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ORIGINAL ARTICLE
Virulence Structure of the Powdery Mildew (Blumeria graminis)Population Occurring on Triticale (x Triticosecale) in PolandHenryk J. Czembor, Olga Domeradzka, Jerzy H. Czembor and Dariusz R. Ma�nkowski
Plant Breeding and Acclimatization Institute – National Research Institute, Radzik�ow, Błonie 05-870, Poland
Keywords
powdery mildew, triticale, virulence structure
Correspondence
J. H. Czembor, Plant Breeding and
Acclimatization Institute, National Research
Institute, Radzik�ow, Poland.
E-mail: j.h.czembor@ihar.edu.pl
Received: May 18, 2013; accepted: December
8, 2013.
doi: 10.1111/jph.12225
Abstract
Powdery mildew, caused by Blumeria graminis is an important disease of
cereals in many production regions. Until end of the last century triticale
had been regarded as a species characterized by high level of resistance for
this disease. However, after several years of intensive production on a big
area in Poland, Germany and other European countries it start to be sus-
ceptible for many pathogens including B. graminis. Because of this, viru-
lence structure of this pathogen population on triticale in Poland was
evaluated across 2008–2010. Leaf samples with symptoms of the powdery
mildew disease were collected randomly from nineteen localities. As a
total, 1402 B. graminis isolates were collected: 23–25 isolates per locality
in each year. Standard differential set of 28 genotypes was used: twenty-
one wheat with known resistance genes and seven triticale. Based on the
obtained results it was possible to observe significant differences in viru-
lence structure between years and localities. No virulence’s against Pm21
(Yangmai5), and Pm3d + 4b (Kadett) were found in any year. All tested
isolates were virulent on Moreno and Lamberto cultivars. In a total, 36%
of tested isolates possessed 9, 11 or 12 virulence’s per genotypes. Twenty
five percent of tested isolates were virulent to 5 triticale cultivars. Correla-
tion between pathotypes frequency and sampling region were not found
what suggest that local epidemics play the most important role in triticale
growing regions in Poland.
Introduction
Blumeria graminis is an obligate biotrophic pathogen
which causes powdery mildew on cereals. It depends
on living plant tissue for survival and reproduction. It
is visible as creamy white pustules of mycelium and
conidia, subsequently punctuated by black fruiting
bodies producing sexual spores, which may survive
the winter on cereal debris (Braun et al. 2000; Troch
et al. 2012). The colonization of a plant is the result of
highly specific recognition mechanisms in the gene-
for-gene response involving avirulence and resistance
genes (Flor 1956, 1971). This mutual connection can
result in co-evolution of host and pathogen. Only one
mutation may cause a pathogen to become virulent to
a new host. Based on this, B. graminis has evolved eight
distinct formae speciales (f. sp.) which display strict host
specialization (Mains 1934; Hardison 1944; Moseman
et al. 1965; Oku et al. 1985; Tosa 1989; Czembor et al.
2010, 2011, 2012): perennial grasses Dactylis spp., Agro-
pyron spp, Poa spp. or Bromus spp. and cereals such as
wheat, barley, rye, which are closely related to Bromus
spp., and oat (Hardison 1944). However, all studies
state that the divergence of the different formae speciales
is likely to be younger than the divergence of their
hosts. This co-evolution type is also known as host-
tracking in contrast to cospeciation, where the host
and pathogen diverged simultaneously (Stukenbrock
and McDonald 2008). Eshed and Wahl (1970) noted,
that the host infection ability of B. graminis f. sp. is not
limited to a single species. Though, a wide range of
powderymildew pathogenicity has been observed, dis-
tinct formae speciales rarely infect species other than the
natural host (Tursumbaev 1974; Ellis 2006). If plants
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH 499
J Phytopathol
are infected by inappropriate formae speciales, attacked
cells die during penetration or very shortly after the
formation of visible haustoria (Olsen et al. 2003). In
last decade several studies tried to tackle the co-evolu-
tionary relationship of the different powdery mildew f.
sp. with their hosts (Wyand and Brown 2003; Inuma
et al. 2007; Walker et al. 2011). Recent research con-
clude that the center of diversity of B. graminis overlap
with the center of origin of their hosts in the Middle
East (Wyand and Brown 2003). The closely related
B. graminis special forms are B. graminis f. sp. tritici and
B. graminis f. sp. secalis (Tosa et al. 1990).
Triticale (x Triticosecale Wittmack) is the intergeneric
hybrid to associate the tolerance for biotic and abiotic
stresses of rye (Secale cereale) with the productivity and
nutritional qualities of wheat (Ammar et al. 2004;
Oettler 2005). This artificial cereal in contrast to wheat
and rye of very recent originwas commercialized at the
end of 1980’s (Oettler 2005). During the last decade
triticale became considerable important in Europe. Its
production area has almost doubled since 2000 up to
almost 3.3 million ha in 2011 (FAOStat 2011). Nowa-
days this hybrid is the thirdmost important small-grain
in Poland (1.26 million ha, FAOStat 2011). Until end
of the last century triticale had been regarded as a spe-
cies characterized by high level of resistance for all dis-
eases. However, in the last decade this resistance was
broken, and based on the observations conducted in
several European countries, including France, Poland,
Germany and Belgium, susceptibility of triticale to
powdery mildew is still increasing (Wakuli�nski et al.
