Physiological races of Puccinia graminis f. sp. tritici in Iran and evaluation of seedling resistance to stem rust in Iranian wheat cultivars

Abstract

Seedling assessment of 13 stem rust samples collected from southwest of Iran revealed that three collections
were virulent for Sr31 and Sr38. Physiological races of RTRTC, HRCTC, RRTTF, TTPTC, TTTQF, JTHTC and
TTKSK were identified for nine collections tested against the north American differential lines. The virulence pattern
of TTKSK previously identified in east Africa was identical to that of TTKSK in the present study, providing
evidence for the migration of this race from East Africa to Iran. Low/ high infection type for the genes Sr22, Sr26,
Sr27, Sr29, Sr32, Sr33, Sr35, SrNin/ Sr7a, Sr8b, Sr9f, Sr12, Sr15, Sr16, Sr17, Sr18, Sr20, Sr23, Sr34, SrPL, SrTt3+10,
SrWld-1, and Sr42 was shown by nine collections. In evaluations of seedling resistance, high infection types of 3 to
4 were shown by all the 29 Iranian wheat cultivars tested with TTKSK. Presence of TTKSK, susceptibility of wheat
cultivars and conducive conditions pose serious threats of stem rust to wheat production in Iran.

Full text

110 ISSN (print): 0031-9465 www.fupress.com/pm
ISSN (online): 1593-2095 © Firenze University Press
Phytopathologia Mediterranea (2013) 52, 1, 110−122
Corresponding author: K. Nazari
Fax: +90 312 327 0798
E-mail: k.nazari@cgiar.org
RESEARCH PAPER
Physiological races of Puccinia graminis f. sp. tritici in Iran and
evaluation of seedling resistance to stem rust in Iranian wheat cultivars
Kumarse NAZARI 1 and masomeh MAFI 2
1 International Centre of Agricultural Research in the Dry Areas, P.O. Box 5466, Aleppo, Syria
2 Islamic Azad University, Science and Research Branch, Hesarak 1477893855, Tehran, Iran
Summary. Seedling assessment of 13 stem rust samples collected from southwest of Iran revealed that three collec-
tions were virulent for Sr31 and Sr38. Physiological races of RTRTC, HRCTC, RRTTF, TTPTC, TTTQF, JTHTC and
TTKSK were identied for nine collections tested against the north American dierential lines. The virulence pat-
tern of TTKSK previously identied in east Africa was identical to that of TTKSK in the present study, providing
evidence for the migration of this race from East Africa to Iran. Low/ high infection type for the genes Sr22, Sr26,
Sr27, Sr29, Sr32, Sr33, Sr35, SrNin/ Sr7a, Sr8b, Sr9f, Sr12, Sr15, Sr16, Sr17, Sr18, Sr20, Sr23, Sr34, SrPL, SrTt3+10,
SrWld-1, and Sr42 was shown by nine collections. In evaluations of seedling resistance, high infection types of 3 to
4 were shown by all the 29 Iranian wheat cultivars tested with TTKSK. Presence of TTKSK, susceptibility of wheat
cultivars and conducive conditions pose serious threats of stem rust to wheat production in Iran.
Key words: Puccinia graminis, physiological races, seedling resistance, Iranian wheat cultivars.
Introduction
Wheat (Triticum aestivum L. and T. durum L.) is the
most important crop in Iran. It is grown on approxi-
mately seven million ha with an annual production
of 14 million t. The three wheat rust diseases, stripe
rust, stem rust, and leaf rust, are the most impor-
tant constraints to wheat production in this country.
Stem (black) rust of wheat, caused by the biotrophic
fungus Puccinia graminis f. sp. tritici (Pgt), was once
the most devastating disease of wheat worldwide
(Pretorius et al., 2000; Singh et al., 2006). Severe crop
losses occur, particularly when susceptible cultivars
are grown in warm and humid areas (Roelfs et al.,
1992). The use of resistant cultivars and eradication
of the alternate host have brought stem rust epidem-
ics under control in almost all wheat-growing areas
of the world for more than four decades. In most of
the world, resistance to stem rust is based on a few
important resistance genes, including Sr31 (Preto-
rius et al., 2000, Singh et al., 2006), which was eec-
tive against Pgt populations worldwide. In 1998, a
severe wheat stem rust infection was observed on
wheat genotypes containing Sr31 in Uganda – this
Sr31-virulent race of Pgt is commonly known as
Ug99 (Pretorius et al., 2000). Subsequently, Ug99 was
designated as race TTKSK using the North Ameri-
can stem rust dierential set (Jin et al., 2007). Race
TTKSK was found in Kenya in 2004 (Jin and Singh,
2006; Wanyera et al., 2006), in Ethiopia in 2005 (Singh
et al., 2006), in Yemen and Sudan in 2006 (Singh et al.,
2008), and virulence for Sr31 was detected in Iran in
2007 (Nazari et al., 2009). This spread of Ug99 from
East Africa to the Middle East is in parallel to the sus-
pected migration pathway of the Yr9-virulent race of
the stripe rust pathogen P. striiformis f. sp. tritici (Pst)
during the 1980s (Singh et al., 2006). This race/race
group caused severe crop losses in all countries in its
pathway (Singh et al., 2004) including 2.5 million t of
grain loss of wheat during 1992–1994 in Iran (Torabi

