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Plant Disease / March 2013 379
Virulence Characterization of International Collections of the Wheat Stripe Rust
Pathogen, Puccinia striiformis f. sp. tritici
D. Sharma-Poudyal, Department of Plant Pathology, Washington State University, Pullman, WA, USA 99164-6430; X. M. Chen, United
States Department of Agriculture–Agricultural Research Service, Wheat Genetics, Quality, Physiology, and Disease Research Unit and De-
partment of Plant Pathology, Washington State University, Pullman; A. M. Wan, Department of Plant Pathology, Washington State Uni-
versity, Pullman; G. M. Zhan and Z. S. Kang, State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Pro-
tection, Northwest A&F University, Yangling, Shaanxi, China; S. Q. Cao and S. L. Jin, Institute of Plant Protection, Gansu Academy of
Agricultural Sciences, Lanzhou, Gansu, China; A. Morgounov and B. Akin, International Winter Wheat Improvement Program,
(ICARDA-CIMMYT) Wheat Improvement Program, Ankara, Turkey; Z. Mert, Central Research Institute for Field Crops, Ankara, Turkey;
S. J. A. Shah, Nuclear Institute for Food and Agriculture, Peshawar, Pakistan; H. Bux, Institute of Plant Sciences, University of Sindh
Jamshoro, Pakistan; M. Ashraf, NUST Centre of Virology and Immunology, National University of Science and Technology (NUST),
Islamabad, Pakistan; R. C. Sharma, ICARDA-Central Asia and the Caucasus Regional Program, 4564, Tashkent, Uzbekistan;
R. Madariaga, National Institute of Agricultural Research, Chillan, Chile; K. D. Puri, Department of Plant Pathology, North Dakota State
University, Fargo 58108-6050; C. Wellings, Plant Breeding Institute, University of Sydney, Camden, NSW, Australia; K. Q. Xi, Field Crop
Development Centre, Alberta Agriculture and Food, Lacombe, Canada; R. Wanyera, Kenyan Agricultural Research Institute, Njoro,
Kenya; K. Manninger, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest;
M. I. Ganzález, Limagrain Ibérica, Marchena, Spain; M. Koyda and S. Sanin, All-Russian Research Institute of Phytopathology, Bolshie
Vyazemy, Russia; and L. J. Patzek, Department of Crop and Soil Sciences, Washington State University, NWREC, Mount Vernon
Abstract
Sharma-Poudyal, D., Chen, X. M., Wan, A. M., Zhan, G. M., Kang, Z. S., Cao, S. Q., Jin, S. L., Morgounov, A., Akin, B., Mert, Z., Shah, S. J. A.,
Bux, H., Ashraf, M., Sharma, R. C., Madariaga, R., Puri, K. D., Wellings, C., Xi, K. Q., Wanyera, R., Manninger, K., Ganzález, M. I., Koyda, M.,
Sanin, S., and Patzek, L. J. 2013. Virulence characterization of international collections of the wheat stripe rust pathogen, Puccinia striiformis f. sp.
tritici. Plant Dis. 97:379-386.
Wheat stripe rust (yellow rust [Yr]), caused by Puccinia striiformis f. sp.
tritici, is an economically important disease of wheat worldwide. Virulence
information on P. striiformis f. sp. tritici populations is important to
implement effective disease control with resistant cultivars. In total, 235 P.
striiformis f. sp. tritici isolates from Algeria, Australia, Canada, Chile,
China, Hungary, Kenya, Nepal, Pakistan, Russia, Spain, Turkey, and Uz-
bekistan were tested on 20 single Yr-gene lines and the 20 wheat genotypes
that are used to differentiate P. striiformis f. sp. tritici races in the United
States. The 235 isolates were identified as 129 virulence patterns on the
single-gene lines and 169 virulence patterns on the U.S. differentials.
Virulences to YrA, Yr2, Yr6, Yr7, Yr8, Yr9, Yr17, Yr25, YrUkn, Yr28, Yr31,
YrExp2, Lemhi (Yr21), Paha (YrPa1, YrPa2, YrPa3), Druchamp (Yr3a,
YrD, YrDru), Produra (YrPr1, YrPr2), Stephens (Yr3a, YrS, YrSte), Lee
(Yr7, Yr22, Yr23), Fielder (Yr6, Yr20), Tyee (YrTye), Tres (YrTr1, YrTr2),
Express (YrExp1, YrExp2), Clement (Yr9, YrCle), and Compair (Yr8, Yr19)
were detected in all countries. At least 80% of the isolates were virulent on
YrA, Yr2, Yr6, Yr7, Yr8, Yr17, YrUkn, Yr31, YrExp2, Yr21, Stephens (Yr3a,
YrS, YrSte), Lee (Yr7, Yr22, Yr23), and Fielder (Yr6, Yr20). Virulences to
Yr1, Yr9, Yr25, Yr27, Yr28, Heines VII (Yr2, YrHVII), Paha (YrPa1, YrPa2,
YrPa3), Druchamp (Yr3a, YrD, YrDru), Produra (YrPr1, YrPr2), Yamhill
(Yr2, Yr4a, YrYam), Tye e (YrTye), Tres (YrTr1, YrTr2), Hyak (Yr17, YrTye),
Express (YrExp1, YrExp2), Clement (Yr9, YrCle), and Compair (Yr8, Yr19)
were moderately frequent (>20 to <80%). Virulence to Yr10, Yr24, Yr32,
YrSP, and Moro (Yr10, YrMor) was low (≤20%). Virulence to Moro was
absent in Algeria, Australia, Canada, Kenya, Russia, Spain, Turkey, and
China, but 5% of the Chinese isolates were virulent to Yr10. None of the
isolates from Algeria, Canada, China, Kenya, Russia, and Spain was
virulent to Yr24; none of the isolates from Algeria, Australia, Canada,
Nepal, Russia, and Spain was virulent to Yr32; none of the isolates from Aus-
tralia, Canada, Chile, Hungary, Kenya, Kenya, Nepal, Pakistan, Russia, and
Spain was virulent to YrSP; and none of the isolates from any country was
virulent to Yr5 and Yr15. Although the frequencies of virulence factors
were different, most of the P. striiformis f. sp. tritici isolates from these coun-
tries shared common virulence factors. The virulences and their frequencies
and distributions should be useful in breeding stripe-rust-resistant wheat
cultivars and understanding the pathogen migration and evolution.
