Plant Pathology (2007) 56, 562–572 Doi: 10.1111/j.1365-3059.2007.01571.

Genetic structure and pathogenicity of populations of

Blackwell Publishing Ltd

Phytophthora infestans from organic potato crops in France,

Norway, Switzerland and the United Kingdom

W. G. Fliera†, L. P. N. M. Kroona, A. Hermansenb*, H. M. G. van Raaija, B. Speiserc,

L. Tammc, J. G. Fuchsc, J. Lambiond, J. Razzaghianb, D. Andrivone, S. Wilcocksonf
and C. Leifertf
a
Plant Research International, P.O. Box 16, 6700 AA Wageningen, the Netherlands; bBioforsk-Norwegian Institute for Agricultural and
Environmental Research, Plant Health and Plant Protection Division, Hoegskoleveien 7, N-1432 Ås, Norway; cSwiss Research Institute of
Organic Agriculture, Ackerstrasse, 5070 Frick, Switzerland; dGroupe de Recherche en Agriculture Biologique, GRAB Site Agroparc BP
1222, F-84911 Avignon Cedex 9, France; eUnité Mixte de Recherches Agrocampus Rennes-INRA BiO3P, BP 35327, F-35653 Le Rheu
Cedex, France; and fUniversity of Newcastle, Nafferton Ecological Farming Group (NEFG), Nafferton Farm, Stocksfield, Northumberland,
NE43 7XD, UK

Genetic variation and pathogenicity of Phytophthora infestans isolates collected from organic potato crops of the
susceptible cv. Bintje and the moderately resistant cv. Santé were assessed in France, Norway, and the United Kingdom
in 2001 and in Switzerland in 2001 and 2002. Population structures differed considerably between the four P. infestans
populations. Those from France, Switzerland and the UK were mainly clonal populations showing restricted levels of
genetic diversity, whilst those from Norway were mixed A1 and A2 mating type populations with high levels of genetic
diversity, suggesting periodical sexual reproduction. Isolates collected from cv. Bintje were on average more aggressive
than or comparable to isolates from cv. Santé. Race complexity varied considerably between the regional P. infestans
populations, with isolates from France and Switzerland showing the highest number of virulence factors. In all pathogen
samples but the French, isolates collected from cv. Santé were more complex than isolates collected from cv. Bintje.
No directional selection towards increased aggressiveness towards the more resistant cultivar Santé was observed. This
suggests that there is no shift towards increased levels of pathogenicity in P. infestans populations following the
large-scale introduction of more resistant potato varieties in organic production systems in Europe.

Keywords: AFLP fingerprinting, epidemic parameters, epidemiology, potato late blight, race structure

& Spits, 2006). The recent displacement of the old clonal

Introduction
The oomycete Phytophthora infestans, the cause of late
blight, is one of the most important pathogens of potato
worldwide. The pathogen affects leaves, stems and tubers,
leading to serious yield losses. To date, the vast majority
of potato cultivars commonly grown in Western Europe
(Colon et al., 1995b) and North America (Platt & Tai,
1998) are susceptible to late blight. The use of numerous
applications of both protective and curative fungicides is
common practice to control potato late blight (Schepers
*E-mail: arne.hermansen@bioforsk.no
†Present address: Fine Agrochemicals Ltd., Hill End House,
Whittington, Worcester WR5 2RQ, UK
Accepted 3 November 2006
population of P. infestans by an aggressive (Day &
Shattock, 1997; Flier & Turkensteen, 1999) and more
diverse population of P. infestans in Western Europe
(Spielman et al., 1991) might have a negative impact on
the efficacy of late blight management tools. Evidence is
accumulating that P. infestans is sexually reproducing in
many countries in Western Europe (Spielman et al., 1991;
Drenth et al., 1994; Sujkowski et al., 1994; Andersson
et al., 1998; Brurberg et al., 1999; Turkensteen et al.,
2000). Sexual reproduction results in variation in the
pathogen and might lead to increased and more rapid
evolution of the pathogen.
In the European Union (EU), organic growers apply a
wide range of measures aimed at controlling late blight in
potato crops, including the use of copper-based fungicides,
early cropping systems, various cultural practices and

