 0) was assessed
against photographs for leaf hairiness on a
qualitative 1-4 scale. The length, breadth and
area were measured and a regression equation
relating the area of leaf 0 to its length and breadth
was obtained,
1981 experiment
The number of rolled loaves, leaf hairiness, and
rate of leaf produetion were estimated by tbe
metbods described for 1980,
Data analysis
1980 experiment
Mean values for the varieties measured on the 26
479
inoculated plants were obtained for eaeh cultivar
X leaf position x leaf surface combination,
Tbreo-way analyses of variance of transformed
and untransformed data were done, using the
three-factor interaction as the error term. For
clarity, mean values and standard errors for
differences between means for main factors are
given only when two-factor interactions are not
signifieant, and for significant two-factor interac-
tions.
198} experiment
With the exception of disease incidence, data
from the glasshouse and outdoor environments
were analysed separate!) accordmg to a standard
split-plot design, with separate error terms for the
main plots (inoculum concentration) and sub-
plots (cultivar. and cultivar x inoculum concen-
tration interaction),
RESULTS
Disease incidence
experiment
Disease ineidence (calculated as the proportion of
leafsurfaces with mildew colonies), over all leaf
positions at each a.ssessment. is shown in Fig. !
for each cuitivar. Final disease incidenee (Table 1)
varied according lo cultivar. leaf position and leaf
surface (all at P<0-001). The highest final inci-
dence was on Crispin (55"'ii of all leaves): the
lowest was on Discovery (5% of all leaves).
Disease incidence was higher on the older leaves
and was always higher on the lower leaf surfaee.
The cultivar x leaf surface interaction was signifi-
cant [P<000]): on some cultivars (Crispin.
Disco\ery and Laxton's Superb) tbe difference
between surfaces was not significant. Similarly,
the cultivar x, leaf position interaction was signifi-
cant (P<0-01): the increa.se in disease with !eaf
age was less marked with some cultivars (e.g.
Di5co\ery. Golden Delicious). Tbe leaf position
X surface interaction was also significant
(/'<0'001); the lower incidence on the younger
icaves was more pronounced on the upper sur-
faee. Each ofthe two-factor interactions was also
signifieant when data were transformed to angles,
1981 experiment
Mean disease ineidence on leaf +2 was derived
for each cultivar and inoculum concentration in
480 M. J. Jeger et al.
1-0
Discovery Tydeman's Larly 'b 5uperb

0-5-

c 0-0
o Grarny
c Ida Sunian Bramley's
HI Seedling
•o
u
-^ 0-5H

in
o O'O
Cox's ^c'der. Delicious CULTIVAR MEAN
P-ppin
0-5-

0-0 •
0 10 20 0 10 20 0 10 20 0 10 20 30
Day5 from inoculalion
F i g . I . Mean disease incidence (proponion of leaf surfaces, over all leaf positions, ihai devcioped milden) ploiied
u ^ a i n s t time for 11 apple L-uhivars inocuiaied with Podosphaerii hm-oiricha tonidia. Each proportion based on 26
p l a n t s x 6 leaves x 2 surraa;s = 3l2 observ'ations.

Table I. Mean disease incidence (proportion of leaves and leaf surfaces wnh
mildew. untrLmsFonned) on 11 apple cullivars inofulaled with Pwlo.tphacra
tciK nirnlm i:ouid\-d in

Leaf position al moculation Leaf surface

-I 0 +2 +4 Upper Lower

Cullitar
Discovery 0-OS 0-03 0-05 0-04 0-06 o-o« 002 {)(»9
Spartan 023 0 3 8 0-40 0-19 0 12 0 12 0-07 0 41
Laxton's Superb 0-4.1 O.30 0-43 017 0 1 f< 0 17 0-23 0-32
Tydeman's Earl_\ 0-3S o-:o 0 25 0-33 0-29 O-ll 0-13 0-39
Bramley's Seedling 0-48 0-45 0-50 0-29 0 23 0-15 0-20 0-50
Suntan 0 53 0-43 0-35 0 36 0-25 0-09 0-21 046
Ida Red 0 4 3 0-40 0 38 0-27 0 31 O i l 0-16 0-47
Granny Smith 0-60 0-48 0.30 0-34 0-32 0 15 O'I4 0-59
Cox's Orange Pippin 0 4 8 0-53 0 43 0-34 0-3K 0-13 0-23 0-53
Golden Delicious 0-48 0-53 0-48 0'48 )t-38 0-25 0-21 0-65
Crispin 0 85 0-75 0 75 0-42 0-36 0-19 0 51 0-60