2005, 2007; Walker et al. 2011). Blumeria graminis f.
sp. tritici causes powdery mildew of wheat (Triticum
aestivum) and B. graminis f. sp. secalis powdery mildew
of rye. Both of them, cause significant yield losses in
many regions of the world. In wheat 41 resistance
genes (Pm1 to Pm46) with more than 60 powdery mil-
dew resistant alleles and in rye 8 Pm genes were
described and it is probable, that Pm genes in triticale
are inherited from both parents (Woolhouse et al.
2005; Walker et al. 2011). Recent research demon-
strated that powdery mildew on triticale has emerged
most probably through a host range expansion of
wheat powdery mildew. It means that powdery mil-
dew has evolved capacity to infect triticale, a new host
species, which is phylogenetically closely related to its
present host wheat (Walker et al. 2011).
Identificationof race-specific resistanceofB. graminis
on triticale play an important role in breeding programs
that are an effective strategy to control this pathogen
(Lillemo et al. 2010). The overall objective of this study
was to characterize virulence structure of the powdery
mildew population on the triticale in different regions
of Poland across 2008–2010. The specific objectives
were: (i) monitoring changes in virulence frequency in
different localities over the years (ii) to compare viru-
lence frequencies and complexity of B. graminis occur-
ring on triticale on wheat differential set with known
resistance genes (iii) to characterize virulence frequen-
cies and complexityon triticale differential set.
Materials and Methods
Isolate sampling
Leaf samples with symptoms of the powdery mildew
disease were collected from winter Hortenso commer-
cial cultivar from nineteen localities, across 2008–2010 (Fig. 1). Localities represent randomly all
regions of Poland: Wr�ocikowo, Dezbina, Masłowice,
Kar _zniczka; Ko�nczewice, Głodowo, Strzelce, Rad-
zik�ow, Szelejewo, Smolice, Seroczyn, Uhnin, Małys-
zyn, Kochcice, Masłowice, Bazk�ow, Przecław (Fig. 1).
Isolation of single pustule Blumeria graminis cultures
For isolation B. graminis single pustule cultures of iso-
lates collected leaf samples were dried in paper bags at
23°C and to stimulate ascospores production they
were stored at 4°C for 8 weeks. After this, leaf samples
with B. graminis ascospores were placed on moist lig-
nin in the lid of petri plate, separately from each loca-
tion and over 3–4 days petri plates were kept upside
down at the height of 20 cm under 10 days old seed-
lings of the very susceptible Lamberto cultivar grow-
ing in a 20–22°C growth chamber with 16-h of light
(10 lE/m2). After 7 days, symptoms of the powdery
mildew were appeared. Fragments of the second fully
developed leaf with single pustule cultures were
placed on Petri dishes with water agar medium (12 g
per agar per l) amended with benzimidazole (30 mg
per l). Every year, from each location, 40 isolates were
collected and 23–25 of them were used for future
investigations. Individual colonies were subcultured
using dissecting needle to transfer conidia to 10 days
old seedlings of Lamberto cultivar. After this, they
were propagated in isolation from each other on Lam-
berto cultivar by uniformly dispersing conidia. As a
total, 1402 B. graminis isolates were collected and rep-
resent the powdery mildew population occurring on
triticale in Poland across 2008–2010.
Virulence structure of Blumeria graminis
To characterize virulence structure of powdery mil-
dew population occurring on triticale in Poland
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Powdery mildew population occurring on triticale in Poland H. J. Czembor et al.
twenty-one wheat and seven triticale differentials
were used (Tables 1, 2). Differential set of wheat culti-
vars and one Pm 6 line possess known powdery mil-
dew resistance genes (Pm), which are commonly used
in European breeding programmes. Triticale differen-
tial set combine highly or moderate resistant geno-
types (Banjo, Beagle, Rhino, Grenado and Borwo)
and highly susceptible (Lamberto and Moreno)
(Anonymus 2007a,b). In average, 10 seedlings of the
differential set genotypes and susceptible cultivar
Lamberto grown separately in a small plastic transpar-
ent box in a growing chamber during 8–10 days at
20–22°C with 16-h of light.
Leaf fragments of each differential with length 2.5–3.0 cm were cut and placed on 12-well plates with
benzimidazole agar medium (12 g per agar per l;
30 mg per l benzimidazole) in one replication. The
inoculation was performed by uniformly dispersing
conidia of each subcultured on Lamberto cultivar
seedling isolate separately. Next, plates were put in
the growing chamber at 17–19°C with alternating
photoperiod 16-h of light. After 8–10 days of incuba-
tion the disease reaction types were scored according
to 0–4 modified scale (Mains 1934). If the disease
symptoms after inoculation on the differentials leaf
fragments were scored for 0, 1 or 2 (0 = immune, no
visible symptoms but may include slight chlorotic
flecking; 1 = highly resistant, fungal development
limited, brown necrotic spotting, any visible myce-
lium, no sporulation, necrosis; 2 = moderately resis-
tant, moderate mycelium with some sporulation, well
developed necrotic lesions, some chlorosis may be vis-
ible) such isolate was classified as avirulent to known
specific resistance genes which possessed wheat geno-
types or to unknown genes from triticale genotypes. If
the disease symptoms were scored for 3 or 4
(3 = moderately susceptible, extensive mycelium,
more sporulation, mycelium extends beyond necrotic
area, chlorosis visible around colonies; 4 = highly sus-
ceptible, large colonies, abundant sporulation, no
apparent necrosis and slight, if any, chlorosis) such
isolate was classified as virulent to known specific
resistance genes of wheat or to unknown genes from
triticale genotypes.
