The European barley powdery mildew virulence survey and disease nursery 1993-1999

Abstract

National barley powdery mildew virulence surveys were co-ordinated through COST817 on a European scale from 1993 to 1999 to allow comparison of results actress national borders. The frequencies of virulence matching resistance genes Mla1, Mla3, Mla6, Mla7, Mla9, Mla12, Mla13, Mlk, M1La and Mig were moderate to high in most years and countries. Several additional sources of resistance were matched by virulence frequencies below 5%. Generally, no increase in aggressiveness against Mlo-resistance was detected, but change may be under way as particular isolates of British origin gave higher infection levels on Mlo-resistant varieties than did other groups of isolates. Therefore, it is important in the future to focus on virulence matching the new sources of resistance and Mlo. Multi-location field trials were established in 1998 and 1999 in order to study powdery mildew resistance in barley genotypes in different environments. The trials showed large interactions of location and phenotypic expression of the resistance. A continued exchange of ideas, methodology and plant material between national survey programmes, and a rapid dissemination of results to farmers and plant breeders across Europe is vital.

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The European barley powdery mildew virulence survey
and disease nursery 1993-1999
Mogens Hovmøller, Valérie Caer, Marja Jalli
To cite this version:
Mogens Hovmøller, Valérie Caer, Marja Jalli. The European barley powdery mildew viru-
lence survey and disease nursery 1993-1999. Agronomie, EDP Sciences, 2000, 20 (7), pp.729-743.
�10.1051/agro:2000172�. �hal-00886083�

Plant Genetics and Breeding
Original article
The European barley powdery mildew virulence survey
and disease nursery 1993–1999
Mogens S. HOVMØLLERa*, Valérie CAFFIERb, Marja JALLIc, Ole ANDERSEN**,
Gottfried BESENHOFER**, Jerzy H. CZEMBOR**, Antonin DREISEITL**,
Friedrich FELSENSTEIN**, Andreas FLECK**, Fritz HEINRICS**, Rickard JONSSON**,
Eckhard LIMPERT**, Peter MERCER**, Svetozar PLESNIK**, Isaak RASHAL**,
Helge SKINNES**, Susan SLATER**, Olga VRONSKA**
a Danish Institute of Agricultural Sciences, Research Centre Flakkebjerg, 4200 Slagelse, Denmark
b Station of Plant Pathology, INRA, BP 57, 49071 Beaucouzé Cedex, France
c Boreal Plant Breeding Ltd., Myllytie 10, 31600 Jokioinen, Finland
(Received 10 May 2000; revised 5 July 2000; accepted 3 August 2000)
Abstract – National barley powdery mildew virulence surveys were co-ordinated through COST817 on a European scale
from 1993 to 1999 to allow comparison of results across national borders. The frequencies of virulence matching resis-
tance genes Mla1, Mla3, Mla6, Mla7, Mla9, Mla12, Mla13, Mlk, MlLa and Mlg were moderate to high in most years and
countries. Several additional sources of resistance were matched by virulence frequencies below 5%. Generally, no
increase in aggressiveness against Mlo-resistance was detected, but change may be under way as particular isolates of
British origin gave higher infection levels on Mlo-resistant varieties than did other groups of isolates. Therefore, it is
important in the future to focus on virulence matching the new sources of resistance and Mlo. Multi-location field trials
were established in 1998 and 1999 in order to study powdery mildew resistance in barley genotypes in different envi-
ronments. The trials showed large interactions of location and phenotypic expression of the resistance. A continued
exchange of ideas, methodology and plant material between national survey programmes, and a rapid dissemination of
results to farmers and plant breeders across Europe is vital.
Erysiphe graminis f. sp. hordei / virulence survey / disease nursery / partial resistance / blumeria graminis f. sp.
hordei
Agronomie 20 (2000) 729–743 729
© INRA, EDP Sciences 2000
Communicated by Hanne Østergård (Roskilde, Denmark)
* Correspondence and reprints
Mogens.Hovmoller@agrsci.dk
** Affiliations are in Appendix.