Leaf surfaee
Upper 0-37 0-28 0 2 4 O-ll 0-iO 0-05
Lower 052 0-53 0-.M 0'4K 0 41 0-23
Coefficient of variation (%) 25-2
Standard errors of differences between means (50 DF):
Cultivar > leaf position 0 08!
Cultivar x leaf surface 0^047
Lca("po!*!lion » leaf surface 0 035
 Resistanee of apple to powdery mildew 481

.? 40 Discouery Spartan Tydeman's Early Lax'on's Superb

E
o
§, 20-1

0
40- Ida Red 5unton Bramiey's Granny Smith
Seedling
o

20-
uo
0
40 Cox's Orange Golden Delicious Crispin CULTIVAR MEAN
Pippin

20-
E
0 —r
10 20 0 10 20 0 10 20 0 10 20 30
Days from inoculation

Fig. 2. Distribution of incubation penods (number of days, over all leaf poMtion, from inw;ula\ioT\ lo firs! sign of
mildew on each leaf surface) for 11 apple cultivars inoculyied with Pudiisphaera Icueotritha conidia. Data are for
colonies appearing in the 25 days of the assessmcnl period.

the glasshouse and outdoor environments. High
levels of mildew ( >0-80) were recorded for all
cultivars except Worcester Pearmain and [>is-
covery and there wa^ good iigreemeni oi"rankings
between culti\yrs in both environments. Dis-
covery and Wcrccstcr Pcurmain showed a low
proportion of mildewed leaves, especiuliy in the
outdoor environment (0-17 and 0-25. respect-
ively). Mean disease incidence increased with
inoculum concentration in the glasshouse, but
not outdoors.
Incuhation period
I9H0 experiment
The distribution of incubation periods (number
of days from inoculalion to sign of the lirst
mildew colony on a surface) is shown in Fig. 2 for
each cultivar. The mean incubation period for
those leaf surfaces whicb developed colonie.s
\aricd according to culti\ar (/'<()'OOI). leaf
position (/»<0001) and leaf surface (/'<001)
(Table Z). Four days separated the cultivar with
the shortest mean incubation period (Crispin,
16-7 days) from the longest (Spartan. 211 days).
The mean ineiibation periods were longer on the
younger leaves. The culti\ar x leaf surface inter-
action was significant (/'<0'0OI) with a marked
differenee in surface.s for some eultivars (e.g. Ida
Red. Spartan) but not for others (e.g. Crispin.
Discovery). No other imeracUons were Signifi-
cant,
1981 experiment
The mean number of days from inoculation to
first sign of a mildew eolony on a leaf, for those
plants which developed colonies before assess-
ments ceased, is summarized m Table 3, Rankings
of euitivars have been inserted to facilitate eom-
parison of tbe environments. The eulti\-ar x ino-
culum concentration interaeiion was not signifi-
eaiH in either environment. Tbe incubation
period varied with cultivar in both glasshouse and
outdoorenvironments(/'<0-05), but with inocu-
lum concentration only in the glasshouse
(P<l)-OS). Incubation periods were consistently
shorter in the glasshouse, with a narrower range
of eultivar \alues O days! than outdoors (4-5
days). Incubation periods, both in the glasshouse
and outdoors, were consistently short on Golden
Delicious and Grcensleeves, intermediate on
Tydeman's Early and Cox's Orange Pippin, and
long on Bramley's Seedling and Worcester Pear-
main, There were differences in rankings between
 482 M. J. Jeger et al.
TaWe 2. Mean incubation period (number of days from inoculation
to first sign of mildew) on leaf surfaces of 11 apple cultivars
inoculated wiih Podosphiuni Ifuinirichu conidia in 1980

L«af surface

Upper Lower

Cul ti tar
Discovery 19-9 202
Spartan 23-9 18 3
Laxlon's Superb 16-3 20 I
Tydeman's Early 22-4 18-4
Bramley's Seedling 2M 17-8
Suntan I7'8 18 5
Ida Red 204 159
Grannv Smith 185 16 5
Cox's Orange Pippin 16-6 181
Golden Delicious 18'3 16-3
Crispin 168 16-6
Leaf position al inoculation