111
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
et al., 1995). It was predicted that Ug99 would follow
the migration pathway from East Africa throughout
Asia according to the historical step-wise movement
of the Yr9-virulence race/race group of Pst in the
1980s (Saari and Prescott, 1985; Stubbs, 1988; Singh
et al., 2006). The wheat-growing areas in Iran are pri-
mary risk areas for Ug99 and may serve as a patho-
gen bridge between East Africa and South Asia.
Since the rst documentation of wheat stem rust
in Iran in 1939 (Esfandiari, 1946), several devastating
epidemics have occurred in major wheat produc-
tion areas, particularly in the southern and northern
humid warm zones (Esfandiari, 1946; Bamdadian,
1971; Scharif et al., 1971; Khazra and Bamdadian,
1974; Bamdadian and Torabi, 1978). Before the intro-
duction of semi-dwarf wheat genotypes from the In-
ternational Maize and Wheat Improvement Centre
(CIMMYT) to Iran in the 1970s, almost all local vari-
eties were susceptible to stem rust. In the years since,
the disease has been under control, with occurrence
reduced to occasional infections on local varieties.
Similar to those in other parts of the world, most
current Iranian cultivars originated from CIMMYT
and possess the 1B.1R translocation carrying Sr31
(McIntosh et al., 1995; Pretorius et al., 2000; Singh et
al., 2006). The frequency of the 1B.1R translocation
in CIMMYT germplasm was once greater than 70%
(Singh et al., 2006).
Stem rust has not been a major problem in wheat
production in Iran in recent decades and therefore
pathogenicity of the Pgt population has not been
studied; there is thus a paucity of information on the
likely evolution of the Pgt population in Iran dur-
ing the last four decades. Little is known about the
pathogenic variability of Pgt in Iran. Using the inter-
national stem rust race analysis system (Stakman et
al., 1962), ten physiological races of Pgt were report-
ed by Scherif and coworkers in 1970 (Scharif et al.,
1971). Using the international stem rust race analysis
system (Stakman et al., 1962), ten physiological races
of Pgt (21, 34, 40, 75, 100, 194, 213, 226, 320, and 321)
were reported in Iran in 1970 (Scharif et al., 1971).
Nasrollahi et al., (2001) reported very unusual viru-
lence combinations for Sr24, Sr25, Sr26, Sr28, Sr29,
Sr31, Sr32, Sr36, and Sr38 from 20 Pgt collections ob-
tained during 1996-99.
Field evaluations of Iranian wheat cultivars and
advanced breeding lines to Ug99 in Kenya in 2006
and 2007 showed that more than 95% of the common
wheat varieties and advanced breeding lines were
susceptible to stem rust race TTKSK (Ug99), indicat-
ing the potential threat of this race to wheat produc-
tion in Iran. The objectives of present study were
to (1) obtain detailed characterization of the physi-
ological specialization of an unusual Pgt population
in wheat growing areas in southwest of Iran in 2007
(Nazari et al., 2009) and (2) assess the vulnerability of
Iranian wheat varieties and advanced breeding lines
to Iranian races of Pgt.
Materials and methods
Sample collection, isolation, and spore multiplication
A eld survey was conducted during late June
2007 in wheat growing areas in southern Iran. The
survey was conducted over 800 km in the upper
Karkheh basin, including Poldokhtar, Khorram
Abad, Boroujerd, Malayer and Hamadan. Eleven
samples were collected from agricultural research
stations and commercial elds (Table 1). Samples
were air-dried at room temperature for at least 24 h
and then stored at 4°C. The susceptible wheat cul-
tivar Morocco was planted as eight seeds per 9 cm
diam. pot lled with potting mix. Seedlings were
grown in a greenhouse at 20°C with 16 h supple-
mentary light using high-pressure sodium lighting.
To retard plant growth and encourage spore produc-
tion, seedlings were treated with 40 mL of 0.25 gL-1
maleic hydrazide acid (C4H4N2O2; Sigma-Aldrich®,
Taufkrichen, Germany) per pot at 1 cm coleoptile
length emergence. When the rst leaves of suscepti-
ble plants were fully expanded, infected stems were
washed under tap water and then placed in a dew
chamber at room temperature for 4 h. Fresh uredini-
ospores were scraped from re-sporulated single pus-
tules using a sterile spatula and transferred to 7- to
9- day- old leaves of cv. Morocco plants. Inoculated
seedlings were incubated in a sealed dew chamber
for 24 h at 20° C and 90% relative humidity (R.H.).
Plants were then placed in greenhouse bench at 20
± 2° C and 16 h light. At 14 days post inoculation,
urediniospores were collected and dried in a con-
tainer with silica gel at 4°C for 48 h and then stored
in an ultra-low freezer at -80°C.
Conrmation of virulence for Sr31
Since some of the samples were collected from
genotypes with Yr9 (also carrying Sr31) in Borou-

Phytopathologia Mediterranea
112
K. Nazari and M. Mafi
jerd and Hamadan, and showed highly compatible
infection responses, a small set, “Quickset”, of dif-
ferential lines was used to quickly assay for viru-
lence to Sr31 (Table 2). These lines included Line
E/ Kavkaz (Sr31), Clement (Sr31), Federation *4/
Kavkaz (Sr31), Kavkaz (Sr31), Mildress (Sr31), Mar-
Table 1. Isolate code, site and year of collection, name of host cultivar for 15 Puccinia graminis f. sp. tritici collections.
Pgt-Code Location Province Year Host Cultivar
SR10 Boroujerd Lorestan 1997 Bread wheat unknown
SRI2 Karaj Alborz 1997 Bread wheat unknown
86-11 Karaj Alborz 2007 Bread wheat Bolani
86-20 Poldokhtar Lorestan 2007 Bread wheat unknown
86-28 Kelardasht Mazandaran 2007 Bread wheat unknown
86-29 Kelardasht Mazandaran 2006 Barley Fasih
86-31 Boroujerd Lorestan 2007 Bread wheat Aristocrat
86-33 Boroujerd Lorestan 2007 Barley unknown
86-35 Boroujerd Lorestan 2007 Bread wheat Banks
86-42 Hamadan Lorestan 2007 Bread wheat TP 67
86-43 Hamadan Hamadan 2007 Bread wheat TP 55
86-47 Hamadan Hamadan 2007 Bread wheat Clement
86-48 Hamadan Lorestan 2007 Bread wheat TP 10
86-55 Atashgah Hamadan 2007 Bread wheat unknown
86-58 Boroujerd Lorestan 2007 Bread wheat unknown
Table 2. Seedling infection types of wheat lines in the ‘Quickset’ used to assay the eectiveness of Sr31 to 13 Puccinia
graminis f. sp. tritici collections.
No. Name/
pedigree
Sr
gene/s
Pgt
SR10
Pgt
SRI2
Pgt
86-11
Pgt
86-20
Pgt
86-28
Pgt
86-29
Pgt
86-31
Pgt
86-33
Pgt
86-35
Pgt
86-42
Pgt
86-48
Pgt
86-55
Pgt
86-58
1 Line E/
Kavkaz
Sr31 ;C1= a;1= ;C1= ;C1- ;C1- ;C1= 3+4 1C ;C1= 1-C 1 4 3+
2 Clement Sr31 12- ;C 1- 2= ;C1= 1-C 4 ;C ;C1= ;C1= ;C1= 4 33+
3 Federation*4/
Kavkaz
Sr31 ;C1= 0; 12= 12= ;C1- ;C1- 4 ;1= 1CN ; 1C 4 33+
4 Kavkaz Sr31 ;C1= ; ;C1= 12= 12= 1C 4 ; ;C1= 2- 2 4 33+
5 Mildress Sr31 ;C1= ;1= 1C 12- 12= 0;1- 3+ 2 12= 12= 12- 4 3+
6 BtSr24 Sr24 1C ;C1= 1-2- 1-2= 2 1- 12= ;C1= 2- 1 11- ;1= 1-C
7 Agent Sr24 ;C1= 1-C 12-
CN
;C1= ;C1= ;C1= ;1= ;C1= ;C1= 2 1C ;1= ;1=
a Infection types were recorded according to ; (eck), and 0- to - 4. Symbols “–” and “+” were used to describe deviation from the pustule
size of major infection type classes. C and N were used to describe extensive chlorosis and necrosis, respectively, associated with infec-
tion types and X was used for mesothetic infection types on same genotype.