Statistical analysis
Analysis of variance was conducted in split-split-plot
fixed design. Experiment factors were: year (plot),
location (sub plot), powdery mildew isolate and geno-
type from differential set (sub-sub plots) (Cochran
and Cox 1992; Box et al. 2005; Montgomery 2005). It
was done using SAS� 9.2 System (SAS Institute Inc.
2009) at probability level 0.05.
II
III
IV
I
Fig. 1 Origins of 1402 Polish Blumeria graminis isolates sampled from triticale during 2008–2010, bi-plot of principal components based on the
virulence frequency of isolates on 21 wheat and 7 triticale differentials and their homogeneous groups.
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH 501
H. J. Czembor et al. Powdery mildew population occurring on triticale in Poland
Parameters of population: virulence frequency,
complexity, diversity, Gilmour codes, abundance and
evenness were calculated using HaGis Tool (Hermann
et al. 1999). The total number of virulent reaction
types for each isolate was reported as a virulence fre-
quency. Virulence complexity signifies the sum on
their virulence to resistance genes in 21 wheat differ-
entials or 7 triticale differentials. Triticale differential
set was divided into three triplets and wheat differen-
tial set was divided into seven triplets. Each of the
three or seven digit indicates virulence or avirulence
of the isolate on the three differentials in a triplet
(Gilmour 1973). The resulting number defines the
virulences of the isolates and their classification as
pathotypes. Abundance signifies the frequency of the
predominant pathotype (%). The evenness corre-
sponding to the variation in frequency of individual
pathotypes – more pathotypes results in higher even-
ness. Principal components analysis (PCA) was made
based on correlation matrix. Cluster analysis was
based on Euclidean distance following the clustering
method of Ward (1963). They were conducted using
virulence frequency of B. graminis isolates collected
from triticale in nineteen localities in Poland during
3 years on 21 wheat differentials and 7 triticale differ-
entials. PCA and cluster analysis were carried out with
InfoStat 1.6.
Results
Virulence structure of B. graminis population on trit-
icale in Poland was evaluated on wheat and triticale
standard differential sets (Tables 1, 2). Wheat
differential set possess commonly known powdery
mildew resistance genes. Triticale differential set
combine highly resistant and highly susceptible
Line/cultivar
Resistance
gene
Chromosome
location
Source of resistance
gene References
Axminster Pm1a 7AL Triticum aestivum Sears and Briggle (1969)
Avalon Pm2 5DS Aegilops tauschii McIntosh and Baker
(1970)
Asosan Pm3a 1AS T. aestivum Briggle and Sears (1966)
Chul Pm3b 1AS T. aestivum Briggle (1969)
Sonora Pm3c 1AS T. aestivum Briggle (1969)
Kolibri Pm3d 1AS T. aestivum Zeller et al. (1993)
Weihenstephan Pm4b 2AL Triticum carthlicum The et al. (1979)
Kormoran Pm5d 7BL T. aestivum Hsam and Zeller (2001)
Pm 6 Pm6 2B Triticum timopheevii Jorgensen and Jensen
(1973)
Transec Pm7 4BS/4BL-2RL Secale cereale Friebe et al. (1996)
Disponent Pm8 1BL/1RS S. cereale Hsam and Zeller (1997)
Maris Huntsman Pm2 + 6 Bennett (1984)
Kadett Pm3d + 4b Bengtsson et al. (1991)
Boxer Pm4b + 5 Wolfe and Barrett (1979)
Sorbas Pm4b + 6 Wolfe and Barrett (1979)
Kronjuvel Pm4b + 8 Heun and Fischbeck
(1987)
Granada Pm5 + 8 Wolfe and Barrett (1979)
Apollo Pm2 + 4b+8 Wolfe and Barrett (1979)
Sappo Pm1 + 2 +
4b + 9
Heun and Fischbeck
(1987)
Amigo Pm17 1AL/1RS Secale cereale Heun et al. (1990)
Yangmai5 Pm21 6VS/6AL Haynaldia villosa Chen et al. (1995)
Table 1 Standard differential set of wheat
with known powdery mildew resistance genes
used to characterize virulence structure of the
Blumeria graminis population on triticale in
Poland across 2008–2010
Table 2 Triticale cultivars used to characterize virulence structure
of the Blumeria graminis population on triticale in Poland across
2008–2010
Cultivar Pedigree Origin
Banjo Merino’s 9 Julanillo B2736 Mexico
Beagle University of Manitoba UM’S 9 TCL BULK Mexico
Borwo MAH 15841-13 9 LAD 794 Poland
Grenado (LA 85/90 9 Presto) 9 Chrono Poland
Lamberto (CT 929/84 9 Moniko) 9 Presto Poland
Moreno n. d. Poland
Rhino Grizzly 9 (Aifong 3 9 Dove) Mexico
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Powdery mildew population occurring on triticale in Poland H. J. Czembor et al.