-1 0 -1-1 +2 -t} +4
Leaf posilion mean 16-9 17-2 177 18-7 201 20-B

Coefficient of vunaiion (".0 12-6

Standard errors of differences between means (50 DFl:
Leaf position 0 7U
Cultivar X leaf surface 1.15

environments: Jester, for example, had the short-
est incubation period outdoors but a. near-median
v a l u e in the glasshouse; Spartan had the opposite
tendencv.
C o l o n y number!)
I9H0 experiment
T h e mean number of colonies'shoot at each
a s s e s s m e n i is shown in Fig. .1 for each cultivar.
D e c r e a s e s in numbers were due to merging of
c o l o n i e s and perhaps visual "fading" with age as
s p o r u l a l i o n declined, Tbe mean, maximum and
final number of colonies during the period of
a s s e s s m e n t (expressed per leaf surface and per
u n i t a r e a of leaf, both with and without logarith-
m i c transformation) were analysed; the untrans-
f o r m c d mean number of colonies/leaf surface
g a v e t h e lowest eoefficient of variation, a satisfac-
t o r y pattern of residuals and varied (Table 4)
a c c o r d i n g to cultivar. leaf position and leaf
s u r f a c e (all at /'<()-00l). Most colonies devel-
oped on Crispin and least on Discovery, There
were more colonies on older rather than younger
leaves, and on lower rather than upper leaf
surfaces, k\\ three interaetions were significant,
although that between cultivar and leaf position
(/'<0-01) was not significant when data were
analysed per unit area of leaf. The cultivar x leaf
surface interaction was significant (/*< 0001); as
with disease incidence, no difference was appar-
ent between surfaces on Crispin. Discovery, and
La,'(ton's Superb. Also, as with disease incidence,
the lower colony numbers on the younger leaves
were more pronounced on tbe upper .surface
(/'<0-05), Each of the interactions was also
significant when data were logarithmically trans-
formed.
I9SI experiment
No reductions in colony numberleaf occurred
with time and tinal numbers counted were ana-
lysed (Table 5), The cultivar x inoeulum concen-
tration interaction was not significant in either
 Resistance of appie to powdery miidew 483
Table 3. Mean incubation period (days from inoculation increase the number of colonies progressively to
10 firsi sign of mildew) on lower surface of leaf + 2 (at nearly double. Logarithmic transformation of
inoculation) on 10 apple cuUivars inoculated wiih data did not improve the precision ofthe analyses
Podosphuera lemotrichu conidia al four concentrations or affeet these conclusions.
and in Iwo posl-iniiculalion environments in 1981