113
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
ton Vásár 17 (Sr31), BtSr24 (Sr24), Trident (Sr38),
and Iranian commercial cultivars known to carry
1B.1R translocations: Falat (Seri 82; Sr31, Sr2) and
Shiroudi (Attila 4Y; Sr31). Morocco, Federation, and
Local Red were used as susceptible checks in this
test (Table 2). Two Pgt collections obtained in 1997
were recovered from -80° C storage from the Cereal
Pathology Unit at the Seed and Plant Improvement
Institute (SPII), Karaj, and were included for further
comparisons. According to Nasrollahi et al., (2001),
Pgt SR10 was avirulent on Sr31, and Pgt SR12 was
avirulent on this gene.
Urediniospores from the long-term storage at
-80°C were heat shocked at 42°C for 4 min and then sus-
pended in distilled water (DW) with 1 mL Tween 20®.
Seedling leaves of the “QuickSet” genotypes were
inoculated with the urediniospore suspensions us-
ing a small inoculator at 20 kPa pressure. Inoculated
seedlings were incubated in dew chamber at 18°C in
the dark for 20 h followed by 4 h at 20°C and uores-
cent light. Plants were then placed in a greenhouse at
18-20°C with 16 h of supplementary light. Seedling
infection types (ITs) were recorded 14 d after inoc-
ulation using the 0 – 4 scale described by Stakman
et al., (1962) (McIntosh et al., 1995). ITs of 0–2 were
considered low (i.e. LITs), indicating host resistance
and pathogen avirulence; ITs of 3–4 were considered
high (i.e. HITs).
Race analyses and virulence phenotyping
The physiological races of seven Pgt collections
(Table 1) obtained from Iran in 2007 and the two Pgt
collections obtained in 1997 were determined using
the North American stem rust dierential set (Jin et
al., 2008, Table 3). The nine races were also used in
seedling assessments of additional sources of gene
combinations (Table 4). In addition to the stem rust
resistance genes assayed in the North American race
analysis system, the same nine Pgt-collections were
used in seedling assessments of an expanded set of
stem rust monogenic lines and selected sources of
Sr-genes from the Australian stem rust dierential
set (McIntosh et al., 1995; Park and Wellings, 1992;
Zwer et al., 1992; Table 5). Expected LITs for individ-
ual genes are presented in the rst column of Table 5.
ITs equal to or lower than the expected LITs for each
Sr gene were considered as LITs, and ITs higher than
the expected LITs or equal to the susceptible checks
were considered as HITs.
Assessment of seedling resistance of Iranian varieties
to stem rust
Twenty-nine Iranian wheat varieties were
screened with four stem rust collections including
two Sr31-virulent Pgt races (Table 6). The cultivar Mo-
rocco was used as the susceptible control. Resistance
assessments were carried out under the same condi-
tions described for race analyses. To determine rela-
tionships among cultivars based upon seedling reac-
tions to the four collections, unweighted pair-group
average linkage Agglomerative Hierarchical Cluster-
ing (AHC) was used for the Jaccard's dissimilarity
coecient of converted low and high seedling ITs
to binary data using XLSTAT software ver. 2011.2.08
(XLSTAT, Addinsoft. http://www.xlstat.com).
Results and discussion
Stem rust occurrence
During the eld survey in mid-June 2007, a severe
stem rust epidemic was observed in experimental
plots in Boroujerd and Hamadan Research Stations
and commercial elds, particularly on the Silakhor pla-
teau in southern Boroujerd. Late stem rust infections
in Lorestan and Hamadan Provinces in Iran (upper
Karkheh basin) were considered unusual, particularly
because stem rust had not been previously recorded in
the Hamadan area where winter wheat cultivars are
grown. Additional surveys in other wheat-growing
areas were conducted and occasional stem rust infec-
tions were recorded. There were high levels of infec-
tion on wheat genotypes known to carry the 1B.1R
chromosome translocation that were included in the
Iranian Yellow Rust Trap Nursery planted in experi-
mental plots in Boroujerd and Hamadan Research Sta-
tions. A range of susceptible ITs with 30–80% severity
were recorded in some commercial elds in Boroujerd.
Conrmation of virulence for Sr31
When the ‘QuickSet’ was inoculated with the 13
Pgt collections, Pgt 86-31 collected from winter wheat
cultivar Aristocrat, Pgt 86-55 and Pgt 86-58 collected
from bread wheat varieties planted within the yel-
low rust trap nurseries in Boroujerd and Hamadan
research stations, respectively, showed HITs of 33+
to 4 on dierential genotypes carrying Sr31 (Line
E/Kavkaz, Clement, Federation*4/Kavkaz, Kavkaz
and Mildress). This indicated presence of virulence