M.S. Hovmøller et al.
730
1. Introduction
The use of host resistance to control barley pow-
dery mildew, caused by the fungus Blumeria
(Erysiphe) graminis f. sp. hordei, is widely recom-
mended because it is environmentally safe and
comes with the seed at no extra cost to the farmer.
However, the use of the same resistance genes
across wide areas leads to selection in favour of
pathotypes with the matching virulence genes in
the pathogen population [1, 5, 21, 31, 50]. This
may result in previously resistant varieties becom-
ing susceptible, often referred to as the ‘break-
down’ of resistance.
For more than fifty years, barley powdery
mildew ‘race-surveys’ [e.g. 17, 37, 49] and later
national ‘virulence surveys’ have been carried out
throughout Europe [e.g. 1, 11, 14, 18, 24, 34, 40,
45, 47, 48, 53]. The surveys in the different coun-
tries often have slightly different objectives, and
therefore use different sampling strategies and test
methods. Nevertheless, most surveys have a com-
mon aim of monitoring changes in frequencies of
pathotypes (or single genes) of relevance for resis-
tance breeding and plant production. Surveys may
also provide the basis for variety diversification
schemes [45] and can be used in giving advice on
disease risk and fungicide management [13].
Finally, survey data may be used to study the
dynamics of the pathogen population on a regional
or international scale [6, 9, 30, 52].
When a particular source of resistance has been
overcome by the pathogen population in one area,
varieties possessing the same resistance are at risk
in neighbouring areas. This is mainly because the
pathogen is easily spread by airborne spores, often
not very far from the plant on which they were pro-
duced but under optimal conditions up to several
hundred km, from one country to the other [16].
To ensure sufficient powdery mildew control by
the use of host resistance, new sources of resis-
tance should currently be entering breeding pro-
grammes, e.g. resistance genes from wild relatives
of barley [25, 44]. Another strategy is to increase
the general level of resistance to powdery mildew
in the barley germ plasm [27]. Such resistance,
denoted ‘partial resistance’, is not based on single
genes with a major effect, and it has been subject
to much interest because it is often considered to
remain effective for a longer time than race-specif-
ic resistance genes [39]. Partial resistance is often
expressed in adult plants, and the efficiency
depends much on environment [36]. Under field
conditions, partial resistance is expressed by a slow
powdery mildew development, and under laborato-
ry conditions, partial resistance can be assessed by
Résumé – Étude des virulences dans les populations d’oïdium de l’orge et évaluation des variétés pour leurs
résistances partielles à l’échelle européenne de 1993 à 1999. Les suivis nationaux de virulences chez l’oïdium de
l’orge ont été coordonnés à l’échelle européenne de 1993 à 1999 dans le cadre de l’action COST817. L’objectif était de
comparer les résultats au-delà des frontières nationales. Les fréquences de virulences correspondant aux gènes de résis-
tance Mla1, Mla3, Mla6, Mla7, Mla9, Mla12, Mla13, Mlk, MlLa et Mlg étaient modérées à fortes pour la plupart des
années et des pays. Pour plusieurs sources de résistance supplémentaires, les fréquences de virulences étaient inférieures
à 5 %. En général, aucune augmentation d’agressivité vis-à-vis de la résistance Mlo n’a été détectée, mais des change-
ments pourraient être en cours puisque des isolats particuliers d’origine britannique inoculés sur des variétés possédant
la résistance Mlo ont présenté des niveaux d’infection plus élevés que d’autres groupes d’isolats. Par conséquent, il est
important dans le futur d’étudier avec attention les virulences correspondant aux nouvelles sources de résistance et à la
résistance Mlo. Des essais au champ multilocaux ont été mis en place en 1998 et 1999 pour étudier la résistance à
l’oïdium des génotypes d’orge dans différents environnements. Ces essais ont montré de grandes interactions entre lieu
et expression phénotypique de la résistance. Il est primordial de poursuivre les échanges d’idées, de méthodologie et de
matériel végétal entre programmes de suivis nationaux, et de distribuer rapidement les résultats aux agriculteurs et aux
sélectionneurs à travers l’Europe.
Erysiphe graminis f. sp. hordei / suivi européen / virulence / résistance partielle / Blumeria graminis f. sp. hordei