Colony area, area mildewed and disease intensity

Glasshouse Outdoor

Cultifar
1981 experiment only
Bramley's Seedling 12-5 (3)" 16-8 (2) Mean colony area, mildewed area/leaf, and dis-
Cox's Orange Pippin 11-2 (5) I5'l (5* ease intensity (proportion of leaf area mildewed)
Discovery 129 (1) 15-0 (7) were calculated and analysed after transforma-
Golden Delicious 10 1 (9) 1.V9 (9)
tion to stabilize the varianees. Disease intensity
Green sleeves 9 5 (10) 14-7 (8)
Jester 10-8 (6) 13-1 (10)
(proportion of leafarca mildewed) was estimated
Spartan 10-5 (7) 16-4 (3) for each leaf by dividing the mildewed area by the
Suntan 11-7 (4) n - 6 (1) single-surfaee leaf area at harvest. Of the three
Tydeman's Ear!y 10-5 (7) 15-1 (5) variates. mildewed area/leaf (transformed to
Worcester Pearmain 126 (2) 15 7 (4) square roots) had the lowest coefficient of varia-
tion (Table 5). The eultivar >; inoculum concen-
Inoeuliiin (conidia ml) tration interaction was not significant in either
0 2 > 10' 12-1 environment. Mildewed area leaf (transformed
1-Ox I0-' 118 to square roots) varied according to culti\ar in
5-0 X 10^ 95
25'Ox 10^
both environments (P<O'OOI) and inoeulum
11-5
concentration (P<0-0] in the glasshouse.
Overall means 11-2 [5-1 /*<0-0.*^ outdoors). Mean mildewedarea.leafwas
much greater on glasshouse plants than tbosc
Coefficient of variation (",.) 27-2 20-3 kept outdoors. The rankings of cultivars in both
Standard errors for differences of means (DF):
Cullivar I-OK (79) 1-27 (48)
environments were generally consistent except
Inoculum concentration 0-64 (9) again for Spartan, Mildewed area/leaf was smal-
lest on Discovery and Worcester Pearmain. inter-
mediate on Bramley. and extensive on Cox's
•• Cultivar rankings (I =cultivar with the value likely to Orange Pippin. Golden Delieious. Greensleeves
impart mos! resislance) in parenibeses. and Suntan, The largest mildewed area leaf on
glasshouse plants was at 5 x 10^ conidia. ml rather
than at the highest inoculum concentration. In
environment. Colony numberleaf varied with the outdoor environment, the highest mildewed
cultivar (P<0-001) and with inoculum concen- area leaf resulted from tbe highest inoculum
tration (/'<0'0! in tbe glasshouse. P<0'00! concentration.
outdoors). Colony numberleaf was about the
same in botb environments, altbough tbe
Production of eonidia
extremes were more apparent outdoors. The
rankings of eultivars in both environments were
1980 e.xperiment
reasonably consistent except that a larger number
of colonies/leaf was reeorded on Spartan out- Production of conidia. expressed per leaf, per unit
doors than would be expected from the glass- area leaf, and per colony gave similar coefficients
house result. Discovery and Worcester Pearmain of variation, Lintransformed eonidia colony gave
developed few colonies, especially in tbe outdoor the best pattern of residuals in tbe analysis of
environment. The effeet of increasing the inocu- variance despite no allowance being made for
lum five-fold, from 0-2 to 1-0 x 10'' eonidia ml. coton\ age, Conidia'colony varied (Table 6)
was to increase the number of colonies in the according to cultivar and leaf position
glassbouse environment to more than double, but (P< 0-001), Production was highest on Ida Red.
further increases in concentration did not result in lowest on Discovery, and was higher on the
more colonies. In the outdoor environment the younger Icaves. especially on cultivars with a high
effect of increasing inoculum concentration 125- mean value (cultivar x leaf position interaetion
fold from 0-2 to 25x10^ eonidia;ml was to significant at /'<O-OOI), Similar results were
484 M. J, Je^er et al.

DtSCOVery Spartan Tydeman's Early Loxlon's Supefb

40

20

-5 0
Ida Red Suntan Bramley's G'Qnny Smitri
^ 40- Seedling
_g
a

a)
0
CULTIVAR MEAN
40- Coxs Oronge Golden Delicious
Pippm

20-

0 -1 T~
0 10 EO 0 10 20 0 10 20 0 10 20 30
Days from inoculation
F i g . 3>. Mean number of mildew colonies shoot plotted against lime for II apple cultivurs inoculaied with
Podtt.sphaera leuiotruliti cnnidia.

Table 4. Mean number of mildew colonies (uniransformcd) during period of

assessment on leave.s and leaf surfaces of 11 apple cultivars inoculaied wiih
leuioiruiui conidia in I9S()

Leaf position al inoculation Leaf surface

-1 0 + 1 +2 +4 Upper Lower

Cultivar
Discovery 0'08 0-03 005 0-06 0-06 o i : 0-02 Jll
Spartan 0 3K 0-69 0 58 0-40 0-19 0-17 012 )-68
Laxton's Superb 0-60 0 46 0 56 026 0 25 0 17 0-31 1-45
Tydeman's EarK 0-54 0-32 0-31 048 0-39 0-14 0-17 { )'56
Bramley's Seedling 1-92 1.^8 0-81 0-55 0-37 0 22 0-31 -4.1
Sunian 140 0-«5 (1-8 i 0-55 051 0 15 0-2S -14
Ida Red iO7 1-29 I-(H) ( M l 0-40 o-i: 0 20 -23
Granny Smith M6 084 0-77 0-7i 0-51 OvlO 0-17 •25
Cox's Orange Pippin 0-95 0-98 0-93 0 70 0 70 0-23 0-34 •15
Golden Delicious M4 1 32 1 -(13 0-92 0-76 0-49 028 -60
Crispin 2-69 1-50 1-41 0-69 0-53 0'27 1 03 -.13

