Detection of Virulence to Resistance Gene Sr24 Within Race TTKS of Puccinia graminis f. sp. tritici.
ABSTRACT The stem rust resistance gene Sr24 is effective against most races of Puccinia graminis f. sp. tritici, including race TTKS (syn. Ug99), and is used widely in commercial wheat cultivars worldwide. In 2006, susceptible infection responses were observed on wheat lines and cultivars carrying Sr24 in a field stem rust screening nursery at Njoro, Kenya. We derived 28 single-pustule isolates from stem rust samples collected from the 2006 Njoro nursery. The isolates were evaluated for virulence on 16 North American stem rust differential lines; on wheat lines carrying Sr24, Sr31, Sr38, and SrMcN; and on a wheat cultivar with a combination of Sr24 and Sr31. All isolates were identified as race TTKS with additional virulence on Sr31 and Sr38. These isolates were divided into two groups: group A (seven isolates and the two control isolates), producing a low infection type, and group B (21 isolates), producing a high infection type on Sr24, respectively. Isolates of group B represented a new variant of race TTKS with virulence to Sr24. Eighteen simple sequence repeat (SSR) markers were used to examine the genetic relationship between these two groups of isolates in race TTKS and five North American races (MCCF, QCCQ, RCRS, RTHS, and TPMK) that are representative of distinct lineage groups. All isolates of race TTKS shared an identical SSR genotype and were clearly different from North American races. The virulence and SSR data indicated that the new variant of race TTKS with Sr24 virulence likely has arisen via mutation within the TTKS genetic lineage. We propose to revise the North American stem rust nomenclature system by the addition of four genes (Sr24, Sr31, Sr38, and SrMcN) as the fifth set. This revision recognizes the virulence on Sr31 and differentiates isolates within race TTKS into two separate races: TTKSK and TTKST, with avirulence and virulence on Sr24, respectively. The occurrence of race TTKST with combined virulence on Sr24 and Sr31 has substantially increased the vulnerability of wheat to stem rust worldwide.
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ABSTRACT: The virulence of wheat stem rust pathogen population in the North Caucasus Region of Russia for the period 2008–2011 has been described. Monopustular urendial isolates (350) were differentiated from the international set of 39 monogenic lines. Using Rogers index, the difference level in gene virulence was revealed in different years. The comparison of the genetic structure of the fungus population at present and the mid-1990s was concluded.Russian Agricultural Sciences 01/2014; 40(1):32-34.
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ABSTRACT: This study was part of a larger pre-breeding effort to develop new parental materials carrying useful genes for disease resistance and adaptation. Firstly, marker-assisted backcrosses were employed to transfer and pyramid combinations of disease resistance genes (Fhb1, Lr34, Lr53, Sr2, Sr26, Sr39, and Sr50) and a reduced height gene (Rht-B1b) into the variety Norstar. Following the third backcross to Norstar, the various backcrossed progenies were inter-mated to derive progenies having combinations of Fhb1 and Rht-B1b plus the targeted leaf and/or stem rust resistance genes. Five NILs (each carrying Fhb1 and Rht-B1b) that differ for the leaf and stem rust resistance genes they possess were recovered. Secondly, a mapping study using the 9K Illumina Infinium iSelect wheat assay was conducted with a F2 mapping population developed by crossing Lr59-25 (0306/2*CSph1b//CSN1AT1B/3/Thatcher) and Superb. Lr59 was mapped 0.5cM distally from the co-segregating SNPs IWA1495, IWA6704, IWA2098 and IWA969 on wheat chromosome arm 6BS.01/2015, Degree: MS, Supervisor: Francois Marias
Plant Disease / June 2008 923
Detection of Virulence to Resistance Gene Sr24 Within Race TTKS
of Puccinia graminis f. sp. tritici
Y. Jin and L. J. Szabo, United States Department of Agriculture–Agricultural Research Service, Cereal Disease
Laboratory, University of Minnesota, St. Paul 55108; Z. A. Pretorius, Department of Plant Sciences, University of
the Free State, Bloemfontein 9300, South Africa; R. P. Singh and R. Ward, International Maize and Wheat Im-
provement Center (CIMMYT), Apdo, Postal 6-641, Mexico D.F., Mexico; and T. Fetch, Jr., Cereal Research Centre,
Agriculture and Agri-Food Canada, Winnipeg, MB, R3T 2M9, Canada
Stem rust, caused by Puccinia graminis
f. sp. tritici, is one of the most destructive
diseases of wheat (Triticum aestivum and
T. turgidum subsp. durum) and barley
(Hordeum vulgare). In many wheat pro-
duction areas, the disease has been con-
trolled effectively through the widespread
use of host resistance. The gene Sr24,
originally transferred from Elytrigia elon-
gata to bread wheat (16), is a valuable
source of resistance, effective against most
stem rust races worldwide, although stem
rust races with Sr24 virulence have been
detected in South Africa (7) and India (2).