Stripe rust (yellow rust), caused by Puccinia striiformis
Westend. f. sp. tritici Erikss., is a worldwide economically
important disease of wheat (5,19,36). Frequent and severe disease
epidemics are common in major wheat-growing countries (45).
Among the countries in the Americas, stripe rust is especially im-
portant in the United States (5), Mexico, Chile, and other Andean
countries (11). Similarly, stripe rust is a serious problem in Europe,
the Middle East (36,45), Central Asia (26), China (4), and the
northern Indian subcontinent (34). In Africa, the disease occurs on
wheat grown in the highlands of Ethiopia, Kenya, and Uganda
(11,37). In recent decades, wheat stripe rust has spread into addi-
tional countries and has become important in Australia, New Zea-
land, and South Africa (45).
Cultivation of resistant cultivars is the most economically effec-
tive method for stripe rust management and minimizes environ-
mental impacts by reducing the use of fungicides (5,19). However,
within a few years of deploying cultivars with race-specific re-
sistance genes, new virulent races (pathotypes) of the rust pathogen
often emerge (20,34,37). As a result, new races can infect previ-
Corresponding author: X. M. Chen, E-mail: xianming@wsu.edu
*The e-Xtra logo stands for “electronic extra” and indicates that three
supplementary tables and one supplementary figure are available online.
PPNS Number 0590, Department of Plant Pathology, College of Agricultural,
Human, and Natural Resource Sciences, Agricultural Research Center, Projec
t
Number WNP00663, Washington State University, Pullman 99164-6430.
Mention of trade names or commercial products in this publication is solely
for the purpose of providing specific information and does not imply
recommendation or endorsement by the United States Department of Agri-
culture (USDA). USDA is an equal opportunity provider and employer.
Accepted for publication 4 October 2012.
http://dx.doi.org/10.1094 /PDIS-01-12-0078-RE
This article is in the public domain and not copyrightable. It may be freely
reprinted with customary crediting of the source. The American Phytopatho-
logical Society, 2013.
e-Xt
r
a*
380 Plant Disease / Vol. 97 No. 3
ously resistant cultivars, rendering them susceptible (5,36). Severe
stripe rust epidemics are often due to the emergence of new races
that cause failure of resistance genes (6). For example, more than
80% of cultivars released in the late 1980s had Yr9 and, as a result,
a new race virulent on Yr9 was reported in 1985; this race caused
epidemics resulting in yield loss of 2.65 million tons in 1990 in
China (4,41). Similarly, Yr27 has been widely used in wheat culti-
vars grown in India and Pakistan and the emergence of new races
virulent to Yr27 has been reported in South Asia between 2002 and
2004 (34). Serious stripe rust outbreaks in south- and central-Asian
countries in 2009 have been attributed to races virulent to Yr27 (2).
These epidemics are further aggravated when new races possess
more complex virulence combinations evolved through mutation,
recombination, or migration over long distance (34,37,45). Such
epidemics result in application of a large amount of fungicides to
manage a disease that would otherwise cause substantial yield loss
(5,6).
Monitoring P. striiformis f. sp. tritici races should be a high
priority in all epidemic regions in the world, because the rust
urediniospores can be wind transported over long distances (34).
Frequent monitoring of the virulence spectra of P. striiformis f. sp.
tritici populations and identification of new races are prerequisites
for devising effective disease management strategies through re-
sistance breeding and prediction of future races (23). Identification
of virulent races is essential for the characterization of non-race-
specific resistance (5). Information on virulence is also useful in
screening cultivars or breeding lines for the determination of resist-
ance levels and exploitation of new resistance genes. In addition,
monitoring the virulence of the stripe rust pathogen population in
different regions helps to understand the current genetic variability
of host–pathogen interactions.
Virulence of the stripe rust pathogen has been routinely studied
at a national scale (4,5,44); however, few studies have compared
virulences at an international scale. Stubbs (37) reviewed and nar-
rated the regional distribution of stripe rust virulences in Africa,
Asia, Europe, and Americas. Recently, Hovmøller et al. (14) car-
ried out a virulence study of international collections of P. strii-
formis f. sp. tritici but isolates were predominantly from Denmark
and the Red Sea area. In addition, the study mainly focused on the
spread of aggressive strains rather than all virulences. Therefore,
the objectives of this study were to identify virulences and races,
and determine their frequencies and distributions of P. striiformis f.
sp. tritici samples collected from 2006 to 2010 in different wheat-
growing countries.
Materials and Methods
Stripe rust isolates. In total, 235 P. striiformis f. sp. tritici
isolates were analyzed; 1 from Algeria collected in 2009, 5 from
Australia (2006), 5 from Canada (2007), 15 from Chile (2007), 60
from China (2006 and 2007), 4 from Hungary (2009), 4 from
Kenya (2006), 21 from Nepal (2007 and 2008), 46 from Pakistan
(2006–09), 2 from Russia (2006), 2 from Spain (2008 and 2009),
54 from Turkey (2009 and 2010), and 16 from Uzbekistan (2009
and 2010). Leaf samples bearing stripe rust uredinia were stored at
4°C upon receipt.