European co-ordination of barley powdery mildew studies 731
parameters influencing infection frequency, latent
period and/or sporulation capacity [26]. The for-
mation of papillae is one major component of par-
tial resistance [15]. As the efficiency of partial
resistance depends on environment it is preferable
to make the tests at various sites, e.g. to expose the
material to different pathogen populations.
Within COST817, national virulence surveys
and evaluation of varieties for partial resistance
were co-ordinated on a European scale. In the pre-
sent paper, the authors present changes and differ-
ences in virulence gene frequencies in a pathogen
population consisting of airborne spores sampled
across wide geographical areas for several succes-
sive years. Examples of different virulence survey
approaches in different European countries are
shown, and the usefulness of the different type of
results obtained is discussed. The paper also
describes results from multinational barley pow-
dery mildew field nurseries, aimed at identifying
promising sources of partial resistance in the bar-
ley germplasm. The success of such work depends
to a large extent on knowledge of the virulence dis-
tribution in the local pathogen population.
2. Materials and methods
2.1. Virulence surveys
The barley powdery mildew virulence surveys
have two main aspects, sampling and virulence
testing. There have been different approaches to
sampling, viz. use of trap plants in barley fields or
at a location distant from barley crops [22]; mobile
spore traps attached to a car roof and which collect
spores by exposing susceptible plants while driving
[30, 41]; collection of isolates from leaf samples
from barley crops [45]. Thus, sampling was not
always carried out on a strictly random basis, but
aimed to collect the most relevant information for
the purpose of the survey (Tab. I). Samples of ran-
dom airborne powdery mildew spores in most
countries were collected during summer when both
autumn sown barley and spring sown barley were
present (Tab. I). In most countries, single colonies
were collected on varieties that were susceptible to
the current powdery mildew population. In some
countries, additional samples were collected on
varieties with Mlo-resistance.
The virulence testing was generally carried out
by inoculating detached leaf segments of differen-
tial lines or varieties placed on agar containing
benzimidazole. The differential lines were chosen
to have different resistance genes (Tab. II). Some
of them have been extensively used in European
varieties [7] whereas others have been included
only recently in breeding programmes and are not
yet widely used by growers. When available, near
isogenic lines of Pallas [28] were used. After 7 to
8 days of incubation (e.g. 16 °C, continuous light,
10 µE·s–1·m–2), the infection types (IT) were
scored on a 0–4 scale [35]. Isolates were classified
as avirulent (ITs 0–3) or virulent (IT 4) on the vari-
eties used; in specific cases, the infection types
were interpreted genetically, indicating the pres-
ence of specific avirulence and virulence alleles
[22].
‘Early’ detection of pathotypes matching new
sources of resistance was carried out through a
detailed screening of resistant varieties in naturally
infected disease nursery plots (Denmark) [18].
Sampling of colonies/lesions took place when their
presence was first reported on a certain
variety/breeding line, often in May–June (sum-
mer). Potential colonies were further multiplied
and inoculated on an extended differential set
(Tab. II), and sometimes further tested on commer-
cial varieties/breeding lines. Additional tests for
increased virulence/aggressiveness on Mlo-resis-
tant varieties were generally done by counting
colonies on trap plants of such varieties in compar-
ison to susceptible control plants. Selected isolates
were further investigated by the procedure devel-
oped by Lyngkjær et al. [33] (Denmark only) or by
repeated tests using seedlings of a larger range of
Mlo-resistant varieties (UK only).
2.2. Disease nurseries
In 1998 and 1999, spring barley nurseries were
sown in up to seven European countries, i.e.
Plant Genetics and Breeding

M.S. Hovmøller et al.
732
Austria, Denmark (two sites in 1998), Finland,
Germany, Latvia, Norway and Sweden. Altogether,
36 varieties and breeding lines were investigated,
and 16 were tested at all sites in both years. The
seed was sown in fields in 2–4 replicates using
small plots or hill plots. The level of powdery
mildew was assessed as an average score for each
small plot, based on natural powdery mildew infec-
tion. The assessments were carried out 2–3 times at
each location and year, where the following scale
(either expressed as a figure between 0 and 9 or in
percent) was used: 0: no powdery mildew symp-
toms in the plot, 1 (= 0.1% leaf area covered): less
than one colony/plant, 2 (= 0.5%): approximately
three colonies/tiller, 3 (= 1%): approximately five
colonies/leaf, 4 (= 5%): two lower leaves approxi-
mately 25% covered by powdery mildew, 5
(= 10%): two lower leaves approximately 50%
covered by powdery mildew, 6 (= 25%): half of the
leaf area appear to be diseased, 7 (= 50%): leaves
appeared more diseased than green, 8 (= 75%):
very little green tissus left, 9 (= 100%): all leaves
dead. In 1999, a set of Pallas near-isogenic lines
(cf. Tab. II) was sown together with disease nurs-
eries in Austria, Denmark, Finland and Sweden in
order to obtain a local estimate of the virulence
spectrum.
3. Results and discussion
3.1. Barley powdery mildew virulence surveys
in Europe
In the following, examples of different
approaches to virulence surveys in Europe are
described.
3.1.1. Early detection of ‘new’ virulence
One purpose of virulence surveys is to observe
the very first indication of a ‘break down’ of newly
utilised resistance genes, e.g. a change in virulence
frequency from 0 to 1% in the aerial population.
Table III presents an example of the evolution of
virulence matching the resistance in recently
released barley varieties in Denmark. Virulence
was detected at least once for all varieties except
Table I. Sampling details for the barley powdery mildew virulence survey in Europe.
Country Sampling details
Season Trap plant exposure Trap plant variety Local contact person
Austria (AT) Summer Mobile spore trap Dvoran S. Plesnik; G. Besenhofer
Czech Republic (CZ) Summer Mobile spore trap Pallas A. Dreiseitl
Germany (DE) Summer Mobile spore trap Igri, Pastoral F. Felsenstein, K. Flath
and in fields
Denmark (DK) Winter Stationary (remote) Igri, Apex, Alexis MS. Hovmoller
Finland (FI) Summer Fields* Golden Promise M. Jalli
France (FR) Winter Mobile spore trap Igri V. Caffier, L. Bousset
Hungary (HU) Summer Mobile spore trap Dvoran S. Plesnik
N. Ireland (NI) Summer Fields Golden Promise P. Mercer, A. Ruddock
Latvia (LV) Summer Fields Otra I. Rashal, I. Kokina, I. Araja
Poland (PL) Summer Fields Manchuria J.H. Czembor, E. Gacek, R. Bilinski;
H.J. Czembor
Slovakia (SK) Summer Mobile spore trap Dvoran S. Plesnik, E. Krippel, M. Sykora
Ukraine (UA) Summer In fields* ? O. Vronska, G. Kosilovich
Great Britain (GB) Winter and Stationary (remote) and Golden Promise, S. Slater, J.D.S. Clarkson
summer from infected leaves Apex, Riviera
* or from infected leaves.