© 2007 The Authors

562 Journal compilation © 2007 BSPP
 Genetic variation in P. infestans from organic potatoes 563

cultivar resistance (Tamm et al., 2004). Protective copper-
based fungicides, which are currently used to control late
blight in most organic production systems, are estimated
to slow down an epidemic by approximately 10 to 30
days, depending on weather conditions and cultivar
resistance. The additional growth period provided by
copper-based fungicide protection is estimated to increase
the income of EU-organic potato growers by between 15
and 45 million euro(D) per annum (Zarb et al., 2002).
In an agro-economic study, Varis et al. (1996) reported
that late blight was a serious problem in cv. Bintje in both
integrated and organic systems in Finland. Total yields
were 10% and 36% lower, respectively, compared to the
conventional cropping system. Similar late blight problems
have been reported in organic potato production in the
Netherlands (Lammerts van Bueren, personal Communi-
cation, Louis Bolk Instituut, Hoofdstraat 24, 3972 LA
Driebergen, the Netherlands).
Maximum annual copper use in organic agriculture has
been continually reduced, and from 1st January 2006 was
limited to 6 kg ha−1 per year (Council Regulation (EEC)
No. 2092/91). This regulation on copper-based fungicides
may interfere with EU policy aiming to support the expansion
of organic production in Europe. Therefore, new disease
management tools are urgently needed to replace copper
containing fungicides in organic potato production, while
securing economic profitability and durability of organic
production systems. A shift towards a more widespread
use of resistant potato cultivars in organic potato production
systems may contribute to a significant reduction of
fungicide use, or even facilitate potato production without
fungicide inputs, while maintaining an economically
acceptable yield and product quality (Inglis et al., 1996).
A potential drawback of the widespread use of more
resistant potato cultivars is the increased instability
of host resistance in potato against P. infestans that may
be associated with the displacement of the old clonal
population of P. infestans with a more aggressive and
variable population of the pathogen in Europe (Flier et al.,
2001, 2003a). This finding is supported by reports in
recent years from commercial potato growers who repeatedly
suffer severe late blight outbreaks in cultivars with high
levels of partial resistance, and high tuber blight incidences,
leading to serious yield losses. However, no EU-wide
monitoring of these incidences is currently in place.
R-gene containing potato cultivars like Escort and Santé,
which are widely grown in organic farming in the
Netherlands, have shown considerable levels of foliar and
tuber blight in recent years, resulting in serious yield
losses. The observation of increased yield losses due to late
blight in organic crops has raised concern about the
possible increase in pathogenicity of P. infestans to more
resistant potato cultivars. Information on the pathogenicity
of P. infestans populations in organic crops may help to
assess the risk of increasing virulence and aggressiveness
following a large scale replacement of susceptible potato
cultivars by those with higher levels of host resistance.
The aim of the present study was (i) to compare
populations of P. infestans collected from organic potato
crops grown in France, Norway, Switzerland and the UK
in terms of pathogenicity (virulence phenotype and
aggressiveness) and genetic marker variation; and (ii) to
compare levels of genetic variation and mean pathogenicity
of isolates collected from the susceptible cv. Bintje with
isolates sampled from the moderately resistant cv. Santé.
Finally, the likelihood of a potential shift towards increased
levels of pathogenicity in P. infestans populations following
a large scale introduction of more resistant potato varieties
is discussed. This study was part of the EU funded project
‘Blight-Mop’ which aimed to develop a systems approach
for late blight management in organic farming.
Materials and methods
Collection and isolation of isolates
Potato leaves naturally infected by P. infestans were
collected from experimental organic plots of cv. Bintje and
Santé in France, Norway, Switzerland and the UK in 2001
(Table 1). Additional samples were collected from similar

Table 1 Sample sites, year of collection, cultivars and number of Phytophthora infestans samples used in subsequent phenotypic and genotypic
analyses

No. isolates characterized for:

Year of Mating type, haplotype

Population code Country Region Location Cultivar collection & pathogenicity AFLP

UKS2001 United Kingdom Northern England Newcastle Santé 2001 24 22

UKB2001 United Kingdom Northern England Newcastle Bintje 2001 28 27
NS2001 Norway Rogaland Saerheim Santé 2001 30 27
NB2001 Norway Rogaland Saerheim Bintje 2001 30 28
FS2001 France Northern Brittany Suscinio Santé 2001 30 27
FB2001 France Northern Brittany Suscinio Bintje 2001 30 34
CHS2001 Switzerland Zurich Reckenholz Santé 2001 14 14
CHB2001 Switzerland Zurich Reckenholz Bintje 2001 4 4
CHS2002 Switzerland Zurich Reckenholz Santé 2002 9 3
CHB2002 Switzerland Zurich Reckenholz Bintje 2002 30 24