Spore production. Urediniospores were revived and increased
by placing leaf sections of about 3 cm in length on moist blotting
paper and incubating overnight at temperatures gradually cycling
from 15 to 4 to 15°C. Fresh urediniospores produced on the leaf
surface were inoculated with a clean, fine paint brush on leaves of
susceptible winter wheat ‘Nugaines’ grown in plastic pots to the
two-leaf stage. Isolates stored as urediniospores in liquid nitrogen
were reactivated by submerging spore-containing glass vials or foil
bags in a water bath at 50°C for 2 min, and were inoculated on
Nugaines seedlings to increase urediniospores (8). Nugaines was
grown in plastic pots (7 by 7 by 7 cm) filled with a potting mixture
of 24 liters of peat moss, 8 liters of perlite, 12 liters of sand, 12
liters of commercial potting soil mix, 16 liters of vermiculite, and
250 g of 14%-14%-14% (available N-P-K) Osmocote fertilizer
(Scotts Miracle-Gro Company). Plants were grown in a rust-free
greenhouse prior to inoculation. Inoculated plants were kept in a
dew chamber for at least 12 h at 10°C, then transferred into a tem-
perature-controlled growth chamber. The temperature of the
growth chamber was programmed between a minimum of 4°C at
2:00 a.m. during the 8-h dark period and a maximum of 20°C at
2:00 p.m. during the 16-h light period. Metal halide lights were
used as a supplement to the daylight of a 16-h photoperiod. Inocu-
lated seedlings were isolated from each other with a transparent
plastic cylinder surrounding each pot to prevent cross-contamina-
tion (7). Urediniospores were collected 16 days after inoculation
and spore collection was repeated three to four times until suffi-
cient quantities were harvested (approximately 20 mg). Uredini-
ospores were dried in a desiccator at 4°C for 1 week before being
stored at 4°C for a short term (up to 2 months) or in liquid nitrogen
Tab le 1 . Twenty single Yr-gene lines of wheat and the set of 20 wheat genotypes for differentiating Puccinia striiformis f. tritici races in the United States
used to test international P. striiformis f. sp. tritici collections for determination of their virulences and avirulencesa
Single Yr gene linesb U.S. differentials
Number Name Yr gene Name Yr gene
1 AvSYrANIL YrA Lemhi Yr21
2 AvSYr1NIL Yr1 Chinese 166 Yr1
3 Siete Cerros T66 Yr2 Heines VII Yr2,YrHVII
4 AvSYr5NIL Yr5 Moro Yr10,YrMor
5 AvSYr6NIL Yr6 Paha YrPa1,YrPa2,YrPa3
6 AvSYr7NIL Yr7 Druchamp Yr3a,YrD,YrDru
7 AvSYr8NIL Yr8 AvSYr5NIL Yr5
8 AvSYr9NIL Yr9 Produra YrPr1,YrPr2
9 AvSYr10NIL Yr10 Yamhill Yr2,Yr4a,YrYam
10 AvSYr15NIL Yr15 Stephens Yr3a,YrS,YrSte
11 AvSYr17NIL Yr17 Lee Yr7,Yr22,Yr23
12 AvSYr24NIL Yr24 Fielder Yr6,Yr20
13 TP981 Yr25 Tyee YrTye
14 AvSYrUknNIL YrUknc Tres YrTr1,YrTr2
15 AvSYr27NIL Yr27 Hyak Yr17,YrTye
16 AvSYr28NIL Yr28 Express YrExp1,YrExp2
17 AvSYr31NIL Yr31 AvSYr8NIL Yr8
18 AvSYr32NIL Yr32 AvSYr9NIL Yr9
19 AvSYrSPNIL YrSP Clement Yr9,YrCle
20 AvS/EXP1/1-1 Line 74 YrExp2 Compair Yr8,Yr19
a NIL = near isogenic line.
b Yr gene lines are in the ‘Avocet Susceptible’ (AvS) background.
c YrUkn was included in the study initially as Yr26 but, later, it was found not to be Yr26 and different from any known Yr genes.
Plant Disease / March 2013 381
for the long term (years). Fresh urediniospores or those stored at
4°C within 2 months were tested on wheat single Yr-gene lines and
differentials (8).
Determination of virulences and virulence patterns. In all, 20
single Yr-gene lines and 20 wheat genotypes used to differentiate
races of P. striiformis f. sp. tritici in the United States (7,8) (Table
1) were used to identify virulences among the P. striiformis f. sp.
tritici isolates. Previously described procedures and conditions (at
the low diurnal temperature profile of 4 to 20°C) were followed to
grow plants and inoculate wheat differentials (8,20).
Seedlings were evaluated for infection type (IT) 20 to 22 days
after inoculation (7). Scoring of ITs from 0 to 9 was done as de-
scribed by Line and Qayoum (20), where 0 = no visible signs or
symptoms; 1 = necrotic or chlorotic flecks, no sporulation; 2 =
necrotic or chlorotic blotches, no sporulation; 3 = necrotic or chlo-
rotic blotches, trace sporulation; 4 = necrotic or chlorotic blotches,
light sporulation; 5 = necrotic or chlorotic blotches, intermediate
sporulation; 6 = necrotic or chlorotic blotches, moderate sporula-
tion; 7 = necrotic or chlorotic blotches, abundant sporulation; 8 =
chlorosis behind sporulating area, abundant sporulation; and 9 = no
necrosis or chlorosis, abundant sporulation. ITs 0 to 6 were consid-
ered avirulent and 7 to 9 virulent (17,40). The virulence test on the
two sets of wheat differentials, per isolate, was done once or re-
peated if the results were inconclusive.
Virulence patterns and frequencies. Virulence and avirulence
patterns based on data from the single Yr-gene lines and the U.S.
differentials were determined separately for all isolates. The viru-
lence or avirulence pattern based on the single Yr-gene lines was
presented by Yr genes whereas the virulence patterns based on the
U.S. differentials were presented by the designated differential
numbers for each isolate. Isolates from Algeria, Spain, and Russia
were included only to calculate the total percentage of virulence
factors in the international collection but not used in the country-
wise analyses of virulence frequency due to the limited sample
numbers. For these analyses, virulence and avirulence data from
both differential sets were combined. The virulence and avirulence
ITs of each isolate on the differential genotypes were assigned with
binary codes of 1 and 0, respectively. Frequencies were calculated
for all virulence factors.
Cluster analysis. Virulence relationships among the isolates
were analyzed using the NTSYSpc software (version 2.10e; (Ap-
plied Biostatistics Inc.) (8,32). A similarity matrix was calculated
based on simple matching coefficients. Cluster analysis was per-
formed based on the similarity matrix to generate a dendrogram
using the unweighted pair group method with arithmetic mean
(UPGMA; 31). A correlation coefficient between cophenetic ma-
trix and similarity matrix was calculated using the Mantel test.