Leaf surface
Upper 064 0-48 0-32 016 0-12 0-05
Lower 1 53 1-28 MS 0-88 073 0'37
CoeiTicient of variation (";.) 44'6
Standard errors of dilTerences heiween means (50 DF-):
Cullivar x leaf position 029
Cullivar y. leaf surface 0-17
Leaf position >• leaf surface 0-12
 Re.vislance of apple lo powdery 4S5
TaWe 5. Mean numher of mildew colonits and mildewed area, leaf (cm- Iransrurmed to
square roots) on the lower surface of leaf +2 lat inoculationl on !0 apple cultivars
inoculaied wilh Podmphaeru h-ui-niriibu conidia a( IOUT conceiHTalipns and iti two post-
in ocufation environmems in t9RI

Numher of colonies Mildewed area 'leaf

Glas^ouse Ouidoore Glssshouse Outdoors

Cultivar
Bramlevs Seedling 2--^ W) 2 34 <41 071 (41
Cox'.-, Orange Pippin 50 m 50 (6) 3-07 (10) 1-06 (7)
Discovery 13 (1) 0 4 (2) 0-41 (1) 0 I 2 (1)
(iolderi Delicious 43 (6) 5-4 (Bt 3fl; (9) 1-31 {%)
Greensleeves 46 (7) 41 (5) 2-fi: (7) 0'97 (5)
Jester 28 C) \-i (3) 1-73 (3) 0-57 (3)
Spartan 35 (4) b-2 (9) 2-53 i6> 1-.13 i9)
Suntan 5-0 (H) 7 3 (10) .3-01 (K) 1-40 (10)
Tydeman's Eail> 5 7 liOl 51 (7) 2-.39 (5) 1-00 (6)
Worcester Pearmain 2 « \2) » 3 tl) 0S6 t2t 0-14 (2>

Inoculum {conidia mi)

00 X 10* 2\ 2S 1 16 0-78
4-7 30 1-79 0-69
50x10' 4I 40 3-61 0-89
2 5 0 X 10- 4!> 5-4 2?i2 1^07

Overail m e a n s 39 3-K 8-42 11

)
Cofiricient of variation {'%• 6I-: 53-8 64 6 50-5
Standard errors of differences of means iDFl:
CuUivar 0-83 (99) 0-84 (70) 0-507 (99) 0-177 (-70)
Inoculum concentratior1 045 CJ) 015 (6) 0 462 (9) 0 102 (6)

^Cultivar rankings (I =cullivar with the value likely to impart mosi resistance) in
parentheses.

ohwined when (he ^wo other nieasuves of con-
produclion were an;i]ysed.
experiment
Production of conidia was expressed per colony
and per cm- of colony: logarithmic [ransforma-
tion was neces.sary lo stabilize the vatiancc. In the
ouldoor etivironment ihcrc were no sigtiificani
differences in eilher variaie due to uultivar or
tnoculumconcentration. In theglasshousc{TahEe
7). spore production dttfered between cuttivars
(/'<0-01.peTCni'eo(ony: /'<O-Clflt. per coionyt.
and between inoculum concentrations i,P<{)-0\)
when expressed per ct)lony. l_/ntransrornicd
numbers of conidta cm- colony differed little
between glasshouse and outdoor ptanls; differ-
ences in conidia'colony between the two environ-
menxs were due xo the larger colonies on glass-
iiouse plants.
Host shtiot attributes
i'^HU experiment
There were significant differences between culli-
viirs tP<0-05) lor each atlrihuie. lr\ general,
large-leaved cultivars (Bramiej. Crispin. Suntan)
were hairier, produced leaves at a lower rate, and
bad fewer leaves at the shoot tip ihan did small-
leaved eullivars (Discovery. Laxlon's Superb.
Tydcman's Early). The former combination of
characteristics was associated, therefore, with
relative susceptibility and ihe latter with relative
resistance. The remaining culfivars (e.g. Cox's
Orange Pippin) could not be categorized so
rcadil>.
experimen!
There were significant cultjvar differences
(P < 005) in the glasshouse and outdoor environ-
 486 M. J. Jeger et al.
Table 6. Mean conidia/colony (ihousaiids) washed from mil-
dewed leaves of 11 apple cullivars 27 days after inoculating with
Podosphaera tciicotricha conidia in 1980