Plant Pathology (2007) 56, 562–572

564 W. G. Flier et al.
experiments in Switzerland in 2002. At each site the
experimental plots consisted of nine cultivars in a rand-
omized block design with four replicates, each subplot
3 m wide consisting of four rows, 0·75 m apart and 15 m
long (Speiser et al., 2006). Sampling started from one
week after the first lesions appeared and continued until
50% of leaf area was infected in the four replicate plots
of each cultivar. Isolations were made by trapping P.
infestans from leaves with single lesions onto potato tuber
slices, followed by culturing on a selective rye agar (RA)
(Grünwald et al., 2001). All isolates were subsequently
maintained on pea agar at 18°C and sent to the Nether-
lands within 3 months of collection, where stock cultures
of 229 isolates were permanently stored in liquid nitrogen
(Flier & Turkensteen, 1999) at Plant Research International,
Wageningen.
Pea agar was prepared by autoclaving 120 g of frozen
peas in 1 L of water. The peas were removed by filtering
through cheesecloth and the broth was autoclaved
again after adding 15 g L−1 agar. In subsequent analyses of
virulence and epidemic parameters, isolates from Switzerland
collected in 2001 and 2002 were pooled due to the low
numbers of isolates collected from Bintje in 2001 and
Santé in 2002.
Culturing and inoculum preparation
All genetic diversity and pathogenicity studies were
performed at Plant Research International. Isolates taken
from liquid nitrogen storage were first inoculated on tuber
slices of the susceptible potato cv. Bintje and incubated in
the dark at 15°C for 5 to 7 days. When sporangia were
present, small tufts of mycelium were placed in a drop of
water on the abaxial epidermis of leaflets of cv. Bintje
placed in 9 cm Petri dishes containing 10 mL 2% water
agar. The inoculated leaflets were incubated for seven
days in a climate chamber at 15°C with a 16 h light
period (Philips fluorescence tubes type 33, intensity of 12
Wm−2). Sporangial inoculum was prepared by washing
leaflets showing abundant sporulation in 15–20 mL tap
water followed by concentration adjustment using a
flowcytometer (Beckman Coulter BV). Sporangial
suspensions were kept at 18°C and used within 30
minutes of preparation.
Race and mating type determination
The resistance gene (R-gene) differential set of potato
clones for race identification consisted of: R1, R2, R3, R4,
R5, R6, R7, R10, R11 (Black et al., 1953; Malcolmson &
Black, 1966) together with the universal suscept, cv.
Bintje. Virulence for R8 and R9 was not assessed as the
corresponding R-gene differentials were excluded from
the set due to virus infection. Tubers of each differential
clone were planted in 12 L plastic pots containing loam-
based compost. Plants were grown under greenhouse
conditions with at least 16 h light a day, supported by Philips
Son-T Agro illumination. The greenhouse temperature
was kept at 20°C with 80% relative humidity.
For race determination, detached leaflets of 6 to 10-
week-old differential plants were placed abaxial face up in
9 cm diameter plastic Petri dishes containing 10 mL 2%
water agar. A sporangial suspension (104 sporangia mL−1)
was sprayed to runoff onto the leaflets with a spraying
nozzle operated at a pressure of 0·5 kg m−2. Inoculated
leaflets were incubated in a growth chamber at 15°C in
the dark for 24 h. Subsequently the remaining water on
the surface leaf was allowed to evaporate by placing the
Petri dishes, without lids, in a laminar flow cabinet for 30
minutes. Incubation was continued in a climate chamber
at 15°C with a photoperiod of 16 h provided by fluorescence
tubes type 33 (Philips) at an intensity of 12 W m−2. Disease
symptoms were recorded seven days after inoculation.
Two leaflets per R-gene differential were inoculated in
each test, and the experiment was repeated. The interaction
between R-gene and virulence factor was considered
compatible when sporulation was clearly visible on
infected leaflets on at least one of the replicate leaflets in
both independent experiments.
Mating type was determined by in vitro crosses with
known A1 and A2 tester strains (IPO98014 and IPO82001,
respectively) according to Grünwald et al. (2001).
Epidemic parameters
The epidemic parameters infection efficiency (IE), lesion
growth rate (LGR) and sporulation density (SPOR) were
measured in detached leaflet assays as described by Flier
et al. (2003a) with minor modifications. Bintje and Santé
plants were grown in the greenhouse from certified seed.
Fully-grown lateral leaflets of cv. Bintje or Santé were
collected and placed in 9 cm diameter Petri dishes filled
with 10 mL of 1·5% water agar. For inoculation, either
10 drops, each of 10 µL, of a sporangium suspension
1·0 × 104 spores mL−1 (IE), or a single drop of 10 µL of
a sporangium suspension 5·0 × 104 spores mL−1 (LGR,
SPOR) were placed on the lower side of each leaflet. Two
replicate leaflets of each plant genotype were inoculated
with each isolate. The whole experiment was repeated.
The Petri dishes containing the inoculated leaflets were
wrapped in transparent polythene bags and incubated in
a climate chamber for one week at 15°C with a light
intensity of 12 Wm−2, 16 h light per day. Infection was
recorded 8 days after inoculation. Infection frequency
(IF), based on the fraction of lesions showing sporulation,
was calculated and transformed into an estimate for IE
according to Colon et al. (1995a) using the formula IE = 1
– H1/k, where H is the fraction of unsuccessful inoculations
and k the average number of sporangia per inoculum
droplet. The developing lesions were measured three
times at three, four and five days after inoculation, using
an electronic calliper. Length and width of each lesion
were measured and the average diameter, lesion area (LA)
and lesion growth rate (LGR) were calculated. Sporulation