European co-ordination of barley powdery mildew studies 733
Plant Genetics and Breeding
Table II. Differential varieties used in the national virulence surveys and known powdery mildew resistance genes in
these (country codeain parenthesis).
No. Pallas line [28] Supplementary variety Resistance gene(s) b
1 Pallas (DK) Mla8
2 P01 (all except GB and NI) Tyra (GB), Delta (NI) Mla1, Ml(Al2)
3 P02 (all except GB and NI) Ricardo (GB) Mla3
4 P03 (all except GB and NI) Midas (GB, NI) Mla6, Mla14
5 P04B (all except GB and NI) Porter (GB), Regina (GB) Mla7, Ml(No3)
6 P08B (all except GB and NI) Roland (GB), Leith (NI) Mla9
7 P10 (all except GB and NI) Hassan (GB, NI) Mla12, Ml(Em2)
8 P11 (all except GB and NI) Digger (GB, NI) Mla13, Ml(Ru3)
9 P16 (all except GB and NI) Hordeum 1063 (GB), P17 (DE, LV) Mlk
10 P23 (all except GB and NI) Lofa Abed (GB), Varunda (NI) MlLa
11 P09 (DK, FR, PL) Mla10, Ml(Du2)
12 P12 (DK, FI, FR, PL) Mla22
13 P13 (LV, PL) Mla23
14 P19 (LV, PL) Mlp
15 P20 (CZ, DK, LV, PL) Mlat
16 P21 (AT, DK, FR, HU, FI, PL) Zephyr (GB, NI) Mlg, Ml(CP)
17 P22 (LV, PL) mlo5
18 P24 (DK, FI, FR, LV, PL) Weihenstephan 37/136 (GB) Mlh
19 Gunnar (DK, PL) Mla3, Ml(Tu2)
20 Punto (DK) Mla3, Ml/Tu2), Ml(Im9), Ml(Hu4)
21 Goldspear (NI) Mla6, MlLa
22 Triumph (AT, HU, PL, SK, GB NI) Mla7, Ml(Ab)
23 Keg (NI) Mla7, Mlk
24 Klaxon (NI) Mla7, Mlk, MlLa
25 Hulda (DK) Mla7, Ml(Im9), Ml(Hu4)
26 Henni (DK) Mla7, U
27 Simon (GB) Mla9, Mlk
28 Benedicte (DK, PL) Mla9, Ml(Im9)
29 Egmont (NI) Mla12, MlLa
30 Goldie (DK, FR, LV, SK) Mla12,MlLa, U
31 Tofta (DK) Mla13,Ml(Im9)
32 Meltan (DK, FR, LV, SK) Mla13,Ml(Im9), Ml(Hu4)
33 Tyne (NI) Mla13, MlLa
34 Dram (NI) Mlk, MlLa
35 Apex (DK, GB) mlo11
36 SV83380 (DK), Lotta (GB) Ml(Ab)
37 Goldfoil (GB) Mlg
38 Weihenstephan 41/145 (GB) Mlra
39 Jarek (LV, PL) MlLa, Ml(Kr)
40 Steffi (DK, FR, LV, PL, SK) Ml(St1), Ml(St2)
41 SI1 (DK, FR, LV, SK) Ml(SI1)
42 Optima (DK) U1
43 Scarlett (DK) U2
aAT Austria, CZ Czech Republic, DE Germany, DK Denmark, FI Finland, FR France, HU Hungary, NI N.Ireland, LV Latvia,
PL Poland, SK Slovakia, UA Ukraine, GB Great Britain.
bDesignation according to [3].