Leaf position at inoculation

Cultivar L 0 +I +2 +3 +4

Discovery 0-9 22-2 19 •4 7 .T 27'7 15•7

Spartan 24-6 17-6 17 .2 38 •6 22-9 32. 1
Laxton's Superb 17-8 IS-8 14 9 21 •3 30-6 28' 0
Tydeman's Early 15-9 37'0 36'•4 36 •4 456 49. 9
Bramlcy's Seedling 91 5'6 11 •7 25 •4 27-3 15' 9
Suntan 2i'O 23-5 28 8 35 •K 48'1 61 9
Ida Red 22'1 22'4 20- 5 45 9 49'0 95- 3
Granny Smith 103 14'2 30- 3 28' 53-6 82- 8
Cox".-; Orange Pippin 91 143 10 4 18 6 34-6 56- 8
Goldeii Delicious 17-7 20-6 41- 1 3J-•2 45-2 8!- 8
Crispin 9-7 18-0 26' 7 53- 3 42-6 S3- 4
Coefficient of variation (%) 138
Standard error of differences between means (66 DF)
Cultivar x leaf position 4-20

m e n t s . The overall mean values were similar in
t h e I w o ejivironinents, except for leaf area at the
t i m e o f harvesting leaves (larger in the glass-
h o u s e ) , and position of the inoculated leaf when
c o l o n i e s were first observed flower outdoors).
A r e a o f harvested leaves decreased in the glass-
h o u s e {/*<0'05) as the inoculum concentration
i n c r e a s e d . Rankings of cultivars in both cnviron-
m e n t s \^'ere generaUy consistent.
DISCUSSION
I n g e n e r a l there was an associated variation in the
c o m p o n e n t s of resistance in 1980. A cultivar with
a l o w proportion of mildewed leaves had fewer
coionies/'leaf, and the colonies had a longer
i n c u b a t i o n period, and a lower production of
c o n i d i a . Extremes of resistance were shown by
D i s c o v e r y (very high) and Golden Delicious and
C r i s p i n (very low). Likewise, a consistency in
c o m p o n e n t s was shown hy some cultivars with
i n t e r m e d i a t e levels of resistance (Laxton's
S u p e r b . . Suntan, Bramley's SeedHng and Granny
S m i t h ) . As has been found in some cereal diseases
(Parlevliet, 1979; Jeger el at., 1983). the associ-
a t i o n between componenis was not consi.sien£ for
all cultivars; in each case the sporulation compo-
n e n t varied independently of the other compo-
n e n t s . O n the basis of rankings with respect to
o t h e r components, spore production was less
than expected on Cox's Orange Pippin and more
than expected on Ida Red, Spartan and Tyde-
man's Early. It is possible that differences in
colony size may account for thisfinding,although
sporulation has been shown to vary indepen-
dently of number and size of colonies of Rtiyn-
ctiospon'um secalis on barley (Habgood, 1977).
In 1981 there was, for some cultivars. an
associated variiiiion of components irrespeclive
of environment; although, for example, the incu-
bation period for Suntan was long, given the large
number of colonies and area mildewed that
subsequently developed. Discovery had tnany
leaves not infected and the few colonies were of
small size, had a long incubation period, and
produced few conidia/colony. Golden Delicious
showed precisely tbe opposite characteristics.
Between these two extremes there were inconsis-
tencies in rankings of two main types. Firstly, the
level of resistance of a cultivar depended upon
environment: this was the case with Greensleeves
which was marginally more susceptible in the
glasshouse than outdoors, and for Spartan which
was more susceptible outdoors. Secondly, culti-
var rankings on a particular component of resis-
tance were inconsistent between environments:
this was apparent, for example, with respect to
the incubation period of Jester compared to oiher
components.
The incubation period, or time from inocula-
 Resistance of apple to powdery miidew 487
Table 7. Mean spore produciion from mildew colonies on leaf
+ 2 {al inoculation) on 10 apple cultivars inoculated with
Podospluiera leucotricha conidia at four concentrations and kepi
in a glasshouse in 1981

Conidia (transformed to
natural logs)

per cm-of eolony' per coiony

Cultivar
Bramlcy"s Seedling U-1 (6)" 12-4 (8)
Cox's Orange Pippin 11-3 (1) 12-0 (5)
Discovery 12-4 (9) 10-9 (2)
Golden Delidous n-7 (2) 12-3 (7)
Green sleeves 12-4 (9) 12-8 (10)
Jester 12-2 (8) 11-9 (4)
Spartan 12-1 (6) 12-6 (9)
Sun I an 11-8 (3) 12-2 (6)
Tydeman's Early i2-U (5) 11-8 (3)
Worcester Pearmain 11-8 (3) 10-5 (1)