Phytopathologia Mediterranea
114
K. Nazari and M. Mafi
Table 3. Seedling infection types produced by nine Puccinia graminis f. sp. tritici collections on the North American set of dierential lines and race designa-
tion according to letter code race nomenclature system.
Set Line Sr gene Expected
low IT Pgt SR10 Pgt SRI2 Pgt 86-11 Pgt 86-20 Pgt 86-28 Pgt 86-29 Pgt 86-33 Pgt 86-31 Pgt 86-55
I ISr5-Ra Sr5 0, 0; a33+ 0; 33+ 33+ 3+ 33+ 0; 3+ 3+
CnS_T.
monococcum deriv
Sr21 1, 2- 33+ 33+ 2++ 2++3 3 33+ 3+ 3+ 33+
Vernstine Sr9e ;1+ ;C1- 1- 1C-2-C 4 2+ 1C-2-C 4 3+4 4
ISr7b-Ra Sr7b 2 3+ 3+4 3+4 4 3+ 3+ 2- 4 4
II ISr11-Ra Sr11 ;2-, 2+3- 4 3+ 3+4 4 3/3+ 3+ 3+4 4 4
ISr6-Ra Sr6 0; 33+ 3+4 33+ 4 4 3+ 4 4 4
ISr8a-Ra Sr8a 2 33+ 11C 11C 4 3+4 1C 2+/3+ 3+ 4
CnSr9g Sr9g 2- 4 4 4 4 3+ 4 4 4 4
III W2691SrTt-1 Sr36 0, 0;, X 33+ 0; 4 3+ 33+ 3+ 0;1= 0;1 0;
W2691Sr9b Sr9b 22+ 33+ ;C1- 4 1+ 33+ 3+4 4 3+4 4
BtSr30Wst Sr30 2 2 1C 3+ 33+ 33+ 2++3 12- 33+ 4
Combination VII Sr13Sr17 0, ;1 33+ 22+ 22+ 4 22+ 22+ 22+ 3 3
IV ISr9a-Ra Sr9a 2-, 23 33+ 4 4 4 3+4 33+ 4 4 4
ISr9d-Ra Sr9d ;2- 4 3+4 4 4 4 4 4 3+4 4
W2691Sr10 Sr10 ;1+ 33+ 33+ 4 4 11+ 33+ 2++ 4 4
CnsSrTmp SrTmp 2- 22+ 22+3 2+3 2+3 12= 2+3 23 2- 2-
V LcSr24Ag Sr24 2 1C ;C1= 1+2- 1+2-C 2 1+ ;C1= 12-C ;C1=
Sr31/6*LMPG Sr31 ;1+ ;C1= ;1= ;C1= ;C1- ;C1- ;C1= 1C 3+4 4
Trident Sr38 1 1C2= 1CN 2+ ;CN1= 22+ 22+ 1-C 33+ 2++/33+
McNair 701 SrMcN ;1 4 4 4 4 33+ 4 4 4 4
Race RTRTC HRCTC RRTTF TTPTC TTTQF RRTTF JTHTC TTKSK TTKSK
a Infection types were recorded according to ; (eck), and 0- to - 4. Symbols “–” and “+” were used to describe deviation from the pustule size of major infection types classes.
C and N were used to describe extensive chlorosis and necrosis, respectively, associated with infection type and X was used for mesothetic infection types on same genotype.
Recorded range of infection types were separated by comma (,).

115
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
to Sr31 in these collections (Table 2). HITs of 3+ to 4
on the wheat commercial varieties Falat (#Seri 82),
Shiroudi (CIMMYT name Attila 4Y and Indian name
PBW343) and MV17, all carrying the 1BL.1RS trans-
location, further conrmed virulence for Sr31 in Pgt
86-31, Pgt 86-55 and Pgt 86-58.
The other 11 Pgt collections showed LITs of ;C1=
to 22– on Sr31 dierential lines and varieties with
1BL.1RS, indicating avirulence for Sr31. LITs of ; to
2 on Sr24 were produced on dierential line BtSr24
and Agent when tested against the 13 collections,
indicating that all Pgt collections were avirulent for
Sr24. Trident was used as a source of Sr38. Except
for the three Sr31 virulent Pgt collections (Pgt 86-31,
Pgt 86-55 and Pgt 86-58) which were also virulent to
Sr38, the other 10 collections showed LITs of 1CN
to X on Trident, indicating avirulence for Sr38. The
three susceptible varieties Federation, Morocco and
Local Red were susceptible to all collections.
Determination of physiological races and virulence
spectra
According to the revised North American race
nomenclature system (Jin et al., 2008), the two col-
lections from Boroujerd and Karaj obtained in 1997
were assigned thus; Pgt SR10 as RTRTC and Pgt
SR12 as HRCTC.
Collection Pgt 86-11 was obtained from a local
susceptible variety Bolani used as a rust spreader
in a disease screening nursery planted at an experi-
mental eld at SPII. This experiment was planted
for leaf rust resistance screening and was intended
to be inoculated with a leaf rust collection. Unex-
pected severe stem rust infections occurred on those
nurseries that were inoculated with leaf rust. Since
Pgt 86-29 was collected from the spreader rows in-
oculated with leaf rust, and stem rust had not been
observed at this station for a minimum of 15 years
(K. Nazari, personal observations), we suggest that
Pgt 86-11 is a result of greenhouse contamination of
the leaf rust collection used in eld inoculation with
Pgt 86-29. High stem rust contamination of the same
leaf rust collection preserved in a cereal pathology
laboratory was conrmed when tested on the North
American dierential set. In addition, the virulence
spectrum of Pgt 86-29 was identical to the Pgt 86-
11 collection obtained from barley cultivar Fasih in
Kelardasht in 2006. The second sample collected
from bread wheat in Kelardasht (Pgt 86-28) was des-
ignated as race TTTQF.
Collection Pgt 86-20 was designated as race TT-
PTC and was originally collected from a bread
wheat variety in southwest Poldokhtar. Collections
originally obtained from Boroujerd in 2007, Pgt 86-31
and Pgt 86-33, were designated as races TTKSK and
Table 4. Seedling infection type of nine Puccinia graminis f. sp. tritici collections on additional sources of stem rust resistance
genes.
No. Genotype Sr- gene Pgt
SR10
Pgt
SRI2
Pgt
86-11
Pgt
86-20
Pgt
86-28
Pgt
86-29
Pgt
86-33
Pgt
86-31
Pgt
86-55
1 Sage Sr24 12= a;N1= 1= ;N1= ;C1= ;1= 1= 12- 12-
2 Custer Sr31 2- 2= 2- 1= 1-CN 1= 1- 3-4 3-4
3 Siouxland Sr24,Sr31 ;C1= ;N1= ;N1= ;N1= ;N1= ;N1= ;N1= 12- 12-C
4 TAM 107 Sr1RS-Am 1C2- 12= 1= 12- 12- 12- 2= 2- 12-
5 Amigo Sr24, Sr1RS-Am 12- 12- 12- ;C1= 12= ;N1= ;N1= 1= 11-
6 Fleming Sr6,Sr24,Sr36,Sr1RS-Am ;C1= ;N1= ;N1= 0; 12= ;N1= 1= ;C1= ;C1=
7 Sisson Sr6,Sr31,Sr36 ; 1= ;N1= 0; 12= 12= 1=N 1-C ;;
8 McNair 701 SrMcN 444443+444
9 Red Chief - 4 4 4 4 4 4 4 4 4
a Infection types were recorded according to ; (eck), and 0- to - 4. Symbols “–” and “+” were used to describe deviation from the pustule
size of major infection types classes. C and N were used to describe extensive chlorosis and necrosis, respectively, associated with infection
type and X was used for mesothetic infection types on same genotype. Recorded range of infection types were separated by comma (,).