Sr24 has been deployed in wheat cultivars
in Australia, South Africa, and North and
South America partly because of the effec-
tiveness against a broad spectrum of stem
rust races and partly because of its close
linkage with Lr24, a gene conferring resis-
tance to leaf rust (8). Sr24 is highly effec-
tive against race TTKS (or Ug99) (5), a
recently emerged race with virulence to
Sr31 that is considered to be a serious
threat to wheat production worldwide
(10,15,19). Results from the 2005 and
2006 stem rust field screening in Kenya
and seedling studies in the United States
suggested that Sr24 is a major component
for TTKS resistance in adapted germ-
plasm. Based on stem rust ratings on the
monogenic resistant line LcSr24Ag as well
as from observations on breeding lines and
cultivars known to carry this gene, Sr24
was highly effective in the stem rust
screening nursery at Njoro, Kenya in 2005
where race TTKS was predominant (6).
Infection responses were resistant to mod-
erately resistant, with terminal stem rust
severity up to 20%. However, in the 2006
stem rust field screening nursery at Njoro,
we observed a low frequency of uredinia
(pustules) with infection responses of
moderately susceptible to susceptible types
on the two monogenic lines for Sr24,
LcSr24Ag, and Agent/9*LMPG, and many
breeding lines and cultivars carrying Sr24,
suggesting that virulence on Sr24 was
present in the nursery. The objective of this
study was to determine variation in viru-
lence and genetic relationships among
isolates of race TTKS.
MATERIALS AND METHODS
Sample collection and storage. Sam-
ples were collected in September 2006
from wheat lines and cultivars known or
suspected to carry Sr24 or Sr31 in a stem
rust nursery (0°20′S, 35°56′E) in Njoro,
Kenya. Leaf sheath tissue bearing moder-
ately susceptible or susceptible pustules
were cut into pieces of 2 to 3 cm in length,
with true stem tissue and nodes removed to
facilitate the drying process. Each sample
consisted of three to five pieces of tissue
collected from the same line within a plot.
Samples were placed in glassine bags and
air dried for 3 to 4 days at room tempera-
ture. A subset of samples was vacuum
dried. Dried samples were mailed using an
express mail service with a transit time of
14 days from the date of mailing to the
date of arrival at the destination. Upon
receipt, the samples were placed immedi-
ately in a –80°C freezer and were stored
for approximately 3 months. In all, 11 field
samples collected from nine cultivars or
lines in the Njoro nursery were processed
in the study: 1 sample from an unknown
line, 1 from a line carrying Sr31, and the
remaining 9 samples from lines suspected
to carry Sr24. Samples stored in glassine
bags were repackaged into ziplock bags
after removal from the storage freezer and
submersed in a water bath at 43°C for 15
min. After the heat-shock treatment, ured-
iniospores from each sample were col-
Jin, Y., Szabo, L. J., Pretorius, Z. A., Singh, R. P., Ward, R., and Fetch, T., Jr. 2008. Detection of
virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis.