Iuoculum conidia/ml):
02x10-''
1-Ox I0-' 11-4
5'Ox 10^
25-0x10^ 11-9
Overall means (untransformed) 2-.^xI(F 3-8 X 10-'^
Coefficient of variation {"/,.} 6-8 7-9
Standard errors of differences of means (DF):
Cultivar 0-29 (79) 0 33 (48)
Inoculum concentration 0-31 (6)

•• Cultivar ranking (I =cultivar wilh the value likeK to impar!

mosi resistance) shown in parentheses.

tion to sign ofthe first colony on a leaf surface,
was measured with a small coefficient of variation
iti both years and environments, A tnore impor-
tant component, cpidemiologically. is the latent
period, or time from inoculation to firsl produc-
tion of a mature eonidium, but this is very
diffieult to assess for apple powdery mildew
-beeause sporulation may preeede symptom ex-
pression by many days. The latent period is also
more influenced by weather conditions (Butt ei
ai.. 1980). There are also practical prohlcms in
recording the incubation period. In this study, for
example, the incubation period was reeorded only
for those leaf surfaces that developed colonies
before the end of the assessment period. Values
for cukivars sueh as Discovery with a low disease
incidence are probably loo low. so that differ-
ences between cultivars arc underestimated. A
compromise is to qualify the incubation period
with the corresponding value for disease inci-
dence. The latter, although not a true component
of resistance, provided good discrimination
between enltivars.
Colony nnmbers were more variable but pro-
vided a good range of eultivar values and gave a
good identification of the high resistance in
Discovery in both years. There was no apparent
advantage in standardizing colony numbers per
unit area of leaf.
The older leaves near the shoot tip had a higher
disease ineidence and eolony nttmber and a
shorter incubation period than the younger
leaves. This almost certainly reflected the relative
amounts of inoeulnm intercepted by leaves at the
— 1.0 and + 1 leaf positions as compared with the
rolled leaves at the shoot tip. For this reason a
 488 M, J. Jeger et al.
b e t t e r indicalor of the intrinsic susceptibility of
each leaf in relation to leafage is given by spore
production. The lower leaf surface proved more
susceptible but this, again, reflects the higher
p r o p o r t i o n of inoculum landing on this surface;
this explanation is supported by the significant
leaf position x leaf surf ace interaction, in thai the
lower leaf surfaces of rolled leaves at the shoot tip
a r e directly exposed to inoculum.
T h e restriction to the lower surface of a
p a r t i c u l a r leaf position (leaf + 2) at inoculation in
198 I led to no loss of precision and the more rapid
assessments enabled the inclusion of area/colony
as a n additional and valuable component of
resistance, providing information, for example,
on t h e relationship between colony numbers and
m i l d e w e d area/leaf Furthermore, expressing
s p o r e produetion as conidia per cm- oi" colony
p r o v e d useful in demonstrating the importance of
c o l o n y area as a determinant of spore production.
Independent of cuhivar, there were overall
differences between the glasshouse and outdoor
p l a n t s . The incubation period, on average, was
a b o u t 4 days shorter in the giasshouse. Likewise.
m i l d e w e d area'leaf was about eight times larger
on p l a n t s in the glasshouse, a difference much
g r e a t e r than that for leaf area. Colony numbers/
leaf a n d conidia/cm-eoJony did not differ greatly
b e t w e e n the two environments. The differences in
i n c u b a t i o n period and mildewed area/leaf in the
t w o environments were most apparent in the
r e s p o n s e s to inoculum concentration. Mildew
development was most extensive on glasshouse
p l a n t s inoculated at one-fifth ofthe highest spore
concentration; colonies on these plants had the
s h o r t e s t incubation period and largest mildewed
area/leaf- No interaction between inoculum con-
c e n t r a t i o n and cultivar was found for colony
n u m b e r s or area/colony in either environnnent in
1981, suggesting thai differences in inoculum
concentration affected cuitivars equally.
An inverse relationship between colony
n u m b e r s and area/colony (Parleviiet, 1979) may
c o n f o u n d the assessment of colony area as a
c o m p o n e n t of resistance, Shaner (1973). working
with Ery'.siphe graminis f sp, triad on two wheat
c u l t i v a r s found similar areas/coiony at high col-
o n y densities, whereas at iow colony densities
a r e a s o n the susceptible cultivar were greater than
on t h e resistant cultivar. Hence, resistance p(^r,ve,
r a t h e r than colony density, may restrict the area/
c o l o n y of powdery miidew on wheat; this conclu-
s i o n c a n also be inferred from the results of
R o b e r t s & Caidwel! (1970).
Variation in resistance to apple mildew, even
within a single genotype (Mowry, 1965), has often
been attributed to host characteristics. Discovery,
Laxton's Superb and Tydeman's Eariy, all with
small glabrous leaves and a high rate of leaf
production, proved relatively resistant; Bramley.
Crispin and Suntan. with the converse character-
istics, proved relatively susceptible. The number
of rolled leaves at the shoot tip and the rale ofleaf
production could influenee the dynamics of
natural infections in the field (Butt el al., 1983),
Leaf hairiness varied considerably between culti-
vars, but there was no evidence to suggest that
hairs act either as spore "traps" or as barriers to
infection. The ranking of cultivars wilh respect lo
host shoot attributes was reasonably consistent
between environments in 1981 and between years.
The main diflerenees were the larger leaf areas in
the glasshouse compared to outdoors and the
reduction of leaf area with inoculum concentra-
tion in the glasshouse, demonstrating the damag-
ing effect of mildew. Stirprisingly, the amount of
unexplained variation in the analysis of host
shoot attributes and components of resistance
was higher for plants in the glasshouse environ-
ment than outdoors.
In our experiments in 1980 and 1981, the
eultivars examined differed and the assessment
techniques varied between experiments. As a
consequence, we have used the relative rankings
of cultivars common to ail experiments as a
qualitative measure ofthe consistency of assessed
components of resistance {Table 8), If compari-
sons of the results of the experiments are re-
stricted to the leaf, inoculum concentration and
cultivars common to both years, then there
appeared to be more variation between the
glasshouse and outdoor environments in 1981
than between the two years: the latter variation
may be associated with differenees in plant mater-
ial, inoculum aggressiveness, and glasshouse con-
ditions. Discovery and Golden Delicious showed
strong and weak partial resistance characteristics
respectively, irrespeetive of environment or year.
The moderate level of resistance in Bramley's
Seedling was stable over years and environments.
The ranking of the moderately susceptible culti-
var Cox's Orange Pippin was also reasonably
consistent. The moderate level of resistance
(apart from spore produetion) in Spartan was
only expressed in the glasshouse in 1980 and 198L
Suntan. except for the long incubation period in
1981 in both environments, was moderately sus-
eeptible in all experiments. Tydeman's Early was
more difficult to characterize when comparing
environments and seasons; this cultivar was
 Resistance of apple lo powdery mildew 489
Table 8, Classiiication of seven apple cuUivars with respect to rankings within four
coinponent.s of resistance to powdery mildew in two years (!980. 19K!| and twti
environments (G. glasshouse: O. outdoors). All rankings refer to assessments made on
ihe lower surface of the leaf in position + 2 at the lime of inoculation