genotypes with potential race-specific resistance for
powdery mildew. Leaf samples used for isolation
the B. graminis single pustule cultures were collected
from winter Hortenso commercial cultivar from
nineteen locations across 2008–2010. Differences for
virulence frequency between genotypes, years and
localities were significant (Table 3). Main variation
was caused by genotypes included into differential
sets and years. Variation between localities has also
important effect on the structure of the powdery
mildew population occurring on the triticale in
Poland. No correlation for virulence frequency in
each localities between years were observed
(Fig. 1). Based on the cluster analysis some homog-
enous groups of localities were observed. However,
localities with similar frequency of virulent isolates
were located in different parts of the country. In
2008 in one locality, Smolice (Central-West
Poland), powdery mildew was not observed and in
Seroczyn (Central-East Poland), Strzelce (Central
Poland) and Małyszyn (Central-West Poland) viru-
lence frequency was low (cluster I). In the next
years, virulence frequencies in these localities
increased to 70% or higher. Cluster II combine
localities for which virulence frequency in 2009 was
lower than in 2008 and in 2010: Ko�nczewice, Rad-
zik�ow (Central Poland), Grodkowice, Bazk�ow (South
Poland), Kar _zniczka (North Poland). In 2010 in
Szelejewo, Wr�ocikowo and Głodowo (cluster III)
virulence frequencies were lower than in 2009 or
2008.
Virulence frequencies of 1402 isolates collected
from triticale in 19 localities during 2008–2010 on 21
wheat differentials are presented in the Table 4. No
virulences against Pm21 (Yangmai5), and Pm3d + 4b
(Kadett) were found in any year. Virulence frequency
against gene combination Pm1 + 2 + 4b + 9 (Sappo)
and gene Pm4b (Weihenstephan) was low. In con-
trast, the frequencies of virulences against genes Pm2,
Pm3c, Pm5, Pm6, Pm7, Pm17 and combinations of
genes Pm2 + 6, Pm5 + 8 was high or very high.
Figure 2 demonstrate relationships between localities
and virulence frequency during 2008–2010 against
genes present only in wheat differential set. Localities
Ko�nczewice, Strzelce (Central Poland) and Przecław
(South-East Poland) had the highest frequency of
isolates with virulence alleles Pm1, Pm3a, Pm3b, Pm3c,
Pm3d or combination Pm1 + 2+4b + 9.Isolates
collected in Wr�ocikowo (North Poland), Radzik�ow
(Central Poland), Smolice, Szelejewo, Smolice
(Central-West Poland) and Kochcice (South-West
Poland) most frequently possess Pm5, Pm6, Pm7 and
Pm8 virulence alleles or virulence alleles combina-
tions Pm2 + 4b,+8, Pm4b + 5, Pm4b + 6, Pm4b + 8,
Pm4b + 6 and Pm2 + 6. Virulence frequencies only on
7 triticale differentials are presented in the Table 5
and the relationship between localities and virulence
frequency on the Fig. 3. All tested isolates were viru-
lent on Moreno and Lamberto cultivars, and virulence
Table 3 Analysis of variance for virulence frequency of the Blumeria
graminis population on triticale in Poland across 2008–2010 on
standard differential sets
Source of
variation d.f.
Sum of
squares
Mean
square F-value P-value
Year 2 1516.84 758.42 389.69 <0.0001
Locality 18 1440.47 80.02 41.12 <0.0001
Error I 36 1579.89 43.88
Isolate 24 161.31 6.72 3.45 <0.0001
Error II 432 1826.73 4.22
Cultivar 27 57551.98 2131.55 1095.22 <0.0001
Year 9 Isolate 54 3572.25 66.15 33.99 <0.0001
Locality
9 Isolate
486 4873.39 10.02 5.15 <0.0001
Year 9 Locality
9 Isolate
972 7916.74 8.14 4.18 <0.0001
Error III 37 204 72407.65 1.94
Total 39 255 153029.72
Table 4 Virulence frequencies of 1402 Polish isolates of Blumeria gra-
minis sampled from triticale in 2008–2010 on 21 wheat differentials
Cultivar Gene or allele
Virulence frequency (%)
2008 2009 2010
Axminster Pm1a 36 53 61
Avalon Pm2 94 68 81
Asosan Pm3a 22 53 59
Chul Pm3b 8 34 47
Sonora Pm3c 68 84 87
Kolibri Pm3d 17 53 45
Weihenstephan Pm4b 10 12 12
Kormoran Pm5d 95 83 92
Pm6 Pm6 92 93 96
Transec Pm7 82 76 82
Disponent Pm8 39 30 21
Maris Huntsman Pm2 + 6 84 79 90
Kadett Pm3d + 4b 0 0 0
Boxer Pm4b + 5 36 40 50
Sorbas Pm4b + 6 51 57 46
Kronjuwel Pm4b + 8 39 46 52
Granada Pm5 + 8 93 96 98
Apollo Pm2 + 4b + 8 32 25 37
Sappo Pm1 + 2 + 4b + 9 7 26 15
Amigo Pm17 54 87 92
Yangmai5 Pm21 0 0 0
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H. J. Czembor et al. Powdery mildew population occurring on triticale in Poland
frequency on Beagle and Rhino cultivars was high.