density (SPOR) was calculated after 8 days of incubation.
Lesion area (mm2) was estimated by image analysis using
the MINIMOP image analyzer (Kontron). Sporangia
from each individual lesion were collected into a single
Plant Pathology (2007) 56, 562–572
 Genetic variation in P. infestans from organic potatoes
vial containing 10 mL ISOTON 2 solution (Beckman
Coulter BV) and counted using a flow cytometer (Beckman
Coulter BV). Spore density (SPOR, sporangia per mm2
lesion area) was calculated from the average of two counts
of 0·5 mL each.
DNA extraction
Isolates were grown for 10 to 14 days at 20°C in pea
broth supplemented with 200 mg L−1 ampicillin. The
mycelium was harvested, lyophilized and stored at −80°C.
Lyophilized mycelium (10 to 20 mg) was ground in micro-
centrifuge tubes with a pestle and sterile sand. Total DNA
was extracted using the Puregene kit (Gentra/Biozym)
according to manufacturer’s instructions. DNA was
suspended in 100 µL of TE (10 mm Tris-HCl [pH 8·0],
1 mm EDTA [pH 8·0]) and stored at −20°C.
Mitochondrial haplotypes
The P1 (1118 bp), P2 (1070 bp), P3 (1308 bp) and P4
(964 bp) regions of the mitochondrial genome were
amplified using primers and methods described by Griffith
& Shaw (1998). Reactions were performed in a PTC200
thermocycler (MJ Research). PCR products were digested
with restriction enzymes CfoI, MspI and EcoRI resulting
in restriction fragment band patterns that could be classified
into four different mtDNA haplotypes: Ia, Ib, IIa and IIb.
Fluorescent amplified fragment length polymorphisms
(AFLPs)
DNA (250 ng) was digested in a 50 µL reaction volume
with EcoRI (10 U) and MseI (10 U) for 6 hours at 37°C
in restriction ligation buffer (10 mm Tris/Ac [pH 7·5],
10 mm MgAc, 50 mm KAc, 5 mm DTT, 50 ng µL−1 BSA).
Digestion was confirmed on agarose gels. Restriction
fragments were ligated to MseI adapters (5′ GACGAT-
GAGTCCTGAG/ TACTCAGGACTCAT 5′) and EcoRI
adapters (5′ CTCGTAGACTGCGTACC/CTGACGCA-
TGGTTAA 5′) using 0·1 µm EcoRI adapter, 1·0 µm
MseI adapter, 0·2 mm ATP and 2·4 Weiss-U T4 DNA
ligase (Amersham Pharmacia Biotech). Ligation was
performed overnight at 10 –12°C and the ligation products
were diluted 10 times with filtered ultra pure water.
Non-selective PCR amplification was performed using
primers Eco00 (5′ GACTGCGTACCAATTC) and
Mse00 (5′ GATGAGTCCTGAGTAA). Non-selective PCR
amplifications were performed in a PTC200 thermocycler
(MJ Research) as described previously by Flier et al.
(2003b). The amplified restriction fragment products
were checked on 1·0% agarose gels. Selective PCR was
performed in a 20 µL reaction volume with 5 µL of 20 ×
diluted amplification products as described previously
(Flier et al., 2003b) using either the primers Eco19 and
Mse 16 or Eco21 and Mse 16. Products were loaded on
Sequagel (Biozym) polyacrylamide gels and run on an
ALFexpress automatic sequencer (Amersham Pharmacia
Biotech). Conditions were 1500 V, 60 mA, 35 W, and
Plant Pathology (2007) 56, 562–572
565
55°C. Thirty six samples were loaded on each gel,
together with flanking Cy5-labelled fluorescent 50 bp
ladders (Amersham Pharmacia Biotech) and two refer-
ence isolates (PIC99016 and NL-VK6C).
Data analysis
All statistical tests for the epidemic parameter data were
performed using the statistical software Genstat version
6·1 (Payne et al., 1993). Restriction fragments of isolates
were visualized on agarose gels using ethidium bromide
under UV illumination, and classified according to mtDNA
haplotype. AFLP patterns were analysed using Imagemas-
ter ID software (Amersham Pharmacia Biotech), manually
correcting for faint bands and exclusion of controversial
bands. A total of 137 distinct and reproducible AFLP
bands were identified using the primers either Eco19 or
Eco21 in combination with Mse16. Bands were treated as
putative single AFLP loci and a binary matrix containing
the presence or absence of these reproducible bands was
constructed and used for further analysis. Statistical
analyses were conducted using TFPGA (Tools for Popu-
lation Genetic Analyses, version 1·3). Each AFLP band
was assumed to represent the dominant genotype at a
single locus, while the absence of that same band repre-
sents the alternative homozygous recessive genotype.
Genotypic diversity analysis was used to determine the
distribution of diversity among populations (France,
Norway, Switzerland and the UK) and among subpopulations
of P. infestans collected from Bintje or Santé. Genotypic
diversity was calculated using Shannon’s information
index (Magguran, 1988) and an unbiased Shannon’s index
(Abu-El Samen et al., 2003). Pair-wise measures of Roger’s
modified genetic distance and population differentiation
was estimated using an exact test (Raymond & Rousset,
1995) in order to assess the significance of the different
statistics for the null hypothesis of no differentiation
at the corresponding hierarchical level. Permutation and
re-sampling tests (jackknifing and bootstrapping) were
carried out to calculate estimates for standard errors.
Cluster analysis of AFLP genotypes was based on allele
frequencies observed for each sub-population. A phenogram
was constructed using the neighbour joining method
algorithm from a Rogers’ modified genetic distance
matrix. Bootstrap sampling (1000 replicates) was performed
for parsimony analysis of the constructed tree.
Results
Mating types and mtDNA haplotypes
Both the A1 and the A2 mating type were detected in
isolates collected from organic potato crops in Europe
in 2001. Only A1 mating type isolates were detected in
pathogen population samples from the UK, France and
Switzerland (2001 sampling only). The A2 mating type
was predominant in isolates collected on cv. Bintje from
Switzerland in 2002. Mixed A1 and A2 mating type
populations were present in Norway, on both cvs. Bintje
566 W. G. Flier et al.