Phytopathologia Mediterranea
116
K. Nazari and M. Mafi
JTHTC, respectively. Race TTKSK was also designat-
ed for Pgt 86-55 collected from Hamadan.
The nine collections were also used in seedling as-
sessments of an expanded set of dierentials includ-
ing Sr24, Sr31, Sr1RS-Am and gene combinations of
Sr24-Sr1RS-Am, Sr24-Sr31, Sr6-Sr24-Sr36-Sr1RS-Am
and Sr6-Sr31-Sr36 present in cultivars Sage, Cruse,
Tam107, Amigo, Siouxland, Fleming and Sission, re-
spectively (Table 4). McNair 701 and Red Chief were
used as susceptible checks in this test. Custer (Sr31)
was only susceptible to the two Sr31-virulent races.
Seedling ITs of ;N1= to 2- for Sage, Tam107, Amigo,
Siouxland and Fleming indicated that all nine races
were avirulent on Sr24 and Sr1RS-Am when pre-
sented singly in Sage and Tam107, respectively, or in
gene combination in Amigo (Sr24-Sr1RS-Am), and
also in combinations with other Sr-genes in Sioux-
land (Sr24-Sr31) and Fleming (Sr6-Sr24-Sr31-Sr1RS-
Am). The Sr6-Sr31-Sr36 gene combination in Sisson
was eective against the nine races. Eectiveness
of Sisson against races RTRTC, RRTTF, TTPTC and
TTTQF was due to avirulence to Sr31, whereas ef-
Table 5. Expected low infection types (LITs) of stem rust resistance gene and reaction of stem rust dierential lines when
inoculated with nine Puccinia graminis f. sp. tritici collections
Entry
No. Name/pedigree Sr gene/s Expected
LIT
Pgt
SR10
Pgt
SRI2
Pgt
86-11
Pgt
86-
20
Pgt
86-
28
Pgt
86-
29
Pgt
86-33
Pgt
86-
31
Pgt
86-
55
Eective Sr-genes
1 SWSR22T.B. Sr22 1+ to 2- a2- ;N1= 1- 11+C 1-C 1 ;1= 0; ;1=
2 Kite Sr26 1 1 1 1 1 12-C 0; 2 ;1= 1
3 Eagle Sr26+Sr9g 0; to 2- 11+2 ;N1= 1- 1- ;1- 1 ;1= 1 ;1-
4 Coorong Sr27 0; ; 0; ;1= 1= 12- ;1= ; 1= ;
5 Pusa/Edch Sr29 2- 1 ;1= 1+2 2 2- 1+2 1 11+2-
C
2
6 C77.19 Sr32 1+ to 2C 11+2 ;1= 1 11+ 11- 11+2- 1-N 2- 1-
7 Tetra Canthatch/
Ag. squarrosa
Sr33 2 2 1 12-CN 1 ;1= 1C ;1=N 12 11-C
8 W3763 Sr35
(SrTm1)
0; to ; 0; 0; 0; 0; 0; 0; 0; 0; 0
9 Ningadhu SrNin ;1= 0; ;C1= ;; ;C1= ;C1= 0; ;1= 0 ;1=
Ineective Sr-genes
1 LINE G Sr7a 1 to 3C 3+ 33+ 33+/3+ 4 3+ 3+ 3+ 3+4 4
2 Barleta Benvenuto Sr8b X=4 3+4 33+ 4 3+ 3+ 33+ 3+4 4
3 ISR5SB Sr9f 2 3+4 4 4 4 3+4 4 4 4 4
4 CH.SP.(TC3B) Sr12 ; to X 4 33+/3+ 33+ 4 3+ 3+ 2++ 4 4
5 W2691SR15NK Sr15 ; to X 4 33+ 33+ 4 3 3+ 3+4 33+ 4
6 Norka Sr15 4 33+ 4 4 3+ 3+ 4 4 4
7 ISR16RA Sr16 2 33+ 2++3 2+3+ 4 3/3+4 33+ 2++3/3 3+4 33+
8 LC/Kenya Hunter Sr17 ;1 33+ 22+ 22+ 4 22+ 2+ 22+ 3+4 4
a Infection types were recorded according to ; (eck), and 0- to - 4. Symbols “–” and “+” were used to describe deviation from the pustule
size of major infection types classes. C and N were used to describe extensive chlorosis and necrosis, respectively, associated with infection
type and X was used for mesothetic infection types on same genotype. Recorded range of infection types were separated by comma (,).