Frequency of isolates virulent to the Grenado triticale
cultivar was low in 2008 and 2010 (10% and 28%,
respectively) and 38% in 2009. The highest frequency
of isolates with virulence alleles to this cultivar was
collected in Uhnin (Central-East Poland). In Kar _znic-
zka (North Poland) a very low number of isolates
were virulent to all triticale differentials. However iso-
lates collected in Dezbina with high frequency possess
virulence against Borwo, Beagle and Banjo cultivars.
In Central-West part of Poland (Smolice, Małyszyn,
Borowo) and in Grodkowice or Dukla (South-East
Poland) frequency of isolates virulent to Borwo, Bea-
gle, Banjo or Rhino cultivars was lower than in the
other areas.
Figure 4 shows the distribution of virulence com-
plexity of the isolates collected in 19 localities from trit-
icale across 2008–2010 on 21 wheat differentials and
Fig. 5 on 7 triticale differentials. For both sets normal
distribution is observed. On the wheat differentials the
complexity of all tested isolates varied from 2 to 18 vir-
ulences per genotype. In 2009 the complexity of testes
isolates was much higher than in 2008 and 2010. Dur-
ing all years more than 10% of tested isolates possessed
9, 11 or 12 virulences per genotype (30% in a total). In
2009 about 30% of tested isolates possessed 13–17 vir-
ulences per genotype. On 7 triticale differentials the
complexity of all tested isolates varied from 1 to 7 viru-
lences per genotype. In 2009 and 2010 the complexity
was higher than in 2008. In both years about 30% of
all tested isolates were virulent to 5 and about 25% of
themwere virulent to 6 triticale cultivars.
Out of the 1402 isolates collected from triticale in
19 localities (456 in 2008, 472 in 2009 and 474 in
2010) and tested on 7 triticale differential cultivars,
there were 28 pathotypes in 2008, 32 in 2009–2010(Table 6). Pathotype diversity on 7 triticale differen-
tials was low, because all isolates were virulent to 2
cultivars. Evenness ranged from 0.80 to 0.89. In 2008
the most abundant pathotypes were 060, 260, 261
and 361 (56.4% in a total) (Table 7). 2009 was domi-
nated by the pathotypes 361, 761, 371, 461, 771, 261,
661 (55.1% in a total). In 2010 the most frequent
pathotypes were 761, 771, 361, 760, 661 and 261
(54.4% in a total). On 21 wheat differentials
–5.00 –2.50 0.00 2.50 5.00
PC 1(27.9)%)
–5.00
–2.50
0.00
2.50
5.00PC
2(1
8.5)
%)
Bąków
Borowo
Dębina
Dukla
Głodowo
GrodkowiceKarżniczka
Kochcice
Kończewice
Małyszyn
Masłowice
Przecław
Radzików
Seroczyn
Smolice
Strzelce
Szelejewo
Uhnin
Wrócikowo
Pm1
Pm2
Pm3a
Pm3b
Pm3c Pm3d
Pm4b
Pm5
Pm6
Pm7
Pm8
Pm2+6
Pm3d+4d
Pm4b+5
Pm4b+6Pm4b+8
Pm5+8
Pm2+4b+8
Pm1+2+4b+9
Pm17
Pm21
Fig. 2 Bi-plot of principal components com-
puted based on the virulence frequency of
1402 Polish Blumeria graminis isolates
collected from triticale in 19 localities during
2008–2010 and tested on 21 wheat differen-
tials.
Table 5 Virulence frequencies of 1402 Polis isolates of Blumeria gra-
minis sampled from triticale in 2008–2010 on 7 triticale differentials
Cultivar
Virulence frequency (%)
2008 2009 2010
Banjo 33 51 67
Beagle 56 67 75
Borwo 17 49 62
Grenado 10 38 28
Lamberto 100 100 100
Moreno 100 100 100
Rhino 47 80 70
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Powdery mildew population occurring on triticale in Poland H. J. Czembor et al.
–4.00 –1.75 0.50 2.75 5.00PC 1(38.8)%)
–4.00
–2.00
0.00
2.00
4.00
PC 2
(26.
1)%
)
BąkówBorowo
Dębina
Dukla
GłodowoGrodkowice
Karżniczka
KochciceKończewice
Małyszyn
Masłowice
Przecław
Radzików
SeroczynSmolice
StrzelceSzelejewo
Uhnin
Wrócikowo
BanjoBeagle
Borwo
Grenado
Lamberto
Moreno
Rhino
Fig. 3 Bi-plot of principal components com-
puted based on the virulence frequency
of 1402 Polish Blumeria graminis isolates
collected from triticale in 19 localities dur-
ing 2008–2010 and tested on 7 triticale
differentials.
0
4
8
12
16
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Porti
on o
f iso
late
s (%
)
Complexities
2008
2009
2010
Fig. 4 Virulence complexity of 1402 Polish Blumeria graminis isolates collected from triticale during the years 2008–2010 and tested on 21 wheat
differentials differentials.