Robustness of the dendrogram branches was determined with the
Winboot programs (29; http://archive.irri.org/science/software/
winboot.asp). In addition, a three-dimensional principal coordinate
(PC) plot was generated in NTSYSpc by transforming the
similarity matrix using the DCENTER module and then using
EIGEN module.
Results
Virulences and their frequencies and distributions. ITs of the
235 P. striiformis f. sp. tritici isolates using the 0-to-9 scale are
given in Supplementary Table S1. ITs observed were mostly either
low (ITs 0 to 2; 38%) or high (ITs 7 to 9; 58%), with only a very
low percentage (4%) showing ITs 3 to 6, which made it relatively
easy to assign isolates to virulence patterns. Stripe rust isolates
from different countries differed in virulence patterns, frequencies,
and distributions, except for Algeria, Russia, and Spain due to a
limited number of samples (Table 2). At an international scale, the
most frequent virulences (≥80%) were those to resistance genes
YrA (89%), Yr2 (92%), Yr6 (92%), Yr7 (90%), Yr8 (80%), Yr17
(88%), YrUkn (89%), Yr31 (99%), YrExp2 (89%), and Yr21 (98%)
and U.S. differentials 10 (91%), 11 (84%), and 12 (84%).
Moderately frequent virulences (between 20 and 80%) included
Yr1 (49%), Yr9 (68%), Yr25 (39%), Yr27 (69%), and Yr28 (79%)
and U.S. differentials 3 (56%), 5 (70%), 6 (40%), 9 (31%), 13
(42%), 14 (41%), 15 (31%), 16 (71%), 19 (54%), and 20 (69%).
The least frequent virulences (≤20%) were to Yr10 (9%), Yr24
(11%), Yr32 (11%), YrSP (9%), and Moro (6%). None of the
isolates were virulent to Yr5 and Yr15.
Out of 36 single Yr genes or gene combinations of the two sets
of differentials, virulences to 25 lines (YrA, Yr2, Yr6, Yr7, Yr8, Yr9,
Yr17, Yr25, YrUkn, Yr28, Yr31, and YrExp2 and U.S. differentials 1,
5, 6, 8, 10, 11, 12, 13, 14, 16, 19, and 20) were observed in all
countries. Isolates from all of these countries were virulent on
Yr21, except four isolates from Pakistan. More than 50% of iso-
lates from these countries were virulent to YrA, Yr2, Yr6, Yr17,
YrUkn, and Yr31 and U.S. differentials 1, 10, and 12. All isolates
from Canada, Hungary, Nepal, and Uzbekistan were virulent to
YrA. Similarly, all isolates from Australia, Canada, Chile, Hungary,
Kenya, Nepal, and Uzbekistan were virulent to Yr2 and Yr31. All
isolates from Turkey were virulent to Yr31. All isolates from Can-
ada and Hungary were virulent to both Yr6 and Yr7, whereas all
isolates from Uzbekistan were virulent on Yr6 and from Kenya and
Nepal were virulent on Yr7. Virulence on Stephens (differential 10)
was detected in all isolates from Australia, Canada, Hungary, and
Uzbekistan. Isolates were virulent to Yr27 from all countries ex-
cept Australia; however, three of five isolates from Australia had an
intermediate reaction (IT 6) on the Yr27 single gene line.
Virulences to Yr1, Yr10, Yr24, Yr32, and YrSP and U.S. differ-
entials 3, 4, 9, and 15 were present but not in all countries. None of
the isolates from Australia, Canada, and Turkey were virulent to
Yr10 and Moro (Yr10 and YrMor). None of the Chinese P. strii-
formis f. sp. tritici isolates were virulent on Moro but some (5%)
were virulent to Yr10. None of the isolates from Canada, China,
and Kenya were virulent to Yr24; none of the isolates from
Australia, Canada, and Nepal were virulent to Yr32; and none of
the isolates from Australia, Canada, Chile, Hungary, Kenya, Nepal,
and Pakistan were virulent to YrSP. Only all Chilean and Kenyan
isolates were avirulent to Hyak (Yr17, YrTye).
Isolates from Algeria, Russia, and Spain, not included in the
country-wise frequency analysis (Table 2), were virulent to Yr2,
Yr6, Yr8, Yr9, Yr17, and YrUkn and U.S. differentials 1 and 10. All
of these isolates were avirulent to Yr5, Yr10, Yr15, Yr24, and Yr32
and U.S. differentials 4 and 15. In addition, the isolates from Alge-
ria and Spain were avirulent to YrSP and U.S. differentials 6 and 9.
Virulence patterns. More virulence patterns were identified
based on the 20 U.S. differentials for most countries than those
based on the 20 single Yr-gene lines. Of the 235 isolates, the single
Yr-gene lines identified 129 whereas the set of U.S. wheat differen-
tials identified 169 virulence patterns (Table 3). The virulence and
avirulence patterns identified from the 235 isolates based on the
single Yr-gene lines and the U.S. wheat differentials are listed in
Supplementary Tables S2 and S3, respectively. Among the 129
virulence patterns identified with the single Yr-gene lines, 101
were detected only with one isolate. The most frequent (13%)
pattern was the one virulent to resistance genes YrA, Yr2, Yr6, Yr7,
Yr8, Yr9, Yr17, YrUkn, Yr27, Yr28, Yr31, and YrExp2 and avirulent
to Yr1, Yr5, Yr10, Yr15, Yr24, Yr25, Yr32, and YrSP. This virulence
pattern was detected in isolates from Canada, China, and Turkey.
The highest frequency (93%) of two associated virulence factors
was found for Yr2 and Yr31. Similarly, the highest frequencies for
three, four, and five virulence factors in combination were 86%
(virulences to Yr2, Yr6, and Yr31), 79% (virulences to Yr2, Yr6,
Yr7, and Yr31), and 74% (virulences to YrA, Yr2, Yr6, Yr7, and
Yr31), respectively. These virulence combinations were present in
all countries.