M.S. Hovmøller et al.
734
Punto and SI1, which is a new source of resistance
(A. Jahoor, personal communication). Some fre-
quencies increased markedly, e.g. virulence match-
ing Steffi, Henni and Goldie. However, Steffi was
never grown extensively in Denmark, whereas
Henni and Goldie occupied up to 10–15% of the
spring barley area. In 1999, Steffi, Goldie, Meltan
and SI1 were also included in the differential sets
in France, Slovakia and Latvia. Results for viru-
lence on Steffi, Goldie and Meltan were similar to
those observed in Denmark in 1999, but virulence
matching SI1 was detected in Slovakia and Latvia.
The Mlo resistance constitutes a particular case.
It is based on a single recessive allele among sev-
eral known mlo-alleles (see Lyngkaer et al., this
volume). Although Mlo-resistant varieties have
been grown since 1979, only low levels of infec-
tion are occasionally seen on these varieties. Such
sporadic infections reflect traits of the different
types of host cells, and not a genetic change in the
pathogen population [27, 32, 42].
In the national survey programmes, most labora-
tories have included Mlo-resistant varieties in their
differential sets. In these sets, Mlo-resistant Apex
sometimes exhibited infection, but the reactions
were generally not repeatable, suggesting that
slightly variable test conditions were the cause of
the sporadic infections seen in some standard sur-
vey tests [45]. In Denmark, increased Mlo-aggres-
siveness has not been detected in the aerial mildew
populations. The Danish investigations were based
on the number of colonies on trap plants of Apex
and Alexis, and generally accounted for less than
1% of those collected on variety Igri, which pos-
sesses Mlra being matched by more than 99% of
the Danish barley powdery mildew population.
Between 1993 and 1997, approximately 100 iso-
lates were analysed by the technique developed by
Lyngkjær et al. [33], and in these tests no isolates
with increased virulence were found.
A comprehensive survey was carried out in GB
in 1998 and 1999 (Tab. IV). Isolates of three dif-
ferent origins were investigated: (1) isolates col-
lected from Mlo-resistant varieties, (2) isolates
from random spore samples giving rise to more
mildew than expected on the Mlo differentials
Apex and Riviera (denoted Apex+), and (3) iso-
lates from the same source as (2) but showing no
infections on Apex or Riviera in the original tests
(denoted Apex0). Specific isolates were tested in
both years, and repeated up to four times. Actual
infection levels varied between tests and years, but
the ranking of varieties remained the same. In gen-
eral, Apex+ isolates gave the highest infection lev-
els in all tests, but in one of the four tests, the iso-
lates collected on Mlo-resistant varieties gave
highest infection (details not shown). The lowest
amount of infection was given by isolates designat-
ed Apex0, i.e. isolates that in the initial survey tests
showed no infection on Apex or Riviera. All the
Mlo-resistant varieties grown remained highly
resistant under field conditions.
A survey carried out in Germany, Czech
Republic and Slovakia in 1997 resulted in a few
isolates denoted ‘partially Mlo-virulent’, i.e. iso-
lates that gave at least five times higher infection
efficiency than ‘wild-types’ and were self-sustain-
able on the Mlo-resistant host [42]. None of the
isolates tested was as aggressive as isolate HL-3,
developed in a selection-mutation experiment by
Table III. Summary of virulence frequencies (%) matching resistance in newly released varieties in Denmark.
Year No isolates Virulence frequencies (%)
Steffi Henni Benedicte Goldie Meltan Optima Scarlett Gunnar SI1 Punto
1996/1997 168 <1 – 2 2 0 – – <1 0 0
1997/1998 152 2 – 5 6 2 – – 1 0 0
1998/1999 190 14 14 5 13 3 6 8 3 0 0
1999/2000 98 31 41 6 14 2 9 12 4 0 0