0
5
10
15
20
25
30
35
40
0 1 2 3 4 5 6 7
Porti
on o
f iso
late
s (%
)
Complexities
200820092010
Fig. 5 Virulence complexity of 1402 Polish
Blumeria graminis isolates collected from triti-
cale during the years 2008–2010 and tested
on 7 triticale differentials.
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H. J. Czembor et al. Powdery mildew population occurring on triticale in Poland
pathotype diversity was very high: 325 pathotypes
were found in 2008, 423 in 2009 and 403 in 2010.
Number of pathotypes with count higher than 1 ran-
ged from 33 (2009) to 63 (2009) and the abundance
ranging from 17.37% to 42.50%, respectively
(Tables 8, 9, 10).
Parameter
Wheat differentials Triticale differentials
2008 2009 2010 2008 2009 2010
No of isolates 456 472 474 456 472 474
No of diff. pathotypes 325 423 403 28 32 32
No of ptathotypes
with count >1
63 33 42 25 30 30
Abundance (%) 42.50 17.37 23.84 99.34 99.58 99.16
Evenness (Shannon) 0.97 0.99 0.98 0.80 0.89 0.85
Diversity: Simple 0.71 0.90 0.85 0.06 0.07 0.07
Diversity: Gleason 52.92 68.54 65.25 4.41 5.03 5.36
Diversity: Shannon 5.60 5.99 5.90 2.65 3.10 2.99
Table 6 Response of 1402 Polish isolates of
Blumeria graminis sampled in 19 localities
from triticale during 2008–2010 on 21 wheat
and on 7 triticale differentials
Table 7 Virulence spectra of 32 pathotypes of Blumeria graminis collected form triticale in 19 localities and investigated during 2008–2010 on 7 triti-
cale differentials and their frequencies
Pathotype Banjo Beagle Borwo Grenado Lamberto Moreno Rhino
Frequency (%)
2008 2009 2010
60 + + 19.08 2.33 2.74
61 + + + 7.02 4.87 3.16
70 (2)a + + + 0.44 0.64 0.00
71 + + + + 0.44 2.97 0.00
160 + + (2) 2.19 1.06 1.27
161 + + + 2.41 1.48 2.32
170 + + + + (2) 0.00 0.00 0.42
171 + (2) + + + + 0.88 1.06 1.05
260 + + + (2) 14.47 1.91 2.11
261 + + + + 10.75 6.78 4.43
270 + + + + (2) 1.10 1.27 0.42
271 + + + + + 0.88 4.03 1.48
360 + + + + (2) 4.82 1.27 4.43
361 + + + + + 12.06 11.44 9.49
370 + + + + + 1.54 1.27 0.42
371 + + + + + + 3.73 8.05 4.01
460 + + + (2) 5.48 1.91 2.32
461 + + + + 2.63 7.63 3.59
470 + + + + (2) 0.00 1.06 0.63
471 + + + + + 0.44 2.12 0.63
560 + + + + (2) 0.66 0.42 1.27
561 + + + + + 0.00 2.33 2.95
570 + + + + + (2) 0.00 0.00 0.63
571 + + + + + + 0.44 2.33 0.84
660 + + + + (2) 0.88 1.27 2.95
661 + + + + + 2.85 5.30 5.06
670 + + + + + (2) 0.00 1.06 1.05
671 + + + + + + 0.00 3.81 1.69
760 + + + + + (2) 1.97 2.75 6.54
761 + + + + + + 1.75 8.90 17.09
770 + + + + + + (2) 0.00 1.27 2.32
771 + + + + + + + 0.44 6.99 11.81
a- 2 = moderately resistant, moderate mycelium with some sporulation, well developed necrotic lesions, some chlorosis may be visible.
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH506
Powdery mildew population occurring on triticale in Poland H. J. Czembor et al.