117
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
Table 6. Name, pedigree, year of release, country of origin and growth habit of 29 Iranian wheat cultivars evaluated for
seedling resistance to four Puccinia graminis f. sp. tritici collections at seedling stage.
Name Pedigree
Cross number and selection history
Year of
release
Growth
habit
Pgt
SR10
Pgt
86-20
Pgt
86-31
Pgt
86-55
Moghan 1 LR/N10B//3*ANE
II8739-4R-1M-1R-0IRN
1974 Spring 1C a;C1=3 4
Moghan 2 LR64A/HUAR
‘II15929-1M-4R-2M-0IND-0IRN
1974 Spring 1=;C1=4 4
Sabalan 908//FN/A12/3/1-32-4382
-0IRN
1981 Facultative 1C ; 3 4
MV17 [Slaviya × (Krasnodari 1 × Bezostaya)] × Zg.4431
Marton Vasar, Hungary
1987 Winter 2- ;1=3 3
Ghods RSH/5/WT/4/N10/K 54*2//FN/3/PTR/6/OMI//KAL/
BB
-0IRN
1988 Spring ;N1=1C 4 4
Falat KVZ/BUHO//KAL/BB (SERI 82) = VEERY 5
CM33027-F-15M-500Y-0M-87B-0Y-0IRN
1990 Spring X-22-4 4
Hirmand BYT/5/JAR/3/CFN//CNO/SR/4/JUP
-0ZBL
1992 Spring X=1–2 4 4
Shiroudi ND/VG9144//KAL/BB/3/YACO/4/VEE#5
CM85836-4Y-0M-0Y-8M-0Y-0PZ-0IRN
1999 Spring 2–244
Atrak JUP/BJY//URES
CM67458-4Y-1M-3Y-1M-3Y-0B-0K
1995 Spring 4 4 4 3
Alamout KVZ/TI71/3/MAYA’S’//BB/INIA/4/KARAJ2/5/
ANZA/3/PI/NDR//HYS
0K
1995 Winter X–2–4 4
Tajan BOW/NKT
CM67428-6M-1Y-05M-3Y-0B-0K
1995 Spring 4 2=4 4
Niknejad F134.71/CROW
SWM11147-1AP-2AP-4AP-1AP-0AP-0MRGH
1995 Spring 33–344
Mahdavi TI/PCH/5/MT48/3/WTE*3//NAR59/TOTA/4/MUS
-0K
1995 Spring ;C1=1C 4 4
Zarin NAI60/HN7//BUC/3/F59.71/GHK
SWO791095-0MDB
1995 Facultative 4 2-4 4
Darab 2 MAYA/NAC
CM39424-1Y-1M-4Y-1M-1Y-1M-0Y-0K
1995 Spring 0;, 33-4 4
Alvand 1-27-6275/CF 1770
0K
1995 Facultative X-33-4 3
Chamran ND/VG9144//KAL/BB/3/YACO/4/VEE#5
CM85836-50Y-0M-0Y-3M-0Y-0IRN
1997 Spring X=3–4 4
Kavir STM/3/KAL//V534/JIT716
-0IRN
1997 Spring X=23–4 4
Marvdasht HD2172/AZADI
-0SHZ
1999 Spring 4 22–4 4
(Continued)

Phytopathologia Mediterranea
118
K. Nazari and M. Mafi
fectiveness against races HRCTC and JTHTC was
due to avirulence to Sr31 and Sr36, and eectiveness
against the two TTKSK collections was due to aviru-
lence to Sr36.
Virulence spectra and eectiveness of Sr-genes
LITs of 0; to 22+ were produced by Sr22, Sr24,
Sr26+9g, Sr27, Sr29, Sr32, Sr33, Sr35 (SrTm1) and
SrNin when tested against the nine Pgt collections.
This indicates eectiveness of these genes against all
Pgt collections. Since HITs of 3+ to 4 were recorded
on the Sr9g monogenic line in Chinese Spring back-
ground for all collections tested, the LITs of 0; to 11+2
produced by Eagle against the nine collections are
considered as indication of avirulence conferred by
Sr26 not Sr9g. In addition to HITs across all collec-
tions for Sr6, Sr9a, Sr9d, Sr9g, Sr11 and SrMcN pre-
sent in the North American dierential lines (Table
3), HITs (susceptible) of 3 to 4 were produced by all
collections when tested on Sr7a, Sr8b, Sr9f, Sr12, Sr15,
Sr16, Sr17, Sr18, Sr20, Sr23, Sr34, SrPL, SrTt3+10, Sr-
Wld1 and Sr42 (Norin 40). The nine collections pro-
duced either HITs or LITs on Sr14, Sr19, Sr21, Sr28,
Sr36, Sr44 and Srdp2 (Table 5).
Race TTKSK and its virulence spectrum
Race TTKSK (syn. Ug99) and related races have
been extensively studied since their rst detection in
Uganda (Pretorius et al., 2000; Wanyera et al., 2006;
Singh et al., 2006; Jin et al., 2007; 2008; 2009). TTKSK
Name Pedigree
Cross number and selection history
Year of
release
Growth
habit
Pgt
SR10
Pgt
86-20
Pgt
86-31
Pgt
86-55
Shahryar KVZ/TI//MAYA/26591-1T-7M-OY-115Y-
OM/3/1-44-21863/4/ANZA/3/PI/NAR59//HYS
-0IRN
2002 Winter 3–2=44
Toos SPN/MCD//CAM/3/NZR
-17H-4H-1H-0H-0IRN
2002 Facultative 4 2=44
Shiraz GV/D6301//ALD/3/AZADI
-0IRN
2002 Spring 3–X=44
Dez KAUZ*2/OPATA//KAUZ
CRG737-1Y-010M-0Y-0IRN
2002 Spring 2=22=44
Arta HD2206/Hork//Bul/6/CMH80A.253/2/M2A/
CML//Ald/3/Ald*4/5/BH1146/H56.71//BH1146/3/
CMH78.390/4/Seri/7/Hel/3*Cno79//2*Seri 82
0IRN
2005 Spring 3-;C1–44
Moghan 3 Luan/3/V763.23/V879.C8//PVN/4/Picus/5/Opata
-0IRN
2005 Spring 2–0;1 4 4
Darya Sha4/Chil
-0IRN
2005 Spring 3 1-C 4 4
Bam VEE#5/NAC//1-66-22
-0K
2006 Spring 12-1C 4 4
Akbari 1-63-31-/3/12300/Tob//Cno/Sx
-0IRN
2006 Spring 2=444
Desprez
Gascogne
TJB 9908 / Marengo - Winter 3 2=44
Morocco -- Spring 4 4 4 4
a Infection types were recorded according to ; (eck), and 0- to - 4. Symbols “–” and “+” were used to describe deviation from the pustule
size of major infection types classes. C and N were used to describe extensive chlorosis and necrosis, respectively, associated with infection
type and X was used for mesothetic infection types on same genotype. Recorded range of infection types were separated by comma (,).
Table 6. Continues.