European co-ordination of barley powdery mildew studies 735
Schwarzbach [42]. HL-3 is one of two known and
intensively studied ‘Mlo-virulent’ isolates; the
other (designated ‘Race I’) was collected in Japan
in the late 1950s [33]. See also the paper by
Lyngkjær et al. in this volume.
It is thus possible, that some selection in favour
of increased growth on Mlo-resistant varieties has
taken place in the barley powdery mildew popula-
tion in Britain and elsewhere in Europe.
3.1.2. Virulence dynamics in Europe
Between 20 and 767 single colonies of barley
powdery mildew were tested annually in each
country. A set of 9 differential lines was included
in most countries to compare virulence frequencies
on a European scale [2]. In general, the nine viru-
lence frequencies were intermediate to high, there-
by having only a minor effect in controlling pow-
dery mildew in Europe (Fig. 1). This was the case
for all regions and years, except the frequencies of
Va3 in the British Isles and France, where varieties
with the matching resistance gene were not grown.
However, the virulence was also present in these
areas, and if varieties with Mla3 resistance were
introduced, this resistance would probably be over-
come within a short time. Frequencies of Va7, Va9,
Va12, Vk and VLa in many cases were higher than
50%, which can be explained by a frequent use of
the matching resistance genes. From 1995 to 1999,
the main changes concerned Va1 (increase in GB,
FR, LV, DK, FI, AT, HU), Va13 (decrease in GB,
FR, DK, increase in CZ), and VLa (increase in GB,
NI, FR, DK, FI, CZ). Other virulences that were
only analysed in some countries had intermediate
to high frequencies, e.g. Va10, Va22, Vg, Vh, Vat,
V1192, VCP, VAb.
Most of the barley varieties used in Europe pos-
sess more than one powdery mildew resistance
gene [7, 8, 10, 12]. In survey programmes that aim
to predict the effect of powdery mildew resistance
in commercial varieties, and to give advice for
breeders and farmers, it is therefore important to
provide frequencies of virulence gene combina-
tions. In many cases, such frequencies deviate
from the product of the single gene frequencies due
to gametic disequilibria (syn. linkage disequilibria
or non-random associations) in the barley powdery
mildew population [e.g. 20, 51].
In the Danish survey, a number of variety groups
were defined according to the presence of resis-
tance genes and combinations thereof (Tab. V). In
general, the virulence frequencies matching single
resistance genes remained intermediate to high
between 1996 and 1999, and so did the combina-
tions (Tab. VI). At present, the powdery mildew
resistances of these varieties are therefore unlikely
to provide sufficient powdery mildew control in
years with favourable conditions for disease devel-
opment. However, in years prior to 1996, several
resistance gene combinations were effective in
controlling mildew under field conditions, while
the genes singly gave insufficient control (data not
shown).
Plant Genetics and Breeding
Table IV. Percent powdery mildew infection, relative to Golden Promise (susceptible standard) on varieties carrying
mlo-resistance. Summary based on Slater and Clarkson [45, 46].
Isolate designation Year collected Year tested No isolates Chariot Landlord Riviera Chalice Apex
Apex0 1970 1999 1 0 0 0 0 0
Apex0 1998 1998 15 0.8 0.1 0.6 6.8 2.2
Apex0 1998 1999 2a
0 0 0 1.3 0
Apex+ 1998 1998 14 3.0 0.4 1.7 10.2 2.2
Apex+ 1998 1999 5b
5.0 0.8 6.0 12.0 8.5
Apex+ 1999 1999 12 1.9 0.3 2.2 5.3 4.5
Mlo 1998 1998 7 3.5 0.6 1.9 11.3 3.6
a
Isolates chosen among the 15 tested in 1998.
b Isolates chosen among the 14 tested in 1998.

M.S. Hovmøller et al.
736

European co-ordination of barley powdery mildew studies 737
Plant Genetics and Breeding
Figure 1. Virulence frequencies in barley powdery mildew populations in Europe in 1995 and 1999*. A grey bar indicates no data for the matching virulence. The
number of isolates tested in each country is indicated in brackets. Country code: AT Austria, CZ Czech Republic, DE Germany, DK Denmark, FI Finland, FR
France, HU Hungary, LV Latvia, NI Northern Ireland, PL Poland, SK Slovakia, UA Ukraine, UK United Kingdom.
* In NI, data from 1998 instead of data from 1999.