The stem rust resistance gene Sr24 is effective against most races of Puccinia graminis f. sp.
tritici, including race TTKS (syn. Ug99), and is used widely in commercial wheat cultivars
worldwide. In 2006, susceptible infection responses were observed on wheat lines and cultivars
carrying Sr24 in a field stem rust screening nursery at Njoro, Kenya. We derived 28 single-
pustule isolates from stem rust samples collected from the 2006 Njoro nursery. The isolates were
evaluated for virulence on 16 North American stem rust differential lines; on wheat lines carry-
ing Sr24, Sr31, Sr38, and SrMcN; and on a wheat cultivar with a combination of Sr24 and Sr31.
All isolates were identified as race TTKS with additional virulence on Sr31 and Sr38. These
isolates were divided into two groups: group A (seven isolates and the two control isolates),
producing a low infection type, and group B (21 isolates), producing a high infection type on
Sr24, respectively. Isolates of group B represented a new variant of race TTKS with virulence to
Sr24. Eighteen simple sequence repeat (SSR) markers were used to examine the genetic rela-
tionship between these two groups of isolates in race TTKS and five North American races
(MCCF, QCCQ, RCRS, RTHS, and TPMK) that are representative of distinct lineage groups. All
isolates of race TTKS shared an identical SSR genotype and were clearly different from North
American races. The virulence and SSR data indicated that the new variant of race TTKS with
Sr24 virulence likely has arisen via mutation within the TTKS genetic lineage. We propose to
revise the North American stem rust nomenclature system by the addition of four genes (Sr24,
Sr31, Sr38, and SrMcN) as the fifth set. This revision recognizes the virulence on Sr31 and dif-
ferentiates isolates within race TTKS into two separate races: TTKSK and TTKST, with aviru-
lence and virulence on Sr24, respectively. The occurrence of race TTKST with combined viru-
lence on Sr24 and Sr31 has substantially increased the vulnerability of wheat to stem rust
Corresponding author: Y. Jin
Mention of a trademark, vendor, or proprietary
product does not constitute a guarantee or warranty
of the product by the United States Department of
Agriculture (USDA) and does not imply its ap-
proval to the exclusion of other product or vendors
that also may be suitable.
USDA–Agricultural Research Service Cereal Dis-
ease Laboratory maintains seed stocks used in this
study and they are available upon request from the
Accepted for publication 7 February 2008.
This article is in the public domain and not copy-
rightable. It may be freely reprinted with custom-
ary crediting of the source. The American Phyto-
pathological Society, 2008.
924 Plant Disease / Vol. 92 No. 6
lected into a gelatin capsule (size 00) using
a small cyclone collector and placed in a
rehydration chamber for 2 to 4 h, where
approximately 80% relative humidity was
maintained by a KOH solution (14). Ap-
proximately 0.5 ml of a light mineral oil
(Soltrol 170) was added into each gelatin
capsule to suspend urediniospores for sub-
sequent inoculation of differential lines.
Differential lines. In addition to the 16
differentials in the P. graminis f. sp. tritici
differential set of North America (11,12),
we included 7 supplemental tester lines:
LcSr24Ag and Agent/9*LMPG (mono-
genic lines for Sr24), Ivan (a hard red
spring wheat cultivar carrying Sr24),
Benno Sr31/6*LMPG (monogenic line for
Sr31), VPM 1 (PI 519303, a tester stock
for Sr38), McNair 701 (CI 15288, a winter
wheat cultivar carrying SrMcN), and
Siouxland (PI 483469, a winter wheat
cultivar carrying Sr24 and Sr31). Four
lines were planted in each corner of a
square pot (5 by 5 cm) containing ver-
miculite. Six pots planted with 16 differen-
tial lines and 7 supplemental lines were
placed in a custom-made plastic tray with
each pot in a fixed position. After planting,
trays were placed in a greenhouse desig-
nated for raising clean plants. Plants were
fertilized using a solution of water-soluble
fertilizer three times: immediately after
plant emergence, after removal from the
mist chamber, and 7 days after inoculation.
