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.

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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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