M.S. Hovmøller et al.
738
3.1.3. Distribution of results
To the extent that survey data aim at giving
advice to farmers and plant breeders, it is essential
that the information is distributed efficiently and as
soon as possible after the tests have been made. In
many cases, results may be distributed to end users
informally at meetings and through personal con-
tacts, or they are published in annual reports [e.g.
34, 45]. In Denmark, results have been published
through ‘Planteinfo’ which can be accessed
through the Internet (http://www.planteinfo.dk).
Booklets, which include results from variety trials,
are published in October-November shortly after
the growing season [19]. Weekly farming newspa-
pers and magazines also display relevant data. ‘PC-
Plant Protection’, a PC-based decision support sys-
tem [43], is another important channel through
which results are transmitted to farmers and advi-
sors. Survey data are utilised in a similar manner in
other European countries [29].
3.2. Field nurseries
A multinational disease nursery aimed at identi-
fying useful sources of resistance was carried out
in 1998 and 1999. The highest levels of powdery
mildew resistance were observed for the genotypes
Hadm15458-96, Hadm15262-96 and Ivana, with
disease scorings close to zero across all environ-
ments (Tab. VII). However, recent studies suggest
that Ivana (in Germany named Eunova) possess
mlo-resistance. The resistance of the two varieties
from Hadmersleben was not expressed in associat-
ed chlorosis or necrosisis, and may be based on
effective, single resistance genes rather than partial
resistance. However, in the absence of isolates with
matching virulence, it may not be possible to draw
conclusions about the genetic basis for these resis-
tances.
There were considerable differences in climatic
conditions between locations and years. The
majority of the genotypes had a strong interaction
with environment, except varieties Arve and Tyra,
which were highly susceptible at all sites in both
years. The phenotypic expression of resistance in
Ohara, Optic, Cooper P 3645 C; Prosa, Hanka,
Thule, Inari, Viivi, Bor88369 and Bor88377
changed according to location, even within the
same country. The Pallas near-isogenic lines sown
Table V. Danish grown spring barley varieties and their powdery mildew resistance.
1. Mla7+Mlk, Mla7 : Limbo, Sultane, Tilda
2. Mla12+Mlg, Mla12 : Ballarina, Caminant, Maud
3. Mla7+Mlk+MlLa+Mlg, Mla7+MlLa : Canut, Escort
4. Mla12+MlAb+MlLa+Mlg, Mla12+Mlab : Optic, Blenheim
5. Mla13+Mlk+Mlg, Mla13 : Caruso, Collie, Digger, Senor
6. Mla3 : Shamu, Baronesse
7. Mla13+MlLa, Mla13+MlAb, Mla13+MlLa+Mlg : Etna, Evelyn, Lysimax
8. Mla1+MlLa, MLa1+MlAb, Mla1 : Cooper, Cork, Texane
Table VI. Summary of virulence frequencies in Denmark from autumn 1996 to autumn 1999, shown as intervals corre-
sponding to highest and lowest frequency, respectively, within groups (cf. Tab. V).
Year Number of isolates Resistance group
1 2 3 4 5 6 7 8
1996/1997 168 55–83 63–70 29–42 9–31 24–41 28 16–20 11–29
1997/1998 152 48–77 63–74 22–43 12–24 17–33 33 13–17 6–22
1998/1999 190 41–59 71–73 31–45 42–57 15–21 17 12–15 29–33
1999/2000 98 35–69 53–55 19–41 15–32 11–21 34 8–14 9–17

European co-ordination of barley powdery mildew studies 739
Plant Genetics and Breeding
Table VII. The maximum percentage of leaf area infected by powdery mildew of tested barley genotypes at all sites in 1998 and 1999.
1998 1999
Barley Known Seed
Austria DK/Sejet Germany Austria Finland Latvia Sweden
genotype resistance provided by
a
DK/Abed Finland Norway DK/Abed Germany Norway
Ivana
b mlo A. Fleck (AT) 75 94 100 27 50 73 71 50 3 50 28 30 25
Ohara ? A. Fleck (AT) 60 94 100 33 1 0 39 56 1 39 20 6 8
Prosa ? A. Fleck (AT) 25 100 100 29 15 15 24 69 3 38 25 11 6
P3645C ? A. Fleck (AT) 5 14 10 17 0 0 11 1 0 5 5 3 3
Cooper Mla1, MlLa O. Andersen (DK) 5 1 1 5 1 0 4 0 0 6 5 3 1
Optic Mla12, MlLa, O. Andersen (DK) 5 0 1 5 1 0 1 0 0 4 5 0 3
MlAb, Mlg
Inari none M. Jalli (FI) 5 63 38 4 1 0 0 10 1 7 10 4 5
Viivi none M. Jalli (FI) 50 81 100 34 5 0 19 8 0 26 8 3 5
Bor 88369 none M. Jalli (FI) 0 0 0 3 0 0 0 0 0 3 0 0 0
Bor 88377 none M. Jalli (FI) 0 0 5 20 0 0 0 0 0 2 8 0 2
Hanka ? F. Heinrics (DE) 5 3 8 19 1 0 9 1 1 4 10 5 5
Hadm.15262-96 ? F. Heinrics (DE) 5 25 1 4 0 0 0 0 0 2 1 0 1
Hadm.15458-96 ? F. Heinrics (DE) 0 26 3 43 0 0 0 0 0 3 7 5 0
Arve Mla9 H. Skinnes (N) 50 81 25 28 13 65 41 6 3 35 25 14 10
Thule Mla9 H. Skinnes (N) 60 100 100 24 25 60 89 75 3 48 18 25 25
Tyra none H. Skinnes (N) 25 88 88 29 8 10 46 44 1 38 18 3 3
Average 23 48 42 20 8 14 22 20 1 19 12 7 6
aAU Austria, DE Germany, DK Denmark, FI Finland, N Norway.
bIn Germany named Eunova.