Table 2 Isolate sample sizes, mating type distributions, mtDNA haplotypes, AFLP genotypes and genotypical diversity of Phytophthora infestans
populations collected from the susceptible potato cv. Bintje and the moderately resistant cv. Santé organically grown in France, Norway, Switzerland
and the United Kingdom in 2001 and 2002

Mating type mtDNA haplotype Genetic diversity

AFLP
a
Population code A1 A2 n.d. Ia Ib IIa n.d. genotypes Hsb Hsrc

UKS2001 24 23 1 5 1·05 0·34

UKB2001 28 6 22 7 1·34 0·41
NS2001 15 15 27 3 15 2·48 0·75
NB2001 2 28 11 19 8 1·67 0·50
FS2001 29 1 19 11 11 2·04 0·62
FB2001 30 14 16 13 2·15 0·61
CHS2001 14 14 2 0·90 0·34
CHB2001 4 3 0·56 0·41
CHS2002 1 8 1 8 3 0·64 0·58
CHB2002 30 29 1 2 0·46 0·14

a
Not determined.
b
Genetic diversity within populations.
c
Relative genetic diversity within populations (corrected for sample size).

and Santé, and in Switzerland on Santé in 2002 (Table 2).

Isolates collected from cv. Bintje in Norway were mainly
A2 (28 out of 30), while mating types in isolates from cv.
Santé were more evenly distributed (15 A1 and 15 A2
strains).
Mitochondrial DNA haplotypes Ia and IIa, both repre-
sentative for isolates associated with recent migrations
of the late blight pathogen, were detected in P. infestans
populations from the UK, France and Switzerland
(Table 2). In the Norwegian population both the Ia and Ib
mtDNA haplotypes were detected. In isolates collected
from cv. Bintje, 19 out of 30 isolates were of the Ib
haplotype. No statistically significant association between
the Ib haplotype and the A1 mating type was observed
(data not shown).
Virulence tests
With the exception of virulence for resistance genes R8
and R9, which were not included in the differential set, all
nine virulence factors were detected in isolates collected
from France, Norway, Switzerland and the UK. The most
common virulence phenotype was race 1,3,7,11 with an
overall frequency of 42·4%, followed by races 1,2,3,7,11
and 1,7, both with a frequency of 9·3% (Table 3). The
most complex race (1,2,3,4,6,7,10,11) was found
exclusively in isolates collected from cv. Santé in Switzer-
land. Race 0 strains were present in all four P. infestans
populations sampled. In total, 23 different races were
detected in 229 isolates. Virulence complexity, measured
as the average number of virulence factors per isolate,
ranged from 2·03 for isolates collected from Norway on
cv. Bintje to 4·78 for isolates collected from cv. Santé from
Switzerland (Fig. 1). Isolates collected from the moderately
resistant cv. Santé showed a significantly higher virulence
complexity than isolates from cv. Bintje, with the
exception of the P. infestans population from France
(Fig. 1).
Epidemic parameters
Considerable variation for the epidemic parameters infec-
tion efficiency (IE), lesion area (LA) and sporulation
density (SPOR) was present in P. infestans populations
sampled from cvs. Bintje and Santé in the four European
countries.
There was no consistent evidence across countries
for cultivar-specific isolates. However, in many cases the
tendency was for more aggressiveness among isolates
from cv. Bintje. Infection efficiency ranged from 0·0005
for Swiss isolates from cv. Santé to 0·0079 for Norwegian
isolates from cv. Bintje (Table 4). Isolates collected from
cv. Bintje showed a higher average IE compared to isolates
from cv. Santé (0·0030 and 0·0016, respectively).
However, no statistically significant effect for cultivar or
cultivar by country was detected (Table 4).
Lesion area ranged from 243 mm2 to 677 mm2 for iso-
lates collected on cv. Santé from Switzerland and the UK,
respectively. Average LA for isolates collected on Bintje
was 511 mm2, compared to 487 mm2 for isolates from
Santé. No significant difference was found for average LA
values for both cultivars, but a highly significant differen-
tial interaction for cultivar by country was detected
(P > 0·001). Sporulation density varied considerably
for P. infestans populations collected from cv. Bintje, but
not for populations sampled from cv. Santé (Table 4).
Average SPOR for isolates collected on cv. Bintje varied
from 276 to 466 sporangia mm−2 for French and Swiss
isolates, respectively. Sporulation density for isolates
originating from cv. Santé varied from 242 to 292
sporangia mm−2 for Norwegian and French isolates,
respectively. Significantly higher (P > 0·001) average SPOR
values were measured on isolates collected from cv. Bintje
compared to cv. Santé (362 versus 261 sporangia mm−2).
No significant cultivar effect was detected for sporulation
capacity estimated as 10LOG(SPOR*LA) (Table 4). A
highly significant differential interaction for cultivar by

Plant Pathology (2007) 56, 562–572

 Genetic variation in P. infestans from organic potatoes 567

Table 3 Incidence (in percentage) of physiological races of Phytophthora infestans in isolate samples collected from the susceptible potato cv. Bintje
and the moderately resistant cv. Santé organically grown in France, Norway, Switzerland and the United Kingdom in 2001 and 2002