Inoculation, incubation, and disease
assessment. Seedling plants of the 23 lines
in each tray were inoculated with a bulk
collection of spores from each sample
when the primary leaves were fully ex-
panded (7 to 9 days after planting). A petri
plate containing water agar (20 g of Difco
agar in 1.0 liter of H2O) also was sprayed
with the inoculum and examined 4 h later
under a microscope to determine the per-
centage of spore germination. Seedlings
were incubated in a dew chamber for 14 h
at 18°C in the dark, and then for an addi-
tional period of 3 to 4 h under fluorescent
light. The inoculated plants were placed on
a greenhouse bench at 18 ± 2°C with a
photoperiod of 16 h. Infection types (ITs),
described by Stakman et al. (17), were
assessed 14 days post-inoculation. ITs 0, ;,
1, 2, or combinations thereof were consid-
ered low ITs, indicating that the corre-
sponding resistance gene was effective. ITs
3 to 4 were considered high ITs, indicating
that the corresponding resistance gene was
not effective against the isolate tested.
Derivation of single-pustule cultures.
Because the primary purpose of this study
was to identify isolates with virulence on
Sr24, we focused on isolating from pus-
tules on Sr24 lines with ITs higher than 2.
Single-pustule isolation on lines with other
genes also was made in an attempt to ob-
tain races in addition to those with viru-
lence on Sr24. After preliminary scoring of
the differential and supplemental lines, a
leaf suitable for single-pustule isolation
(i.e., pustules were well spaced) was se-
lected and remaining plants were removed
from the pot. The leaf was trimmed to
remove other pustules if more than one
pustule was present. The seedling with the
single pustule was incubated in a mist
chamber overnight to germinate any con-
taminant spores, followed by incubation in
an isolation cubicle in a greenhouse. The
new crop of urediniospores produced from
the single pustule was collected by scrap-
ing the spores directly into a gelatin cap-
sule 1 or 2 days after mist incubation, and
collection continued for a period of 3 days.
The spores collected from a single pustule
were used to directly inoculate a differen-
tial set. The culture derived from the sin-
gle-pustule isolation procedure was con-
sidered a pure culture, subsequently
increased on a susceptible line (McNair
701), and stored in a –80°C freezer or liquid
nitrogen for future use. Each single-pustule-
derived isolate was evaluated for virulence
on the differential and supplemental lines
twice. Two isolates of race TTKS, isolate
98UGA-1-1 collected from Uganda in 1999
(10) and isolate 04KEN156/04 collected
from Kenya in 2004 (19), were evaluated on
the differential and supplemental lines to
compare their virulence pattern with the
isolates derived from the 2006 collections
from Njoro, Kenya.
Table 1. Infection types produced on Sr24 lines and other supplemental differentials by isolates derived from stem rust samples collected from the 2006 stem
rust nursery planted at Njoro, Kenyaa
TTKS check culture
TTKS check culture
a Infection types (ITs) at the seedling stage following the descriptions of Stakman et al. (16), where ITs 0, ;, 1, 2, or combinations thereof were considered
low ITs, and ITs 3 to 4 were considered high ITs.
b Isolates included in the simple sequence repeat analysis.
Plant Disease / June 2008 925
Determination of simple sequence re-
peat genotypes. DNA was extracted from
either urediniospores or infected wheat
leaf tissue using an OmniPrep DNA ex-
traction kit (GenoTech, St. Louis) as de-
scribed by Anikster et al. (1). Polymerase
chain reaction (PCR) amplification condi-
tions of simple sequence repeat (SSR) loci
and detection of alleles were as described
previously (18). SSR primers used were
PgtSSR3, PgtSSR4, PgtSSR6, PgtSSR11,
PgtSSR90, PgtSSR129, PgtSSR134,
PgtSSR140, PgtSSR147, PgtSSR151,
PgtSSR162, and PgtSSR164 (18). In all,
36 isolates were used in the SSR analysis,
which included 13 isolates of race TTKS
avirulent on Sr24 (Table 1 and 04KEN152/
04KEN157/04, 04KEN158/04, 04KEN159/
04, 04KEN160/04, and 04KEN161/04), 18
isolates of race TTKS virulent on Sr24 (Ta-
ble 1), and 5 standard U.S. isolates
(74MN1409, race TPMK; 96MN83a-3, race
RTHS; 77ND82-a, race RCRS; 03LA94c,
race QCCQ; and 03ND110a, race MCCF).