Of the 169 virulence patterns based on the U.S. differentials, 122
patterns each were detected with only one isolate. The most
frequent (8%) virulence pattern, which was virulent on U.S.
differentials 1 (Yr21), 5 (YrPa1, YrPa2, YrPa3), 8 (YrPr1, YrPr2),
10 (Yr3a, YrS, YrSte), 12 (Yr6, Yr20), 14 (YrTr1, YrTr2), 16
(YrExp1, YrExp2), 17 (Yr8), and 20 (Yr8, Yr19) and avirulent on 2
(Yr1), 3 (Yr2, YrHVII), 4 (Yr10, YrMor), 6 (Yr3a, YrD, YrDru), 7
(Yr5), 9 (Yr2, Yr4a, YrYam), 11 (Yr7, Yr22, Yr23), 13 (YrTye), 15
382 Plant Disease / Vol. 97 No. 3
(Yr17, YrTye), 18 (Yr9), and 19 (Yr9, YrCle) was detected in
isolates from Chile, China, and Turkey. Twenty of the virulence
patterns obtained from the international isolate resembled races
identified in the United States. Virulences on U.S. differentials 1
and 10 appeared together at the highest frequency (90%). The
highest frequencies for combinations of virulences on three (1, 10,
and 11) and four (1, 10, 11, and 12) of the U.S. differentials were
78 and 70%, respectively. These virulence combinations were
detected in all of the countries.
Cluster analysis. Cluster analysis was performed on combined
virulence and avirulence data obtained from the single Yr-gene
lines and the U.S. differentials. A cutoff point of 0.74 similarity
coefficient was determined based on mean value of similarity
range. In general, isolates from different countries were grouped
together in the same groups. All 235 isolates clustered into 11 viru-
lence groups (VGs) (Fig. 1). These 11 VGs were further grouped
into two major VGs at a similarity coefficient of 0.48. The first
major group consisted of VG 1 to VG 8 and accounted for 97% of
the isolates; the second major group consisted of VG 9 to VG 11
and accounted for 3% of the isolates. VGs 1 and 5 were the largest
groups and accounted for 81% of isolates. VG 1 had 69 isolates
(29%) (all virulent to Yr1, YrA, Yr6, Yr9, Yr21, Yr31, and Stephens
Tab le 2 . Number and frequency of virulences in Puccinia striiformis f. sp. tritici isolates collected from different countries on single Yr-gene lines (Yr) and
U.S. differentials (Diff)
Number (N) and frequency (%) of virulence in P. striiformis f. sp. tritici isolates from different countriesa
Tot al AU CA CL CN HU KE NP PK TR UZ
Number Yr gene % N % N % N % N % N % N % N % N % N % N %
Yr
1 A 89 4 80 5 100 9 60 59 98 4 100 2 50 21 100 32 70 53 98 16 100
2 1 49 2 40 0 0 4 27 25 42 2 50 3 75 15 71 26 57 21 39 14 88
3 2 93 5 100 5 100 15 100 54 90 4 100 4 100 21 100 41 89 49 91 16 100
4 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
5 6 92 3 60 5 100 9 60 56 93 4 100 3 75 20 95 44 96 52 96 16 100
6 7 90 2 40 5 100 12 80 57 95 4 100 4 100 21 100 42 91 51 94 10 63
7 8 80 1 20 3 60 6 40 53 88 3 75 3 75 18 86 34 74 51 94 10 63
8 9 68 2 40 3 60 5 33 30 50 3 75 4 100 12 57 39 85 40 74 16 100
9 10 9 0 0 0 0 5 33 3 5 2 50 1 25 4 19 5 11 0 0 1 6
10 15 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
11 17 88 5 100 5 100 14 93 41 68 4 100 4 100 18 86 45 98 50 93 15 94
12 24 11 1 20 0 0 4 27 0 0 1 25 0 0 1 5 13 28 4 7 1 6
13 25 39 1 20 1 20 6 40 18 30 3 75 2 50 8 38 17 37 22 41 12 75
14 Ukn 89 3 60 4 80 10 67 49 82 2 50 3 75 21 100 45 98 52 96 16 100
15 27 69 0 0 3 60 4 27 40 67 3 75 2 50 16 76 38 83 45 83 9 56
16 28 79 4 80 5 100 13 87 37 62 3 75 1 25 18 86 36 78 50 93 15 94
17 31 99 5 100 5 100 15 100 59 98 4 100 4 100 21 100 45 98 54 100 16 100
18 32 11 0 0 0 0 5 33 1 2 2 50 0 0 0 0 13 28 4 7 1 6
19 SP 10 0 0 0 0 0 0 16 27 0 0 0 0 0 0 0 0 4 7 2 13
20 Exp2 89 2 40 5 100 12 80 56 93 4 100 4 100 20 95 43 93 49 91 10 63
Diff
1 21 98 5 100 5 100 15 100 60 100 4 100 4 100 21 100 41 89 54 100 16 100
2 1 49 2 40 0 0 4 27 25 42 2 50 3 75 15 71 26 57 21 39 14 88
3 2,HVII 56 5 100 3 60 2 13 22 37 4 100 1 25 9 43 33 72 35 65 13 81
4 10,Mor 7 0 0 0 0 4 27 0 0 2 50 0 0 4 19 5 11 0 0 1 6
5 Pa1,Pa2,Pa3 70 5 100 1 20 5 33 49 82 3 75 2 50 16 76 31 67 33 61 16 100
6 3a,D,Dru 40 4 80 1 20 6 40 23 38 2 50 1 25 10 48 17 37 15 28 14 88
7 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
8 Pr1,Pr2 77 3 60 4 80 7 47 53 88 4 100 1 25 12 57 35 76 46 85 14 88
9 2,4a,Yam 31 0 0 0 0 3 20 20 33 2 50 0 0 5 24 11 24 19 35 11 69
10 3a,S,Ste 91 5 100 5 100 12 80 54 90 4 100 2 50 20 95 39 85 52 96 16 100
11 7,22,23 84 2 40 5 100 10 67 52 87 4 100 3 75 18 86 40 87 50 93 10 63
12 6,20 84 3 60 4 80 8 53 41 68 4 100 3 75 20 95 43 93 52 96 16 100
13 Tye 42 1 20 2 40 1 7 24 40 3 75 2 50 9 43 22 48 21 39 12 75
14 Tr1,Tr2 41 1 20 4 80 5 33 30 50 2 50 1 25 6 29 21 46 20 37 4 25
15 17,Tye 31 1 20 2 40 0 0 20 33 2 50 0 0 2 10 20 43 17 31 8 50
16 Exp1,Exp2 71 2 40 4 80 7 47 41 68 4 100 4 100 19 90 35 76 40 74 8 50
17 8 80 1 20 3 60 6 40 53 88 3 75 3 75 18 86 34 74 51 94 10 63
18 9 68 2 40 3 60 5 33 30 50 3 75 4 100 12 57 39 85 40 74 16 100
19 9,Cle 54 1 20 3 60 4 27 24 40 3 75 3 75 9 43 25 54 38 70 15 94
20 8,19 69 1 20 3 60 5 33 49 82 3 75 3 75 15 71 30 65 43 80 7 44
a AU = Australia, CA = Canada, CL = Chile, CN = China, HU = Hungary, KE = Kenya, NP = Nepal, PK = Pakistan, TR = Turkey, and UZ = Uzbekistan.