Di.sease Incubation Colony

incidence period n timbers
Conidia/
I9S1 1981 1981 colony

CuUivar 1980 G O 1980 G 0 1980 G 0 1980 198P

Very resist a at
Discovery I 1 I I 1 6 1 1 1 i 1

Moderately resistant
Spartan 2 2 4 3 5 3 T 2 6 7 7
Bramley's Seedling 3 3 2 4 2 2 4 2 3 6

Moderately susceptible
Tydeman's Early 4 7 4 2 5 4 3 7 4 6 2
Stinlan 6 5 4 5 3 1 4 5 7 5 4
Cox's Orange Pippin 5 4 3 6 4 4 6 5 3 -}
3

Very susceptible
Golden Delicious 7 4 6 7 7 7 4 5 A 5

" Ratikings from assessments made in glasshouse: cultivars did not differ significantly
outdoors.

moderately rcsislant in glasshouse evaluation in
1980, suseeptible in gl!isshouse evaliaalion in
1981, and moderately reststanl outdoors in 1981.
Consistency in assessing resistance was obtained
where (here was a high degree of a.ssoeialion
between components. No eultivars were identi-
fied which consistently, over years and environ-
ments, showed strong resistance characteristies
with respecl to one component but weak eharac-
leristics with respect to another.
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