GENALEX 6 (9) was used for principal
coordinate analysis of the SSR data.
RESULTS AND DISCUSSION
In total, 28 single-pustule-derived iso-
lates of P. graminis f. sp. tritici from the
2006 Njoro collections were used in this
study (Table 1). When tested against the 16
single-gene differential lines of the North
American stem rust nomenclature system
(11,12), all isolates produced a near-
immunity reaction (IT 0 to 0;) on line
W2691SrTt-1 carrying resistance gene
Sr36 and a low IT (2+) on line CnsSrTmp
carrying resistance gene SrTmp, but high
(or susceptible) ITs (3 to 4) on all other
differential lines except for line Combina-
tion VII (Sr13+Sr17; Table 2). The IT (2+
to 2++) produced on Combination VII was
due to the effect of Sr13 at a relatively low
incubation temperature (18°C). However,
it is considered a high IT for the intended
differential gene Sr17 because, when a
race is avirulent on Sr17, the expected low
IT is from ; to ;1 (8,13). All 28 isolates
derived from the 2006 Njoro collections
produced a virulence–avirulence pattern on
the 16 differential lines identical to that of
TTKS control isolates 98UGA-1-1 and
On the seven supplemental wheat lines
containing resistance genes Sr24, Sr31,
Sr38, SrMcN, and a combination of Sr24
and Sr31, all isolates produced a high IT (3
to 4) on lines carrying genes Sr31, Sr38,
and SrMcN (Tables 1 and 2). The isolates
were differentiated into two groups based
on their reactions to resistance gene Sr24:
group A consisted of 9 isolates (including
two control isolates) producing a low IT
(1+ to 2) on Sr24 lines and group B con-
sisted of 21 isolates producing a relatively
high IT (3- to 3+) on lines carrying Sr24 as
well as on cv. Siouxland (Sr24+Sr31). The
isolates in group A produced low ITs typi-
cal of what is expected on Sr24 when chal-
lenged by an avirulent race, and were simi-
lar to isolates reported previously from
Uganda (10) and Kenya (19) with aviru-
lence on Sr24 (6). Although we did not
observe a fully compatible reaction (IT 4)
by group B isolates on lines with Sr24, the
observed ITs (3- to 3+) were sufficiently
high and considered compatible on Sr24.
This group of isolates likely represents a
new variant within race TTKS that pro-
duced susceptible infection responses on
Sr24 lines in the 2006 field stem rust nurs-
ery at Njoro.
The group B isolates with virulence on
Sr24 were distinctly different from the
Sr24-virulent race detected in South Africa
in the 1980s. The stem rust culture
UVPgt52, isolated from race 2SA100 de-
scribed by Le Roux and Rijkenberg (7),
was identified as race LKCS (Y. Jin and Z.
Pretorius, unpublished data). Compared
with the original description, the LKCS
phenotype differed on Sr7b, Sr9b, and
Sr11. These differences could be ascribed
to different tester lines in the respective
differential sets and interpretation of in-
termediate ITs. However, LKCS differs
from TTKS with respect to several other
avirulence genes, including Sr21, Sr30,
Sr31, and Sr38, suggesting that these races
Eighteen SSR markers (18) were used to
examine the genetic relationship between
31 selected isolates of the TTKS race clus-
ter, including reference isolate 98UGA1-1,
9 Kenyan isolates collected in 2004, and
21 Kenyan isolates collected in 2006. This
set included 13 isolates that are avirulent
on Sr24 and 18 that are virulent on Sr24.