119
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
(Ug99) was the rst characterized race of Pgt with
virulence to gene Sr31 (Pretorius et al., 2000). Using
a set of 16 stem rust monogenic lines of the North
American nomenclature system (Roelfs and Martens,
1988), Wanyera et al., (2006) designated Ug99 as race
TTKS and it was redesignated as TTKSK when Sr31,
Sr24, Sr38 and SrMcN were added as a fth set to the
North American dierential set (Jin et al., 2008).
In addition to Sr31, Ug99 carries a striking com-
bination of virulence for important stem rust resist-
ance genes from hexaploid and tetraploid origins
which have been extensively used in agriculture
(Singh et al., 2006). Stem rust samples collected from
Kenya in 2004 were found to be identical to the origi-
nal Ug99 when tested for virulence phenotype us-
ing the 16-line North American dierential system
(Wanyera et al., 2006). The original Ug99 collected
from Uganda in 1988 was determined for virulence
for Sr5, Sr6, Sr7b, Sr8a, Sr8b, Sr9b, Sr9e, Sr9g, Sr11,
Sr15, Sr17, Sr30, Sr31 and Sr38 and avirulence for
Sr21, Sr22, Sr24, Sr25, Sr26, Sr27, Sr29, Sr32, Sr33,
Sr34, Sr35, Sr36, Sr39, Sr40, Sr42, Sr43, SrAgi and
SrEm (Pretorius et al., 2000). The Kenyan Ug99 col-
lections were virulent on a gene present in Waldorn
(SrWld-1) (Wanyera et al., 2006), an important gene
for stem rust resistance in North American hard red
spring wheat varieties (Leonard, 2001; Leonard and
Szabo, 2005). In addition to the abovementioned
genes, the Ug99 races from Kenya were also aviru-
lent for SrTmp, Sr13, Sr37 and Sr44 derived from
Triumph 64 (Roelfs and McVey, 1979), T. timopheevii
(McIntosh, 1988), T. turgidum L. var. dicoccum culti-
var Kaphli (Knott, 1962) and Thinopyrum intermedium
(Friebe et al., 1996), respectively. Stem rust resistance
gene Sr21 was initially reported as an eective gene
against Ug99 (Pretorius et al., 2000) but compatible
reaction with an IT of 3 was recorded on diploid and
hexaploid sources of Sr21 (Einkorn and CnSSr21Tm)
when Kenyan collections were tested for virulence
(Wanyera et al., 2006). Einkorn showed LITs of X+
and ;1= to TTKSK races from Boroujerd and Ham-
adan, respectively, while an IT of 3+ was observed
when the same races when CnS-T. monococcum was
used as the source of Sr21 in the North American
dierential set. The virulence pattern of the Ug99
collections collected from Uganda and Kenya were
identical to those of the two TTKSK races identied
in the present study. Use of an expanded set of des-
ignated Sr-genes revealed that the two TTKSK races
from southwest Iran produced HITs on Line G (Sr7a),
Barleta Benvenuto (Sr8b), ISR5SB (Sr9f), CH.SP.TC3B
(Sr12), W2691SR15NK and Norka (Sr15), LC/Kenya
Hunter (Sr17), LCSR18PL (Sr18), LCSR20MG (Sr20),
Exchange (Sr23), Compair (Sr34), W2691SRTt2
(Sr37), Peliss (SrPL), Fed.*2/SrTt3 (SrTt3+Sr10),
Baart/Waldorn (SrWld 1) and Norin 40 (Sr42). These
two races showed LITs for Sr1RS-Am present in TAM
107, Amigo and Fleming; SrNin in Ningadhu; and
SrAgi in Taf 2.
Evaluation of seedling resistance to Ug99
Using AHC analysis, the 30 varieties (Table 6) were
classied into two major resistance groups at 33.3%
and 25% of Jaccard’s coecient of dissimilarity com-
prising 26 (87%) and four (13%) varieties, respectively
(Figure 1). At 25% dissimilarity the two clusters were
divided into four sub-clusters (resistance groups).
The major sub-cluster comprises 19 varieties (63%)
because of their LIT to the two Sr31-avirulent col-
lections (Pgt SR10 and Pgt 86-20) and HIT to the two
TTKSK races (Pgt 86-31 and Pgt 86-55). Known varie-
ties for 1B.1RS translocation, Falat (Seri 82), Shiroudi
(Attila 4Y) and MV17 were clustered in this group.
The second sub-cluster was formed by Alamout, Ta-
jan, Marvedasht, Toos, Darya, and Gascogne. These
four varieties showed LIT to Pgt 86-20 while HIT
was recorded against the other three Pgt collections
including the two Sr31 virulent races. Niknejad and
Atrak, and Morocco and Akbari were classied into
sub-cluster 3 and 4, respectively. The sub-cluster 4 is
representative of the two cultivars without eective
genes against the four Pgt collections, while the two
cultivars in sub-cluster 3 were resistant to Pgt SR10
(Figure 1). The identity of resistance gene/genes in
wheat varieties conferring resistance to Pgt SR10 and
Pgt 86-2010 in sub-clusters 2 and 3 is unknown.
In conclusion, the TTKSK races had identical
virulence phenotypes to the virulence phenotypes of
the TTKSK races identied from Kenya and Uganda,
indicating that the race TTKSK in Iran belongs to the
same Ug99 lineage that likely migrated from Yemen
to Iran in 2007 (Nazari et al., 2009). Given the regu-
lar north-easterly airows out of Yemen (Singh et al.,
2006; Singh et al., 2008), and the relative proximity
of Yemen compared to other countries where race
TTKSK has been conrmed, it is possible that race
TTKSK spread from Yemen to south-western Iran.
According to the predicted Ug99 migration
pathway (Singh et al., 2006; Singh et al., 2008) based