Table
8Virulence
spectra
ofthemost
frequentPolishpathotypesofBlumeriagraminisco
llectedform
triticalein
19localitiesin2008on21wheatdifferentialsandtheirfrequencies
Pathotype
Pm
1a
Pm
2
Pm
3a
Pm
3b
Pm
3c
Pm
3d
Pm
4b
Pm
5d
Pm
6Pm
7Pm
8
Pm
2+6
Pm
3d+4b
Pm
4b+5
Pm
4b+6
Pm
4b+8
Pm
5+8
Pm
2+4b+8
Pm
1+2
+4b+9
Pm
17
Pm
21
Frequency
(%)
2265022
++
++
++
++
1.97
2265020
++
++
++
+1.75
2060020
++
++
1.54
2065020
++
++
++
1.32
2067672
++
++
++
++
++
++
1.32
3067672
++
++
++
++
++
++
+1.32
3267672
++
++
++
++
++
++
++
1.32
2065630
++
++
++
++
+1.10
2665022
++
++
++
++
+1.10
7265020
++
++
++
++
+1.10
2065672
++
++
++
++
++
+0.88
2265420
++
++
++
++
0.88
3065020
++
++
++
+0.88
2064020
++
++
+0.66
2065420
++
++
++
+0.66
2065430
++
++
++
++
0.66
2067620
++
++
++
++
+0.66
2067670
++
++
++
++
++
+0.66
2260020
++
++
+0.66
2264020
++
++
++
0.66
2265000
++
++
++
0.66
2265422
++
++
++
++
+0.66
2267622
++
++
++
++
++
+0.66
2267632
++
++
++
++
++
++
0.66
2267670
++
++
++
++
++
++
0.66
3265020
++
++
++
++
0.66
3277670
++
++
++
++
++
++
++
0.66
3665022
++
++
++
++
++
0.66
6265022
++
++
++
++
++
0.66
6665022
++
++
++
++
++
0.66
7665022
++
++
++
++
++
+0.66
7765022
++
++
++
++
++
++
0.66
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH 507
H. J. Czembor et al. Powdery mildew population occurring on triticale in Poland
Table
9Virulence
spectra
ofthemost
frequentPolishpathotypesofBlumeriagraminisco
llectedform
triticalein
19localitiesin
2009on21wheatdifferentialsandtheirfrequencies
Pathotype
Pm
1a
Pm
2
Pm
3a
Pm
3b
Pm
3c
Pm
3d
Pm
4b
Pm
5d
Pm
6Pm
7Pm
8
Pm
2+6
Pm
3d+4b
Pm
4b+5
Pm
4b+6
Pm
4b+8
Pm
5+8
Pm
2+
4b+8
Pm
1+
2+4b+9
Pm
17
Pm
21
Frequency
(%)
2265022
++
++
++
++
1.06
65022
++
++
++
++
+0.85
265022
++
++
++
++
0.85
3265022
++
++
++
++
+0.85
67432
++
++
+2
++
++
0.64
1065022
++
++
++
+0.64
2765672
++
++
++
++
++
++
++
0.64
3065022
++
++
++
++
0.64
4665022
++
++
++
++
+0.64
4667432
++
++
++
++
++
++
0.64
7765672
++
++
++
++
++
++
++
++
0.64
Table
10Virulence
spectra
ofthemost
frequentPolishpathotypesofBlumeriagraminisco
llectedform
triticalein
19localitiesin2009on21wheatdifferentialsandtheirfrequencies
Pathotype
Pm
1a
Pm2
Pm
3a
Pm
3b
Pm
3c
Pm
3d
Pm
4b
Pm5d
Pm6
Pm7
Pm8
Pm
2+6
Pm
3d+4b
Pm
4b+5
Pm
4b+6
Pm
4b+8
Pm
5+8
Pm
2+
4b+8
Pm
1+2
+4b+9
Pm
17
Pm
21
Frequency
(%)
3265022
++
++
++
++
+1.90
6665022
++
++
++
++
++
1.27
65022
++
++
++
++
+1.05
7365022
++
++
++
++
++
+1.05
7365672
++
++
++
++
++
++
++
+1.05
7765232
++
++
++
++
++
++
++
0.84
7765672
++
++
++
++
++
++
++
++
0.84
2265422
++
++
++
++
+0.63
3264022
++
++
++
++
0.63
7665022
++
++
++
++
++
+0.63
7765022
++
++
++
++
++
++
0.63
7765272
++
++
++
++
++
++
++
+0.63
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH508
Powdery mildew population occurring on triticale in Poland H. J. Czembor et al.
Discussion
In a short time triticale like wheat and rye has become
one of the most important cereal in Poland. Based on
high yield potential and high nutritive value this crop
has become competitive with other cereals, mainly
rye. Until 2005 triticale was resistant to most airborne
pathogens that are economically important diseases
causing significant losses in yield and reduce grain
quality. Therefore, in breeding programs the degree of
resistance to diseases was not taken into account.
However, the acreage of triticale increased signifi-
cantly over the years and the immune mechanism
was broken. At the moment the degree of resistance
of new varieties to diseases, including powdery mil-
dew, is one of the basic criteria for providing for their
sustainability for modern ecologically friendly agricul-
ture (Wakuli�nski et al. 2007).
Recent research has provided a compelling amount
of evidence that powdery mildew on triticale has
emerged most probably through a host range expan-
sion of powdery mildew on wheat (Walker et al.
2011). A characteristic of the interaction between
the pathogen and the host is based on epidemiologi-
cal studies aimed at understanding the structure of
the pathogen population and the study of mecha-
nisms of resistance. As the authors point out, pow-
dery mildew is characterized by a high frequency of
virulence genes (Menzies et al. 1989; Imani et al.
2002; Inuma et al. 2007; Wakuli�nski et al. 2007).
This study represents a successful attempt of viru-
lence profile data from pathogenicity. The host
expansion is known as the evolution of the ability to
exploit a novel host in addition to the host of origin
(Giraud et al. 2010). The pathogenicity tests show
that powdery mildew isolates collected from triticale
are highly pathogenic on most of tested triticale cul-
tivars. All observed virulence profiles identified on
the triticale cultivars were highly aggressive. In this
study only triticale variety Grenado was character-
ized by a lack of virulence reaction to powdery mil-
dew isolates collected from triticale. Tested isolates
were able also to infect several wheat varieties with
known Pm genes. In present study only two varieties
from differential set, Yangmai 5 and Kadett, with
corresponding Pm resistance genes, respectively
Pm21 and Pm3d + 4b were characterized by a lack of
virulence in relation to powdery mildew isolates
obtained from triticale. Obtained results suggest that
the disease resistance in triticale has been based on
major genes which follow the gene-for-gene hypoth-
esis. Pathogenicity tests show that isolates collected
from wheat and rye were occasionally able to infect
triticale and underscores the close relatedness of this
intergeneric hybrid with its parents wheat and rye
(Linde-Laursen 1977; Walker et al. 2011). Troch
et al. (2012) came to similar conclusions. In the cited
studies the researchers examined 70 B. graminis f. sp.
tritici isolates on the wheat lines with known Pm
resistance genes, but only 40 isolates were patho-
genic on triticale.