Country

France Norway Switzerland UK

a
Race Bintje Santé Bintje Santé Bintje Santé Bintje Santé Average

0 0·0 6·7 6·7 13·3 0·0 4·3 7·1 0·0 4·8

1 0·0 0·0 40·0 3·3 0·0 4·3 7·1 0·0 6·9
3 0·0 0·0 0·0 3·3 0·0 0·0 0·0 0·0 0·4
1,3 0·0 0·0 0·0 0·0 0·0 0·0 3·6 0·0 0·4
1,7 0·0 0·0 16·7 13·3 41·2 0·0 3·6 0·0 9·3
1,10 0·0 0·0 10·0 0·0 0·0 0·0 0·0 0·0 1·3
1,11 0·0 0·0 0·0 0·0 0·0 0·0 3·6 0·0 0·4
1,2,7 0·0 0·0 0·0 0·0 35·3 0·0 0·0 0·0 4·4
1,3,7 0·0 0·0 3·3 0·0 0·0 0·0 0·0 4·2 0·9
1,3,11 3·3 3·3 0·0 3·3 0·0 0·0 32·1 4·2 5·8
1,2,3,7 0·0 0·0 0·0 0·0 2·9 0·0 0·0 0·0 0·4
1,2,7,10 0·0 0·0 0·0 0·0 2·9 0·0 0·0 0·0 0·4
1,3,7,11 40·0 83·3 20·0 53·3 5·9 21·7 35·7 79·2 42·4
1,3,10,11 6·7 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·8
1,2,3,7,10 3·3 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·4
1,2,3,7,11 20·0 3·3 0·0 6·7 2·9 21·7 7·1 12·5 9·3
1,2,3,10,11 6·7 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·8
1,3,4,7,11 0·0 3·3 0·0 0·0 0·0 0·0 0·0 0·0 0·4
1,3,7,10,11 13·3 0·0 0·0 0·0 8·8 21·7 0·0 0·0 5·5
1,2,3,4,7,11 3·3 0·0 0·0 0·0 0·0 0·0 0·0 0·0 0·4
1,2,3,5,7,11 0·0 0·0 0·0 3·3 0·0 0·0 0·0 0·0 0·4
1,2,3,7,10,11 3·3 0·0 3·3 0·0 0·0 13·0 0·0 0·0 2·5
1,2,3,4,6,7,10,11 0·0 0·0 0·0 0·0 0·0 13·0 0·0 0·0 1·6

a
Numbers refer to the described R-genes in the differential host plants that each race is capable of infecting.

Figure 1 Average number of virulence factors

for each Phytophthora infestans population
collected from the susceptible potato cv. Bintje
and the moderately resistant cv. Santé
organically grown in France, Norway, the UK
(2001) and Switzerland (2001 and 2002). Bars
indicate SED of the mean.

country was detected (P > 0·001) for both SPOR values
and 10Log (SPORCAP).
Population structure
A total of 69 AFLP genotypes were detected in 210
isolates using 137 AFLP loci amplified with two primer
combinations. A neighbour-joining tree showing the
genetic similarities between AFLP genotypes is presented
in Fig. 2. No AFLP genotype was detected in more than
one national P. infestans population, and no isolates with
AFLP genotypes associated with the US-1 clonal lineage,
typical of the old population of P. infestans, were detected
(Fig. 2) (data not shown). A total of 38 AFLP genotypes
were detected only once, and the most frequent AFLP
genotype (CHB04) was found in 21 isolates. The normalized
Shannon index of genetic diversity varied from 0·14 for
Swiss isolates collected from cv. Bintje in 2002 to 0·75 for
Norwegian isolates collected from cv. Santé (Table 2).
Modified Roger’s genetic distance coefficients for
cultivar specific subpopulations of P. infestans indicate
considerable differences between P. infestans populations
sampled from organic potato crops from France, Norway,
Switzerland and the UK (Table 5, Fig. 3). Cultivar specific

Plant Pathology (2007) 56, 562–572

568 W. G. Flier et al.

Table 4 Average restricted maximal likelihood (REML) estimates for epidemiological parameters of Phytophthora infestans isolates collected from
the susceptible potato cv. Bintje and the moderately resistant cv. Santé organically grown in France, Norway, Switzerland and the UK in 2001 and
2002

Epidemiological componentsa

IE LA SPOR LOG(SPORCAP)
10

Country of origin Bintje Santé Bintje Santé Bintje Santé Bintje Santé

Switzerland 0·0006 0·0005 426 243 466 246 5·2 4·7

France 0·0019 0·0010 676 549 276 292 5 5·1
Norway 0·0079 0·0013 363 479 281 242 4·7 5
UK 0·0015 0·0035 579 677 425 264 5·1 5·2
Average 0·0030 0·0016 511 487 362 261 5·0 5·0

χ2Cultivar 0·409 0·666 <0·001 0·81

χ2Cultivar × Country 0·242 <0·001 <0·001 <0·001

LSD(0·95)Cultivar 0·0061 188 88 0·2

LSD(0·95)Country 0·0063 186 88 0·2
LSD(0·95)Cultivar × Country 0·0064 200 94 0·2

IE = infection efficiency, LA = lesion area, SPOR = sporulation density, 10LOG(SPORCAP) = 10Log(LA × SPOR).
a