Phytopathologia Mediterranea
120
K. Nazari and M. Mafi
on the recorded west-east migration pathway of
Yr9-virulent Pst races during the 1980s, the wheat-
growing areas in southern Iran were expected to be
more vulnerable to Ug99 incursion than the south-
western areas. Southern areas in Iran are drier and
warmer than south-western areas, and wheat varie-
ties with early maturity are grown to avoid terminal
heat-stress late in the season. The cultivars Chamran
(CIMMYT name Atilla 50Y) and Dez are the pre-
dominant wheat varieties grown in this region, and
both are susceptible to Ug99 at seedling stages (pre-
sent study) and in the eld (in Kenya and Yemen).
Environmental conditions are favourable to stem
rust disease development during December–March
in Yemen, when wheat crops in southern Iran are at
the heading stage. The wind trajectories during this
period have shown a frequent tendency for airborne
particles originating from Yemen to move towards
southern Iran (Hodson et al., 2005; Singh et al., 2006).
It would be reasonable to conclude that the occur-
rence of Ug99 in southwest Iran, as indicated in the
present study, and not in southern wheat-growing
areas, is due to lack of timing and monitoring of
stem rust infection. It is possible that wheat in south-
ern Iran has escaped infection or that initially un-
detected infections moved to south-western Iran. A
case could be made for possible independent airow
originating from Yemen and directly heading to the
areas where TTKSK races were detected. Facultative
and winter wheat varieties are grown in Boroujerd
and Hamadan, and stem rust has not been a problem
in these areas during recent decades, in particular in
Hamadan where winter wheat varieties are grown
and winter temperatures do not allow the pathogen
to grow in early growth stages. However, the most
recent pathogenicity survey of Pgt in the southern
part of Iran indicated reoccurrence of Ug99 (TTKSK)
in farmer elds (Patpour et al. 2011, BGRI Workshop,
Figure 1. Dendrogram of 29 Iranian wheat varieties based on UPGMA cluster analysis and the Jaccard similarity coef-
cients calculated from evaluation of seedling resistance against four physiological races of Puccinia graminis f. sp. tritici

121
Vol. 52, No. 1, April, 2013
Physiological races of Puccinia graminis f. sp. tritici in Iran
St Paul, Minnesota, USA), indicating the validity of
predicted pathway of Ug99 by Nazari et al., (2009).
The occurrence of race TTKSK in Iran, the sus-
ceptibility of Iranian wheat cultivars, the presence of
environmental conditions conducive to disease epi-
demics in dierent parts of the country, and the wide
spread occurrence of the alternate host Berberis spp.
in vast mountainous areas of Iran, indicate a serious
threat by stem rust to wheat production in Iran and
hence to neighbouring countries. Aecial infections
on Berberis spp. were observed in Zagros and Alborz
mountain ranges (Scharif et al., 1971; Bamdadian and
Torabi, 1978). Although wheat is not grown on a large
scale in mountainous areas, cultivation of suscepti-
ble local varieties near Berberis could allow for sexual
recombination to take place. The favourability of en-
vironmental conditions both for stem rust epidemics
on wheat and aecial infection on Berberis, in combina-
tion with the susceptibility of currently grown wheat
varieties in the Caspian Sea region, means that this
area would be an ideal place in the Central and West
Asia and North Africa regions for the development
of new races and inoculum build-up. Historical stem
rust epidemics have occurred near the Caspian Sea
(Scharif and Bamdadian, 1974). Evaluation of Iranian
variety reactions to Ug99 indicated that greater than
98% of tested materials were susceptible to stem rust
race TTKSK, implying the vulnerability of wheat
production to stem rust epidemics. Susceptibility
of the representative set of Iranian varieties to race
TTKSK in seedling (present study) and adult-plant
stages (Njoro, Kenya) reinforce the serious threat of
race TTKSK to wheat production in Iran.
Along with the immediate needs for strengthen-
ing breeding programs for resistance to Ug99 stem
rust, given the serious implications of the airborne
nature of rust pathogens and the susceptibility of
wheat varieties to Ug99, there is a clear need for a
regional coordinated monitoring system and track-
ing of the movement of Ug99 in projected ‘at-risk’
regions of countries in East Africa, the Middle East,
Central Asia and South Asia.
Acknowledgements
The authors would like to thank technical stas
of the Cereal Pathology Unit in the Cereal Research
Department, Seed and Plant Improvement Institute,
Karaj, Iran. Special thanks go to M. Nasrollahi, M.
Chichi, T. Hossain Pour and M. Bahari from Agricul-
tural Research Centres in Lorestan and Hamadan-
Hamadan provinces for their assistance in sample
collection and eld surveys. Research support was
provided by Cereal Research Department, Seed and
Plant Improvement Institute.
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Accepted for publication: September 12, 2012