In addition, five standard U.S. isolates
were included. Sixty-five alleles were
scored for the 18 SSR loci examined, indi-
cating that these loci are polymorphic for
this set of isolates (data not shown). All 31
isolates of the TTKS race cluster had an
identical SSR genotype and were distinct
from the five U.S. isolates (Fig. 1). These
results confirm the avirulence and viru-
lence phenotype data, indicating that the
collections of race TTKS from Kenya in
2004 and 2006 are of the same genetic
lineage as the
(98UGA1-1) made in Uganda in 1998.
Each of the 18 isolates with virulence on
Sr24 (group B) had identical SSR geno-
types compared with the isolates avirulent
on Sr24 (group A), indicating that the new
variant of race TTKS with Sr24 virulence
has arisen via mutation within the TTKS
genetic lineage rather than representing a
separate genetic lineage. Additional DNA
markers will need to be developed to dif-
ferentiate between these two subgroups of
The unique virulence on Sr31 as well as
variations within race TTKS cannot be
recognized based on the current 16 differ-
ential lines used in the North American
stem rust nomenclature system. We pro-
Table 2. Infection types produced by the two groups of Puccinia graminis f. sp. tritici TTKS isolates
on the revised North American set of differential lines and their new race designationsa
Set, lineb Accession no. Sr gene Group A isolates Group B isolates
a Infection types (ITs) at the seedling stage following the descriptions of Stakman et al. (16), where ITs
0, ;, 1, 2, or combinations thereof were considered low ITs, and ITs 3 to 4 were considered high ITs.
b Differential sets I to IV are described in Roelfs and Martens (12) and Roelfs et al. (11).
c IT 2++ produced on combination VII was due to the effect of Sr13 at a relatively low incubation
temperature (18°C). However, it is considered a high IT for the intended differential gene Sr17 be-
cause, when a race is avirulent on Sr17, the expected low IT is from ; to ;1 (8,13).
926 Plant Disease / Vol. 92 No. 6
pose to revise this nomenclature system by
the addition of four genes, Sr24, Sr31,
Sr38, and SrMcN, as the fifth set. These
genes are important in wheat breeding.
This revision recognizes the new virulence
on Sr31 and differentiates isolates within
race TTKS into two separate races:
TTKSK and TTKST, with avirulence and
virulence, respectively, on Sr24. With a
few exceptions, races virulent on Sr24,
Sr31, or Sr38 are rare in the stem rust
population in North America as well as
worldwide. Although races virulent on
SrMcN are common in the North American
stem rust population, the gene is very use-
ful in distinguishing isolates frequently
occurring on barley from those occurring
on wheat, as well as isolates from the al-
ternate host. McNair 701 (SrMcN) has
been used as a supplemental differential in
Canadian race surveys (3,4).
The emergence of virulence on Sr24
within the TTKS race cluster likely has
increased the vulnerability of wheat to
stem rust worldwide because of the wide-
spread use of this gene in breeding. Com-
mercial cultivars with resistance based on
Sr24 and/or Sr31, particularly in the East
African region, must be viewed with cir-
cumspection in terms of potential stem rust
epidemics. In South Africa, previous ex-
perience has shown the devastating effect
of Sr24 virulence on cultivars protected by
this gene alone (7). The occurrence of
virulence to both Sr31 and Sr24 in East
Africa has highlighted the need for devel-
oping and deploying cultivars with combi-
nations of effective resistance genes to
enhance their longevity. Alternatively,
cultivars with multiple minor genes to
achieve stable resistance also could be
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Fig. 1. Plot of principal coordinate analysis of Puccinia graminis f. sp. tritici isolates based on simple
sequence repeat data. In all, 31 Kenyan isolates of race TTKS were analyzed, including 13 avirulent on
Sr24 (group A) and 18 virulent on Sr24 (group B). Five common North American races (one isolate of
each race) were included for reference. The first three eigenvectors (coordinates) explained 93% of the