subpopulations of isolates from each country are without
exception most closely related to each other (Fig. 3). The
French pathogen population is most closely related to the
Swiss population sampled in 2001, although a significant
difference (P > 0·001) was detected between the French
population on cv. Bintje and the Swiss population from cv.
Santé, based on an exact test for population differentiation
(Table 5). The two Norwegian P. infestans subpopulations
were significantly different from other subpopulations,
except the Norwegian subpopulation on Santé, which
was not different from the Swiss subpopulation on Bintje
in 2001 (Table 5). Based on AFLP marker data, both
Swiss P. infestans subpopulations collected in 2001 differ
from the 2002 samples collected on cv. Santé, but not from
the 2002 samples from cv. Bintje. The pathogen population
from the UK showed some similarity to the Swiss population
collected in 2001 but not to other P. infestans populations
(Fig. 3, Table 5).
Discussion
Genetic variation in populations of P. infestans collected
from organic potato crops from France, Norway, Switzerland
and the UK were compared in terms of virulence phenotype,
aggressiveness and genetic marker variation. Using the
same traits, isolates collected from the susceptible cv.
Bintje were compared with isolates sampled from the
moderately resistant cv. Santé. The genetic structure of the
four P. infestans populations sampled varied from mainly
clonal populations showing restricted levels of genetic
diversity to mixed A1 and A2 mating type populations
showing high levels of genetic diversity, suggesting
periodic sexual reproduction.
Based on mating type distribution and mtDNA
haplotyping, all four European P. infestans populations
sampled belong to the newly established pathogen
population that was introduced around 1976 (Drenth
et al., 1994). In the UK and France, only the A1 mating
type was recovered and all isolates were of the Ia or IIa
mtDNA haplotype, both associated with the recently
introduced European P. infestans population. The absence
of A2 mating type strains in the sample from the UK
population is in line with the report by Day & Shattock
(1997) in which the A2 frequency in England and Wales
from 1993 to 1995 was estimated as 0–3%. Also, the
predominance of A1 isolates from Brittany is similar to
previous findings by Lebreton et al. (1998), who reported
A2 strains only from tomatoes, sampled in north-western
France from 1996 to 1997. In Norway, a late blight
population comprising both A1 and A2 mating type
strains was present at the site of the experimental field in
2001, with the majority of the A1 isolates (88%) collected
from cv. Santé. In a multiple year sampling (1993–1996)
of 128 isolates of P. infestans collected from south-
west Norway, the A1:A2 ratio was calculated as 7:3
(Hermansen et al. 2000), which is quite different from the
more limited 2001 data presented here.
The Ib haplotype, associated with the old clonal
P. infestans populations present in Europe during most of
the 20th Century (Spielman et al., 1991), was found in
37% of the Norwegian isolates but was not absolutely
associated with the A1 mating type strains, as was the case
in the old clonal population. These results suggest that
meiotic recombination has broken the association
between the A1 mating type and the Ib haplotype, and
therefore supports the view that sexual reproduction
occurs in the Norwegian late blight population (Brurberg
et al. 1999). The Swiss pathogen population was the only
one that was sampled over two years. Evidence exists
that oospores play a role in late blight epidemics in
Switzerland (Knapova & Gisi, 2002). In 2001, only A1
mating type isolates were recovered, which were all of the
Ia haplotype. In 2002, a strong shift towards A2 mating
type and IIa haplotype was observed. Only one A1 isolate
was recovered, which had the Ia haplotype. The observed
shifts in both mating type and mtDNA haplotype frequencies

Plant Pathology (2007) 56, 562–572

 Genetic variation in P. infestans from organic potatoes 569

in the Swiss isolate collection indicate that migration and

genetic drift at the end of each growing season may
strongly influence population structure and diversity in
regional P. infestans populations.
Race complexity varied considerably between the
regional P. infestans populations sampled. In all pathogen
samples but the French, isolates collected from cv. Santé
were more complex than isolates collected from cv. Bintje.
This may be related to the presence of the R1 and R10
resistance genes in cv. Santé (Flier et al., unpublished
data), although race 0 isolates were recovered from
cv. Santé at three sampling locations. The collection of
isolates without specific virulence factors from an R-gene
containing cultivar may be explained by experimental
errors in virulence testing, or physiological aging of the
host leading to a lower expression of R-gene induced
defence mechanisms (Stewart, 1990). Virulence for R5
was only detected in isolates from Norway, while
virulence for R6 was only found in the Swiss population.
Specific virulence for R4 was not detected in Norwegian
samples, and UK isolates were characterized by a lack of
virulence to R10. In a previous study of virulence diversity
in Norwegian P. infestans isolates collected in 1996
(Hermansen et al., 2000), it was found that virulence to
R5 and R6 was rare while virulence for R4 was common.
In that study, about 10% of the isolates came from the
same region as isolates from the present study, and no
regional pattern of the virulence data was found. There
appear to be significant differences in virulence spectrum
that may reflect random shifts in race composition
and differences in R-gene deployment in popular potato
cultivars in each country.
AFLP fingerprinting supported the idea of moderate
genetic substructuring between the four P. infestans
populations sampled. No AFLP based P. infestans
genotype was detected in more than one sampling location
and many of the AFLP genotypes were only detected once.
It is concluded that high levels of genetic variation are
being maintained in both putatively sexually reproducing
local populations (e.g. Norway) and asexual reproducing
populations (e.g. France). Given the very limited sampling
scheme which comprised a collection of approximately 30
isolates from two cultivars, it is remarkable that values up
to 0·75 for the normalized Shannon index of diversity are
found, indicating high levels of genetic diversity. These
findings are in line with an earlier report on genetic
diversity of isolates from Norway and Finland (Brurberg
et al., 1999). Diversity in isolate samples also differed

Figure 2 Dendrogram of genotypes of Phytophthora infestans

collected from the susceptible potato cv. Bintje and the moderately
resistant cv. Santé (numbers of identical isolates in parentheses)
organically grown in France, Norway, Switzerland and the UK in 2001
and 2002. Neighbour joining tree was constructed using AFLP
markers. The scale shown is the genetic distance calculated using
Roger’s modified genetic distance coefficients. Numbers at the nodes
represent bootstrap values supporting the branches, generated from
1000 random permutations. Isolate VK6C, an A1 isolate collected in the
Netherlands in 1958, (Flier et al., 2001) was included as an outgroup.

Plant Pathology (2007) 56, 562–572

570 W. G. Flier et al.

Figure 3 Cluster analysis of 10 subpopulations

of Phytophthora infestans collected from the
susceptible potato cv. Bintje and the
moderately resistant cv. Santé organically
grown in France, Norway, Switzerland and the
UK in 2001 and 2002. Dendrogram is based on
UPMGA clustering using Roger’s modified
genetic distance coefficients.