Recent research suggests that the disease resistance
in triticale has probably been overcome by a few mod-
ifications in effector repertoire of B. graminis f. sp.
tritici to adapt to triticale genotypes. The fact that it
has taken decades for the resistance of triticale to be
overcome is probably because the total acreage of trit-
icale was rather small compared to wheat and rye for
many years. A similar breakdown of disease resistance
was found for Magnaporthe oryzae f. sp. oryzae, which
emerged from a host range expansion from Setaria
millet. It has been possibly brought by the loss of
strain-specific effector gene, which allows fungus to
colonize rice (Schulze-Lefert and Panstruga 2011).
Other examples of host range expansion of pathogens
to triticale are the spreading the rice blast to wheat
and triticale in Brasil and spreading of scald of rye to
triticale (Zaffarano et al. 2008). In other recent
research 59 varieties of winter triticale, 13 varieties of
spring triticale and 14 varieties of rye were inoculated
with 45 B. graminis isolates collected from wheat, rye
and triticale with different virulences. Powdery mil-
dew isolates originating from wheat and rye showed
lower pathogenicity on triticale cultivars than isolates
originating from triticale. Among 72 tested triticale
cultivars, 53 showed resistance to inoculation with
B. graminis f. sp. secalis and 62 showed resistance to
inoculation with B. graminis f. sp. tritici. Authors
pointed out that triticale varieties grown in Poland
were very susceptible to powdery mildew population
only cultivar Grenado showed resistance reaction
(Czembor et al. 2013).
Troch et al. (2012) tested 70 isolates on wheat lines
with known powdery mildew resistance genes and
identified 63 virulence profiles.. However, among 40
isolates pathogenic on triticale, only 14 displayed
unique virulence profiles on the triticale cultivars. In
this study 1402 powdery mildew isolates were col-
lected from triticale and tested on 21 wheat differen-
tial cultivars with known PM resistance genes as well
as on 7 triticale varieties. For the identification of
proper virulence profiles it is necessary to create a trit-
icale differential set. The virulence frequency occur-
ring in the population of powdery mildew on triticale
should be tested on triticale differentials to determine
J Phytopathol 162 (2014) 499–512 � 2014 Blackwell Verlag GmbH 509
H. J. Czembor et al. Powdery mildew population occurring on triticale in Poland
the effectiveness of major resistance genes in triticale.
The effects of known resistance genes from wheat and
rye could not be predicted in proper way when incor-
porated in triticale. Therefore, it is now enormously
important to create a separate differentials of triticale
varieties for analyzing the virulence structure of
B. graminis population occurring on triticale. The 7
initial triticale differential cultivars show strong devi-
ating virulence combination and complexities and can
be used to characterize isolates and to test effective-
ness of race-specific resistance genes in commercial
used cultivars. Additionally, other cultivars with
race-specific resistances should be added for future
analysis.
In this study powdery mildew isolates were col-
lected in 19 locations across Poland to validate the
hypothesis that triticale powdery mildew population
is structured geographically. Early research of Eshed
and Wahl (1970) assumed that isolates collected from
Israel have a wider host range that elsewhere in the
world, and reflecting to the border genetic diversity
of host plants in the Middle East. Recent research on
triticale could not confirm this clime. Authors
assumed that the isolates from Israel were only path-
ogenic on wheat, not on triticale and rye. As well as
if isolates were pathogenic on triticale, their viru-
lence profiles on triticale cultivars did not differ sig-
nificantly among the different sampled regions
(Belgium, France and Poland; Troch et al. 2012).
Probably the triticale cultivars from different Euro-
pean breeding companies have the same very narrow
genetic background and carry the same R genes for
powdery mildew resistance (Walker et al. 2011). In
this study it any relationship between the location
on the map of the country and the increase in viru-
lence of the population of powdery mildew present
on triticale was found. Sites in the same homoge-
neous group are located in different parts of the
country. Studies conducted by Cichy and Olejniczak
(2010) suggest that overcoming the resistance of triti-
cale cereal mildew is observed throughout the coun-
try, particularly in areas such as research and
breeding points, and areas of cultivation of triticale.
Therefore, it can be assumed that the host range
expansion of wheat isolates to the new host triticale
occurred recently a multiple times at different loca-
tions, as well in Poland and in Europe (Walker et al.
2011; Troch et al. 2012). Population genetic analysis
of wheat powdery mildew demonstrated that popula-
tions were geographically differentiated (Parks et al.
2008). Long distance dispersal of fungal spores by the
wind can spread diseases across and between conti-
nents (Limpert et al. 1999).
Acknowledgements
We would like to thank for all the field technicians
who sent samples infected with powdery mildew used
in this work. Present research was funded by the Min-
istry of Science and Higher Education, Republic of
Poland (Code No. N N 310 314834).
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