M.S. Hovmøller et al.
740
in 1999 in Austria, Denmark, Finland and Sweden
clearly indicated that the level of infection was
much lower in the northern than in the central part
of Europe, and that the composition of the
pathogen population was very different (data not
shown). The main value of this type of multi-loca-
tion test is to get information about ‘stability’ of
resistance across different environments including
the effect of different pathogen populations.
Decisions on the type of the resistance (single- or
multi-gene) to investigate would require closer
studies of the infection process.
4. Conclusions and the way ahead
Besides an efficient dissemination of results, it
is currently important to focus on the detection of
virulence matching the new sources of resistance
being introduced into the barley germplasm.
Annual assessments of virulences already present
in high frequencies in most parts of Europe may be
less important in the future. As the mlo alleles are
so widely used in Europe, a survey for the potential
development of increased aggressiveness on Mlo-
resistant varieties should have high priority.
Continued exchange of ideas, methodology and
material (e.g. differential varieties representing
new sources of resistance) and rapid distribution of
results across national boundaries, as carried out
through COST817, is absolutely vital. It is also
important to make a link between the national sur-
vey programmes and multinational survey activi-
ties (e.g. [13, 30, 31]).
The use of survey data to draw conclusions
about general population genetic aspects of the
barley powdery mildew pathogen should proceed
with caution because many important evolutionary
forces are often not known [38, 51]. Selection due
to host resistance genes is one powerful force
which strongly influences the composition of the
population [4, 9, 21], but which may give rise to
patterns that easily can be misinterpreted, e.g.
gametic disequilibrium. Examples of how gametic
disequilibrium and subsequent hitch-hiking effects
may give rise to misleading interpretation of
changes in unnecessary virulence alleles and com-
plexity of pathotypes have been given elsewhere
[23]. Time of sampling, knowledge of likely source
varieties for the spores/isolates collected, the possi-
bilities and limitations given by the differential
varieties used, and the theoretical consequences
thereof, are other important aspects which should
be kept in mind before genetic conclusions are
drawn on the basis of survey data.
Acknowledgements: The authors are grateful for the
invaluable contributions made by all other COST817
members of the barley powdery mildew sub-group for
virulence surveys and the working group for partial
resistance: I. Araja, R. Bilinski, L. Bousset,
H.J. Czembor, J.D.S. Clarkson, K. Flath, J. Fuchs,
E. Gacek, G. Kosilovich, I. Kokina, E. Krippel,
M. Lyngkjær, L. Munk, H. Østergård, M. Rasmussen,
A. Ruddock, M. Sykora, R. Zederbauer, B. Schwatz.
All the participants wish to thank COST817 for support-
ing travel expenses that were necessary for meeting and
to carry out short-term scientific missions. These activi-
ties allowed people to interact and discuss scientific
matters across national borders, and altogether they con-
tributed to the success of the action. J. Fuchs and
E. Limpert are grateful for additional support from
COST Switzerland.
Appendix
Ole ANDERSEN: Sejet Plant Breeding Station,
8700 Horsens, Denmark
Gottfried BESENHOFER: Bundesamt und
Forschungszentrum fuer Landwirtschaft,
Spargelfeldstrasse 191, PO Box 400, 1226 Vienna,
Austria
Jerzy H. CZEMBOR: Plant Breeding and Acclimatization
Institute, IHAR, Department of Genetics and Plant
Breeding, 05-870 Blonie, Radzikow, Poland
Antonin DREISEITL: Agricultural Research Institute,
Havlickova 2787, PO Box 55, 76741 Kromeriz,
Czech Republic
Friedrich FELSENSTEIN: EpiGene GmbH Biotechnology
in Plant Protection, Hohenbachernstrasse 19–21,
85354 Freising, Germany
Andreas FLECK: Probstdorfer Saatzucht, Saatzuchtstrase 11,
2301 Gross Enzersdorf, Austria
Fritz HEINRICS: Saatzucht Hadmersleben, Kroppenstedter
Strasse, 39398 Hadmersleben, Germany
Rickard JONSSON: Cereal Breeding Dept., Svalöf Weibull
AB, 26881 Svalöv, Sweden

European co-ordination of barley powdery mildew studies 741
Eckhard LIMPERT: ETH Zentrum/LFW,
Phytomedizin/Pathologie, Universitätsstrasse 2,
8092 Zürich, Switzerland
Peter MERCER:
Plant Pathology Research Division, Dept.
Agriculture and Rural Development , Northern Ireland,
Newforge Lane, Belfast BT9 5PX, UK
Svetozar PLESNIK: Comenius University, Faculty of
Natural Sciences, Mlynska Dolina B-1,
84215 Bratislava, Slovakia
Isaak RASHAL: Institute of Biology of the University of
Latvia, Plant Genetics Laboratory, Salaspils, 2169,
Latvia
Helge SKINNES: Department of Horticulture and Crop
Sci., PO Box 5022, 1432 Aas, Norway
Susan SLATER: National Institute of Agricultural Botany,
Cambridge, CB3 OLE, UK
Olga VRONSKA: Ukrain. Acad. Agr. Sci., Institute of
Agriculture, Obroshino, Lviv Province, 292084,
Ukraine
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