Isolates from Algeria, Spain, and Russia were used to calculate the total virulence percentage (%) but country-wise virulence frequency was not calculated
for the three countries due to the limited sample numbers.
Tab le 3 . Number of Puccinia striiformis f. sp. tritici virulence patterns
based on single Yr-gene lines and U.S. differentials from different coun-
tries
Number of races
Countries Number of isolates Yr-gene Differentials
Algeria 1 1 1
Australia 5 5 5
Canada 5 4 5
Chile 15 13 14
China 60 39 40
Hungary 4 4 4
Kenya 4 4 4
Nepal 21 15 20
Pakistan 46 28 42
Russia 2 2 2
Spain 2 2 2
Turkey 54 27 45
Uzbekistan 16 9 13
Totala 235 129a 169a
aTotal number of virulence patterns was calculated from different patterns
from the 235 isolates regardless of the numbers in each country as some
patterns shared by different countries.
Plant Disease / March 2013 383
[Yr3a, YrS, YrSte]) from all countries except Algeria, Canada,
Chile, and Spain, with an average similarity of 76% (Supplemen-
tary Figure S1). VG 5 was the largest group, with 121 (51%) iso-
lates from all countries except Algeria, having similarity of about
77%. Isolates belonging to VG 5 had different frequencies of viru-
lences on all differentials tested except Yr5 and Yr15. Isolates be-
longing to VG 2 were virulent to Yr1, Yr2, Yr6, Yr7, Yr8, Yr9,
Yr17, Yr25, and Yr31 and U.S. differentials 1, 3, 11, 12, 13, 19, and
20. These isolates were all avirulent to Yr5, Yr10, Yr15, Yr17,
Yr24, Yr27, Yr32, and YrSP and U.S. differentials 4, 5, 6, 9, and
15. Isolates on VG 3 were virulent to YrA, Yr1, Yr2, Yr7, Yr9,
Yr31, and YrExp2 and U.S. differentials 1, 3, 10, 13, and 20 but
avirulent to Yr5, Yr10, Yr15, Yr17, Yr24, Yr26, Yr27, Yr32, and
YrSP and U.S. differentials 4, 12, and 16. Similarly, isolates be-
longing to VG 4 were all virulent to YrA, Yr1, Yr6, Yr7, Yr9, Yr31,
and YrExp2 and U.S. differentials 1, 5, 7, 12, 13, and 19 but aviru-
lent to Yr2, Yr5, Yr10, Yr15, Yr24, Yr27, Yr28, Yr32, and YrSP and
U.S. differentials 3, 4, 6, 14, 15, 16, and 20. The isolates in VG 6
all had virulences to YrA, Yr2, Yr6, Yr7, Yr8, Yr9, Yr17, Yr31, and
YrExp2 and U.S. differentials 1, 12, 19, and 20. These isolates
were avirulent on Yr5, Yr15, and YrSP and U.S. differential 9. VG
7 isolates were all virulent on Yr2, Yr7, Yr17, Yr31, and YrExp2
and U.S. differential 1, 8, 16, and 18 and were all avirulent to Yr1,
Yr5, Yr10, Yr15, Yr25, Yr27, and YrSP and U.S. differentials 3, 4,
6, 9, 11, 15, 17, and 20. The isolates in VG 8 were virulent to Yr2,
Yr17, Yr28, Yr31, and YrExp2 and U.S. differential 1.
In general, the isolates in VGs 9 to 11 had relatively narrow
virulence spectra compared with those of VGs 1 to 8. The isolates
in VG 9 were all virulent to Yr2, Yr17, and Yr31 and U.S. differen-
tials 1, 3, 5, 6, and 10. The VG 10 isolates had virulences to Yr2,
Yr10, Yr31, and Yr32 and U.S. differentials 1, 5, and 14. All iso-
lates in VG 11 were virulent on Yr2, Yr6, Yr17, YrUkn, and Yr31
and U.S. differentials 1, 3, 12, 13, and 15. Isolates belonging to
MG 2 (VG 9-11) were avirulent to Yr5, Yr7, Yr8, Yr9, Yr25, Yr27,
and YrSP and U.S. differentials 8, 9, 11, 16, 19, and 20.
Of the 235 isolates, 3 isolates, 1 each from Chile (virulent on
YrA, Yr1, Yr2, Yr6, Yr7, Yr8, Yr9, Yr10, Yr17, Yr25, YrUkn, Yr28,
Yr31, Yr32, and YrExp2 and U.S. differentials 1, 2, 4, 6, 8, 9, 10,
Fig. 1. Dendrogram based on virulence phenotypes of Puccinia striiformis f. sp. tritici on 20 single Yr-gene lines and 20 U.S. differentials using the unweighted pair group
method with arithmetic mean method. Three out-group isolates were not shown in the figure (see the text for details). Numbers along the nodes are bootstrap values >30%.
AU = Australia, CA = Canada, CL = Chile, CN = China, DZ = Algeria, ES = Spain, HU = Hungary, KE = Kenya, NP = Nepal, PK = Pakistan, RU = Russia, TR = Turkey, and UZ
= Uzbekistan.