Table 5 Matrix of genetic distance and population differentiation for Phytophthora infestans populations collected from the susceptible potato cv.
Bintje and the moderately resistant cv. Santé organically grown in France, Norway, Switzerland and the UK in 2001 and 2002. Values above the
diagonal are probabilitiesa for each pair wise comparison using an exact test (Raymond & Rousset, 1995), values below the diagonal are Wright’s
modified Roger’s distance

NB2001 NS2001 FB2001 FS2001 UKB2001 UKS2001 CHB2001 CHS2001 CHB2002 CHS2002

NB2001 0·000 0·000 0·000 0·000 0·000 0·000 0·000 0·000 0·000
NS2001 0·228 0·000 0·000 0·000 0·000 0·607 0·000 0·000 0·000
FB2001 0·311 0·267 1·000 0·000 0·000 1·000 0·000 0·000 0·000
FS2001 0·340 0·283 0·155 0·000 0·000 1·000 0·400 0·000 0·000
UKB2001 0·362 0·326 0·274 0·264 0·006 0·995 0·000 0·000 0·000
UKS2001 0·369 0·312 0·280 0·273 0·231 0·999 0·018 0·000 0·000
CHB2001 0·380 0·329 0·260 0·238 0·286 0·281 1·000 0·000 1·000
CHS2001 0·363 0·323 0·260 0·230 0·279 0·273 0·184 0·000 0·168
CHB2002 0·438 0·396 0·402 0·387 0·392 0·384 0·426 0·402 0·000
CHS2002 0·390 0·361 0·347 0·326 0·340 0·320 0·355 0·321 0·370

a
Probability level considered significant if <0·05.

from year to year. For the Swiss sampling site, where two
years of data were available, no AFLP genotype detected
in the 2001sampling was recovered in the following year
and a strong shift in mating type distribution was observed.
The results presented here are in line with other studies
reporting strong year-to-year effects on pathogen diversity
in the Netherlands and England and Wales (UK)
(Zwankhuizen et al., 2000; Day et al., 2004).
Recent work by Carlisle et al. (2002) has shown that
differences in aggressiveness between P. infestans isolates
can be detected with improved resolution when moderately
resistant cultivars are used as tester cultivars. In the current
experiments, significant differences were detected in
epidemic parameters despite the fact that the susceptible
cv. Bintje was used. The detection of significant cultivar by
country differential interactions for the epidemic parameters
LGR, LA and SPOR is in line with the view that the four
late blight populations that were sampled show some level
of genetic differentiation.
No evidence has been found to support the hypothesis
that P. infestans strains collected from the moderately
resistant cv. Santé show increased levels of pathogenicity
compared to isolates collected from the susceptible cv.
Bintje. On the contrary, isolates collected from cv. Bintje
were (for the epidemic parameters tested) on average
more aggressive than, or comparable to, isolates from cv.
Santé. This result is consistent with earlier findings by
Pilet (2003) and Montarry et al. (2006), who found
that isolates from partially resistant potato cultivars
showed lower aggressiveness levels than isolates collected
from susceptible cultivars. However, it should be noted
that the observed differences in aggressiveness for isolates
sampled from cvs Bintje and Santé were not consistently
observed for all countries and that significant country by
cultivar differential interactions existed.
In this work, the possible confounding effect of adaptation
to cv. Bintje cannot be excluded, since all sporangial
suspensions were produced and tested on cv. Bintje.

Plant Pathology (2007) 56, 562–572

 Genetic variation in P. infestans from organic potatoes
However, previous results (Flier et al., unpublished data)
indicate this effect to be of limited importance in
aggressiveness testing.
Although the sample sizes were small, no evidence was
found to suggest a directional selection towards increased
aggressiveness to the more resistant cv. Santé and therefore
such shifts are unlikely to occur under field conditions.
However, a complicating factor in making general predictions
on stability of resistance to late blight is the presence of
considerable differences in structure and diversity of
regional P. infestans populations. Recent international
and intercontinental collaborative studies have explored
the stability and evaluation of cultivar resistance exposed
to indigenous late blight isolates or natural inoculum
(Hansen et al., 2005; Forbes et al., 2005).
It is recommended, therefore, that together with a large
scale introduction of more resistant potato cultivars, a
monitoring programme is set-up to evaluate the stability
of the resistance of regionally grown cultivars. Such a
monitoring programme could serve as an early warning
system, valuable in resistance management in both organic
and non-organic potato production systems in Europe.
The Concerted Action EUCABLIGHT, a consortium of
European blight researchers and breeders, has agreed on
improved methods for assessment of resistant germplasm
in field trials and in the laboratory (http://www.
eucablight.org, ‘Protocols’ section). The inclusion of com-
mon standards with a range of late blight resistance will
allow researchers to compare the expression of resistance
in clones grown in different climates and exposed to
different strains and populations of P. infestans (Colon
et al. 2005).
Acknowledgements
This research was supported by the European Commission
(EU-Framework Five project QLK5-CT-2000- 01 065
BLIGHT MOP) and the Netherlands Ministry of Agriculture,
Nature Management and Food Safety (LNV-DWK
research programmes 342 and 397). We thank all those
that were involved in providing isolates and we are very
grateful for all the stimulating discussions with the
members of the BLIGHT MOP community.
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