384 Plant Disease / Vol. 97 No. 3
11, 12, 16, 17, 18, and 19), China (virulent on YrA, Yr1, Yr2, Yr7,
Yr9, Yr17, Yr27, Yr28, Yr31, YrSP, and YrExp2 and U.S.
differentials 1, 2, 5, 6, 8, 10, 11, 13, 15, and 18), and Pakistan (Yr2,
Yr6, Yr7, Yr9, Yr17, Yr25, YrUkn, Yr27, Yr28, Yr31, and YrExp2
and U.S. differentials 1, 3, 5, 6, 9, 10, 11, 14, 16, 18, and 19) did
not cluster into any group.
The three-dimensional PC analysis showed the pairwise distance
between isolates and groupings of isolates based on virulence data
(Fig. 2). In general, isolates originating from different countries did
not differentiate into unique groups. These results further sup-
ported the inclusion of isolates originating from different countries
within the same VGs, as revealed by the cluster analysis (Fig. 1).
For example, isolates CL07-12 and PK09-30 from Chile and Paki-
stan, respectively, had similar virulence patterns. However, even
some isolates from the same country were found to be distantly
related; for example, PK07-9 and PK06-3 from Pakistan (Fig. 2).
The first dimension extracted 26% of the total virulence variation,
and second and third dimensions accounted for 15 and 7%, respec-
tively, of the total virulence variation.
Discussion
In all, 20 single Yr-gene lines and 20 U.S. wheat differentials
were used to determine virulences and virulence patterns of 235 P.
striiformis f. sp. tritici isolates collected from 13 countries. The
results revealed common and unique virulences and patterns in the
P. striiformis f. sp. tritici populations in these countries. Virulence
patterns were generally different among countries; however, most
of the virulences were common among isolates from different
countries. Because the P. striiformis f. sp. tritici collections from
the 13 countries varied greatly in sample number, the results from
virulence analyses were used to make general conclusions about
the overall collections; however, country-wise interpretation should
be made cautiously where the sample number was limited.
Therefore, major emphases have been given to the descriptive
analysis rather than inferential statistics.
Comparison of the major virulences in the isolates from different
countries was done based on the resistance genes of the single Yr-
gene lines and U.S. differential genotypes. The P. striiformis f. sp.
tritici isolates in different countries were all virulent to YrA, Yr2,
Yr6, Yr7, Yr31, Yr21, and Stephens (Yr3a, YrS, YrSte). Widespread
deployment of the same resistance genes over large wheat-growing
regions eventually contributes to identical and similar virulence
frequencies in the P. striiformis f. sp. tritici populations. For
example, resistant genes Yr2, Yr6, and Yr7 were used extensively
in Central Asia, West Asia, and North Africa. This may explain
why all the isolates from these regions are virulent on these genes
(1). Our finding is consistent with previous report that virulence to
YrA was common in all wheat-growing continents (25,38).
Virulence for Yr2 was reported in the United States in 1964 (20)
and in Turkey in 1967 and, in 1970, it was traced to the Indian
subcontinent (33). Yr2 is very common in both winter and spring
wheat, and common in wheat distributed through CIMMYT (25).
In addition, Yr2 avirulence gene in P. striiformis f. sp. tritici is
prone to mutation (35). Therefore, virulence to Yr2 may have
evolved simultaneously or migrated to all countries with isolates
tested in the present study. Stubbs (36) also reported widespread
presence of Yr2 on an international scale back to the early 1980s.
The high frequency of Yr6 virulence in all countries may be
explained by the presence of Yr6 in common wheat and durum
wheat (10). Similarly, the high frequency of Yr7 virulence may be
due to the worldwide use of Yr7 through Thatcher (Yr7) and its
presence in old cultivars or landraces (24). Stubbs (36) and
Hovmøller et al. (14) also reported worldwide distribution of Yr7
virulence. The widespread and high-frequency virulence factors
may have been fixed in pathogen populations throughout the
world.
The widespread and high frequency of Yr8 virulence may be due
to worldwide use of this gene from Aegilops comosa and its com-
mon presence in grasses (36). Virulence on Yr8 was detected in the
Middle East in 1973 (13), in England in 1978 (16), in Australia in
the 1980s (43), and in Iran during 1997 to 1999 (28). Virulence to
Yr8 was detected in the United States in 2000 (7). The present
study revealed that Yr8 virulence is widespread, and this finding
agrees with the results of Hovmøller et al. (14). Similarly, the high
frequency of Yr9 virulence and its presence in all isolates in the
present study may have evolved from extensive use of Yr9, origi-
nating from Petkus rye (Secale cereale), in wheat-breeding pro-
grams worldwide (31,36). Yr9 virulence was first identified in the
former Soviet Union in 1973 and in The Netherlands in 1974 (39).
Until 1996, races virulent to Yr9 were reported in other regions or
countries from East Africa to South Asia (34), in China (42), in
South America (Ecuador, Colombia, Bolivia, and Chile) and Mex-
ico (40), and in Australasia (46). Yr9 virulence is common in most
races identified in the United States since 2000 (8). The emergence
and spread of Yr9-virulent races caused serious stripe rust out-
breaks in many major wheat-growing regions (5–8,34).
Fig. 2. Three-dimensional principal coordinate plots of Puccinia striiformis f. sp. tritici isolates based on virulence and avirulence phenotypes on the single Yr-gene lines and
U.S. wheat differentials.
Plant Disease / March 2013 385
Cultivars with Yr27 were deployed extensively in Syria, Turkey,
Iran, India, Pakistan, and other south-Asian countries to address
the failure of Yr9. The wide cultivation of these cultivars created
selection pressure for the pathogen and, thus, virulence for Yr27
emerged in South Asia between 2002 and 2004 (34). In the present
study, the Yr9 and Yr27 virulences were common in isolates from
Pakistan, Nepal, Turkey, and Uzbekistan. Use of Yr9 and Yr27 led
to the emergence of new races virulent on both Yr9 and Yr27 in the
Middle East and South Asia (1). Severe stripe rust epidemics in
Central and Western Asia and North Africa during the 2010 wheat
season was attributed to the Yr27 virulence lineage along with the
favorable weather conditions (2).
In the present study, Yr17 virulence was observed in 88% of all
isolates and 98% from Pakistan isolates. In contrast, Hovmøller et
al. (14) and Bahri et al. (1) reported approximately 3% in interna-
tional isolates collected from Azerbaijan, Australia, Denmark,
Eritrea, France, Iran, Italy, Kazakhstan, Kyrgistan, Mexico, Paki-
stan, South Africa, the United Kingdom, the United States, Uzbeki-
stan, and Yemen and only approximately 4% in P. striiformis f. sp.
tritici collections from Pakistan. The difference in the Yr17 viru-
lence frequencies might be due to different differential genotypes
used in their studies and the present study. In their studies,
Hovmøller et al. (14) and Bahri et al. (1) used VPM1 (Yr17+). The
other Yr gene or genes in VPM1 might have masked the virulence
to Yr17 in their isolates. In the U.S. Pacific Northwest, the Yr17
single-gene line has been widely susceptible, whereas VPM1 is
still resistant (X. M. Chen, unpublished data).
The least frequent group of virulences was different among P.
striiformis f. sp. tritici populations in various countries. Yr10
virulence has been reported in Eastern Europe, the eastern
Mediterranean region (including East Africa), and North America
(8,14,20,36). The presence of Yr10 virulence in Southeast Asia,
Nepal, and Pakistan differed from the findings of Stubbs (36) and
Hovmøller et al. (14). Although virulence to Yr10 occurs in low
frequency (5%) in China, it may have a serious implication
because Yr10 has been reported to be effective (41) and, thus, has
been widely used in breeding programs (18).
The P. striiformis f. sp. tritici populations in different countries
shared most of the virulences but their frequencies and virulence
spectra were different. These differences may have resulted from
selection benefits for certain races with new virulences, higher
fitness, or aggressiveness against resistance genes commonly de-
ployed in the regions. Consequently, such differences in selection
may determine the frequencies of races in a population (23,34).
Recombination shuffles virulence genes and creates more geno-
types or races (15,36). Somatic hybridization has shown to result in
new races (21,48). Mixed infection of races on same plants under
field conditions may facilitate nuclear migration through uredini-
ospore germ tubes and infectious hyphae within plant tissue, which
can lead to the development of new races (22). Furthermore, sexual
recombination, although not proven under natural conditions for P.
striiformis f. sp. tritici, may play a role in generating new races in
areas where the alternate host, barberry, coexists with wheat and
the weather conditions are favorable for barberry infection by P.
striiformis f. sp. tritici (15). However, the deployment of the same
resistance genes across different continents is more likely to select
identical or similar virulences in large regions. The presence of
similar virulences in the international collections and in the U.S.
populations (9) suggests that the P. striiformis f. sp. tritici
population at the international scale mostly possesses the same
genetic background of virulences (36). We are currently
characterizing these P. striiformis f. sp. tritici isolates using
molecular markers, which will help us understand genetic
structures of the pathogen. In addition, this study will further
clarify whether similar races in different countries were due to
simultaneous evolution or migration. Migration of P. striiformis f.
sp. tritici has been reported within and among continents
(3,30,34,43,47).
Virulence to Yr5 and Yr15 were not detected in this study. This
result is consistent with previous reports of rare detection of the
virulences throughout the world. Yr5 was originally identified in
hexaploid Triticum spelta album. The gene confers resistance to
nearly all P. striiformis f. sp. tritici isolates worldwide. Virulence
to Yr5 has been reported only in India and Australia (27,47) but at
a very low frequency. Yr15 is from T. turgidum var. dicoccoides
(wild emmer) (12). Yr15 virulence was reported in Afghanistan and
Denmark; otherwise, lines with Yr15 are resistant to diverse P.
striiformis f. sp. tritici isolates from different geographical origins
(12,14,25). Thus, Yr5 and Yr15 still can be used in wheat-breeding
programs. However, use of the race-specific genes alone may not
provide long-lasting resistance. Therefore, effective race-specific
genes like Yr5 and Yr15 and race-non-specific genes should be
used in combination to achieve sustainable control of stripe rust.
In addition to the individual virulences and avirulences dis-
cussed above, we identified a large number of virulence patterns,
similar to races or pathotypes that are usually determined on a
relatively small number of selected host genotypes used as differ-
entials (4,8,20,36,47). With the 20 single Yr-gene lines, the 235
isolates were differentiated into 129 virulence patterns, while 169
patterns were identified using the 20 U.S. differentials. The U.S.
differentials identified more virulence patterns, as expected, be-
cause the 20 differential genotypes have at least 34 resistance
genes, more than the 20 genes in the single Yr-gene lines (Table 1).
The relatively large number of virulence patterns identified with
both sets of the single Yr-gene lines and the U.S. differentials is
expected considering the samples came from 13 countries. This
might also be attributed to the fact that collectors tended to send
diverse samples, which met our major objective of characterizing
different virulences and patterns rather than focusing on frequen-
cies. Regarding individual countries, the number of virulence pat-
terns ranged from 1 (Algeria) to 39 (China) based on reactions on
the 20 Yr-gene lines and 1 to 45 (Turkey) based on the U.S. differ-
entials. The numbers of virulence patterns are not comparable
among countries, because the numbers of isolates varied greatly by
country. However, the upper range of the virulence pattern num-
bers is similar to what we have found in the United States in recent
years (8). The virulence patterns based on both the Yr-gene lines
and the U.S. differentials were clustered into 11 VGs. These groups
share common virulences and avirulences within groups and have
distinctions between groups. The present study is to report the
maximum number of virulences and virulence patterns for people
to be aware of, which should be more useful for selecting effective
resistance genes and gene combinations in developing resistant
cultivars. Although the virulence patterns described in the present
study are not referred to as races, the virulence data generated
using the 20 Yr-gene lines, in comparison with the U.S. cultivar
differentials, may lead to the establishment of a standardized set of
Yr-gene differentials. More efforts are being undertaken in this
direction.
Acknowledgments
This research was supported by the United States Department of Agriculture–
Agricultural Research Service (project number 5348-22000-014-00D) and
Washington State University (project number 11W-3061-7824 and 13C-3061-
3925). We thank D. A. Johnson and T. D. Murray for critical review of the
manuscript.
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